Sustainable Crop Productivity and Quality under Climate Change: Responses of Crop Plants to Climate Change

By Bing Liu

Sustainable Crop Productivity and Quality under Climate Change: Responses of Crop Plants to Climate Change explores the physiological, biochemical, and molecular basis of the responses of major crop plants to a range of climate change scenarios. From the development of climate-resilient crop varieties which lead to enhanced crop productivity and quality to better utilization of natural resources to ensure food security through modern breeding techniques, it presents insights into improving yield while securing the environment.

Understanding the impact of climate on crop quality and production is a key challenge of crop science. Predicted increases in climate variability necessitate crop varieties with intrinsic resilience to cooccurring abiotic stresses such as heat, drought, and flooding in a future climate of elevated CO2. This book presents a much-needed mechanistic understanding of the interactions between multiple stress responses of plants that is required to identify and take advantage of acclimation traits in major crop species as a prerequisite for securing robust yield and good quality.

This book is an excellent reference for crop and agricultural scientists, plant scientists, and researchers working on crop plant ecophysiology/stress physiology and future crop production.

• Includes breeding strategies for developing climate-resilient crop varieties
• Presents a comprehensive overview of the current challenges, approaches, and best practices
• Authored by frontline researchers and experts who work at the fields of climate change impacts on crop productivity

• Language: English
• Publisher: Academic Press
• Release date: Jun 7, 2022
• ISBN: 9780323854504

Book preview

Chapter 1

Crop exposure to cold stress: responses in physiological, biochemical and molecular levels

Junhong Guo¹,², Shengqun Liu¹, Xiangnan Li¹,² and Fulai Liu³,    ¹Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, P. R. China,    ²College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, P. R. China,    ³Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Taastrup, Denmark

Abstract

Climate change triggers and exacerbates more extreme weather events, such as cold stress, drought stress, and heat stress. Among these abiotic stresses, cold stress is one of the major environmental stresses that limits the growth and development of crops and decreases crop productivity. Higher plants respond to cold stress at different levels including physiological modifications, changes in concentrations of metabolites, and genes expression, such as CBFs and CORs. To cope with cold stress, plants have evolved a series of mechanisms that allow them to adapt to cold stress at the physiological, biochemical, and molecular levels. To date, much progress has been achieved in cold sensing and signaling transduction, as a responses to cold stress. In the present chapter, we summarize the recent research progress on the main physiological, biochemical, and molecular mechanisms of crops under cold stress.

Keywords

Cold stress; signal transduction; physiological and biochemical; molecular mechanism; priming

1.1 Introduction

Global climate change triggers and exacerbates more extreme weather events (Field et al., 2014), such as water stress and temperature stress, which adversely affect crop growth and productivity. Extreme temperature occurs more and more frequently over the past few decades, especially low temperature (IPCC, 2014). As one of the most common abiotic stresses, low temperature stress limits crop growth and productivity by causing various damages, including modifications of the morphophysiological, changes the process of biochemical and molecular (Ding, Shi, et al., 2019; Kaplan et al., 2004; Shinozaki et al., 2003; Yadav., 2010). Cold stress occurring at temperature sensitive stages in the life cycle of crops, especially in the reproductive stages, can determine crop yield production (Thakur et al., 2010). Many studies have shown that low temperature adversely affects flower and seed development, which prolonged reproductive duration, poor pollen germination, depressed grained filling and grain yield reduction (Mitchell et al., 2016; Nayyar et al., 2005; Xu et al., 2020).

Low temperature is a major factor affecting crops geographical distribution, growth, development and productivity. Major crop species that originate from tropical and subtropical regions, such as maize and rice, are chilling sensitive, whereas temperate crops, such as wheat and barley, have evolved sophisticated mechanisms to adapt to low temperature and therefore enhanced freezing tolerance. Cold stress includes freezing stress (<0°C) and chilling stress (0°C–15°C) (Ding, Shi, et al., 2019), which can mediates a series of physiological and biochemical changes, such as alterations photosynthesis, the production of reactive oxygen species (ROS), malondialdehyde (MAD) content, sucrose concentration, the production of lipid peroxides, the accumulation of proline, electrolyte leakage, and plant endogenous hormones abscisic acid (ABA) and gibberellin (GA) changes.

