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Abiotic Stress in Crop Production
Romana Kopecká, Michaela Kameniarová, Martin Černý and 2 more
International Journal of Molecular Sciences · 2023 · Meta-analysis · CC BY
Abstract
The vast majority of agricultural land undergoes abiotic stress that can significantly reduce agricultural yields. Understanding the mechanisms of plant defenses against stresses and putting this knowledge into practice is, therefore, an integral part of sustainable agriculture. In this review, we focus on current findings in plant resistance to four cardinal abiotic stressors—drought, heat, salinity, and low temperatures. Apart from the description of the newly discovered mechanisms of signaling and resistance to abiotic stress, this review also focuses on the importance of primary and secondary metabolites, including carbohydrates, amino acids, phenolics, and phytohormones. A meta-analysis of transcriptomic studies concerning the model plant Arabidopsis demonstrates the long-observed phenomenon that abiotic stressors induce different signals and effects at the level of gene expression, but genes whose regulation is similar under most stressors can still be traced. The analysis further reveals the transcriptional modulation of Golgi-targeted proteins in response to heat stress. Our analysis also highlights several genes that are similarly regulated under all stress conditions. These genes support the central role of phytohormones in the abiotic stress response, and the importance of some of these in plant resistance has not yet been studied. Finally, this review provides information about the response to abiotic stress in major European crop plants—wheat, sugar beet, maize, potatoes, barley, sunflowers, grapes, rapeseed, tomatoes, and apples.
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From PubMed Central, U.S. National Library of Medicine, as current on Oct 22, 2026. Paragraph numbers are ours, so an answer can point at one.
1. Introduction
Abiotic stressors, such as drought, soil salinity, heat, and cold, are major limiting factors affecting crop production both qualitatively and quantitatively. These threats are likely to become even more significant under climate change and the pressures of an ever-growing human population. Recently, the global human population reached 8 billion people and the latest projections by the United Nations suggest that the world’s population could grow to around 8.5 billion by 2030 and 9.7 billion by 2050. Environmental change is, therefore, a big challenge for agriculture and its efforts to meet the growing need for food worldwide. Unfortunately, the vast majority of land is exposed to stressful conditions. Compared to record yields, abiotic stress can reduce yields by more than 60% on average. From a global perspective, climate extremes exhibit an increasing poleward gradient, and temperature variability patterns demonstrate the growing prevalence of heat extremes over cold ones. A recent study based on sub-national yield data and a machine learning algorithm showed that climate extremes could explain up to half of the global crop yield variability. The study also suggested that under the condition of regular irrigation, the yield anomalies are associated more strongly with temperature-related extremes than precipitation-related factors.
In this review, we focus on the European region, which, although medium in size, encompasses all the important climatic zones, including arid regions in the south and polar regions in the north. According to FAOSTAT, in 2021, Europe was the largest producer of important crops such as barley (Hordeum vulgare), grapes (Vitis vinifera), and sugar beet (Beta vulgaris), and the second largest producer of wheat (Triticum aestivum), tomatoes (Solanum lycopersicum), potatoes (Solanum tuberosum), cucumbers (Cucumis sativus), and apples (Malus domestica).
The effects of climate change in Europe are regionally differentiated (Figure 1). In the Mediterranean region, temperatures are rising faster than in other parts of Europe and this increase is accompanied by increasing water demands and the risk of forest fires during the summer. Desertification and a decrease in crop yields are serious threats to this area. In central and eastern Europe, summer precipitation is decreasing and the number of warm temperature extremes is rising. Temperate and boreal vegetation over middle latitudes suffer from serious damage caused by accelerated phenological events overlapping with late-spring frosts. Northern Europe is also affected by rising temperatures, but in this case, it can lead to increased crop yields through the introduction of new crop varieties, longer growing seasons, and the expansion of areas suitable for crop production. A recent bioinformatic analysis of European crop losses over the last few decades showed that drought and heat waves were associated more with yield loss in cereals (9% and 7.3%, respectively) than in non-cereals (3.8% and 3.1%, respectively). The effect of cold waves was almost five times smaller.
The need to understand the mechanisms of resistance to abiotic stress and sustainable agriculture under a changing climate is reflected in the increasing number of publications focusing on crops and abiotic stressors (Figure 1B).
Crops require different conditions for optimal growth and to achieve marketable quality and these conditions govern where they are best cultivated. The ten most commonly grown crops in Europe and the countries most involved in their production are shown in Figure 2A. In order of their level of production in 2021, the most cultivated crops are wheat, sugar beet, maize (Zea mays), potatoes, barley, sunflowers (Helianthus annuus), grapes, rapeseed (Brassica napus), tomatoes, and apples. Wheat is one of the main crops cultivated not only in Europe (Figure 2A) but also worldwide. It can adapt to a wide range of temperatures and environmental conditions, but excessive rainfall, together with high temperatures, can cause the spread of some common diseases that lower yields. Water deficiency and high soil salinity also constrain wheat growth and development. Another important cereal, maize, which has high water requirements, is susceptible to drought, particularly at certain critical stages of growth such as at the seedling or reproductive stage. Sugar beet is a fairly salt-tolerant crop due to a number of mechanisms that help it to regulate the distribution of salt and other solutes within its tissues and maintain its water content. In contrast, potatoes are one of the most drought-sensitive crops and high levels of salt in the soil adversely affect tuber development. Barley is perhaps the most salt-tolerant cereal and exhibits a high level of resistance to abiotic stress. Its high natural adaptability to a variety of growing conditions makes barley a promising crop for future production in a changing climate. Sunflowers are the second most important oil crop in Europe. Due to their relatively high resistance to abiotic stresses, they are often grown in semiarid and arid conditions. Nevertheless, their growth and production are still limited in drought and salt-stressed conditions. Tomatoes can grow in almost all climatic regions of the world; however, their production is affected by drought, high salinity, and temperature extremes. Apple fruit production is endangered by late-spring frosts that harm flower buds. Rapeseed (oilseed rape or canola) is the principal oil crop in Europe and like other temperate region crops, it is susceptible to multiple abiotic stresses. The seed yield of rapeseed can be reduced more by heat stress than by drought alone.
In this review, we focus on various aspects of four important abiotic stressors that affect crop plants: drought, salinity, heat, and cold. Recent advances in the understanding of stress signaling and resistance in crop plants are summarized. We include a meta-analysis of gene expression in response to abiotic stress in the model plant Arabidopsis. This analysis revealed uncharacterized genes that are responsive to all abiotic stressors, as well as the transcriptional modulation of Golgi-targeted proteins in response to heat stress, which has not previously been well described.
2.1.1. Europe Is Experiencing the Hottest Summers in Recorded History
According to the Intergovernmental Panel on Climate Change, the temperature increase is likely to reach 1.5 °C between 2030 and 2052 if it continues to increase at the current rate. In Europe, 2020 was the warmest year on record at 2.16 °C above average. Last year (2022), the average annual temperature was the second highest on record, while summer was the hottest. Moreover, the average rate of temperature increase in Europe has almost tripled since 1981. The areas most affected by high temperatures were in western and northern Europe and several countries experienced their highest summer wildfire emissions for at least the last 20 years.
2.1.2. The Temperature Optimum for Most Crops Grown in Europe Is Exceeded for Weeks during the Season
Temperature optima differ according to the crop species, cultivar, and stage of development. Based on the temperature optima for the most important European crops (Table 1), it can be concluded that temperatures above 30 °C are no longer optimal for European crop production. We searched for the number of days exceeding this threshold in the less heat-exposed regions of central Europe in 2022. For example, data from the Czech Hydrometeorological Institute (Doksany weather station) and the German Weather Service showed that 30 °C was exceeded on 35 days, and on an average of 17.3 days, respectively. These data show that during a year, crop plants are exposed to superoptimal temperature conditions, not for just a few days but rather for weeks, even in the colder European regions.
2.1.3. Role of High Temperatures in Crop Production
Heat stress is defined as exposure to temperatures above the optimum that are sufficient to cause irreversible damage to plant growth and development. Higher temperatures directly affect plant vegetative stages, resource allocation, and, above all, reproductive processes, which can lead to a substantial reduction in yields. Extremely high temperatures result in rapid cellular injury and cell death. Heat stress in the vegetative phase of a plant’s growth can lead to a lower rate of photosynthesis followed by biomass reduction. Higher temperatures significantly affect the reproductive phases of development. For species of the genus Brassica, temperatures exceeding 29.5 °C during the period from bolting to the end of flowering reduce flowers, pod numbers, seed weight, and thus, total yield. Aiqing et al. stated that heat exposure during spring wheat gametogenesis is a major determining factor for yield loss. Bheemanahalli et al. observed a 2–93% reduction in pollen germination after heat-stress treatment on spring wheat genotypes. Maize yield is usually lowered by kernel abortion, which can be a result of the low utilization of soluble sugar resulting from the modulation of starch synthesis during heat and drought stress. These authors also emphasized the detrimental effect of thermal stress on pollen viability. High temperatures during the whole grain-filling stage in maize resulted in a 28% decrease in grain weight. Many authors have shown that crop plants are very sensitive to heat stress, especially during reproductive phases.
2.1.4. High-Temperature Signaling in Model Plant and Crops
Several thermosensors and thermosensitive elements have been characterized in reaction to heat stress. Thermosensors are elements that meet three conditions: a change in their structure or activity is based on direct interaction with heat-stress conditions; this change leads to important signals or responses; and these processes lead to physiological and morphological alterations or responses to stress. Following these conditions, changes in membrane fluidity and changes in protein conformation can be evaluated as thermosensors. Changes in membrane fluidity induced by high temperatures lead to Ca2+ influx due to the activation of Ca2+-permeable channels belonging to the CYCLIC NUCLEOTIDE-GATED CHANNEL (CNGC) family. Specific CNGCs have been shown to mediate thermotolerance in Arabidopsis thaliana and Oryza sativa. Important components of Ca2+ signaling pathways are annexins. This multifunctional protein family is now known to be associated with heat-stress responses in wheat, barley, rye (Secale cereale), rice, and tomatoes. A change in protein conformation in reaction to heat stress has been confirmed in specific photoreceptors. PHYTOCHROME B (PHYB) in Arabidopsis has been observed to participate in temperature perception through its temperature-dependent reversion from the active Pfr state to the inactive Pr state. The reversion of phytochrome is followed by downstream components that can be better specified as thermoresponsive. The most well-known group of thermoresponsive interacting partners is the phytochrome-interacting factor (PIF) family. The importance of PIFs for thermomorphogenesis has been observed in Arabidopsis and members of this family have also been identified in wheat, tomatoes, and rice, whereas increased expression levels of PIFs under high temperatures have been confirmed in maize. The activity of PIF4 can influence the function of the heat-responsive gene EARLY FLOWERING 3 (ELF3) in Arabidopsis, barley, and wheat. Moreover, ELF3 has recently been recognized as a thermosensor. The complex interactions of ELF3, PIF4, and PHYB suggest their function as a PHYB-ELF3-PIF4 module that regulates the plant’s responses to environmental cues, with implications for plant biorhythms. Other important signaling components are protein kinases, Reactive Oxygen Species (ROS), and transcription factors. Protein kinases play an important role in ROS activity in response to heat. After ROS production, the Mitogen-Activated Protein Kinase (MAPK) signaling pathway is activated and induces the expression of transcription factors. One group of activated transcription factors is HSFs (heat-shock factors), which can induce the expression of various heat-shock proteins (HSP). BcHSFA1, Sly-HSFA1a, ZmHSF05, TaHSFA2e, and OsHSFA2dI are associated with improved heat tolerance and have been identified as activators of HSP expression in rapeseed, tomatoes, maize, wheat, and rice. The activity of HSFs can be regulated by heat-shock proteins (HSPs) and alternative splicing. The alternative splicing mechanism has been confirmed as a novel component of heat-shock memory in wheat, barley, rice, maize, and tomatoes. Signaling mechanisms are summarized in Figure 3 in the red section.
2.2.1. High Temperatures without Precipitation Are Causing Drought across Europe
High temperatures are strongly associated with drought stress. Drought is a condition in which rain is either lacking or insufficient for so long that a considerable hydrological imbalance results. As a direct consequence of water shortage, plants, being sessile organisms, are affected by drought stress. Drought stress is becoming more significant with decreased availability and increasing demand for water. Agriculture presently accounts for 70% of global clean water demand and this percentage is expected to increase rapidly over the coming years. According to the European Drought Observatory, drought is not limited only to some specific regions in Europe. Insufficient rainfall, as indicated by the standardized precipitation index, was detected during the summer of 2022 in all main crop-producing countries in Europe, and it correlated with a significantly lower soil-moisture anomaly index across the whole of Europe.
2.2.2. Impact of Drought on Different Crops at Different Developmental Stages
The effect of drought on yield depends on the severity of the drought stress. Severe drought causes plant death so yield loss without irrigation could be total, as has been shown for barley under field conditions. A meta-study based on data from field experiments showed that the loss of yield when water was reduced by approximately 40% varied from around 21% in wheat to 39% in maize. A 10% yield decrease has been predicted for wheat and maize as a result of drought in European countries. Like other abiotic stresses, yield loss caused by drought varies with cultivars, and this factor should not be overlooked when species are compared regarding their drought resistance. Moreover, drought also impairs crop quality, e.g., lower seed oil content has been reported in seeds of rapeseed under water-shortage conditions. A relevant factor in yield loss is also the plant developmental stage when affected by drought. Plants exposed to drought in the reproductive stage are more vulnerable to drought; therefore, better timing of plant development could improve yields. Prolonged exposure to drought stress during the reproductive phase decreases grain filling, flower production, seed composition, and longevity.
2.2.3. Drought in Plant Physiology
The main problem associated with drought is the initiation of many intertwined positive feedback loops that exacerbate drought-stress conditions and lead to restrictions in above-ground growth. One such limitation is the closure of stomata as a mechanism to protect against water loss, which, in turn, limits the CO2 concentration. Limiting CO2 inhibits the productivity of the photosynthetic process and promotes the formation of ROS as a byproduct of the electron transport chain, without a sufficient level of terminal energy acceptors. ROS, in turn, impair the photosynthetic apparatus and cause oxidation of other important molecules, including proteins and lipids. The transpiration ratio for CO2 fixation is around 400 in C3 plants. However, the limitation of CO2 levels has serious drawbacks and the importance of maintaining sufficient CO2 levels has led to the evolutionary decoupling of light reactions and CO2 uptake in CAM plants. Another feature of stomata closure is the onset of leaf-tissue overheating. A decrease in the mass flow of water reduces nutrient acquisition and causes a loss of turgor, ultimately leading to a reduction in plant growth, leaf area, and leaf numbers, resulting in a reduced photosynthetically active area. Plants are forced to synthesize osmoprotective compounds rather than investing their resources in optimal growth. Overall, drought stress affects diverse physiological processes, ultimately leading to growth restrictions and low production.
2.2.4. The Role of Root Growth in Drought Resistance
The response to drought stress depends on its severity but the main counteracting mechanisms involve improving water uptake, reducing water loss, and tolerating water deficiency. Water uptake is mainly driven by efficient root growth. Interestingly, breeding technologies in the past were more focused on above-ground organs neglecting root systems or acquiring their properties only implicitly or indirectly. Thus, roots and their plasticity are a promising source of genetic variation for stress adaptation. Over the last decade, different groups have identified QTL, which influences root and physiological traits in important crops. The generally favorable properties of the root system for drought conditions are deep and branched rooting and efficient water uptake. Plants with shallow roots such as Styrian pumpkin (Cucurbita pepo L. Styriaca) could have serious problems with water uptake in field conditions currently prevalent. In this sense, the importance of root growth angle has been demonstrated by characterizing the DEEPER ROOTING 1 (OsDRO1) gene in rice. OsDRO1 promotes deep rooting and maintains a high yield under drought conditions Recently, the homologous gene in maize ZmDRO1 has been shown to modulate root angle, and its higher expression following stress signals has been associated with higher yields in field conditions. However, DRO1 ectopic expression without a stress signal could have a negative impact, even in non-stressed conditions, as has been shown for maize. The positive effect of root architecture on drought resistance has also been demonstrated in Arabidopsis expressing the StDRO1 gene from potatoes. These reports suggest that identifying these genes in other crops such as wheat and barley and breeding focused on root architecture could be fruitful strategies for preserving yields under drought conditions.
