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An Overview of Biomembrane Functions in Plant Responses to High-Temperature Stress

Yue Niu, Yun Xiang

Frontiers in Plant Science · 2018 · Review

doi:10.3389/fpls.2018.00915

Abstract

Biological membranes are highly ordered structures consisting of mosaics of lipids and proteins. Elevated temperatures can directly and effectively change the properties of these membranes, including their fluidity and permeability, through a holistic effect that involves changes in the lipid composition and/or interactions between lipids and specific membrane proteins. Ultimately, high temperatures can alter microdomain remodeling and instantaneously relay ambient cues to downstream signaling pathways. Thus, dynamic membrane regulation not only helps cells perceive temperature changes but also participates in intracellular responses and determines a cell's fate. Moreover, due to the specific distribution of extra- and endomembrane elements, the plasma membrane (PM) and membranous organelles are individually responsible for distinct developmental events during plant adaptation to heat stress. This review describes recent studies that focused on the roles of various components that can alter the physical state of the plasma and thylakoid membranes as well as the crucial signaling pathways initiated through the membrane system, encompassing both endomembranes and membranous organelles in the context of heat stress responses.

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From PubMed Central, U.S. National Library of Medicine, as current on Oct 21, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

1The Fifth Assessment Report of the IPCC showed that the increase in the global average surface temperature from 1880 to 2012 reached 0.85°C, and the last three decades in particular were persistently warmer than any preceding decades. Moreover, the report predicted that the extreme annual daily maximum temperature would be elevated by approximately 1–3°C by the mid-21st century. Although warming has been observed to benefit crop production in some high-latitude regions, the increasing threat of climate change has had negative impacts on crop yields over a wide range of areas, and the detrimental effects are expected to be aggravated in the next century. In addition, secondary disasters that accompany high temperatures, such as drought and soil salinization, could trigger dramatic crop loss worldwide and even lead to global food shortages in the future. In fact, regardless of the climatological extremes, plants, being sessile, are inevitably exposed to a wide range of temperature stresses, including daily and/or seasonal temperature fluctuations that may reach dozens of degrees. Each plant species naturally exhibits its own optimal temperature range for growth and reproduction, and thus, extreme variations can rapidly exert a thermodynamic influence on the intracellular macromolecules (nucleic acids and proteins) and substructures of plant cells. For instance, a temperature of 5°C above optimal growing conditions can induce a series of changes in the organization of cell compartments, including the organelles and cytoskeleton, as well as the membrane microdomains necessary for plant survival at high temperatures. Plants have evolved different adaptation mechanisms to withstand adverse conditions for optimal growth, the most common of which involve the activation of stress-induced gene expression related to the homeostatic adjustment of plant metabolism and development. Therefore, breeding efforts focused on the transformation of these genes as supported by genetic approaches have been employed to efficiently improve plant adaptability to extreme temperatures. In particular, heat shock transcription factors and heat shock proteins (HSFs/HSPs) have been demonstrated to constitute a master regulatory pathway involved in the response to heat stress based on half a century of research, and some of these genes have since been applied in sustainable agriculture. Nevertheless, in considering the mechanisms underlying the high-temperature stress response, one should not ignore how plants first quickly perceive and translate the stress into intracellular response signaling. In this respect, cell membranes, which constitute the barrier to the external environment and separate the cytosol into several microcompartments, are well suited for sensing stress and providing a “crosstalk" interface. Subtle alterations in lipids may affect various properties of the membrane, including its fluidity, thickness, permeability, and packing, and thus affect the clustering of important membrane proteins, which are sensitive to ambient conditions. However, unlike in animal cells, membrane structures in plant cells possessing a cell wall may display an enormous and specific variety of components and functions. Combined with the diversity of plant responses to adverse environments, this complexity is such that the majority of the underlying thermotolerance mechanisms in plants remain unclear. The various challenges remaining in this field will be addressed in the following open questions.

2In this review, we provide an overview of the currently known factors and/or mechanisms that can affect the states and properties of the plasma membrane (PM) and thylakoid membrane as well as the endoplasmic reticulum system (ER) in responses to and in tolerance of high-temperature stress in land plants (largely in reference to Arabidopsis thaliana). Some critical perspectives on the roles of membranes in these processes will also be presented, and we will discuss membrane-stress responses under heat stress within different plant taxa, including several psychrophiles, mesophiles, and thermophiles in the plant kingdom (as classified by;; Table 1).

PM Composition and Microdomain

3Membranes serve as a selectively permeable barrier, and they are primarily composed of proteins and lipids in moving mosaics. Lipids with a polar head group and diverse types of long hydrophobic tails spontaneously form two leaflets in aqueous environments due to their amphipathic properties. Lipid species can be divided into three primary classes by chemical structure, namely, glycerolipids, sphingolipids and sterols. Among the abundant glycerolipids, phospholipids predominantly occur in the PM and mitochondrial envelope, while galactolipids primarily constitute the thylakoid membrane. Phospholipids contain two fatty acyl chains and a variable polar head group assembled to the glycerol backbone. Although phospholipids are usually sorted by their polar head groups, the fatty acid moieties greatly control their physicochemical properties. The number and position of C–C bonds within hydrophobic acyl tails and the length of the carbon chains are thought to be key factors in determining the membrane fluidity. Moreover, the lipid composition of each leaflet reflects another membrane property (asymmetry). Lipids are selectively embedded in membrane bilayers; phosphatidylcholine (PC), glycolipids and sphingomyelin are predominantly enriched on the exoplasmic face of the PM and the lumenal side of internal organelles, while phosphatidylserine (PS), phosphatidylethanolamine (PE), and phosphatidylinositol (PI) are primarily found on the cytoplasmic side; cholesterol shows preferential accumulation on the exoplasmic leaflet, although it can move freely between the two leaflets. Additionally, some minor phospholipids, such as phosphatidic acid (PA), phosphatidylinositol-4-monophosphate (PIP) and phosphatidylinositol-4,5-biphosphate (PIP2), are also enriched on the cytoplasmic leaflet.

4The fluid mosaic hypothesis proposed by indicated that lipids formed a discontinuous, fluid bilayer in which proteins were embedded via specific interactions with lipids. Today, evidence regarding the structure and function of membranes inspires us to consider the biomembrane as a more complex and exquisite device. Different regions of membranes with defined lipids and clusters of proteins are not always equal, forming discrete platforms with varying sizes and traits in the plane of the membrane (which are denominated as membrane microdomains) (;;;;; Figure 1). Historically, lipid rafts enriched in sphingolipids, sterols and glycosylphosphatidylinositol (GPI)-anchored proteins were thought to be equivalent to membrane microdomains or detergent-insoluble membranes (treated with 1% Triton X-100 at 4°C;;; ). Over the past decade, this idea has come to be considered controversial, if all of the above concepts reflect the authentic membrane substructure. With the development of experimental approaches, the microdomains of membranes can now be distinguished at multiple scales (reviewed by ). Nanoscale domains based on lipid rafts (2–100 nm) are incorporated into larger microdomains (e.g., raft platforms) via the interactions between specific lipids and proteins; both cytoskeleton and cell wall components prop up the largest units, which are denominated as the membrane compartments (40–300 nm), depending on the cytoskeletal and cell wall restriction of the lateral diffusion of membrane proteins. In contrast to lipid rafts with a highly dynamic nature in mammalian cells, special lateral membrane compartments in plant cells are more stable. Substantial evidence supports the notion that the microdomain acts as a harbor in which cellular signaling is clustered by the interactions between membrane components (including previously isolated channels, receptors, other signaling complexes and specific lipids) during many physiological processes, such as biotic and abiotic stress responses, membrane transport and polarized plant growth. An ROS-generating enzyme known as respiratory burst oxidase homolog D (RBOHD) has been suggested to localize to membrane microdomains (;; Figure 1) and could be activated by a heat-induced cytosolic calcium increase to immediately produce an oxidative burst. However, numerous microdomain-associated proteins remain to be elucidated in plants. Notably, increasing evidence from mammals has illustrated that several HSPs localize to PM rafts via interactions with specific lipids (reviewed by ). These HSPs include abundant HSP70, HSP90 and other small HSPs (e.g., HSP27), the functions of which have been suggested to include the recruitment of signaling proteins to the PM, the folding of membrane proteins, assisting polypeptides in translocation across the membrane bilayer, and rapidly remodeling and protecting the PM under cellular stresses. Although the mechanism controlling the interactions between HSPs and membrane lipids and proteins is less well known, it is speculated that the structure of lipid rafts is crucial for HSPs to perform their individual functions in cell responses. Whether HSPs in plants exhibit similar behaviors at PM microdomains has not yet been explored.

Lipid Saturation and Desaturases

5Plants that survive under extreme temperatures must first maintain constant membrane fluidity and integrity, which requires dynamic changes in the membrane composition. Early studies have shown that the ratio of saturated and unsaturated fatty acids differs greatly between lipid species and tissues. In addition, the saturated and monounsaturated fatty acid contents increase in response to elevated temperatures, while the proportion of polyunsaturated fatty acids can be increased by a sudden drop in temperature. Temperature is the most important contributing factor in regulating the unsaturation degree of fatty acid chains, and thus, it has a large impact on the properties of membrane bilayers. The numbers and sites of double bonds within fatty acid chains are modified by desaturases via an oxygen-dependent reaction. In plants, the fatty acid desaturase (FAD) family, which plays an important role in adaptation to high-temperature stress, has been studied extensively. Among the eight members of the Arabidopsis FAD family (FAD1 to FAD8), FAD2 and FAD3 are located in the ER membrane, while the others are plasmid-specific desaturases (;; Figure 1). Although the synthesis and unsaturation of the major lipids are performed in the chloroplasts or ER in higher plants, acyl chain modifications of lipids embedded in the PM rely on regulation by various desaturases and on lipid transfer. Ambient stresses, such as temperature fluctuations, are perceived by the PM and/or membranous organelles and can affect FAD activities at both the transcriptional and post-transcriptional levels, thereby altering the membrane fluidity. Recently, increasing evidence has shown that FAD2 and FAD3 are unstable and less enriched at elevated temperatures. The seedlings of the fad2 mutant are unable to elongate their stems at 12°C and die at 6°C; similarly, the lethal temperature for fad1 is 2°C. Interestingly, the dwarf fad2 plant has been found to exhibit enhanced reactive oxygen species (ROS) and salicylic acid (SA) signaling, which are considered to regulate the heat stress response. Additionally, other fad mutants, such as fad5, show higher growth rates depending on the thermal conditions. FAD3, FAD7, and FAD8 have all been demonstrated to confer high-temperature instability, and three transgenic lines have exhibited higher levels of trienoic fatty acids in response to extreme temperatures. In fact, the varying amounts of unsaturated fatty acids incorporated into the major glycerolipids in fad mutants alter the composition and properties of their membranes, which may be the reason why their cells can sense and react to high temperatures. Confusingly, however, the mechanism through which FADs rapidly react to sudden temperature fluctuations and upstream factors with temperature sensitivity to regulate the activities of FADs remains unclear in plants.

Membrane Asymmetry and Lipid Translocases

6It is not only the chemical constitution of lipid membrane bilayers that is closely associated with the temperature; the multiple types of molecular motion by lipids (including rotation around their own axes, lateral diffusion within a monolayer and flip-flopping between the two monolayers) involved in the physical properties of the membrane are also highly temperature dependent. The transbilayer translocation of lipids is crucial for maintaining lipid asymmetry, which is necessary for membrane stability and the production of transport vesicles; translocation is also related to the demands of cell growth as well as cellular responses to physiological stresses. For instance, PS acts as a common type of phospholipid that is inserted in the membranes, and the flipping of the PS under stress is considered to be an important “eat-me” signal for macrophages in eukaryotes. In general, the asymmetrical distribution of lipids can be achieved through the actions of three protein families, scramblases, ABC transporters and P4-ATPases, which are found in plants and other organisms. The first group of proteins catalyzes the ATP-free bidirectional movement of lipids, whereas most ABC transporters shift lipids from the cytoplasmic to the exoplasmic leaflet (flopping), and P4-ATPases do just the opposite (flipping) (; Figure 1). The implications of scramblases in abiotic stress responses in the plant kingdom remain unclear, but there are a number of reports on the involvement of the other two types of floppase/flippase in responding to environmental challenges, including extreme temperatures. ABC transporters in A. thaliana belong to a large protein family with 129 members. Among these transporters, a previous study showed that reducing the functions of plasmid-specific ABC proteins TGD1, 2, 3, and 4 can effectively suppress the low-temperature-induced phenotype of the vte2 mutant. Earlier research indicated that the transcription of a homolog (TUR2) of the yeast ABC transporter gene PDR5 was induced by low temperatures in Spirodela polyrrhiza. found that the expression of ABC1 was specifically induced under a combination of saline and heat shock stresses in Suaeda salsa. Moreover, a subsequent report suggested that similar to other abiotic-stress-related genes, ABC transporters were abundantly enriched during cold acclimation in the grapevine Vitis amurensis. Likewise, 12 P4-ATPases in the Arabidopsis genome designated ALA1 to ALA12 were shown to perform inward lipid translocation, and the evidence obtained to date demonstrates that the functions of the proteins in this group are all affected to varying degrees by temperature fluctuations. For instance, ALA1 was shown to play a crucial role in chilling tolerance, while ALA3 regulates vegetative and reproductive growth in a temperature-dependent manner. ALA6 and ALA7 determine the fitness of pollen by regulating adaptations to daily temperature swings, and ALA6 has been verified to directly participate in thermotolerance. In addition, a recent study suggested that ALA10 contributed to regulating the activities of FAD2/FAD3 to control galactolipid synthesis in leaf development, and this positive regulation is susceptible to chilling stress. Nevertheless, solid evidence for the involvement of lipid translocation in temperature sensing has yet to be obtained.