To cope with cold stress, plants have evolved series of sophisticated mechanisms to adapt to low temperature. The cell membrane is the barrier that protects cells from injury as well as the primary place for sensing cold signals. Chilling tolerance is closely related to the composition, structure, and metabolic process of membrane lipids.

1.2 Cold signal perception and transduction

Plants perceive low temperature by a protein receptor on the plasma membrane. Cold stress can change membrane proteins, content of metabolites and redox state by decreasing cell membrane fluidity. Under cold stress, changes of cell membrane fluidity and membrane protein conformation are considered to be the first physical changes in the plant (Huang et al., 2014; Vaultier et al., 2006; Yamazaki et al., 2008; Zheng et al., 2014). After exposure to low temperature, the plant cytoskeleton undergoes depolymerization, which is necessary for low temperature induction of gene expression in plant cells.

Evidence indicates that calcium signaling is involved in signal transduction in response to cold stress (Almadanim et al., 2017; Zheng et al., 2014). It is well documented that cold signals transduction involves the activation of Ca²+ channels and/or Ca²+ pumps to induces Ca²+ influx (Ca²+ signature) in plant cells. Ca²+ signals triggered by cold stimulus are transmitted by Ca²+ sensors, such as calmodulins (CaMs), CaM-like proteins (CMLs), Ca²+-dependent protein kinases (CPKs/CDPKs), and calcineurin B-like proteins (CBLs) (Kim et al., 2003; Liu, Xu, et al., 2018; Weckwerth et al., 2015; Yuan et al., 2018). For example, low temperature induced a rapid and transient Ca²+ influx in whole seedlings of Arabidopsis thaliana by using the technical of Ca²+ imaging based on aequorin (Zhu et al., 2013). Plants have various cytoplasmic membrane-localized receptor proteins/kinase in the perception and transduction of developmental and environmental signals. Ma et al. identified a cold sensor, COLD1, involved in the recognition of cold stress signal in rice (Manishankar and Kudla, 2015). The authors found that COLD1 is localized in the endoplasmic reticulum and plasma membrane; also, basal Ca²+ concentration is higher in rice plants expressing the cold-tolerant COLD1 allele. And they also observed the structure changes of COLD1 proteins dependent on temperature changes (Manishankar and Kudla, 2015). Overexpression of OsCOLD1jap significantly enhanced chilling tolerance, whereas rice plants deficiency or down-regulation of OsCOLD1jap are sensitive to cold. COLD1 interact with G protein to activate the Ca²+ channel for sensing low temperature (Ma et al., 2015).

Phytochromes are plant photoreceptors that regulate photomorphogenesis. Phytochrome B (phyB) is considered the primary photoreceptor that regulates plant growth in Arabidopsis seedlings under the different conditions. Light and low temperatures are two major factors affecting plant growth and development. Recent studies suggested that phyB was considered as a thermosensor (Jung et al., 2016; Legris et al., 2016), which act as downstream of CBFs to positively freezing tolerance by regulating the expression of stress-related genes. Overexpression phyB contributes to enhanced cold tolerance, while phyB mutants exhibits a freezing-sensitive phenotype (Jiang et al., 2020).

In respond to low temperature, Ca²+ acts as a second messenger and can be recognized by calcium-binding proteins (Liu et al., 2021). The concentration of cytosolic Ca²+ can increase due to influx free Ca²+ from apoplast or vacuoles(Ding, Lei, et al., 2019), which induced the expression of CBF/COR gene in the cold signaling pathway. Calcium decoding proteins, such as CAMs, CBLs and CDPKs play vital roles as Ca²+ sensors in respond to cold stress. For example, overexpression OsCDPK7 increased rice cold tolerance, via mediating the activity of membrane channels and sugar metabolism (Almadanim et al., 2017).

