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Review

Insights on Calcium-Dependent Protein Kinases (CPKs) Signaling for Abiotic Stress Tolerance in Plants

1
Department of Plant Breeding and Genetics, University of Agriculture, Faisalabad 38000, Pakistan
2
Center for Advanced Studies in Agriculture and Food Security, University of Agriculture, Faisalabad 38040, Pakistan
3
Industrial Crops Research Institute, Yunnan Academy of Agricultural Sciences, Kunming 650200, China
4
Department of Bioinformatics and Biotechnology, Government College University, Faisalabad 38040, Pakistan
5
Education Scientific Center of Nanotechnology, Far Eastern Federal University, 690950 Vladivostok, Russia
6
Mountain Research Centre for Field Crops, Sher-e-Kashmir University of Agricultural Sciences and Technology of Kashmir, Srinagar 190001, India
7
Department of Biotechnology, Chonnam National University, Chonnam 59626, Korea
*
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
Int. J. Mol. Sci. 2019, 20(21), 5298; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms20215298
Submission received: 28 June 2019 / Revised: 16 October 2019 / Accepted: 17 October 2019 / Published: 24 October 2019
(This article belongs to the Special Issue Plant Genomics 2019)

Abstract

:
Abiotic stresses are the major limiting factors influencing the growth and productivity of plants species. To combat these stresses, plants can modify numerous physiological, biochemical, and molecular processes through cellular and subcellular signaling pathways. Calcium-dependent protein kinases (CDPKs or CPKs) are the unique and key calcium-binding proteins, which act as a sensor for the increase and decrease in the calcium (Ca) concentrations. These Ca flux signals are decrypted and interpreted into the phosphorylation events, which are crucial for signal transduction processes. Several functional and expression studies of different CPKs and their encoding genes validated their versatile role for abiotic stress tolerance in plants. CPKs are indispensable for modulating abiotic stress tolerance through activation and regulation of several genes, transcription factors, enzymes, and ion channels. CPKs have been involved in supporting plant adaptation under drought, salinity, and heat and cold stress environments. Diverse functions of plant CPKs have been reported against various abiotic stresses in numerous research studies. In this review, we have described the evaluated functions of plant CPKs against various abiotic stresses and their role in stress response signaling pathways.

Graphical Abstract

1. Introduction

Plants have several adaptive features to cope with biotic and abiotic stresses under challenging environmental situations. Plants respond to these stresses by inducing the expression of stress-responsive genes through a complex signaling pathway. The expression of these stress-responsive genes is induced upon changes in calcium ion (Ca2+) concentrations, due to various biotic and abiotic stimuli [1,2], which enable plant adaptations in a wide range of stressed environments.
Calcium (Ca) as a ubiquitous secondary messenger regulates the stress signaling mechanism in plants. Changes in Ca2+ concentration are sensed by several calcium-binding proteins, especially calcium-dependent protein kinases [3]. The calcium-dependent abiotic and biotic stress signaling mechanisms are most commonly dominated by calcium-dependent protein kinases, which play a pivotal role in the regulation of plant responsiveness to salt, drought, and cold and heat stresses as well as other environmental factors. Ca2+ is involved in abscisic acid (ABA)-dependent biotic and abiotic stress signals in various plant species [4,5]. The calcium-dependent protein kinases phosphorylate the ABA-responsive element-binding factors (ABFs). ABA regulation by Ca2+ is associated with plant defense systems through induction of antioxidants [6], including reactive oxygen species (ROS) [2], and other enzymes like superoxide dismutase (SOD), catalase 3 (CAT3), ascorbate peroxidase (APX), glutathione peroxidase (GPX), and glutathione reductase (GR) [6,7]. It is also involved in the induction of some nonenzymatic antioxidants like ascorbic acid, α-tocopherol, carotenoids, and glutathione and controls multiple abiotic stress response processes [6,8,9,10]. This review will provide insight into the role of calcium-dependent protein kinases (CPKs) in abiotic stress tolerance in different plant species.

2. CPK Enzymes and Related Kinases

Several calcium-binding protein families have been identified in plants, which are potentially involved in the regulation of calcium-dependent abiotic stress response mechanisms. These Ca2+ sensors decode and transmit complex information, present in the form of calcium signal, to the phosphorylation events and regulate stress-responsive genes through protein interactions [11]. These Ca2+ signal-decoding groups include calcium-dependent protein kinases (CDPKs or CPKs), calmodulins (CaMs), calmodulin-like protein kinases (CMLs), calcineurin β-like proteins (CBLs), and Ca2+/calmodulin-dependent protein kinase (CCaMK) [12,13]. Among all these kinases, CPKs, CMLs, and CBLs have only been discovered in plants and some protozoans, while CaMs are highly conserved among all eukaryotes [11,14]. CaMs, CBLs, and CMLs are small proteins that function as calcium signal communicators through binding to downstream effectors (EFs) [15,16]. CaMs evolved from CMLs, which are considered as the most primitive calcium-binding proteins [13]. Among all these, CPKs were identified in plants as well as green algae, oomycetes, and in some protozoans [17], but they are not present in animals. CPKs, through direct binding with Ca2+, have a predominant regulatory role for the Ca-sensing protein families [17].

3. CPK Family in Plants

CPKs are considered as the versatile player for the regulation of abiotic stress management in plants [17]. In 1984, the very first plant CPKs were identified in Pisum sativum [18]. These proteins were initially purified from soybeans in 1987. A CPK encoding gene was cloned from Arabidopsis thaliana in 1991, which opened new ways for CPK gene cloning in several other plant species [11,19,20]. The presence of CPKs in almost all parts of the plant demonstrates that these kinases have a high potential for regulating various signal transduction pathways and have a significant influence on plant growth and development [17,21,22,23].

3.1. CPK Distribution and Localization in Plants

CPKs show a widespread distribution in different plant species. The whole-genome sequencing of plant species (e.g., Arabidopsis [24]) enables researchers to conduct genome-wide identifications of variable CPK encoding genes. These studies identified 34 CPK-encoding genes in the genome of Arabidopsis thaliana, 20 in Triticum aestivum (wheat), and 31 in Oryza sativa (rice) [20,25,26]. Solanum lycopersicum (tomato), which is a model plant of the Solanaceae family, has 29 CPK-encoding genes [27]. Genome-wide exploration of some other plants such as Zea mays (maize), Hordeum vulgare (barley), Cucumis melo (melon), Populus trichocarpa (poplar), Gossypium raimondii (cotton), Manihot esculenta (cassava), and Vitis vinifera (grapevine) revealed the presence of 40, 28, 18, 30, 41, 27, and 19 CPK-encoding genes, respectively [28,29,30,31,32,33,34] (Table 1). Mostly, CPK-encoding genes are expressed in leaves, meristems, roots, and flowers, while some are expressed only in specific tissues [23,35,36].
Similarly, CPKs are also found in pollens, embryonic cells, guard cells, xylem, and meristem [36]. These Ca-dependent functional proteins are involved in biological functioning in cellular and subcellular compartments. Numerous CPKs of Arabidopsis are membrane-localized. It is considered that the myristylation causes CPKs to target the membrane [62]. This cellular and subcellular localization indicates a significant role of CPKs in several signaling transduction pathways under stress stimuli.