Heat-Induced PM Stress Perception

7Temperature is a physical cue, and it directly alters the fluidity of biomembranes and the remodeling of membrane microdomains. This may have comprehensive effects not only on the membrane composition but also on specific interactions between lipids and proteins such as ion channels and kinases, subsequently altering the conformation and function of proteins and triggering particular signal transduction pathways (;; Figure 1). Cells remodel and reestablish membrane fluidity to cope with a change in the ambient temperature via the real-time control of lipid saturation and fatty acid length. Above all, subtle changes in membrane fluidity should be promptly perceived by PM sensors. Although studies have indicated that there are several ion channels that function as temperature sensors in animal cells, such as the transient receptor potential cation channel subfamily V (TRPV) and cyclic nucleotide-gated channels (CNGCs;; ), the PM thermosensor in plants long remained unidentified until the existence of primary sensors for heat stress was revealed in the PM of Physcomitrella patens. However, the membrane fluidizer benzyl alcohol can mimic the effects of high temperatures on the PM calcium-dependent heat shock response (HSR); conversely, the rigidifying agent dimethyl sulfoxide can decrease the heat-activated expression of HSPs, which also supports the conclusion that heat-mediated calcium channels are probably regulated by membrane fluidity. Further evidence of the role of these calcium channels as “thermosensors” in plants is needed. In particular, it is poorly understood how these calcium channels perceive and distinguish among different types of high-temperature stress (e.g., basal heat shock, warm priming/acclimation before heat shock, gradual temperature increases, hot-day/cold-night, or short-term and long-term heat stress).

Heat-Induced Second Messengers and Signal Cascades

8One of the earliest identified plant responses to elevated temperatures was a specific transient Ca2+ influx from the extracellular matrix to the cytoplasm. The effective suppression of the HSR pathway in higher plants by both calcium chelators and channel blockers suggested that an inward flux of Ca2+ and the ensuing signaling could play critical roles in the heat stress response. The presence of a calcium spike within seconds of thermal treatment in most model plants strongly indicates that heat-sensitive calcium-permeable channels are present in the PM and can transiently open or close during the thermotolerance process. Over 40 putative calcium channels located in the PM in the A. thaliana genome are regarded as the candidate heat sensors. indicated that cyclic nucleotide-gated ion channel 6 (CNGC6) might mediate the heat-activated Ca2+ influx and the expression of HSPs in A. thaliana during plant adaptive responses to heat (Figure 1). Additionally, CNGC6 was also activated by cytosolic cyclic adenosine monophosphate (cAMP), the concentration of which could be rapidly increased within 2 min after heat shock. The binding of free Ca2+ ions to calmodulins (CaMs) has been demonstrated to trigger PM calcium signal cascades, which can activate the HSF and HSP networks. In A. thaliana, AtCaM3 is primarily involved in the activation of transcription factors comprising HSFs, multiprotein bridging factor 1c (MBF1c), WRKY DNA-binding domain superfamily protein (WRKY39) and dehydration-responsive element binding protein (DREB) (;;; Figure 1). MBF1c has been demonstrated to regulate the expression of over 30 heat-related transcripts, including HSFB2a and HSFB2b as well as DREB2A, which is upstream of HSFA3. WRKY39 facilitates the jasmonic acid and SA signaling pathways under heat stress. With respect to the HSFs and the HSF-HSP signaling pathway, the numerous efforts aimed at understanding these proteins began as early as 1960s and 1970s and will therefore not be addressed in this review (see reviews from;;; ). AtCaM3 binds to the Arabidopsis CaM-binding protein kinase 3 (AtCBK3) to promote the phosphorylation of HSFA1a via the activation of a heat-induced transient Ca2+ increase, while calmodulin-dependent phosphatase 7 (PP7) mediates the dephosphorylation of HSFA1a in a Ca2+-dependent manner.

9Hydrogen peroxide (H2O2) is considered to be the other crucial second messenger when plants are exposed to elevated temperatures, because a rapid accumulation of H2O2 can occur within several minutes. The PM-located protein RBOHD is involved in the generation of H2O2 and is directly activated by an increase in cytosolic calcium and/or the phosphorylation of a calcium-dependent protein kinase (CDPK;; Figure 1). The downstream signal cascades of RBOHD also comprise certain HSFs, mitogen-activated protein kinases (MAPKs) and MBF1c, which are involved in HSR (,;; Figure 1). For example, HSFA4a might be a sensor of the H2O2 signaling, while HSFA5 serves as a repressor of this pathway. MAPKs can affect the expression and activity of catalase (CAT) to control the ROS levels while conversely regulating the expression of RBOHD in various genera.

10In addition, studies have shown that more than 1000 lipids are engaged in stress-induced cell signaling, a number far exceeding that of structural lipids. Lipids themselves appear to be versatile, acting not only as structural components but also as signaling mediators. One well-known example is the obvious rapid increases in PA and PIP2 observed under heat stress, the synthesis of which are catalyzed by PM-localized phospholipase D (PLD) and phosphatidylinositol-4-phosphate 5-kinase (PIPK), respectively (; Figure 1). Heat-induced changes in membrane fluidity might activate phospholipases and kinases on the PM, including PLD and PIPK. Additionally, PIP2 is hydrolyzed by membrane-bound PLCs and releases diacylglycerol (DAG) and inositol 1,4,5-triphosphate (IP3), which increases rapidly within 3 min after heat shock in Arabidopsis. IP3, which is generally considered a classic second messenger that is phosphorylated into IP6, is implicated in the regulation of intracellular calcium stores (; Figure 1). However, an IP6 receptor has yet to be identified in plants. Furthermore, PIP2 itself also plays an important role in biotic and abiotic stress-signaling transduction that are related, for example, to membrane stability, the cytoskeletal order and the budding of secretory vesicles. PA is a structural lipid, and it acts as a key coordinator of the PLC signaling pathway in plants. Arabidopsis AtPLC3 and AtPLC9 are associated with the regulation of small HSP (sHSP) expression during the thermotolerance process by the same mechanisms.

Cold-Induced PM Stress Signal Cascades

11A growth temperature that is higher or lower than the optimum range is defined as heat or cold stress. Although this concept is related to different plants, in general, cold-sensitive species can be harmed at temperatures below 15°C, while cold-tolerant plants may survive at temperatures close to 5°C. As temperature effects, the cold signaling responses involve similar stages as those observed in plants exposed to heat. For instance, the cold first has an influence on the membrane fluidity via fatty acid saturation. In contrast to heat stress, low temperatures cause changes in the physical state of the membrane bilayer from a fluid-crystalline phase to a solid-gel phase, accompanied by decreased permeability, which is referred to as the membrane rigidity. Incremental membrane rigidity can also alter the activities of some channels, kinases and G-protein-associated receptors on the PM and thus rapidly induce increases in intracellular calcium, PA, and ROS similar to those in heat-treated cells. However, differences between these two types of temperature stress arise in the subsequent signal cascades. The increased PA, which can be produced by activated PLD under cold conditions, can trigger ROS production in cells and may be involved in the ABA-dependent responses under cold stress. In addition, a Ca2+ signature can be decoded by many calcium sensors, among which the CaM-binding transcription activator (CAMTA3) has been shown to bind to the promoters of C-repeat-binding factors (CBF2/DREB1C) and induce their gene expression. The MAPK cascades are also implicated in the up-regulation of CBF/DREB1s transcription factors during cold stress signaling, including that of MPK3, MPK4, and MPK6 in Arabidopsis. CBF-dependent cold-responsive (COR) gene expression is considered to be a central regulatory pathway in the cold stress response, which is regulated by ICEs (inducers of CBF expression; ). The numbers and categories of COR genes are diverse; some of their products have been found to maintain cell membrane structures, activate ROS-scavenging enzymes, and promote the accumulation of osmolytes when plants are exposed to cold stress. Interestingly, identified 130 CORs that were similarly induced by warm temperatures according to analyses in CBF-overexpressing plants. Furthermore, HSFC1 positively regulates COR gene expression independent of the CBF2 signaling pathway under freezing conditions. Thus, the different types of temperature (heat or cold)-induced signal transduction share an affinity with each other in terms of both molecular components and signaling pathways, which may start at temperature-altered membrane fluidity and induce responsive gene expression to maintain cell integrity and function. Additionally, similar to studies on HSR, the specific plant sensors for the cold stress response and the mechanisms by which the sensors perceive cold signaling remain to be further elucidated.

Roles of the Chloroplast and Mitochondrion in Heat Stress Sensing and Responses

12The chloroplast and mitochondrion are membranous organelles in which carbon metabolism and energy exchange occur. Due to the ROS [including H2O2, superoxide anions (O2∙-), hydroxyl radicals (•OH), and singlet oxygen (1O2)] that are produced in the electron transport chain and the accompanying metabolic energy distribution during photosynthesis and respiration, chloroplast and mitochondrion components are the major targets of oxidative damage in plants, especially in the presence of other environmental stresses, such as high temperatures. Moreover, because both the chloroplast and mitochondrion are semiautonomous organelles regulated by the nucleus, the communication of organelle stresses to the nucleus and the modulation of the expression of stress-related genes, which are defined as retrograde signaling pathways, are considered to be extremely significant during physiological challenges, including heat stress (; Figure 2).

Chloroplasts

13In chloroplasts, the photosynthetic apparatus primarily consists of the thylakoid membrane; all the components related to photon capture, electron transfer and energy exchange are found in different compartments of the thylakoid, and its lipid composition and physical state therefore appear to be particularly important for the photosynthetic system. Unlike the PM, the thylakoid membrane is composed of highly unsaturated glyceroglycolipids containing considerable amounts of monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG) as well as small amounts of phosphatidylglycerol (PG) and sulfoquinovosyldiacylglycerol (SQDG). Hence, polyunsaturated fatty acids unavoidably become a site of attack by lipid peroxyl radicals under heat stress if the fatty acid moiety is near the QB site on the PSII electron acceptor side, suggesting that the fluidity of the thylakoid membrane is important for PSII function (;;; Figure 2). Moreover, both 1O2 formation on the electron acceptor side and •OH production on the electron donor side result from the inactivation of PSII electron transport when plants are exposed to heat stress. For instance, high temperatures efficiently shift the midpoint redox potential of QA/QA-, which leads to the suppression of electron transfer from QA to QB on the electron acceptor side of PSII. In the green alga Chlamydomonas reinhardtii, 1O2 formation as initiated by heat-induced lipid peroxidation, in which lipoxygenase plays the primary role, has been demonstrated. Lipid peroxidation products also have a pernicious effect on PSII proteins via oxidative modification, protein cleavage and irreversible protein aggregation. Studies have shown that the reaction center binding protein D1 can be cleaved in spinach thylakoid membranes under heat stress and that lipid peroxidation occurs in spinach thylakoids, and 1O2 is subsequently produced, which in turn causes D1 protein degradation via interactions with the protein. In addition, heat-induced lipid peroxidation can facilitate the denaturation and destabilization of PsbO (PsbP and PsbQ in spinach PSII) binding to the PSII core complex and promote manganese ion release from the Mn4O5Ca cluster, which has been demonstrated to be the main reason for the inactivation of electron transport on the donor side of PSII. In maintaining the chloroplast membrane under heat stress, a remarkable role is played by the vesicle-inducing protein in plastid 1 (VIPP1), which localizes to the chloroplast envelope and thylakoid membrane. VIPP1 was recently indicated to be a GTPase involved in maintaining the integrity of photosynthetic membranes via an effect on membrane remodeling when plants were subjected to stresses.