1.3 Physiological and biochemical response to cold stress in crops

Among various environmental stresses, cold stress is one of the most important factors limiting crop growth, development, productivity, and distribution. Crops respond to cold stress via modifications of cell membrane structure and cold-induced proteins expression, accumulation of osmotic protective substance such as soluble sugars and proline, changes of the chloroplast ultrastructure and the photosynthetic machinery (Fig. 1.1). For instance, the accumulation of protective proteins including LATE EMBRYOGENESIS ABUNDANT (LEA) proteins, COLD SHOCK PROTEINS (CSPs) and ANTI-FREEZING PROTEINS (AFPs) during cold acclimation is important for cold tolerance in plants. LEA proteins play important roles in the regulation of cold stress, where the overexpression of AtLEA33 confers tolerance to cold stress in Escherichia coli and enhanced osmotic stress tolerance and ABA sensitivity in A. thaliana (Zhao et al., 2011).

Figure 1.1 Summary of physiological processes and molecular mechanisms of cold stress. JA, jasmonic acid; GA, gibberellins; ABA, abscisic acid; ROS, reactive oxygen species.

1.3.1 Cold stress effect cell membranes

Membranes are a primary site of cold-induced injury. Accumulated evidence has suggested that the lipid composition of plasma membrane and chloroplast envelopes were changed after exposure to low temperature, resulting in decreased content of unsaturated fatty acid of membranes, thus leading to membranes’ damage. The change in membrane composition increases the production of ROS, which leads to membrane rigidification.

1.3.2 Cold stress effect photosynthesis

Photosynthesis is a complex process, balancing the light energy absorbed by the photosystems with the energy consumed by metabolic sinks of the plant (Fu et al., 2016; Liang et al., 2007; Yamasaki et al., 2002). It is a physiological and biochemical process, converting water and carbon dioxide into biomass and oxygen by using sunlight, and is strongly affected by cold stress (Fu et al., 2016; Liang et al., 2007). Chloroplasts are the primary organelles of photosynthesis and play a vital role in solar energy capture and carbon fixation (Gan et al., 2019). The maintenance of normal chloroplast physiological functions is essential for plant growth and development (Liu, Zhou, et al., 2018). However, the functionality of chloroplasts is highly sensitive to cold stress, which inhibits photosynthesis. Low temperature damaged the ultrastructure of chloroplasts, altered pigments and the concentration of metabolites. The thylakoid membranes of chloroplasts contain photosystem complexes, which are the center of the light reactions of photosynthesis (Gan et al., 2019). Low temperature modifications of the composition and structure of the photosynthetic membrane can embrittle the photosynthetic membrane and slow enzymatic reactions. It has been reported that low temperature directly affects the structure and activity of the plant photosynthetic apparatus, by decreasing photosynthetic efficiency and producing excess ROS (Liu, Zheng, et al., 2018). Previous studies have indicated that the abundance of various proteins involved in photosynthesis, including chlorophyll a/d-binding protein and photosystem II reaction center proteins, are up-regulated or down-regulated under cold stress (Liang et al., 2007; Yamasaki et al., 2002).

1.3.3 Clod stress effect anti-oxidative system

Anti-oxidative system in plants comprising of enzymatic and non-enzymatic antioxidants, which play key roles in scavenging/detoxification of excess ROS under cold stress (Peng et al., 2015). The production of ROS such as hydrogen peroxide (H2O2) and superoxide anion (O2−) increase when plants are exposed to cold stress. Previous studies suggested that ROS are highly reactive and toxic, which lead to the oxidative destruction of cells (Dreyer and Dietz, 2018). It has been documented that anti-oxidative system such as ascorbate, reduced glutathione, superoxide dismutase (SOD) and catalase (CAT), play vital roles in plant against cold stress (Choudhury et al., 2017). Regulation of the antioxidants and activities of antioxidant enzymes is an important mechanism to combat oxidative stress (Devireddy et al., 2021). SOD plays a vital role in the detoxification of O2− into H2O2 and O2, while H2O2 was scavenged by the catalytic action of ascorbate peroxidase (APX and CAT) (Chen et al., 2006).