3.2. CPK Domain Organization and Calcium Ion Signal Decryption

On account of specific abiotic stress stimuli, the plant activates distinct physiological and biochemical response pathways. These stimuli are perceived by some protein and nonprotein elements. Protein elements include enzymes, transcription factors, and disparate receptors, while nonproteins comprise some secondary messengers such as calcium ion cyclic nucleotides, hydrogen ions, lipids, and active oxygen species [17,63]. Among them, Ca is a crucial secondary messenger involved in the signal transduction in all eukaryotes. It regulates the cell polarity and is essential for the regulation of stress-responsive cellular processes, cell morphogenesis, as well as plant growth and development [3,11,64,65]. These calcium signals are recognized by several protein kinases (CPKs), which regulate the response of downstream factors.
The CPK-encoding protein commonly has four functional domains, viz., calcium-binding domain (CBD), N terminus variable domain (NTD), protein kinase domain (PKD), and autoinhibitory junction (AJ), but many CPKs also contain an amino-terminal domain with varying sequence lengths, which is a source of functional diversity in the CPK family [62]. Sometimes, the C-terminus variable domain (CTD) also considered as a distinct domain instead of NTD. Different plant species contain varying numbers of CPK genes that are functionally important. The CBD contains four loops where calcium ions directly bind, called EF-hands, and are 20 amino acids in length [20,66,67,68]. The PKD domain has a characteristic serine/threonine phosphorylation site, which responds during regulation of CBD and AJ through Ca signals [68,69]. Among the number of CPK proteins, the majority of them have a myristylation site upstream from their N-terminal variable domain, showing that no CPKs appear in the form of membrane integral proteins [23]. The N-terminus of CPKs has a greater percentage of proline, glutamine, serine, and threonine (PEST) sequences, which carry out swift proteolytic degradation. There is an auto-inhibitory domain adjacent to the conserved domains, having a pseudo-substrate domain activity, and can cause inhibition of the regulatory pathways [68]. The variation in the length of CPK genes is due to the NTD, CT domain, and EF hand of the calcium-binding domain. Ca2+ through binding with the EF-hand motif, carries out the phosphorylation of the CPK substrate by removing autoinhibition of kinase activity [22,70]. The highly conserved calmodulin-like domain regulates all the activities of the CPKs by binding the four Ca2+ ions to four EF hands at its downstream end. Proteomics of most of the CPKs show that the autophosphorylation of proteins at serine and threonine through a calcium-dependent manner regulate the kinase activity (Figure 1).
CPKs are monomolecular Ca-signaling protein kinases that regulate protein phosphorylation. In response to extrinsic and intrinsic cues, the variation in Ca2+ concentration, also called “Ca2+ signatures”, is recognized, interpreted, and transduced to the downstream toolkit by a group of Ca2+-binding proteins. Phosphorylation events cause the activation of CPKs.

3.3. Functional Characterization of Plant CPKs

CPKs are differentially involved in diverse and indispensable functions in various plant species. CPKs show their role against biotic and abiotic stress tolerance upon interaction with specific calcium signals. With respect to abiotic stresses, CPKs are involved in drought [71], salinity [72], and heat [73] and cold [74] stress response signaling by regulating the ABA-responsive transcriptional factors and ion channel regulation [75]. Some Arabidopsis CPKs (e.g., CPK13) are also involved in potassium ion (K+) channel regulation and other ion transportation in guard cells [11]. CPKs are also a major participant for providing pathogen-related immunity to plants. In several plant species, CPKs enhance the resistance against fungal elicitors [1,76,77], bacterial invasions [78], and many other pathogen-related diseases [60,79]. Some CPKs are involved in the regulation of the jasmonic acid (JA)-dependent pathway during insect and plant interaction and indirectly regulate plant resistance against insects [80]. The crucial role of CPKs have also been reported in various growth and developmental processes in plants. CPK-encoding genes (AtCPK28) in Arabidopsis play a positive role in stem elongation and contribute to secondary growth by interacting with the gibberellic acid (GA) pathway [81,82]. Similarly, some CPKs regulate pollen tube growth [83], latex biosynthesis [55,84], higher biomass accumulation [85], wounding and herbivory attack [80,86], germination and seedling growth [87], early maturity [88,89], pigmentation and fruit development [90], and several other metabolic and developmental pathways [91]. Still, the role and functionality of various CPK-encoding genes against biotic and abiotic stresses are veiled.

4. Role of CPKs in Abiotic Stress Tolerance

CPKs are recognized as a key Ca sensor group of protein kinase, having a multigene family in the whole plant kingdom [55,92]. The functions of these CPKs are completely dependent on Ca2+ signatures. Most of CPK functionality has been identified only in vitro, which is why only specific stress response-associated functions are known [93]. CPKs are not only involved in ion channel regulation but also respond to multiple stress-related pathways through interactions with other distant transcription factors through phosphorylation. Several loss-of-function and gain-of-function studies have confirmed the role of CPKs in abiotic stress tolerance. The cytosolic Ca2+ concentration fluxes, induced by various environmental stresses, viz., heat [47], cold [94] light [95], drought [96,97], salt [72,98], and osmotic [99] and pathogen-related factors [100], activate the plant’s transcriptional and metabolic activities [101]. Expression analyses and genome-wide studies have discovered the CPKs transcript activity, protein, and substrate recognition in different plant parts [93]. CPKs are also involved in the ABA-dependent abiotic stress signaling in various plant species. Several CPK genes are involved in the regulation of ABA signaling pathways in plants. Transient gene expression analyses in protoplasts of maize show that CPK11 (closely related to AtCPK4 and AtCPK11) acts upstream of mitogen-activated proteins (MPK5) and is required for the activation of defense functions and antioxidant enzyme activity by regulating the expression of MPK5 genes. Similarly, CPK11 induced by hydrogen peroxide (H2O2) regulates and controls the activity of SOD and APX production induced by the ABA signaling pathway [102,103]. CPK activity confirmed by global expression analyses, shows that several CPK members are expressed differentially under varying ABA, salinity, drought, and heat and cold levels [93]. The change in the expression of CPK genes indicates the role of CPKs in plant adaptation against abiotic stress environments.

