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Plant Metabolomics: An Overview of the Role of Primary and Secondary Metabolites against Different Environmental Stress Factors

Uzma Salam, Shakir Ullah, Zhong-Hua Tang and 5 more

Life · 2023 · Review · CC BY

Abstract

Several environmental stresses, including biotic and abiotic factors, adversely affect the growth and development of crops, thereby lowering their yield. However, abiotic factors, e.g., drought, salinity, cold, heat, ultraviolet radiations (UVr), reactive oxygen species (ROS), trace metals (TM), and soil pH, are extremely destructive and decrease crop yield worldwide. It is expected that more than 50% of crop production losses are due to abiotic stresses. Moreover, these factors are responsible for physiological and biochemical changes in plants. The response of different plant species to such stresses is a complex phenomenon with individual features for several species. In addition, it has been shown that abiotic factors stimulate multi-gene responses by making modifications in the accumulation of the primary and secondary metabolites. Metabolomics is a promising way to interpret biotic and abiotic stress tolerance in plants. The study of metabolic profiling revealed different types of metabolites, e.g., amino acids, carbohydrates, phenols, polyamines, terpenes, etc, which are accumulated in plants. Among all, primary metabolites, such as amino acids, carbohydrates, lipids polyamines, and glycine betaine, are considered the major contributing factors that work as osmolytes and osmoprotectants for plants from various environmental stress factors. In contrast, plant-derived secondary metabolites, e.g., phenolics, terpenoids, and nitrogen-containing compounds (alkaloids), have no direct role in the growth and development of plants. Nevertheless, such metabolites could play a significant role as a defense by protecting plants from biotic factors such as herbivores, insects, and pathogens. In addition, they can enhance the resistance against abiotic factors. Therefore, metabolomics practices are becoming essential and influential in plants by identifying different phytochemicals that are part of the acclimation responses to various stimuli. Hence, an accurate metabolome analysis is important to understand the basics of stress physiology and biochemistry. This review provides insight into the current information related to the impact of biotic and abiotic factors on variations of various sets of metabolite levels and explores how primary and secondary metabolites help plants in response to these stresses.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 19, 2026. Paragraph numbers are ours, so an answer can point at one.

1. Introduction

1Comprehensively, biotic and abiotic stresses negatively affect crop production and cause a marked decrease in annual crop yield, i.e., qualitative and quantitative. Recently, biologists, especially agriculturists, need to find an alternative way to deal with biotic and abiotic stresses such as herbivores, insects, and pathogens, as well as salinity, trace metals (TM) contamination, drought, and extreme temperatures respectively. All these stresses affect the physiological and morphological aspects, such as the hindering of the functional groups of important molecules, e.g., enzymes, polynucleotides, transport systems for substantial ions and nutrients, as well as the growth and metabolic activities of plants. However, to cope with these stresses, plants adopt several mechanisms, including metabolomics, transcriptomics, proteomics, and genomics, individually or in combination. The plant metabolome consists of the following two kinds of metabolites: primary and secondary metabolites. Primary metabolites are essential for the proper growth and development of plants and microorganisms. On the contrary, secondary metabolites are formed near the stationary phase of growth and have no direct role in growth, reproduction, and development. The metabolic profiling of primary and secondary metabolites provides extensive knowledge of biochemical processes that occurs in plant metabolism.

2Modern research endorsed the purpose of several important genes, metabolites, proteins, and molecular systems that induced plant reactions to drought, salt stress, cold, TM, heat, and certain other biotic and abiotic factors. Metabolomics analyses have become an influential tool to monitor plants’ responses to different environmentally stressed conditions. Therefore, the findings of such studies give an understanding of the working of plants in definite circumstances, which are considered an important part of enlightening the molecular processes in responses to various stress conditions. An appropriate data analysis, detection, identification, and evaluation of these metabolites are possible with the help of advanced metabolic tools such as gas chromatography-mass spectrometry (GC-MS), liquid chromatography-mass spectrometry (LC-MS) nuclear magnetic resonance (NMR).

3Furthermore, it is estimated that biotic and abiotic stresses are responsible for more than 50% of crop losses in the world. The findings of Bayer in 2008 demonstrated that crop losses caused by abiotic stressors were significantly higher than by biotic factors. However, the exact loss of crop yield depends on the plant’s developmental stage and the intensity and duration by which various stresses occur. Among other stresses, salinity affects more than 800 million hectares of land—nearly 50% of the total irrigated area, which provides about 33% of the world’s food. In the same way, drought also causes a loss of more than 50% of the average yield of crops. Subsequently, other studies indicated that abiotic factors, such as temperature (low or high), salinity, and drought, significantly decreased plant production if existing alone or in combination. Interestingly, another concern is the aggregation of reactive oxygen species (ROS), which is produced by excessively stressed accumulators of cadmium (Cd), chromium (Cr), lead (Pb), zinc (Zn), and copper (Cu) that can cause oxidation and dysfunction of biological molecules, hence disturbing certain physical and biological processes in plants. Optimizing metabolic flux by the organellar electron transport chain (ETC) is essential in reducing oxidative stress. Consequently, keeping the redox state of a cell is another essential issue that provides the decreasing power necessary for the foraging of ROS.

4Therefore, there is a need for novel, easy, inexpensive, ecologically friendly, and robust crop types that can be conceived by cross-breeding or genetic engineering. For example, recently, different wheat, rice, barley, maize, and other economically crucial varieties of crop plants have been considered very necessary than model plants. However, the development of some modern ‘omics tools, such as genomics, proteomics, transcriptomics, and metabolomics, has rationalized the research of crop plants and abetted the complete study of acquaintances concerning biological components and plant breeding. In this concern, metabolomics gives the possibility to accelerate the selection of superior breeding stock and the screening of elite crop types. Primary and secondary metabolites, with their functional diversity, play an important role in fine-tuning the environmental stress tolerance and productivity in crops. Understanding plant behavior under multiple environmental stressors is one of the ways to deal with agricultural sustainability. In this piece of work, more than 200 published works were considered to provide an overview of the role of primary and secondary metabolites against several abiotic and biotic stressors.

2. Instrumentation Applied in Metabolomics Studies

5The identification of different classes of metabolites in plants is largely based on using hyphenated mass spectrometric methods to chromatographic equipment and electrophoretic approaches. Choosing an appropriate ionization technique and analyzer type for metabolite analysis is important in a mass spectrometer. Through the study of mass spectrometry (MS), ionized molecules are calculated. Similarly, mass-to-charge ratio values (m/z, m-mass, or z-charge) of the produced ions are assessed with the precision of one mass unit and to the fourth decimal point, small or high-resolution mass spectra, after elimination in the MS analyzer. The use of a high-resolution mass analyzer permits the accomplishment of the elemental composition of the identified ions existing in mass spectra. At first, it is probable to estimate the elemental composition and molecular mass of the molecules from enumerated m/z values for protonated [M + H]+ and deprotonated molecules [M − H]−. The clear documentation of compounds is highly dependent on the applied MS system. MS machines designed with electrospray ionization (ESI) and matrix-assisted laser desorption or ionization (MALDI) source could be utilized. The ionization of MALDI can be joined to one or two unified times of flight analyzer (TOF and TOF/TOF). The source of ESI works well through quadrupole (Q), ion trap (IT), time of flight (TOF) analyzer, and a mixture of them. The maximum resolution in the mass analyzer could be attained by ion cyclotron resonance through Fourier Transformation Instruments (FT ICR MS) when the ESI is employed as an ionization system.

6Moreover, designing the experiment according to the Metabolomics Standard Initiative (MSI) is also crucial, which endorses defined measures for the right biological materials preparation, procedures of metabolite extraction, and analytical protocols. Following the regulations that have been stipulated, a sufficient number of sample replications and the conditions under which plant development should occur to be investigated and defined. Similarly, the control of MS parameters in mass spectra registration is necessary. Such data deliver environments for suitable documentation and quantification of metabolites and consistent statistical quantification.

7After employing this method, different statistical calculations could be performed to determine the metabolites’ capacities that allow the defining changes of a specific compound in definite situations. The number of primary and secondary metabolites in a single organism may range from several hundred to tens of thousands, with little variation across orders of magnitude in concentration. Some strategies developed for metabolites analysis include metabolic profiling, metabolic fingerprinting, and target analysis.

8Metabolic profiling is expected a simultaneous measure of a set of metabolites in a sample. Several analytical techniques can be used for metabolic profiling, such as (GC-MS), (LC-MS), and (NMR). To date, GC-MS is the most advanced analytical approach to metabolic profiling in plants. Using GC-MS, it is possible to recognize several hundred compounds belonging to various classes, including sugar, organic acids, amino acids, alcohols, amines, and fatty acids. Similarly, LC-MS provides a better alternative for non-volatile compounds. The importance of LC-MS is increasing in metabolomics, especially after the adoption of ultra-performance liquid chromatography technology that can increase separation efficiency and decrease analysis time. Substantially, NMR spectroscopy offers an entirely different analytical technique compared to MS-based approaches. The sensitivity of the NMR technique is much lower than MS-based techniques; however, the structural content information, reproducibility, and computable aspect could be superior to them. Moreover, the preparation of the sample is simple, more convenient, and non-destructive measurement may possible. These properties of NMR make it an ideal tool for the identification of metabolites through metabolic profiling.