14Chloroplast retrograde signaling can be initiated by the accumulation of the chlorophyll intermediate Mg-protoporphyrin IX (Mg-ProtoIX, belonging to tetrapyrroles), as shown by gun (genome uncoupled) mutants, which exhibit impaired communication from the chloroplast to the nucleus, controlling photosynthesis-associated nuclear gene (PhANG) expression (;;;;;;;; Figure 2). GUN1, which encodes a unique plastid-localized pentatricopeptide repeat (PPR) protein, has been shown to be required to transmit stress signaling to the nuclear transcription factor ABA insensitive 4 (ABI4; ). Additionally, ABI4 is considered to be a central regulator that is involved in many essential environmental signaling pathways and in the developmental as well as central metabolic processes of cells or organelles (reviewed by ). Findings in Chlamydomonas reinhardtii have further indicated that Mg-ProtoIX transiently promotes the expression of heat shock protein 70 (HSP70), which may localize to both the plastid and cytoplasm. In addition, nuclear gene transcriptional studies on the above green alga showed that more than half of tetrapyrrole-interrelated genes were also activated by heat stress. Moreover, the chloroplast ribosomal protein S1 (RPS1) was reported to activate the expression of HSFA2, which is considered to regulate heat-stress-responsive genes during heat acclimation.

Mitochondria

15In the mitochondria, a type of phospholipid known as cardiolipin (CL), which has a high percentage of polyunsaturated fatty acids, is embedded in the mitochondrial membrane, where lipid peroxidation occurs (;; Figure 2). Damaged CL strongly decreases the activity of cytochrome c oxidase (CCO) under stress. Moreover, in A. thaliana, cardiolipin synthase (CLS) is required for mitochondrial morphogenesis and the response to high-temperature stress. The physical state of the mitochondrial membrane is also crucial; the depolarization of the mitochondrial membrane by the protonophore CCCP has been shown to inhibit ROS generation under thermal treatment. Additionally, the mitochondrion is one of the key compartments in ROS generation, especially when the rate of the electron transport chain has been decreased by environmental stresses. ROS negatively affect both lipids and proteins. The products of protein oxidation consist mostly of tryptophan and products of carbonylation and fragmentation. For example, some Krebs cycle enzymes, other redox enzymes, and HSPs as well as Mn superoxide dismutase (Mn-SOD) and the voltage-dependent anion channel from rice leaf mitochondria, can be carbonylated under stress (; Figure 2).

16The mitochondrial retrograde signaling pathway also shows a relationship with ROS generation and accumulation (;; Figure 2). When electron transport is disrupted by abiotic stresses, the increased expression of nuclear-encoded alternative oxidase 1 (AOX1) regulates the ROS level to trigger retrograde responses in plants. The AOX1A promoter sequence is one of the targets of ABI4 in A. thaliana; ABI4 is involved in mitochondrion-to-nucleus retrograde signaling as well as that in chloroplasts. Because mitochondrial complexes I and III are the primary sites of ROS generation, a mutation in complex I can promote ROS accumulation and decrease the expression of COR genes. Mitochondrion-derived DEXH box RNA helicases or PPR proteins also induce ROS accumulation and are involved in ABA responses.

Calcium Ions and HSPs in Chloroplasts and Mitochondria

17The roles of Ca2+ and HSPs in the regulation of organelle signaling under high-temperature stress should not be ignored. Earlier studies showed that chloroplasts contained high total Ca2+concentrations, while the potential of the plant inner mitochondrial membrane may affect the level of cytosolic Ca2+ and, thus, the expression of heat-responsive genes. However, further studies are needed in this field.

18The HSPs exhibit a chaperone function, folding polypeptides into a mature state or preventing misfolded proteins from aggregation, and they have been found to accumulate in cells under thermal stress. Because most proteins in chloroplasts and mitochondria are encoded by nuclear genes, and the polypeptides are exported from the nucleus to the organelles, HSPs are correspondingly required for the protein conformational changes during these processes. HSP70 acts upstream of other HSPs and cooperates with other chaperones in protein folding, refolding and disaggregation. Chloroplast stromal HSP70 was found to be involved in PSII repair under stress and to be affected by the redox state of the chloroplast. Another HSP, HSP90, more likely serves as a regulator of signal transfer to the nucleus, including the modulation of photosynthesis-related genes and stress-related genes, although it can also stabilize unfolded proteins. The sHSPs are chaperones that show high diversity among species and tissues and can prevent improper protein aggregation and partially unfold under stress conditions. Several lines of evidence have suggested that a small chloroplast HSP, HSP21, is involved in plant adaptations to heat stress and oxidative stress. A recent study demonstrated that HSP21 could bind to and stabilize PSII core proteins D1 and D2 under heat stress, which was activated by the GUN5-associated retrograde signaling pathway. GUN5 encodes an Mg chelatase that can insert Mg2+ into the protoporphyrin ring during tetrapyrrole biosynthesis, which regulates ROS-induced gene expression. Furthermore, HSP21 was demonstrated to interact with another protein, plastid transcriptionally active 5 (pTAC5), which is required for plastid-encoded RNA polymerase (PEP)-dependent transcription, and the latter protein plays a crucial role in plastid development under heat stress.

ER Stress

19The ER is the largest endomembrane system, and it is responsible for protein synthesis, folding, modification and export as well as lipid metabolism. More than a third of the total proteins pass through the secretory pathway via the ER lumen. Therefore, ER homeostasis is highly susceptible to environmental cues, inevitably resulting in the production of misfolded proteins or the accumulation of unfolded proteins, which are also known as ER stress. The mechanism underlying the response to ER stress at the transcriptional and translational levels is referred to as the unfolded protein response (UPR), which includes the detection of unfolded or misfolded proteins; the activation of chaperones, foldases and pertinent factors; and the reduction of the secreted and membrane protein contents. If the UPR is overextended and ER homeostasis cannot be sustained, cells will initiate programmed death. In addition to aberrant proteins, instability of phospholipid metabolism also leads to ER stress and activates the UPR. Studies on yeast and mammalian cells revealed that an imbalanced PC to PE ratio is a crucial cause of ER stress. However, the link between lipid functions and the ER stress response is still poorly understood in plants. verified that Arabidopsis glycerolipid homeostasis might be sustained at the post-transcriptional level under ER stress. Additionally, a study on maize illustrated that ER stress could affect the enzyme activity of diacylglycerol kinase (DGA), choline phosphate cytidylyltransferase, phosphatidylinositol-4-kinase, and PIPK.

ER Stress Sensors Perceive High-Temperature Stress

20Nascent proteins require molecular chaperones to prevent their aggregation and assist in their folding into functional conformations. Binding protein (BiP), an HSP70, is a common chaperone in the ER that is recruited by the DNAJ protein ERdj3 to bind unfolded proteins (; Figure 1). Other chaperones known as foldases have also been described in several previous reviews.

21Plants harbor two primary signaling pathways that have been reported to sense ER stress. One is aided by membrane-associated transcription factors (the basic leucine zipper transcription factors bZIP17 and bZIP28), and the other involves an RNA splicing factor (the inositol-requiring enzyme IRE1) (; Figure 1). The bZIP28 can specifically sense heat-triggered ER stress via BiP, after which it translocated into the Golgi, and its TF domain on the cytosol side can be cleaved by proteolytic processing. The TF portion subsequently enters the nucleus to activate the expression of stress-related genes. In addition, IRE1 is activated by interaction with unfolded proteins and then recognizes and splices the mRNA of bZIP60, after which the splicing products enter the nucleus to trigger the expression of UPR genes (;; Figure 1). Heat stress has been validated as a direct and efficient factor that influences the nuclear relocation of bZIP28 and the mRNA splicing of bZIP60.

Conclusion and Perspective

22Temperature fluctuation is an unusual ambient signal that causes concurrent alterations in multiple cellular compartments, including the PM, cytosol, energy-associated organelles and chromatin. In fact, there is widespread support for the notion that an increase in PM fluidity as induced by high temperatures first activates stress-signaling pathways (reviewed by ). However, how should the concept of “primary heat sensors” be understood? If the macromolecules in plant cells are defined as thermosensors that are able to not only precisely perceive various temperature changes but also differentially trigger specific signaling pathways, the most feasible strategy might be to first divert ambient temperature signals into different cell signaling patterns before they are perceived by sensors. From this perspective, the specific role of the membrane might be to serve as both a thermometer and a stress encoder. Additionally, subtle changes in the lipid composition of fatty acid chains or head groups can alter both the membrane properties and the interaction with specific proteins and even the membrane substructures (microdomains), which are highly sensitive to environmental perturbation; in this context, the membrane clearly meets the requirement for encoding stress. Of course, more evidence must be obtained and evaluated to dissect the mechanisms of membrane-associated stress sensing and signaling. One important reason why it is so difficult to study these mechanisms is that membrane structures in plant cells possessing a cell wall exhibit an enormous variety of membrane components with diverse localizations, interactions, and functions. The conventional methods for the investigation of membrane proteins have obvious limitations (e.g., specific protein associations can be disrupted by detergents;; ). The other reason is that the available studies on lipids and relevant enzymes are not equivalent to the attention paid to the proteins involved in signal transduction, despite the fact that membrane lipids show the best fit for the response to various environmental cues among these molecules. Fortunately, the direct visualization of the distribution of membrane constituents that rely on fluorescence microscopy approaches makes it possible to detect the dynamic interaction and distribution of PM substructures (reviewed by;; ). In addition, based on improvements in the sensitivity and accuracy of mass spectrometry and chromatography as well as microarray transcriptome analyses, it is possible to obtain knowledge of the entire lipidome and the complicated regulatory network at a certain time point in an individual tissue type under stresses.

23Furthermore, numerous vesicles in cells are also an important part of the membrane system whose formation and trafficking in plants have been shown to be involved in membrane repair under abiotic and biotic stresses (reviewed by;; ). However, much about the underlying mechanism of communication between extra-membrane and membranous organelles remains to be elucidated. Moreover, heat stress is inevitably associated with various other stresses during actual crop production. For example, high temperatures are often accompanied by high light, which can accelerate the plant injury inflicted by drought and salinity stress in inland regions. Elevated temperatures have also been shown to promote the infection of plant cells by pathogens and cause damage to SA defense. The identification and elucidation of these “crosstalk” mechanisms seem precisely the task of the day.

24In short, although studies on the underlying mechanisms of plant adaptation to high temperature and the engineering of crop plants with higher thermotolerance are making steady progress, many questions are still open and need to be further addressed. Important issues include the following:

25Are other primary thermosensors present in the PM or other intracellular compartments that synergistically trigger multiple and/or specific responses?

26How is the signaling that is triggered by various forms, durations and intensities of high-temperature stress transmitted?

27What precise role do membrane microdomains play in the plant HR?

28How can the dynamic remodeling of membranes under various heat stresses be recorded or mimicked?

29How do second messengers transmit multiple signals to downstream components of HS signal transduction chains?

30How do the UPR in chloroplasts, the cytosol and the ER coordinately and collaboratively function in protein homeostasis?

31How does the PM contact other membranous organelles under elevated temperatures?

32How does the lipid metabolism in chloroplasts and the ER participate in membrane sensing and remodeling during the rapid HR?

33Apart from HSF-HSP responses, are there other HSR effectors that switch the comprehensive responses on/off in plant cells?

34How is heat stress sensing distinguished from and integrated with the sensing of other stresses?

Author Contributions

35YN prepared and wrote this manuscript. YX contributed by organizing and reviewing a major part of the manuscript.

