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Review

Convergence and Divergence: Signal Perception and Transduction Mechanisms of Cold Stress in Arabidopsis and Rice

by
Xiaoshuang Wei
1,
Shuang Liu
2,
Cheng Sun
2,
Guosheng Xie
2,* and
Lingqiang Wang
1,*
1
State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Agriculture, Guangxi University, Nanning 530004, China
2
MOA Key Laboratory of Crop Ecophysiology and Farming System in the Middle Reaches of the Yangtze River, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, China
*
Authors to whom correspondence should be addressed.
Plants 2021, 10(9), 1864; https://doi.org/10.3390/plants10091864
Submission received: 3 August 2021 / Revised: 6 September 2021 / Accepted: 6 September 2021 / Published: 9 September 2021
(This article belongs to the Special Issue Plants Response to Temperature Extremes)
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Abstract

:
Cold stress, including freezing stress and chilling stress, is one of the major environmental factors that limit the growth and productivity of plants. As a temperate dicot model plant species, Arabidopsis develops a capability to freezing tolerance through cold acclimation. The past decades have witnessed a deep understanding of mechanisms underlying cold stress signal perception, transduction, and freezing tolerance in Arabidopsis. In contrast, a monocot cereal model plant species derived from tropical and subtropical origins, rice, is very sensitive to chilling stress and has evolved a different mechanism for chilling stress signaling and response. In this review, the authors summarized the recent progress in our understanding of cold stress response mechanisms, highlighted the convergent and divergent mechanisms between Arabidopsis and rice plasma membrane cold stress perceptions, calcium signaling, phospholipid signaling, MAPK cascade signaling, ROS signaling, and ICE-CBF regulatory network, as well as light-regulated signal transduction system. Genetic engineering approaches of developing freezing tolerant Arabidopsis and chilling tolerant rice were also reviewed. Finally, the future perspective of cold stress signaling and tolerance in rice was proposed.

1. Introduction

Cold stress limits the geographical distribution, growth habits, and productivity of plants [1]. There are two types of cold stress, including chilling stress (0 to 15 °C) and freezing stress (below 0 °C). Many temperate plants, such as Arabidopsis, rapeseed, wheat, and rye, have acquired a complex network that senses and responds to freezing stress. Molecular mechanisms and regulation networks of plasma membrane cold perception, signaling and freezing stress tolerance of these plants have been well-reviewed [2,3,4,5,6,7,8,9]. On the other hand, rice (Oryza sativa L.), one of the most important cereal crops, is susceptible to chilling stress, especially in high elevation and high latitude temperate zones [10]. Many novel regulatory genes have been identified in chilling stress perception and signaling in rice in the past decade [11,12,13]. This allows us to compare and distinguish the similarities and differences of cold stress sensing and signaling mechanisms between Arabidopsis and rice [8,9].
Plants respond to the decreased temperatures through sophisticated processes at different levels. Initially, plant cells perceive cold stress signals through the plasma membrane (PM) rigidification, PM-bound G-protein associated receptors, or cold sensors, such as Ca2+ influx channels, two-component histidine kinases, protein and nucleic acid conformations, or metabolite concentrations [6,14]. Then, the second messengers, including calcium ion, reactive oxygen species (ROS), and inositol phosphates, are generated. These second messengers further modulate the intracellular calcium (Ca2+) level. Perturbation in cytosolic Ca2+ level is sensed by calcium-binding protein (Ca2+ sensors), which interact with their target proteins, to transduce calcium signal in the cell. These proteins orchestrate cold stress signal transduction, activate protein phosphorylation cascades, and adjust the expression of transcription factors and cold regulated (COR) genes in plants [6].
This review summarized the recent progress in (i) cold stress perceptions, including PM-associated receptor-like kinases (RLK) and cold sensors; (ii) cold stress signaling mechanisms, including calcium signaling, phospholipids signaling, MAPK (mitogen-activated protein kinase) cascade signaling, and ROS signaling; (iii) ICE (inducer of CBF expression)-CBF (C-repeat binding factor) transcriptional regulatory network; (iv) the light-regulated signal transduction system in cold stress tolerance. We highlighted the similarities and differences in cold-induced responses contributing to freezing tolerant Arabidopsis and chilling tolerant rice. Finally, we evaluated the genetic engineering for improving cold stress tolerance in plants and explored future research of cold stress signaling and tolerance mechanism in rice.