1.3.4 Clod stress effect hormones

Plant hormones are small molecular weight compounds, which involves plant growth and development (Devireddy et al., 2021). Also, a variety studies suggest that cold stress responses are mediated by plant hormones (Eremina et al., 2016; Hu et al., 2017; Wang et al., 2016; Zwack et al., 2016). Abscisic acid (ABA) is a key hormone involved in cold stress responses in plants. In bermudagrass, exogenous ABA application enhanced cold tolerance by maintaining cell membrane stability and altering gene expression of ABA or cold related genes, including ABF1, CBF1 and LEA (Huang et al., 2017). Ectopic overexpression the ABA receptor OSPYL3 in Arabidopsis, which improved cold tolerance (Lenka et al., 2018). In wheat, exogenous ABA could enhance cold tolerance by increasing the activities of antioxidant enzymes, including CAT, SOD, POD, APX, GR, DHAR and MDHAR (Yu et al., 2020). In sugarcane, ABA applications could improve cold resistance by decreasing the content of malondialdehyde (MDA), which contribute to alleviate cell membrane damage (Huang et al., 2014). Also, the content of proline, ABA and the ration of ABA/GA3 are increases, these play important roles in sugarcane respond to cold stress (Huang et al., 2014).

Jasmonate (JA), small molecular derivatives from lipids, plays a vital role in plant response to cold stress (Hu et al., 2013, 2017; Liu, Wang, et al., 2017; Song et al., 2014; Wang et al., 2016). After exposure to cold stress, the content of JA increased by up-regulating the expression of JA biosynthetic genes, which positively tolerated cold stress in A. annua (Liu, Wang, et al., 2017). Exogenous application of JA significantly enhanced plant freezing tolerance in Arabidopsis, while blocking endogenous JA biosynthesis and signaling decreased plants freezing stress tolerance (Hu et al., 2013). Consistent with this, the production of endogenous JA was increased after exposure to cold stress (Hu et al., 2013). In addition, several JAZ proteins, repressors of the JA signaling pathway, physically interact with ICE1 and ICE2 and repress their transcriptional functions and overexpression of JAZ1 and JAZ4 represses freezing stress responses in Arabidopsis (Hu et al., 2013). It is suggested that JA acts as a critical upstream signal of the ICE-CBF/DREB pathway to positively regulate Arabidopsis freezing tolerance (Hu et al., 2013).

Gibberellin (GA) has various functions in regulating plant growth processes (Colebrook et al., 2014). Besides growth regulation, GAs are also able to coordinate plant growth and stress responses to contribute cold resistance by reducing GA levels and signaling after exposure to cold stress (Colebrook et al., 2014). Overexpression OsSLR1, encodes a rice DELLA protein, enhanced chilling tolerance by mediated SLR1 physically interacted with OsGRF6 to increase OsGA2ox1 expression and decrease the GA content (Li et al., 2021). Low temperature-induced CBF1 expression, result in increasing the accumulation of DELLA protein by decreasing GA content. CBF1 enhances freezing tolerance through the synergistic DELLA-dependent and COR-dependent pathways (Achard et al., 2008). In addition, DELLA proteins act as repressors of the GA hormones signaling pathway, and GRF modulated contribute to cold stress responsive gene expression (Lantzouni et al., 2020). In Capsella bursa-pastoris, overexpression CbCBF contribute to enhance cold tolerance and growth inhibition by interacting with GA and cell cycle pathways (Zhou et al., 2014). Auxin is one of the major growth hormones, which regulates all aspects of plant developmental processes (Rahman, 2013). Previous studies indicated that cold stress affects auxin transport rather than auxin signaling pathway and inhibits the inflorescence in Arabidopsis (Shibasaki et al., 2009). Cytokinin (CK) play important roles in plant growth, metabolism and development. CRF4, cytokinin response factor 4, is able to bind to the promoter of COR15a and affects the gene expression of COR15a. It’s indicated that a potential connection between CRF4 and the cold signaling pathway, possibly positively plant freezing tolerance by mediating CBFs and COR15a (Zwack et al., 2016). Also, several studies found that CK receptors double mutant ahk2ahk3 exhibit increased freezing tolerance (Jeon et al., 2010). It is also suggested that CK play vital roles in plant respond to cold stress. In summary, various hormones involved in the regulation of cold stress response in plant, and exists interaction between different hormones.