Conflict of Interest Statement

36The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References 260

1.
Adhikari N. D. Froehlich J. E. Strand D. D. Buck S. M. Kramer D. M. Larkin R. M. (2011 ). GUN4-porphyrin complexes bind the ChlH/ GUN5 subunit of Mg-Chelatase and promote chlorophyll biosynthesis in Arabidopsis. Plant Cell 23 1449–1467.
Not in our library10.1105/tpc.110.082503
2.
Aguilar P. S. de Mendoza D. (2006 ). Control of fatty acid desaturation: a mechanism conserved from bacteria to humans. Mol. Microbiol. 62 1507–1514.
Not in our library10.1111/j.1365-2958.2006.05484.x
3.
P4-ATPases as Phospholipid Flippases—Structure, Function, and Enigmas · 2016
No notice
4.
Arispe N. Doh M. De Maio A. (2002 ). Lipid interaction differentiates the constitutive and stress-induced heat shock proteins Hsc70 and Hsp70. Cell Stress Chaperones 7 330–338.
Not in our library10.1379/1466-1268(2002)007<0330:lidtca>2.0.co;2
5.
Asada K. (2006 ). Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 141 391–396.
Not in our library10.1104/pp.106.082040
6.
Axelsen K. B. Palmgren M. G. (1998 ). Evolution of substrate specificities in the P-type ATPase superfamily. J. Mol. Evol. 46 84–101.
Not in our library10.1007/pl00006286
7.
Bahuguna R. N. Jha J. Pal M. Shah D. Lawas L. M. Khetarpal S. (2015 ). Physiological and biochemical characterization of NERICA-L-44: a novel source of heat tolerance at the vegetative and reproductive stages in rice. Physiol. Plant 154 543–559.
Not in our library10.1111/ppl.12299
8.
Baniwal S. K. Bharti K. Chan K. Y. Fauth M. Ganguli A. Kotak S. (2004 ). Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J. Biosci. 29 471–487.
Not in our library10.1007/bf02712120
9.
Baniwal S. K. Chan K. Y. Scharf S. K. Nover L. (2007 ). Role of heat stress transcription factor HsfA5 as specific repressor of HsfA4. J. Biol. Chem. 282 3605–3613.
Not in our library10.1074/jbc.m609545200
10.
Barajas-López Jde D. Blanco N. E. Strand Å. (2013 ). Plastid-to-nucleus communication, signals controlling the running of the plant cell. Biochim. Biophys. Acta 1833 425–437.
Not in our library10.1016/j.bbamcr.2012.06.020
11.
Baral A. Shruthi K. S. Mathew M. K. (2015 ). Vesicular trafficking and salinity responses in plants. IUBMB Life 67 677–686.
Not in our library10.1002/iub.1425
12.
Lipid remodelling: Unravelling the response to cold stress in Arabidopsis and its extremophile relative Eutrema salsugineum · 2017
No notice
13.
Beck C. F. (2005 ). Signaling pathways from the chloroplast to the nucleus. Planta 222 743–756.
Not in our library10.1007/s00425-005-0021-2
14.
Bernfur K. Rutsdottir G. Emanuelsson C. (2017 ). The chloroplast-localized small heat shock protein Hsp21 associates with the thylakoid membranes in heat-stressed plants. Protein Sci. 26 1773–1784.
Not in our library10.1002/pro.3213
15.
Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops · 2013
No notice
16.
Bligny R. Douce R. (1980 ). Precise localization of cardiolipin in plant cells. Biochim. Biophys. Acta 617 254–263.
Not in our library10.1016/0005-2760(80)90168-x
17.
Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance · 2013
No notice
18.
Botella C. Sautron E. Boudiere L. Michaud M. Dubots E. Yamaryo-Botté Y. (2016 ). ALA10, a phospholipid flippase, controls FAD2/FAD3 desaturation of phosphatidylcholine in the ER and affects chloroplast lipid composition in Arabidopsis thaliana. Plant Physiol. 170 1300–1314.
Not in our library10.1104/pp.15.01557
19.
Braam J. (1992 ). Regulated expression of the calmodulin-related TCH genes in cultured Arabidopsis cells: induction by calcium and heat shock. Proc. Natl. Acad. Sci. U.S.A. 89 3213–3216.
Not in our library10.1073/pnas.89.8.3213
20.
Brand J. J. Becker D. W. (1984 ). Evidence for direct roles of calcium in photosynthesis. J. Bioenerg. Biomembr. 16 239–249.
Not in our library10.1007/bf00744278
21.
Brown D. A. Rose J. K. (1992 ). Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68 533–544.
Not in our library10.1016/0092-8674(92)90189-j
22.
Browse J. Somerville C. (1991 ). Glycerolipid synthesis: biochemistry and regulation. Annu. Rev. Plant Physiol. Plant. Mol. Biol. 42 467–506.
Not in our library10.1146/annurev.pp.42.060191.002343
23.
Buchanan B. B. Gruissem W. Jones R. L. (2015 ). Biochemistry and Molecular Biology of Plants. West Sussex: Wiley Blackwell Press.
Not in our library
24.
Cacas J. L. Furt F. Le Guédard M. Schmitter J. M. Buré C. Gerbeau-Pissot P. (2012 ). Lipids of plant membrane rafts. Prog. Lipid Res. 51 272–299.
Not in our library10.1016/j.plipres.2012.04.001
25.
Caiveau O. Fortune D. Cantrel C. Zachowski A. Moreau F. (2001 ). Consequences of omega-6-oleate desaturase deficiency on lipid dynamics and functional properties of mitochondrial membranes of Arabidopsis thaliana. J. Biol. Chem. 276 5788–5794.
Not in our library10.1074/jbc.m006231200
26.
Chan T. Shimizu Y. Pospíšil P. Nijo N. Fujiwara A. Taninaka Y. (2012 ). Quality control of photosystem II: lipid peroxidation accelerates photoinhibition under excessive illumination. PLoS One 7:e52100.
Not in our library10.1371/journal.pone.0052100
27.
Che P. Bussell J. D. Zhou W. Estavillo G. M. Pogson B. J. Smith S. M. (2010 ). Signaling from the endoplasmic reticulum activates brassinosteroid signaling and promotes acclimation to stress in Arabidopsis. Sci. Signal. 3:ra69.
Not in our library10.1126/scisignal.2001140
28.
Chen S. T. He N. Y. Chen J. H. Guo F. Q. (2017 ). Identification of core subunits of photosystem II as action sites of HSP21, which is activated by the GUN5-mediated retrograde pathway in Arabidopsis. Plant J. 89 1106–1118.
Not in our library10.1111/tpj.13447
29.
Chen T. H. H. (1994 ). Plant adaptation to low temperature stress. Can. J. Plant Pathol. 16 231–236.
Not in our library10.1080/07060669409500760
30.
Chinnusamy V. Ohta M. Kanrar S. Lee B. H. Hong X. Agarwal M. (2003 ). ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev. 17 1043–1054.
Not in our library10.1101/gad.1077503
31.
Chinnusamy V. Zhu J. Zhu J. K. (2007 ). Cold stress regulation of gene expression in plants. Trends Plant Sci. 12 444–451.
Not in our library10.1016/j.tplants.2007.07.002
32.
Cook D. Fowler S. Fiehn O. Thomashow M. F. (2004 ). A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 101 15243–15248.
Not in our library10.1073/pnas.0406069101
33.
Cossani C. M. Reynolds M. P. (2012 ). Physiological traits for improving heat tolerance in wheat. Plant Physiol. 160 1710–1718.
Not in our library10.1104/pp.112.207753
34.
Deng Y. Humbert S. Liu J. X. Srivastava R. Rothstein S. J. Howell S. H. (2011 ). Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 108 7247–7252.
Not in our library10.1073/pnas.1102117108
35.
Deng Y. Srivastava R. Howell S. H. (2013 ). Endoplasmic reticulum (ER) stress response and its physiological roles in plants. Int. J. Mol. Sci. 14 8188–8212.
Not in our library10.3390/ijms14048188
36.
Dhanda S. S. Munjal R. (2012 ). Heat tolerance in relation to acquired thermotolerance for membrane lipids in bread wheat. Field Crops Res. 135 30–37.
Not in our library10.1016/j.fcr.2012.06.009
37.
Di Paolo G. De Camilli P. (2006 ). Phosphoinositides in cell regulation and membrane dynamics. Nature 443 651–657.
Not in our library10.1038/nature05185
38.
Doherty C. J. Van Buskirk H. A. Myers S. J. Thomashow M. F. (2009 ). Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell 21 972–984.
Not in our library10.1105/tpc.108.063958
39.
Dorne A. J. Joyard J. Douce R. (1990 ). Do thylakoids really contain phosphatidylcholine? Proc. Natl. Acad. Sci. U.S.A. 87 71–74.
Not in our library10.1073/pnas.87.1.71
40.
Dubots E. Botté C. Boudière L. Yamaryo-Botté Y. Jouhet J. Maréchal E. (2012 ). Role of phosphatidic acid in plant galactolipid synthesis. Biochimie 94 86–93.
Not in our library10.1016/j.biochi.2011.03.012
41.
Dyer J. M. Mullen R. T. (2001 ). Immunocytological localization of two plant fatty acid desaturases in the endoplasmic reticulum. FEBS Lett. 494 44–47.
Not in our library10.1016/s0014-5793(01)02315-8
42.
Enrique Gomez R. Joubès J. Valentin N. Batoko H. Satiat-Jeunemaître B. Bernard A. (2017 ). Lipids in membrane dynamics during autophagy in plants. J. Exp. Bot. 69 1287–1299.
Not in our library10.1093/jxb/erx392
43.
Escribá P. V. González-Ros J. M. Goñi F. M. Kinnunen P. K. Vigh L. Sánchez-Magraner L. (2008 ). Membranes: a meeting point for lipids, proteins and therapies. J. Cell Mol. Med. 12 829–875.
Not in our library10.1111/j.1582-4934.2008.00281.x
44.
Evans D. E. Briars S. A. Williams L. E. (1991 ). Active Ca2+-transport by plant cell membranes. J. Exp. Bot. 42 285–303.
Not in our library10.1093/jxb/42.3.285
45.
Eyster K. M. (2007 ). The membrane and lipids as integral participants in signal transduction: lipid signal transduction for the non-lipid biochemist. Adv. Physiol. Educ. 31 5–16.
Not in our library10.1152/advan.00088.2006
46.
Fedyaeva A. V. Stepanov A. V. Lyubushkina I. V. Pobezhimova T. P. Rikhvanov E. G. (2014 ). Heat shock induces production of reactive oxygen species and increases inner mitochondrial membrane potential in winter wheat cells. Biochemistry 79 1202–1210.
Not in our library10.1134/s0006297914110078
47.
Fowler S. Thomashow M. F. (2002 ). Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14 1675–1690.
Not in our library10.1105/tpc.003483
48.
Fragkostefanakis S. Mesihovic A. Hu Y. Schleiff E. (2016 ). Unfolded protein response in pollen development and heat stress tolerance. Plant Reprod. 29 81–91.
Not in our library10.1007/s00497-016-0276-8
49.
Frei N. F. D. Robatzek S. (2009 ). Trafficking vesicles: pro or contra pathogens? Curr. Opin. Plant Biol. 12 437–443.
Not in our library10.1016/j.pbi.2009.06.002
50.
Fu S. Yang L. Li P. Hofmann O. Dicker L. Hide W. (2011 ). Aberrant lipid metabolism disrupts calcium homeostasis causing liver endoplasmic reticulum stress in obesity. Nature 473 528–531.
Not in our library10.1038/nature09968
51.
Fujimoto T. Parmryd I. (2017 ). Interleaflet coupling, pinning, and leaflet asymmetry—major players in plasma membrane nanodomain formation. Front. Cell Dev. Biol. 4:155.
Not in our library10.3389/fcell.2016.00155
52.
Furt F. Simon-Plas F. Mongrand S. (2011 ). “Lipids of the plant plasma membrane,” in The Plant Plasma Membranes, eds Murphy A. S. Schulz B. Peer W. (Berlin: Springer Press), 3–30.
Not in our library10.1007/978-3-642-13431-9_1
53.
Gao F. Han X. Wu J. Zheng S. Shang Z. Sun D. (2012 ). A heat-activated calcium-permeable channel-Arabidopsis cyclic nucleotide-gated ion channel 6 – is involved in heat shock responses. Plant J. 70 1056–1069.
Not in our library10.1111/j.1365-313x.2012.04969.x
54.
Gao X. van der Veen J. N. Vance J. E. Thiesen A. Vance D. E. Jacobs R. L. (2015 ). Lack of phosphatidylethanolamine N-methyltransferase alters hepatic phospholipid composition and induces endoplasmic reticulum stress. Biochim. Biophys. Acta 1852 2689–2699.
Not in our library10.1016/j.bbadis.2015.09.006
55.
Gascard P. Tran D. Sauvage M. Sulpice J. C. Fukami K. Takenawa T. (1991 ). Asymmetric distribution of phosphoinositides and phosphatidic acid in the human erythrocyte membrane. Biochim. Biophys. Acta 1069 27–36.
Not in our library10.1016/0005-2736(91)90100-m
56.
