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. 2025 Jan 2;5(1):1. doi: 10.1007/s44154-024-00195-5

Mechanisms for cell survival during abiotic stress: focusing on plasma membrane

Xiao Su 1,2, Lijuan Yao 1,2, Xuechen Wang 1,2, Yuan Zhang 1,2, Guifang Zhang 1,2,✉, Xiaojuan Li 1,2,✉
PMCID: PMC11693639

Abstract

Plants are continually challenged by abiotic stressors, including drought, salinity, and extreme temperatures, which can adversely affect their growth and development. The plasma membrane, acting as a pivotal interface between the cell and its environment, is particularly susceptible to such stresses. This review focuses on current understanding of how abiotic stresses affect plasma membrane integrity in plants. The review also explores the critical roles of plasma membrane proteins and lipids under stress conditions, highlighting signal transduction pathways that the plasma membrane initiates to mitigate abiotic stress. By consolidating these findings, this review provides a comprehensive overview that is pivotal for advancing the development of stress-tolerant plant varieties. The insights gained from this synthesis are expected to contribute significantly to the enhancement of plant resilience in the face of environmental challenges.

Keywords: Abiotic stress, Plasma membrane integrity, Signal transduction, Stress tolerance

Introduction

The growth, development, and geographic distribution of plants, as well as the quality and yield of crops, are profoundly influenced by their growing environment. Among various environmental factors, abiotic stress significantly affects agricultural productivity, plant growth and development (Li et al. 2019; Miyazaki et al. 2021; Pei et al. 2022; Islam et al. 2024; Liang et al. 2024). Adverse abiotic conditions, such as high temperature, low temperature, drought, and salt, pose substantial challenges to plant health (Zhang et al. 2020; Li et al. 2022a, b; Kopecká et al. 2023; Wang et al. 2024). Plants have evolved various defense mechanisms enabling them to adapt abiotic stress at both physiologically and molecularly level (Li et al. 2022a, b; Kopecká et al. 2023; Kuppusamy et al. 2023; Rui and Wang.2024; Rahman et al. 2024).

The plasma membrane (PM) serves as a crucial barrier between the cell and its surroundings, playing a pivotal role in maintaining intracellular stability and facilitating substance exchange with the external environment (Medina-Puche and Lozano-Durán. 2022). Meanwhile, the PM, which comprised predominantly of membrane proteins and lipids, acts as the primary environmental sensor in plants (Sun et al. 2022). Environmental signals are primarily detected and transduced through changes in membrane lipids and membrane proteins. Furthermore, the PM exhibits fluidity, selectivity, and other characteristics essential for the normal cellular activities. Therefore, maintaining the integrity of the PM is crucial for the proper functioning of plant PM.

Under abiotic stress conditions, the PM is highly susceptible to damage. Drought-induced osmotic stress affects the structural integrity of the PM, altering its permeability and thereby increasing the pressure on plants to survive in water-deficient environments (Munnik et al. 2021; Ozturk et al. 2021). Salt stress also induces osmotic stress on the PM. Additionally, salt stress introduces ion injury to the PM, and the combined effects of osmotic stress and ion injury slowly destruction the structural integrity of the PM, further intensifying the survival challenges for plants in high-salinity environments (Arif et al. 2020; Zhou et al. 2024). Low temperatures stress causes physiological drought by inhibiting plant water uptake and transport, leading to drought-like symptoms despite the presence of soil moisture. Low temperatures stress also impairs plant growth and development, causing strength loss and surface lesions, as well as biochemical changes at the enzymatic level alter the viscosity, permeability, and fluidity of PM (Almadanim et al. 2018; Ruiz-Lopez et al. 2021). High temperatures also present significant challenges to the integrity of PM and should not be disregarded, which are exacerbated by the heightened fluidity of membrane lipids, the process of lipid peroxidation, and the degradation of proteins across various metabolic pathways. (Burgos et al. 2011; Bourgine and Guihur 2021; Ruiz-Lopez et al. 2021; Zhao et al. 2021a, b; Sharma et al. 2023).

To withstand environmental stresses, plants have developed intricated regulatory networks that allow them to react and adjust to their surroundings. This involves the stress adaptation model of plants under abiotic stress (Gusain et al. 2023). In this model, the PM is regarded as a dynamic system, which does not passively endure stress but can sense stress signals (Nguyen et al. 2018). In this review, we summarize recent researches on the damages on the PM under abiotic stress and the mechanism of PM response to abiotic stress, providing references for future research on plant responses to abiotic stress.

Plasma membrane integrity is important for plant

The PM is not only a basic physical barrier shielding the cell interior from the external environment, but also a selective barrier that facilitates a multitude of precisely regulated cell functions, including signal transduction, cellular communication (Amorim-Silva et al. 2019; Jaillais and Ott 2019; Fichman et al. 2022). Composed of lipids and proteins, PM is equipped with a variety of receptors and sensors that can recognize changes in factors such as temperature, humidity, and the presence of various molecules (Jiang et al. 2019; Zhao et al. 2019). Upon sensing these environmental cues, the PM initiates a cascade of events by converting the perceived changes into specific signals. These signals are then relayed through a network of signaling pathways within the cell. These pathways involve the activation of enzymes, generation of second messengers, and modulation of gene expression, ultimately leading to a coordinated cellular response that aligns with the new environmental conditions. This intricate process ensures that the plant can adapt and survive in a dynamic and ever-changing world (Zandalinas and Mittler 2021).

Proteins at the cell surface, which use the PM as a platform, are essential for a variety of cellular functions and biological processes (Gouguet et al. 2021). As one of the most important organelles in the cell, the PM is responsible for a variety of physiological processes that rely on its structural integrity. When PM integrity is compromised, transmembrane transport may also be impacted. For example, obstacles to material transport will affect the absorption of nutrients and the discharge of waste by plant cells, thus interfering with metabolic processes (Li et al. 2023). In the long term, damage to the PM integrity lead to electrolyte leakage even cell death, results in dwarfing, shrinkage of the leaves, as well as reduced biomass yield (Kim et al. 2016; Petrov et al. 2018; Medina-Puche et al. 2020; Ruiz-Lopez et al. 2021; Kopecká et al. 2023; Baena et al. 2024). Therefore, in order to enhance the capacity to environmental changes, it is imperative that the integrity of the PM be preserved and repaired.

The damage to plasma membrane under the different abiotic stresses

Growing evidence indicate that stress-induced damages on integrity of membrane systems, are closely associated with disrupting cellular homeostasis and function (Yamazaki et al. 2008; Li and Kim 2022). In this section, we provide a detailed summary of the damages inflicted on the PM by various stress factors, evaluating the physiological and biochemical impacts on plant health and resilience.

Low temperatures stress

Plant growth, development, distribution, and seasonal behavior are all significantly influenced by temperature. Both excessive low and high temperatures are detrimental to the of plants (Adhikari et al. 2021; Ding et al. 2020). Freezing injury, occurring below 0 °C and cold stress, encompassing temperatures ranging from 0 to 20 °C, are common abiotic stresses to plant cells. These stresses impact the PM through distinct mechanisms. Freezing injury is characterized by the formation of ice crystals, which lead to direct mechanical damage and cell dehydration. This ultimately results in structural alterations in the PM, increased electrolyte leakage, and overall membrane damage (Schapire et al. 2008; Yamazaki et al. 2008). Whereas, cold stress primarily affects membrane fluidity and the functionality of membrane proteins, without the formation of ice crystals (Sangwan et al. 2002). Research has shown that the lipid content of PM can alter in response to cold stress. When plants are exposed to cold stress, PM retains an excessive amount of diacylglycerol, reducing fluidity of PM and then cause rupture of PM (Ruiz-Lopez et al. 2021). Low temperature was also reported to reduce PM fluidity of pineapple. The integrity of PM lost, according to the ultrastructure observation of pineapple cells undergo low-temperature storage (Zhang et al. 2011). Moreover, phosphatidylinositol (PI) levels dropped, PM ATPase activity decreased, and PM phosphatidylic acid (PA) levels rose (Zhou et al. 2014). It is postulated that low temperature may affect PM ATPase activity and decrease PM integrity by changing the lipid composition of the PM, based on the effect of PA level on PM ATPase activity(Zhou et al. 2014; Ponce-Pineda et al. 2021). Both freezing and cold stress can lead to severe PM damage, including expansion-induced lysis (EIL) and loss of osmotic responsiveness (LOR), underscoring the critical need to maintain PM integrity under such environmental challenges (Uemura et al. 2003).