2. Cold Stress Perceptions at Plasma Membrane (PM) in Arabidopsis and Rice

One of the major consequences of the temperature downshift is a decrease in membrane fluidity affecting membrane-associated cellular functions, and the PM is proposed as a primary sensor of low-temperature stress [15,16,17]. The feature of primary perception of temperature in plants has been proposed [18]. Different microdomains with lipid raft formation and composition, including sphingolipids in the PM, are responsible for sensing the particular temperature ranges [8,15]. Many putative calcium channels, PM-bound G-protein associated receptors, plasma membrane-localized receptor-like kinases (RLKs) have been identified as cold sensors in plants. Calcium channels responsible for Ca2+ influx have been considered a major sensor class for low temperature [19,20,21]. Through the membrane rigidification-activated mechano-sensitive or ligand-activated Ca2+ channels, cold stress induces a transient Ca2+ influx into the cytosol (Figure 1a). Two Arabidopsis calcium-permeable mechano-sensitive channels, AtMCA1 and AtMCA2, are involved in a cold-induced increase in [Ca2+]cyt and cold stress tolerance [22]. A cold sensor OsCOLD1 is the novel PM and endoplasmic reticulum (ER)-located protein, which interacted with α subunit 1 of the G protein (RGA1), enhancing the calcium transients in the cytosol in cold signal transduction in rice [23]. Two cyclic nucleotide-gated channels, OsCNGC14 and OsCNGC16, mediate the calcium signaling and promote chilling tolerance in rice seedlings. Their homologous proteins AtCNGC2 and AtCNGC4 in Arabidopsis promote chilling growth and freezing tolerance [24]. OsCNGC9 positively regulates chilling tolerance by mediating cytoplasmic calcium signaling in rice [25] (Figure 1b). Therefore, calcium channels play a central role in cold stress sensing in Arabidopsis and rice.
On the other hand, a new calcium sensor synaptotagmin without the EF-hand motif, AtSYT1, localized to the PM and ER, participates in the exocytosis process in the calcium-dependent pathway under freezing stress in Arabidopsis [26] (Figure 1a). In rice, thirteen SYT homologous N-terminal-TM-C2 domain proteins (OsNTMC2) have been annotated [27]. However, the function of OsNTMC2 in vesicle trafficking and PM repair in cold stress response awaits further investigations.
Many receptor-like protein kinases, such as two-component histidine kinases, RLKs, and G-protein associated kinases, have played pivotal roles in cold stress sensing in Arabidopsis and rice. Two-component signaling systems, AHK2/3, AHP2/3/5, and ARR7, mediate the cold stress signaling through inhibiting ABA signaling [28,29]. Besides, AtCRLK1 binds to calcium and calmodulin (CaM), interacts with phosphorylates AtMEKK1 in freezing signaling and tolerance [30]. Moreover, AtCRPK1 phosphorylates 14-3-3λ which shuttles from the cytosol to the nucleus, then interacts with and destabilizes the CBFs in freezing stress tolerance [31]. In addition, AtPXL1 interacts with and phosphorylates histidine-rich dehydrin1 (AtHIRD1) and a light-harvesting protein complex I (AtLHCA1) to positively regulate cold and heat stress tolerances during the germination stage [32].
In rice, there are several identified PM-localized kinases involved in cold stress perception. OsACA6, a PM Ca2+-ATPase, interacts with CaM-binding protein OsCaMBP1, calcium-dependent protein kinase (CDPK)-related kinase OsCRK2, and receptor-like kinase (RLK) OsRLK2 [33]. PM-localized OsCPK17 interacts with and phosphorylates the sucrose-phosphate synthase OsSPS4 and aquaporin OsPIP2;1/OsPIP2;6, can enhance the cold stress tolerance in rice [34](Figure 1b). CTB4a, a conserved leucine-rich repeat receptor-like kinase, interacts with a beta subunit of adenosine triphosphate (ATP) synthase AtpB and improves the yield under cold stress [35]. Interestingly, the protein level of phospholipase Dα1 (OsPLDα1) increases at one minute after cold treatment. It activates OsMPK6 and OsSIZ1, followed by the regulations of OsDREB1s expression in cold signaling [36] (Figure 1b). Therefore, there is much convergence of primary PM-located protein kinases in cold stress perceptions between Arabidopsis and rice.