1.4 Molecular mechanisms in response to cold stress

Low temperature adversely affects plants growth, development and productivity. To cope with low temperature, plants have evolved a series of sophisticated mechanisms to respond cold stress on the molecular levels. The cold signaling pathway ICE-CBF-COR is the best studied mechanism in respond to cold stress. The ICE, CBF transcription factors, and COR are the core components (Wang, Jin, et al., 2017). Apart from basic components, some other activators or repressors are involved in this pathway that regulate plant in respond to cold stress. Also, plant hormones and light have been reported to play important roles in the response to cold stress by CBF-dependent or CBF-independent pathways (Barrero-Gil and Salinas, 2017). The CBF-dependent pathway plays a central role in the plants respond to cold stress (Fowler and Thomashow, 2002; Jaglo-Ottosen et al., 1998; Lee et al., 2021).

Upon exposure to cold stress, a set of cold-regulated (COR) genes are induced to increased plants chilling stress and freezing stress have been widely studied (Jaglo-Ottosen et al., 1998). Accumulated evidence suggests that cold stress induced the gene expression of ICE, subsequently, CBF expression was induced and then activated downstream COR genes expression (Chinnusamy et al., 2003; Gilmour et al., 1998; Wang, Jin, et al., 2017). The transcription factors CBFs/DREB play a central role in plant respond to cold stress. In Arabidopsis, CBF1, CBF2 and CBF3 are rapidly up-regulated upon exposure to low temperature (Achard et al., 2008; Jiang et al., 2017; Park et al., 2015). The family of CBFs belong to the family of AP2/EREBP family, which can bind to CRT/DRE cis elements and activate transcription of the downstream COR genes. The ICE act as a positive upstream regulator of CBF. In Arabidopsis, overexpression of CBF1 enhances cold tolerance by activating the genes expression of COR (Jaglo-Ottosen et al., 1998). Overexpression of CBF1 and CBF3 increases freezing tolerance, which activates COR gene expression (Liu et al., 1998; Maruyama et al., 2004). Additionally, the cbf triple mutant of Arabidopsis was more sensitive to freezing stress than single mutants cbf1, cbf2, and cbf3 (Jia et al., 2016; Zhao et al., 2016). Previous studies have shown that ICE1 and ICE2 positively regulate the expression of CBFs. ICE1 is ubiquitinated or sumoylated by HOS1 or SIZs, which can increase or inhibit the degradation of ICE1, thus inhibiting or maintaining the expression of CBF/COR genes (Dong et al., 2006; Park et al., 2011). Accumulated evidence shown that the overexpression ICE1 increase the freezing tolerance and the loss of function ice1 mutant exhibits chilling and freezing sensitivity (Chinnusamy et al., 2003).