3. Workflow of Plant Metabolomics Analysis

9The metabolomics of plants is very complex and varied in their chemical structure. Extensive identifications and a wide range of metabolic depictions could be attained with the arrangement of two or more metabolomics approaches and analytical methods, with the difference in extraction protocols. Metabolomics analyses comprise the following three key tentative methods: (1) sample preparation, (2) data gaining, and (3) the identification of compounds by using the statistical analysis of the data. The preparation of the sample is a key step because it can contribute to the identification of a wide range of metabolites, which is comprised of tissue collecting, drying, or quenching, and metabolite extraction for analysis (derivatization). Thus, care should be taken in this step to avoid engaging in undesirable variation that can significantly disturb the analysis results. Many methods of enzyme quenching, such as drying, enzyme inhibitors and acids, and high meditations of organic solvents, could also distress the analysis and identification.

10Plant metabolites are structurally different with high complications, such as dissimilar size, solubility, explosive nature, separation, amount, and stability. The extraction method of metabolites relies on varied factors such as the type of plant organs, physical and chemical properties of the targeted metabolites, chemical structure, and the solvent used. Generally, metabolite extraction methods include solvent extraction, supercritical fluid extraction, solid-phase extraction, and sonication. Moreover, other methods are used to extract the essential oils, such as hydrodistillation, vapor-hydrodistillation, vapor-distillation, hydro diffusion, organic solvent extraction, and cold pressing. Though, it is critically essential to evaluate metabolite extraction methodologies for a precise metabolite extraction study because a solvent composition that is good for one chemical class may not be suitable for another chemical class. Moreover, this could not be appropriate for extracting large numbers of metabolites from a specific tissue. So, it is important to understand and monitor the effects of the applied solvent treatment on the sample's metabolic content and profile obtained.

11The measurement of complex metabolites needs an advanced analytical platform for sample analysis. Every platform’s range has a particular constraint, maybe in selectivity or sensitivity. The selection of the analytical platform relies on the study initiated, the group of compounds, and their physiochemical properties, such as polarity, solubility, volatility, and concentration levels. Additionally, one issue is that metabolites occur in a wide dynamic range of concentrations such as nanomolar and millimolar in the plant body. Subsequently, another problem is that not every metabolite is present in each tissue.

12However, the most applied metabolomics approaches in analytical studies are liquid or gas chromatography synchronized with mass spectrometry (LC/GC-MS) and nuclear magnetic resonance spectrometry (NMR). Subsequently, another report demonstrated an integrated technique that combines metabolites extraction and analysis with proteomic and RNA from a single sample that permits the immediate inquiry of all molecular levels and examines their interrelation and co-variance structure. Consequently, biochemical regulation could result in the co-variance design of molecular dynamics in a cellular system. In the context of metabolomics, the block diagram (Figure 1) of a typical experiment shows the following key steps:Sample collection and organization;Metabolites extraction;Derivatization and separation;Data acquisition;Data analysis;Metabolites identification;Data submission to public repositories.

13Sample collection and organization;

14Metabolites extraction;

15Derivatization and separation;

16Data acquisition;

17Data analysis;

18Metabolites identification;

19Data submission to public repositories.

4. Metabolomics for Plant Stress Responses

20Metabolomics is the scientific study of the set of metabolites present within an organism, plant cell, or tissue. However, plant stress is any amendment in the growth and developmental conditions that distracts metabolic homeostasis and needs to modify the metabolic pathways in a process generally designated as acclimatization. Over the last decade, metabolomics has developed promptly and is recognized as the prevailing technology in changing climatic conditions and assessing or elucidating testing phenotypes in assorted living systems. Substantially, it may contribute to studying stress biology in plants or other organisms by recognizing various molecules, such as by-products of stress metabolism and compounds of stress signal transduction and related to the plant acclimation responses. Their application has been driven in several fields, including medicinal, imitation biology, or analytical molding of plants, animals, and microscopic organisms.

21Additionally, to the applicability of other fields, nowadays metabolomics could also be used on a large scale in the assortment procedure of plants and resistant to the varying environmental states. Different findings revealed that drought stress, salinity, extreme temperature, and soil flooding could cause significant instabilities in the pattern of plant metabolome. Metabolomics signifies the ultimate omic’s level in a living system or reveals modifications in the traits of an organism or function. Different findings show the study of metabolomics under several environmental abiotic stresses, such as temperature, salinity and drought, and soil flooding. In the same way, various metals and metalloids including, sulfur, phosphorus, oxidative stress, TM, and the combination of other several stress factors in plants (Table 1). Various environmental factors that could negatively disturb the homeostasis and growth of plants are shown below (Figure 2).

4.1. The Response of Primary Metabolites to Abiotic Stresses

22Plants established several adaptive mechanisms to endure abiotic factors, containing variations of metabolism in various directions, to confirm their existence in combative environmental situations (Table 2). Several plant metabolites could assist and reduce the effect of the harsh stress of salt, drought, and water by acting as osmolytes and osmoprotectants. Examples of such metabolites include dimethylsulfoniopropionate (DMSP) and glycine betaine; sugars, such as sucrose, trehalose, and fructan; amino acids, such as proline and ectoine, as well as some metabolites of polyols, sorbitol, and mannitol. In plants, a wide range of waxy layers known as epicuticular wax keeps water balance during water shortage and acts as a mechanical stoppage to encounter disease-causing agents. Additionally, ascorbic acids, glutamine, alpha-tocopherol, anthocyanins, and carotene shield plant tissues by foraging the intermediates of bustling oxygen produced during oxidative stress. Similarly, several other smaller compounds guard plants against oxidation damage related to various constrictions.

23Besides, the plant’s defense system is related to generating phytoalexins, stimulating the common phenylpropanoid pathway and producing lignin biosynthesis. Further, phytochemicals and hormones such as salicylic acid and methyl salicylate, methyl jasmonate and jasmonic acid, as well as other small molecules formed due to stress, play a significant role against environmental stresses. All of these may also function as signaling compounds by stimulating the resistance system and reactions of acclimation. Among the defense systems of plants, osmotic regulation is one of the broadly pronounced responses to the water shortage that needs the accretion of harmonious solutes, such as sugars, amino acids, polyols, and glycine betaine. These chemical compounds do a significant job in sustaining cell turgor and stabilizing cell membranes and protein. Moreover, other studies designate the importance of these compounds in rehabilitating redox stability through the scavenging of ROS, which could adversely affect cellular structures and metabolism.

4.1.1. Amino Acids

24Amino acids are considered a precursor for protein and other organic molecules, e.g., nucleic acids, which designate an active part in the responses of a plant under several stress factors. Amino acids could also play a significant role in signaling and controlling molecules. Various studies showed that many amino acids stored in plants are apparent to different abiotic stresses. Moreover, the exposure of plants to such stresses appearance an accumulation of proline and other amino acids. In plants, the role played by stored amino acids differs after acting as an osmolyte to adjust ions passage, reducing stomatal opening and reclamation of TM. Moreover, amino acids can also disturb the synthesis and activity of several enzymes, gene expression, and redox state of homeostasis. The accumulation of proline and ectoine is considered the most extensively dispersed osmolytes, as they act as osmoprotectants to protect plants from harmful effects and exciting environmental stresses, including low and high temperature, salinity, UVr, water, and osmotic stresses.

25Primarily, proline is produced from a glutamate and proline metabolizing enzyme, pyrroline-5-carboxylate synthetase (P5CS), which reduces glutamate to pyrroline-5-carboxylate (P5C). At last, from the reduction of P5C, this stress-responsive amino acid forms by pyrroline-5-carboxylate reductases (P5CR). In transgenic plants, the significant role of proline was established during osmotic stress. For example, overexpression of the P5CS gene in soybean increased proline content and, thus, tolerance to salt stress in transgenic plants. Besides osmolytes, proline is thought to accomplish many other important functions related to plant resistance, e.g., ROS scavenging, redox balancing, cytosolic pH buffer, molecular chaperon, and a stabilizer of protein structure. Subsequently, in response to abiotic factors, the enlarged levels of proline were observed for several years to be the stress-responsive feature in plants. The relationship between the accumulation of proline as osmolytes and stress tolerance had a great share because of its applicability to different crops.

26Remarkably, some of the metabolites were related to drought resistance and drought vulnerability of the considered hybrids. Additionally, studies on drought responses at metabolomics levels indicated that Andean potatoes with a phenotype designating greater stress exposure have more proline related to the genetically assembled plant that was a higher dearth-tolerant. It was established that the cultivar with a sensitive phenotype has high-level certain amino acids, containing proline and Gamma-aminobutyric acid (GABA) when barley exposed to salinity stress. It may well advocate a greater liability of these plants to such stress. According to, this accretion could be associated with the deterioration of the leaf and slowing the development of a more subtle genotype. Furthermore, studies on Arabidopsis revealed that proline could be a lethal compound under heat stress, while Charlton et al. found that water deficiency was the cause of the decrease in isoleucine concentration in Pea and Arabidopsis plants.

4.1.2. Polyamines

27Plants are tested by different stress factors and adversely affect their growth, yield, and geographical circulation. To survive the combative environmental stress circumstances, plants have developed many adaptive strategies, amongst which the accumulation of metabolites plays an important defensive role. Metabolites strongly involved in stress resistance are the low-molecular-weight (LMW) acyclic polyamines. Polyamines are the LMW nitrogen-containing organic compounds with more than two amino groups with a positive charge at the cellular pH, allowing them to link with negatively charged molecules, such as nucleic acids, phospholipids, and proteins. Usually, polyamines are polycations essential for plant growth and development and play an important role in abiotic stress resistance in higher plants. Triamine spermidine, tetraamine spermine, and their diamine predecessor, putrescine, are the general polyamines. Because of their cationic nature, these compounds have often been correlated to environmental stresses, such as drought, chilling, heat, TM, and salinity.