3. Cold Stress Signal Transduction Mechanisms in Arabidopsis and Rice

Following the cold stress perceptions, cold stress signal transduction events occur in the cytosol and nucleus of plant cells. The second messengers, such as Ca2+ and reactive oxygen species (ROS), transmit the external cold signals to intracellular signaling systems. Progress has been made in calcium signaling, phospholipid signaling, MAPK cascade signaling, and ROS signaling in the past decades. Here, we compare the recent advances in signal transduction pathways of freezing stress in Arabidopsis and chilling stress in rice (Figure 2 and Figure 3), highlighting the divergence and convergence in cold stress in both plant species.

3.1. Calcium Signaling

Calcium influx into the cytosol is an early event in cold stress [6,17]. This transient elevation in calcium concentration is also called intracellular calcium signature. Calcium influx is primarily sensed by the calcium sensor proteins, containing the helix-loop-helix domain with the EF-hand motif. In plants, calcium sensors include four major classes: CaM/CaM-like protein (CML), calcium-dependent protein kinase (CDPK or CPK), calcineurin B-like (CBL) protein, and CBL-interacting protein kinase (CIPK). In addition, a small annexin family has been identified as a calcium sensor to cold stress response in Arabidopsis.
In Arabidopsis, overexpression of AtCaM3 hinders the cold induction of RD29A and KIN1, and the AtCaM4 negatively regulates freezing tolerance by interacting with a CaM-binding protein PATL1 [37]. AtCBL1 interacts with AtCIPK7 and binds to the DREB core element of COR promoters to negatively regulate freezing tolerance [38]. CaM-binding transcription activator protein CAMTA3 binds to the conserved CG-1 element in the CBF2 promoter, regulating CBF2 expression in cold stress signaling [39]. A vacuolar Ca2+/H+ antiporter AtCAX1 enhances the DREB1 transcription in cold acclimation response [40]. Recently, an AtOST1-AtANN1cascade was found to regulate calcium signaling in the CBF1-dependent manner to enhance freezing tolerance in Arabidopsis [41]. This evidence demonstrated the negative and positive regulations of calcium sensors to freezing tolerance in Arabidopsis.
In rice, a CaM-like protein OsCML16 and its six putative targets have been identified to be involved in cold stress response in rice [42]. However, there is no report about the role of OsCaMs in cold stress signaling. OsCDPK7 enhances cold stress tolerance by the increased accumulation of a putative target gene rab16A [43,44]. OsCDPK13 enhances cold stress tolerance by activating a ubiquitin-like nuclear protein OsCRTintP1, calreticulin interacting protein 1 [45,46]. OsCPK24 interacts with and phosphorylates OsGrx10, a glutathione-dependent thioltransferase, in cold stress response [47]. Overexpression of OsCIPK3, a CBL-interacting protein kinase, improves cold stress tolerance [48]. It is worth mentioning that OsCIPK31 is strongly induced by cold and salt stress and interacts with AtCBL3, suggesting the convergence of CBL/CIPK pathways in cold stress signaling Arabidopsis and rice [49]. As described above, the CaM-associated signaling pathways in cold stress signaling wait for further confirmations in Arabidopsis and rice.

3.2. Phospholipid Signaling

An increasing number of studies have shown that the metabolism of the membrane lipids plays an important role in the temperature stress response in plants. In Arabidopsis, in a few seconds after cold exposure, diacylglycerol kinase (DGK) is activated to converse diacylglycerol (DAG) into phosphatidic acid (PA), followed by a change in membrane fluidity [50]. Overexpression of a PM-bound phospholipase gene PLDδ enhances freezing tolerance in rice seedlings [51]. Suppressed expression of PLDα1 results in a significant increase in freezing tolerance [52]. Acyl-coenzyme A: diacylglycerol acyltransferase DGAT1 enhances freezing tolerance via CBF2 regulon and NADPH oxidase RbohD (respiratory burst oxidase homolog D)-dependent H2O2 production in Arabidopsis [53]. The acyl-coenzyme A-binding protein (ACBP) family has six members (AtACBP1-6) in Arabidopsis. Overexpression of AtACBP6 enhances freezing tolerance by activating PLDδ to decrease phosphatidylcholine (PC) levels and accumulate PA [54]. Overexpression of AtACBP1 increases freezing sensitivity via the expression of PLDα1 and PLDδ and maintains a membrane-associated PA pool [55]. Further, a temperature-induced lipid pathway has been demonstrated. The FAD2, FAD5 and ACT1 have been identified as the key enzymes in influencing fatty acid flux between the eukaryotic and prokaryotic pathways cold stress response in Arabidopsis [56].
In plants, glycerol-3-phosphate acyltransferase (GPAT) of chloroplasts is a key enzyme to catalyze transferring the acyl group of acyl-(acyl-carrier-protein) (ACP) into the sn-1 position of glycerol 3-phosphate in the first step of glycerolipid biosynthesis in chloroplasts. Ectopic overexpressing of AtGPAT in rice largely induces the unsaturation of fatty acids and chilling tolerance of photosynthesis under low temperature [57]. In rice, the ω-3 fatty acid (FA) desaturase (FAD8) mutant does not acclimate to cold stress [58]. OsPLDα1 increases the levels of PA that bind to OsMPK6 in cold signaling and tolerance [36]. Interestingly, comparative glycerolipidomics analysis of freezing stress (−6 °C and −12 °C) in Arabidopsis and chilling stress (4 °C and 10 °C) in rice has illustrated that Arabidopsis has a higher double bond index (DBI) and lower average acyl chain length (ACL) than rice under cold stress condition [59]. Accordingly, glycerolipid metabolism and signaling show great potentials in applying cold stress tolerance engineering in Arabidopsis and rice.