4.1. CPK-Mediated Drought Response Signaling

Drought stress is a major destructive factor affecting plant growth and development. It decreases water potential in plants as a result, where ABA accumulation controls the opening and closing of stomata, which leads to a lower photosynthetic activity [104]. It decreases the biomass and grain yield in plants. Under drought, plants adopt several conformational changes in the cell. These include ABA-dependent stomatal movement through regulation of guard cells, osmotic adjustments through the accumulation of osmolytes, regulating the oxidative damage by ROS homeostasis, and so on [93,105]. Changes in cytosolic Ca2+ concentrations due to water deficiency initiates CPK activity, resulting in the release of ABA in the cell [97]. ABA induces the injection of a calcium chelator (i.e., 1,2-bis (2-aminophenoxy) ethane-N,N,N′,N′-tetra acetic acid; BAPTA), into the guard cell, which causes the closing of the stomata and, eventually, control of the transpiration process. Several plant CPKs are involved in drought stress-response mechanisms through an ABA-dependent manner. The CPK-encoding gene (CPK10) of Arabidopsis and an identified interacting heat shock protein (HSP1) lead to a drought-sensitive genotype. CPK10 T-DNA insertional mutants show sensitivity to drought stress as compared to the wild types. AtCPK9 and AtCPK10 are involved in Ca2+-dependent ABA-mediated stomatal regulation through interaction with AtCPK33 [106]. The light-induced Arabidopsis encoding gene (CPK13) is involved in inhibiting stomatal opening and contributes to the drought stress responsiveness [11]. Some drought-responsive CPKs also have some associated functions. In rice, for example, OsCPK9 controls both drought stress tolerance and spikelet fertility through an ABA-dependent manner. Results of overexpression of OsCPK9 (OsCPK9-OX) induces stomatal closure through osmotic adjustment and increases the pollen viability and spikelet fertility under polyethylene glycol (PEG-6000)-induced drought stress [71]. Another CPK-encoding gene from the wild grapevine (CPK20) acts as a regulator for drought and its associated with heat/cold responsive pathways. Expression of these genes studied in transgenic Arabidopsis reveals that VaCPK20 overexpression exhibits a high level of tolerance to drought and cold stress through regulation of stress responder genes, viz., ABA-responsive element binding factor 3 (ABF3) or sodium/hydrogen exchanger 1 (NHX1), and cold regulator gene (COR47) [107]. While a CPK-encoding gene of broad bean (VfCPK1) reported being highly expressed in leaf epidermal peels, it is not considered a tissue-specific gene and is only expressed under drought stress [108]. This CPK-encoding gene shows no relationship with both high (37 °C) and low (4 °C) temperatures. The increase in the number of transcripts of VfCPK1 under drought stress only plays a role in the up-regulation of ABA-responsive genes and other kinases that are involved in the signal transduction pathway [108].
Some CPKs are involved in the regulation of antioxidant production and osmolyte homeostasis to combat drought stress. AtCPK8 regulates the movement of the stomatal guard cell and H2O2 homeostasis in response to cellular Ca2+. An Arabidopsis T-DNA insertion mutant of CPK8 was found to be more sensitive to drought stress as compared to the wild-type plant, which reveals their drought response functionality [97]. CPKs phosphorylate some interactional proteins and perform interactive functioning in plants. Under drought stress, AtCPK8 with an interacting protein CAT3 controls the Ca2+-dependent ABA-mediated regulation of stomatal guard cells. The CPK8 mutant was more sensitive to drought stress, while overexpressing CPK8 in transgenic plants exhibited tolerance [97,109]. CaCPK1 activity increases the chickpea responsiveness to drought stress, and its activity is ubiquitous in all tissues of the plant [110]. The activation of drought-responsive CPK-encoding genes is also triggered by various biochemical pathways. A rice CPK-encoding gene (OsCPK1) specifically activated by sucrose starvation was involved in mechanism to prevent drought stress injury during germination by negatively regulating the expression of GA biosynthesis and activating the expression of a 14-3-3 protein ‘GF14c’ [111].
Some closely related CPK-encoding isoforms show functional diversity in response to drought stress. For example, functional divergence is present between two closely homologous (TaCPK7 and TaCPK12) genes of wheat [112]. Functional analysis of TaCPK7 and TaCPK12 reveals that TaCPK7 responded to H2O2, drought, salt, and low temperature, while TaCPK12 responded only through the ABA signaling pathway [112]. Several transgenic studies have been conducted to characterize the functions of CPKs in different plant species in relation to drought stress response signaling in plants. The ZoCDPK1 genes from ginger overexpressed in tobacco (Nicotiana tabacum) conferred drought as well as salinity tolerance by improving the photosynthesis and growth of the plant [113]. Enhanced expression of ZoCDPK1 under drought and JA treatment was observed, but no variation was found in expression because of low-temperature stress and abscisic acid treatment. ZoCDPK1 induces the expression of stress-responsive genes (i.e., early responsive to dehydration stress (ERD1) and responsive to dehydration (RD21A)). In ginger, it controls the stress signaling pathway and works in a CTR/DRE-independent manner [113]. Expression of CPK encoding genes of maize studied in Arabidopsis shows that ZmCPK4 is involved in resistance to drought stress through ABA-regulated stomatal regulation. ZmCPK4 induced by H2O2 and ABA treatment shows that there might be an association between mitogen-activated protein kinase (MAPKs) members and ZmCPK4 in the upregulation of ABA-regulatory components, especially ABA-insensitive (ABI5), ABF3, and Ras-associated binding protein (RAB18) [87]. The functions of several drought-responsive CPK-encoding genes are summarized in Table 2. (Details of all the genes are given in Table S1)