28The results of Khan et al. and Capell et al. showed that the accumulation of spermidine with the up-regulation of spermidine synthase of Cucurbita ficifolia augmented several stress responses in a recombinant Arabidopsis plant, such as waterlogging and salinity stresses. It was shown that spermidine acts as a signaling molecule and controls the assertion of intricate genes in drought resistance. Furthermore, it has been demonstrated that polyamines are attributed to being involved in maintaining membranes shielding from damage under stressful environments and controlling the formation of nucleic acid as well as enzyme activity. Additionally, different findings revealed that polyamines play a significant role in oxidative stress by mitigating the balance state of ROS through their direct contact or indirectly regulating the antioxidant system and suppressing ROS production. Moreover, some authors hypothesized that polyamines could act as a cellular signal in plants throughout the stress responses.

4.1.3. Carbohydrates

29Carbohydrates produced during photosynthesis are the main building units that provide energy and support to the plant biomass. Extensive studies revealed that non-living factors lead to the assemblage of non-structural saccharides, such as sucrose and lactose, simple sugars, or polyhydric compounds (alcohols and phenols), amongst various species of plants. Particularly, there is a robust association between carbohydrate accretion and osmotic stress resistance, including oxidative stress (ROS) conditions, salt stress, and the scarcity of water. As a source of carbon and energy in a cell, soluble carbohydrates may take a significant part in the metabolic processes of plants. Several stress factors may impact the level of these soluble carbohydrates because the accumulation of carbohydrates is associated with photosynthesis. Rosa et al. demonstrated that certain soluble sugars, such as sucrose and hexoses, improved stress tolerance by down-regulating the stress-related genes and up-regulating growth-related genes. Though, the contents of certain carbohydrates, such as raffinose, glucose, fructose, and maltose, are highly sensitive to environmental stresses and increase. However, the contents of myoinositol were reduced in barley roots during water-scarce conditions. The findings of Sperdouli and Moustakas revealed an increase and contact of augmented soluble carbohydrates, sustaining a great antioxidant defense in the leaves of Arabidopsis thaliana under dry environmental stress conditions. Studies showed renovation of carbon metabolism under salt-related stress (paraquat) in A. thaliana tissues and inferred by the researchers as a substitute approach to staying alive.

30In water-deficit conditions, soluble sugars function as osmoprotectants, decreasing the harmful impact of osmotic stress and helps in sustaining the turgidity of cell and cell membrane stability by keeping plants from humiliation. Under stress conditions, the increase in sugar quantity is generally the result of carbohydrate hydrolysis that needs enzymes with hydrolytic usage. Moreover, carbohydrates that are soluble, such as disaccharides (sucrose and trehalose), oligosaccharides (raffinose and stachyose), and polymer of fructose molecules (fructans) next to their linked metabolic enzymes are essential compatible osmolytes associated with the scavenging of unstable molecules (ROS) during their assortment in plant tissues. In low-temperature stress, sugar alcohols, such as polyols, function as osmoprotectants and shield cell membranes against ice adhesion. Moreover, carbohydrates may act as signaling molecules. The demonstrated data advocate a specific response of carbohydrates in plants. However, it should be noted that the accumulation of carbohydrates depends on the kind of stress to which it bared.

4.1.4. Glycine Betaine

31Glycine betaine (GB) is a widely studied quat compound, which is active in retaining the water balance between the plant cell and the environment during drought conditions. Moreover, GB playing a significant role in stabilizing the macromolecules, shielding photosynthesis, detoxification of reactive oxygen radicals, and as an osmoprotectant. Several studies indicated their importance in improving plant tolerance under various abiotic factors. It has been shown that plants are distinguished according to the formation of GB, such as barley, spinach, maize, and wheat, produce and accumulate a higher quantity of GB in their chloroplast. However, some plant species cannot obtain substantial amounts of GB during stress, such as A. thaliana, rice, and tobacco. Furthermore, it has been shown that transgenic plants could mitigate the impact of abiotic stresses. Therefore, efforts have been made to improve tolerance through glycine betaine biosynthesis to achieve transgenic plants. In transgenic plants, such as Arabidopsis, the cyanobacteria genes, such as glycine sarcosine methyltransferase, and in transgenic maize, a greater amount of GB accumulates. As a result, in transgenic Arabidopsis, resistance to drought and salt is greater; nevertheless, a recombinant plant of maize retained well in cold-related to non-transgenic cultivars.

32Moreover, through genetic engineering, other transgenic plants with a GB-producing capacity have been achieved, including Brassica juncea and tobacco with greater tolerance to salt and chilling, indicating a progressive ability to propagate and grow well related to wild-type in abiotic environmental conditions. Besides, transgenic tomatoes with GB synthesis were more resistant to cold stress and produced fruit at a rate from 10 to 30% higher than the wild type.. Though, the meditations of GB produced in every transgenic plant were scarce to control the osmotic stress to which plants were exposed. Similarly, previous studies showed that GB could enhance root growth and reduce oxidative stress. Additionally, the exogenous application of GB improves the stress tolerance of Cr in chickpea plants and salinity stress in wheat. Consequently, further protecting approaches of GB, such as defense against ROS and heavy metals stress, should be considered, which may enhance the tolerance level.

4.1.5. Lipids

33Lipids are a fundamental component of biological membranes, particularly the plasma membrane, which serves as the contact between the cell and its surroundings. Lipids can be grouped into eight major types based on the chemical structure in conjunction with distinctive hydrophobic and hydrophilic components, such as fatty acids, glycerides, phosphoglycerides, sphingolipids, steroids, isoprenoids, glycolipids, and polyketides. Being sessile organisms, plants are subjected to a wide variety of biotic and abiotic factors, such as temperature, drought, heavy metals, salinity, and pathogen attack. However, lipid-mediated signaling occurs in response to all these stressors (Figure 2). The plasma membrane, which is typically the signaling source of lipids, is commonly used by plants to sense these stimuli and transform the signal into subsequent biochemical metabolism. Generally, these are acclimating enzymes that have all been proposed as signaling lipids, such as phospholipases, lipid kinases, and phosphatases. Commonly, lysophospholipid, fatty acid, phosphatides, triacylglycerol, inositol phosphate, oxylipins, sphingolipids, and nacylethanolamine are considered the major contributing signaling lipids molecules. The conformation and activity of cellular proteins and metabolites are influenced by signaling lipids because they have the ability to temporarily attract molecular markers to the membrane.

34The enzyme phospholipase A (PLA) is very important in the formation of fatty acids and lysophospholipids. Usually, lysophospholipids are present in very limited amounts in plant tissues; however, in stressed conditions such as freezing their quantity increases. Some reports revealed the physiological role of lysophospholipids against various environmental stresses. Similarly, the phospholipase A2 (PlA2) has been shown to increase the production of some elicitors in poppy plants, while lysophosphatidyl-choline and lysophosphatidyl-ethanolamine act as signals transducers in arbuscular symbiosis in potato.

35Fatty acids have also been demonstrated as stress-responsive lipids in plants. Oleic acids modulate nitric oxide-related proteins, thereby regulating nitric oxide and mitigating tolerance in Arabidopsis. Moreover, fatty acids also regulate drought, salt, and heavy metals tolerance, as well as the wound-induced responses of pathogens/herbivores in plants. Likewise, the responsive role of phosphatidic acid (PA), inositol polyphosphates, oxylipins, sphingolipids, and some other lipids have been studied in various plant species. Some of the environmental stress factors under which the plant lipid responses were reported to include chilling, freezing, and wounding, pathogens, low-temperature stress, salt stress, and water and drought stress response.

4.2. The Response of Secondary Metabolites to Abiotic Stresses

36Primary metabolites are compounds that are related to important physiological functions in organisms. Hence, they are generally found in all plant species and are directly involved in growth, development, and reproduction. Compared to primary metabolites, secondary metabolites are very definite in their function, as they are not directly involved in plant growth, development, and reproduction of organisms. Generally, they are species-specific that could be redundant in different situations. Usually, they are made under particular conditions for a definite purpose, such as defense against pathogens infection, enhanced resistance to abiotic stresses, and protect the harmful effect of UVr. Furthermore, secondary metabolites produce different compounds important for several biochemical and biophysical processes in plant cells and tissues (Table 2). However, they have no common familiar physiological functions in plants, such as photosynthesis, respiration, translocation, transportation of solute, acclimatization of nutrients, and differentiation.

37In addition, the specified plant species produce these natural products, and their concentration level is controlled to some extent with the growing period, environments, and adjustment progress. Substantially, they attracted insects and animals for fertilization and seed spreading. The accumulation of phenyl amides in beans to the impact of abiotic factor (heat) was described, proposing an antioxidant role of these secondary metabolites. Modern research tries to identify the key roles the secondary metabolites play in plants as indicators, antioxidants, and for other purposes. Secondary metabolites are also important in plants used by humans. Besides, the compounds of secondary plant metabolites are distinctive means of food essences, medicines, flavorings, and other industrial materials. In plants, the accretion of certain metabolites frequently occurs exposed to different stress factors, such as several phytohormones, elicitors, TM, and signal transduction compounds.