In addition, various studies have documented that transcription factors and proteins responsible for protein post-translational modification (PTM) are involved in CBF-dependent signaling pathways. For instance, HOS1 (high expression of osmotically response gene) is an E3 ligase act as a negative regulator of cold responses. Dong et al. study shows that HOS1 physically interacts with ICE1 and mediates the ubiquitination of ICE1 in vitro and in vivo, results in the degradation of ICE1 proteins, which is required for HOS1. Overexpression of HOS1 in the loss of function hos1 mutant, represses the genes expression of CBFs and increases freezing stress sensitive (Dong et al., 2006). SIZ1, a SUMO E3 ligase, is contribute to conjugate of SUMO to protein substrates. SIZ1 mediated the sumoylation of ICE1 in vitro, the sumoylation of ICE1 reduced polyubiquitination of the protein in vitro, thus enhanced the stability of ICE1 protein. The siz1–2 and siz1–3 mutants are sensitive to chilling and freezing stress by reduced the gene expression of CBFs, whereas overexpression of SIZ1 increases the plant cold resistance (Miura et al., 2007). Miura found that the serine 403 of ICE1 is involved in regulating the transactivation and stability of the ICE1 protein. Overexpression of ICE1(S403A) enhanced freezing tolerance than ICE1(WT) in Arabidopsis, and the expression of genes such as CBF3/DREB1A, COR47 and KIN1 was increased in overexpression of ICE1(S403A). Furthermore, the protein level of ICE1(S403A) was not changed after exposure to cold stress, whereas the ICE1(WT) protein level was reduced, and polyubiquitylation of the ICE1(S403A) protein in vivo was obviously blocked. It’s indicated that the serine 403 of ICE is a key residue and play vital roles in the plant respond to low temperature (Miura et al., 2011; Mohideen et al., 2009). In addition, Ding et al. demonstrate that the protein kinase OST1, a key component in ABA signaling, is a positive regulator in CBF-dependent cold signaling. Upon exposure to low temperature, OST1 phosphorylates ICE and suppresses HOS1-mediated ICE1 degradation, thus inducing the expression of downstream cold tolerance genes (Ding et al., 2015).

1.5 Strategies to improve the cold tolerance of crops

Cold stress is one of the major environmental factors affecting crops growth. It has limited the yield of some crops, such as maize, rice, barley and cotton. Also, it affects the quality of crops, threaten food security. Therefore, improved crops cold resistance to cold stress or finding strategies to reduce the adverse effects of cold stress on crop yield and quality is important for ensuring crop production and food security. A variety of strategies could improve plant cold tolerance, but some of them are time-consuming and some are cost-consuming (Antoniou et al., 2016). Among of these, priming has been considered as an efficient strategy to improve plant cold tolerance (Li et al., 2013, 2014, 2016, 2018; Liu, Li, et al., 2017; Sun et al., 2018, 2020; Zuo et al., 2017). Priming, defined as the pre-exposure of plants to a moderate stimulus in the early growth stage, can induce more rapidly and/or more efficiently to respond subsequently more severe stress (Wang, Liu, et al., 2017). Stress priming studies include cis- and trans- priming experiments. Cis-priming, both stresses are physically and chemically identical, whereas in the trans-priming, the trigger stresses are different from pre-treatment (Baier et al., 2019). For instance, improved freezing tolerance of wheat and chickpea by drought priming pre-treatment (Li et al., 2015; Saini et al., 2019).

Cold acclimation is plant exposure to non-freezing low temperature and increased freezing tolerance (Furtauer et al., 2019). Many species are increased cold stress tolerance by the means of cold acclimation. Cold acclimation is a process involving various physiological and biochemical, including reduction of photosynthesis, accumulation of osmolytes, and up-regulation of COR genes and related proteins (Jackson et al., 2015; Król et al., 2015; Lado and Manzi, 2017; Ma et al., 2009). Recent studies have documented that some effective strategies to improve cold resistance, such as seed priming, chemical priming and abiotic stress priming (Fig. 1.2).

Figure 1.2 Represents the mechanism of improving cold tolerance by stress memory after priming in corps. MDA, malondialdehyde; SOD, superoxide dismutase; APX, ascorbate peroxidase; CAT, catalase; ROS, reactive oxygen species; ABA, abscisic acid; JA, jasmonic acid; SA, salicylic acid.