4.2. CPKs-Mediated Salt Response Signaling

Salt stress is also a major abiotic factor limiting plant growth and global agricultural productivity. Salinity, mostly due to the accumulation of sodium Na+ and chloride Cl ions, causes an ion imbalance that leads the plants toward oxidative stress [152]. These ions also induce the toxicity of other ions in plants. Salts also increases the production of ROS in plants. Several studies have presented the functioning of CPK-encoding genes in plants against salt stresses. In Arabidopsis, AtCPK27 genes were found in favor of plant adaptation against salt stress [125]. Disruption in the expression of CPK27 in a T-DNA insertional mutant shows salt hypersensitivity at early growth stages in Arabidopsis. CPK27 regulated H2O2 and ionic homeostasis. AtCPK3 functions in guard cell movement through osmotic adjustment and ion channel regulation during salt accumulation [11,117,118]. The overexpression of AtCPK3 also increases ABA sensitivity and salt hypersensitivity, affecting the seedling growth and stomatal regulation [98,117]. AtCPK6 belongs to a subclass of the CPK gene family in Arabidopsis whose expression is induced under salt-stressed conditions. AtCPK6 and other kinases are activated because of cytoplasmic Ca2+ elevation in the calcium-dependent pathway, which depends on ABA. These kinases combined with AtCPK6 trigger the salt and osmotic stress tolerance. Overexpression of AtCPK6 in Arabidopsis increases the drought and salt tolerance in transgenic plants. RT-PCR analyses showed an increase in the expression of salt-regulated genes in plants, in which the AtCPK6 gene was over-expressed [119].
OsCPK12 positively modulates salt stress tolerance, and it is associated with decreases in the resistance against blast disease by increasing the sensitivity to ABA and inducing the accumulation of ROS in rice [1]. In Arabidopsis, AtCPK27 was found to be favorable for plant adaptation against salt stress. Disruption in the expression of CPK27 in T-DNA insertional mutant shows salt hypersensitivity at early growth stages. Under salt stress, CPK27 regulates H2O2 and ionic homeostasis and makes plants resistant to salt stress (Figure 2) [125].
OsCPK21 genes regulate the ABA-dependent salt stress signaling pathway. The high survival rate of transgenic rice seedlings developed by a mini scale, full-length cDNA over-expresser (FOX) gene hunting system was found due to the overexpression of OsCPK21-FOX under salt stress. In these plants, many salt-induced and ABA-regulating genes were expressed more as compared to wild-type plants. Overexpression of OsCPK21 increases exogenous ABA and enhances salt tolerance by regulating and inducing the salt tolerance genes [136].
VaCPK21 gene up-regulation is positively involved in salt stress-response signaling mechanisms in grapevines. Overexpression of this gene in transgenic Arabidopsis and V. amurensis callus cell lines shows that under the salt stress, VaCPK21 acts as a regulator for genes that respond to salt stress (i.e., AtRD26, kinase-like protein (AtKIN1), AtRD29B, AtNHX1, catalase (AtCAT1), copper superoxide dismutase (AtCSD1), cold regulator (AtCOR15 and AtCOR15)), and are found functionally important for salt stress tolerance [149]. Similarly, CaCPK1 and CaCPK2 activities are enhanced during high salt stress in leaves of chickpea plants. These isoforms play a role in the regulation of phytohormones and defense signaling pathways [110].

4.3. CPK-Dependent Cold and Heat Stress Signaling

Several CPK-encoding genes are differentially expressed under cold and heat treatments, but their exact molecular response mechanism is still unknown. OsCPK17 was reported to be important for the cold stress response by targeting the sucrose synthase and plasma membrane intrinsic proteins in rice [135]. OsCPK24 causes inhibition of glutaredoxin (OsGrx10) to sustain higher glutathione levels and phosphorylation, through the Ca2+ signaling pathway, and responds positively to cold stress tolerance in rice [74]. MaCDPK7 was found as a positive regulator of heat-induced fruit ripening and chilling stress tolerance in bananas [146].
PeCPK10 provides cold and drought stress tolerance through ABA-induced stomatal closing in P. euphratica. Its constitutive expression regulates ABA-responsive genes (i.e., RD29B and COR15A) that regulate the cellular functioning. Transgenic Arabidopsis with over-expressed PeCPK10 showed lower water loss under drought stress and tolerance against freezing. Expression analyses reveal that PeCPK10 localizes in cytoplasm quickly in response to changes in Ca2+ concentrations and regulates the stomata guard cells, while nuclear-localized PeCPK10 only regulates the transcriptional factors [150]. CPK16 and CPK32 in grapevine plants positively regulate stilbene (a phenolic secondary metabolite) biosynthesis and CPK30 individually involved in both cold and drought tolerance [153]. In maize, ZmCPK1 and ZmCPK25 gene expressions were increased or decreased, respectively, upon exposure to cold stress. ZmCPK1 is negatively related with the regulation of the cold stress signaling mechanism. Studies of transgenic Arabidopsis also show that ZmCPK1 inversely regulates the expression of ethylene response factor (ZmERF3) genes and impairs cold stress tolerance [33]. CsCDPK20 and CsCDPK26 act as regulatory factors for heat stress-responsive genes and control positive heat stress signaling in the tea plant [144].

4.4. Role of CPKs in ROS Detoxification

Drought, salt, and heat stress triggers ROS production in plants, which must be detoxified by the plant to prevent itself from oxidative stress. Mitochondria, chloroplasts, and peroxisomes are the central organelles for ROS accumulation [105,154]. ABA-induced ROS production in plants is reported to be dependent on nicotinamide adenine dinucleotide phosphate hydrogen (NADPH) oxidase [105], which plays a vital role in oxidative bursting and activating plant defense responses [155,156]. Plant CPKs have been reported to regulate ROS production [2]. For instance, StCPK4 functions in the phosphorylation of NADPH oxidase and indirectly regulates ROS accumulation [143]. In B. napus, BnaCPK2 controls the activity of the respiratory burst oxidase homolog protein D (RbohD) during cell death and ROS production [2]. Arabidopsis CPK32 interacts with ABF4 in the ABA signaling pathway [126]. AtCPK6 from Arabidopsis decreases ROS production by reducing lipid peroxidation and confers drought stress [119]. Likewise, OsCPK12 promotes salt stress tolerance in rice through decreasing ROS accumulation [1]. The other CPKs and ROS responses are summarized in Table 2.