High temperature stress

High temperatures have emerged as a primary challenge in global crop production (Larkindale and Vierling 2008; Saidi et al. 2009; Zhai et al. 2017; Djanaguiraman et al. 2018a, b; Bheemanahalli et al. 2019; Haider et al. 2021). Transmission electron microscopy (TEM) analysis of wheat cells ultrastructure showed damage to the PM under high temperature stress (Djanaguiraman et al. 2018a, b). Although the exact cause of this damage remains unclear, the research indicated that the PM was negatively impacted by the high temperatures. Lipid peroxidation, protein denaturation, and imbalance of membrane fluidity may all induce PM damage. Plant peroxidase activity increases in response to high temperature stress, damaging membrane lipids and associated proteins (Li and Kim 2022). Lipid peroxidation within PM is often gauged by the level of malondialdehyde (MDA), a substance that poses a threat to cellular health when its concentration increases (Hu et al. 2023). Moreover, elevated membrane fluidity, resulting from increased lipid unsaturation levels and stigmasterol content, can lead to PM rupture. All these factors collectively contribute to the observed PM damage (Djanaguiraman et al. 2018a, b; Raja et al. 2020; Hu et al. 2023).

Drought stress

Drought stress significantly reduces the relative water content and transpiration rate in plants, leading to the oxidation of unsaturated fatty acids and protein degradation. It also damages the semipermeability and integrity of the PM, resulting in cytosolic electrolyte leakage (Kocheva et al. 2009; Petrov et al. 2018). The reduction of turgor pressure and the alteration in plant cell PM tension caused by excessive osmotic stress could be the source of the damage to PM induced by drought (Kocheva et al. 2009, 2014; Shi et al. 2023; Guo et al. 2024; Zhang et al. 2024). Under drought conditions, the phospholipid degradation in winter wheat leaves were primarily phosphatidylcholine (PC), phosphatidylethanolamine (PE), and phosphatidylglycerol (PG), with PC experiencing the greatest degradation. Membrane electrolyte leakage significantly increased after these phospholipids decreased, indicating that severe phospholipid degradation precedes membrane integrity loss. Degradation of PM phospholipids may contribute to the loss of the PM integrity (Wang et al. 2020). In addition, drought can induce oxidative stress in plants (Fu et al. 2023). Drought-induced oxidative stress damages plant membrane systems through ROS. Plants have developed defense mechanisms against oxidative stress and plant drought stress tolerance is directly correlated with the effectiveness of their enzymatic scavenging mechanisms. Suppressing the expression of ldi-miR396b upregulated LdPMaT1 during drought stress in lily, enhancing ROS scavenge capacity and drought resilience (Fu et al. 2023). Collectively, drought stress damages the plant PM through hypertonic osmotic stress, lipid oxidation, and phospholipid degradation, as well as oxidative stress. Plants counter these challenges using enzymatic scavenging mechanisms localized at the PM.

Salt stress

Soil salinity, characterized by the predominance of soluble ions in the soil, negatively impacts on photosynthetic capacity, transpiration rate, enzymatic activities, cellular homeostasis, metabolism, ion transport, and plant morphology (van Zelm et al. 2020; Zhao et al. 2021a, b; He et al. 2022; Joshi et al. 2022; Liu et al. 2022; Morita et al. 2023; Xiao and Zhou 2023; Zhou et al. 2024). For example, salt stress led to the synthesis and accumulation of ROS, which interferes activity of enzyme localized on PM and alters the membrane permeability (Arif et al. 2020; Joshi et al. 2022; Ma et al. 2023).

de Freitas et al. reported that salt stress damages the PM of sorghum cells within seven days, leading to electrolyte leakage (de Freitas et al. 2019). Furthermore, research in rice also shows that salt stress can cause electrolyte leakage in plant leaves, indicating PM damage in rice leaf cells under salt tolerance (Roy et al. 2022). In summary, salt stress can damage the PM through various mechanisms, including osmotic stress, ion toxicity, ROS outbreaks, and membrane protein denaturation (Guo et al. 2019; Lv et al. 2021).

Function of plasma membrane in response to stresses

In response to the challenge of abiotic stress, the PM has evolved complex mechanisms to enhance stress tolerance and maintain cellular integrity. Lipid composition and contents maybe remodeled, and numerous PM proteins (Table 1) functioned as sensors to transmit precise signals to the cell’s interior (Manasa et al. 2022; Ramazam et al. 2023).

Table 1.

Membrane proteins involved in abiotic stress response

Proteins Category Types involved in abiotic stress responses Description References
CRLK1 Kinases and phosphatases Low temperature Activating the MAPKs (Yang et al. 2010)
CRPK1 Low temperature Phosphorylating target proteins to enhance cold tolerance (Liu et al. 2017)
COLD1 Receptor proteins Low temperature Sensing the cold signal and interacting with RGA1 to enhance Ca2+ influx (Ma et al. 2015)
SOS1 Transporter proteins High salt Maintaining ion balance and reducing Na + toxicity (Lu et al. 2023)
MCAs Ion channels proteins Low temperature Drought Promoting Ca2+ influx (Yoshimura et al. 2021)
AKT1 Salt Facilitating K + uptake and osmotic adjustment (Li et al. 2023)
MSL10 Drought Sensing osmotic stress and enhance Ca2+ influx (Basu et al. 2020)
OSCA1.2 Drought Enhancing to osmotic adjustment and drought resistance by regulating Ca2+ influx (Han et al. 2024)
CNGCs High temperature Promoting Ca2+ influx (Niu et al. 2020)
RbohD Hydrolases High temperature Elevating ROS to activate the MAPKs (Rivas et al. 2024)
PIP2 Aquaporins Salt Regulating osmotic water flow (Baena et al. 2024)
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Plasma membrane lipid remodeling in stress resistance

Lipid diversity and homeostasis are important for PM to respond against external pressures. By increasing the synthesis of specific lipids or reducing their degradation, plants adjust the fluidity and phase transition temperature of the membrane to adapt to varying environmental conditions (Bakht et al. 2006; Tarazona et al. 2015; Tshabuse et al. 2018; Guo et al. 2019; Sharma et al. 2023). For instance, in winter wheat leaves under drought conditions, the contents of PC, PE, and PG in the PMs exhibited a very similar trends relative to stress duration. Membrane lipid fluidity is positively correlated with Double Bond Index (DBI), which serves as an important metric for assessing membrane integrity. After 8 h of drought stress, the DBI of PC increased significantly and persisted for several days. Whereas, the DBI of PI, PG, and Phosphatidylserine (PS) significantly decreased at different times within the first 1–4 days after drought stress, while no notable alteration was observed in the DBI of PE. These findings indicated that PC was the primary phospholipid that responds to water stress by increasing unsaturation (Wang et al. 2020). Changes of the composition and degree of desaturation of fatty acids were also detected under drought stress. It was reported that drought stress led to a significant decrease in the contents of C16:1, C16:3 and C18:3 fatty acids and an increase in the levels of C16:0 and C18:2 fatty acids (Gigon et al. 2004; Liu et al.2019; Yin et al. 2024).

A thorough examination of lipidomics and transcriptomics revealed alterations in lipid metabolism in the root membrane of maize seedlings under low temperature stress. Cold stress from low temperatures caused an increase in phosphatidic acid (PA) and PE levels, alongside a decrease in PC content. A reduction in PC levels can compromise membrane integrity under stress, while an increase in PA content helps to mitigate cold stress damage in maize seedlings (Zhao et al. 2021, b). Another research demonstrated the significance of PC in plant stress resistance by showing that it serves as the primary substrate for the activation of phospholipase Dα (PLDα) induced by freezing. PLDα activity might contribute to freeze-induced lipid hydrolysis and damage the integrity of the PM. During freezing, increased lipolysis activity of PLDα altered the composition of membrane lipids, with the wild PC of type level decreasing significantly more than those in PLDα-deficient plants (pldα). This corresponds with increased cold tolerance in pldα (Welti et al. 2002). Diacylglycerol (DAG) was also detected to be large accumulate in plant PMs under low temperature stress, which reduces the fluidity of membrane and increased the risk of membrane rupture. To preserve the PM integrity and fluidity, the PM protein SYT1 can bind DAG on the membrane and transfer it to the ER using its special SMP structure (Ruiz-Lopez et al. 2021; Qian et al. 2022).

In response to heat stress, heat-tolerant soybean genotype DS25-1 showed significantly lower expression levels of FAD3A and FAD3B genes compared to heat-susceptible genotype DT97-4290. This led to a decrease in the content of polyunsaturated linolenic acid (18:3), which consequently led to a decrease in the level of lipid unsaturated fats. The decrease in18:3 in DS25-1 aids in the preservation membrane function and high-temperature tolerance (Narayanan et al. 2020). A similar adaptation mechanism to heat stress in peanuts is reported by lipidomic analysis in peanut (Arachis hypogaea L.) anthers. Under heat stress, lipid unsaturation levels according to the amount of 18:3 fatty acid was reduced through downregulate FAD3 expression. (Zoong Lwe ZS et al. 2020). In TrFQR1-transgenic white clover (Trifolium repens), the heat resistance is enhanced through an increase in lipid saturation and the ratio of PC to PE, which improve PM integrity and stability under heat stress conditions (Cheng et al. 2023).