Giraud E. Van Aken O. Ho L. H. Whelan J. (2009 ). The transcription factor ABI4 is a regulator of mitochondrial retrograde expression of ALTERNATIVE OXIDASE1a. Plant Physiol. 150 1286–1296.
Not in our library10.1104/pp.109.139782
57.
Gomès E. Jakobsen M. K. Axelsen K. B. Geisler M. Palmgren M. G. (2000 ). Chilling tolerance in Arabidopsis involves ALA1, a member of a new family of putative aminophospholipid translocases. Plant Cell 12 2441–2454.
Not in our library10.1105/tpc.12.12.2441
58.
Gong M. van der Luit A. Knight M. Trewavas A. (1998 ). Heat-shock induces changes in intracellular Ca2+ level in tobacco seedlings in relation to thermotolerance. Plant Physiol. 116 429–437.
Not in our library10.1104/pp.116.1.429
59.
Grover A. Agarwal M. Katiyar-Agarwal S. Sahi C. Agarwal S. (2000 ). Production of high temperature tolerant transgenic plants through manipulation of membrane lipids. Curr. Sci. 79 557–559.
Not in our library
60.
Guo L. (2011 ). Phosphatidic acid binds and stimulates Arabidopsis sphingosine kinases. J. Biol. Chem. 286 13336–13345.
Not in our library10.1074/jbc.m110.190892
61.
Gupta D. Tuteja N. (2011 ). Chaperones and foldases in endoplasmic reticulum stress signaling in plants. Plant Signal. Behav. 6 232–236.
Not in our library10.4161/psb.6.2.15490
62.
Gupta K. J. Hincha D. K. Mur L. A. (2011 ). No way to treat a cold. New Phytol. 189 360–363.
Not in our library10.1111/j.1469-8137.2010.03586.x
63.
Guy C. (1999 ). Molecular responses of plants to cold shock and cold acclimation. J. Mol. Microbiol. Biotechnol. 1 231–242.
Not in our library
64.
Guy C. L. (1990 ). Cold acclimation and freezing stress tolerance role of protein metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41 187–223.
Not in our library10.1146/annurev.pp.41.060190.001155
65.
Hadlington J. L. Denecke J. (2000 ). Sorting of soluble proteins in the secretory pathway of plants. Curr. Opin. Plant Biol. 3 461–468.
Not in our library10.1016/s1369-5266(00)00114-x
66.
A Global Survey of Gene Regulation during Cold Acclimation in Arabidopsis thaliana · 2005
No notice
67.
Hao H. Fan L. Chen T. Li R. Li X. He Q. (2014 ). Clathrin and membrane microdomains cooperatively regulate RbohD dynamics and activity in Arabidopsis. Plant Cell 26 1729–1745.
Not in our library10.1105/tpc.113.122358
68.
Haslberger T. Weibezahn J. Zahn R. Lee S. Tsai F. T. Bukau B. (2007 ). M domains couple the ClpB threading motor with the DnaK chaperone activity. Mol. Cell 25 247–260.
Not in our library10.1016/j.molcel.2006.11.008
69.
He J. Duan Y. Hua D. Fan G. Wang L. Liu Y. (2012 ). DEXH box RNA helicase-mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between abscisic acid and Auxin signaling. Plant Cell 24 1815–1833.
Not in our library10.1105/tpc.112.098707
70.
Heckathorn S. A. Downs C. A. Sharkey T. D. Coleman J. S. (1998 ). The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. Plant Physiol. 116 439–444.
Not in our library10.1104/pp.116.1.439
71.
Heinz E. (1993 ). “Biosynthesis of polyunsaturated fatty acids,” in Lipid Metabolism in Plants, ed. Moore T. S. (Boca Raton, FL: CRC Press), 33–90.
Not in our library
72.
Hemme D. Veyel D. Muhlhaus T. Sommer F. Jüppner J. Unger A. K. (2014 ). Systems-wide analysis of acclimation responses to long-term heat stress and recovery in the photosynthetic model organism Chlamydomonas reinhardtii. Plant Cell 26 4270–4297.
Not in our library10.1105/tpc.114.130997
73.
Landscape of the lipidome and transcriptome under heat stress in Arabidopsis thaliana · 2015
No notice
74.
Horiguchi G. Fuse T. Kawakami N. Kodama H. Iba K. (2000 ). Temperature dependent translational regulation of the ER omega-3 fatty acid desaturase gene in wheat root tips. Plant J. 24 805–813.
Not in our library10.1111/j.1365-313x.2000.00925.x
75.
Dual impact of elevated temperature on plant defence and bacterial virulence in Arabidopsis · 2017
No notice
76.
Iba K. (2002 ). Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. Annu. Rev. Plant Biol. 53 225–245.
Not in our library10.1146/annurev.arplant.53.100201.160729
77.
Intergovernmental Panel on Climate Change [IPCC] (2014a ). Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Geneva: IPCC, 151.
Not in our library
78.
Intergovernmental Panel on Climate Change [IPCC] (2014b ). Food Security and Food Production System,” in Climate Change 2014: Impacts, Adaptation and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press, 485–533.
Not in our library
79.
Jacobson K. Mouritsen O. G. Anderson R. G. (2007 ). Lipid rafts: at a crossroad between cell biology and physics. Nat. Cell Biol. 9 7–14.
Not in our library10.1038/ncb0107-7
80.
Jagadish S. V. Murty M. V. Quick W. P. (2015 ). Rice responses to rising temperatures–challenges, perspectives and future directions. Plant Cell Environ. 38 1686–1698.
Not in our library10.1111/pce.12430
81.
Jarsch I. K. Konrad S. S. Stratil T. F. Urbanus S. L. Szymanski W. Braun P. (2014 ). Plasma membranes are subcompartmentalized into a plethora of coexisting and diverse microdomains in Arabidopsis and Nicotiana benthamiana. Plant Cell 26 1698–1711.
Not in our library10.1105/tpc.114.124446
82.
Jin Y. Zhuang M. Hendershot L. M. (2009 ). ERdj3, a luminal ER DnaJ homologue, binds directly to unfolded proteins in the mammalian ER: identification of critical residues. Biochemistry 48 41–49.
Not in our library10.1021/bi8015923
83.
Kachroo A. Venugopal S. C. Lapchyk L. Falcone D. Hildebrand D. Kachroo P. (2004 ). Oleic acid levels regulated by glycerolipid metabolism modulate defense gene expression in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 101 5152–5157.
Not in our library10.1073/pnas.0401315101
84.
Kaplan F. Kopka J. Haskell D. W. Zhao W. Schiller K. C. Gatzke N. (2004 ). Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol. 136 4159–4168.
Not in our library10.1104/pp.104.052142
85.
Karnovsky M. J. Kleinfeld A. M. Hoover R. L. Klausner R. D. (1982 ). The concept of lipid domains in membranes. J. Cell Biol. 94 1–6.
Not in our library10.1083/jcb.94.1.1
86.
Khuu N. Gidda S. Shockey J. M. Dyer J. M. Mullen R. T. (2011 ). The N termini of Brassica and tung omega-3 fatty acid desaturases mediate proteasome-dependent protein degradation in plant cells. Plant Signal. Behav. 6 422–425.
Not in our library10.4161/psb.6.3.14522
87.
Kim K. H. Alam I. Kim Y. G. Sharmin S. A. Lee K. W. Lee S. H. (2012 ). Overexpression of a chloroplast-localized small heat shock protein OsHSP26 confers enhanced tolerance against oxidative and heat stresses in tall fescue. Biotechnol. Lett. 34 371–377.
Not in our library10.1007/s10529-011-0769-3
88.
Kodama H. Horiguchi G. Nishiuchi T. Nishimura M. Iba K. (1995 ). Fatty acid desaturation during chilling acclimatization is one of the factors involved in conferring low-temperature tolerance to young tobacco leaves. Plant Physiol. 107 1177–1185.
Not in our library10.1104/pp.107.4.1177
89.
Konigshofer H. Tromballa H. W. Loppert H. G. (2008 ). Early events in signalling high-temperature stress in tobacco BY2 cells involve alterations in membrane fluidity and enhanced hydrogen peroxide production. Plant Cell Environ. 31 1771–1780.
Not in our library10.1111/j.1365-3040.2008.01880.x
90.
Konrad S. S. Ott T. (2015 ). Molecular principles of membrane microdomain targeting in plants. Trends Plant Sci. 20 351–361.
Not in our library10.1016/j.tplants.2015.03.016
91.
Kotak S. Larkindale J. Lee U. von Koskull-Döring P. Vierling E. Scharf K. D. (2007 ). Complexity of the heat stress response in plants. Curr. Opin. Plant Biol. 10 310–316.
Not in our library10.1016/j.pbi.2007.04.011
92.
Koussevitzky S. Nott A. Mockler T. C. Hong F. Sachetto-Martins G. Surpin M. (2007 ). Signals from chloroplasts converge to regulate nuclear gene expression. Science 316 715–719.
Not in our library10.1126/science.1140516
93.
Kristensen B. K. Askerlund P. Bykova N. V. Egsgaard H. Møller I. M. (2004 ). Identification of oxidized proteins in the matrix of rice leaf mitochondria by immunoprecipitation and two-dimensional liquid chromatography-tandem mass spectrometry. Phytochemistry 65 1839–1851.
Not in our library10.1016/j.phytochem.2004.04.007
94.
Kropat J. Oster U. Rudiger W. Beck C. F. (1997 ). Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-shock genes. Proc. Natl. Acad. Sci. U.S.A. 94 14168–14172.
Not in our library10.1073/pnas.94.25.14168
95.
Kropat J. Oster U. Rudiger W. Beck C. F. (2000 ). Chloroplast signalling in the light induction of nuclear HSP70 genes requires the accumulation of chlorophyll precursors and their accessibility to cytoplasm/nucleus. Plant J. 24 523–531.
Not in our library10.1111/j.1365-313x.2000.00898.x
96.
Kusumi A. Fujiwara T. K. Chadda R. Xie M. Tsunoyama T. A. Kalay Z. (2012 ). Dynamic organizing principles of the plasma membrane that regulate signal transduction: commemorating the fortieth anniversary of Singer and Nicolson’s fluid mosaic model. Annu. Rev. Cell Dev. Biol. 28 215–250.
Not in our library10.1146/annurev-cellbio-100809-151736
97.
Kusumi A. Nakada C. Ritchie K. Murase K. Suzuki K. Murakoshi H. (2005 ). Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Annu. Rev. Biophys. Biomol. Struct. 34 351–378.
Not in our library10.1146/annurev.biophys.34.040204.144637
98.
Kusumi A. Suzuki K. G. Kasai R. S. Ritchie K. Fujiwara T. K. (2011 ). Hierarchical mesoscale domain organization of the plasma membrane. Trends Biochem. Sci. 36 604–615.
Not in our library10.1016/j.tibs.2011.08.001
99.
Lamosa P. Burke A. Peist R. Huber R. Liu M. Y. Silva G. (2000 ). Thermostabilization of proteins by diglycerol phosphate, a new compatible solute from the hyperthermophile Archaeoglobus fulgidus. Appl. Environ. Microbiol. 66 1974–1979.
Not in our library10.1128/aem.66.5.1974-1979.2000
100.
Langer T. Lu C. Echols H. Flanagan J. Hayer M. K. Hartl F. U. (1992 ). Successive action of DnaK, DnaJ and GroEL along the pathway of chaperone-mediated protein folding. Nature 356 683–689.
Not in our library10.1038/356683a0
101.
Larkin R. M. Alonso J. M. Ecker J. R. Chory J. (2003 ). GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299 902–906.
Not in our library10.1126/science.1079978
102.
Larkindale J. Hall J. D. Knight M. R. Vierling E. (2005 ). Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol. 138 882–897.
Not in our library10.1104/pp.105.062257
103.
Larkindale J. Knight M. R. (2002 ). Protection against heat stress induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol. 128 682–695.
Not in our library10.1104/pp.010320
104.
Laude A. J. Prior I. A. (2004 ). Plasma membrane microdomains: organization, function and trafficking. Mol. Membr. Biol. 21 193–205.
Not in our library10.1080/09687680410001700517
105.
Lee B. H. Lee H. Xiong L. Zhu J. K. (2002 ). A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. Plant Cell 14 1235–1251.
Not in our library10.1105/tpc.010433
106.
Lenoir G. Williamson P. Holthuis J. C. (2007 ). On the origin of lipid asymmetry: the flip side of ion transport. Curr. Opin. Chem. Biol. 11 654–661.
Not in our library10.1016/j.cbpa.2007.09.008
107.
León P. Gregorio J. Cordoba E. (2013 ). ABI4 and its role in chloroplast retrograde communication. Front. Plant Sci. 3:304.
Not in our library10.3389/fpls.2012.00304
108.