5. Functional Interaction of CPKs with Other Kinases in Abiotic Stress Signaling

CPK crosstalk and several interactions have been revealed in molecular regulatory pathways by functional studies. CPKs are not only involved in specific stress responses but also in multiple stress-related pathways by interacting with other distant proteins and regulating phosphorylation events. In Arabidopsis, CPK28 supports the turnover and phosphorylation of plasma membrane-related receptor-like cytoplasmic kinase (botrytis-induced kinase 1, BIK1), an important convergent substrate of multiple pattern recognition receptor (PRR) complexes for plant immunity [36]. AtCPK8 regulates and phosphorylates CAT3. It is involved in Ca2+-dependent ABA and H2O2-induced guard cell regulation and provides drought resistance [97,109]. Molecular responses of AtCPK1 studied by using real-time PCR (RT-PCR) show that the investigated gene expressions, viz., pyrroline-5-carboxylate synthetase 1(P5CS1), galactinol synthase 1(GOLS1), RD22 (dehydration-responsive protein), RD29A, C-repeat binding factor (CBF4), and KIN2 (kinases), were upregulated by ATCPK1 and conferred salinity stress tolerance [157]. Further, AtCPK1 in loss-of-function and gain-of-function mutants were studied. It provides salt and drought stress resistance by up and down-regulation of stress responder genes, viz., zinc finger protein (ZAT10), APX2, COR15A, and RD29A [157]. AtCPK12 phosphorylates several salt stress response-related proteins during regulatory functioning [72]. Another grapevine gene (VaCPK21) transgenically expressed in Arabidopsis interacts with several salt stress-related genes (i.e., AtRD29, AtRD26, AtKIN1, AtNHX1, AtCSD1, AtCAT1, AtCOR15, and AtCOR47). Likewise, VaCPK20 responds to cold and drought stress tolerance by regulating COR47, NHX1, KIN1, or ABF3 in transgenic Arabidopsis [107,149].
In vivo interaction validated by co-immunoprecipitation assays (Co-IP) revealed that OsCPK4, a dual-face protein, was involved in the regulation of the stability of cytoplasmic kinase (CPK176) in rice. OsCPK4 plays a vital role in the negative regulation of receptor-like OsCPK176 accumulation. OsCPK4 and OsCPK176 phosphorylation events provide pattern-triggered immunity [130]. OsCPK17 phosphorylates the sucrose-phosphate synthase (OsSPS4) and plasma membrane intrinsic proteins (OsPIP2;1 and OsPIP2;6) (aquaporin), which are essential in sugar metabolism and membrane channel activity against cold stress responses in rice [135]. Moreover, OsCPK24 is involved in the phosphorylation of glutathione-dependent thioltransferase and inhibition of OsGRX10 to maintain a higher level of glutathione. This regulatory pathway induces the overall cold stress responsiveness in rice [74]. The plant CPK-encoding genes also induce the regulation of other stress-responsive genes, viz., AtRBOHF, AtRBOHD, AtABI1, AtRAB18, AtRD29B, AtHSP101, AtHSP70, Arabidopsis heat stress transcription factor A2 (AtHSFA2), AtP5CS2, proline transporter (AtProT1), AtPOD, and AtAPX1 for drought, salt, heat and cold stresses [11]. In tea plants, CsCDPK20 and CsCDPK26 have an interactive function for thermo-tolerance [144]. BnaCPK2 interacts with NADPH oxidase-like RbohD and controls ROS accumulation and cell death in oilseed rape [2]. In Arabidopsis, CPK9 controls the ABA ion channel regulation through a Ca2+-dependent manner. Overexpression studies revealed that CPK9 and CPK33 mutually controlled the regulation of guard cells and stomatal movement [75]. CPK16 and CPK32 in grapevine plants positively regulate stilbene (a phenolic secondary metabolite) biosynthesis and CPK30 individually involved in both drought and cold tolerance [153]. Moreover, VaCPK1 and VaCPK26 genes are also involved in the same regulatory pathway ([89]. The overexpression of VaCPK29 up-regulates stress-responsive genes (i.e., dehydration elements (DREs) AtABF3, AtDREB1A, AtDREB2A, AtRD29A, and AtRD29B), which provide resistance to heat as well as osmotic stress [73]. Under in vitro conditions, post-transcriptionally miR390-regulated StCDPK1 controls the downstream auxin efflux carrier of PIN-proteins (StPIN4), which are involved in potato tuber development [142].
Arabidopsis CPKs interact and phosphorylate the basic leucine zipper domain (bZIP) transcription factor FD and have a crucial role in florigen complex formation, which induces late flowering in plants [127]. Biochemical analyses show that the cold-induced marker gene (Zmerf3), which is a type II ethylene response factor, is suppressed by ZmCPK1 in maize. It is supposed that the ZmCPK1 directly phosphorylates the ERF3 protein and, as a result, inactivates ERF and has a negative role in the cold stress response [33]. ZmCPK11 controls the upstream ZmMPK5, which is involved in ABA-dependent defense-related signaling in maize. CPK-encoding genes also have several interactive functions concerning plant growth and development. In Xenopus oocytes, AtCPK32 potentially regulates the cyclic nucleotide-gated ion channel regulating gene (CNGC18). AtCPK32 stimulation of CNGC18 regulates pollen tube depolarization in Arabidopsis [83]. Constitutively active OsCDPK1 in gain and loss-of-function transgenic rice targets the G-box factor 14-3-3c protein (GF14c). The expression of this protein causes the biosynthesis of GA and improves drought tolerance in rice seedlings [111]. AtCPK28 seems to be a regulatory component for the control of stem length and vascular development in Arabidopsis. The mutant of CPK28 (i.e., cpk28) was involved in the altered expression of NAC transcriptional regulators, such as NST1 and NST3, as well as gibberellin-3-beta-oxigenase 1 (GA3ox1), a regulator of gibberellic acid homeostasis [81]. After ABA treatment, the dual functioning OsCPK9-OX in rice increases the transcript levels of drought and spikelet fertility-responsive genes, viz., OsRSUS, Rab21, Osbzip66, and OsNAC45. The results confirmed by quantitative reverse transcription polymerase chain reaction (qRT-PCR) demonstrate that OsCPK9 in interacting with these genes switches on the molecular regularization of ABA and stress-associated pathways [71]. The ZoCDPK1 gene from ginger promotes the expression of drought and salinity stress associated genes, viz., RD2A (dehydration responsive protein 2A) and ERD1 (early responsive to dehydration stress 1) in tobacco. This DRE/CRT-independent regulatory pathway improves photosynthesis and plant growth as well [113]. Constitutive expression of calcium-dependent protein kinase of Populus euphratica (PeCPK10) regulates (RD29B and COR15A) cold and drought genes [150]. This cross-talk between CPK isoforms and the interactive partners increases the complexities among the signaling pathways.

6. Conclusions

The multifaceted role of CPKs in plants is consequential for abiotic stress tolerance in plants. Regardless of the reported functional detail on CPK-encoding genes, there are many other important isoforms identified whose expression profiles and involvement in abiotic stress signal transduction pathways in plants are still not clearly known. Future research is required to extend and identify the remaining CPK-encoding genes, their interactional regulators, and their functional exploration with respect to abiotic stress responses. These research studies are helpful to improve the plant’s adaptation under unpredictable environments and to minimize threats to the world’s food security.