2.2.5. Roots and Hydrotropism
Because water is not distributed homogeneously in the soil, growth toward regions of the soil with higher water potential could be crucial in water-limiting conditions. The signaling pathway employing the Ca2+ channel pattern along root cells, endoplasmic reticulum-localized type 2A Ca2+-ATPase (ECA1), and MIZU-KUSSEY1 (MIZ1), have been shown to play an important role in root hydrotropism in the model plant Arabidopsis, although the complete molecular mechanism, including the sensor, remains unclear. Part of the mechanism could be hyperosmolality-gated Ca2+-permeable ion channels such as OSCA1 that can modulate Ca2+ concentration in response to osmotic stress and distinguish between osmotic and ionic stress. Recently, the role of plasma membrane-localized OSCA1.1 in root bending and hydrotropism has also been confirmed. As a promising candidate for drought resistance, OsOSCA1.2 hyperosmolality gating has been studied by cryogenic electron microscopy, and the characterization of OSCA genes has also been performed for barley, soybeans, and maize. However, the detailed molecular mechanism of hydrotropism is still not completely known, even in the model plant Arabidopsis. We should emphasize that experiments explaining root responses must be planned with respect to the natural root environment because some artificial conditions, such as the illumination of roots, could interfere with hydrotropism and affect other water-related root features such as root hair growth.
2.2.6. Long-Distance Signaling of Water Deficit
Regulation of transpiration is the main process in reducing water loss. Here, the key mechanism is the hormonal regulation of stomata closure by abscisic acid (ABA). Part of the long-distance signaling component is the root-derived small peptide CLAVATA3/ESR (CLE)-RELATED PROTEIN 25 (CLE25). In response to drought, CLE25 moves from the roots to the leaves, where it is perceived by BARELY ANY MERISTEM (BAM) receptors and induces accumulation of ABA by activating the biosynthetic enzyme NINE-CIS-EPOXYCAROTENOID DIOXYGENASE 3 (NCED3). ABA has been established as a very necessary stress-related phytohormone through research focused on crop plants. The role of ABA and its interaction with other plant hormones is discussed in Section 4.2 on metabolites. The signal for stomata closure is also mediated by ROS. In response to stress, H2O2 activates the receptor LEUCINE-RICH REPEAT RECEPTOR PROTEIN KINASE (HPCA1) to open the Ca2+ channels and close the stomata. Mutants in HPCA1 have also confirmed the role of this receptor in ABA downstream events, leading to stomata control. In contrast to Arabidopsis, ROS signaling in crops is far from being elucidated. In addition to stomata control, water loss can also be reduced through modifications to the cuticle, changes in leaf anatomy, or by utilizing the unique metabolism found in CAM plants. The signaling mechanisms are summarized in the yellow section in Figure 3.
2.2.7. Other Mechanisms of Drought Resistance
Tolerance to drought is based on counteracting the decrease in water potential by accumulating osmoprotectants, adjusting the metabolism, increasing water-usage effectiveness (WUE), and reducing the impact of the secondary effects of drought, including improving antioxidant metabolism and protecting photosynthesis. The role of metabolites in stress tolerance is discussed in more detail in a separate section.
2.3.1. Plants Are Variable in Their Resistance to Salt
Most crop plants are glycophytes that are sensitive to salinity stress. It has been estimated that approximately half of all irrigated land is affected by salinity. Highly saline soil can result from natural processes (weathering, rain with sea-salt content) or human activity (land clearing, irrigation) (reviewed in). The level of salinity is usually evaluated by the electrical conductivity of a saturated extract of soil or irrigation water. Salt-sensitive vegetables such as beans (Phaseolus vulgaris), carrots (Daucus carota), or onions (Allium cepa) can only tolerate low levels of salinity, with a threshold of detrimental effects around 1 dS/m, which is well below the level of 4 dS/m used to classify soils as saline. Salt-tolerant plants include those with a threshold greater than 4 dS/m. A broad overview of the salt-stress thresholds in soil for different plant species was prepared and published by Utah State University Extension and an extension, including thresholds for irrigation water, has also been reviewed. The yield of a crop grown in soils of increasing salinity varies not only with plant species but also with cultivars, as has been demonstrated recently under laboratory conditions for olives (Olea europaea) and maize and in field conditions for wheat, barley, and potatoes. Although searching for resistant cultivars or varieties is thus a promising strategy for maintaining yields where the salinity of the land is increasing, it is clearly not a final solution.
2.3.2. Key Mechanism for Salt-Stress Resistance
Salt stress negatively affects plant growth, development, and production. Increased levels of salt have two distinct biophysical consequences: induction of the osmotic stress and accumulation of ions to cytotoxic levels. This section focuses on the second of these consequences. One of the key results of excess salt is ion imbalance within the cell, as the homeostatic balance between ion ratios is thought to be the basic mechanism of tolerance to increased salt levels. In plants, the Salt Overly Sensitive (SOS) pathway is a core mechanism for salt tolerance. The principal determinant of Na+ extrusion from the cytoplasm to the apoplast is the cytoplasmic membrane-embedded Na+/H+ anti-porter SOS1. The activation of this antiporter in Arabidopsis is driven by two calcium sensors, CALCINEURIN B-LIKE PROTEIN 4 (AtCBL4/AtSOS3) and CALCINEURIN B-LIKE PROTEIN 10 (AtCBL10/AtSCABP8), and CBL-INTERACTING PROTEIN KINASE 24 (AtCIPK24/AtSOS2). The calcium sensors perceive the salt-induced [Ca2+]cyt and promote SOS2 activity. Activated SOS2 is recruited to the plasma membrane to phosphorylate the AtSOS1 antiporter, which, in turn, prevents the accumulation of Na+ at toxic levels. Mutants in the SOS pathway exhibit higher sensitivity to salt treatment and their overexpression has been shown to significantly increase salt tolerance. Recently, orthologs of members of the SOS pathway have been identified and confirmed in crop plants. Like the model plant Arabidopsis, SOS1 mutants in rice or maize also exhibit salt hypersensitivity. Members of the SOS pathway have also been confirmed in tomatoes and maize, although, to date, the SOS pathway has not been fully described and confirmed in other crops.
2.3.3. Salt-Stress Signaling and Role of ROS
The SOS pathway is dependent on the initial salt-induced increase in cytosolic calcium. It has recently been demonstrated that candidates for the Na+ sensor are glycosyl inositol phosporylceramide (GIPC) sphingolipids that are regulated by INOSITOL PHOSPHORYLCERAMIDE GLUCURONOSYLTRANSFERASE 1 (AtMOCA1/AtIPUT1). GIPC sphingolipids directly bind Na+ ions in the apoplast and regulate Ca2+ influx to the cell by an unknown ion channel, and their decreased levels in a moca1 mutant were followed by lower [Ca2+]cyt and salt hypersensitivity. Liu et al. (2022) confirmed the importance of IbIPUT1 in sweet potatoes (Ipomoea batatas) but its role is less known in other important crop plants.
Salt stress is tightly connected with ROS metabolism and signaling in cells. ROS, along with the vacuolar ion channel TWO PORE CHANNEL1 (TPC1), assist with a salt-induced calcium wave in the plant body that optimizes the response to salt stress by regulating gene expression before the onset of stress in distal shoot tissues. ROS are generated by RESPIRATORY BURST OXIDASE HOMOLOGS (RBOH) in the response to salt treatment and RBOH inhibition suppresses Na+ efflux from the cells. Although stress-induced-extracellular H2O2 is perceived by HPCA1, leading to an increase in [Ca2+]cyt, it is unlikely to play a primary role in the regulation of [Ca2+]cyt in response to salt stress because both hpca1 mutants and wild-type plants respond to NaCl treatment similarly. ROS signaling plays an important role in salt tolerance but excess ROS beyond their signaling function significantly reduces tolerance to salt stress, as demonstrated in plants that possess an improved antioxidant system through the overexpression of antioxidant enzymes or the foliar application of nanoparticles. The signaling mechanisms are summarized in the green section in Figure 3.
2.4.1. Crop Sensitivity to Low Temperatures
Crops can be classified with respect to their frost resistance as chilling sensitive, chilling tolerant, or freezing tolerant. Sensitivity to temperature thresholds varies according to crop species, cultivar, and an individual plant’s developmental stage. Many important crops can build a cold tolerance but sudden temperature changes, the occurrence of which is increasing with climate change, do not allow for the process of acclimatization. The absence of low-temperature-induced cold-hardening caused by the warm weather prevalent during the fall/winter and reduced snow cover may expose the plants to unforeseen freezing conditions, which they cannot survive. If the temperature is not lethal, low temperatures can still influence the vegetative and reproductive growth of the plants. Cold stress can lead to poor germination, chlorosis, wilting, growth retardation, flower abscission, pollen sterility, or reduced fruit set. Low temperatures affect not just the overall yield but also the seed and plant quality. A significant decrease in seed size (24%), starch (34%), protein (33%), and fat (43%) reserves caused by cold has been observed in chickpeas (Cicer arietinum), along with an increase in the level of soluble sugars. The total content of grapevine phenolic compounds can decrease after prolonged cold stress. Low temperatures reduce the amylose, amylopectin, and total starch concentrations in grains of wheat, whereas more drastic changes have been observed when low-temperature treatments occur during the booting stage rather than at the jointing stage.
Among the selected crops cultivated in Europe, wheat belongs to a freezing-tolerant species. Potatoes are considered chilling-tolerant crops, whereas maize, tomatoes, and grapes are considered chilling-sensitive crops. Sugar beet is a potential winter crop but low winter temperatures limit its production. It has been shown that temperatures as low as −5 °C do not affect the survival of sugar beet plants, whereas at −7 °C, the plant survival rate decreases to 50% and temperatures from −9 °C to −15 °C completely kills them. Even though wheat is known to tolerate freezing conditions, wheat production can be influenced by late-spring frosts and severe winter frosts without adequate snow cover.
2.4.2. Low-Temperature Signaling
Low temperatures cause changes in the fluidity of the plant cell membrane that are followed by the activation of Ca2+ channels and receptor-like kinases in the plasma membrane. These changes trigger a cascade of Ca2+ and MAPK signals, similar to the heat-stress-sensing mechanism. In plants, there is no known exclusive protein that serves as a cold receptor but there are several candidates, including the G-protein signaling receptor COLD1, CNGCs, glutamate receptors, and PHYB. In rice, COLD1 coupled with RICE G-PROTEIN α SUBUNIT1 (OsRGA1, not to be confused with Arabidopsis DELLA protein AtRGA1) is involved in cold sensing by modulating calcium signals. The expression of CNGCs increases after exposure to cold in rice, tobacco (Nicotiana tabacum), and Brassica oleracea. CNGCs have been described as thermosensors both in Arabidopsis and moss but their molecular mechanisms are still not fully understood. In rice, cngc14 and cngc16 mutants display reduced survival rates and a higher accumulation of hydrogen peroxide after exposure to heat or chilling stress, which indicates a critical role of CNGC genes under both conditions. Glutamate receptors AtGLR1.2 and 1.3 positively enhance cold tolerance in Arabidopsis by promoting jasmonate accumulation in response to cold. The perception of low temperatures initializes the ICE-CBF-COR signaling pathway, which consists of an INDUCER OF CBF EXPRESSION (ICE), C-REPEAT BINDING FACTOR (CBFs), and COLD-RESPONSIVE GENES (CORs). ICE1 is an MYC-like basic helix–loop–helix transcription factor that binds to the MYC cis-acting elements in the CBF promoter and positively regulates its function. The function of ICE1 depends on its post-translational modification by HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES 1 (HOS1). In maize, ICE1 not only regulates the expression of CBFs directly but also changes amino-acid metabolism and thus regulates mitochondrial oxidative bursts that impair cold tolerance. CBFs are described as master transcription factors that regulate the expression of approximately 12% of COR genes, whose products function in the cold acclimation process and the acquisition of freezing tolerance. Proteins involved in cold adaptation include dehydrins, Late Embryogenesis Abundant (LEA) proteins, antifreeze proteins, ROS detoxifiers, enzymes of osmoprotectants biosynthesis, lipid metabolism proteins, chloroplast proteins, and the other metabolites described in a separate section. In Arabidopsis, the three tandemly arranged CBF genes, CBF1, CBF2, and CBF3, are involved in cold acclimation and their expression is induced within 15 min of exposure to low temperatures. Despite the fact that freezing-sensitive tomatoes are unable to cold-acclimate, they encode three CBF homologs; however, only one of them, SlCBF1, is cold-inducible. Even so, the overexpression of tomato LeCBF1 in transgenic Arabidopsis increases its freezing tolerance. CBF homologs have been found in many other crop species such as wheat, barley, maize, lettuce, and apples. The involvement of TaCBF14 and TaCBF15 from winter wheat in the cold acclimation process has been demonstrated by the overexpression of these genes in spring barley, where the transgenes improved the frost tolerance of barley by several degrees.
2.4.3. Role of Redox Changes in Cold Signaling
Recently, H2O2 has been shown to activate plant cold responses through its effect on the sulfenylation of cytosolic ENOLASE 2 (ENO2). In response to H2O2, ENO2 forms oligomers that are imported into the nucleus, where they activate CBF expression. Another described mechanism by which temperatures regulate the activity of CBFs is through cold-mediated redox changes that induce the structural switching and functional activation of CBFs. After exposure to cold, THIOREDOXIN H2 (Trx-h2), which is anchored to cytoplasmic endomembranes through myristoylation, is released and translocates to the nucleus, where it interacts with CBF1. Trx-h2 reduces the oxidized CBF proteins and switches them to an active state to regulate downstream targets. The importance of Trx-h2 in cold tolerance has been demonstrated in Citrullus lanatus but the role of redox regulation in cold signaling in other crops is still not fully understood. The signaling mechanisms are summarized in the blue section in Figure 3.
3.1. Meta-Analysis of Stress-Responsive Genes
Abiotic stresses activate specific molecules and mechanisms in plant organisms. Plants often experience different combinations of stresses, which can result in interactions between specific signaling pathways. A strong effect of combined abiotic stresses on yield parameters has been observed in wheat, maize, and barley. The fresh weight of maize shoots was reduced by 48% (heat-drought), 11% (heat), and 24% (drought) after stress treatment of the FH-988 genotype. The same attribute was reduced by 19% (heat-drought), 13% (heat), and 18% (drought) after stress treatment of the NT-6621 maize genotype. Combined heat and drought stress in barley led to a reduction in yields by more than 95% in all tested varieties. Multiple stress responses could lead to the activation of pathways and specific effects that are still not fully understood. The identification of specific target genes that occur in multiple abiotic stresses could provide a new perspective on this topic.
Meta-analyses are efficient approaches to the identification of important genes in abiotic stress responses. Recently, these bioinformatic analyses uncovered important abiotic stress targets in soya, wheat, and rice. The results of the transcriptomic studies, which are available in the Expression Atlas database, provide a rich resource that allows analyses and comparisons of the effects of different stressors. Here, we focus on the common regulation of genes significantly modulated by drought (or low water potential), heat, cold, or salinity. A total of 10,317 genes were found to be regulated by at least one stress condition, which at least doubled a gene’s expression (Figure 4).
In total, heat regulated 5992 genes (2462 upregulated, 3530 downregulated), cold regulated 4473 genes (2182 upregulated, 2291 downregulated), drought regulated 3875 genes (1509 upregulated, 2366 downregulated), and salt regulated 1857 genes (1143 upregulated, 714 downregulated). The weakest response was observed for the salt-stress treatment. Moreover, salt-responsive genes showed the most regulation compatible with other abiotic stresses. The highest overlap that reflected a similar pattern of expression was seen for salt stress and drought, with 89% of 211 regulated genes. Similar patterns were also observed for common genes with temperature stresses. The least compatible, in terms of gene expression, was the cold treatment, with approximately 50% of genes co-regulated in the same way as heat stress, and surprisingly, also drought stress. Of the total number of 190 genes regulated by all four stresses, only a small fraction (38 upregulated and 11 downregulated) was affected in the same manner.
3.2. Subcellular Localization of Products of Genes Involved in Abiotic Stress Response
Plants respond to unfavorable conditions by changing the patterns of protein expression. Stress signals are usually first recognized by the plasma membrane, where most receptor proteins are localized. Mitochondria and chloroplasts are the primary sites for the production of ROS, and abiotic stress causes an imbalance between ROS and their scavengers, which negatively impacts the cell environment. ROS also act as a signal that is transduced through cellular compartments and regulates gene and protein expression levels. Since different subcellular elements play distinct roles in stress responses, the predicted subcellular localization of the stress-regulated genes’ products was subsequently analyzed (Figure 5A). The relative number of high-confidence marker proteins of genes regulated by abiotic stress was obtained from the SUBA5 (Figure 5A; Arabidopsis Subcellular Database;), and the database provided the predicted localizations for half of the products of regulated genes.