Lipid remodeling in response to salt stress varies among different plant species (Yu et al. 2021). For instance, in the halophyte ice plant (Mesembryanthemum crystallinum L.), an increase in non-bilayer forming and negatively charged lipids (PE and PS) was observed in the PM under salt stress (Guo et al. 2019, 2022). Positive correlations between the PS level and plant salt tolerance were also reported in Salicornia europaea L. The increased PS level minimizes membrane damage, reduces PM depolarization, and maintains K+/Na+ balance, thus enhances salt tolerance of the transgenic lines (Lv et al. 2021). In Barley (Hordeum vulgare), PCs play crucial roles in the concentration-dependent adaptive reactions to salt stress(Sarabia et al. 2020). Growing number of highly unsaturated PC species improved membrane fluidity, which may protect PM integrity and enhance resistance to salt stress.(Sarabia et al. 2020).

Plants respond to stressors partly through changes in lipid content. The stability of plant membrane lipids contribute to stress resistance, and lipids also participate in the transduction of abiotic stress signals as signaling molecules. Thus, exploring the physiological role of plant lipids under stress has significantly theoretical and practical implications.

Key roles of membrane-localized proteins in perception and response to abiotic stress

Plants constantly sense changes of the environment and integrate this information to develop a coordinated, whole-plant response strategy. This adaptive capability is enabled by a complex network of molecular, chemical, and physical elements that collaborate within a sophisticated communication framework (Gusain et al. 2023; Xiao and Zhou 2023; Ruan et al. 2024). To mitigate the effects of abiotic stressors and ensure survival under adverse conditions, plants have evolved a plethora of molecular mechanisms designed for detection, response, and adaptation to unfavorable environmental scenarios.

PM plays a crucial role in heat sensing, containing calcium channels, such as cyclic nucleotide-gated channels (CNGCs), that respond to temperature changes by mediating Ca2+ entry and triggering heat-shock proteins (HSPs) accumulation (Fig. 1) (Bourgine and Guihur 2021; Guihur et al. 2022). Moreover, during heat stress, the Phospholipase C Isoform 3 (PLC3) and PLC9, which take phosphoinositides (PI) as substrate, are quickly activated in the initial stage of a heat stress, leading to cytosolic Ca2+ accumulates. The hydrolysis of phosphatidylinositol 4,5-bisphosphate by PLC3 and PLC9 results in the formation of DAG and inositol-1,4,5-trisphosphate (IP3), respectively. This process activates the release of Ca2+ from intracellular stores, triggering a signaling cascade involving kinases and calmodulins (CaMs) (Fig. 1) (Gao et al. 2014; Ren et al. 2017; Abdelrahman et al. 2020; Kumar et al. 2020). Subsequently, heat shock transcription factors are activated to enhance plant heat tolerance. (Ul Haq et al. 2019).

Fig. 1.

Fig. 1

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Diagram illustrating the signal transduction pathways that high temperture stress activates. Heat stress affects membrane fluidity and stability, causing Ca2+ to enter the cytosol through the opening of cyclic nucleotide-gated channels (CNGCs) on the PM. This influx of Ca2+ triggers a specific signaling cascade where Ca2+ binding to CNGC-bound CaMs activates kinases. These kinases then phosphorylate and activate heat shock transcription factors (HSFs). Additionally, membrane instability can initiate lipid signaling through phospholipase D (PLD) and phosphatidylinositol phosphate kinase (PIPK) enzymes. Phospholipase C (PLC) hydrolyzes phosphatidylinositol 4,5-bisphosphate (PIP2) to produce inositol trisphosphate (IP3), which interacts with IP3 receptors (IP3R) to release intracellular Ca2+ from the endoplasmic reticulum (ER), further initiating a signaling cascade. Cytosolic Ca2+ binds to calcium-dependent protein kinases (CDPKs) and CaM3, activating HSFs in the cytosol and enhancing reactive oxygen species (ROS) production through the phosphorylation of NADPH oxidase, specifically the RBOHD. Eventually, HSFs translocate into the nucleus and bind to heat shock elements (HSEs) to promote the expression of heat shock protein (HSP) related genes

In response to low-temperature stress, the PM serves as the primary sensor, rigidifying and decreasing in fluidity (Wei et al. 2021). The CHILLINGTOLERANCE DIVERGENCE 1 (COLD1) protein interacts with G-protein α subunit 1 (RGA1) to facilitate Ca2+ influx after sensing the cold signal (Ma et al. 2015). Ca2+ flowes by the activated Ca2+-permeable mechanosensitive channel (MCAs) (Gusain et al. 2023; Mori et al. 2018). These Ca2+ signals, detected by variety of Ca2+ sensors like CaMs and calcineurin B-like (CBLs), trigger the ICE-CBF-COR signaling pathway via the MAPKs cascade reaction, preserving PM integrity and enhancing cold tolerance ultimately (Fig. 2) (Adhikari et al. 2022; Hwarari et al. 2022; Gusain et al. 2023; Khan et al. 2023). Moreover, cold-activated PM protein CRPK1 modulates the CBF-dependent cold signaling by phosphorylating 14–3-3 proteins, promoting CBF proteins destabilization in the nucleus (Fig. 2) (Liu et al. 2017).

Fig. 2.

Fig. 2

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Diagram illustrating the signal transduction pathways that low temperture activates. During cold stress, the PM hardens and Ca2+ enters through mechanosensitive channels (MCAs). COLD1 detects the cold signal and interacts with RGA1 to enhance Ca2+ flow. To transmit cold signals, Ca2+/calmodulin (CaM) upregulates the kinase activity of calcium/calmodulin-regulated receptor-like kinase 1 (CRLK1) and facilitates its interaction with mitogen-activated protein kinase kinase 1 (MEKK1), activating the MAPKs. Calcium levels during cold stress are regulated by calcineurin B-like proteins through the serine-threonine protein kinase CIPK. In Arabidopsis, the upregulation of CBL1 and its interaction with CIPK7 create a freezing-tolerant phenotype and induce the expression of various Cold-Regulated (COR) genes. CRPK1 phosphorylates the 14–3-3 protein in the nucleus, facilitating the regulation of CBF-dependent cold signaling. The SIZ1-dependent sumoylation of the Inducer of CBF Expression 1 (ICE1) may activate and stabilize the protein, promoting CBF expression. The induction of CBF genes leads to the activation of C-repeat Binding Factors (CBFs), which target COR genes, contributing to increased freezing tolerance

When exposed to salt stress, plants rapidly detect excess Na+, triggering a sodium stress response cascade. Glycosyl Inositol Phosphorylceramide (GIPC), which is essential components of the outer lipid bilayer, may sensing extracellular salt by directly binding Na+. The sodium-bound GIPC interacts with the calcium channel, then activate Ca2+ channel to increases cytoplasmic Ca2+ concentration (Fig. 3) (Jiang et al. 2019). As a crucial secondary messenger, Ca2+ initiates a calcium signaling cascade to modulate plant-wide adaptive responses (Manishankar et al. 2018). The SOS pathway, pivotal for salt tolerance, ensures Na+ /K+ homeostasis within plant cells. Phosphatidic acid (PA) maintains Na+/K+ homeostasis by promoting Na+ efflux and K+ influx, regulating SOS pathway and Arabidopsis K+ transporter 1 (AKT1) under salt stress. PA binds to SOS2, a key component of the SOS pathway, and when under salt stress, this promotes the activity and PM localization of SOS2, which activates of the Na+/H+ reverse transporter SOS1 and to promote Na+ efflux. SOS2 also increases the phosphorylation of SOS3-like calcium-binding protein 8 (SCaBP8) in response to salt stress, reducing the inhibition of AKT1 and increasing K+ influx (Fig. 3) (Fuglsang and Palmgren 2021; Li et al. 2023). This signaling system allows plants to minimize Na+-induced PM damage and maintain integrity (Xiao and Zhou 2023).

Fig. 3.