38Some famous examples of secondary plant metabolites with medicinal properties include the anesthetic and antipyretic compounds salicin taken from Salix sp., which is used to make aspirin. Similarly, other pharmacological secondary metabolites, such as taxol (anticancer), sequestered from pacific yew (Taxus brevifolia), and the strong obsessive compound morphine removed from opium (Papaver somniferum). Secondary metabolites have the following three major groups: phenolics, terpenes, and S and N comprising compounds (Figure 3).

4.2.1. Phenolic Compounds

39In plants, phenolic compounds are recognized as the largest and essential group of secondary metabolites changing from simpler aromatic rings to more complicated ones, such as lignin, and play a significant physiological role in increasing the resistance and adaptableness suboptimal circumstances during the life cycle of plants. Phenolics are produced in optimum and sub-optimum environments in plants and play a major role in various developmental mechanisms, such as cell division, balancing hormones, photosynthetic processes, and reproduction, as well as in the mineralization of nutrients. These compounds constitute secondary metabolites, including lignins and tannins, flavonoids, isoflavonoids, anthocyanins, and coumarins. Moreover, all these chemical compounds are produced in plants by the phenylpropanoid pathway, in that phenylalanine compound is the main substratum that can do significant work in the resistance mechanism of plants against various stress factors in the environment.

40The pathway of phenylpropanoid is regulated by biotic and abiotic factors, including drought, salt stress, TM, low or high temperature, wounding, pathogen attack, herbicide treatment, nutrient deficiencies, and UV radiations causing the accumulation of different phenolic compounds. Consequently, the aggregations of phenolic compounds in plant materials are considered an important sustaining strategy of plants in harsh environmental situations. Hence, respond to these stresses and contribute to the removal of ROS, catalyzed-oxygenated reaction with the establishment of metabolic structures and obstructing the processes of oxidative enzymes, thus increasing evolutionary aptness. Besides, phenolic accumulation is also considered a reliable feature and key defense mechanism under stress, leading to the enhanced creation of free radicals and other oxidative species in plants.

41Moreover, to survive in oxidative stress conditions, plants had established two diverse biological ways, such as escaping ROS creation and eliminating it through enzymatic and non-enzymatic processes, such as the deposition of LMW antioxidants. Further, studies revealed that the accumulation of LMW antioxidants results due to the activities of phenylalanine ammonia-lyase (PAL), chalcone synthase (CHS), and other essential enzymes. Various physiological processes of plants related to growth and development in plants comprising seed germination, cell division, and synthesis of photosynthetic pigments, are influenced by phenolic acids and flavonoid accumulation for persistence and adaptation to environmental conflicts. In particular, phenolic compounds consult greater tolerance in plants such as TM stress, which enhances the production of ROS and reduced growth, and phenolic compounds (flavonoids), in response, protect plants from oxidative stress damage through the chelation process. Similarly, when plants are exposed to other abiotic factors can also affect their life cycle. Under drought conditions, the concentration of ferulic acid decreased, while the p-coumaric acid and caffeic acid increased in maize xylem sap, which could be supportive in stiffening and lignification of the cell wall. Spatially confined fluctuations in cell wall phenolics were presented to be engaged in the advanced inhibition of wall extensibility and root growth, which can enable root acclimation to drought.

42Various environmental stress factors mediated the synthesis of flavonoids, isoflavonoids, and anthocyanins. In plants, flavonoids play a defensive role due to their antioxidant properties when exposed to a water-deficit situation. Moreover, Nakabayashi et al. indicated that flavonoid significantly improves resistance in A. thaliana in water scare conditions. Similarly, phenolic acids and flavonoids as antioxidants and sunshades are involved in plants’ response to a dry environment. Other studies reported that different polyphenolic was associated with gene expression reforms in an account of potato plants under drought conditions, though the fluctuations were greatly specific to the cultivar. Rodziewicz et al. and Parida et al. suggested that polyphenols are involved in conserving osmotic potential in cells and confiscating free radicals during drought stress. Besides, polyphenols affect the source and movement of organic and inorganic soil nutrients existing for plants and microbes and indicate a reply to nutrient insufficiency, therefore offering a way for identifying nutrient ailments earlier to the occurrence of evident symptoms. Stress conditions of drought and waterlogging increased the flavonoids quercetin and rutin in the herbaceous pharmaceutical plant Hypericum brasiliense, whereas cold stress caused a different reaction. Comparatively, a greater decrease in flavonoids was noticed in the sensitive genotypes; thus, they could show that the flavonoid content was imperative in sustaining the greater antioxidant activity in water-stressed conditions.

43Furthermore, anthocyanins were identified to increase their content in plant tissues against drought and cold stress because of their antioxidant and ROS scavenging properties, which cause protection to plant cells. In red-fleshed apple callus culture, low temperature (16 °C) tempted an increased level of anthocyanin.

44Additionally, the assembly of phenolics rises into the cell wall either as suberin or lignin under low-temperature stress. Though, suberin deposition and lignification increase the adaptability and resistance to cold stress. Similarly, to respond to the negative effects of Uvr, endogenous phenolic compounds (flavonoids) accumulate in plant cells and make a shield under the epidermal layer, which protects the plant and the component of the cell from these harmful radiations. Moreover, flavonolignan silymarin has been reported to accumulate in in-vitro cultures of Silybum marianum upon application of abiotic stress treatments, such as NaCl, polyethylene glycol, and gamma irradiation, because of the defensive mechanisms that cells perform to counteract the stress of these factors. Therefore, stress elicitation successfully produces high-value phytoconstituents from medicinal crops.

4.2.2. Terpenoids

45Plants have developed a complex resistance system that depends on the swift perception and instigation of secondary metabolites to adopt different environmental stress factors in an ecosystem. Among all, terpenoids establish a broad and structurally diverse group of lipophilic secondary metabolites, which are produced in plants from isoprene units (C5H8). Physiologically, terpenoids play an important role as phytohormones, such as the sesquiterpenoid abscisic acid (ABA) and the diterpenoids gibberellic acid (GA), against biotic and abiotic stresses. Studies have shown that the phytohormone abscisic acid (ABA) triggers defense mechanisms, such as facilitating responses to drought and water stress by adapting the membrane properties. Moreover, terpenoids show antioxidant and antibiotic activity that maintains lipid membranes and increases environmental stress tolerance against herbivores.

46Terpenoids also function as phytoalexins (LMW antimicrobial compounds), prepared as part of the plant defense mechanism in response to abiotic and biotic factors. For example, many diterpene phytoalexins have been reported in Oryza sativa. Similarly, in cotton plants, sesquiterpenoid phytoalexins, such as gossypol, hemigossypolone, and heliocides, as defensive metabolites accumulated both above and below the ground against pathogens and herbivores. Moreover, in maize and rice leaves and roots, diterpene phytoalexins are produced, including zealexins, kauralexins, and oryzalexins that exhibit antimicrobial properties and respond against pathogenic fungal blast diseases, such as rice blast caused by Magnaporthe grisea. Additionally, UVr and TM stress induced the accumulation of rice phytoalexins. According to Vaughan et al., the accumulation of phytoalexins in response to drought is root-specific and does not affect the level of phytoalexins aboveground. However, the reduced content of the terpenoid compound was described in cotton species in drought conditions. Yusuf et al. noticed that the increased content of soluble alcohol tocopherol with antioxidant properties shows a significant role in the mitigation of stress by stabilizing the cell membranes induced by salinity, TM, and osmotic potential in B. juncea. Furthermore, the content of saponins in soybean plants was recognized as one of the crucial secondary metabolites related to the resistance of salt stress.

4.2.3. Nitrogen-Containing Secondary Metabolites

47Plants have developed several defense mechanisms against invading enemies, such as microbial pathogens and herbivorous animals, as well as abiotic factors, e.g., drought, waterlogging, and salinity, which are considered for the high loss of crop production worldwide. However, plants have developed a complex defense system of secondary metabolism against these stressors, including the nitrogen-containing secondary metabolites, such as alkaloids, cyanogenic glycosides or glucosinolates, and non-protein amino acids (Figure 4). Previously, nitrogen-containing secondary metabolites were considered unwanted materials of plants and are known now for their resistivity towards different stress factors. Among the phytochemicals, alkaloids are heterogeneous groups of secondary metabolites consisting of one or more nitrogen atoms produced under abiotic stress conditions. It has been found that alkaloids perform a significant role against microbial pathogens and herbivorous animals. Besides, more alkaloid contents and derivatives are produced in abiotic stress conditions. For example, poppy plants make more alkaloids when there is a drought period as well as under salinity stress. In lupins (Lupinus termis) cultivars, the content of alkaloids was also influenced by the drought and activated yeast extract treatment.

48Additionally, glucosinolates and cyanogenic glycosides are sulfur and nitrogen-containing secondary metabolites derived from glucose and amino acids. Similarly, Rodziewicz et al. demonstrated that all these natural compounds play a significant role against different environmental factors (biotic and abiotic). Mewis et al. showed that in A. thaliana, under drought and water logging conditions tend to increase aliphatic compounds of glucosinolate and flavonoids. Moreover, in B. juncea, the increased level of glucosinolate was observed during the vegetative stage under water deficit conditions. In plants, apart from the essential 20 amino acids, there are more than 200 free plant cell amino acids that are not assimilated into proteins. These free amino acids are called non-protein amino acids. Their major function in plants is to respond to various environmental stresses.