The most obvious change was seen in mitochondria after temperature stress. Both heat and cold stress showed a similar pattern, with a highly enriched group of upregulated genes and a small group of downregulated genes targeted to the mitochondria. A similar pattern was observed for salinity and drought but here it was less apparent. Interestingly, genes of plastid localized proteins showed different patterns compared to those of mitochondria, with a higher fraction of downregulated genes, especially after cold and salinity treatment. A very specific response to stress was found for Golgi-localized proteins that were downregulated mainly under heat-stress conditions (Figure 5B). Less is known concerning the role of the Golgi than, for example, the role of hormones, either in crops or in Arabidopsis. In total, products of about 90 genes responsive to stresses were localized to the Golgi, 55 of which were downregulated by heat stress, suggesting an exceptional interaction between heat and the Golgi. The main process represented by these genes includes vesicular transportation, methylation, and pectin biosynthesis related to cell-wall organization. Pectin metabolism has been shown to play a role in heat tolerance in Arabidopsis and rice. Drought and salinity partially overlap in their biophysical effect on plant cells by inducing osmotic stress, and both stresses show similar patterns in terms of cytosolic and extracellular responses. However, they differ significantly in the downregulation of mitochondrial and plastid proteins. Overall, the analysis showed different signatures of specific abiotic stresses.
3.3. Functions of Common Genes Responding Identically to at Least Three Different Abiotic Stresses
Based on the results of the above analysis, 419 genes were found to be affected by at least 3 different stresses that are associated with significant processes in the plant’s abiotic stress response, and these genes are regulated in a similar manner (Figure 6, Table S1).
The most represented groups in both upregulated and downregulated genes were cofactor biosynthesis, amino acid metabolism, transcription factors, transport, plant hormone signal transduction, and other enzymes. Categories specific to upregulated genes were carbohydrate metabolism and protein processing in the endoplasmic reticulum. The importance of carbohydrate metabolism for abiotic stress responses has been observed in durum wheat, barley, and tomatoes. The endoplasmic reticulum plays an important role in the reprogramming transcription and translation of stress response regulators. For example, the defense mechanisms of wheat-seedling leaves under salt stress are known to be associated with the endoplasmic reticulum, and SlbZIP60 splicing has been observed as part of the endoplasmic reticulum stress pathway in response to heat and virus infection in tomatoes. Endoplasmic reticulum stress signaling has also been associated with drought tolerance in maize. Categories specific to downregulated genes were purine metabolism, lipid, steroid metabolism, and histones. Drought-tolerant spring-wheat cultivars affected by drought stress exhibit significant changes in purine metabolism. The intermediate product of the purine catabolic pathway, allantoin, has been found to accumulate in higher amounts in the leaves of drought-tolerant genotypes of rice. Maize hybrid ND476 may save energy during drought stress by reducing purine and sterol metabolism. Drought stress in rapeseed has been shown to result in changes in lipid metabolism, specifically a decrease in leaf polar lipids. Changes in membrane lipid metabolism in maize leaves under cold stress were observed by Gu et al.. Lipid alterations during heat stress have also been observed in wheat and tomatoes. Histone modifications altering the responses to salt and drought stress have been observed in rice. Tomato HSFB1 with a histone-like motif has also been observed to function as a transcription coactivator.
3.4. Specific Universal Stress Responsive Genes Affected by Heat, Cold, Drought, and Salinity
A total of 49 genes were found to be affected by all 4 stresses and were associated with various significant processes in plant abiotic stress responses (Figure 7).
In terms of regulation changes, 38 and 11 genes were identified as upregulated and downregulated, respectively. By demonstrating the well-known gene-specific transcriptional regulators associated with the stress response, the analysis supported the idea that their stress response is universal.
The first example is AT5G05410, also known as a DEHYDRATION-RESPONSIVE ELEMENT BINDING PROTEIN 2 (DREB2A). The overexpression of its ortholog OsDREB2A in transgenic rice plants revealed significant tolerance to osmotic, salt, and dehydration stress. ZmDREB2.9-S, ZmDREB2.2, and ZmDREB2.1/2A were upregulated in response to cold, drought, and abscisic acid and may play redundant roles in stress resistance in maize. The overexpression of GmDREB2A;2 in soybean (Glycine max) resulted in improved performance in water-deficit experiments, higher rates in physiological parameters, and a trend of higher yield. AT1G77450 is an upstream transcription factor of the MYB30 transcriptional cascade, which is a key regulator for Arabidopsis root-cell elongation. It also plays a role in stress-induced senescence under ROS signaling. This transcription factor has also been identified in wheat, with a confirmed regulatory role in response to Fusarium graminearum infection.
A second example is the common stress target AT3G14440 (NCED3), a gene in abscisic acid biosynthesis. The expression of NCED3 was found to be significantly upregulated in TaHSFA2d-4A transgenic plants. Wheat homologs of Arabidopsis NCED3 have also been associated with drought tolerance in wheat. NCED3 has also been identified and its role in stress tolerance has been demonstrated in rice, maize, soybeans, and tomatoes.
The most represented group plays an important role in plant metabolism. Specifically, upregulated AT3G14440 and AT1G07430 have been associated with ABA biosynthesis and the regulation of ABA-signaling, supporting the role of ABA as a central regulator of abiotic stress resistance in plants. A drought-tolerant wheat cultivar exhibited a smaller reduction in grain number and a smaller increase in endogenous ABA than a drought-sensitive cultivar. Holesteens et al. (2022) confirmed the regulation of salt-stress responses by ABA in tomatoes. Downregulated AT4G29740 and upregulated AT2G36750 play a role in the metabolism of cytokinins. This observation is consistent with the fact that heat, drought, salt, and cold stress impair the ability of plants to manage water. A reduction in active cytokinin levels can be a result of cold and dehydration stresses in rice. Positive effects of cytokinins on drought tolerance in wheat have been observed by Wang et al. and are discussed, together with other hormones, in a later section.
AT5G11110 and AT3G13784 contribute to sugar synthesis. According to Pommerreging et al. (2018), sugar molecules can function as ROS scavengers and stabilizers of cell membranes and the osmotic cell potential
The members of another strongly represented group play important roles in plant defense. For example, AT1G67360 is involved in the formation of Arabidopsis leaf-lipid droplets that are associated with secondary metabolite biosynthesis and plant resistance to stress. Reduced expression of AT5G03210 in Arabidopsis leads to increased susceptibility to the Plum pox virus. AT2G32190 has been identified as the cysteine-rich transmembrane module that negatively regulates salt stress in Arabidopsis. Downregulated AT2G43550 encodes a defensin-like family protein, and a defense-like gene from winter wheat is possibly involved in enhanced tolerance against pathogens during cold acclimation. The presence of genes related to the biotic stress response supports the notion of intersections between biotic and abiotic stress responses. This phenomenon has been observed in Arabidopsis, rice, maize, wheat, and tomatoes.
In addition to the well-known genes involved in stress responses, our bioinformatic analysis also revealed five interesting candidates in stress responses without a characterized biological function: AT1G67920, AT5G61820, AT5G15190, AT5G19875, and AT2G26530.
4. Stress and Metabolites
Plants respond to abiotic stress by producing various metabolites that help them to deal with ever-changing environments. Fine-tuning the production of primary metabolites, such as carbohydrates, organic and amino acids, is essential for plant growth, development, defense, and stress adaptation. Secondary metabolites (SM) are synthesized from the intermediates of primary carbon metabolism and are important for a plant’s defenses and its interactions with the environment. They include phenolics, carotenoids, flavonoids, sulfur-containing SM, nitrogen-containing SM, and volatile organic compounds. In responding to stress, these compounds have roles as antioxidants, ROS scavengers, compatible solutes, and signal molecules, as well as in helping to maintain membrane stability. Plant hormones are small compounds derived from various essential metabolic pathways that regulate primary and secondary metabolism on the molecular scale. On the higher scales, phytohormones orchestrate growth, development, and interaction with the environment, including biotic and abiotic stresses. Many studies of plant metabolome changes in response to abiotic stress have been conducted in recent years. Table 2 summarizes the metabolites involved in the responses to heat, drought, salinity, and cold, which have been identified in various crop species in the last six years (2017–2022). This review does not discuss ROS metabolism and signaling, which was comprehensively summarized in.
4.1.1. Amino Acids and Analogues
Changes in amino acid levels are associated with all abiotic stresses (Table 2). Of the amino acids, proline is a multi-functional molecule that accumulates in high concentrations in response to a variety of abiotic stresses and provides a supply of energy for plant growth once the stress is relieved. Together with other osmolytes, it also mitigates the adverse effects of oxidative stress by scavenging oxygen species. The use of transgenic plants engineered to synthesize proline more rapidly has been reported in numerous studies as having a positive influence on abiotic stress tolerance. The main proline biosynthetic gene is PYRROLINE-5-CARBOXYLATE SYNTHASE (P5CS) and its stress-inducible expression has been shown to be a better strategy than constitutive expression. This is because negative effects, such as hampered growth and decreased productivity of transgenic plants, can be reduced. Glycine-betaine, an amino acid analog, is another osmoprotectant that interacts with molecules involved in ROS scavenging and membrane stabilization and it also plays a role in the induction of stress-responsive genes. Modification of the glycine–betaine biosynthetic pathway has also been shown to improve the abiotic stress resistance of crops. In plants, glycine–betaine is synthesized from choline and betaine aldehyde via oxidation mediated by the key enzymes choline monooxygenase and BETAINE ALDEHYDE DEHYDROGENASE (BADH). The overexpression of BADH is beneficial to drought tolerance in maize and salt-stress tolerance in tomatoes and it improves temperature-stress tolerance in wheat. BADH genes are also present in species that do not accumulate glycine betaine such as Arabidopsis and rice. Two genes, ALDH10A8 and ALDH10A9, have been identified to code for BADH in Arabidopsis and shown to function in the plant’s response to heat stress. It has been suggested that ALDH10A8 and ALDH10A9 contribute to γ-aminobutyric acid (GABA) biosynthesis, which acts as a compatible solute and signal molecule and can alleviate the effects of various abiotic stresses.
4.1.2. Organic Acids
Organic acids can regulate a broad range of cellular processes by modifying cellular pH and the cell redox state. They are also involved in the chemical modification of proteins, which alters their in vivo activity. Besides their roles in development, nutrient uptake, and detoxification, their synthesis and metabolism are strongly influenced by abiotic stress conditions. Krebs cycle intermediates serve as direct markers of photosynthetic function and as mediators of osmotic adaptation. Salt-tolerant cultivars of broccoli showed higher concentrations of several Krebs-cycle metabolites, e.g., citric, succinic, malic, and fumaric acids, as well as the substrates of some anaplerotic reactions such as aspartic and glutamic acid. Enhanced acetic acid accumulation in Arabidopsis improves its drought-stress tolerance via jasmonic acid signaling. Endogenous citric acid levels increase in response to various types of abiotic stress and the exogenous application of citric acid appears to alleviate the negative impact of these stresses on crop growth and yield.
4.1.3. Carbohydrates
Sugars are not only a source of energy for the plant but they also act as regulators of various biological processes. In addition, they can serve as compatible solutes that protect cell membranes and proteins and maintain cell turgor pressure. Abiotic stress triggers the accumulation of soluble sugars and polyols in plants, including sucrose, glucose, trehalose, fructose, mannitol, sorbitol, and inositol.
Sucrose is the main form of assimilated carbon and the major transport molecule in higher plants. Under stress conditions, sucrose acts as an osmoregulatory molecule that prevents dehydration and regulates the expression of transcription factors and other genes involved in hormonal and defense signaling. Since stress conditions may inhibit photosynthesis and thus limit the amount of sucrose supply, sucrose transporters (SUCs or SUTs) are a key component in securing sucrose distribution and plant stress tolerance.
Trehalose is a nonreducing disaccharide that can protect cell molecules by stabilizing biological membranes and proteins from environmental stress. TREHALOSE-6-PHOSPHATE SYNTHASE (TPS) and TREHALOSE-6-PHOSPHATE PHOSPHATASE (TPP) are two key enzymes that contribute to its biosynthesis in plants. Jiang et al. generated OsTPP3-overexpressing rice plants that exhibited increased tolerance to simulated drought conditions as a result of changes in the expression of ABA biosynthetic and abiotic stress-related genes. Enhanced tolerance to heat stress has been observed in tomato plants overexpressing a trehalose-6-phosphate synthase/phosphatase fusion gene derived from E. coli. An improvement in crop performance under osmotic stress by manipulating the levels of trehalose has been conferred in various other species such as common beans, maize, or soybeans. Trehalose-6-phosphate (T6P), a precursor of trehalose, is an essential signal metabolite and acts as a regulator of sucrose levels in plants. Under changing environmental conditions, modification of T6P signaling seems to be an effective approach to boosting plants’ performance. The application of plant-permeable analogs of T6P to vegetative tissue improves recovery from drought.
Fructans are water-soluble polymers of fructose that are frequently correlated with improved freezing tolerance. Their protective function is provided by their high water solubility and the resistance of fructan to membrane-damaging crystallization at freezing temperatures. Starch represents the primary carbon reserve in plants. Dynamic changes in the starch–sugar interconversion enable plants to cope with abiotic stresses through the redistribution of energy and carbon when photosynthetic processes are limited. Cellulose is the main component of the cell wall and its content has been shown to be reduced after exposure to salt stress. Cell wall extensibility, which is provided by the relaxation of cell-wall polysaccharides, seems to be an important feature under stress conditions that enables cells to enlarge. The modification of cell-wall architecture is partially mediated by xyloglucan modification using XYLOGLUCAN ENDOTRANSGLUCOSYLASES/HYDROLASES (XTH,). In tomato plants, the constitutive expression of a hot pepper (Capsicum annuum), xyloglucan endotransglucosylase/hydrolase CaXTH3, increased plant tolerance to salt and drought stresses without a negative impact on phenotype. Pectins are acidic polysaccharides and their increased content in the cell-wall composition of root tips correlates with a higher salt tolerance of soybeans.
4.1.4. Sugar Alcohols
Sugar alcohols, referred to as polyols, act both as osmotic regulators and redox balance maintainers that help plants deal with adverse conditions. One of them, mannitol, is present in many crop species but not all plants can synthesize it. The exogenous application of mannitol to salt-stressed wheat has been shown to improve its salt tolerance by enhancing the activities of antioxidant enzymes, and the ectopic expression of the MANNITOL-1-PHOSPHATE DEHYDROGENASE gene (mtlD) for the biosynthesis of mannitol has been shown to improve wheat and peanut (Arachis hypogaea) tolerance to water stress and salinity. Inositol is a cyclic polyol that has been shown to positively regulate cold tolerance in rapeseed by inhibiting CALCINEURIN B-LIKE1 (CBL1) and the induction of Ca2+ Influx. The overexpression of the inositol biosynthetic gene MYO-INOSTITOL-1-PHOSPHATE SYNTHASE (GsMIPS2) from wild soybeans has been shown to increase the tolerance of Arabidopsis to salt stress. Sorbitol is produced in parallel with sucrose during photosynthesis and serves as an energy translocation compound. The exogenous application of sorbitol was shown to alleviate the negative effects of salt by reducing the H2O2 and malondialdehyde (MDA) contents in salt-sensitive tomatoes but had no positive effect on a salt-tolerant cultivar.
4.2. Secondary Metabolites
Secondary metabolites are derivatives of primary metabolites that are produced by plants. They can be divided into three major groups: phenolics, terpenes, and nitrogen/sulfur-containing compounds.
4.2.1. Phenolics
Phenolics are ubiquitous aromatic compounds that have roles in plant-defense mechanisms against pathogens and abiotic stressors such as drought, salinity, and UV. For example, in the total content of phenolic acids of wheat genotypes, flavonoids have been shown to increase as the growing temperature increases. Under water-deficit stress, a stress-tolerant genotype of durum wheat has been shown to have higher total phenolic content in leaf tissue compared to stress-sensitive genotypes and higher total phenolic content in mature grains compared to a control. In response to salt stress, total phenolic and flavonoid compounds have been shown to increase in wheat and maize. The redirection of metabolic flux from lignin biosynthesis to flavonoid biosynthesis under salt, heat, and drought has been shown to lead to the accumulation of flavonoid glycosides in rice. Thermal stress in tomato and watermelon plants has been shown to cause the accumulation of soluble phenolics. The importance of flavonoids in freezing tolerance has been demonstrated in different Arabidopsis accessions.
4.2.2. Terpenes
Terpenes perform complex roles in plant defenses against pathogens and herbivores, as well as other stressors. For example, terpenoids, specifically phytoalexins, accumulate in maize roots under drought and salinity stress, suggesting that they play a role in osmotic stress tolerance; Bertamini et al. observed a connection between monoterpene emission and heat-stress resistance in grapevines. Emissions of terpenes from tomato plants under salinity stress have been shown to increase in proportion to the salt concentration in the soil. Mono- and sesquiterpene emissions have been shown to increase with the severity of cold and heat stress in tomatoes.