Fig. 3

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Diagram illustrating the signal transduction pathways that high salt stress activates. The SOS pathway plays a critical role in maintaining ionic homeostasis and may interact with other signaling networks to regulate plant salt tolerance more precisely. During salt stress, glycosyl inositol phosphoryl ceramide (GIPC), a type of negatively charged membrane lipid, likely contributes to salt sensing by directly binding to Na+. This interaction activates a calcium channel, leading to a Ca2+ influx that triggers an adaptive reaction to increased salt concentrations. The Ca2+-binding protein SOS3 activates the protein SOS2, which subsequently activates SOS1 to expel Na+ from the cell. For a precise plant salt stress response, intracellular calcium signals are effectively detected by Ca2+ sensors like SCaBP8. SCaBP8 interacts with SOS2 to inhibit the transport of K+ through AKT1 channels. Salinity reduces the amount of AHA1 binding to the SNARE complex but increases PIP2 binding to SYP132, facilitating the redistribution of PIP2 from the PM to endosomal membranes

Although the specific signaling molecules enabling plants to detect water availability changes remain unclear, several studies suggest that changes in external osmolarity directly affect PM mechanics, such as tension and subcellular volumes. Drought leads to osmotic and ionic imbalance, triggering a complex network of osmotic stress signal transduction pathways (Fig. 4) (Mukarram et al. 2021; Gorgues et al. 2022; Kim et al. 2024). Drought leads to osmotic and ionic imbalance, triggering a complex network of osmotic stress signal transduction pathways. Membrane proteins, such as RLKs, histone kinases, and integrin-like proteins, serve as osmotic stress sensors. Arabidopsis histidine kinase 1 (ATHK1/AHK1) at the PM enhances drought tolerance and activates drought response genes, such as the synthesis of proline and sucrose (Fig. 4) (Tran et al. 2007). Although unclear if a MAPK pathway is involved, calcium channels likely perceive osmotic stress in drought responses. The MCA channel, the mechanosensitive (MS) channel of Ca2+, is directly triggered by membrane tension to facilitate the flow of Ca2+ and the use of Ca2+ as a second messenger in signal transduction. (Fig. 4) (Yoshimura et al. 2021). In Arabidopsis, mechanosensitive channel like MscSlike 10 (MSL10) and Reduced hyperosmolality-induced [Ca2+]i increase 1.2 (OSCA1.2), detect osmotic stress signals, promoting Ca2+ influx to encourage drought-resistant gene expression, maintain PM integrity, and confer drought resistance (Fig. 4) (Yuan et al. 2014; Murthy et al. 2018; Basu et al. 2020; Han et al. 2024). These findings suggest that plants perceive osmotic stress through various proteins on the PM and that precise information is transmitted to all plant tissues through delivering Ca2+.

Fig. 4.

Fig. 4

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Diagram illustrating the signal transduction pathways that drought stress activates. Under drought conditions, plants experience osmotic stress, which is detected by calcium channels known as MCAs, OSCA1.2 and MSL10. These channels initiate the influx of calcium ions, which then function as secondary messengers to relay signals. ATHK1/AHK1, acting as an osmotic stress signal-sensing protein, subsequently activates MAPKs upon detecting these osmotic stress signals

Conclusion

Plants face numerous abiotic challenges, such as temperature extremes (both high and low), drought, and high salt stress, when exposed to the environment. Although these stresses often do not lead to immediate plant death, they can adversely affect overall plant growth. Several studies have shown that abiotic stress can compromise the integrity of PM. PM repair after damage are crucial for cells maintaining function. However, the underlying mechanisms remain to be further illustrated in plant cells. This review examines the recent findings on how abiotic stress affects PM integrity and how plants respond to such damage. Our goal is to enhance understanding of the relationship between abiotic stress and PM integrity, to explore novel mechanisms by which plants can resist abiotic damage, and to provide a valuable resource for crop breeding research in this review. By shedding light on these interactions, we aim to assist future researchers in developing strategies to improve plant resilience against environmental challenges.

Acknowledgements

We apologize for the omission of any pertinent original reference due to space limitations.

Authors’ contributions

Xiao Su wrote the manuscript. Lijuan Yao, Xuechen Wang and Yuan Zhang made corrections for the manuscript. Guifang Zhang revised the manuscript critically. Xiaojuan Li contributed to design the review and to make the final corrections for the manuscript. All authors read and approved the final manuscript under the supervision of Xiaojuan Li before the submission.

Funding

This research was supported by the National Natural Science Foundation of China (32470434, 32471821,91954202), the National Key R&D Program of China during the 14th Five-year Plan Period (2023YFD2200101), the Third Xinjiang Scientific Expedition Program (Grant No.2022xjkk1200).

Data availability

All data generated or analyzed during this study are included in this published article.

Declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

All participants have consented to this submission to the journal.

Competing interests

The authors declare that they have no competing interests.

Footnotes

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Guifang Zhang, Email: gfzhang2019@bjfu.edu.cn.

Xiaojuan Li, Email: lixj@bjfu.edu.cn.