Levitt J. (ed.) (1980 ). “Responses of plants to environmental stress,” in Chilling, Freezing, and High Temperature Stresses, (New York, NY: Academic Press).
Not in our library
109.
Lherminier J. Elmayan T. Fromentin J. Elaraqui K. T. Vesa S. Morel J. (2009 ). NADPH oxidase-mediated reactive oxygen species production: subcellular localization and reassessment of its role in plant defense. Mol. Plant Microbe Interact. 22 868–881.
Not in our library10.1094/mpmi-22-7-0868
110.
Li B. Liu H. T. Sun D. Y. Zhou R. G. (2004 ). Ca2+ and calmodulin modulate DNA-binding activity of maize heat shock transcription factor in vitro. Plant Cell Physiol. 45 627–634.
Not in our library10.1093/pcp/pch074
111.
Li S. Zhou X. Chen L. Huang W. Yu D. (2010 ). Functional characterization of Arabidopsis thaliana WRKY39 in heat stress. Mol. Cells 29 475–483.
Not in our library10.1007/s10059-010-0059-2
112.
Li W. Zhang C. Lu Q. Wen X. Lu C. (2011 ). The combined effect of salt stress and heat shock on proteome profiling in Suaeda salsa. J. Plant Physiol. 168 1743–1752.
Not in our library10.1016/j.jplph.2011.03.018
113.
Lillemeier B. F. Pfeiffer J. R. Surviladze Z. Wilson B. S. Davis M. M. (2006 ). Plasma membrane-associated proteins are clustered into islands attached to the cytoskeleton. Proc. Natl. Acad. Sci. U.S.A. 103 18992–18997.
Not in our library10.1073/pnas.0609009103
114.
Lingwood D. Simons K. (2010 ). Lipid rafts as a membrane organizing principle. Science 327 46–50.
Not in our library10.1126/science.1174621
115.
Liu C. Willmund F. Golecki J. R. Cacace S. Hess B. Markert C. (2007a ). The chloroplast HSP70B-CDJ2-CGE1 chaperones catalyse assembly and disassembly of VIPP1 oligomers in Chlamydomonas. Plant J. 50 265–277.
Not in our library10.1111/j.1365-313x.2007.03047.x
116.
Liu H. T. Li G. L. Chang H. Sun D. Y. Zhou R. G. Li B. (2007b ). Calmodulin-binding protein phosphatase PP7 is involved in thermotolerance in Arabidopsis. Plant Cell Environ. 30 156–164.
Not in our library10.1111/j.1365-3040.2006.01613.x
117.
Liu H. C. Charng Y. Y. (2013 ). Common and distinct functions of Arabidopsis class A1 and A2 heat shock factors in diverse abiotic stress responses and development. Plant Physiol. 163 276–290.
Not in our library10.1104/pp.113.221168
118.
Liu H. C. Liao H. T. Charng Y. Y. (2011 ). The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. Plant Cell Environ. 34 738–751.
Not in our library10.1111/j.1365-3040.2011.02278.x
119.
Liu H. T. Gao F. Cui S. J. Han J. L. Sun D. Y. Zhou R. G. (2006 ). Primary evidence for involvement of IP3 in heat-shock signal transduction in Arabidopsis. Cell Res. 16 394–400.
Not in our library10.1038/sj.cr.7310051
120.
Liu H. T. Gao F. Li G. L. Han J. L. Liu D. L. Sun D. Y. (2008 ). The calmodulin-binding protein kinase 3 is part of heat-shock signal transduction in Arabidopsis thaliana. Plant J. 55 760–773.
Not in our library10.1111/j.1365-313x.2008.03544.x
121.
Liu J. X. Howell S. H. (2016 ). Managing the protein folding demands in the endoplasmic reticulum of plants. New Phytol. 211 418–428.
Not in our library10.1111/nph.13915
122.
Liu Y. He C. (2016 ). Regulation of plant reactive oxygen species (ROS) in stress responses: learning from AtRBOHD. Plant Cell Rep. 35 995–1007.
Not in our library10.1007/s00299-016-1950-x
123.
Lv Y. Shao G. Qiu J. Jiao G. Sheng Z. Xie L. (2017 ). White leaf and panicle 2, encoding a PEP-associated protein, is required for chloroplast biogenesis under heat stress in rice. J. Exp. Bot. 68 5147–5160.
Not in our library10.1093/jxb/erx332
124.
Malinsky J. Opekarová M. Grossmann G. Tanner W. (2013 ). Membrane microdomains, rafts, and detergent-resistant membranes in plants and fungi. Annu. Rev. Plant Biol. 64 501–529.
Not in our library10.1146/annurev-arplant-050312-120103
125.
Marla S. R. Shiva S. Welti R. Liu S. Burke J. J. Morris G. P. (2017 ). Comparative transcriptome and lipidome analyses reveal molecular chilling responses in chilling-tolerant sorghums. Plant Genome 10 1–16.
Not in our library10.3835/plantgenome2017.03.0025
126.
Martinière A. Lavagi I. Nageswaran G. Rolfe D. J. Maneta-Peyret L. Luu D. T. (2012 ). Cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proc. Natl. Acad. Sci. U.S.A. 109 12805–12810.
Not in our library10.1073/pnas.1202040109
127.
Maruyama K. Takeda M. Kidokoro S. Yamada K. Sakuma Y. Urano K. (2009 ). Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A. Plant Physiol. 150 1972–1980.
Not in our library10.1104/pp.109.135327
128.
Matsuda O. Sakamoto H. Hashimoto T. Iba K. (2005 ). A temperature sensitive mechanism that regulates post-translational stability of a plastidial omega-3 fatty acid desaturase (FAD8) in Arabidopsis leaf tissues. J. Biol. Chem. 280 3597–3604.
Not in our library10.1074/jbc.m407226200
129.
McClung C. R. Davis S. J. (2010 ). Ambient thermometers in plants: from physiological outputs towards mechanisms of thermal sensing. Curr. Biol. 20 R1086–R1092.
Not in our library10.1016/j.cub.2010.10.035
130.
Loss of the Arabidopsis thaliana P4-ATPases ALA6 and ALA7 Impairs Pollen Fitness and Alters the Pollen Tube Plasma Membrane · 2015
Not checked
131.
McDowell S. C. López-Marqués R. L. Poulsen L. R. Palmgren M. G. Harper J. F. (2013 ). Loss of the Arabidopsis thaliana P4-ATPase ALA3 reduces adaptability to temperature stresses and impairs vegetative, pollen, and ovule development. PLoS One 8:e62577.
Not in our library10.1371/journal.pone.0062577
132.
Meehl G. A. Tebaldi C. (2004 ). More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305 994–997.
Not in our library10.1126/science.1098704
133.
Merchant S. S. Allen M. D. Kropat J. Moseley J. L. Long J. C. Tottey S. (2006 ). Between a rock and a hard place: trace element nutrition in Chlamydomonas. Biochim. Biophys. Acta 1763 578–594.
Not in our library10.1016/j.bbamcr.2006.04.007
134.
Miller G. Mittler R. (2006 ). Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann. Bot. 98 279–288.
Not in our library10.1093/aob/mcl107
135.
Miller G. Schlauch K. Tam R. Cortes D. Torres M. A. Shulaev V. (2009 ). The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2:ra45.
Not in our library10.1126/scisignal.2000448
136.
Miquel M. James D. Jr. Dooner H. Browse J. (1993 ). Arabidopsis requires polyunsaturated lipids for low-temperature survival. Proc. Natl. Acad. Sci. U.S.A. 90 6208–6212.
Not in our library10.1073/pnas.90.13.6208
137.
Mishkind M. Vermeer J. E. Darwish E. Munnik T. (2009 ). Heat stress activates phospholipase D and triggers PIP accumulation at the plasma membrane and nucleus. Plant J. 60 10–21.
Not in our library10.1111/j.1365-313x.2009.03933.x
138.
Mittler R. Finka A. Goloubinoff P. (2012 ). How do plants feel the heat? Trends Biochem. Sci. 37 118–125.
Not in our library10.1016/j.tibs.2011.11.007
139.
Mittler R. Vanderauwera S. Gollery M. Van Breusegem F. (2004 ). Reactive oxygen gene network of plants. Trends Plant Sci. 9 490–498.
Not in our library10.1016/j.tplants.2004.08.009
140.
Cold Signaling and Cold Response in Plants · 2013
No notice
141.
Mochizuki N. Brusslan J. A. Larkin R. Nagatani A. Chory J. (2001 ). Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc. Natl. Acad. Sci. U.S.A. 98 2053–2058.
Not in our library10.1073/pnas.98.4.2053
142.
Møller I. M. Kristensen B. K. (2004 ). Protein oxidation in plant mitochondria as a stress indicator. Photochem. Photobiol. Sci. 3 730–735.
Not in our library10.1039/b315561g
143.
Mullarkey M. Jones P. (2000 ). Isolation and analysis of thermotolerant mutant of wheat. J. Exp. Bot. 51 139–146.
Not in our library10.1093/jexbot/51.342.139
144.
Nathan D. F. Vos M. H. Lindquist S. (1997 ). In vivo functions of the Saccharomyces cerevisiae Hsp 90 chaperone. Proc. Natl. Acad. Sci. U.S.A. 94 12949–12956.
Not in our library10.1073/pnas.94.24.12949
145.
Nievola C. C. Carvalho C. P. Carvalho V. Rodrigues E. (2017 ). Rapid responses of plants to temperature changes. Temperature 4 371–405.
Not in our library10.1080/23328940.2017.1377812
146.
Niu Y. Qian D. Liu B. Ma J. Wan D. Wang X. (2017 ). ALA6, a P4-type ATPase, is involved in heat stress responses in Arabidopsis thaliana. Front. Plant Sci. 8:1732.
Not in our library10.3389/fpls.2017.01732
147.
Ohnishi N. Zhang L. Sakamoto W. (2018 ). VIPP1 involved in chloroplast membrane integrity has GTPase activity in vitro. Plant Physiol. 177 328–338.
Not in our library10.1104/pp.18.00145
148.
O’Quin J. B. Bourassa L. Zhang D. Shockey J. M. Gidda S. K. Fosnot S. (2010 ). Temperature-sensitive post-translational regulation of plant omega-3 fatty-acid desaturases is mediated by the endoplasmic reticulum-associated degradation pathway. J. Biol. Chem. 285 21781–21796.
Not in our library10.1074/jbc.m110.135236
149.
Ortiz-Masia D. Perez-Amador M. A. Carbonell P. Aniento F. Carbonell J. Marcote M. J. (2008 ). Characterization of PsMPK2, the first C1 subgroup MAP kinase from pea (Pisum sativum L.). Planta 227 1333–1342.
Not in our library10.1007/s00425-008-0705-5
150.
Pan R. H. Jones A. D. Hu J. P. (2014 ). Cardiolipin-mediated mitochondrial dynamics and stress response in Arabidopsis. Plant Cell 26 391–409.
Not in our library10.1105/tpc.113.121095
151.
Paradies G. Ruggiero F. M. Petrosillo G. Quagliariello E. (1998 ). Peroxidative damage to cardiac mitochondria: cytochrome oxidase and cardiolipin alterations. FEBS Lett. 424 155–158.
Not in our library10.1016/s0014-5793(98)00161-6
152.
Park S. Lee C. M. Doherty C. J. Gilmour S. J. Kim Y. Thomashow M. F. (2015 ). Regulation of the Arabidopsis CBF regulon by a complex low-temperature regulatory network. Plant J. 82 193–207.
Not in our library10.1111/tpj.12796
153.
Penfield S. (2008 ). Temperature perception and signal transduction in plants. New Phytol. 179 615–628.
Not in our library10.1111/j.1469-8137.2008.02478.x
154.
Pitzschke A. Hirt H. (2009 ). Disentangling the complexity of mitogen-activated protein kinases and reactive oxygen species signaling. Plant Physiol. 149 606–615.
Not in our library10.1104/pp.108.131557
155.
Plieth C. (1999 ). Temperature sensing by plants: calcium-permeable channels as primary sensors — a model. J. Membr. Biol. 172 121–127.
Not in our library10.1007/s002329900590
156.
Plieth C. Hansen U. P. Knight H. Knight M. R. (1999 ). Temperature sensing by plants: the primary characteristics of signal perception and calcium response. Plant J. 18 491–497.
Not in our library10.1046/j.1365-313x.1999.00471.x
157.
Pomorski T. G. Menon A. K. (2016 ). Lipid somersaults: uncovering the mechanisms of protein-mediated lipid flipping. Prog. Lipid Res. 64 69–84.
Not in our library10.1016/j.plipres.2016.08.003
158.
Pospíšil P. Haumann M. Dittmer J. Dau H. (2003 ). Stepwise transition of the tetra-manganese complex of photosystem II to a binuclear Mn2(μ-O)2 complex in response to a temperature jump: a time-resolved structural investigation employing X-Ray absorption spectroscopy. Biophys. J. 84 1370–1386.
Not in our library10.1016/s0006-3495(03)74952-2
159.
Pospíšil P. Prasad A. (2014 ). Formation of singlet oxygen and protection against its oxidative damage in photosystem II under abiotic stress. J. Photochem. Photobiol. B Biol. 137 39–48.
Not in our library10.1016/j.jphotobiol.2014.04.025
160.