5. Conclusion and Future Perspectives

49The acceleration of climate change increases the severity of damage to crop productivity under environmental stress. Understanding the role that primary and secondary metabolites play during stress resistance mechanisms is important for developing crop species and improving their stress resistance, ensuring that the need for food security is met for a growing global population. However, less has been understood about the function of these metabolites against environmental stresses in plants, especially abiotic stresses. In the current review, we have provided an overview of the role of primary (amino acids, polyamines, carbohydrates, glycine betaine, and lipids) and secondary (phenolics, flavonoids, terpenoids, alkaloids, and glycosides) metabolites against several abiotic factors, such as drought, salinity, temperature, UVr, and TM. Analysis of more than 200 articles allowed us to describe the main responses of primary and secondary metabolite products of different plant species to abiotic stresses. Metabolomics has occupied a prominent place in plant stress physiology and biology research. Metabolic change due to abiotic stress is complex to describe the variability between different plant species. Nevertheless, metabolomics needs more extensive research in data annotation, assessment, processing, and evaluation. Progress in “omics” tools and bioinformatics and enhanced assimilation of the data from varying molecular levels is needed. Hence, to expose the full picture of sustaining mechanism, which will lead to new biomarkers of resistance towards biotic and abiotic stresses. Affirmation of the impact of environmental stresses on plants and their metabolite level responses recorded valued genes about the mechanism underlying such acclimation. However, the balancing mechanism between the gene expression and the subsequent metabolic phenotype is a big challenge nowadays. Therefore, comprehensive research of the dynamic behavior of metabolic systems is a great task for researchers in systematic biology. Furthermore, identifying the genetic background behind the diversity of primary and secondary metabolites produced by plants will help in improving and developing stress tolerance. Manipulating and overexpressing genes related to the biosynthetic pathway of secondary metabolites could be a solution for plant tolerance to environmental stress conditions.