3.3. MAPK Cascade Signaling

In plants, the MAPK cascade consists of three sequentially phosphorylating and activating components, a MAP kinase kinase kinase (MEKK/MAPKKK), a MAP kinase kinase (MEK/MAPKK), and a MAP kinase (MPK/MAPK). MAPKs phosphorylate various downstream substrates, including transcription factors, protein kinases, phospholipases, and cytoskeleton-associated proteins, finally leading to the activation of specific gene expressions under stress conditions [60].
In Arabidopsis, MAPKKK protein AtANP1 initiates a phosphorylation cascade with AtMPK3 under cold stress [61]. The complete cascade AtCRLK1-AtMEKK1-AtMKK2-AtMPK4/6 has been established to positively regulate freezing tolerance [62]. Recently, AtMPK6 is found to phosphorylate AtMYB15 to reduce the binding affinity of AtCBF3 and freezing tolerance [63]. AtMPK3 and AtMPK6 phosphorylate AtICE1 to promote its degradation, thereby negatively regulate freezing tolerance [64]. AtMPK6 phosphorylates AtMYB5 to positively regulate freezing tolerance [63]. However, the AtMEKK1-AtMKK1/2-AtMPK4 cascade promotes freezing tolerance by antagonizing the AtMPK3/6 pathway [65]. These results indicate that AtMPK3, AtMPK4, and AtMPK6 proteins cooperatively regulate freezing tolerance in Arabidopsis.
In rice, there is not identified complete MAPK pathway involved in cold stress signaling until now. Our previous study established that the OsMKK6-OsMPK3 cascade modulates chilling signaling and tolerance in rice [66]. OsMPK3 phosphorylates and stabilizes OsICE1, which directly transactivates the expression of OsTPP1, thereby positively regulating chilling tolerance [67]. Moreover, PA binds to OsMPK6 and mediates chilling stress signaling and tolerance [36]. Therefore, these results have demonstrated a divergence in MAPK signaling pathways and regulation network in cold stress response in Arabidopsis and rice.

3.4. ROS Signaling

Under cold stress, excess ROS is produced and brings about oxidative damage and cold stress response in plant cells. In Arabidopsis, AtMEKK1-AtMKK2-AtMPK4/AtMPK6 cascade regulates the ROS-scavenging enzymes to maintain redox homeostasis under cold stress [62]. Overexpression of a ROS-regulated C2H2 zinc finger transcription factor AtZAT12 decreases the expressions of AtCBF1/2/3 genes under cold stress [68]. In addition, AtHAP5A, a heme-associated protein, positively modulates the freezing resistance by binding AtXTH21 and inhibits ROS accumulation under freezing stress [69]. Stromal and thylakoid-bound ascorbate peroxidases sAPX and tAPX trigger COR15A, PAL1, and CHS expressions under cold stress [70]. AtTrx-h2 regulates the expressions of COR genes under freezing stress [71].
H2O2 levels are increased within 1.5 h of 10 °C stress in rice seedlings [72]. A subset of 121 early-response genes was upregulated during the initial 24 h of 10 °C stress [73]; Among them, four are transcription factor genes, including ROS-bZIP1 and asl/ocs-like element-containing genes. A hypothetical model of ROS-mediated regulon (ROS-bZIP-as1/ocs) is assembled independent of CBF/DREB- or ABA-mediated regulons in cold stress response [72,73]. Comparative metabolomics analysis of indica (9311) and japonica (Nipponbare) varieties revealed a ROS-dominated dynamic model involved in chilling stress adaptation and tolerance in rice [74]. Overexpression of OsZFP245 enhances cold stress tolerance by regulating proline levels and ROS-scavenging activities in rice seedlings [75]. Overexpressing OsAPX1 prevents the over-accumulation of H2O2 and reduces lipid peroxidation in the spikelet tissues at the booting stage of rice [76]. Natural variation reveals that OsSAP16 controls low-temperature germination in rice [77]. Therefore, there exist specific and different pathways of ROS-mediated cold signaling in rice.