Pospíšil P. Šnyrychová I. Nauš J. (2007 ). Dark production of reactive oxygen species in photosystem II membrane particles at elevated temperature: EPR spin-trapping study. Biochim. Biophys. Acta 1767 854–859.
Not in our library10.1016/j.bbabio.2007.02.011
161.
Pospíšil P. Tyystjärvi E. (1999 ). Molecular mechanism of high-temperature-induced inhibition of acceptor side of photosystem II. Photosynth. Res. 62 55–66.
Not in our library10.1023/a:1006369009170
162.
Pospíšil P. Yamamoto Y. (2017 ). Damage to photosystem II by lipid peroxidation products. Biochim. Biophys. Acta 1861 457–466.
Not in our library10.1016/j.bbagen.2016.10.005
163.
Prasad A. Ferretti U. Sedlářová M. Pospíšil P. (2016 ). Singlet oxygen production in Chlamydomonas reinhardtii under heat stress. Sci. Rep. 6:20094.
Not in our library10.1038/srep20094
164.
Pröschold T. Harris E. H. Coleman A. W. (2005 ). Portrait of a species: Chlamydomonas reinhardtii. Genetics 170 1601–1610.
Not in our library10.1534/genetics.105.044503
165.
Pyatrikas D. V. Rikhvanov E. G. Fedoseeva I. V. Varakina N. N. Rusaleva T. M. Tauson E. L. (2014 ). Mitochondrial retrograde regulation of HSP101 expression in Arabidopsis thaliana under heat stress and amiodarone action. Russ. J. Plant Physiol. 61 80–89.
Not in our library10.1134/s1021443714010117
166.
Ramot D. Macinnis B. L. Goodman M. B. (2008 ). Bidirectional temperature-sensing by a single thermosensory neuron in C. elegans. Nat. Neurosci. 11 908–915.
Not in our library10.1038/nn.2157
167.
Ren H. Gao K. Liu Y. Sun D. Zheng S. (2017 ). The role of AtPLC3 and AtPLC9 in thermotolerance in Arabidopsis. Plant Signal. Behav. 12:e1162368.
Not in our library10.1080/15592324.2016.1162368
168.
Rhoads D. M. Subbaiah C. C. (2007 ). Mitochondrial retrograde regulation in plants. Mitochondrion 7 177–194.
Not in our library10.1016/j.mito.2007.01.002
169.
Rhoads D. M. Umbach A. L. Subbaiah C. C. Siedow J. N. (2006 ). Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol. 141 357–366.
Not in our library10.1104/pp.106.079129
170.
Rikhvanov E. G. Fedoseeva I. V. Pyatrikas D. V. Borovskii G. B. Voinikov V. K. (2014 ). Role of mitochondria in the operation of calcium signaling system in heat-stressed plants. Russ. J. Plant Physiol. 61 141–153.
Not in our library10.1134/s1021443714020125
171.
Ritossa F. (1962 ). A new puffing pattern induced by temperature shock and DNP in Drosophila. Experientia 18 571–573.
Not in our library10.1007/bf02172188
172.
Ron D. Walter P. (2007 ). Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8 519–529.
Not in our library10.1038/nrm2199
173.
Ruelland E. Cantrel C. Gawer M. Kader J. C. Zachowski A. (2002 ). Activation of phospholipases C and D is an early response to a cold exposure in Arabidopsis suspension cells. Plant Physiol. 130 999–1007.
Not in our library10.1104/pp.006080
174.
Ruelland E. Zachowski A. (2010 ). How plants sense temperature. Environ. Exp. Bot. 69 225–232.
Not in our library10.1016/j.envexpbot.2010.05.011
175.
Rutgers M. Schroda M. (2013 ). A role of VIPP1 as a dynamic structure within thylakoid centers as sites of photosystem biogenesis? Plant Signal. Behav. 8:e27037.
Not in our library10.4161/psb.27037
176.
Saidi Y. Finka A. Chakhporanian M. Zryd J. P. Schaefer D. G. Goloubinoff P. (2005 ). Controlled expression of recombinant proteins in Physcomitrella patens by a conditional heat-shock promoter: a tool for plant research and biotechnology. Plant Mol. Biol. 59 697–711.
Not in our library10.1007/s11103-005-0889-z
177.
Saidi Y. Finka A. Goloubinoff P. (2011 ). Heat perception and signalling in plants: a tortuous path to thermotolerance. New Phytol. 190 556–565.
Not in our library10.1111/j.1469-8137.2010.03571.x
178.
Saidi Y. Finka A. Muriset M. Bromberg Z. Weiss Y. G. Maathuis F. J. (2009 ). The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell 21 2829–2843.
Not in our library10.1105/tpc.108.065318
179.
Saidi Y. Peter P. Finka A. Cicekli C. Vigh L. Goloubinoff P. (2010 ). Membrane lipid composition affects plant heat sensing and modulates Ca2+-dependent heat shock response. Plant Signal. Behav. 5 1530–1533.
Not in our library10.4161/psb.5.12.13163
180.
Sánchez-García A. Mancha M. Heinz E. Martínez-Rivas J. M. (2004 ). Differential temperature regulation of three sunflower microsomal oleate desaturase (FAD2) isoforms overexpressed in Saccharomyces cerevisiae. Eur. J. Lipid Sci. Technol. 106 583–590.
Not in our library10.1002/ejlt.200401005
181.
Scharf K. D. Berberich T. Ebersberger I. Nover L. (2012 ). The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim. Biophys. Acta 1819 104–119.
Not in our library10.1016/j.bbagrm.2011.10.002
182.
Schramm F. Larkindale J. Kiehlmann E. Ganguli A. Englich G. Vierling E. (2008 ). A cascade of transcription factor DREB2A and heat stress transcription factor HsfA3 regulates the heat stress response of Arabidopsis. Plant J. 53 264–274.
Not in our library10.1111/j.1365-313x.2007.03334.x
183.
Schroda M. Hemme D. Mühlhaus T. (2015 ). The Chlamydomonas heat stress response. Plant J. 82 466–480.
Not in our library10.1111/tpj.12816
184.
Schroda M. Vallon O. Wollman F. A. Beck C. F. (1999 ). A chloroplast-targeted heat shock protein 70 (HSP70) contributes to the photoprotection and repair of photosystem II during and after photoinhibition. Plant Cell 11 1165–1178.
Not in our library10.1105/tpc.11.6.1165
185.
Segawa K. Kurata S. Yanagihashi Y. Brummelkamp T. R. Matsuda F. Nagata S. (2014 ). Caspase-mediated cleavage of phospholipid flippase for apoptotic phosphatidylserine exposure. Science 344 1164–1168.
Not in our library10.1126/science.1252809
186.
Segawa K. Suzuki J. Nagata S. (2011 ). Constitutive exposure of phosphatidylserine on viable cells. Proc. Natl. Acad. Sci. U.S.A. 108 19246–19251.
Not in our library10.1073/pnas.1114799108
187.
Shah M. Patel K. Fried V. A. Sehgal P. B. (2002 ). Interactions of STAT3 with caveolin-1 and heat shock protein 90 in plasma membrane raft and cytosolic complexes. Preservation of cytokine signaling during fever. J. Biol. Chem. 277 45662–45669.
Not in our library10.1074/jbc.m205935200
188.
Shakeel S. Haq N. U. Heckathorn S. A. Hamilton E. W. Luthe D. S. (2011 ). Ecotypic variation in chloroplast small heat-shock proteins and related thermotolerance in Chenopodium album. Plant Physiol. Biochem. 49 898–908.
Not in our library10.1016/j.plaphy.2011.05.002
189.
Shank K. J. Su P. Brglez I. Boss W. F. Dewey R. E. Boston R. S. (2001 ). Induction of lipid metabolic enzymes during the endoplasmic reticulum stress response in plants. Plant Physiol. 126 267–277.
Not in our library10.1104/pp.126.1.267
190.
Sharkey T. D. (2000 ). Some like it hot. Science 287 435–437.
Not in our library10.1126/science.287.5452.435
191.
Shinozaki K. Uemura M. Bailey-Serres J. Bray E. A. Weretilnyk E. (2015 ). “Responses to abiotic stress,” in Biochemistry and Molecular Biology of Plants, eds Buchanan B. B. Gruissem W. Vickers K. Jones R. L. (Hoboken, NJ: John Wiley & Sons Press).
Not in our library
192.
Siddhanta A. Shields D. (1998 ). Secretory vesicle budding from the trans-Golgi network is mediated by phosphatidic acid levels. J. Biol. Chem. 273 17995–17998.
Not in our library10.1074/jbc.273.29.17995
193.
Simons K. Ikonen E. (1997 ). Functional rafts in cell membranes. Nature 387 569–572.
Not in our library10.1038/42408
194.
Simons K. Toomre D. (2000 ). Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1 31–39.
Not in our library10.1038/35036052
195.
Singer S. D. Zou J. Weselake R. J. (2016 ). Abiotic factors influence plant storage lipid accumulation and composition. Plant Sci. 243 1–9.
Not in our library10.1016/j.plantsci.2015.11.003
196.
Singer S. J. Nicolson G. L. (1972 ). The fluid mosaic model of the structure of cell membranes. Science 175 720–731.
Not in our library10.1126/science.175.4023.720
197.
Smart C. C. Fleming A. J. (1996 ). Hormonal and environmental regulation of a plant PDR5-like ABC transporter. J. Biol. Chem. 271 19351–19357.
Not in our library10.1074/jbc.271.32.19351
198.
Smékalová V. Doskočilová A. Komis G. Samaj J. (2014 ). Crosstalk between secondary messengers, hormones and MAPK modules during abiotic stress signalling in plants. Biotechnol. Adv. 32 2–11.
Not in our library10.1016/j.biotechadv.2013.07.009
199.
Somerville C. Browse J. Jaworski J. G. Ohlrogge J. B. (2000 ). “Lipids,” in Biochemistry and Molecular Biology of Plants, eds Buchanan B. B. Gruissem W. Jones R. L. (Rockville, MD: American Society of Plant Biologists Press), 456–527.
Not in our library
200.
Song W. Maeda H. DellaPenna D. (2010 ). Mutations of the ER to plastid lipid transporters TGD1,2, 3 and 4 and the ER oleate desaturase FAD2 suppress the low temperature-induced phenotype of Arabidopsis tocopherol-deficient mutant vte2. Plant J. 62 1004–1018.
Not in our library10.1111/j.1365-313x.2010.04212.x
201.
Stout R. G. Summers M. L. Kerstetter T. McDermott T. R. (1997 ). Heat- and acid-tolerance of a grass commonly found in geothermal areas within Yellowstone National Park. Plant Sci. 130 1–9.
Not in our library10.1016/s0168-9452(97)00205-7
202.
Strand A. Asami T. Alonso J. Ecker J. R. Chory J. (2003 ). Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrin IX. Nature 421 79–83.
Not in our library10.1038/nature01204
203.
Sun A. Z. Guo F. Q. (2016 ). Chloroplast retrograde regulation of heat stress responses in plants. Front. Plant Sci. 7:398.
Not in our library10.3389/fpls.2016.00398
204.
Suri S. S. Dhindsa R. S. (2008 ). A heat-activated MAP kinase (HAMK) as a mediator of heat shock response in tobacco cells. Plant Cell Environ. 31 218–226.
Not in our library10.1111/j.1365-3040.2007.01754.x
205.
Susek R. E. Ausubel F. M. Chory J. (1993 ). Signal-transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene-expression from chloroplast development. Cell 74 787–799.
Not in our library10.1016/0092-8674(93)90459-4
206.
Suzuki N. Koussevitzky S. Mittler R. Miller G. (2012 ). ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ. 35 259–270.
Not in our library10.1111/j.1365-3040.2011.02336.x
207.
Suzuki N. Sejima H. Tam R. Schlauch K. Mittler R. (2011 ). Identification of the MBF1 heat-response regulon of Arabidopsis thaliana. Plant J. 66 844–851.
Not in our library10.1111/j.1365-313x.2011.04550.x
208.
Sweetlove L. J. Heazlewood J. L. Herald V. Holtzapffel R. Day D. A. Leaver C. J. (2002 ). The impact of oxidative stress on Arabidopsis mitochondria. Plant J. 32 891–904.
Not in our library10.1046/j.1365-313x.2002.01474.x
209.
Tang G. Q. Novitzky W. P. Carol Griffin H. Huber S. C. Dewey R. E. (2005 ). Oleate desaturase enzymes of soybean: evidence of regulation through differential stability and phosphorylation. Plant J. 44 433–446.
Not in our library10.1111/j.1365-313x.2005.02535.x
210.
Tang T. Liu P. Zheng G. Li W. (2016 ). Two phases of response to long-term moderate heat: variation in thermotolerance between Arabidopsis thaliana and its relative Arabis paniculata. Phytochemistry 122 81–90.
Not in our library10.1016/j.phytochem.2016.01.003
211.
Tanner W. Malinsky J. Opekarová M. (2011 ). In plant and animal cells, detergent-resistant membranes do not define functional membrane rafts. Plant Cell 23 1191–1193.
Not in our library10.1105/tpc.111.086249
212.