References

  1. Abdelrahman M, Ishii T, El-Sayed M, Tran LP (2020) Heat sensing and lipid reprograming as a signaling switch for heat stress responses in wheat. Plant Cell Physiol 61(8):1399–1407. 10.1093/pcp/pcaa072 [DOI] [PubMed] [Google Scholar]
  2. Adhikari L, Makaju SO, Lindstrom OM, Missaoui AM (2021) Mapping freezing tolerance QTL in alfalfa: based on indoor phenotyping. BMC Plant Biol 21(1):403. 10.1186/s12870-021-03182-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Adhikari L, Baral R, Paudel D, Min D, Makaju SO, Poudel HP, Acharya JP, Missaoui AM (2022) Cold stress in plants: strategies to improve cold tolerance in forage species. Plant Stress 4:2667–3064. 10.1016/j.stress.2022.100081 [Google Scholar]
  4. Almadanim MC, Gonçalves NM, Rosa MTG, Alexandre BM, Cordeiro AM, Rodrigues M, Saibo NJM, Soares CM, Romão CV, Oliveira MM (1865) Abreu IA (2018) The rice cold-responsive calcium-dependent protein kinase OsCPK17 is regulated by alternative splicing and post-translational modifications. Biochim Biophys Acta Mol Cell Res 2:231–246. 10.1016/j.bbamcr.2017.10.010 [DOI] [PubMed] [Google Scholar]
  5. Amorim-Silva V, García-Moreno Á, Castillo AG, Lakhssassi N, Esteban Del Valle A, Pérez-Sancho J, Li Y, Posé D, Pérez-Rodriguez J, Lin J, Valpuesta V, Borsani O, Zipfel C, Macho AP, Botella MA (2019) TTL proteins scaffold brassinosteroid signaling components at the plasma membrane to optimize signal transduction in Arabidopsis. Plant Cell 31(8):1807–1828. 10.1105/tpc.19.00150 [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Arif Y, Singh P, Siddiqui H, Bajguz A, Hayat S (2020) Salinity induced physiological and biochemical changes in plants: an omic approach towards salt stress tolerance. Plant Physiol Biochem 156:64–77. 10.1016/j.plaphy.2020.08.042 [DOI] [PubMed] [Google Scholar]
  7. Baena G, Xia L, Waghmare S, Yu Z, Guo Y, Blatt MR, Zhang B, Karnik R (2024) Arabidopsis SNARE SYP132 impacts on PIP2:1 trafficking and function in salinity stress. Plant J 118(4):1036–1053. 10.1111/tpj.16649 [DOI] [PubMed] [Google Scholar]
  8. Bakht J, Bano A, Dominy P (2006) The role of abscisic acid and low temperature in chickpea (Cicer arietinum) cold tolerance. II. Effects on plasma membrane structure and function. J Exp Bot 57(14):3707–3715. 10.1093/jxb/erl120 [DOI] [PubMed] [Google Scholar]
  9. Basu D, Shoots JM, Haswell ES (2020) Interactions between the N- and C-termini of the mechanosensitive ion channel AtMSL10 are consistent with a three-step mechanism for activation. J Exp Bot 71(14):4020–4032. 10.1093/jxb/eraa192 [DOI] [PubMed] [Google Scholar]
  10. Bheemanahalli R, Sunoj VSJ, Saripalli G, Prasad PVV, Balyan HS, Gupta PK, Grant N, Gill KS, Jagadish SVK (2019) Quantifying the impact of heat stress on pollen germination, seed set, and grain filling in spring wheat. Crop Sci 59(2):684–696. 10.2135/cropsci2018.05.0292 [Google Scholar]
  11. Bourgine B, Guihur A (2021) Heat shock signaling in land plants: from plasma membrane sensing to the transcription of small heat shock proteins. Front Plant Sci 12:710801. 10.3389/fpls.2021.710801 [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Burgos A, Szymanski J, Seiwert B, Degenkolbe T, Hannah MA, Giavalisco P, Willmitzer L (2011) Analysis of short-term changes in the Arabidopsis thaliana glycerolipidome in response to temperature and light. Plant J 66(4):656–668. 10.1111/j.1365-313X.2011.04531.x [DOI] [PubMed] [Google Scholar]
  13. Cheng B, Zhou M, Tang T, Hassan MJ, Zhou J, Tan M, Li Z, Peng Y (2023) A Trifolium repens flavodoxin-like quinone reductase 1 (TrFQR1) improves plant adaptability to high temperature associated with oxidative homeostasis and lipids remodeling. Plant J 115(2):369–385. 10.1111/tpj.16230 [DOI] [PubMed] [Google Scholar]
  14. de Freitas PAF, de Carvalho HH, Costa JH, Miranda RS, Saraiva KDDC, de Oliveira FDB, Coelho DG, Prisco JT, Gomes-Filho E (2019) Salt acclimation in sorghum plants by exogenous proline: physiological and biochemical changes and regulation of proline metabolism. Plant Cell Rep 38(3):403–416. 10.1007/s00299-019-02382-5 [DOI] [PubMed] [Google Scholar]
  15. Ding Y, Shi Y, Yang S (2020) Molecular regulation of plant responses to environmental temperatures. Mol Plant 13(4):544–564. 10.1016/j.molp.2020.02.004 [DOI] [PubMed] [Google Scholar]
  16. Djanaguiraman M, Boyle DL, Welti R, Jagadish S, Prasad P (2018a) Decreased photosynthetic rate under high temperature in wheat is due to lipid desaturation, oxidation, acylation, and damage of organelles. BMC Plant Biol 18(1):55. 10.1186/s12870-018-1263-z [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Djanaguiraman M, Perumal R, Ciampitti IA, Gupta SK, Prasad PVV (2018b) Quantifying pearl millet response to high temperature stress: thresholds, sensitive stages, genetic variability and relative sensitivity of pollen and pistil. Plant Cell Environ 41(5):993–1007. 10.1111/pce.12931 [DOI] [PubMed] [Google Scholar]
  18. Fichman Y, Zandalinas SI, Peck S, Luan S, Mittler R (2022) HPCA1 is required for systemic reactive oxygen species and calcium cell-to-cell signaling and plant acclimation to stress. Plant Cell 34(11):4453–4471. 10.1093/plcell/koac241 [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Fu L, Zhang J, Li M, Wang C, Chen Y, Fan X, Sun H (2023) Ldi-miR396-LDPMaT1 enhances reactive oxygen species scavenging capacity and promotes drought tolerance in Lilium distichum Nakai autotetraploids. Plant Cell Environ 47(8):2733–2748. 10.1111/pce.14783 [DOI] [PubMed] [Google Scholar]
  20. Fuglsang AT, Palmgren M (2021) Proton and calcium pumping P-type ATPases and their regulation of plant responses to the environment. Plant Physiol 187(4):1856–1875. 10.1093/plphys/kiab330 [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Gao K, Liu Y, Li B, Zhou R, Sun D, Zheng S (2014) Arabidopsis thaliana phosphoinositide-specific phospholipase C isoform 3 (AtPLC3) and AtPLC9 have an additive effect on thermotolerance. Plant Cell Physiol 55(11):1873–1883. 10.1093/pcp/pcu116 [DOI] [PubMed] [Google Scholar]
  22. Gigon A, Matos AR, Laffray D, Zuily-Fodil Y, Pham-Thi AT (2004) Effect of drought stress on lipid metabolism in the leaves of Arabidopsis thaliana (ecotype columbia). Ann Bot 94(3):345–351. 10.1093/aob/mch150 [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Gorgues L, Li X, Maurel C, Martinière A, Nacry P (2022) Root osmotic sensing from local perception to systemic responses. Stress Biol 2(1):36. 10.1007/s44154-022-00054-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gouguet P, Gronnier J, Legrand A, Perraki A, Jolivet MD, Deroubaix AF, German-Retana S, Boudsocq M, Habenstein B, Mongrand S, Germain V (2021) Connecting the dots: from nanodomains to physiological functions of REMORINs. Plant Physiol 185(3):632–649. 10.1093/plphys/kiaa063 [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Guihur A, Rebeaud ME, Goloubinoff P (2022) How do plants feel the heat and survive? Trends Biochem Sci 47(10):824–838. 10.1016/j.tibs.2022.05.004 [DOI] [PubMed] [Google Scholar]
  26. Guo Q, Liu L, Barkla BJ (2019) Membrane lipid remodeling in response to salinity. Int J Mol Sci 20(17):4264. 10.3390/ijms20174264 [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Guo Q, Liu L, Rupasinghe TWT, Roessner U, Barkla BJ (2022) Salt stress alters membrane lipid content and lipid biosynthesis pathways in the plasma membrane and tonoplast. Plant Physiol 189(2):805–826. 10.1093/plphys/kiac123 [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Guo Z, Wang S, Zhang F, Xiang D, Yang J, Li D, Bai B, Dai M, Luo J, Xiong L (2024) Common and specific genetic basis of metabolite-mediated drought responses in rice. Stress Biol 4(1):6. 10.1007/s44154-024-00150-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Gusain S, Joshi S, Joshi R (2023) Sensing, signalling, and regulatory mechanism of cold-stress tolerance in plants. Plant Physiol Biochem 197:107646. 10.1016/j.plaphy.2023.107646 [DOI] [PubMed] [Google Scholar]
  30. Han Y, Zhou Z, Jin R, Dai F, Ge Y, Ju X, Ma X, He S, Yuan L, Wang Y, Yang W, Yue X, Chen Z, Sun Y, Corry B, Cox CD, Zhang Y (2024) Mechanical activation opens a lipid-lined pore in OSCA ion channels. Nature 628(8009):910–918. 10.1038/s41586-024-07256-9 [DOI] [PubMed] [Google Scholar]