4. ICE-CBF Transcriptional Cascade

ICE and CBF homologs are highly conserved in Arabidopsis and rice. In Arabidopsis, ICE-CBF transcriptional cascade has been established as the main regulatory response toolkit to cold signaling and freezing tolerance [78]. There are several identified positive and negative regulators, including HK2/3, CAMTA3, OST1, HOS1, and SIZ1/2 for ICE1, ICE1 for CBF3, MYB15 for CBFs, and SRF6 for COR [79,80,81]. ICE1 binds toe CBF3 promoter and induces the CBF3 expression in cold stress signaling [82]. Overexpression of ICE2 induces the expression of CBF1 and enhances freezing tolerance [83]. A RING-finger ubiquitin E3 ligase, HOS1, interacts with ICE1 and targets for polyubiquitylation and proteolysis of ICE1 after 12 h of cold stress [79]. SIZ1 catalyzes sumoylation of ICE1 during cold acclimation and thus reduces the ICE1 polyubiquitylation [80]. OsSFR6 enhances freezing tolerance in Arabidopsis [84]. However, there are no such reports of cold signaling in rice.
Furthermore, OST1 phosphorylates and stabilizes ICE1 to enhance freezing tolerance [85]. ICE1 interacts with and negatively regulates the expression of MYB15 during cold acclimation [81]. EIN3, an ethylene-insensitive 3 gene, negatively regulates the expressions of CBFs and type-A ARRs [86]. Two repressors of jasmonate acid (JA) signaling, JAZ1, and JAZ4, interact with and suppress ICE1 and ICE2 transcription activity, finally repressing the CBF3 expression and freezing tolerance [87]. ZAT12 regulon inhibits the CBF cold-response regulatory pathway [68]. CAMTA3, a CaM-binding transcription factor, binds to the CG-1 element in the promoter of ZAT12 under cold stress [28].
In rice, transcript levels of OsICE1 and OsICE2 remain constant during cold stress, indicating that they are posttranslationally modified under cold stress [88]. Ectopic overexpression of OsICE1 and OsICE2 in Arabidopsis imparts freezing tolerance by inducing CBF expressions [89]. OsDREB1A and OsDREB1B transcripts are induced within 40 min after cold stress. Overexpressing OsDREB1A increases chilling stress tolerance in rice [90]. Ectopic overexpression of OsDREB1A and OsDREB1B in Arabidopsis enhances the expressions of stress-inducible genes rd29a, cor15a, and rd17 [91]. In particular, OsMYBS3 represses the transcriptional level of the OsDREB1-dependent cold response pathway in rice [92]. OsROC1 enhances the chilling tolerance by activating OsDREB1 in rice [93]. These results have revealed the convergence in the ICE-CBF cascade and divergence in the regulation of the ICE-CBF cascade in cold stress signaling in both species. As expected, new kinases, phosphatases, and transcriptional regulatory factors upstream and downstream of DREBs will integrate the convergent and divergent networks of cold stress signaling in Arabidopsis and rice.

5. Light Modulates the Cold Stress Tolerance

Cross talk between light signaling and cold signaling has been elucidated in the model plant Arabidopsis and tomato and cereals species [13]. For example, in Arabidopsis, there are five phytochromes isoforms phyA-E. By using Arabidopsis phys mutants, Franklin and Whitelam confirmed that phyB and D prevent the realization of FR-induced cold tolerance at 16 °C [94,95]. Interestingly, phytochrome A and B function antagonistically to regulate cold stress via abscisic acid (ABA)-dependent jasmonate signaling in tomatoes [96]. Similar results have been obtained in wheat and barley [97]. In barley, the light-regulated signal transduction system was reported to connect the circadian clock, phospholipid signaling pathway, calcium signaling elements, and the downstream HvCBF3/4 genes expressions under cold stress [98].
In rice, phyB negatively regulates chilling tolerance. The phytochrome B-deficient mutant (phyB) shows the more stabilized chloroplast structure and higher unsaturated fatty acid (USFA) content in membrane lipids, thereby alleviating the chilling-induced photoinhibition. Moreover, expressions of genes associated with USFA syntheses such as OsFAD7 and OsFAD8 are higher in the phyB mutant than in the wild type, suggesting that OsFAD7 and OsFAD8 are the downstream genes of phyB [99]. On the other hand, phyB negatively regulates the OsDREB1 expression through interacting with OsPIL16 to reduce the membrane integrity under cold stress [100]. Therefore, phyB probably senses the red light signals and transduces the low-temperature signal together with a series of downstream genes, at least in part through changes in the composition and stability of cell membranes under cold stress. Nevertheless, there are many gaps to bridge between red light signal reception and cold stress response in plants.