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88.
Le Lay P., Isaure M.-P., Sarry J.-E., Kuhn L., Fayard B., Le Bail J.-L., Bastien O., Garin J., Roby C., Bourguignon J. Metabolomic, proteomic and biophysical analyses of Arabidopsis thaliana cells exposed to a caesium stress. Influence of potassium supply. Biochimie. 2006;88:1533-1547.
Not in our library10.1016/j.biochi.2006.03.013
89.
Xu N., Fan X., Yan X., Li X., Niu R., Tseng C. Antibacterial bromophenols from the marine red alga Rhodomela confervoides. Phytochemistry. 2003;62:1221-1224.
Not in our library10.1016/s0031-9422(03)00004-9
90.
Lu Y., Lam H., Pi E., Zhan Q., Tsai S., Wang C., Kwan Y., Ngai S. Comparative metabolomics in Glycine max and Glycine soja under salt stress to reveal the phenotypes of their offspring. J. Agric. Food Chem. 2013;61:8711-8721.
Not in our library10.1021/jf402043m
91.
Ahsan N., Nakamura T., Komatsu S. Differential responses of microsomal proteins and metabolites in two contrasting cadmium (Cd)-accumulating soybean cultivars under Cd stress. Amino Acids. 2012;42:317-327.
Not in our library10.1007/s00726-010-0809-7
92.
Heinemann B., Hildebrandt T.M. The role of amino acid metabolism in signaling and metabolic adaptation to stress-induced energy deficiency in plants. J. Exp. Bot. 2021;72:4634-4645.
Not in our library10.1093/jxb/erab182
93.
Khan A., Ali S., Murad W., Hayat K., Siraj S., Jawad M., Khan R.A., Uddin J., Al-Harrasi A., Khan A. Phytochemical and pharmacological uses of medicinal plants to treat cancer: A case study from Khyber Pakhtunkhwa, North Pakistan. J. Ethnopharmacol. 2021;281:114437.
Not in our library10.1016/j.jep.2021.114437
94.
Hildebrandt T.M. Synthesis versus degradation: Directions of amino acid metabolism during Arabidopsis abiotic stress response. Plant Mol. Biol. 2018;98:121-135.
Not in our library10.1007/s11103-018-0767-0
95.
Khan N., Ali S., Zandi P., Mehmood A., Ullah S., Ikram M., Ismail M.A.S., Babar M. Role of sugars, amino acids and organic acids in improving plant abiotic stress tolerance. Pak. J. Bot. 2020;52:355-363.
Not in our library10.30848/pjb2020-2(24)
96.
Rodziewicz P., Swarcewicz B., Chmielewska K., Wojakowska A., Stobiecki M. Influence of abiotic stresses on plant proteome and metabolome changes. Acta Physiol. Plant. 2014;36:1-19.
Not in our library10.1007/s11738-013-1402-y
97.
Verbruggen N., Hermans C. Proline accumulation in plants: A review. Amino Acids. 2008;35:753-759.
Not in our library10.1007/s00726-008-0061-6
98.
Meena M., Divyanshu K., Kumar S., Swapnil P., Zehra A., Shukla V., Yadav M., Upadhyay R. Regulation of L-proline biosynthesis, signal transduction, transport, accumulation and its vital role in plants during variable environmental conditions. Heliyon. 2019;5:e02952.
Not in our library10.1016/j.heliyon.2019.e02952
99.
Yang M.M., Wang J., Dong L., Kong D.J., Teng Y., Liu P., Fan J.J., Yu X.H. Lack of association of C3 gene with uveitis: Additional insights into the genetic profile of uveitis regarding complement pathway genes. Sci. Rep. 2017;7:1-8.
Not in our library10.1038/s41598-017-00833-1
100.
Hanif S., Saleem M.F., Sarwar M., Irshad M., Shakoor A., Wahid M.A., Khan H.Z. Biochemically triggered heat and drought stress tolerance in rice by proline application. J. Plant Growth Regul. 2021;40:305-312.
Not in our library10.1007/s00344-020-10095-3
101.
Rashedy A.A., Abd-ElNafea M.H., Khedr E.H. Co-application of proline or calcium and humic acid enhances productivity of salt stressed pomegranate by improving nutritional status and osmoregulation mechanisms. Sci. Rep. 2022;12:1-10.
Not in our library10.1038/s41598-022-17824-6
102.
Abeed A.H., Eissa M.A., Abdel-Wahab D.A. Effect of exogenously applied jasmonic acid and kinetin on drought tolerance of wheat cultivars based on morpho-physiological evaluation. J. Soil Sci. Plant Nutr. 2021;21:131-144.
Not in our library10.1007/s42729-020-00348-1
103.
Vasquez-Robinet C., Mane S.P., Ulanov A.V., Watkinson J.I., Stromberg V.K., De Koeyer D., Schafleitner R., Willmot D.B., Bonierbale M., Bohnert H.J. Physiological and molecular adaptations to drought in Andean potato genotypes. J. Exp. Bot. 2008;59:2109-2123.
Not in our library10.1093/jxb/ern073
104.
Li Q., Zhao Y., Ding W., Han B., Geng S., Ning D., Ma T., Yu X. Gamma-aminobutyric acid facilitates the simultaneous production of biomass, astaxanthin and lipids in Haematococcus pluvialis under salinity and high-light stress conditions. Bioresour. Technol. 2021;320:124418.
Not in our library10.1016/j.biortech.2020.124418
105.
Lv W.-T., Lin B., Zhang M., Hua X.-J. Proline accumulation is inhibitory to Arabidopsis seedlings during heat stress. Plant Physiol. 2011;156:1921-1933.
Not in our library10.1104/pp.111.175810
106.
Charlton A.J., Donarski J.A., Harrison M., Jones S.A., Godward J., Oehlschlager S., Arques J.L., Ambrose M., Chinoy C., Mullineaux P.M. Responses of the pea (Pisum sativum L.) leaf metabolome to drought stress assessed by nuclear magnetic resonance spectroscopy. Metabolomics. 2008;4:312-327.
Not in our library10.1007/s11306-008-0128-0
107.
Kalaji H.M., Jajoo A., Oukarroum A., Brestic M., Zivcak M., Samborska I.A., Cetner M.D., Łukasik I., Goltsev V., Ladle R.J. Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol. Plant. 2016;38:102.
Not in our library10.1007/s11738-016-2113-y
108.
Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance · 2017
No notice
109.
Polyamines function in stress tolerance: from synthesis to regulation · 2015
No notice
110.
Fischer W., Calderón M., Haag R. Hyperbranched polyamines for transfection. Nucleic Acid Transfection. 2010;95-129.
Not in our library10.1007/128_2010_64
111.
Polyamine Function in Plants: Metabolism, Regulation on Development, and Roles in Abiotic Stress Responses · 2019
No notice
112.
Polyamines: Small Amines with Large Effects on Plant Abiotic Stress Tolerance · 2020
No notice
113.
Capell T., Bassie L., Christou P. Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc. Natl. Acad. Sci. USA. 2004;101:9909-9914.
Not in our library10.1073/pnas.0306974101
114.
Zhao J., Wang X., Pan X., Jiang Q., Xi Z. Exogenous putrescine alleviates drought stress by altering reactive oxygen species scavenging and biosynthesis of polyamines in the seedlings of Cabernet Sauvignon. Front. Plant Sci. 2021;12.
Not in our library10.3389/fpls.2021.767992
115.
Vickers N.J. Animal communication: When i’m calling you, will you answer too? Curr. Biol. 2017;27:R713-R715.
Not in our library10.1016/j.cub.2017.05.064
116.
Gill S.S., Tuteja N. Polyamines and abiotic stress tolerance in plants. Plant Signal. Behav. 2010;5:26-33.
Not in our library10.4161/psb.5.1.10291
117.
Saxena R., Adhikari D., Goyal H. Biomass-based energy fuel through biochemical routes: A review. Renew. Sustain. Energy Rev. 2009;13:167-178.
Not in our library10.1016/j.rser.2007.07.011
118.
Ruppert A.M., Weinberg K., Palkovits R. Hydrogenolysis goes bio: From carbohydrates and sugar alcohols to platform chemicals. Angew. Chem. Int. Ed. 2012;51:2564-2601.
Not in our library10.1002/anie.201105125
119.
Cao X., Zhu C., Zhong C., Hussain S., Zhu L., Wu L., Jin Q. Mixed-nitrogen nutrition-mediated enhancement of drought tolerance of rice seedlings associated with photosynthesis, hormone balance and carbohydrate partitioning. Plant Growth Regul. 2018;84:451-465.
Not in our library10.1007/s10725-017-0352-6
120.
Rosa M., Prado C., Podazza G., Interdonato R., González J.A., Hilal M., Prado F.E. Soluble sugars: Metabolism, sensing and abiotic stress: A complex network in the life of plants. Plant Signal. Behav. 2009;4:388-393.
Not in our library10.4161/psb.4.5.8294
121.
Sicher R.C., Timlin D., Bailey B. Responses of growth and primary metabolism of water-stressed barley roots to rehydration. J. Plant Physiol. 2012;169:686-695.
Not in our library10.1016/j.jplph.2012.01.002
122.
Sperdouli I., Moustakas M. Interaction of proline, sugars, and anthocyanins during photosynthetic acclimation of Arabidopsis thaliana to drought stress. J. Plant Physiol. 2012;169:577-585.
Not in our library10.1016/j.jplph.2011.12.015
123.
Basu P., Ali M., Chaturvedi S. Osmotic adjustment increases water uptake, remobilization of assimilates and maintains photosynthesis in chickpea under drought. Experiment. 2007;45:261-267.
Not in our library
124.
Kaplan F., Guy C.L. β-Amylase induction and the protective role of maltose during temperature shock. Plant Physiol. 2004;135:1674-1684.
Not in our library10.1104/pp.104.040808
125.
Keunen E., Peshev D., Vangronsveld J., Van Den Ende W., Cuypers A. Plant sugars are crucial players in the oxidative challenge during abiotic stress: Extending the traditional concept. Plant Cell Environ. 2013;36:1242-1255.
Not in our library10.1111/pce.12061
126.
Saddhe A.A., Manuka R., Penna S. Plant sugars: Homeostasis and transport under abiotic stress in plants. Physiol. Plant. 2021;171:739-755.
Not in our library10.1111/ppl.13283
127.
Krasavina M.S., Burmistrova N.A., Raldugina G.N. The role of carbohydrates in plant resistance to abiotic stresses. Emerging Technologies and Management of Crop Stress Tolerance. 2014;229-270.
Not in our library
128.
Raza S.H., Athar H.R., Ashraf M., Hameed A. Glycinebetaine-induced modulation of antioxidant enzymes activities and ion accumulation in two wheat cultivars differing in salt tolerance. Environ. Exp. Bot. 2007;60:368-376.
Not in our library10.1016/j.envexpbot.2006.12.009
129.
Chen T.H., Murata N. Glycinebetaine: An effective protectant against abiotic stress in plants. Trends Plant Sci. 2008;13:499-505.
Not in our library10.1016/j.tplants.2008.06.007
130.
Giri J. Glycinebetaine and abiotic stress tolerance in plants. Plant Signal. Behav. 2011;6:1746-1751.
Not in our library10.4161/psb.6.11.17801
131.
Sakamotto A., Muratta N. The role of glycine betaine in protection of plants against stress: Clue from transgenic plants. Plant Cell Environ. 2002;25:163-171.
Not in our library10.1046/j.0016-8025.2001.00790.x
132.
Quan R., Shang M., Zhang H., Zhao Y., Zhang J. Improved chilling tolerance by transformation with betA gene for the enhancement of glycinebetaine synthesis in maize. Plant Sci. 2004;166:141-149.
Not in our library10.1016/j.plantsci.2003.08.018
133.
Prasad K., Sharmila P., Kumar P., Saradhi P.P. Transformation of Brassica juncea (L.) Czern with bacterial codA gene enhances its tolerance to salt stress. Mol. Breed. 2000;6:489-499.