4.2.3. Nitrogen/Sulfur-Containing Compounds
Nitrogen/sulfur-containing compounds include cyanogenic glycosides, alkaloids, and glucosinolates. These compounds are known for their role in biotic stress resistance but they also play an important role in abiotic stress. For example, drought stress in Chinese cabbage has been shown to induce the accumulation of glucosinolates in leaves, leading to stomatal closure, and glucosinolate metabolism has been shown to be overrepresented in wheat under the combined stresses of salt and heat. Alkaloids are better known for their role in biotic stress resistance, but they also play important roles in oxidative stress and abiotic stress since high temperatures during the initiation of flowering up to pod ripening have been shown to result in a higher alkaloid content of lupin seeds.
4.3. Phytohormones
Plant hormones are one of the most important elements in a plant’s ability to adapt to different environmental conditions. Although hormone molecules are produced in low concentrations, they are acutely sensitive to changing conditions and provide important short- and long-distance signals. Recently, stress-related phytohormones have been classified into nine groups—ABA, auxins (AUX), brassinosteroids (BR), cytokinins (CK), ethylene (ET), gibberellins (GA), jasmonates (JA), salicylic acid (SA), and strigolactones (SL). The biosynthetic pathways of phytohormones were recently comprehensively reviewed in. Here, we focus mainly on their role in stress responses to abiotic stresses in crop plants.
Phytohormones can be classified according to many stress-related criteria. One of these is the significance of the phytohormone in plant stress resistance. Based on this criterion, hormones, together with their signaling cascades, can be divided into three groups: those that mainly increase resistance, those that decrease resistance to abiotic stresses, and hormones with highly context-dependent effects (Figure 8). ABA, SA, JA, BR, AUX, and SL can be classified as belonging to the first category. ABA is known to be a master resistance regulator for a range of stresses and plays an important role in water management. However, its signaling also modulates other aspects of stress resistance, such as the cold-responsive CBF regulon (Table 3). In addition to improved water management, plants under stress require the protection and maintenance of photosynthetic processes, control of the ROS level, and biosynthesis of protective compounds such as osmolytes, cryoprotectants, or scavengers of reactive species (Table 3). Another mechanism for increasing resistance to stress is the regulation of growth. AUX are hormones that have a significant impact on root growth and their asymmetric distribution plays an important role in responses to drought and salt stress (Table 3). This strategy may be slower than stomata closure but could be very important in longer time scales. It is not surprising that the phytohormones within this group show agonistic and synergistic properties with each other. Well-known examples are the positive effects of JA, SL, and BR on ABA or interactions between BR and AUX. Interestingly, melatonin has been shown to have a positive effect on stress resistance in various crops but it reportedly decreases the level of ABA, a process that is conserved across the different abiotic stresses.
GA is the only member of the second group. It is a hormone that has predominantly negative effects on plants under stress (Table 3). In non-stressful conditions, GA is an activator of plant growth. This function can be beneficial under some challenging conditions requiring growth such as thermomorphogenesis but it seems that higher GA activity is not particularly compatible with stress resistance. Some hormones in the first group, for example, SA, also improve plant morphological traits (Table 3) but there is likely a difference between growth induced by reducing the negative impact of environmental cues and the direct induction of growth without effective stress reduction.
The effects of two hormone groups, cytokinins and ethylene, appear to be ambiguous. It seems that the effects of these hormones are highly dependent, not only on the plant species but also on the individual members of hormonal signaling, the plant tissue, and the specific conditions affecting the plant. It is, therefore, difficult to classify them into one of the previous categories; their action could be characterized as highly context-dependent. An ambiguous effect of ethylene can be seen, for example, in the response to cold. Ethylene has been shown to act as a negative regulator of freezing tolerance in Arabidopsis by repressing the expression of cold-responsive CBF genes; however, elsewhere, it has been proven that applying 1-aminocyclopropane-1-carboxylate (ACC) can promote freezing resistance in grapevines through the upregulation of ethylene-responsive transcription factor VaERF057. Cytokinins are an important class of hormones whose function is accompanied by intensive crosstalk with other hormones. The molecular mechanism of mutual antagonism between CK and ABA is well-described. The inhibitory effect of CK on root growth suggests a negative role of CK on drought tolerance. This has been confirmed in some studies that utilized mutants of CK signaling in the model plant Arabidopsis. However, under severe stress, CKs have also been shown to significantly increase drought resistance in tobacco and rice. The effect of cytokinin is also dependent on its concentration because, although increased levels of CK activate the antioxidant system, a contrary effect has been observed in tobacco and Arabidopsis plants with high CK levels.
4.4. Other Growth Regulators
Several other growth regulators are known, which are gradually coming to the attention of scientists. Among them, polyamines and melatonin have been studied intensively.
Melatonin has been known for almost 20 years; however, its potential role as a phytohormone with multiple physiological actions has only recently emerged. Interestingly, melatonin has been shown to have a positive effect on stress resistance in various crops but it reportedly decreases the level of ABA, a process that is conserved across the different abiotic stresses.
Polyamines, such as putrescine, spermidine, and spermine, are small organic molecules that are typically elevated in plants under abiotic stress conditions. Moreover, it has been shown that their exogenous application could increase tolerance to drought or cold stress.
Many studies have shown that phytohormones and other growth regulators can improve plant performance under abiotic stress. Thus, the modulation of their metabolism by inhibitors and activators is a promising strategy for protecting plants from yield losses.
5. Conclusions and Future Prospects
Research in recent decades has successfully described some of the molecular mechanisms underlying plant resistance to different abiotic stresses. In this review, we focused on the novel mechanisms of plant resistance to four fundamental environmental factors—drought, heat, cold, and salinity. The majority of the reviewed mechanisms, including stress signaling, hormonal regulation, and metabolic changes, have been revealed in the model plant Arabidopsis but not all mechanisms can be easily applied to crop plants. For example, differences can be found in the effects that plant hormones have on different plant species under stress conditions (Table 3). Novel and species-specific defense mechanisms could be revealed through modern statistical analyses such as genome-wide association studies and further progress can be expected in the identification, characterization, and confirmation of promising targets in the near future. In addition to the analysis of different alleles or single nucleotide polymorphisms, differences in the stress tolerance of younger and older tissues within the same plant body suggest that gene and protein regulation may still teach us many things about plant resistance.
The specificity of calcium signaling remains an open question. It has been shown that various stimuli can activate diverse calcium signatures, resulting in specific gene regulations. However, parameters such as the period or amplitude of the calcium signature cannot fully explain the molecular mechanism of the selection of targets to be activated. In field conditions, plants are usually exposed to multiple stresses. Similar to previous works, our meta-analysis has shown that targets of gene expression can be regulated differently under the influence of different stressors (Figure 4). Thus, experiments employing multiple stress conditions and their performance under field conditions are expected to confirm known mechanisms or raise new questions concerning plant stress resistance in nature. An important factor in stress resistance is light. Light is, of course, the primary source of energy for plants but stress responses are also significantly modulated by light conditions. However, laboratory experiments typically use well-controlled and homogeneous light conditions that differ significantly from the natural variations in the field. As a result, the effects of light on plants in the field are not well-understood. Another aspect of field conditions that could have both stimulatory and inhibitory effects on plants and their response to the environment is the presence of a potent microbiome. Recent research has confirmed the importance of bacteria in plant tolerance. The interactions between plants and other organisms, including hormonal regulations, are very complex and likely highly species-specific but continuing to advance our understanding of them is highly beneficial as we strive to improve the sustainability of our agriculture systems.
The presented meta-analysis also showed that although the number of genes regulated similarly in response to all cardinal stress factors is small, some of them have not yet been characterized. However, whether any of these genes are as critical as DREB2A or NCED3 is a topic for future research.
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Pei S., Liu Y., Li W., Krichilsky B., Dai S., Wang Y., Wang X., Johnson D.M., Crawford B.M., Swift G.B., et al. OSCA1 Is an Osmotic Specific Sensor: A Method to Distinguish Ca2+-mediated Osmotic and Ionic Perception. New Phytol. 2022;235:1665-1678.
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Akita K., Miyazawa Y. The Mechanosensitive Ca2+ Channel, OSCA1.1, Modulates Root Hydrotropic Bending in Arabidopsis Thaliana. Environ. Exp. Bot. 2022;197:104825.
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She K., Pan W., Yan Y., Shi T., Chu Y., Cheng Y., Ma B., Song W. Genome-Wide Identification, Evolution and Expressional Analysis of OSCA Gene Family in Barley (Hordeum vulgare L.). Int. J. Mol. Sci. 2022;23:13027.
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Liu C., Wang H., Zhang Y., Cheng H., Hu Z., Pei Z.-M., Li Q. Systematic Characterization of the OSCA Family Members in Soybean and Validation of Their Functions in Osmotic Stress. Int. J. Mol. Sci. 2022;23:10570.
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Wang P., Qi S., Wang X., Dou L., Jia M., Mao T., Guo Y., Wang X. The OPEN STOMATA1–SPIRAL1 Module Regulates Microtubule Stability during Abscisic Acid-Induced Stomatal Closure in Arabidopsis. Plant Cell. 2023;35:260-278.
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Yuan W., Suo J., Shi B., Zhou C., Bai B., Bian H., Zhu M., Han N. The Barley MiR393 Has Multiple Roles in Regulation of Seedling Growth, Stomatal Density, and Drought Stress Tolerance. Plant Physiol. Biochem. 2019;142:303-311.
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Li Z., Liu C., Zhang Y., Wang B., Ran Q., Zhang J. The BHLH Family Member ZmPTF1 Regulates Drought Tolerance in Maize by Promoting Root Development and Abscisic Acid Synthesis. J. Exp. Bot. 2019;70:5471-5486.
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Yang Y., Shi J., Chen L., Xiao W., Yu J. ZmEREB46, a Maize Ortholog of Arabidopsis WAX INDUCER1/SHINE1, Is Involved in the Biosynthesis of Leaf Epicuticular Very-Long-Chain Waxes and Drought Tolerance. Plant Sci. 2022;321:111256.
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Petrov P., Petrova A., Dimitrov I., Tashev T., Olsovska K., Brestic M., Misheva S. Relationships between Leaf Morpho-Anatomy, Water Status and Cell Membrane Stability in Leaves of Wheat Seedlings Subjected to Severe Soil Drought. J. Agron. Crop Sci. 2018;204:219-227.
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Maiquetía M., Cáceres A., Herrera A. Mycorrhization and Phosphorus Nutrition Affect Water Relations and CAM Induction by Drought in Seedlings of Clusia Minor. Ann. Bot. 2009;103:525-532.
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Gong Z., Xiong L., Shi H., Yang S., Herrera-Estrella L.R., Xu G., Chao D.-Y., Li J., Wang P.-Y., Qin F., et al. Plant Abiotic Stress Response and Nutrient Use Efficiency. Sci. China Life Sci. 2020;63:635-674.
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Parihar P., Singh S., Singh R., Singh V.P., Prasad S.M. Effect of Salinity Stress on Plants and Its Tolerance Strategies: A Review. Environ. Sci. Pollut. Res. 2015;22:4056-4075.
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Kotuby-Amacher J., Koenig R., Kitchen B. Salinity and Plant Tolerance. 2000;1-8.
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Regni L., del Pino A.M., Mousavi S., Palmerini C.A., Baldoni L., Mariotti R., Mairech H., Gardi T., D’Amato R., Proietti P. Behavior of Four Olive Cultivars During Salt Stress. Front. Plant Sci. 2019;10:867.
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Chen F., Fang P., Peng Y., Zeng W., Zhao X., Ding Y., Zhuang Z., Gao Q., Ren B. Comparative Proteomics of Salt-Tolerant and Salt-Sensitive Maize Inbred Lines to Reveal the Molecular Mechanism of Salt Tolerance. Int. J. Mol. Sci. 2019;20:4725.
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van Straten G., Bruning B., de Vos A.C., González A.P., Rozema J., van Bodegom P.M. Estimating Cultivar-Specific Salt Tolerance Model Parameters from Multi-Annual Field Tests for Identification of Salt Tolerant Potato Cultivars. Agric. Water Manag. 2021;252:106902.
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Chourasia K.N., Lal M.K., Tiwari R.K., Dev D., Kardile H.B., Patil V.U., Kumar A., Vanishree G., Kumar D., Bhardwaj V., et al. Salinity Stress in Potato: Understanding Physiological, Biochemical and Molecular Responses. Life. 2021;11:545.
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Guo Q., Meng L., Han J., Mao P., Tian X., Zheng M., Mur L.A.J. SOS1 Is a Key Systemic Regulator of Salt Secretion and K+/Na+ Homeostasis in the Recretohalophyte Karelinia Caspia. Environ. Exp. Bot. 2020;177:104098.
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Ma L., Liu X., Lv W., Yang Y. Molecular Mechanisms of Plant Responses to Salt Stress. Front. Plant Sci. 2022;13:934877.
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Yang Y., Guo Y. Elucidating the Molecular Mechanisms Mediating Plant Salt-Stress Responses. New Phytol. 2018;217:523-539.
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Yue Y., Zhang M., Zhang J., Duan L., Li Z. SOS1 Gene Overexpression Increased Salt Tolerance in Transgenic Tobacco by Maintaining a Higher K+/Na+ Ratio. J. Plant Physiol. 2012;169:255-261.
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el Mahi H., Pérez-Hormaeche J., de Luca A., Villalta I., Espartero J., Gámez-Arjona F., Fernández J.L., Bundó M., Mendoza I., Mieulet D., et al. A Critical Role of Sodium Flux via the Plasma Membrane Na+/H+ Exchanger SOS1 in the Salt Tolerance of Rice. Plant Physiol. 2019;180:1046-1065.
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Olías R., Eljakaoui Z., Li J.U.N., de Morales P.A.Z.A., Marín-Manzano M.C., Pardo J.M., Belver A. The Plasma Membrane Na+ /H+ Antiporter SOS1 Is Essential for Salt Tolerance in Tomato and Affects the Partitioning of Na+ between Plant Organs. Plant Cell Environ. 2009;32:904-916.
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Egea I., Pineda B., Ortíz-Atienza A., Plasencia F.A., Drevensek S., García-Sogo B., Yuste-Lisbona F.J., Barrero-Gil J., Atarés A., Flores F.B., et al. The SlCBL10 Calcineurin B-Like Protein Ensures Plant Growth under Salt Stress by Regulating Na+ and Ca2+ Homeostasis. Plant Physiol. 2018;176:1676-1693.
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Cho J.H., Sim S.-C., Kim K.-N. Calcium Sensor SlCBL4 Associates with SlCIPK24 Protein Kinase and Mediates Salt Tolerance in Solanum lycopersicum. Plants. 2021;10:2173.
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Liu C., Zhu M., Sun J. Overexpression of an Inositol Phosphorylceramide Glucuronosyltransferase Gene IbIPUT1 Inhibits Na+ Uptake in Sweet Potato Roots. Genes. 2022;13:1140.
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Chung J.-S., Zhu J.-K., Bressan R.A., Hasegawa P.M., Shi H. Reactive Oxygen Species Mediate Na+-Induced SOS1 MRNA Stability in Arabidopsis. Plant J. 2007;53:554-565.
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Yan H., Li Q., Park S.-C., Wang X., Liu Y., Zhang Y., Tang W., Kou M., Ma D. Overexpression of CuZnSOD and APX Enhance Salt Stress Tolerance in Sweet Potato. Plant Physiol. Biochem. 2016;109:20-27.
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Evans M.J., Choi W.-G., Gilroy S., Morris R.J. A ROS-Assisted Calcium Wave Dependent on the AtRBOHD NADPH Oxidase and TPC1 Cation Channel Propagates the Systemic Response to Salt Stress. Plant Physiol. 2016;171:1771-1784.
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Faizan M., Bhat J.A., Chen C., Alyemeni M.N., Wijaya L., Ahmad P., Yu F. Zinc Oxide Nanoparticles (ZnO-NPs) Induce Salt Tolerance by Improving the Antioxidant System and Photosynthetic Machinery in Tomato. Plant Physiol. Biochem. 2021;161:122-130.
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Ding Y., Shi Y., Yang S. Advances and Challenges in Uncovering Cold Tolerance Regulatory Mechanisms in Plants. New Phytol. 2019;222:1690-1704.
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Li X., Pu H., Liu F., Zhou Q., Cai J., Dai T., Cao W., Jiang D. Winter Wheat Photosynthesis and Grain Yield Responses to Spring Freeze. Agron. J. 2015;107:1002-1010.
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Thakur P., Kumar S., Malik J.A., Berger J.D., Nayyar H. Cold Stress Effects on Reproductive Development in Grain Crops: An Overview. Environ. Exp. Bot. 2010;67:429-443.