6. Downstream Response Pathways in the Arabidopsis Freezing Stress and Rice Chilling Stress

The development of genetically engineered plants by the repression and overexpression of selected genes seems to be a viable option to hasten the breeding of cold stress tolerance-improved crop plants. Genetic engineering of cold stress tolerance was reviewed in crop and horticultural plants in 2011 [101]. The recent progress in freezing tolerant transgenic Arabidopsis and chilling tolerant transgenic rice has been updated (Table 1 and Table 2). In Arabidopsis, engineering of freezing stress tolerance have been obtained through protein kinases and their associated proteins such as AtLCBK1 [102], AtBZR1 [103], AtCRF4 [104], ARR22 [105], and AtTCF1 [106]. Many transcription factors, such as bZIP, ZFP, WRKY, MYB, NAC, GT, DEAR, AP2, AREB, and ERF, have been applied to improve freezing stress tolerance. Furthermore, AtACBP6 [107] and AtLCBK1 [102] have been identified as positive regulators of freezing tolerance. Based on the four signaling pathways above, these engineered genes function downstream of phospholipid signaling, ROS signaling, and CBF regulon under freezing stress response (Table 1). Thus, these regulatory and functional proteins can adjust the balance of dehydration, detoxification, and metabolism under freezing stress in Arabidopsis, increasing the widespread distribution and adaptation to temperature stress in natural habitats.
In rice, a transgenic approach has been adopted to improve cold stress tolerance. We update the engineering cold stress-tolerant rice since 2011 (Table 2). Based on the functions of these genes in cold stress tolerance in rice, they can be divided into positive regulatory genes and negative regulatory genes. Positive regulatory genes include OsCAF1B [114], OsSHMT1 [115], OsUGT90A1 [116], OsPYL10 [117], OsRBGD3 [118], OsPYL3 [119], OsSAPK6 [120], OsPUB2/3 [121], OsRAN1 [122], OsRAN2 [123], OsZFP182 [124], OsCTZFP8 [125], OsbZIP46 [120], ONAC095 [126], OsNAC5 [127], OsWRKY76 [128], OsTERF2 [129] and OsMYB2 [130]. In addition, negative regulatory genes include OsMYB30 [131], OsbZIP52 [132], OsSPX1 [129] and OsWRKY45 [133]. Based on the four signaling pathways above, these engineered genes function downstream of ABA signaling, ROS signaling, and CBF regulon under chilling stress response in rice (Table 2). Therefore, these genes are responsible for ROS homeostasis, proton transport, pectin degradation, and trehalose biosynthesis under cold stress in rice.
Table
Table 2. List of transgenic chilling stress rice lines since 2011.
Table 2. List of transgenic chilling stress rice lines since 2011.
GenesProteinsSignaling
Pathways		Chilling Stress RegulationReferences
OsCAF1BCCR4-associated factor 1ROSPositive[114]
OsSHMT1Serine hydroxymethyltransferaseROSPositive[115]
OsUGT90A1UDP-glycosyltransferaseROSPositive[116]
OsPYL3pyrabactin resistance-likeABAPositive[119]
OsRBGD3RNA-binding glycine-rich proteinABAPositive[118]
OsPYL10ABA receptor 10ABAPositive[117]
OsSAPK6SNF-1 related protein kinase 2ABAPositive[120]
OsPUB2/3U-box E3 Ub ligasesCBFPositive[121]
OsRAN1small GTPaseROSPositive[122]
OsRAN2small GTPaseROSPositive[123]
OsZFP182TFIIIA-type zinc finger proteinROSPositive[124]
OsCTZFP8C2H2 zinc finger proteinROSPositive[125]
OsbZIP46bZIP transcription factorABAPositive[120]
OsbZIP52bZIP transcription factorABANegative[132]
ONAC095NAC transcription factorABAPositive[126]
OsNAPNAC transcription factorABAPositive[134]
OsNAC5NAC transcript factorROSPositive[127]
OsMBY30MYB transcription factorROSNegative[131]
OsMYB2MYB transcription factorROSPositive[130]
OsWRKY76WRKY transcript factorROSPositive[128]
OsWRKY45WRKY transcript factorROSNegative[133]
OsTERF2ethylene response factorROSPositive[88]
OsSPX1SPX domain proteinROSPositive[129]
OsBURP16Polygalacturonase 1βROSNegative[135]
OsAOX1aalternative oxidase 1ROSPositive[136]
OsAPX2ascorbate peroxidaseROSPositive[137]
OsAPXaascorbate peroxidaseROSPositive[76]
OVP1V-PPaseROSPositive[138]
OsTPS1trehalose-6-phosphate synthaseCBFPositive[139]