Supplementary Materials

Author Contributions

Conceptualization, R.M.A. and L.S.; Validation, G.C., M.W., M.A.R.R., F.A., and S.H.W.; Investigation, L.S., M.W., and F.A.; Resources, M.W., B.A., M.A.R.R., M.A.N., and S.H.W.; Writing—original draft preparation, R.M.A. and L.S.; Writing—review and editing, M.A.R.R., L.S. and M.A.N.; Visualization, G.C., M.W., M.A.R.R.; Supervision, L.S.; Project administration, R.M.A.; Funding acquisition, R.M.A.

Funding

This research was funded by the Punjab Agricultural Research Board (PARB) of Pakistan under the project grant # PARB-938.

Acknowledgments

The authors wish to acknowledge the Center for Advance Studies in Agriculture and Food Security (CAS-AFS) at the University of Agriculture, Faisalabad Pakistan for providing the research opportunity to the Master’s Candidates of Plant Breeding and Genetics.

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

ABAAbscisic acid
AJAutoinhibitory junction
APXAscorbate peroxidase
AtABI1Arabidopsis thaliana ABA-insenstive-1
AtCDPK/AtCPKArabidopsis thaliana-calcium dependent protein
AtCSD1Arabidopsis thaliana copper superoxide dismutase 1
AtHSP101 and 70Arabidopsis thaliana heat shock protein 101 and 70
AtProT1Arabidopsis thaliana proline transporter 1
AtRBOHDArabidopsis thaliana respiratory burst oxidase protein D
AtRBOHFArabidopsis thaliana respiratory burst oxidase protein F
BaCDPK/BaCPKBrassica napus calcium dependent protein kinase
BIK1Botrytis-induced kinase 1
bZIPBasic leucine zipper domain
CaCalcium
Ca2+Calcium ion
CaCDPK/CaCPKCicer arietinum calcium dependent protein kinase
CaMsCalmodulins
CATCatalase
CAT3Catalase-3
CBDCalcium binding domain
CBF4C-repeat binding factor 4
CBLsCalcineurin β-like proteins
CCaMKCalcium/Calmodulin-dependent protein kinase
CDPKs/CPKsCalcium dependent protein kinases
CMLsCalmodulin-like protein Kinase
CNGC18Cyclic nucleotide-gated ion channel 18
Co-IPCo-immunoprecipitation assay
CORCold regulator
CTC-terminus
CTRC-repeat
DREDehydration elements
EFElongation Factor
ERD1Early responsive to dehydration stress 1
ERF3Ethylene response factor 3
FaCDPK/FaCPKFragaria x ananassa calcium dependent protein kinase
GAGibberellic acid
GA3ox1Gibberellin-3-betaoxigenase 1
GOLS1Galactinol synthase 1
GPXGlutathione peroxidase
GRGlutathione reductase
H2O2Hydrogen peroxide
HSFHeat stress transcription factor
HSPHeat shock protein
HvCDPK/HvCPKHordeum vulgare calcium dependent protein kinase
JAJasmonic acid
K+Potassium ion
LeCDPK/LeCPKSolanum lycopersicum calcium dependent protein kinase
MaCDPK/MaCPKMusa acuminate calcium dependent protein kinase
MPK5Mitogen-activated protein kinase 5
MsCPKMedicago sativa calcium dependent protein kinase
NaCDPK/NaCPKNicotiana attenuate calcium dependent protein kinase
NADPHNicotinamide Adenine Dinucleotide Phosphate Hydrogen
NHXSodium/Hydrogen exchanger
NSTNAC-transcription factors
NtCDPK/NtCPKNicotiana tabacum calcium dependent protein kinase
N-VDN-terminus variable domain
OsCPK/OsCDPKOryza sativa calcium dependent protein kinase
OsGrx10Oryza sativa glutaredoxin 10
OXOverexpression
P5CS1Pyrroline-5-carboxylate synthetase 1
PaCDPK/PaCPKPhalaenopsis amabilis calcium dependent protein kinase
PeCDPK/PeCPKPopulus euphratica calcium dependent protein kinase
PEGPolyethylene glycol
PESTProline, glutamine, serine and threonine
PgCDPK/PgCPKPanax ginseng calcium dependent protein kinase
PIPPlasma membrane intrinsic protein
PKDProtein kinase domain
PnCDPK/PnCPKPopulus euphratica calcium dependent protein kinase
PRRPattern recognition receptor
qRT-PCRQuantitative reverse transcription Polymerase chain reaction
RAB18Ras-associated binding protein 18
RbohDRespiratory burst oxidase homolog protein D
RD2ADehydration responsive protein 2A
RD29ADehydration responsive protein 29A
ROSReactive oxygen species
RT-PCRReal-time PCR
SiCDPK/SiCPKSetaria italic calcium dependent protein kinase
SODSuperoxide dismutase
StCDPK/StCPKSolanum tuberosum calcium dependent protein kinase
TaCDPK/TaCPKTriticum aestivum calcium dependent protein kinase
T-DNATransfer DNA
VaCDPK/VaCPKVitis amurensis calcium dependent protein kinase
VaCPK/VaCDPKVitis amurenssis calcium dependent protein kinase
VfCPK/VfCDPKVicia faba calcium dependent protein kinase
VrCDPK/VrCPKVigna radiata calcium dependent protein kinase
ZmCDPK1/ZmCPK1Zea mays calcium dependent protein kinase 1
ZoCDPK/ZoCPKZingiber officinale calcium dependent protein kinase