  31. He Y, Chen W, Tan J, Luo X, Zhou Y, Gong X, Yao J, Zhuang C, Jiang D (2022) Rice CENTRORADIALIS 2 regulates seed germination and salt tolerance via ABA-mediated pathway. Theor Appl Genet 135(12):4245–4259. 10.1007/s00122-022-04215-8 [DOI] [PubMed] [Google Scholar]
  32. Hu H, Jia Y, Hao Z, Ma G, Xie Y, Wang C, Ma D (2023) Lipidomics-based insights into the physiological mechanism of wheat in response to heat stress. Plant Physiol Biochem 205:108190. 10.1016/j.plaphy.2023.108190 [DOI] [PubMed] [Google Scholar]
  33. Haider S, Iqbal J, Naseer S, Yaseen T, Shaukat M, Bibi H, Ahmad Y, Daud H, Abbasi NL, Mahmood T (2021) Molecular mechanisms of plant tolerance to heat stress: current landscape and future perspectives. Plant Cell Rep 40(12):2247–2271. 10.1007/s00299-021-02696-3 [DOI] [PubMed] [Google Scholar]
  34. Hwarari D, Guan Y, Ahmad B, Movahedi A, Min T, Hao Z, Lu Y, Chen J, Yang L (2022) ICE-CBF-COR signaling cascade and its regulation in plants responding to cold stress. Int J Mol Sci 23(3):1549. 10.3390/ijms23031549 [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Islam SNU, Kouser S, Hassan P, Asgher M, Shah AA, Khan NA (2024) Gamma-aminobutyric acid interactions with phytohormones and its role in modulating abiotic and biotic stress in plants. Stress Biol 4(1):36. 10.1007/s44154-024-00180-y [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Jaillais Y, Ott T (2019) The nanoscale organization of the plasma membrane and its importance in signaling: a proteolipid perspective1. Plant Physiol 182(4):1682–1696. 10.1104/pp.19.01349 [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Jiang Z, Zhou X, Tao M, Yuan F, Liu L, Wu F, Wu X, Xiang Y, Niu Y, Liu F, Li C, Ye R, Byeon B, Xue Y, Zhao H, Wang HN, Crawford BM, Johnson DM, Hu C, Pei C, Zhou W, Swift GB, Zhang H, Vo-Dinh T, Hu Z, Siedow JN, Pei ZM (2019) Plant cell-surface GIPC sphingolipids sense salt to trigger Ca2+ influx. Nature 572(7769):341–346. 10.1038/s41586-019-1449-z [DOI] [PubMed] [Google Scholar]
  38. Joshi S, Nath J, Singh AK, Pareek A, Joshi R (2022) Ion transporters and their regulatory signal transduction mechanisms for salinity tolerance in plants. Physiol Plant 174(3):e13702. 10.1111/ppl.13702 [DOI] [PubMed] [Google Scholar]
  39. Kim H, Kwon H, Kim S, Kim MK, Botella MA, Yun HS, Kwon C (2016) Synaptotagmin 1 negatively controls the two distinct immune secretory pathways to powdery mildew fungi in Arabidopsis. Plant Cell Physiol 57(6):1133–1141. 10.1093/pcp/pcw061 [DOI] [PubMed] [Google Scholar]
  40. Kim J, Kidokoro S, Yamaguchi-Shinozaki K, Shinozaki K (2024) Regulatory networks in plant responses to drought and cold stress. Plant Physiol 195(1):170–189. 10.1093/plphys/kiae105 [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Kocheva K, Kartseva T, Landjeva S, Georgiev G (2009) Physiological response of wheat seedlings to mild and severe osmotic stress. Cereal Res Commun 37(2):199–208. 10.1556/CRC.37.2009.2.6 [Google Scholar]
  42. Kocheva K, Nenova V, Karceva T, Petrov P, Georgiev GI, Börner A, Landjeva S (2014) Changes in water status, membrane stability and antioxidant capacity of wheat seedlings carrying different Rht-B1 dwarfing alleles under drought stress. J Agro Crop Sci 200(2):83–91. 10.1111/jac.12047 [Google Scholar]
  43. Kopecká R, Kameniarová M, černý M, Brzobohatý B, Novák J, (2023) Abiotic stress in crop production. Int J Mol Sci 24(7):6603. 10.3390/ijms24076603 [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Kumar RR, Arora K, Goswami S, Sakhare A, Singh B, Chinnusamy V, Praveen S (2020) MAPK enzymes: a ROS activated signaling sensors involved in modulating heat stress response, tolerance and grain stability of wheat under heat stress. Biotech 10(9):380. 10.1007/s13205-020-02377-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Kuppusamy A, Alagarswamy S, Karuppusami KM, Maduraimuthu D, Natesan S, Ramalingam K, Muniyappan U, Subramanian M, Kanagarajan S (2023) Melatonin enhances the photosynthesis and antioxidant enzyme activities of mung bean under drought and high-temperature stress conditions. Plants (Basel) 12(13):2535. 10.3390/plants12132535 [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Khan FS, Goher F, Paulsmeyer MN, Hu C, Zhang J (2023) Calcium (Ca2+) sensors and MYC2 are crucial players during jasmonates-mediated abiotic stress tolerance in plants. Plant Biol 25(7):1025–1034. 10.1111/plb.13560 [DOI] [PubMed] [Google Scholar]
  47. Larkindale J, Vierling E (2008) Core genome responses involved in acclimation to high temperature. Plant Physiol 146(2):323–324. 10.1104/pp.107.112060 [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Li J, Shen L, Han X, He G, Fan W, Li Y, Yang S, Zhang Z, Yang Y, Jin W, Wang Y, Zhang W, Guo Y (2023) Phosphatidic acid-regulated SOS2 controls sodium and potassium homeostasis in Arabidopsis under salt stress. EMBO J 42(8):e112401. 10.15252/embj.2022112401 [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Li M, Kim C (2022) Chloroplast ROS and stress signaling. Plant Commun 3(1):100264. 10.1016/j.xplc.2021.100264 [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Li J, Yu D, Qanmber G, Lu L, Wang L, Zheng L, Liu Z, Wu H, Liu X, Chen Q, Li F, Yang Z (2019) Ghklcr1, a kinesin light chain-related gene, induces drought-stress sensitivity in Arabidopsis. Sci China Life Sci 62(1):63–75. 10.1007/s11427-018-9307-y [DOI] [PubMed] [Google Scholar]
  51. Li Z, Cheng B, Wu X, Zhang Y, Feng G, Peng Y (2022a) Spermine-mediated metabolic homeostasis improves growth and stress tolerance in creeping bentgrass (Agrostis stolonifera) under water or high-temperature stress. Front Plant Sci 13:944358. 10.3389/fpls.2022.944358 [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Li X, Gao Y, Wu W, Chen L, Wang Y (2022b) Two calcium-dependent protein kinases enhance maize drought tolerance by activating anion channel ZmSLAC1 in guard cells. Plant Biotechnol J 20(1):143–157. 10.1111/pbi.13701 [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Liang X, Li J, Yang Y, Jiang C, Guo Y (2024) Designing salt stress-resilient crops: Current progress and future challenges. J Integr Plant Biol 66(3):303–329. 10.1111/jipb.13599 [DOI] [PubMed] [Google Scholar]
  54. Liu Z, Jia Y, Ding Y, Shi Y, Li Z, Guo Y, Gong Z, Yang S (2017) Plasma membrane CRPK1-mediated phosphorylation of 14–3-3 proteins induces their nuclear import to fine-tune CBF signaling during cold response. Mol Cell 66(1):117–128. 10.1016/j.molcel.2017.02.016 [DOI] [PubMed] [Google Scholar]
  55. Liu X, Ma D, Zhang Z, Wang S, Du S, Deng X, Yin L (2019) Plant lipid remodeling in response to abiotic stresses. Environ Exp Bot 169:174–184. 10.1016/j.envexpbot.2019.06.005 [Google Scholar]
  56. Liu G, Jiang W, Tian L, Fu Y, Tan L, Zhu Z, Sun C, Liu F (2022) Polyamine oxidase 3 is involved in salt tolerance at the germination stage in rice. J Genet Genomics 49(5):458–468. 10.1016/j.jgg.2022.01.007 [DOI] [PubMed] [Google Scholar]
  57. Lu K, Song R, Guo J, Zhang Y, Zuo J, Chen H et al (2023) CycC1;1–WRKY75 complex-mediated transcriptional regulation of SOS1 controls salt stress tolerance in Arabidopsis. Plant Cell 35(7):2570–2591. 10.1093/plcell/koad105 [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Lv S, Tai F, Guo J, Jiang P, Lin K, Wang D, Zhang X, Li Y (2021) Phosphatidylserine synthase from Salicornia europaea is involved in plant salt tolerance by regulating plasma membrane stability. Plant Cell Physiol 62(1):66–79. 10.1093/pcp/pcaa141 [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Ma L, Li X, Zhang J, Yi D, Li F, Wen H, Liu W, Wang X (2023) MsWRKY33 increases alfalfa (Medicago sativa L.) salt stress tolerance through altering the ROS scavenger via activating MsERF5 transcription. Plant Cell Environ 46(12):3887–3901. 10.1111/pce.14703 [DOI] [PubMed] [Google Scholar]
  60. Ma Y, Dai X, Xu Y, Luo W, Zheng X, Zeng D, Pan Y, Lin X, Liu H, Zhang D, Xiao J, Guo X, Xu S, Niu Y, Jin J, Zhang H, Xu X, Li L, Wang W, Qian Q, Ge S, Chong K (2015) COLD1 confers chilling tolerance in rice. Cell 160(6):1209–1221. 10.1016/j.cell.2015.01.046 [DOI] [PubMed] [Google Scholar]