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Borjas A.H., de Leon T.B., Subudhi P.K. Genetic Analysis of Germinating Ability and Seedling Vigor under Cold Stress in US Weedy Rice. Euphytica. 2016;208:251-264.
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Nayyar H., Bains T.S., Kumar S., Kaur G. Chilling Effects during Seed Filling on Accumulation of Seed Reserves and Yield of Chickpea. J. Sci. Food Agric. 2005;85:1925-1930.
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Król A., Amarowicz R., Weidner S. The Effects of Cold Stress on the Phenolic Compounds and Antioxidant Capacity of Grapevine (Vitis vinifera L.) Leaves. J. Plant Physiol. 2015;189:97-104.
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Zhang C., Gu K., Gu D., Zhang S., Wu J. Quantifying the Effect of Low-Temperature Events on the Grain Quality Formation of Wheat. J. Cereal Sci. 2021;100:103257.
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Zhao Y., Li J., Zhao R., Xu K., Xiao Y., Zhang S., Tian J., Yang X. Genome-Wide Association Study Reveals the Genetic Basis of Cold Tolerance in Wheat. Mol. Breed. 2020;40:36.
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Fennell A. Freezing Tolerance and Injury in Grapevines. J. Crop. Improv. 2004;10:201-235.
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Webster T.M., Grey T.L., Scully B.T., Johnson W.C., Davis R.F., Brenneman T.B. Yield Potential of Spring-Harvested Sugar Beet (Beta Vulgaris) Depends on Autumn Planting Time. Ind. Crops Prod. 2016;83:55-60.
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Trnka M., Rötter R.P., Ruiz-Ramos M., Kersebaum K.C., Olesen J.E., Žalud Z., Semenov M.A. Adverse Weather Conditions for European Wheat Production Will Become More Frequent with Climate Change. Nat. Clim. Chang. 2014;4:637-643.
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Guo X., Liu D., Chong K. Cold Signaling in Plants: Insights into Mechanisms and Regulation. J. Integr. Plant Biol. 2018;60:745-756.
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Nawaz Z., Kakar K.U., Ullah R., Yu S., Zhang J., Shu Q.-Y., Ren X. Genome-Wide Identification, Evolution and Expression Analysis of Cyclic Nucleotide-Gated Channels in Tobacco (Nicotiana tabacum L.). Genomics. 2019;111:142-158.
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Zheng Y., Luo L., Wei J., Chen Q., Yang Y., Hu X., Kong X. The Glutamate Receptors AtGLR1.2 and AtGLR1.3 Increase Cold Tolerance by Regulating Jasmonate Signaling in Arabidopsis Thaliana. Biochem. Biophys. Res. Commun. 2018;506:895-900.
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Nawaz Z., Kakar K.U., Saand M.A., Shu Q.-Y. Cyclic Nucleotide-Gated Ion Channel Gene Family in Rice, Identification, Characterization and Experimental Analysis of Expression Response to Plant Hormones, Biotic and Abiotic Stresses. BMC Genom. 2014;15:853.
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Kakar K.U., Nawaz Z., Kakar K., Ali E., Almoneafy A.A., Ullah R., Ren X., Shu Q.-Y. Comprehensive Genomic Analysis of the CNGC Gene Family in Brassica Oleracea: Novel Insights into Synteny, Structures, and Transcript Profiles. BMC Genom. 2017;18:869.
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Finka A., Cuendet A.F.H., Maathuis F.J.M., Saidi Y., Goloubinoff P. Plasma Membrane Cyclic Nucleotide Gated Calcium Channels Control Land Plant Thermal Sensing and Acquired Thermotolerance. Plant Cell. 2012;24:3333-3348.
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Tang K., Zhao L., Ren Y., Yang S., Zhu J., Zhao C. The Transcription Factor ICE1 Functions in Cold Stress Response by Binding to the Promoters of CBF and COR Genes. J. Integr. Plant Biol. 2020;62:258-263.
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Dong C.-H., Agarwal M., Zhang Y., Xie Q., Zhu J.-K. The Negative Regulator of Plant Cold Responses, HOS1, Is a RING E3 Ligase That Mediates the Ubiquitination and Degradation of ICE1. Proc. Natl. Acad. Sci. USA. 2006;103:8281-8286.
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Jiang H., Shi Y., Liu J., Li Z., Fu D., Wu S., Li M., Yang Z., Shi Y., Lai J., et al. Natural Polymorphism of ZmICE1 Contributes to Amino Acid Metabolism That Impacts Cold Tolerance in Maize. Nat. Plants. 2022;8:1176-1190.
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Park S., Lee C., Doherty C.J., Gilmour S.J., Kim Y., Thomashow M.F. Regulation of the Arabidopsis CBF Regulon by a Complex Low-temperature Regulatory Network. Plant J. 2015;82:193-207.
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Park S., Gilmour S.J., Grumet R., Thomashow M.F. CBF-Dependent and CBF-Independent Regulatory Pathways Contribute to the Differences in Freezing Tolerance and Cold-Regulated Gene Expression of Two Arabidopsis Ecotypes Locally Adapted to Sites in Sweden and Italy. PLoS ONE. 2018;13:e0207723.
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Thomashow M.F., Gilmour S.J., Stockinger E.J., Jaglo-Ottosen K.R., Zarka D.G. Role of the Arabidopsis CBF Transcriptional Activators in Cold Acclimation. Physiol. Plant. 2001;112:171-175.
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Zhang X., Fowler S.G., Cheng H., Lou Y., Rhee S.Y., Stockinger E.J., Thomashow M.F. Freezing-Sensitive Tomato Has a Functional CBF Cold Response Pathway, but a CBF Regulon That Differs from That of Freezing-Tolerant Arabidopsis. Plant J. 2004;39:905-919.
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Würschum T., Longin C.F.H., Hahn V., Tucker M.R., Leiser W.L. Copy Number Variations of CBF Genes at the Fr-A2 Locus Are Essential Components of Winter Hardiness in Wheat. Plant J. 2017;89:764-773.
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Francia E., Barabaschi D., Tondelli A., Laidò G., Rizza F., Stanca A.M., Busconi M., Fogher C., Stockinger E.J., Pecchioni N. Fine Mapping of a HvCBF Gene Cluster at the Frost Resistance Locus Fr-H2 in Barley. Theor. Appl. Genet. 2007;115:1083-1091.
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Qin F., Sakuma Y., Li J., Liu Q., Li Y.-Q., Shinozaki K., Yamaguchi-Shinozaki K. Cloning and Functional Analysis of a Novel DREB1/CBF Transcription Factor Involved in Cold-Responsive Gene Expression in Zea mays L. Plant Cell Physiol. 2004;45:1042-1052.
Not in our library10.1093/pcp/pch118
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Park S., Shi A., Mou B. Genome-Wide Identification and Expression Analysis of the CBF/DREB1 Gene Family in Lettuce. Sci. Rep. 2020;10:5733.
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An J.-P., Yao J.-F., Wang X.-N., You C.-X., Wang X.-F., Hao Y.-J. MdHY5 Positively Regulates Cold Tolerance via CBF-Dependent and CBF-Independent Pathways in Apple. J. Plant Physiol. 2017;218:275-281.
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Soltész A., Smedley M., Vashegyi I., Galiba G., Harwood W., Vágújfalvi A. Transgenic Barley Lines Prove the Involvement of TaCBF14 and TaCBF15 in the Cold Acclimation Process and in Frost Tolerance. J. Exp. Bot. 2013;64:1849-1862.
Not in our library10.1093/jxb/ert050
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Liu W.-C., Song R.-F., Qiu Y.-M., Zheng S.-Q., Li T.-T., Wu Y., Song C.-P., Lu Y.-T., Yuan H.-M. Sulfenylation of ENOLASE2 Facilitates H2O2-Conferred Freezing Tolerance in Arabidopsis. Dev. Cell. 2022;57:1883-1898.e5.
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Lee E.S., Park J.H., Wi S.D., Kang C.H., Chi Y.H., Chae H.B., Paeng S.K., Ji M.G., Kim W.-Y., Kim M.G., et al. Redox-Dependent Structural Switch and CBF Activation Confer Freezing Tolerance in Plants. Nat. Plants. 2021;7:914-922.
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Xu A., Wei N., Hu H., Zhou S., Huang Y., Kong Q., Bie Z., Nie W.-F., Cheng F. Thioredoxin H2 Inhibits the MPKK5-MPK3 Cascade to Regulate the CBF–COR Signaling Pathway in Citrullus Lanatus Suffering Chilling Stress. Hortic. Res. 2023;10:uhac256.
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Zhang H., Zhu J., Gong Z., Zhu J.-K. Abiotic Stress Responses in Plants. Nat. Rev. Genet. 2022;23:104-119.
Not in our library10.1038/s41576-021-00413-0
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Qaseem M.F., Qureshi R., Shaheen H. Effects of Pre-Anthesis Drought, Heat and Their Combination on the Growth, Yield and Physiology of Diverse Wheat (Triticum aestivum L.) Genotypes Varying in Sensitivity to Heat and Drought Stress. Sci. Rep. 2019;9:6955.
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Ayub M., Ashraf M.Y., Kausar A., Saleem S., Anwar S., Altay V., Ozturk M. Growth and Physio-Biochemical Responses of Maize (Zea mays L.) to Drought and Heat Stresses. Plant Biosyst. 2021;155:535-542.
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Mahalingam R., Bregitzer P. Impact on Physiology and Malting Quality of Barley Exposed to Heat, Drought and Their Combination during Different Growth Stages under Controlled Environment. Physiol. Plant. 2019;165:277-289.
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Shahriari A.G., Soltani Z., Tahmasebi A., Poczai P. Integrative System Biology Analysis of Transcriptomic Responses to Drought Stress in Soybean (Glycine max L.). Genes. 2022;13:1732.
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Saidi M.N., Mahjoubi H., Yacoubi I. Transcriptome Meta-Analysis of Abiotic Stresses-Responsive Genes and Identification of Candidate Transcription Factors for Broad Stress Tolerance in Wheat. Protoplasma. 2022.
Not in our library10.1007/s00709-022-01807-5
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Soltanpour S., Tarinejad A., Hasanpur K., Majidi M. A Meta-Analysis of Microarray Data Revealed Hub Genes and Transcription Factors Involved in Drought Stress Response in Rice (Oryza sativa L.). Funct. Plant Biol. 2022;49:898-916.
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Sugio A., Dreos R., Aparicio F., Maule A.J. The Cytosolic Protein Response as a Subcomponent of the Wider Heat Shock Response in Arabidopsis. Plant Cell. 2009;21:642-654.
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Bieniawska Z., Espinoza C., Schlereth A., Sulpice R., Hincha D.K., Hannah M.A. Disruption of the Arabidopsis Circadian Clock Is Responsible for Extensive Variation in the Cold-Responsive Transcriptome. Plant Physiol. 2008;147:263-279.
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Hannah M.A., Wiese D., Freund S., Fiehn O., Heyer A.G., Hincha D.K. Natural Genetic Variation of Freezing Tolerance in Arabidopsis. Plant Physiol. 2006;142:98-112.
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Schlaen R.G., Mancini E., Sanchez S.E., Perez-Santángelo S., Rugnone M.L., Simpson C.G., Brown J.W.S., Zhang X., Chernomoretz A., Yanovsky M.J. The Spliceosome Assembly Factor GEMIN2 Attenuates the Effects of Temperature on Alternative Splicing and Circadian Rhythms. Proc. Natl. Acad. Sci. USA. 2015;112:9382-9387.
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Wong M.M., Bhaskara G.B., Wen T.-N., Lin W.-D., Nguyen T.T., Chong G.L., Verslues P.E. Phosphoproteomics of Arabidopsis Highly ABA-Induced1 Identifies AT-Hook–Like10 Phosphorylation Required for Stress Growth Regulation. Proc. Natl. Acad. Sci. USA. 2019;116:2354-2363.
Not in our library10.1073/pnas.1819971116
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Bhaskara G.B., Nguyen T.T., Verslues P.E. Unique Drought Resistance Functions of the Highly ABA-Induced Clade A Protein Phosphatase 2Cs. Plant Physiol. 2012;160:379-395.
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Allu A.D., Soja A.M., Wu A., Szymanski J., Balazadeh S. Salt Stress and Senescence: Identification of Cross-Talk Regulatory Components. J. Exp. Bot. 2014;65:3993-4008.
Not in our library10.1093/jxb/eru173
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Guan Q., Wu J., Yue X., Zhang Y., Zhu J. A Nuclear Calcium-Sensing Pathway Is Critical for Gene Regulation and Salt Stress Tolerance in Arabidopsis. PLoS Genet. 2013;9:e1003755.
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Osakabe Y., Yamaguchi-Shinozaki K., Shinozaki K., Tran L.-S.P. Sensing the Environment: Key Roles of Membrane-Localized Kinases in Plant Perception and Response to Abiotic Stress. J. Exp. Bot. 2013;64:445-458.
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Khan M., Ali S., Al Azzawi T.N.I., Saqib S., Ullah F., Ayaz A., Zaman W. The Key Roles of ROS and RNS as a Signaling Molecule in Plant–Microbe Interactions. Antioxidants. 2023;12:268.
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Mittler R., Zandalinas S.I., Fichman Y., van Breusegem F. Reactive Oxygen Species Signalling in Plant Stress Responses. Nat. Rev. Mol. Cell Biol. 2022;23:663-679.
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Heazlewood J.L., Verboom R.E., Tonti-Filippini J., Small I., Millar A.H. SUBA: The Arabidopsis Subcellular Database. Nucleic Acids Res. 2007;35:D213-D218.
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Huang Y.-C., Wu H.-C., Wang Y.-D., Liu C.-H., Lin C.-C., Luo D.-L., Jinn T.-L. PECTIN METHYLESTERASE34 Contributes to Heat Tolerance through Its Role in Promoting Stomatal Movement. Plant Physiol. 2017;174:748-763.
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Wang M., Zhu X., Peng G., Liu M., Zhang S., Chen M., Liao S., Wei X., Xu P., Tan X., et al. Methylesterification of Cell-Wall Pectin Controls the Diurnal Flower-Opening Times in Rice. Mol. Plant. 2022;15:956-972.
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Liebermeister W., Noor E., Flamholz A., Davidi D., Bernhardt J., Milo R. Visual Account of Protein Investment in Cellular Functions. Proc. Natl. Acad. Sci. USA. 2014;111:8488-8493.
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Woodrow P., Ciarmiello L.F., Annunziata M.G., Pacifico S., Iannuzzi F., Mirto A., D’Amelia L., Dell’Aversana E., Piccolella S., Fuggi A., et al. Durum Wheat Seedling Responses to Simultaneous High Light and Salinity Involve a Fine Reconfiguration of Amino Acids and Carbohydrate Metabolism. Physiol. Plant. 2017;159:290-312.
Not in our library10.1111/ppl.12513
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Derakhshani Z., Bhave M., Shah R.M. Metabolic Contribution to Salinity Stress Response in Grains of Two Barley Cultivars with Contrasting Salt Tolerance. Environ. Exp. Bot. 2020;179:104229.
Not in our library10.1016/j.envexpbot.2020.104229
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Zhang H., Xiong Y., Huang G., Xu X., Huang Q. Effects of Water Stress on Processing Tomatoes Yield, Quality and Water Use Efficiency with Plastic Mulched Drip Irrigation in Sandy Soil of the Hetao Irrigation District. Agric. Water Manag. 2017;179:205-214.
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Afrin T., Seok M., Terry B.C., Pajerowska-Mukhtar K.M. Probing Natural Variation of IRE1 Expression and Endoplasmic Reticulum Stress Responses in Arabidopsis Accessions. Sci. Rep. 2020;10:19154.
Not in our library10.1038/s41598-020-76114-1
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Zhang J., Liu D., Zhu D., Liu N., Yan Y. Endoplasmic Reticulum Subproteome Analysis Reveals Underlying Defense Mechanisms of Wheat Seedling Leaves under Salt Stress. Int. J. Mol. Sci. 2021;22:4840.
Not in our library10.3390/ijms22094840
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Kaur N., Kaitheri Kandoth P. Tomato BZIP60 MRNA Undergoes Splicing in Endoplasmic Reticulum Stress and in Response to Environmental Stresses. Plant Physiol. Biochem. 2021;160:397-403.
Not in our library10.1016/j.plaphy.2021.01.033
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Xiang Y., Sun X., Gao S., Qin F., Dai M. Deletion of an Endoplasmic Reticulum Stress Response Element in a ZmPP2C-A Gene Facilitates Drought Tolerance of Maize Seedlings. Mol. Plant. 2017;10:456-469.