Taylor S. W. Fahy E. Murray J. Capaldi R. A. Ghosh S. S. (2003 ). Oxidative post-translational modification of tryptophan residues in cardiac mitochondrial proteins. J. Biol. Chem. 278 19587–19590.
Not in our library10.1074/jbc.c300135200
213.
Testerink C. Munnik T. (2005 ). Phosphatidic acid: a multifunctional stress signalling lipid in plants. Trends Plant Sci. 10 368–375.
Not in our library10.1016/j.tplants.2005.06.002
214.
Thibault G. Shui G. Kim W. McAlister G. C. Ismail N. Gygi S. P. (2012 ). The membrane stress response buffers lethal effects of lipid disequilibrium by reprogramming the protein homeostasis network. Mol. Cell 48 16–27.
Not in our library10.1016/j.molcel.2012.08.016
215.
Thompson T. E. Tillack T. W. (1985 ). Organization of glycosphingolipids in bilayers and plasma membranes of mammalian cells. Annu. Rev. Biophys. Biophys. Chem. 14 361–386.
Not in our library10.1146/annurev.bb.14.060185.002045
216.
Triantaphylides C. Havaux M. (2009 ). Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci. 14 219–228.
Not in our library10.1016/j.tplants.2009.01.008
217.
Triantaphylides C. Krischke M. Hoeberichts F. A. Ksas B. Gresser G. Havaux M. (2008 ). Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol. 148 960–968.
Not in our library10.1104/pp.108.125690
218.
Trösch R. Mühlhaus T. Schroda M. Willmund F. (2015 ). ATP-dependent molecular chaperones in plastids - More complex than expected. Biochim. Biophys. Acta 1847 872–888.
Not in our library10.1016/j.bbabio.2015.01.002
219.
van Meer G. Voelker D. R. Feigenson G. W. (2008 ). Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9 112–124.
Not in our library10.1038/nrm2330
220.
Vega V. L. De Maio A. (2005 ). Increase in phagocytosis after geldanamycin treatment or heat shock: role of heat shock proteins. J. Immunol. 175 5280–5287.
Not in our library10.4049/jimmunol.175.8.5280
221.
Vereb G. Szollosi J. Matko J. Nagy P. Farkas T. Vigh L. (2003 ). Dynamic, yet structured: the cell membrane three decades after the Singer-Nicolson model. Proc. Natl. Acad. Sci. U.S.A. 100 8053–8058.
Not in our library10.1073/pnas.1332550100
222.
Vigh L. Escribá P. V. Sonnleitner A. Sonnleitner M. Piotto S. Maresca B. (2005 ). The significance of lipid composition for membrane activity: new concepts and ways of assessing function. Prog. Lipid Res. 44 303–344.
Not in our library10.1016/j.plipres.2005.08.001
223.
Vigh L. Nakamoto H. Landry J. Gomez-Munoz A. Harwood J. L. Horvath I. (2007a ). Membrane regulation of the stress response from prokaryotic models to mammalian cells. Ann. N. Y. Acad. Sci. 1113 40–51.
Not in our library10.1196/annals.1391.027
224.
Vigh L. Török Z. S. Balogh G. Glatz A. Piotto S. Horváth I. (2007b ). “Membrane-regulated stress response,” in A Theoretical and Practical Approach in Molecular Aspects of the Stress Response: Chaperones, Membranes and Networks, eds Csermely P. Vigh L. (Austin, TX: Landes Bioscience), 114–142.
Not in our library10.1007/978-0-387-39975-1_11
225.
von Koskull-Döring P. Scharf K. D. Nover L. (2007 ). The diversity of plant heat stress transcription factors. Trends Plant Sci. 12 452–457.
Not in our library10.1016/j.tplants.2007.08.014
226.
Voss B. Meinecke L. Kurz T. Al-Babili S. Beck C. F. Hess W. R. (2011 ). Hemin and magnesium-protoporphyrin IX induce global changes in gene expression in Chlamydomonas reinhardtii. Plant Physiol. 155 892–905.
Not in our library10.1104/pp.110.158683
227.
Wallis J. G. Browse J. (2002 ). Mutants of Arabidopsis reveal many roles for membrane lipids. Prog. Lipid Res. 41 254–278.
Not in our library10.1016/s0163-7827(01)00027-3
228.
Walter P. Ron D. (2011 ). The unfolded protein response: from stress pathway to homeostatic regulation. Science 334 1081–1086.
Not in our library10.1126/science.1209038
229.
Wang G. F. Li W. Q. Li W. Y. Wu G. L. Zhou C. Y. Chen K. M. (2013 ). Characterization of rice NADPH oxidase genes and their expression under various environmental conditions. Int. J. Mol. Sci. 14 9440–9458.
Not in our library10.3390/ijms14059440
230.
Wang L. Xue Y. Xing J. Song K. Lin J. (2018 ). Exploring the spatiotemporal organization of membrane proteins in living plant cells. Annu. Rev. Plant Biol. 69 525–551.
Not in our library10.1146/annurev-arplant-042817-040233
231.
Ward J. M. Maser P. Schroeder J. I. (2009 ). Plant ion channels: gene families, physiology, and functional genomics analyses. Annu. Rev. Physiol. 71 59–82.
Not in our library10.1146/annurev.physiol.010908.163204
232.
Weis E. Berry J. A. (1988 ). Plants and high temperature stress. Symp. Soc. Exp. Biol. 42 329–346.
Not in our library
233.
Wood R. Harlow R. D. (1969 ). Structural analyses of rat liver phosphoglycerides. Arch. Biochem. Biophys. 135 272–281.
Not in our library10.1016/0003-9861(69)90540-2
234.
Woodson J. D. Chory J. (2008 ). Coordination of gene expression between organellar and nuclear genomes. Nat. Rev. Genet. 9 383–395.
Not in our library10.1038/nrg2348
235.
Wu H. C. Jinn T. L. (2010 ). Ethylesterase activity and cytosolic Ca2+ oscillation are crucial for plant thermotolerance. Plant Signal. Behav. 5 1252–1256.
Not in our library10.4161/psb.5.10.12607
236.
Wu H. C. Jinn T. L. (2012 ). Oscillation regulation of Ca2+/calmodulin and heat-stress related genes in response to heat stress in rice (Oryza sativa L.). Plant Signal Behav. 7 1056–1057.
Not in our library10.4161/psb.21124
237.
Wu J. Lightner J. Warwick N. Browse J. (1997 ). Low-temperature damage and subsequent recovery of fab1 mutant Arabidopsis exposed to 2 degrees C. Plant Physiol. 113 347–356.
Not in our library10.1104/pp.113.2.347
238.
Wu J. Zhang Y. Yin L. Qu J. Lu J. (2014 ). Linkage of cold acclimation and disease resistance through plant-pathogen interaction pathway in Vitis amurensis grapevine. Funct. Integr. Genomics 14 741–755.
Not in our library10.1007/s10142-014-0392-1
239.
Xing Y. Jia W. Zhang J. (2008 ). AtMKK1 mediates ABA induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J. 54 440–451.
Not in our library10.1111/j.1365-313x.2008.03433.x
240.
Xiong F. S. Mueller E. C. Day T. A. (2000 ). Photosynthetic and respiratory acclimation and growth response of Antarctic vascular plants to contrasting temperature regimes. Am. J. Bot. 87 700–710.
Not in our library10.2307/2656856
241.
Yabuuchi H. O’Brien J. S. (1968 ). Positional distribution of fatty acids in glycerophosphatides of bovine gray matter. J. Lipid Res. 9 65–67.
Not in our library
242.
Yadav D. K. Pospíšil P. (2012 ). Role of chloride ion in hydroxyl radical production in photosystem II under heat stress: electron paramagnetic resonance spin-trapping study. J. Bioenerg. Biomembr. 44 365–372.
Not in our library10.1007/s10863-012-9433-4
243.
Yamamoto Y. Aminaka R. Yoshioka M. Khatoon M. Komayama K. Takenaka D. (2008 ). Quality control of photosystem II: impact of light and heat stresses. Photosynth. Res. 98 589–608.
Not in our library10.1007/s11120-008-9372-4
244.
Yamamoto Y. Kai S. Ohnishi A. Tsumura N. Ishikawa T. Hori H. (2014 ). Quality control of PSII: behavior of PSII in the highly crowded grana thylakoids under excessive light. Plant Cell Physiol. 55 1206–1215.
Not in our library10.1093/pcp/pcu043
245.
Yamashita A. Nijo N. Pospísil P. Morita N. Takenaka D. Aminaka R. (2008 ). Quality control of photosystem II: reactive oxygen species are responsible for the damage to photosystem II under moderate heat stress. J. Biol. Chem. 283 28380–28391.
Not in our library10.1074/jbc.m710465200
246.
Yamauchi Y. Furutera A. Seki K. Toyoda Y. Tanaka K. Sugimoto Y. (2008 ). Malondialdehyde generated from peroxidized linolenic acid causes protein modification in heat-stressed plants. Plant Physiol. Biochem. 46 786–793.
Not in our library10.1016/j.plaphy.2008.04.018
247.
Yamauchi Y. Sugimoto Y. (2010 ). Effect of protein modification by malondialdehyde on the interaction between the oxygen-evolving complex 33 kDa protein and photosystem II core proteins. Planta 231 1077–1088.
Not in our library10.1007/s00425-010-1112-2
248.
Yao J. Liu B. Qin F. (2011 ). Modular thermal sensors in temperature-gated transient receptor potential (TRP) channels. Proc. Natl. Acad. Sci. U.S.A. 108 11109–11114.
Not in our library10.1073/pnas.1105196108
249.
Yoshioka M. Uchida S. Mori H. Komayama K. Ohira S. Morita N. (2006 ). Quality control of photosystem II. Cleavage of reaction center D1 protein in spinach thylakoids by FtsH protease under moderate heat stress. J. Biol. Chem. 281 21660–21669.
Not in our library10.1074/jbc.m602896200
250.
Yu C. Y. Nguyen V. C. Chuang L. Kanehara K. (2018 ). Membrane glycerolipid equilibrium under endoplasmic reticulum stress in Arabidopsis thaliana. Biochem. Biophys. Res. Commun. 500 103–109.
Not in our library10.1016/j.bbrc.2018.03.025
251.
Downregulation of chloroplast RPS1 negatively modulates nuclear heat-responsive expression of HsfA2 and its target genes in Arabidopsis. · 2012
Not checked
252.
Zhang L. Kondo H. Kamikubo H. Kataoka M. Sakamoto W. (2016 ). VIPP1 has a disordered C-terminal tail necessary for protecting photosynthetic membranes against stress. Plant Physiol. 171 1983–1995.
Not in our library10.1104/pp.16.00532
253.
Zhang M. Barg R. Yin M. Gueta-Dahan Y. Leikin-Frenkel A. Salts Y. (2005 ). Modulated fatty acid desaturation via overexpression of two distinct omega-3 desaturases differentially alters tolerance to various abiotic stresses in transgenic tobacco cells and plants. Plant J. 44 361–371.
Not in our library10.1111/j.1365-313x.2005.02536.x
254.
Zhang Z. W. Zhang G. C. Zhu F. Zhang D. W. Yuan S. (2015 ). The roles of tetrapyrroles in plastid retrograde signaling and tolerance to environmental stresses. Planta 242 1263–1276.
Not in our library10.1007/s00425-015-2384-3
255.
Zheng S. Z. Liu Y. L. Li B. Shang Z. L. Zhou R. G. Sun D. Y. (2012 ). Phosphoinositide-specific phospholipase C9 is involved in the thermotolerance of Arabidopsis. Plant J. 69 689–700.
Not in our library10.1111/j.1365-313x.2011.04823.x
256.
Zhong L. Zhou W. Wang H. Ding S. Lu Q. Wen X. (2013 ). Chloroplast small heat shock protein HSP21 interacts with plastid nucleoid protein pTAC5 and is essential for chloroplast development in Arabidopsis under heat stress. Plant Cell 25 2925–2943.
Not in our library10.1105/tpc.113.111229
257.
Zhou J. Xia X. J. Zhou Y. H. Shi K. Chen Z. Yu J. Q. (2014 ). RBOH1- dependent H2O2 production and subsequent activation of MPK1/2 play an important role in acclimation-induced cross-tolerance in tomato. J. Exp. Bot. 65 595–607.
Not in our library10.1093/jxb/ert404
258.
Zhu J. K. (2016 ). Abiotic stress signaling and responses in plants. Cell 167 313–324.
Not in our library10.1016/j.cell.2016.08.029
259.
Zong X. J. Li D. P. Gu L. K. Li D. Q. Liu L. X. Hu X. L. (2009 ). Abscisic acid and hydrogen peroxide induce a novel maize group C MAP kinase gene, ZmMPK7, which is responsible for the removal of reactive oxygen species. Planta 229 485–495.
Not in our library10.1007/s00425-008-0848-4
260.
Zrobek-Sokolnik A. (2012 ). “Temperature stress and responses of plants,” in Environmental Adaptations and Stress Tolerance of Plants in the Era of Climate Change, eds Ahmad P. Prasad M. N. V. (New York, NY: Springer Press), 113–134.
Not in our library10.1007/978-1-4614-0815-4_5

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