7. Conclusions and Perspectives

This review analyzes the convergence in cold sensors PM-bound calcium channels and receptor-like protein kinases in cold stress sensing in Arabidopsis and rice. Identifying these proteins in calcium signaling and MAPK cascades will be helpful to strengthen the cold-induced perception mechanisms in Arabidopsis and rice. On the other hand, there is convergence in calcium signaling, MAPK cascade signaling, ICE-CBF transcriptional pathways, and divergence in phospholipid signaling and ROS signaling. These signaling pathways have evolved into distinctive and integrative networks in cold stress responses in both species.
In the future, regulon engineering will be a novel strategy by using a master regulatory switch to cause transcriptional changes in the cold response of rice [140]. An efficient engineering approach will be to generate constitutively active mutant genes, for example, by deleting the inhibitory domains of transcription factors or changing phosphorylation mimicking/depriving status in the signal transducers such as MAPK, MAPKK, or receptor kinases. Meanwhile, to prevent constitutive overexpression of cold-responsive genes from consuming extra energy and producing undesirable traits, tissue-specific and cold stress-inducible promoters will be beneficial for the genetic improvement of cold tolerance in rice. Finally, a multi-genes site-specific assembly system will be developed. Elite constructs with multiple stress tolerant genes via CRISPR-Cas9 strategy should be designed to enhance rice crop productivity to cold stress.

Author Contributions

L.W. and G.X. conceived the idea and design of manuscript; X.W., S.L. and C.S. collected the references and summarized the data. X.W., L.W. and G.X. wrote the manuscript. L.W. and G.X. finalized the manuscript. All authors contributed to this article and approved the submitted version. All authors have read and agreed to the published version of the manuscript.

Funding

This work was granted by the Natural Science Foundation of Guangxi (grant no. 2020GXNSFDA238027), the National Natural Science Foundation of China (grant no. 31571583, 31771775, 31171524).