Not in our library10.1023/a:1026542109965
134.
Holmström K.O., Somersalo S., Mandal A., Palva T.E., Welin B. Improved tolerance to salinity and low temperature in transgenic tobacco producing glycine betaine. J. Exp. Bot. 2000;51:177-185.
Not in our library10.1093/jexbot/51.343.177
135.
Niesche R., Haase M. Emotions and ethics: A Foucauldian framework for becoming an ethical educator. Educ. Philos. Theory. 2012;44:276-288.
Not in our library10.1111/j.1469-5812.2010.00655.x
136.
Singh D., Singh C.K., Singh D., Sarkar S.K., Prasad S.K., Sharma N.L., Singh I. Glycine betaine modulates chromium (VI)-induced morpho-physiological and biochemical responses to mitigate chromium toxicity in chickpea (Cicer arietinum L.) cultivars. Sci. Rep. 2022;12:8005.
Not in our library10.1038/s41598-022-11869-3
137.
Khedr R.A., Sorour S.G.R., Aboukhadrah S.H., El Shafey N.M., Abd Elsalam H.E., El-Sharnouby M.E., El-Tahan A.M. Alleviation of salinity stress effects on agro-physiological traits of wheat by auxin, glycine betaine, and soil additives. Saudi J. Biol. Sci. 2022;29:534-540.
Not in our library10.1016/j.sjbs.2021.09.027
138.
Heavy Metal Stress and Some Mechanisms of Plant Defense Response · 2015
No notice
139.
Fahy E., Subramaniam S., Brown H.A., Glass C.K., Merrill A.H., Murphy R.C., Raetz C.R., Russell D.W., Seyama Y., Shaw W. A comprehensive classification system for lipids1. J. Lipid Res. 2005;46:839-861.
Not in our library10.1194/jlr.e400004-jlr200
140.
Okazaki Y., Saito K. Roles of lipids as signaling molecules and mitigators during stress response in plants. Plant J. 2014;79:584-596.
Not in our library10.1111/tpj.12556
141.
Munnik T., Zarza X. Analyzing plant signaling phospholipids through 32 P i-labeling and TLC. Plant Lipid Signaling Protocols. 2013;3-15.
Not in our library10.1007/978-1-62703-401-2_1
142.
Welti R., Li W., Li M., Sang Y., Biesiada H., Zhou H.-E., Rajashekar C., Williams T.D., Wang X. Profiling membrane lipids in plant stress responses: Role of phospholipase Dα in freezing-induced lipid changes in Arabidopsis. J. Biol. Chem. 2002;277:31994-32002.
Not in our library10.1074/jbc.m205375200
143.
Viehweger K., Dordschbal B., Roos W. Elicitor-activated phospholipase A2 generates lysophosphatidylcholines that mobilize the vacuolar H+ pool for pH signaling via the activation of Na+-dependent proton fluxes. Plant Cell. 2002;14:1509-1525.
Not in our library10.1105/tpc.002329
144.
Drissner D., Kunze G., Callewaert N., Gehrig P., Tamasloukht M.B., Boller T., Felix G., Amrhein N., Bucher M. Lyso-phosphatidylcholine is a signal in the arbuscular mycorrhizal symbiosis. Science. 2007;318:265-268.
Not in our library10.1126/science.1146487
145.
Mandal M.K., Chandra-Shekara A., Jeong R.-D., Yu K., Zhu S., Chanda B., Navarre D., Kachroo A., Kachroo P. Oleic acid–dependent modulation of NITRIC OXIDE ASSOCIATED1 protein levels regulates nitric oxide–mediated defense signaling in Arabidopsis. Plant Cell. 2012;24:1654-1674.
Not in our library10.1105/tpc.112.096768
146.
Upchurch R.G. Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnol. Lett. 2008;30:967-977.
Not in our library10.1007/s10529-008-9639-z
147.
Markham J.E., Lynch D.V., Napier J.A., Dunn T.M., Cahoon E.B. Plant sphingolipids: Function follows form. Curr. Opin. Plant Biol. 2013;16:350-357.
Not in our library10.1016/j.pbi.2013.02.009
148.
Ballaré C.L. Jasmonate-induced defenses: A tale of intelligence, collaborators and rascals. Trends Plant Sci. 2011;16:249-257.
Not in our library10.1016/j.tplants.2010.12.001
149.
Kang L., Wang Y.S., Uppalapati S.R., Wang K., Tang Y., Vadapalli V., Venables B.J., Chapman K.D., Blancaflor E.B., Mysore K.S. Overexpression of a fatty acid amide hydrolase compromises innate immunity in Arabidopsis. Plant J. 2008;56:336-349.
Not in our library10.1111/j.1365-313x.2008.03603.x
150.
Sun Y., Li Y., Sun X., Wu Q., Yang C., Wang L. Overexpression of a Phosphatidylinositol-Specific Phospholipase C Gene from Populus simonii× P. nigra Improves Salt Tolerance in Transgenic Tobacco. J. Plant Biol. 2022;65:365-376.
Not in our library10.1007/s12374-022-09359-0
151.
Pinosa F., Buhot N., Kwaaitaal M., Fahlberg P., Thordal-Christensen H., Ellerström M., Andersson M.X. Arabidopsis phospholipase Dδ is involved in basal defense and nonhost resistance to powdery mildew fungi. Plant Physiol. 2013;163:896-906.
Not in our library10.1104/pp.113.223503
152.
Rapid phosphatidic acid accumulation in response to low temperature stress in Arabidopsis is generated through diacylglycerol kinase · 2013
No notice
153.
McLoughlin F., Arisz S.A., Dekker H.L., Kramer G., De Koster C.G., Haring M.A., Munnik T., Testerink C. Identification of novel candidate phosphatidic acid-binding proteins involved in the salt-stress response of Arabidopsis thaliana roots. Biochem. J. 2013;450:573-581.
Not in our library10.1042/bj20121639
154.
Uraji M., Katagiri T., Okuma E., Ye W., Hossain M.A., Masuda C., Miura A., Nakamura Y., Mori I.C., Shinozaki K. Cooperative function of PLDδ and PLDα1 in abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol. 2012;159:450-460.
Not in our library10.1104/pp.112.195578
155.
Wink M. Introduction: Biochemistry, physiology and ecological functions of secondary metabolites. Annual Plant Reviews Volume 40: Biochemistry of Plant Secondary Metabolism. 2010;1-19.
Not in our library
156.
Böttger A., Vothknecht U., Bolle C., Wolf A. Lessons on Caffeine, Cannabis & Co. 2018;171-178.
Not in our library
157.
Debona D., Rodrigues F.A., Datnoff L.E. Silicon's role in abiotic and biotic plant stresses. Annu. Rev. Phytopathol. 2017;55:85-107.
Not in our library10.1146/annurev-phyto-080516-035312
158.
Plant Secondary Metabolites as Defense Tools against Herbivores for Sustainable Crop Protection · 2022
No notice
159.
Ochoa-Villarreal M., Howat S., Hong S., Jang M.O., Jin Y.-W., Lee E.-K., Loake G.J. Plant cell culture strategies for the production of natural products. BMB Rep. 2016;49:149.
Not in our library10.5483/bmbrep.2016.49.3.264
160.
Edreva A., Velikova V., Tsonev T. Phenylamides in plants. Russ. J. Plant Physiol. 2007;54:287-301.
Not in our library10.1134/s1021443707030016
161.
Pagare S., Bhatia M., Tripathi N., Pagare S., Bansal Y. Secondary metabolites of plants and their role: Overview. Curr. Trends Biotechnol. Pharm. 2015;9:293-304.
Not in our library
162.
Elateeq A.A., Ahmed M., Abdelkawy A.M., Toaima N.M., Bosila H.A., Zarad M.M., Ebrahim H.S., Jiao J., Hongyi P., Ullah S. Establishment of Gypsophila paniculata root culture for biomass, saponin, and flavonoid production. Not. Bot. Horti Agrobot. Cluj-Napoca. 2022;50:12886.
Not in our library10.15835/nbha50312886
163.
Bosila H., Hamza M.A., El-Ateeq A. Enhancement of callus growth and hyoscyamine alkaloid production in Hyoscyamus muticus by nanotechnology, biotic elicitor and precursor. Int. J. ChemTech. Res. 2016;9:135-142.
Not in our library
164.
Jasmonic Acid Signaling Pathway in Response to Abiotic Stresses in Plants · 2020
No notice
165.
Elshahawy O.A., Zeawail M.E.-F., Hamza M.A., Elateeq A.A., Omar M.A. Improving the Production of Total Phenolics and Flavonoids and the Antioxidant Capacity of Echinacea purpurea Callus through Biotic Elicitation. Egypt. J. Chem. 2022;65:137-149.
Not in our library10.21608/ejchem.2022.145210.6328
166.
Mahdi J., Mahdi A., Mahdi A., Bowen I. The historical analysis of aspirin discovery, its relation to the willow tree and antiproliferative and anticancer potential. Cell Prolif. 2006;39:147-155.
Not in our library10.1111/j.1365-2184.2006.00377.x
167.
Yazici L. Influence of different sowing times on yield and biochemical characteristics of different opium poppy (Papaver somniferum L.) genotypes. J. King Saud Univ.-Sci. 2022;34:102337.
Not in our library10.1016/j.jksus.2022.102337
168.
Grace S.C. Phenolics as antioxidants. Antioxid. React. Oxyg. Species Plants. 2005;141:168.
Not in our library
169.
Waterman P.G. Roles for secondary metabolites in plants. Ciba Foundation Symposium 171-Secondary Metabolites: Their Function and Evolution: Secondary Metabolites: Their Function and Evolution: Ciba Foundation Symposium 171. 2007.
Not in our library
170.
Kabera J.N., Semana E., Mussa A.R., He X. Plant secondary metabolites: Biosynthesis, classification, function and pharmacological properties. J. Pharm. Pharm. 2014;2:377-392.
Not in our library
171.
Saltveit M.E. Synthesis and metabolism of phenolic compounds. Fruit Veget. Phytochem. Chem. Hum. Health. 2017;2:115.
Not in our library
172.
Dong N.Q., Lin H.X. Contribution of phenylpropanoid metabolism to plant development and plant–environment interactions. J. Integr. Plant Biol. 2021;63:180-209.
Not in our library10.1111/jipb.13054
173.
Valifard M., Mohsenzadeh S., Niazi A., Moghadam A. Phenylalanine ammonia lyase isolation and functional analysis of phenylpropanoid pathway under salinity stress in'Salvia'species. Aust. J. Crop Sci. 2015;9:656-665.
Not in our library
174.
Amarowicz R., Weidner S. Phenolic compounds and properties of antioxidants in grapevine roots (Vitis vinifera L.) under drought stress followed by recovery. Acta Soc. Bot. Pol. 2009;78:389-405.
Not in our library
175.
Nada R.S., Ashmawi A.E., Mady E., Randhir T.O., Elateeq A.A. Effect of Organic Manure and Plant Growth Promoting Microbes on Yield, Quality and Essential Oil Constituents of Fennel Bulb (Foeniculum vulgare Mill.). J. Ecol. Eng. 2022;23:149-164.
Not in our library10.12911/22998993/147252
176.
Cheynier V., Comte G., Davies K.M., Lattanzio V., Martens S. Plant phenolics: Recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiol. Biochem. 2013;72:1-20.
Not in our library10.1016/j.plaphy.2013.05.009
177.
Kuluev B., Mikhaylova E., Berezhneva Z., Nikonorov Y., Postrigan B., Kudoyarova G., Chemeris A. Expression profiles and hormonal regulation of tobacco NtEXGT gene and its involvement in abiotic stress response. Plant Physiol. Biochem. 2017;111:203-215.
Not in our library10.1016/j.plaphy.2016.12.005
178.
Signorelli S., Coitiño E.L., Borsani O., Monza J. Molecular mechanisms for the reaction between OH radicals and proline: Insights on the role as reactive oxygen species scavenger in plant stress. J. Phys. Chem. B. 2014;118:37-47.
Not in our library10.1021/jp407773u
179.