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Figure 1. Structure and activation process of plant CPKs. (A) CPK domain structure under the inactive state, (B) activation of CPKs after the binding of Ca2+ to the active site of the protein kinase domain (PKD), the autoinhibitory junction (AJ), and calmodulin-like domain (CaM-like domain, CaM-LD).
Figure 1. Structure and activation process of plant CPKs. (A) CPK domain structure under the inactive state, (B) activation of CPKs after the binding of Ca2+ to the active site of the protein kinase domain (PKD), the autoinhibitory junction (AJ), and calmodulin-like domain (CaM-like domain, CaM-LD).
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Figure 2. Role of different CPKs under various abiotic stresses; (A) Ca2+-dependent ABA-mediated drought and salt stress signal recognition by CPKs; (B) Ca2+ binding at the active site of protein kinase domain (PKD); (C) some drought-responsive genes involved in metabolite regulation and signal transduction pathways; (D) some salt-responsive genes and their role in antioxidant production (i.e., H2O2), as well as ROS detoxification; (E) some cold stress-responsive genes and their interaction genes activation; and (F) phosphorylation events controlling the anion channel regulation, K+-inward channel regulation, Ca2+-concentration, and channel regulation in the cell, and ABA-mediated CATALASE 3 regulation in plant cells.
Figure 2. Role of different CPKs under various abiotic stresses; (A) Ca2+-dependent ABA-mediated drought and salt stress signal recognition by CPKs; (B) Ca2+ binding at the active site of protein kinase domain (PKD); (C) some drought-responsive genes involved in metabolite regulation and signal transduction pathways; (D) some salt-responsive genes and their role in antioxidant production (i.e., H2O2), as well as ROS detoxification; (E) some cold stress-responsive genes and their interaction genes activation; and (F) phosphorylation events controlling the anion channel regulation, K+-inward channel regulation, Ca2+-concentration, and channel regulation in the cell, and ABA-mediated CATALASE 3 regulation in plant cells.
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Table 1. Genome-wide identification of calcium-dependent protein kinases (CPKs) among various plant species.
Table 1. Genome-wide identification of calcium-dependent protein kinases (CPKs) among various plant species.
Sr. #Common NameBotanical NameNo. of CPKsGenome Size (Mb)Reference
1AlgaeVolvox carteri6131.2[37]
2AppleMalus domestica28881.3[37]
3ArabidopsisArabidopsis thaliana34135[20]
4BananaMusa acuminata44523[38]
5BarleyHordeum vulgare27667[39]
6BarleyHordeum vulgare28667[31]
7Barrel cloverMedicago truncatula11360[37]
8Black cottonwoodPopulus trichocarpa28422.9[37]
9PoplarPopulus trichocarpa30500[34]
10ButcherMicromonas pusilla222[13,37]
11Cacao treeTheobroma cacao17346[13,37]
12CanolaBrassica napus251130[40]
13CassavaManihot esculenta26532.5[30]
14Caster beanRicinus communis15400[37]
15Castor beanRicinus communis15400[13,37]
16Chinese liquoriceGlycyrrhiza uralensis23379[41]
17ChlamydomonasChlamydomonas reinhardtii14111.1[13,37]
18ClementineCitrus clememtina26301.4[37]
19Cocoa treeTheobroma cacao17346[37]
20ColumbineAquilegia coerulea16306.5[13,37]
21CottonGossypium raimondii41880[28]
22CottonGossypium hirsutum982250–2430[42]
23CucumberCucumis sativus19323.99[43]
24CucumberCucumis sativus18203[37]
25Finger MilletEleusine coracana41593[44]
26FlaxLinum usitatissimum47318.3[37]
27Flooded gumEucalyptus grandis22691[37]
28Foxtail MilletSetaria italic27405.7[37]
29Foxtail MilletSetaria italic29405.7[45]
30Foxtail milletSetaria italica27405.7[13,37]
31GrapeVitis vinifera19500[29]
32GrapevineVitis amurensis17500[46]
33GrapevineVitis amurensis13500[47]
34Green algaeCoccomyxa subellipsoidea249[13,37]
35Green algaeOstreococcus lucimarinus313.2[13,37]
36Green beanPhaseolus vulgaris25521.1[37]
37LinseedLinum usitatissimum47318.3[13,37]
38MaizeZea mays352500[48]
39MaizeZea mays402500[49]
40MaizeZea mays472500[37]
41MelonCucumis melo18375[32]
42Monkey flowerMimulus guttatus25321.7[37]
43MustardBrassica rapa49283.8[37]
44Norway sprucePicea abies111960[37]
45Oilseed rapeBrassica rapa49283.8[13,37]
46OrangeCitrus sinensis24319[13,37]
47PapayaCarica papaya15135[13,37]
48PapayaCarica papaya15135[37]
49PeachPrunus persica17227.3[37]
50PepperCapsicum annuum31407.5[50]
51Pigeon PeaCajanus cajan23852[51]
52PotatoSolanum tubersum21800[37]
53PotatoSolanum tuberosum23800[52]
54Purple false bromeBrachypodium distachyon27272[37]
55Purple false bromeBrachipodium distachyon27272[37]
56Red Shepherd’s PurseCapsella rubella32134.8[37]
57RiceOryza sativa29430[53]
58RiceOryza sativa22430[54]
59RiceOryza sativa30372[37]
60Rubber treeHevea brasiliensis301332[55]
61Salt cressThellungiella halophile31238.5[13,37]
62Shepherd’s PurseCapsella rubella32134.8[37]
63SorghumSorghum bicolor28697.5[37]
64SoybeanGlycine max391115[56]
65SoybeanGlycine max501115[57]
66SoybeanGlycine max391115[58]
67SoybeanGlycine max41978[13,37]
68SpikemossesSelaginella moellendorffii11212.5[13,37]
69Spreading earthmossPhyscomitrella patens25480[13,37]
70Sweet orangeCitrus sinensis24319[37]
71SwitchgrassPanicum virgatum531358[37]
72TobaccoNicotiana tabacum15323.75[59]
73TomatoSolanum lycopersicum29900[60]
74TomatoSolanum lycopersicum28900[37]
75TomatoSolanum lycopersicum29900[61]
76WheatTriticum aestivum202125[26]
77Wild StrawberryFragaria vesca14240[37]
Table 2. Various functions of CPKs in biotic and abiotic stresses in different plant species.
Table 2. Various functions of CPKs in biotic and abiotic stresses in different plant species.
Sr. #Specie NameGeneFunctionReference
1Arabidopsis thalianaAtCPK1Cellular homeostasis, resistance fungal elicitor.[76,78,114,115,116]
2AtCPK3Salt resistance.[117,118]
3AtCPK4Regulate ABA-regulatory transcription factors (e.g., ABF, ABF4, drought resistance).[98]
4AtCPK5Regulate immunity responses, ROS-dependent cell-to-cell communication.[78]
5AtCPK6Drought tolerance, ABA-dependent osmotic adjustment.[119]
6AtCPK8Drought tolerance through interaction with protein CAT3.[97,109]
7AtCPK9Regulate the ABA-dependent signaling pathway interacting with CPK33.[75]
8AtCPK10Drought responsiveness, ABA-mediated stomatal movements.[106]
9AtCPK11Phosphorylation of AtDi19, ABA signaling.[120]
10AtCPK12Seed germination, activation of ABA regulators.[72,121]
11AtCPK16Root-gravitropism phosphorylate AtACS7.[122]
12AtCPK21Hyperosmotic adjustments.[123]
13AtCPK23Salt stress, drought stress.[124]
14AtCPK27Salinity resistance, H2O2 and ionic homeostasis.[125]
15AtCPK28Vascular development, stem elongation, ethylene synthesis, lignin deposition.[81,82]
16AtCPK32ABA-regulatory gene activation.[126]
17AtCPK33Regulates flowering, biosynthesis of florigen and flowering locus T protein.[127]
18Cicer areitinum
(Chickpea)
CaCPK1Salt stress, drought stress, phytohormones, and defense signaling pathways.[110]
19CaCPK2
20Capsicum annuum
(Peppers)
CaCPK3Pathogen resistance, defense functioning (i.e., regulates jasmonic and salicylic acid), ethephon.[79]
21Fragaria x ananassa
(Garden strawberry)
FaCPK1low-temperature tolerance, fruit ripening.[128]
22Medicago sativa
(Alfalfa)
MsCPK3Heat stress resistance, embryogenesis.[129]
23Oryza sativa
(Rice)
OsCPK1Drought stress, seed germination, and GA biosynthesis.[111]
24OsCPK4Microbial-associated immunity, OsRLCK176 degradation.[130]
25OsCDPK5Fungal attacks phosphorylate OsERG1 and OsERG3.[131]
26OsCPK9Drought stress tolerance, ABA sensitivity spikelet fertility.[71]
27OsCPK10Pseudomonas syringae pv resistance, SA and JA regulator.[132]
28OsCPK12Salt tolerance, blast disease resistance, induce ROS production, leaf senescence,[1,133]
29OsCDPK13Regulate cold, salt, dehydration responses.[134]
30OsCPK17Cold stress interacts with sucrose synthase and plasma membrane intrinsic proteins.[135]
31OsCPK21Salt tolerance, ABA pathway activation.[136]
32OsCPK24Cold stress tolerance, inhibition of OsGrx10.[74]
33OsCPK31Starch accumulation, early grain filling.[137]
34Nicotiana tabacum
(Tobacco)
NtCPK1Signaling localization for repression of shoot growth, GA biosynthesis.[138]
35NtCPK2Biotic stress immunity.[139]
36NtCPK32Pollen tube growth interacts with CNGC18.[83]
37Hevea brasiliensis
(Rubber tree)
HbCDPK1Latex biosynthesis, rubber production.[84]
38Panax ginseng
(Chinese ginseng)
PgCDPK1aRegulate ginseng growth.[85]
39Phalaenopsis amabilis
(Moth orchid)
PaCPK1Cold stress sensitivity, wounding, pathogen attack.[86]
40Triticum aestivum
(Wheat)
TaCDPK1Regulate metabolic and developmental pathways.[91]
41TaCPK7Drought stress, salt stress, ABA signaling pathway.[112]
42TaCPK12
43Zingiber officinale
(Ginger)
ZoCDPK1Salinity and drought stress tolerance.[113]
44Zea mays
(Maize)
ZmCPK1Cold stress regulates ZmERF3 expression.[33]
45ZmCPK4Upregulate ABA-regulatory components (i.e., ABI5, ABF3 and RAB18) with MAPKs.[87]
46ZmCPK11Superoxide dismutase and ascorbate peroxidase production, ABA pathway.[103]
47Vigna radiata
(Mung bean)
VrCPK1Salt stress tolerance.[140]
48Vicia faba
(Broad bean)
VfCPK1Drought stress resistance.[108]
49Solanum lycopersicum
(Tomato)
SlCDPK2Flowering.[141]
50SlCDPK10Xanthomonas oryzae pv. oryzae and Pseudomonas syringae resistance.
51SlCDPK18Xanthomonas oryzae pv. oryzae and Pseudomonas syringae resistance.[60]
52Solanum tuberosum
(Potato)
StCPK1Tuber formation.[142]
53StCPK4Fungal pathogen resistance, ROS production.[143]
54StCDPK5Blight resistance and susceptibility, ROS defense functioning.[100]
55StCDPK7Resistance against Phytophthora infestans.[77]
56Nicotiana attenuate
(Coyote tobacco)
NaCDPK4Wound-induced jasmonic acid (JA) accumulation, insect resistance.[80]
57NaCDPK5
58Camellia sinensis
(Tea plant)
CsCDPK20High-temperature stress resistance.[144]
59CsCDPK26
60Hordeum vulgare (Barley)HvCPK3Resistance against powdery mildew.[145]
61HvCPK4
62Brassica napus
(Oilseed rape)
BnaCPK2ROS accumulation, cell death.[2]
63Musa acuminate (Banana)MaCDPK7Heat-induced fruit ripening, chilling, stress tolerance.[146]
64MaCDPK2Sensitive to Foc-TR4 infection, biotic stress tolerance.[147]
65MaCDPK4Sensitive to Foc-TR4 infection, biotic stress tolerance.
66MaCDPK3Responsive for drought, cold, and salinity.
67Vitis amurensis
(Grapevine)
VaCPK1Salt stress, heat-responsiveness, stilbene bio-synthesis.[89,148]
68VaCPK26Salt stress, Stilbene bio-synthesis, through the induced expression of stilbene synthase (STS) genes.[89,148]
69VaCPK20Drought stress, cold stress.[107]
70VaCPK21Salt stress signaling.[149]
71Pharbitis nil
(Picotee)
PnCPK1Seed germination, seedling growth, flowering, regulation of light-dependent pathways, embryogenesis.[90]
72Populus euphratica (Desert poplar)PeCPK10Drought and cold stress tolerance, ABA-responsive genes regulator.[150]
73Cucumis melo
(Hami melon)
HmCDPK2Resistance against Penicillium infection.[151]