Not in our library10.1016/j.molp.2016.10.003
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Casartelli A., Melino V.J., Baumann U., Riboni M., Suchecki R., Jayasinghe N.S., Mendis H., Watanabe M., Erban A., Zuther E., et al. Opposite Fates of the Purine Metabolite Allantoin under Water and Nitrogen Limitations in Bread Wheat. Plant Mol. Biol. 2019;99:477-497.
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Dong A., Yang Y., Liu S., Zenda T., Liu X., Wang Y., Li J., Duan H. Comparative Proteomics Analysis of Two Maize Hybrids Revealed Drought-Stress Tolerance Mechanisms. Biotechnol. Biotechnol. Equip. 2020;34:763-780.
Not in our library10.1080/13102818.2020.1805015
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Benhassaine-Kesri G., Aid F., Demandre C., Kader J.-C., Mazliak P. Drought Stress Affects Chloroplast Lipid Metabolism in Rape (Brassica napus) Leaves. Physiol. Plant. 2002;115:221-227.
Not in our library10.1034/j.1399-3054.2002.1150207.x
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Gu Y., He L., Zhao C., Wang F., Yan B., Gao Y., Li Z., Yang K., Xu J. Biochemical and Transcriptional Regulation of Membrane Lipid Metabolism in Maize Leaves under Low Temperature. Front. Plant Sci. 2017;8:2053.
Not in our library10.3389/fpls.2017.02053
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Narayanan S., Tamura P.J., Roth M.R., Prasad P.V.V., Welti R. Wheat Leaf Lipids during Heat Stress: I. High Day and Night Temperatures Result in Major Lipid Alterations. Plant Cell Environ. 2016;39:787-803.
Not in our library10.1111/pce.12649
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Spicher L., Glauser G., Kessler F. Lipid Antioxidant and Galactolipid Remodeling under Temperature Stress in Tomato Plants. Front. Plant Sci. 2016;7:167.
Not in our library10.3389/fpls.2016.00167
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Cheng X., Zhang S., Tao W., Zhang X., Liu J., Sun J., Zhang H., Pu L., Huang R., Chen T. INDETERMINATE SPIKELET1 Recruits Histone Deacetylase and a Transcriptional Repression Complex to Regulate Rice Salt Tolerance. Plant Physiol. 2018;178:824-837.
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Ma S., Tang N., Li X., Xie Y., Xiang D., Fu J., Shen J., Yang J., Tu H., Li X., et al. Reversible Histone H2B Monoubiquitination Fine-Tunes Abscisic Acid Signaling and Drought Response in Rice. Mol. Plant. 2019;12:263-277.
Not in our library10.1016/j.molp.2018.12.005
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Bharti K., von Koskull-Doring P., Bharti S., Kumar P., Tintschl-Korbitzer A., Treuter E., Nover L. Tomato Heat Stress Transcription Factor HsfB1 Represents a Novel Type of General Transcription Coactivator with a Histone-Like Motif Interacting with the Plant CREB Binding Protein Ortholog HAC1[W]. Plant Cell. 2004;16:1521-1535.
Not in our library10.1105/tpc.019927
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Mi H., Muruganujan A., Huang X., Ebert D., Mills C., Guo X., Thomas P.D. Protocol Update for Large-Scale Genome and Gene Function Analysis with the PANTHER Classification System (v.14.0). Nat. Protoc. 2019;14:703-721.
Not in our library10.1038/s41596-019-0128-8
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Mallikarjuna G., Mallikarjuna K., Reddy M.K., Kaul T. Expression of OsDREB2A Transcription Factor Confers Enhanced Dehydration and Salt Stress Tolerance in Rice (Oryza sativa L.). Biotechnol. Lett. 2011;33:1689-1697.
Not in our library10.1007/s10529-011-0620-x
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Filyushin M.A., Kochieva E.Z., Shchennikova A.V. ZmDREB2.9 Gene in Maize (Zea mays L.): Genome-Wide Identification, Characterization, Expression, and Stress Response. Plants. 2022;11:3060.
Not in our library10.3390/plants11223060
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Pagliarini R.F., Marinho J.P., Molinari M.D.C., Marcolino-Gomes J., Caranhoto A.L.H., Marin S.R.R., Oliveira M.C.N., Foloni J.S.S., Melo C.L.P., Kidokoro S., et al. Overexpression of Full-Length and Partial DREB2A Enhances Soybean Drought Tolerance. Agron. Sci. Biotechnol. 2021;8:1-21.
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Maki H., Sakaoka S., Itaya T., Suzuki T., Mabuchi K., Amabe T., Suzuki N., Higashiyama T., Tada Y., Nakagawa T., et al. ANAC032 Regulates Root Growth through the MYB30 Gene Regulatory Network. Sci. Rep. 2019;9:11358.
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Mahmood K., El-Kereamy A., Kim S.-H., Nambara E., Rothstein S.J. ANAC032 Positively Regulates Age-Dependent and Stress-Induced Senescence in Arabidopsis thaliana. Plant Cell Physiol. 2016;57:2029-2046.
Not in our library10.1093/pcp/pcw120
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Soni N., Altartouri B., Hegde N., Duggavathi R., Nazarian-Firouzabadi F., Kushalappa A.C. TaNAC032 Transcription Factor Regulates Lignin-Biosynthetic Genes to Combat Fusarium Head Blight in Wheat. Plant Sci. 2021;304:110820.
Not in our library10.1016/j.plantsci.2021.110820
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Zhao Y., Miao J., He J., Tian X., Gao K., Ma C., Tian X., Men W., Li H., Bi H., et al. Wheat Heat Shock Factor TaHsfA2d Contributes to Plant Responses to Phosphate Deficiency. Plant Physiol. Biochem. 2022;185:178-187.
Not in our library10.1016/j.plaphy.2022.05.035
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Mei F., Chen B., Li F., Zhang Y., Kang Z., Wang X., Mao H. Overexpression of the Wheat NAC Transcription Factor TaSNAC4-3A Gene Confers Drought Tolerance in Transgenic Arabidopsis. Plant Physiol. Biochem. 2021;160:37-50.
Not in our library10.1016/j.plaphy.2021.01.004
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- 250.
Capelle V., Remoué C., Moreau L., Reyss A., Mahé A., Massonneau A., Falque M., Charcosset A., Thévenot C., Rogowsky P., et al. QTLs and Candidate Genes for Desiccation and Abscisic Acid Content in Maize Kernels. BMC Plant Biol. 2010;10:2.
Not in our library10.1186/1471-2229-10-2
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Asghar M.A., Du J., Jiang H., Li Y., Sun X., Shang J., Liu J., Liu W., Imran S., Iqbal N., et al. Shade Pretreatment Enhanced Drought Resistance of Soybean. Environ. Exp. Bot. 2020;171:103952.
Not in our library10.1016/j.envexpbot.2019.103952
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Ayaz M., Ahmad R., Shahzad M., Khan N., Shah M.M., Khan S.A. Drought Stress Stunt Tomato Plant Growth and Up-Regulate Expression of SlAREB, SlNCED3, and SlERF024 Genes. Sci. Hortic. 2015;195:48-55.
Not in our library10.1016/j.scienta.2015.08.025
- 253.
- 254.
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Dong B., Zheng X., Liu H., Able J.A., Yang H., Zhao H., Zhang M., Qiao Y., Wang Y., Liu M. Effects of Drought Stress on Pollen Sterility, Grain Yield, Abscisic Acid and Protective Enzymes in Two Winter Wheat Cultivars. Front. Plant Sci. 2017;8:1008.
Not in our library10.3389/fpls.2017.01008
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Holsteens K., de Jaegere I., Wynants A., Prinsen E.L.J., van de Poel B. Mild and Severe Salt Stress Responses Are Age-Dependently Regulated by Abscisic Acid in Tomato. Front. Plant Sci. 2022;13:269.
Not in our library10.3389/fpls.2022.982622
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Maruyama K., Urano K., Yoshiwara K., Morishita Y., Sakurai N., Suzuki H., Kojima M., Sakakibara H., Shibata D., Saito K., et al. Integrated Analysis of the Effects of Cold and Dehydration on Rice Metabolites, Phytohormones, and Gene Transcripts. Plant Physiol. 2014;164:1759-1771.
Not in our library10.1104/pp.113.231720
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Wang N., Chen J., Gao Y., Zhou Y., Chen M., Xu Z., Fang Z., Ma Y. Genomic Analysis of Isopentenyltransferase Genes and Functional Characterization of TaIPT8 Indicates Positive Effects of Cytokinins on Drought Tolerance in Wheat. Crop J. 2023;11:46-56.
Not in our library10.1016/j.cj.2022.04.010
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Pommerrenig B., Ludewig F., Cvetkovic J., Trentmann O., Klemens P.A.W., Neuhaus H.E. In Concert: Orchestrated Changes in Carbohydrate Homeostasis Are Critical for Plant Abiotic Stress Tolerance. Plant Cell Physiol. 2018;59:1290-1299.
Not in our library10.1093/pcp/pcy037
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Brocard L., Immel F., Coulon D., Esnay N., Tuphile K., Pascal S., Claverol S., Fouillen L., Bessoule J.-J., Bréhélin C. Proteomic Analysis of Lipid Droplets from Arabidopsis Aging Leaves Brings New Insight into Their Biogenesis and Functions. Front. Plant Sci. 2017;8:894.
Not in our library10.3389/fpls.2017.00894
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Castelló M.J., Carrasco J.L., Navarrete-Gómez M., Daniel J., Granot D., Vera P. A Plant Small Polypeptide Is a Novel Component of DNA-Binding Protein Phosphatase 1-Mediated Resistance to Plum Pox Virus in Arabidopsis. Plant Physiol. 2011;157:2206-2215.
Not in our library10.1104/pp.111.188953
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Xu Y., Yu Z., Zhang D., Huang J., Wu C., Yang G., Yan K., Zhang S., Zheng C. CYSTM, a Novel Non-Secreted Cysteine-Rich Peptide Family, Involved in Environmental Stresses in Arabidopsis Thaliana. Plant Cell Physiol. 2017;59:423-438.
Not in our library10.1093/pcp/pcx202
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Koike M., Okamoto T., Tsuda S., Imai R. A Novel Plant Defensin-like Gene of Winter Wheat Is Specifically Induced during Cold Acclimation. Biochem. Biophys. Res. Commun. 2002;298:46-53.
Not in our library10.1016/s0006-291x(02)02391-4
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Saijo Y., Loo E.P. Plant Immunity in Signal Integration between Biotic and Abiotic Stress Responses. New Phytol. 2019;225:87-104.
Not in our library10.1111/nph.15989
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Menna A., Nguyen D., Guttman D.S., Desveaux D. Elevated Temperature Differentially Influences Effector-Triggered Immunity Outputs in Arabidopsis. Front. Plant Sci. 2015;6:995.
Not in our library10.3389/fpls.2015.00995
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Webb K.M., Oña I., Bai J., Garrett K.A., Mew T., Vera Cruz C.M., Leach J.E. A Benefit of High Temperature: Increased Effectiveness of a Rice Bacterial Blight Disease Resistance Gene. New Phytol. 2009;185:568-576.
Not in our library10.1111/j.1469-8137.2009.03076.x
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Negeri A., Wang G.-F., Benavente L., Kibiti C.M., Chaikam V., Johal G., Balint-Kurti P. Characterization of Temperature and Light Effects on the Defense Response Phenotypes Associated with the Maize Rp1-D21autoactive Resistance Gene. BMC Plant Biol. 2013;13:106.
Not in our library10.1186/1471-2229-13-106
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Byamukama E., Seifers D.L., Hein G.L., de Wolf E., Tisserat N.A., Langham M.A.C., Osborne L.E., Timmerman A., Wegulo S.N. Occurrence and Distribution of Triticum Mosaic Virus in the Central Great Plains. Plant Dis. 2013;97:21-29.
Not in our library10.1094/pdis-06-12-0535-re
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Liu B., Ouyang Z., Zhang Y., Li X., Hong Y., Huang L., Liu S., Zhang H., Li D., Song F. Tomato NAC Transcription Factor SlSRN1 Positively Regulates Defense Response against Biotic Stress but Negatively Regulates Abiotic Stress Response. PLoS ONE. 2014;9:e102067.
Not in our library10.1371/journal.pone.0102067
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Rivero R.M., Mittler R., Blumwald E., Zandalinas S.I. Developing Climate-resilient Crops: Improving Plant Tolerance to Stress Combination. Plant J. 2022;109:373-389.
Not in our library10.1111/tpj.15483
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Erb M., Kliebenstein D.J. Plant Secondary Metabolites as Defenses, Regulators, and Primary Metabolites: The Blurred Functional Trichotomy. Plant Physiol. 2020;184:39-52.
Not in our library10.1104/pp.20.00433
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Santner A., Calderon-Villalobos L.I.A., Estelle M. Plant Hormones Are Versatile Chemical Regulators of Plant Growth. Nat. Chem. Biol. 2009;5:301-307.
Not in our library10.1038/nchembio.165
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Liu B., Kong L., Zhang Y., Liao Y. Gene and Metabolite Integration Analysis through Transcriptome and Metabolome Brings New Insight into Heat Stress Tolerance in Potato (Solanum tuberosum L.). Plants. 2021;10:103.
Not in our library10.3390/plants10010103
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Joshi J., Hasnain G., Logue T., Lynch M., Wu S., Guan J.-C., Alseekh S., Fernie A.R., Hanson A.D., McCarty D.R. A Core Metabolome Response of Maize Leaves Subjected to Long-Duration Abiotic Stresses. Metabolites. 2021;11:797.
Not in our library10.3390/metabo11110797
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Bheemanahalli R., Impa S.M., Krassovskaya I., Vennapusa A.R., Gill K.S., Obata T., Jagadish S.V.K. Enhanced N-metabolites, ABA and IAA -conjugate in Anthers Instigate Heat Sensitivity in Spring Wheat. Physiol. Plant. 2020;169:501-514.
Not in our library10.1111/ppl.13109
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Lecourieux D., Kappel C., Claverol S., Pieri P., Feil R., Lunn J.E., Bonneu M., Wang L., Gomès E., Delrot S., et al. Proteomic and Metabolomic Profiling Underlines the Stage- and Time-dependent Effects of High Temperature on Grape Berry Metabolism. J. Integr. Plant Biol. 2020;62:1132-1158.
Not in our library10.1111/jipb.12894
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Qu M., Chen G., Bunce J.A., Zhu X., Sicher R.C. Systematic Biology Analysis on Photosynthetic Carbon Metabolism of Maize Leaf Following Sudden Heat Shock under Elevated CO2. Sci. Rep. 2018;8:7849.
Not in our library10.1038/s41598-018-26283-x
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Paupière M.J., Müller F., Li H., Rieu I., Tikunov Y.M., Visser R.G.F., Bovy A.G. Untargeted Metabolomic Analysis of Tomato Pollen Development and Heat Stress Response. Plant Reprod. 2017;30:81-94.
Not in our library10.1007/s00497-017-0301-6
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Andrade A., Boero A., Escalante M., Llanes A., Arbona V., Gómez-Cádenas A., Alemano S. Comparative Hormonal and Metabolic Profile Analysis Based on Mass Spectrometry Provides Information on the Regulation of Water-Deficit Stress Response of Sunflower (Helianthus annuus L.) Inbred Lines with Different Water-Deficit Stress Sensitivity. Plant Physiol. Biochem. 2021;168:432-446.
Not in our library10.1016/j.plaphy.2021.10.015
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Itam M., Mega R., Tadano S., Abdelrahman M., Matsunaga S., Yamasaki Y., Akashi K., Tsujimoto H. Metabolic and Physiological Responses to Progressive Drought Stress in Bread Wheat. Sci. Rep. 2020;10:17189.
Not in our library10.1038/s41598-020-74303-6
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Hong Y., Ni S.-J., Zhang G.-P. Transcriptome and Metabolome Analysis Reveals Regulatory Networks and Key Genes Controlling Barley Malting Quality in Responses to Drought Stress. Plant Physiol. Biochem. 2020;152:1-11.
Not in our library10.1016/j.plaphy.2020.04.029
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Marček T., Hamow K.Á., Végh B., Janda T., Darko E. Metabolic Response to Drought in Six Winter Wheat Genotypes. PLoS ONE. 2019;14:e0212411.
Not in our library10.1371/journal.pone.0212411
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Wu X., Cai K., Zhang G., Zeng F. Metabolite Profiling of Barley Grains Subjected to Water Stress: To Explain the Genotypic Difference in Drought-Induced Impacts on Malting Quality. Front. Plant Sci. 2017;8:1547.
Not in our library10.3389/fpls.2017.01547
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Sprenger H., Erban A., Seddig S., Rudack K., Thalhammer A., Le M.Q., Walther D., Zuther E., Köhl K.I., Kopka J., et al. Metabolite and Transcript Markers for the Prediction of Potato Drought Tolerance. Plant Biotechnol. J. 2018;16:939-950.