1.5.1 Seed priming for enhanced cold tolerance

Seed priming has been documented to improve seed performance by changing physiological process and metabolic concentrations after applying natural and synthetic compounds. Seed priming improved seed germination and seeding establishment contribute to adaptive abiotic stresses. A wide of seed priming has been reported, such as osmo-priming, chemical priming, hormonal priming, hydro-priming and redox priming, that contribute to promote plants cold resistance. For instance, seed priming with putrescine increased chilling stress tolerance in tobacco by increasing antioxidant enzyme activity and reducing the MDA concentration (Xu et al., 2010). In rice, seed priming effectively alleviated the negative effects of chilling stress by increasing the activities of antioxidant enzymes, accumulating of glutathione and free proline, thus decreased the chilling induced oxidative stress (Hussain et al., 2016). Likewise, seed priming with phytohormones as an effective method for mitigating the adverse effects of cold stress. For examples, in rice, seed priming with SA enhanced chilling tolerance by increasing antioxidant enzymes activity and reducing oxidative damage (Pouramir-Dashtmian et al., 2014). In maize, SA and H2O2 synergistically priming promoted hormones metabolism and signal transduction, and increased energy supply and antioxidant enzymes activities under chilling stress, which contribute to alleviate chilling injury and enhance chilling tolerance (Li et al., 2017). In wheat, seed priming with melatonin increased the germination rate and antioxidant capacity, and accelerate starch degradation under low temperature, which contribute to alleviate chloroplasts injury of wheat seedling (Zhang et al., 2021). In summary, seed priming enhanced seedlings cold stress tolerance by increasing ROS scavenging capacity, accumulation of osmotic protective substance, reducing the content of MDA and alleviating oxidative injury.

1.5.2 Cold priming for enhanced cold tolerance

Higher plants have developed a series of strategies to improve cold stress tolerance. Cold priming has been reported to have significantly impacts on plant cold tolerance. It’s defined as plants exposure to a moderately sub-optimal low temperature in the early stage, which contribute to more quickly and actively to respond to subsequent severe cold stress (Li et al., 2014). Cold priming is involved in various physiological responses, such as photosynthesis, antioxidant system, and metabolism. For instances, in wheat, earlier cold priming (5.2°C) induced subsequently cold stress tolerance by increasing antioxidant enzymes activity in chloroplasts and mitochondria, depressing the oxidative burst in photosynthetic apparatus, thus, improved subsequently cold stress tolerance (Li et al., 2014). Cold priming combined with foliar melatonin improved subsequently low temperature stress tolerance by increasing photosynthetic rate, stomatal conductance, antioxidant capacity and altering the related genes expression in wheat plants (Sun et al., 2018). Cold and SA priming conferring freezing stress tolerance by accumulation of free proline and sucrose, coordinating carbon and nitrogen metabolism in wheat plants (Wang et al., 2021). In a word, cold priming improved subsequently low temperature tolerance by changing photosynthesis rate, ROS scavenging capacity and the related cold-induced genes expression.

1.5.3 Cross-stress priming for enhanced cold tolerance

Other than seed priming and cold priming, drought priming or salt priming could induce low temperature tolerance. Previous study shown that salt priming with NaCl solution (30 mM) during seed germination could improve seedlings cold tolerance in wheat by enhancing the photochemical efficiency of photosystems, decreasing accumulation of MDA and alleviating cell death (Li et al., 2019). In chickpea, drought priming increased subsequently cold tolerance through maintaining the membrane stability and better cellular functioning in the cold, which can be correlated with low MDA content, high lipoxygenase activity, catalase activity, ascorbate peroxidase activity and glutathione reductase activity, and better mitochondrial functioning (Saini et al., 2019). Likewise, melatonin combined with drought priming induced cold tolerance by modulating subcellular antioxidant systems and ABA levels in barley (Li et al., 2016).

1.6 Conclusions and prospects

In the past years, much progress has been documented the mechanism of plants respond to cold stress from the aspects of physiological, biochemical and molecular. However, how plants sense cold signals remain unclear. When the plant suffers from low temperature, plants activate the process of cold responses in CBF-dependent and CBF-independent manners. Although the cold signaling pathway has been extensively studied, the molecular mechanism of cold signal perception and transduction must be studied in the future. Furthermore, priming is a useful method to improve crop cold tolerance; however, little information has been reported relative to signaling pathways involved in stress memory. Thus, understanding how plants respond to cold stress and the mechanisms of stress memory for improved cold tolerance are very important.

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