Dehghan S., Sadeghi M., Pöppel A., Fischer R., Lakes-Harlan R., Kavousi H.R., Vilcinskas A., Rahnamaeian M. Differential inductions of phenylalanine ammonia-lyase and chalcone synthase during wounding, salicylic acid treatment, and salinity stress in safflower, Carthamus tinctorius. Biosci. Rep. 2014;34:273-282.
Not in our library10.1042/bsr20140026
180.
Hernandez-Aguilar C., Dominguez-Pacheco A., Tenango M.P., Valderrama-Bravo C., Hernández M.S., Cruz-Orea A., Ordonez-Miranda J. Characterization of bean seeds, germination, and phenolic compounds of seedlings by UV-C radiation. J. Plant Growth Regul. 2021;40:642-655.
Not in our library10.1007/s00344-020-10125-0
181.
Mencin M., Abramovič H., Jamnik P., Petkovšek M.M., Veberič R., Terpinc P. Abiotic stress combinations improve the phenolics profiles and activities of extractable and bound antioxidants from germinated spelt (Triticum spelta L.) seeds. Food Chem. 2021;344:128704.
Not in our library10.1016/j.foodchem.2020.128704
182.
Huihui Z., Xin L., Zisong X., Yue W., Zhiyuan T., Meijun A., Yuehui Z., Wenxu Z., Nan X., Guangyu S. Toxic effects of heavy metals Pb and Cd on mulberry (Morus alba L.) seedling leaves: Photosynthetic function and reactive oxygen species (ROS) metabolism responses. Ecotoxicol. Environ. Saf. 2020;195:110469.
Not in our library10.1016/j.ecoenv.2020.110469
183.
Kohli S.K., Handa N., Sharma A., Gautam V., Arora S., Bhardwaj R., Wijaya L., Alyemeni M.N., Ahmad P. Interaction of 24-epibrassinolide and salicylic acid regulates pigment contents, antioxidative defense responses, and gene expression in Brassica juncea L. seedlings under Pb stress. Environ. Sci. Pollut. Res. 2018;25:15159-15173.
Not in our library10.1007/s11356-018-1742-7
184.
Handa N., Kohli S.K., Sharma A., Thukral A.K., Bhardwaj R., Abd_Allah E.F., Alqarawi A.A., Ahmad P. Selenium modulates dynamics of antioxidative defence expression, photosynthetic attributes and secondary metabolites to mitigate chromium toxicity in Brassica juncea L. plants. Environ. Exp. Bot. 2019;161:180-192.
Not in our library10.1016/j.envexpbot.2018.11.009
185.
Alvarez S., Marsh E.L., Schroeder S.G., Schachtman D.P. Metabolomic and proteomic changes in the xylem sap of maize under drought. Plant Cell Environ. 2008;31:325-340.
Not in our library10.1111/j.1365-3040.2007.01770.x
186.
Fan L., Linker R., Gepstein S., Tanimoto E., Yamamoto R., Neumann P.M. Progressive inhibition by water deficit of cell wall extensibility and growth along the elongation zone of maize roots is related to increased lignin metabolism and progressive stelar accumulation of wall phenolics. Plant Physiol. 2006;140:603-612.
Not in our library10.1104/pp.105.073130
187.
Li B., Fan R., Sun G., Sun T., Fan Y., Bai S., Guo S., Huang S., Liu J., Zhang H. Flavonoids improve drought tolerance of maize seedlings by regulating the homeostasis of reactive oxygen species. Plant Soil. 2021;461:389-405.
Not in our library10.1007/s11104-020-04814-8
188.
Nakabayashi R., Yonekura-Sakakibara K., Urano K., Suzuki M., Yamada Y., Nishizawa T., Matsuda F., Kojima M., Sakakibara H., Shinozaki K. Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J. 2014;77:367-379.
Not in our library10.1111/tpj.12388
189.
Nichols S.N., Hofmann R.W., Williams W.M. Physiological drought resistance and accumulation of leaf phenolics in white clover interspecific hybrids. Environ. Exp. Bot. 2015;119:40-47.
Not in our library10.1016/j.envexpbot.2015.05.014
190.
André C.M., Schafleitner R., Legay S., Lefèvre I., Aliaga C.A.A., Nomberto G., Hoffmann L., Hausman J.-F., Larondelle Y., Evers D. Gene expression changes related to the production of phenolic compounds in potato tubers grown under drought stress. Phytochemistry. 2009;70:1107-1116.
Not in our library10.1016/j.phytochem.2009.07.008
191.
Parida A.K., Dagaonkar V.S., Phalak M.S., Umalkar G., Aurangabadkar L.P. Alterations in photosynthetic pigments, protein and osmotic components in cotton genotypes subjected to short-term drought stress followed by recovery. Plant Biotechnol. Rep. 2007;1:37-48.
Not in our library10.1007/s11816-006-0004-1
192.
Naikoo M.I., Dar M.I., Raghib F., Jaleel H., Ahmad B., Raina A., Khan F.A., Naushin F. Role and regulation of plants phenolics in abiotic stress tolerance: An overview. Plant Signal. Mol. 2019;2:157-168.
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193.
de Abreu I.N., Mazzafera P. Effect of water and temperature stress on the content of active constituents of Hypericum brasiliense Choisy. Plant Physiol. Biochem. 2005;43:241-248.
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194.
Djoukeng J.D., Arbona V., Argamasilla R., Gomez-Cadenas A. Flavonoid profiling in leaves of citrus genotypes under different environmental situations. J. Agric. Food Chem. 2008;56:11087-11097.
Not in our library10.1021/jf802382y
195.
Ancillotti C., Bogani P., Biricolti S., Calistri E., Checchini L., Ciofi L., Gonnelli C., Del Bubba M. Changes in polyphenol and sugar concentrations in wild type and genetically modified Nicotiana langsdorffii Weinmann in response to water and heat stress. Plant Physiol. Biochem. 2015;97:52-61.
Not in our library10.1016/j.plaphy.2015.09.012
196.
Xiang M., Ding W., Wu C., Wang W., Ye S., Cai C., Hu X., Wang N., Bai W., Tang X. Production of purple Ma bamboo (Dendrocalamus latiflorus Munro) with enhanced drought and cold stress tolerance by engineering anthocyanin biosynthesis. Planta. 2021;254:50.
Not in our library10.1007/s00425-021-03696-z
197.
Wang N., Zhang Z., Jiang S., Xu H., Wang Y., Feng S., Chen X. Synergistic effects of light and temperature on anthocyanin biosynthesis in callus cultures of red-fleshed apple (Malus sieversii f. niedzwetzkyana). Plant Cell Tissue Organ Cult. (PCTOC). 2016;127:217-227.
Not in our library10.1007/s11240-016-1044-z
198.
Cabane M., Afif D., Hawkins S. Lignins and abiotic stresses. Advances in Botanical Research. 2012;219-262.
Not in our library
199.
Bulotta S., Oliverio M., Russo D., Procopio A. Biological Activity of Oleuropein and Its Derivatives. 2013;3605-3638.
Not in our library
200.
Elateeq A.A., Sun Y., Nxumalo W., Gabr A.M. Biotechnological production of silymarin in Silybum marianum L.: A review. Biocatal. Agric. Biotechnol. 2020;29:101775.
Not in our library10.1016/j.bcab.2020.101775
201.
Elateeq A.A., Saad Z., Eissa M., Ullah S. Effect of chitosan and light conditions on the production of callus biomass, total flavonoids and total phenolics in Ginkgo biloba L. Al-Azhar J. Agric. Res. 2021;46:28-42.
Not in our library10.21608/ajar.2021.218197
202.
Mujib A., Fatima S., Malik M.Q. Gamma ray–induced tissue responses and improved secondary metabolites accumulation in Catharanthus roseus. Appl. Microbiol. Biotechnol. 2022;106:6109-6123.
Not in our library10.1007/s00253-022-12122-7
203.
Disease Resistance Mechanisms in Plants · 2018
No notice
204.
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.
Not in our library
205.
Kumar S., Shah S.H., Vimala Y., Jatav H.S., Ahmad P., Chen Y., Siddique K.H. Abscisic acid: Metabolism, transport, crosstalk with other plant growth regulators, and its role in heavy metal stress mitigation. Front. Plant Sci. 2022;13:972856.
Not in our library10.3389/fpls.2022.972856
206.
Al Musayeib N.M., Musarat A., Maqsood F. Terpenes: A Source of Novel Antimicrobials, Applications and Recent Advances. Eco-Friendly Biobased Products Used in Microbial Diseases. 2022;247-270.
Not in our library
207.
Gu C.-Z., Xia X.-M., Lv J., Tan J.-W., Baerson S.R., Pan Z.-q., Song Y.-Y., Zeng R.-S. Diterpenoids with herbicidal and antifungal activities from hulls of rice (Oryza sativa). Fitoterapia. 2019;136:104183.
Not in our library10.1016/j.fitote.2019.104183
208.
Yang C.-Q., Wu X.-M., Ruan J.-X., Hu W.-L., Mao Y.-B., Chen X.-Y., Wang L.-J. Isolation and characterization of terpene synthases in cotton (Gossypium hirsutum). Phytochemistry. 2013;96:46-56.
Not in our library10.1016/j.phytochem.2013.09.009
209.
Vaughan M.M., Christensen S., Schmelz E.A., Huffaker A., Mcauslane H.J., Alborn H.T., Romero M., Allen L.H., Teal P.E. Accumulation of terpenoid phytoalexins in maize roots is associated with drought tolerance. Plant Cell Environ. 2015;38:2195-2207.
Not in our library10.1111/pce.12482
210.
Massacci A., Nabiev S., Pietrosanti L., Nematov S., Chernikova T., Thor K., Leipner J. Response of the photosynthetic apparatus of cotton (Gossypium hirsutum) to the onset of drought stress under field conditions studied by gas-exchange analysis and chlorophyll fluorescence imaging. Plant Physiol. Biochem. 2008;46:189-195.
Not in our library10.1016/j.plaphy.2007.10.006
211.
Yusuf M.A., Kumar D., Rajwanshi R., Strasser R.J., Tsimilli-Michael M., Sarin N.B. Overexpression of γ-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: Physiological and chlorophyll a fluorescence measurements. Biochim. Et Biophys. Acta (BBA)-Bioenerg. 2010;1797:1428-1438.
Not in our library10.1016/j.bbabio.2010.02.002
212.
Wu W., Zhang Q., Zhu Y., Lam H.-M., Cai Z., Guo D. Comparative metabolic profiling reveals secondary metabolites correlated with soybean salt tolerance. J. Agric. Food Chem. 2008;56:11132-11138.
Not in our library10.1021/jf8024024
213.
Accumulation of Flavonols over Hydroxycinnamic Acids Favors Oxidative Damage Protection under Abiotic Stress · 2016
No notice
214.
Davodnia B., Ahmahdi J., Fabriki Ourang S. Evaluation of drought and salinity stresses on morphological and biochemical characteristics in four species of Papaver. Eco-Phytochem. J. Med. Plants. 2017;5:24-36.
Not in our library
215.
Mewis I., Khan M.A., Glawischnig E., Schreiner M., Ulrichs C. Water stress and aphid feeding differentially influence metabolite composition in Arabidopsis thaliana (L.). PLoS ONE. 2012;7:e48661.
Not in our library10.1371/journal.pone.0048661
216.
Taha R.S., Seleiman M.F., Alhammad B.A., Alkahtani J., Alwahibi M.S., Mahdi A.H. Activated Yeast extract enhances growth, anatomical structure, and productivity of Lupinus termis L. plants under actual salinity conditions. Agronomy. 2020;11:74.
Not in our library10.3390/agronomy11010074
217.
Miyagawa H. Studies on nitrogen-containing secondary metabolites playing a defensive role in plants. J. Pestic. Sci. 2009;34:110-112.
Not in our library10.1584/jpestics.j09-02

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