Not in our library10.1111/pbi.12840
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Moschen S., di Rienzo J.A., Higgins J., Tohge T., Watanabe M., González S., Rivarola M., García-García F., Dopazo J., Hopp H.E., et al. Integration of Transcriptomic and Metabolic Data Reveals Hub Transcription Factors Involved in Drought Stress Response in Sunflower (Helianthus annuus L.). Plant Mol. Biol. 2017;94:549-564.
Not in our library10.1007/s11103-017-0625-5
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Chen Y., Wang J., Yao L., Li B., Ma X., Si E., Yang K., Li C., Shang X., Meng Y., et al. Combined Proteomic and Metabolomic Analysis of the Molecular Mechanism Underlying the Response to Salt Stress during Seed Germination in Barley. Int. J. Mol. Sci. 2022;23:10515.
Not in our library10.3390/ijms231810515
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Wan H., Qian J., Zhang H., Lu H., Li O., Li R., Yu Y., Wen J., Zhao L., Yi B., et al. Combined Transcriptomics and Metabolomics Analysis Reveals the Molecular Mechanism of Salt Tolerance of Huayouza 62, an Elite Cultivar in Rapeseed (Brassica napus L.). Int. J. Mol. Sci. 2022;23:1279.
Not in our library10.3390/ijms23031279
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El-Badri A.M., Batool M., Mohamed I.A.A., Wang Z., Khatab A., Sherif A., Ahmad H., Khan M.N., Hassan H.M., Elrewainy I.M., et al. Antioxidative and Metabolic Contribution to Salinity Stress Responses in Two Rapeseed Cultivars during the Early Seedling Stage. Antioxidants. 2021;10:1227.
Not in our library10.3390/antiox10081227
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Liu L., Wang B., Liu D., Zou C., Wu P., Wang Z., Wang Y., Li C. Transcriptomic and Metabolomic Analyses Reveal Mechanisms of Adaptation to Salinity in Which Carbon and Nitrogen Metabolism Is Altered in Sugar Beet Roots. BMC Plant Biol. 2020;20:138.
Not in our library10.1186/s12870-020-02349-9
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Shen Q., Yu J., Fu L., Wu L., Dai F., Jiang L., Wu D., Zhang G. Ionomic, Metabolomic and Proteomic Analyses Reveal Molecular Mechanisms of Root Adaption to Salt Stress in Tibetan Wild Barley. Plant Physiol. Biochem. 2018;123:319-330.
Not in our library10.1016/j.plaphy.2017.12.032
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Borrelli G.M., Fragasso M., Nigro F., Platani C., Papa R., Beleggia R., Trono D. Analysis of Metabolic and Mineral Changes in Response to Salt Stress in Durum Wheat (Triticum Turgidum Ssp. Durum) Genotypes, Which Differ in Salinity Tolerance. Plant Physiol. Biochem. 2018;133:57-70.
Not in our library10.1016/j.plaphy.2018.10.025
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Hossain M.S., Persicke M., ElSayed A.I., Kalinowski J., Dietz K.-J. Metabolite Profiling at the Cellular and Subcellular Level Reveals Metabolites Associated with Salinity Tolerance in Sugar Beet. J. Exp. Bot. 2017;68:5961-5976.
Not in our library10.1093/jxb/erx388
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Cao D., Lutz A., Hill C.B., Callahan D.L., Roessner U. A Quantitative Profiling Method of Phytohormones and Other Metabolites Applied to Barley Roots Subjected to Salinity Stress. Front. Plant Sci. 2017;7:2070.
Not in our library10.3389/fpls.2016.02070
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Yu T., Zhang J., Cao J., Li X., Li S., Liu C., Wang L. Metabolic Insight into Cold Stress Response in Two Contrasting Maize Lines. Life. 2022;12:282.
Not in our library10.3390/life12020282
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Xu G., Li L., Zhou J., Lv D., Zhao D., Qin S. Comparison of Transcriptome and Metabolome Analysis Revealed Differences in Cold Resistant Metabolic Pathways in Different Apple Cultivars under Low Temperature Stress. Hortic. Plant J. 2022.
Not in our library10.1016/j.hpj.2022.09.002
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Liu X., Wei R., Tian M., Liu J., Ruan Y., Sun C., Liu C. Combined Transcriptome and Metabolome Profiling Provide Insights into Cold Responses in Rapeseed (Brassica napus L.) Genotypes with Contrasting Cold-Stress Sensitivity. Int. J. Mol. Sci. 2022;23:13546.
Not in our library10.3390/ijms232113546
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Urrutia M., Blein-Nicolas M., Prigent S., Bernillon S., Deborde C., Balliau T., Maucourt M., Jacob D., Ballias P., Bénard C., et al. Maize Metabolome and Proteome Responses to Controlled Cold Stress Partly Mimic Early-sowing Effects in the Field and Differ from Those of Arabidopsis. Plant Cell Environ. 2021;44:1504-1521.
Not in our library10.1111/pce.13993
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Raza A., Su W., Hussain M.A., Mehmood S.S., Zhang X., Cheng Y., Zou X., Lv Y. Integrated Analysis of Metabolome and Transcriptome Reveals Insights for Cold Tolerance in Rapeseed (Brassica napus L.). Front. Plant Sci. 2021;12:1796.
Not in our library10.3389/fpls.2021.721681
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Garzon C.D., Lequart M., Rautengarten C., Bassard S., Sellier-Richard H., Baldet P., Heazlewood J.L., Gibon Y., Domon J.-M., Giauffret C., et al. Regulation of Carbon Metabolism in Two Maize Sister Lines Contrasted for Chilling Tolerance. J. Exp. Bot. 2020;71:356-369.
Not in our library10.1093/jxb/erz421
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Kou S., Chen L., Tu W., Scossa F., Wang Y., Liu J., Fernie A.R., Song B., Xie C. The Arginine Decarboxylase Gene ADC1, Associated to the Putrescine Pathway, Plays an Important Role in Potato Cold-Acclimated Freezing Tolerance as Revealed by Transcriptome and Metabolome Analyses. Plant J. 2018;96:1283-1298.
Not in our library10.1111/tpj.14126
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Kavi Kishor P.B., Suravajhala P., Rathnagiri P., Sreenivasulu N. Intriguing Role of Proline in Redox Potential Conferring High Temperature Stress Tolerance. Front. Plant Sci. 2022;13:867531.
Not in our library10.3389/fpls.2022.867531
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Guo M., Zhang X., Liu J., Hou L., Liu H., Zhao X. OsProDH Negatively Regulates Thermotolerance in Rice by Modulating Proline Metabolism and Reactive Oxygen Species Scavenging. Rice. 2020;13:61.
Not in our library10.1186/s12284-020-00422-3
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Vendruscolo E.C.G., Schuster I., Pileggi M., Scapim C.A., Molinari H.B.C., Marur C.J., Vieira L.G.E. Stress-Induced Synthesis of Proline Confers Tolerance to Water Deficit in Transgenic Wheat. J. Plant Physiol. 2007;164:1367-1376.
Not in our library10.1016/j.jplph.2007.05.001
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Mattioli R., Costantino P., Trovato M. Proline Accumulation in Plants. Plant Signal. Behav. 2009;4:1016-1018.
Not in our library10.4161/psb.4.11.9797
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Guan C., Cui X., Liu H., Li X., Li M., Zhang Y. Proline Biosynthesis Enzyme Genes Confer Salt Tolerance to Switchgrass (Panicum virgatum L.) in Cooperation with Polyamines Metabolism. Front. Plant Sci. 2020;11:46.
Not in our library10.3389/fpls.2020.00046
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Raza A., Charagh S., Abbas S., Hassan M.U., Saeed F., Haider S., Sharif R., Anand A., Corpas F.J., Jin W., et al. Assessment of Proline Function in Higher Plants under Extreme Temperatures. Plant Biol. 2023;25:379-395.
Not in our library10.1111/plb.13510
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Guerzoni J.T.S., Belintani N.G., Moreira R.M.P., Hoshino A.A., Domingues D.S., Filho J.C.B., Vieira L.G.E. Stress-Induced Δ1-Pyrroline-5-Carboxylate Synthetase (P5CS) Gene Confers Tolerance to Salt Stress in Transgenic Sugarcane. Acta Physiol. Plant. 2014;36:2309-2319.
Not in our library10.1007/s11738-014-1579-8
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Karabudak T., Bor M., Özdemir F., Türkan İ. Glycine Betaine Protects Tomato (Solanum lycopersicum) Plants at Low Temperature by Inducing Fatty Acid Desaturase7 and Lipoxygenase Gene Expression. Mol. Biol. Rep. 2014;41:1401-1410.
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Gupta P., Rai R., Vasudev S., Yadava D.K., Dash P.K. Ex-Foliar Application of Glycine Betaine and Its Impact on Protein, Carbohydrates and Induction of ROS Scavenging System during Drought Stress in Flax (Linum Usitatissimum). J. Biotechnol. 2021;337:80-89.
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Zhao H., Zhang Q., Zhang M., Jin Y.-K., Jiang Z.-Z., Jiang N., Wang Q., Qu J., Guan S.-Y., Wang P.-W. Drought Tolerance in High-Generation Transgenic Maize Inbred Lines Overexpressing the Betaine Aldehyde Dehydrogenase Gene. Cereal Res. Commun. 2021;49:183-192.
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Wang G.P., Zhang X.Y., Li F., Luo Y., Wang W. Overaccumulation of Glycine Betaine Enhances Tolerance to Drought and Heat Stress in Wheat Leaves in the Protection of Photosynthesis. Photosynthetica. 2010;48:117-126.
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Zhang X.-Y., Liang C., Wang G.-P., Luo Y., Wang W. The Protection of Wheat Plasma Membrane under Cold Stress by Glycine Betaine Overproduction. Biol. Plant. 2010;54:83-88.
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Zhao J., Missihoun T.D., Bartels D. The Role of Arabidopsis Aldehyde Dehydrogenase Genes in Response to High Temperature and Stress Combinations. J. Exp. Bot. 2017;68:4295-4308.
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Sita K., Kumar V. Role of Gamma Amino Butyric Acid (GABA) against Abiotic Stress Tolerance in Legumes: A Review. Plant Physiol. Rep. 2020;25:654-663.
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Panchal P., Miller A.J., Giri J. Organic Acids: Versatile Stress-Response Roles in Plants. J. Exp. Bot. 2021;72:4038-4052.
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Chevilly S., Dolz-Edo L., Morcillo L., Vilagrosa A., López-Nicolás J.M., Yenush L., Mulet J.M. Identification of Distinctive Physiological and Molecular Responses to Salt Stress among Tolerant and Sensitive Cultivars of Broccoli (Brassica Oleracea Var. Italica). BMC Plant Biol. 2021;21:488.
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Kim J.-M., To T.K., Matsui A., Tanoi K., Kobayashi N.I., Matsuda F., Habu Y., Ogawa D., Sakamoto T., Matsunaga S., et al. Acetate-Mediated Novel Survival Strategy against Drought in Plants. Nat. Plants. 2017;3:17097.
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Shi D., Sheng Y. Effect of Various Salt–Alkaline Mixed Stress Conditions on Sunflower Seedlings and Analysis of Their Stress Factors. Environ. Exp. Bot. 2005;54:8-21.
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Yu J., Du H., Xu M., Huang B. Metabolic Responses to Heat Stress under Elevated Atmospheric CO2 Concentration in a Cool-Season Grass Species. J. Am. Soc. Hortic. Sci. 2012;137:221-228.
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Hu L., Zhang Z., Xiang Z., Yang Z. Exogenous Application of Citric Acid Ameliorates the Adverse Effect of Heat Stress in Tall Fescue (Lolium arundinaceum). Front. Plant Sci. 2016;7:179.
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El-Hawary M., Nashed M. Effect of Foliar Application by Some Antioxidants on Growth and Productivity of Maize under Saline Soil Conditions. J. Plant Prod. 2019;10:93-99.
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Sami F., Yusuf M., Faizan M., Faraz A., Hayat S. Role of Sugars under Abiotic Stress. Plant Physiol. Biochem. 2016;109:54-61.
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Zepeda A.C., Heuvelink E., Marcelis L.F.M. Carbon Storage in Plants: A Buffer for Temporal Light and Temperature Fluctuations. In Silico Plants. 2023;5:diac020.
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Zandalinas S.I., Balfagón D., Gómez-Cadenas A., Mittler R. Plant Responses to Climate Change: Metabolic Changes under Combined Abiotic Stresses. J. Exp. Bot. 2022;73:3339-3354.
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Jia W., Zhang L., Wu D., Liu S., Gong X., Cui Z., Cui N., Cao H., Rao L., Wang C. Sucrose Transporter AtSUC9 Mediated by a Low Sucrose Level Is Involved in Arabidopsis Abiotic Stress Resistance by Regulating Sucrose Distribution and ABA Accumulation. Plant Cell Physiol. 2015;56:1574-1587.
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Jiang D., Chen W., Gao J., Yang F., Zhuang C. Overexpression of the Trehalose-6-Phosphate Phosphatase OsTPP3 Increases Drought Tolerance in Rice. Plant Biotechnol. Rep. 2019;13:285-292.
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Lyu J.I., Park J.H., Kim J.-K., Bae C.-H., Jeong W.-J., Min S.R., Liu J.R. Enhanced Tolerance to Heat Stress in Transgenic Tomato Seeds and Seedlings Overexpressing a Trehalose-6-Phosphate Synthase/Phosphatase Fusion Gene. Plant Biotechnol. Rep. 2018;12:399-408.
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Nuccio M.L., Wu J., Mowers R., Zhou H.-P., Meghji M., Primavesi L.F., Paul M.J., Chen X., Gao Y., Haque E., et al. Expression of Trehalose-6-Phosphate Phosphatase in Maize Ears Improves Yield in Well-Watered and Drought Conditions. Nat. Biotechnol. 2015;33:862-869.
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Asaf S., Khan A.L., Khan M.A., Imran Q.M., Yun B.-W., Lee I.-J. Osmoprotective Functions Conferred to Soybean Plants via Inoculation with Sphingomonas Sp. LK11 and Exogenous Trehalose. Microbiol. Res. 2017;205:135-145.
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Griffiths C.A., Sagar R., Geng Y., Primavesi L.F., Patel M.K., Passarelli M.K., Gilmore I.S., Steven R.T., Bunch J., Paul M.J., et al. Chemical Intervention in Plant Sugar Signalling Increases Yield and Resilience. Nature. 2016;540:574-578.
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Hisano H., Kanazawa A., Kawakami A., Yoshida M., Shimamoto Y., Yamada T. Transgenic Perennial Ryegrass Plants Expressing Wheat Fructosyltransferase Genes Accumulate Increased Amounts of Fructan and Acquire Increased Tolerance on a Cellular Level to Freezing. Plant Sci. 2004;167:861-868.
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Tamura K., Sanada Y., Tase K., Kawakami A., Yoshida M., Yamada T. Comparative Study of Transgenic Brachypodium Distachyon Expressing Sucrose:Fructan 6-Fructosyltransferases from Wheat and Timothy Grass with Different Enzymatic Properties. Planta. 2014;239:783-792.
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Thalmann M., Santelia D. Starch as a Determinant of Plant Fitness under Abiotic Stress. New Phytol. 2017;214:943-951.
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Takahashi D., Johnson K.L., Hao P., Tuong T., Erban A., Sampathkumar A., Bacic A., Livingston D.P., Kopka J., Kuroha T., et al. Cell Wall Modification by the Xyloglucan Endotransglucosylase/Hydrolase XTH19 Influences Freezing Tolerance after Cold and Sub-zero Acclimation. Plant Cell Environ. 2021;44:915-930.
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Choi J.Y., Seo Y.S., Kim S.J., Kim W.T., Shin J.S. Constitutive Expression of CaXTH3, a Hot Pepper Xyloglucan Endotransglucosylase/Hydrolase, Enhanced Tolerance to Salt and Drought Stresses without Phenotypic Defects in Tomato Plants (Solanum lycopersicum Cv. Dotaerang). Plant Cell Rep. 2011;30:867-877.
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An P., Li X., Zheng Y., Matsuura A., Abe J., Eneji A.E., Tanimoto E., Inanaga S. Effects of NaCl on Root Growth and Cell Wall Composition of Two Soya Bean Cultivars with Contrasting Salt Tolerance. J. Agron. Crop Sci. 2014;200:212-218.
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Seckin B., Sekmen A.H., Türkan İ. An Enhancing Effect of Exogenous Mannitol on the Antioxidant Enzyme Activities in Roots of Wheat Under Salt Stress. J. Plant Growth Regul. 2009;28:12-20.