  61. Manishankar P, Wang N, Köster P, Alatar AA, Kudla J (2018) Calcium signaling during salt stress and in the regulation of ion homeostasis. J Exp Bot 69(17):4215–4226. 10.1093/jxb/ery201 [DOI] [PubMed] [Google Scholar]
  62. Morita S, Tamba N, Shibasaka M, Sasano S, Kadoike T, Urase Y, Maruyama M, Fukuoka A, Yanai J, Masumura T, Ogihara Y, Satoh S, Tanaka K, Katsuhara M, Nakayama H (2023) In planta evidence that the HAK transporter OsHAK2 is involved in Na+ transport in rice. Biosci Biotechnol Biochem 87(5):482–490. 10.1093/bbb/zbad020 [DOI] [PubMed] [Google Scholar]
  63. Medina-Puche L, Tan H, Dogra V, Wu M, Rosas-Diaz T, Wang L, Ding X, Zhang D, Fu X, Kim C, Lozano-Duran R (2020) A defense pathway linking plasma membrane and chloroplasts and co-opted by pathogens. Cell 182(5):1109–1124. 10.1016/j.cell.2020.07.020 [DOI] [PubMed] [Google Scholar]
  64. Medina-Puche L, Lozano-Durán R (2022) Plasma membrane-to-organelle communication in plant stress signaling. Curr Opin Plant Biol 69:102269. 10.1016/j.pbi.2022.102269 [DOI] [PubMed] [Google Scholar]
  65. Miyazaki K, Ohkubo Y, Yasui H, Tashiro R, Suzuki R (2021) Overexpression of rice OsLEA5 relieves the deterioration in seed quality caused by high-temperature stress. Plant Biotechnol (Tokyo) 38(3):367–371. 10.5511/plantbiotechnology.21.0603a [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Mori K, Renhu N, Naito M, Nakamura A, Shiba H, Yamamoto T, Suzaki T, Iida H, Miura K (2018) Ca2+-permeable mechanosensitive channels MCA1 and MCA2 mediate cold-induced cytosolic Ca2+ increase and cold tolerance in Arabidopsis. Sci Rep 8(1):55010.1038/s41598-017-17483-y/s41598-017-17483-y [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Mukarram M, Choudhary S, Kurjak D, Petek A, Khan MMA (2021) Drought: sensing, signalling, effects and tolerance in higher plants. Physiol Plant 172(2):1291–1300. 10.1111/ppl.13423 [DOI] [PubMed] [Google Scholar]
  68. Munnik T, Mongrand S, Zársky V, Blatt M (2021) Dynamic membranes—the indispensable platform for plant growth, signaling, and development. Plant Physiol 185(3):547–549. 10.1093/plphys/kiaa107 [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Murthy SE, Dubin AE, Whitwam T, Jojoa-Cruz S, Cahalan SM, Mousavi SAR, Ward AB, Patapoutian A (2018) OSCA/TMEM63 are an evolutionarily conserved family of mechanically activated ion channels. Elife 1(7):e41844. 10.7554/eLife.41844 [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Manasa SL, Panigrahy M, Panigrahi KCS, Rout GR (2022) Overview of cold stress regulation in plants. Bot Rev 88(3):359–387. 10.1007/s12229-021-09267-x [Google Scholar]
  71. Narayanan S, Zoong-Lwe ZS, Gandhi N, Welti R, Fallen B, Smith JR, Rustgi S (2020) Comparative lipidomic analysis reveals heat stress responses of two soybean genotypes differing in temperature sensitivity. Plants (Basel) 9(4):457. 10.3390/plants9040457 [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Nguyen HC, Lin KH, Ho SL, Chiang CM, Yang CM (2018) Enhancing the abiotic stress tolerance of plants: from chemical treatment to biotechnological approaches. Physiol Plant 164(4):452–466. 10.1111/ppl.12812 [DOI] [PubMed] [Google Scholar]
  73. Niu W, Han X, Wei S, Shang Z, Wang J, Yang D et al (2020) Arabidopsis cyclic nucleotide-gated channel 6 is negatively modulated by multiple calmodulin isoforms during heat shock. J Exp Bot 71(1):90–104. 10.1093/jxb/erz445 [DOI] [PubMed] [Google Scholar]
  74. Ozturk M, Turkyilmaz Unal B, García Caparrós P, Khursheed A, Gul A, Hasanuzzaman M (2021) Osmoregulation and its actions during the drought stress in plants. Physiol Plant 172(2):1321–1335. 10.1111/ppl.13297 [DOI] [PubMed] [Google Scholar]
  75. Petrov P, Petrova A, Dimitrov I, Tashev T, Olsovska K, Brestic M, Misheva S (2018) Relationships between leaf morpho-anatomy, water status and cell membrane stability in leaves of wheat seedlings subjected to severe soil drought. J Agron Crop Sci 204(3):219–227. 10.1111/jac.12255 [Google Scholar]
  76. Pei D, Hua D, Deng J, Wang Z, Song C, Wang Y, Wang Y, Qi J, Kollist H, Yang S, Guo Y, Gong Z (2022) Phosphorylation of the plasma membrane H+-ATPase AHA2 by BAK1 is required for ABA-induced stomatal closure in Arabidopsis. Plant Cell 34(7):2708–2729. 10.1093/plcell/koac106 [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Ponce-Pineda IG, Carmona-Salazar L, Saucedo-García M, Cano-Ramírez D, Morales-Cedillo F, Peña-Moral A, Guevara-García ÁA, Sánchez-Nieto S, Gavilanes-Ruíz M (2021) MPK6 kinase regulates plasma membrane H+-ATPase activity in cold acclimation. Int J Mol Sci 22(12):6338. 10.3390/ijms22126338 [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Qian T, Li C, Liu F, Xu K, Wan C, Liu Y, Yu H (2022) Arabidopsis synaptotagmin 1 mediates lipid transport in a lipid composition-dependent manner. Traffic 23(6):346–356. 10.1111/tra.12844 [DOI] [PubMed] [Google Scholar]
  79. Raja V, Qadir SU, Alyemeni MN, Ahmad P (2020) Impact of drought and heat stress individually and in combination on physio-biochemical parameters, antioxidant responses, and gene expression in Solanum lycopersicum. 3 Biotech 10(5):208. 10.1007/s13205-020-02206-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Ramazan S, Jan N, John R (2023) Comparative protein analysis of two maize genotypes with contrasting tolerance to low temperature. BMC Plant Biol 23(1):183. 10.1186/s12870-023-04198-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Rahman MM, Keya SS, Sahu A, Gupta A, Dhingra A, Tran LP, Mostofa MG (2024) Acetic acid: a cheap but chief metabolic regulator for abiotic stress tolerance in plants. Stress Biol 4(1):34. 10.1007/s44154-024-00167-9 [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. 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(10):e1162368. 10.1080/15592324.2016.1162368 [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Rivas FJM, Fernie AR, Aarabi F (2024) Roles and regulation of the RBOHD enzyme in initiating ROS-mediated systemic signaling during biotic and abiotic stress. Plant Stress 11:100327. 10.1016/j.stress.2023.100327
  84. Roy S, Mishra M, Kaur G, Singh S, Rawat N, Singh P, Singla-Pareek SL, Pareek A (2022) OsCyp2-p, an auxin-responsive cyclophilin, regulates Ca2+ calmodulin interaction for an ion-mediated stress response in rice. Physiol Plant 174(2):e13631. 10.1111/ppl.13631 [DOI] [PubMed] [Google Scholar]
  85. Ruan M, Zhao H, Wen Y, Chen H, He F, Hou X, Song X, Jiang H, Ruan YL, Wu L (2024) The complex transcriptional regulation of heat stress response in maize. Stress Biol 4(1):24. 10.1007/s44154-024-00165-x [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Ruiz-Lopez N, Pérez-Sancho J, Del Valle AE, Haslam RP, Vanneste S, Catalá R, Perea-Resa C, Damme DV, García-Hernández S, Albert A, Vallarino J, Lin J, Friml J, Macho AP, Salinas J, Rosado A, Napier JA, Amorim-Silva V, Botella MA (2021) Synaptotagmins at the endoplasmic reticulum-plasma membrane contact sites maintain diacylglycerol homeostasis during abiotic stress. Plant Cell 33(7):2431–2453. 10.1093/plcell/koab122 [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Rui L, Wang W (2024) Fortify the defense frontline: MAPKs phosphorylate receptor-like cytoplasmic kinase to maintain plant resistance in soybean. Stress Biol 4(1):22. 10.1007/s44154-024-00164-y [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Saidi Y, Finka A, Muriset M, Bromberg Z, Weiss YG, Maathuis FJ, Goloubinoff P (2009) The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell 21(9):2829–2843. 10.1105/tpc.108.065318 [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Sangwan V, Orvar BL, Beyerly J, Hirt H, Dhindsa RS (2002) Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J 31(5):629–638. 10.1046/j.1365-313x.2002.01384.x [DOI] [PubMed] [Google Scholar]
