CDPKs in immune and stress signaling

Abstract

Ca(2+) has long been recognized as a conserved second messenger and principal mediator in plant immune and stress responses. How Ca(2+) signals are sensed and relayed into diverse primary and global signaling events is still largely unknown. Comprehensive analyses of the plant-specific multigene family of Ca(2+)-dependent protein kinases (CDPKs) are unraveling the molecular, cellular and genetic mechanisms of Ca(2+) signaling. CDPKs, which exhibit overlapping and distinct expression patterns, sub-cellular localizations, substrate specificities and Ca(2+) sensitivities, play versatile roles in the activation and repression of enzymes, channels and transcription factors. Here, we review the recent advances on the multifaceted functions of CDPKs in the complex immune and stress signaling networks, including oxidative burst, stomatal movements, hormonal signaling and gene regulation.

Figure 1

Relation tree of selected plant CDPKs. The full-length amino acid sequences of CDPKs (see supplementary material online) from Arabidopsis (At, blue), rice (Os, pink), soybean (Gm, brown), potato (St, black), barley (Hv, purple), tobacco (Nt, green), coyote tobacco (Na, green), tomato (Le, yellow) and grapevine (ACPK1, gray), maize (Zm, gray), alfalfa (Mt, gray), ice plant (Mc, gray) and peanut (Ah, gray) were aligned and analyzed with ClustalX and TreeView algorithms. The CDPK family is divided into four major subgroups (I–IV). The branched lengths are proportional to divergence and the scale of 0.1 represents 10% change. The CDPKs with known biological functions are highlighted in bold.

Figure 2

CDPK signaling network in immune responses. Microbe-associated molecular pattern (MAMP) perception by different cell-surface receptor kinases (RLKs) with distinct extracellular domains triggers transient CDPK activation to regulate transcription factors and early gene expression either independently or in coordination with MAPK cascades. Several CDPKs also activate NADPH oxidases (respiratory burst oxidase homologs, RBOHs) to induce early reactive oxygen species (ROS) production. By contrast, the sustained CDPK activation by extracellular (Avr9) or intracellular effector proteins leads to biosynthesis of salicylic acid (SA), jasmonic acid (JA) and ethylene (ET) through regulatory gene induction or enzyme activation such as phenylalanine ammonia-lyase (PAL) and ACC synthase (ACS). CDPKs also trigger a prolonged oxidative burst involved in cell death and hypersensitive response (HR). Constitutively active NtCDPK2 inhibits MAPK [salicylic acid-induced protein kinase (SIPK) and wound-induced protein kinase (WIPK)] activation by Avr9–Cf9 in an ET-dependent manner. Herbivores can be sensed through wounding or herbivore-associated elicitors (HAEs) by unknown receptors to activate MAPKs and Ca²⁺ influx. The co-regulation of ACS by MAPKs and CDPKs leads to ET production, whereas LeCPK1 inhibits the plasma membrane H⁺-ATPase to induce extracellular alkalinization. AtCPK3 and AtCPK13 mediate herbivore-induced gene expression by phosphorylating the transcription factor HsfB2a whereas only AtCPK3 negatively regulates Ca²⁺ channels. NaCDPK4 and NaCDPK5 negatively regulate defense against herbivores by inhibiting JA accumulation and subsequent production of defense metabolites. Abbreviations: MKKs, mitogen-activated protein kinase kinases; MKKKs, mitogen-activated protein kinase kinase kinases; MPKs, mitogen-activated protein kinases; TF, transcription factor.

Figure 3

CDPK signaling network in abiotic stress responses. Plants sense drought and salinity through Na⁺ toxicity, osmotic stress and ABA synthesis to activate CDPKs, which regulate K⁺ uptake, ROS production, accumulation of compatible osmolytes (proline), water transport (aquaporin, AQP) and gene expression. Redundant CDPKs modulate gene expression by activating the transcription factors ABFs and AtDi19s. AtCPK12 is a negative regulator that stimulates the protein phosphatase ABIs, inhibiting SnRK2- and CDPK-dependent transcriptional regulation. CDPKs also promote stomatal closure by inhibiting the K⁺ inward channel (KAT1), and activating slow-type anionic channels (SLAC1 and SLAH3). CDPKs and SnRK2s share common substrates (ABFs and channels) and common down-regulators (ABIs). Some CDPKs also inhibit permeable Ca²⁺ channels or Ca²⁺-pumps (ACA2) in a negative feedback loop. Several CDPKs have been shown to trigger cold tolerance; however, the molecular mechanism is not understood.