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Atif, R.M.; Shahid, L.; Waqas, M.; Ali, B.; Rashid, M.A.R.; Azeem, F.; Nawaz, M.A.; Wani, S.H.; Chung, G. Insights on Calcium-Dependent Protein Kinases (CPKs) Signaling for Abiotic Stress Tolerance in Plants. Int. J. Mol. Sci. 2019, 20, 5298. https://0-doi-org.brum.beds.ac.uk/10.3390/ijms20215298

AMA Style

Atif RM, Shahid L, Waqas M, Ali B, Rashid MAR, Azeem F, Nawaz MA, Wani SH, Chung G. Insights on Calcium-Dependent Protein Kinases (CPKs) Signaling for Abiotic Stress Tolerance in Plants. International Journal of Molecular Sciences. 2019; 20(21):5298. https://0-doi-org.brum.beds.ac.uk/10.3390/ijms20215298

Chicago/Turabian Style

Atif, Rana Muhammad, Luqman Shahid, Muhammad Waqas, Babar Ali, Muhammad Abdul Rehman Rashid, Farrukh Azeem, Muhammad Amjad Nawaz, Shabir Hussain Wani, and Gyuhwa Chung. 2019. "Insights on Calcium-Dependent Protein Kinases (CPKs) Signaling for Abiotic Stress Tolerance in Plants" International Journal of Molecular Sciences 20, no. 21: 5298. https://0-doi-org.brum.beds.ac.uk/10.3390/ijms20215298

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