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Plasma membrane-localized proteins perceive the cold stress signals in Arabidopsis and rice. (a) In Arabidopsis, freezing stress initiates the PM rigidification, PM-associated calcium channels MCA1/2, calcium sensor SYT1 and kinases including CRLK1, AtHK1/2/3, and CRPK1, as well as PM-localized PXL1, participate in primary cold stress sensing and perception. (b) In rice, chilling stress initiates the PM rigidification, many PM-associated proteins, including calcium channels ACA6, CNGC14/16, phospholipidase PLDα1, aquaporin proteins PIP2;1/PIP2;6, G-protein-associated cold sensor COLD1 and kinases GT4a and CPK17, participate in primary cold stress sensing and perception. However, a specific calcium channel for calcium influx is still not known.
Figure 1. Plasma membrane-localized proteins perceive the cold stress signals in Arabidopsis and rice. (a) In Arabidopsis, freezing stress initiates the PM rigidification, PM-associated calcium channels MCA1/2, calcium sensor SYT1 and kinases including CRLK1, AtHK1/2/3, and CRPK1, as well as PM-localized PXL1, participate in primary cold stress sensing and perception. (b) In rice, chilling stress initiates the PM rigidification, many PM-associated proteins, including calcium channels ACA6, CNGC14/16, phospholipidase PLDα1, aquaporin proteins PIP2;1/PIP2;6, G-protein-associated cold sensor COLD1 and kinases GT4a and CPK17, participate in primary cold stress sensing and perception. However, a specific calcium channel for calcium influx is still not known.
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Figure 2. Putative model of cold stress signaling networks toward freezing stress tolerance in Arabidopsis. The cold-induced calcium signature in the cytosol is recognized by the calcium sensor proteins, including CaM, CDPK, CBL1/CIPK7, and CAMAT3, as well as the bZIP transcription factor SGB1 pathway. In addition, CRLK1-MEK1-MKK1/2-MPK4/6 cascade, ROS signaling, and phospholipid signaling work together to regulate cold stress signaling, and many ICE1-DREB transcription activators and repressors have been identified to regulate the COR gene expressions, finally leading to freezing tolerance in Arabidopsis.
Figure 2. Putative model of cold stress signaling networks toward freezing stress tolerance in Arabidopsis. The cold-induced calcium signature in the cytosol is recognized by the calcium sensor proteins, including CaM, CDPK, CBL1/CIPK7, and CAMAT3, as well as the bZIP transcription factor SGB1 pathway. In addition, CRLK1-MEK1-MKK1/2-MPK4/6 cascade, ROS signaling, and phospholipid signaling work together to regulate cold stress signaling, and many ICE1-DREB transcription activators and repressors have been identified to regulate the COR gene expressions, finally leading to freezing tolerance in Arabidopsis.
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Figure 3. Putative model of chilling stress signaling networks toward cold stress tolerance in rice. There are at least four chilling stress signaling pathways in rice. MYB4-ROS-bZIP cascade is involved in the ROS signaling process. MKK6-MP3 cascade and phospholipid signaling work with calcium signaling concomitantly in chilling stress signaling in rice. ICE1-DREB transcriptional regulatory cascade is conserved in the Arabidopsis and rice. Furthermore, these pathways’ upstream and downstream signal transducer proteins play cooperative and regulatory roles in cold stress tolerance in rice.
Figure 3. Putative model of chilling stress signaling networks toward cold stress tolerance in rice. There are at least four chilling stress signaling pathways in rice. MYB4-ROS-bZIP cascade is involved in the ROS signaling process. MKK6-MP3 cascade and phospholipid signaling work with calcium signaling concomitantly in chilling stress signaling in rice. ICE1-DREB transcriptional regulatory cascade is conserved in the Arabidopsis and rice. Furthermore, these pathways’ upstream and downstream signal transducer proteins play cooperative and regulatory roles in cold stress tolerance in rice.
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Table
Table 1. List of transgenic freezing stress Arabidopsis lines since 2011.
Table 1. List of transgenic freezing stress Arabidopsis lines since 2011.
GenesProteinsSignaling PathwaysFreezing Stress RegulationReferences
AtLCBK1long-chain base kinasesPhospholipidPositive[102]
AtBZR1brassinazole-resistant 1CBFPositive[103]
AtCRF4cytokinin response factor 4CBFPositive[104]
AtOST1open stomata 1CBFPositive[85]
AtACBP6Acyl-coenzyme A-binding protein 6PhospholipidPositive[107]
AHP2/3/5histidine phosphotransfer protein 2/3/5CBFPositive[28]
ARR22Arabidopsis response regulatorCBFPositive[105]
AtTCF1Tolerant to Chilling and FreezingROSNegative[106]
AtVOZ2vascular one zinc-finger proteinROSNegative[108]
AtCCA1circadian clock-associated 1CBFPositive[109]
AtMYB96MYB transcription factorCBFPositive[110]
AtFTL1AP2 transcription factorCBFPositive[111]
AtPMEI13pectin methyl-esterase inhibitorROSNegative[112]
AtSAG101lipase-like regulatorsPhospholipidNegative[113]
AtEDS1lipase-like regulatorsPhospholipidNegative[113]
AtPAD4lipase-like regulatorsPhospholipidNegative[113]
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Wei, X.; Liu, S.; Sun, C.; Xie, G.; Wang, L. Convergence and Divergence: Signal Perception and Transduction Mechanisms of Cold Stress in Arabidopsis and Rice. Plants 2021, 10, 1864. https://doi.org/10.3390/plants10091864

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Wei X, Liu S, Sun C, Xie G, Wang L. Convergence and Divergence: Signal Perception and Transduction Mechanisms of Cold Stress in Arabidopsis and Rice. Plants. 2021; 10(9):1864. https://doi.org/10.3390/plants10091864

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Wei, Xiaoshuang, Shuang Liu, Cheng Sun, Guosheng Xie, and Lingqiang Wang. 2021. "Convergence and Divergence: Signal Perception and Transduction Mechanisms of Cold Stress in Arabidopsis and Rice" Plants 10, no. 9: 1864. https://doi.org/10.3390/plants10091864

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