  90. Sarabia LD, Boughton BA, Rupasinghe T, Callahan DL, Hill CB, Roessner U (2020) Comparative spatial lipidomics analysis reveals cellular lipid remodelling in different developmental zones of barley roots in response to salinity. Plant Cell Environ 43(2):327–343. 10.1111/pce.13653 [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Schapire AL, Voigt B, Jasik J, Rosado A, Lopez-Cobollo R, Menzel D, Salinas J, Mancuso S, Valpuesta V, Baluska F, Botella MA (2008) Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell 20(12):3374–3388. 10.1105/tpc.108.063859 [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Sharma P, Lakra N, Goyal A, Ahlawat YK, Zaid A, Siddique KHM (2023) Drought and heat stress mediated activation of lipid signaling in plants: a critical review. Front Plant Sci 14:1216835. 10.3389/fpls.2023.1216835 [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. Shi Z, Zhou M, Song W, Liu Y, Wang R, Wang Y, Zhang R, Zhao J, Ren W (2023) Trash to treasure: lactate and protein lactylation in maize root impacts response to drought. Sci China Life Sci 66(8):1903–1914. 10.1007/s11427-023-2361-1 [DOI] [PubMed] [Google Scholar]
  94. Sun Y, Wang Y, Zhang X, Chen Z, Xia Y, Wang L, Sun Y, Zhang M, Xiao Y, Han Z, Wang Y, Chai J (2022) Plant receptor-like protein activation by a microbial glycoside hydrolase. Nature 610(7931):335–342. 10.1038/s41586-022-05214-x [DOI] [PubMed] [Google Scholar]
  95. Tran LS, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci U S A 104(51):20623–20628. 10.1073/pnas.0706547105 [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Tshabuse F, Farrant JM, Humbert L, Moura D, Rainteau D, Espinasse C, Idrissi A, Merlier F, Acket S, Rafudeen MS, Thomasset B, Ruelland E (2018) Glycerolipid analysis during desiccation and recovery of the resurrection plant Xerophyta humilis (Bak) Dur and Schinz. Plant Cell Environ 41(3):533–547. 10.1111/pce.13063 [DOI] [PubMed] [Google Scholar]
  97. Tarazona P, Feussner K, Feussner I (2015) An enhanced plant lipidomics method based on multiplexed liquid chromatography–mass spectrometry reveals additional insights into cold- and drought-induced membrane remodeling. Plant J 84(3):621–633. 10.1111/tpj.13013 [DOI] [PubMed] [Google Scholar]
  98. Uemura M, Warren G, Steponkus PL (2003) Freezing sensitivity in the sfr4 mutant of Arabidopsis is due to low sugar content and is manifested by loss of osmotic responsiveness. Plant Physiol 131(4):1800–1807. 10.1104/pp.102.013227 [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Ul Haq S, Khan A, Ali M, Khattak AM, Gai WX, Zhang HX, Wei AM, Gong ZH (2019) Heat shock proteins: dynamic biomolecules to counter plant biotic and abiotic stresses. Int J Mol Sci 20(21):5321. 10.3390/ijms20215321 [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. van Zelm E, Zhang Y, Testerink C (2020) Salt tolerance mechanisms of plants. Annu Rev Plant Biol 71(1):403–433. 10.1146/annurev-arplant-050718-100005 [DOI] [PubMed] [Google Scholar]
  101. Wang Y, Zhang X, Huang G, Feng F, Liu X, Guo R, Gu F, Zhong X, Mei X (2020) Dynamic changes in membrane lipid composition of leaves of winter wheat seedlings in response to PEG-induced water stress. BMC Plant Biol 20(1):84. 10.1186/s12870-020-2257-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
  102. Wei X, Liu S, Sun C, Xie G, Wang L (2021) Convergence and divergence: signal perception and transduction mechanisms of cold stress in Arabidopsis and rice. Plants 10(9):1864. 10.3390/plants10091864 [DOI] [PMC free article] [PubMed] [Google Scholar]
  103. Welti R, Li W, Li M, Sang Y, Biesiada H, Zhou HE, Rajashekar CB, Williams TD, Wang X (2002) Profiling membrane lipids in plant stress responses. Role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis. J Biol Chem 277(35):31994–32002. 10.1074/jbc.M205375200 [DOI] [PubMed] [Google Scholar]
  104. Wang L, Wang Y, Yin P, Jiang C, Zhang M (2024) ZmHAK17 encodes a Na+-selective transporter that promotes maize seed germination under salt conditions. New Crops 1:2949–9526. 10.1016/j.ncrops.2024.100024 [Google Scholar]
  105. Xiao F, Zhou H (2023) Plant salt response: perception, signaling, and tolerance. Front Plant Sci 13:1053699. 10.3389/fpls.2022.1053699 [DOI] [PMC free article] [PubMed] [Google Scholar]
  106. Yamazaki T, Kawamura Y, Minami A, Uemura M (2008) Calcium-dependent freezing tolerance in Arabidopsis involves membrane resealing via synaptotagmin SYT1. Plant Cell 20(12):3389–3404. 10.1105/tpc.108.062679 [DOI] [PMC free article] [PubMed] [Google Scholar]
  107. Yang T, Chaudhuri S, Yang L, Du L, Poovaiah BW (2010) A calcium/calmodulin-regulated member of the receptor-like kinase family confers cold tolerance in plants. J Biol Chem 285(10):7119–7126. 10.1074/jbc.M109.035659 [DOI] [PMC free article] [PubMed] [Google Scholar]
  108. Yoshimura K, Iida K, Iida H (2021) MCAs in Arabidopsis are Ca2+-permeable mechanosensitive channels inherently sensitive to membrane tension. Nat Commun 12(1):6074. 10.1038/s41467-021-26363-z [DOI] [PMC free article] [PubMed] [Google Scholar]
  109. Yuan F, Yang H, Xue Y, Kong D, Ye R, Li C, Zhang J, Theprungsirikul L, Shrift T, Krichilsky B, Johnson DM, Swift GB, He Y, Siedow JN, Pei ZM (2014) OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514(7522):367–371. 10.1038/nature13593 [DOI] [PubMed] [Google Scholar]
  110. Yin L, Xu J, Zhang L, Liu D, Zhang C, Liu T, Wang S, Deng X (2024) Altered fatty acid composition confers improved drought acclimation in maize. Plant Physiol Bioch 206:108274. 10.1016/j.plaphy.2023.108274 [DOI] [PubMed] [Google Scholar]
  111. Yu L, Zhou C, Fan J, Shanklin J, Xu C (2021) Mechanisms and functions of membrane lipid remodeling in plants. Plant J 107(1):37–53. 10.1111/tpj.15273 [DOI] [PubMed] [Google Scholar]
  112. Zandalinas SI, Mittler R (2021) Vascular and nonvascular transmission of systemic reactive oxygen signals during wounding and heat stress. Plant Physiol 186(3):1721–1733. 10.1093/plphys/kiab157 [DOI] [PMC free article] [PubMed] [Google Scholar]
  113. Zhai Y, Wang H, Liang M, Lu M (2017) Both silencing- and over-expression of pepper CaATG8c gene compromise plant tolerance to heat and salt stress. Environ Exp Bot 141(10–18):0098–8472. 10.1016/j.envexpbot.2017.06.009 [Google Scholar]
  114. Zhao JL, Zhang LQ, Liu N, Xu SL, Yue ZL, Zhang LL, Deng ZP, Burlingame AL, Sun DY, Wang ZY, Sun Y, Zhang SW (2019) Mutual regulation of receptor-like kinase SIT1 and B’κ-PP2A shapes the early response of rice to salt stress. Plant Cell 31(9):2131–2151. 10.1105/tpc.18.00706 [DOI] [PMC free article] [PubMed] [Google Scholar]
  115. Zhao S, Zhang Q, Liu M, Zhou H, Ma C, Wang P (2021a) Regulation of plant responses to salt stress. Int J Mol Sci 22(9):4609. 10.3390/ijms22094609 [DOI] [PMC free article] [PubMed] [Google Scholar]
  116. Zhao X, Wei Y, Zhang J, Yang L, Liu X, Zhang H, Shao W, He L, Li Z, Zhang Y, Xu J (2021b) Membrane lipids’ metabolism and transcriptional regulation in maize roots under cold stress. Front Plant Sci 12:639132. 10.3389/fpls.2021.639132 [DOI] [PMC free article] [PubMed] [Google Scholar]
  117. Zhang T, Bai L, Guo Y (2024) SCAB1 coordinates sequential Ca2+ and ABA signals during osmotic stress induced stomatal closure in Arabidopsis. Sci China Life Sci 67(1):1–18. 10.1007/s11427-023-2480-4 [DOI] [PubMed] [Google Scholar]
  118. Zhang W, Liu J, Zhang Y, Qiu J, Li Y, Zheng B, Hu F, Dai S, Huang X (2020) A high-quality genome sequence of alkaligrass provides insights into halophyte stress tolerance. Sci China Life Sci 63(9):1269–1282. 10.1007/s11427-020-1662-x [DOI] [PubMed] [Google Scholar]
  119. Zhang S, Jiang H, Peng S, Korpelainen H, Li C (2011) Sex-related differences in morphological, physiological, and ultrastructural responses of populus cathayana to chilling. J Exp Bot 62(2):675–686. 10.1093/jxb/erq306 [DOI] [PMC free article] [PubMed] [Google Scholar]
  120. Zoong Lwe ZS, Welti R, Anco D, Naveed S, Rustgi S, Narayanan S (2020) Heat stress elicits remodeling in the anther lipidome of peanut. Sci Rep 10(1):22163. 10.1038/s41598-020-78695-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. Zhou Y, Pan X, Qu H, Underhill SJR (2014) Low temperature alters plasma membrane lipid composition and atpase activity of pineapple fruit during blackheart development. J Bioenerg Biomembr 46(1):59–69. 10.1007/s10863-013-9538-4 [DOI] [PubMed] [Google Scholar]
  122. Zhou H, Shi H, Yang Y, Feng X, Chen X, Xiao F, Lin H, Guo Y (2024) Insights into plant salt stress signaling and tolerance. J Genet Genomics 51(1):16–34. 10.1016/j.jgg.2023.08.007 [DOI] [PubMed] [Google Scholar]

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