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Abebe T., Guenzi A.C., Martin B., Cushman J.C. Tolerance of Mannitol-Accumulating Transgenic Wheat to Water Stress and Salinity. Plant Physiol. 2003;131:1748-1755.
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Patel K.G., Mandaliya V.B., Mishra G.P., Dobaria J.R., Thankappan R. Transgenic Peanut Overexpressing MtlD Gene Confers Enhanced Salinity Stress Tolerance via Mannitol Accumulation and Differential Antioxidative Responses. Acta Physiol. Plant. 2016;38:181.
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Yan L., Zeng L., Raza A., Lv Y., Ding X., Cheng Y., Zou X. Inositol Improves Cold Tolerance Through Inhibiting CBL1 and Increasing Ca2+ Influx in Rapeseed (Brassica napus L.). Front. Plant Sci. 2022;13:775692.
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Nisa Z., Chen C., Yu Y., Chen C., Mallano A.I., Xiang-bo D., Xiao-li S., Yan-ming Z. Constitutive Overexpression of Myo-Inositol-1-Phosphate Synthase Gene (GsMIPS2) from Glycine Soja Confers Enhanced Salt Tolerance at Various Growth Stages in Arabidopsis. J. Northeast Agric. Univ. (Engl. Ed.). 2016;23:28-44.
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Jain M., Tiwary S., Gadre R. Sorbitol-Induced Changes in Various Growth and Biochemici Parameters in Maize. Plant Soil Environ. 2010;56:263-267.
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Theerakulp P., Gunnula W. Exogenous Sorbitol and Trehalose Mitigated Salt Stress Damage in Salt-Sensitive but Not Salt-Tolerant Rice Seedlings. Asian J. Crop Sci. 2012;4:165-170.
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Ashraf M.A., Iqbal M., Rasheed R., Hussain I., Riaz M., Arif M.S. Environmental Stress and Secondary Metabolites in Plants. Plant Metabolites and Regulation under Environmental Stress. 2018.
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Zaynab M., Fatima M., Abbas S., Sharif Y., Umair M., Zafar M.H., Bahadar K. Role of Secondary Metabolites in Plant Defense against Pathogens. Microb. Pathog. 2018;124:198-202.
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Kumar S., Abedin M.M., Singh A.K., Das S. Role of Phenolic Compounds in Plant-Defensive Mechanisms. Plant Phenolics in Sustainable Agriculture. 2020;517-532.
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Shamloo M., Babawale E.A., Furtado A., Henry R.J., Eck P.K., Jones P.J.H. Effects of Genotype and Temperature on Accumulation of Plant Secondary Metabolites in Canadian and Australian Wheat Grown under Controlled Environments. Sci. Rep. 2017;7:9133.
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Hichem H., Mounir D., Naceur E.A. Differential Responses of Two Maize (Zea mays L.) Varieties to Salt Stress: Changes on Polyphenols Composition of Foliage and Oxidative Damages. Ind. Crops Prod. 2009;30:144-151.
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Rivero R.M., Ruiz J.M., García P.C., López-Lefebre L.R., Sánchez E., Romero L. Resistance to Cold and Heat Stress: Accumulation of Phenolic Compounds in Tomato and Watermelon Plants. Plant Sci. 2001;160:315-321.
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Toffolatti S.L., Maddalena G., Passera A., Casati P., Bianco P.A., Quaglino F. Role of Terpenes in Plant Defense to Biotic Stress. Biocontrol Agents and Secondary Metabolites. 2021;401-417.
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Vaughan M.M., Christensen S., Schmelz E.A., Huffaker A., Mcauslane H.J., Alborn H.T., Romero M., Allen L.H., Teal P.E.A. Accumulation of Terpenoid Phytoalexins in Maize Roots Is Associated with Drought Tolerance. Plant Cell Environ. 2015;38:2195-2207.
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Bertamini M., Grando M.S., Zocca P., Pedrotti M., Lorenzi S., Cappellin L. Linking Monoterpenes and Abiotic Stress Resistance in Grapevines. BIO Web Conf. 2019;13:1003.
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Tomescu D., Şumălan R., Copolovici L., Copolovici D. The Influence of Soil Salinity on Volatile Organic Compounds Emission and Photosynthetic Parameters of Solanum lycopersicum L. Varieties. Open Life Sci. 2017;12:135-142.
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Copolovici L., Kännaste A., Pazouki L., Niinemets Ü. Emissions of Green Leaf Volatiles and Terpenoids from Solanum lycopersicum Are Quantitatively Related to the Severity of Cold and Heat Shock Treatments. J. Plant Physiol. 2012;169:664-672.
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Fini A., Brunetti C., Loreto F., Centritto M., Ferrini F., Tattini M. Isoprene Responses and Functions in Plants Challenged by Environmental Pressures Associated to Climate Change. Front. Plant Sci. 2017;8:1281.
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Yogendra K.N., Sarkar K., Kage U., Kushalappa A.C. Potato NAC43 and MYB8 Mediated Transcriptional Regulation of Secondary Cell Wall Biosynthesis to Contain Phytophthora Infestans Infection. Plant Mol. Biol. Rep. 2017;35:519-533.
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Eom S., Baek S.-A., Kim J., Hyun T. Transcriptome Analysis in Chinese Cabbage (Brassica Rapa Ssp. Pekinensis) Provides the Role of Glucosinolate Metabolism in Response to Drought Stress. Molecules. 2018;23:1186.
Not in our library10.3390/molecules23051186
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Shunkao S., Theerakulpisut P., Wanichthanarak K., Pongdontri P., Thitisaksakul M. Integrative Physiological and Metabolomics Study Reveals Adaptive Strategies of Wheat Seedlings to Salt and Heat Stress Combination. Plant Growth Regul. 2022.
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Jansen G., Jürgens H.-U., Ordon F. Effects of Temperature on the Alkaloid Content of Seeds of Lupinus angustifolius Cultivars. J. Agron. Crop Sci. 2009;195:172-177.
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Ding F., Wang X., Li Z., Wang M. Jasmonate Positively Regulates Cold Tolerance by Promoting ABA Biosynthesis in Tomato. Plants. 2022;12:60.
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Chi C., Xu X., Wang M., Zhang H., Fang P., Zhou J., Xia X., Shi K., Zhou Y., Yu J. Strigolactones Positively Regulate Abscisic Acid-Dependent Heat and Cold Tolerance in Tomato. Hortic. Res. 2021;8:237.
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Yuan G.-F., Jia C.-G., Li Z., Sun B., Zhang L.-P., Liu N., Wang Q.-M. Effect of Brassinosteroids on Drought Resistance and Abscisic Acid Concentration in Tomato under Water Stress. Sci. Hortic. 2010;126:103-108.
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Altamura M.M., Piacentini D., della Rovere F., Fattorini L., Falasca G., Betti C. New Paradigms in Brassinosteroids, Strigolactones, Sphingolipids, and Nitric Oxide Interaction in the Control of Lateral and Adventitious Root Formation. Plants. 2023;12:413.
Not in our library10.3390/plants12020413
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Li Z., Su X., Chen Y., Fan X., He L., Guo J., Wang Y., Yang Q. Melatonin Improves Drought Resistance in Maize Seedlings by Enhancing the Antioxidant System and Regulating Abscisic Acid Metabolism to Maintain Stomatal Opening Under PEG-Induced Drought. J. Plant Biol. 2021;64:299-312.
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Stavang J.A., Gallego-Bartolomé J., Gómez M.D., Yoshida S., Asami T., Olsen J.E., García-Martínez J.L., Alabadí D., Blázquez M.A. Hormonal Regulation of Temperature-Induced Growth in Arabidopsis. Plant J. 2009;60:589-601.
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Shi Y., Tian S., Hou L., Huang X., Zhang X., Guo H., Yang S. Ethylene Signaling Negatively Regulates Freezing Tolerance by Repressing Expression of CBF and Type-A ARR Genes in Arabidopsis. Plant Cell. 2012;24:2578-2595.
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Sun X., Zhao T., Gan S., Ren X., Fang L., Karungo S.K., Wang Y., Chen L., Li S., Xin H. Ethylene Positively Regulates Cold Tolerance in Grapevine by Modulating the Expression of Ethylene Response Factor 057. Sci. Rep. 2016;6:24066.
Not in our library10.1038/srep24066
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Huang X., Hou L., Meng J., You H., Li Z., Gong Z., Yang S., Shi Y. The Antagonistic Action of Abscisic Acid and Cytokinin Signaling Mediates Drought Stress Response in Arabidopsis. Mol. Plant. 2018;11:970-982.
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Nguyen K.H., van Ha C., Nishiyama R., Watanabe Y., Leyva-González M.A., Fujita Y., Tran U.T., Li W., Tanaka M., Seki M., et al. Arabidopsis Type B Cytokinin Response Regulators ARR1, ARR10, and ARR12 Negatively Regulate Plant Responses to Drought. Proc. Natl. Acad. Sci. USA. 2016;113:3090-3095.
Not in our library10.1073/pnas.1600399113
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Nishiyama R., Watanabe Y., Leyva-Gonzalez M.A., Van Ha C., Fujita Y., Tanaka M., Seki M., Yamaguchi-Shinozaki K., Shinozaki K., Herrera-Estrella L., et al. Arabidopsis AHP2, AHP3, and AHP5 Histidine Phosphotransfer Proteins Function as Redundant Negative Regulators of Drought Stress Response. Proc. Natl. Acad. Sci. USA. 2013;110:4840-4845.
Not in our library10.1073/pnas.1302265110
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Rivero R.M., Kojima M., Gepstein A., Sakakibara H., Mittler R., Gepstein S., Blumwald E. Delayed Leaf Senescence Induces Extreme Drought Tolerance in a Flowering Plant. Proc. Natl. Acad. Sci. USA. 2007;104:19631-19636.
Not in our library10.1073/pnas.0709453104
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Peleg Z., Reguera M., Tumimbang E., Walia H., Blumwald E. Cytokinin-Mediated Source/Sink Modifications Improve Drought Tolerance and Increase Grain Yield in Rice under Water-Stress. Plant Biotechnol. J. 2011;9:747-758.
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Hönig M., Plíhalová L., Husičková A., Nisler J., Doležal K. Role of Cytokinins in Senescence, Antioxidant Defence and Photosynthesis. Int. J. Mol. Sci. 2018;19:4045.
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Novák J., Pavlů J., Novák O., Nožková-Hlaváčková V., Špundová M., Hlavinka J., Koukalová Š., Skalák J., Černý M., Brzobohatý B. High Cytokinin Levels Induce a Hypersensitive-like Response in Tobacco. Ann. Bot. 2013;112:41-55.
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Pavlů J., Kerchev P., Černý M., Novák J., Berka M., Jobe T.O., López Ramos J.M., Saiz-Fernández I., Rashotte A.M., Kopriva S., et al. Cytokinin Modulates the Metabolic Network of Sulfur and Glutathione. J. Exp. Bot. 2022;73:7417-7433.
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Asthir B., Kaur S., Mann S.K. Effect of Salicylic and Abscisic Acid Administered through Detached Tillers on Antioxidant System in Developing Wheat Grains under Heat Stress. Acta Physiol. Plant. 2009;31:1091-1096.
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Rezaul I.M., Baohua F., Tingting C., Weimeng F., Caixia Z., Longxing T., Guanfu F. Abscisic Acid Prevents Pollen Abortion under High-Temperature Stress by Mediating Sugar Metabolism in Rice Spikelets. Physiol. Plant. 2019;165:644-663.
Not in our library10.1111/ppl.12759
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Martínez-Andújar C., Martínez-Pérez A., Albacete A., Martínez-Melgarejo P.A., Dodd I.C., Thompson A.J., Mohareb F., Estelles-Lopez L., Kevei Z., Ferrández-Ayela A., et al. Overproduction of ABA in Rootstocks Alleviates Salinity Stress in Tomato Shoots. Plant Cell Environ. 2021;44:2966-2986.
Not in our library10.1111/pce.14121
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Rubio S., Noriega X., Pérez F.J. Abscisic Acid (ABA) and Low Temperatures Synergistically Increase the Expression of CBF/DREB1 Transcription Factors and Cold-Hardiness in Grapevine Dormant Buds. Ann. Bot. 2019;123:681-689.
Not in our library10.1093/aob/mcy201
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Nai G., Liang G., Ma W., Lu S., Li Y., Gou H., Guo L., Chen B., Mao J. Overexpression VaPYL9 Improves Cold Tolerance in Tomato by Regulating Key Genes in Hormone Signaling and Antioxidant Enzyme. BMC Plant Biol. 2022;22:344.
Not in our library10.1186/s12870-022-03704-8
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Abeysingha D.N., Ozga J.A., Strydhorst S., Doyle P., Iqbal M., Yang R., Reinecke D.M. The Effect of Auxins on Amelioration of Heat Stress-induced Wheat (Triticum aestivum L.) Grain Loss. J. Agron. Crop Sci. 2021;207:970-983.
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Dubas E., Moravčíková J., Libantová J., Matušíková I., Benková E., Żur I., Krzewska M. The Influence of Heat Stress on Auxin Distribution in Transgenic B. Napus Microspores and Microspore-Derived Embryos. Protoplasma. 2014;251:1077-1087.
Not in our library10.1007/s00709-014-0616-1
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Park J.S., Kim H.J., Cho H.S., Jung H.W., Cha J.-Y., Yun D.-J., Oh S.-W., Chung Y.-S. Overexpression of AtYUCCA6 in Soybean Crop Results in Reduced ROS Production and Increased Drought Tolerance. Plant Biotechnol. Rep. 2019;13:161-168.
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Huang D., Wang Q., Duan D., Dong Q., Zhao S., Zhang M., Jing G., Liu C., van Nocker S., Ma F., et al. Overexpression of MdIAA9 Confers High Tolerance to Osmotic Stress in Transgenic Tobacco. PeerJ. 2019;7:e7935.
Not in our library10.7717/peerj.7935
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van den Berg T., Korver R.A., Testerink C.S., ten Tusscher K.H.W.J. Modeling Halotropism: A Key Role for Root Tip Architecture and Reflux Loop Remodeling in Redistributing Auxin. Development. 2016;143:3350-3362.
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Ding Y., Sheng J., Li S., Nie Y., Zhao J., Zhu Z., Wang Z., Tang X. The Role of Gibberellins in the Mitigation of Chilling Injury in Cherry Tomato (Solanum lycopersicum L.) Fruit. Postharvest Biol. Technol. 2015;101:88-95.
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Fatma M., Iqbal N., Sehar Z., Alyemeni M.N., Kaushik P., Khan N.A., Ahmad P. Methyl Jasmonate Protects the PS II System by Maintaining the Stability of Chloroplast D1 Protein and Accelerating Enzymatic Antioxidants in Heat-Stressed Wheat Plants. Antioxidants. 2021;10:1216.
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Yoshida C.H.P., Pacheco A.C., de Lapaz A.M., Gorni P.H., Vítolo H.F., Bertoli S.C. Methyl Jasmonate Modulation Reduces Photosynthesis and Induces Synthesis of Phenolic Compounds in Sweet Potatoes Subjected to Drought. Bragantia. 2020;79:319-334.
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Abdelaal K.A.A., Attia K.A., Alamery S.F., El-Afry M.M., Ghazy A.I., Tantawy D.S., Al-Doss A.A., El-Shawy E.-S.E., Abu-Elsaoud M.A., Hafez Y.M. Exogenous Application of Proline and Salicylic Acid Can Mitigate the Injurious Impacts of Drought Stress on Barley Plants Associated with Physiological and Histological Characters. Sustainability. 2020;12:1736.
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Chakma R., Biswas A., Saekong P., Ullah H., Datta A. Foliar Application and Seed Priming of Salicylic Acid Affect Growth, Fruit Yield, and Quality of Grape Tomato under Drought Stress. Sci. Hortic. 2021;280:109904.
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Marzec M., Daszkowska-Golec A., Collin A., Melzer M., Eggert K., Szarejko I. Barley Strigolactone Signalling Mutant Hvd14.d Reveals the Role of Strigolactones in Abscisic Acid-dependent Response to Drought. Plant Cell Environ. 2020;43:2239-2253.
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Zhang X., Zhang L., Ma C., Su M., Wang J., Zheng S., Zhang T. Exogenous Strigolactones Alleviate the Photosynthetic Inhibition and Oxidative Damage of Cucumber Seedlings under Salt Stress. Sci. Hortic. 2022;297:110962.
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Omoarelojie L.O., Kulkarni M.G., Finnie J.F., Van Staden J. Strigolactone Analog (Rac-GR24) Enhances Chilling Tolerance in Mung Bean Seedlings. S. Afr. J. Bot. 2021;140:173-181.
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