Calcium Signaling in Plant Programmed Cell Death

Abstract

Programmed cell death (PCD) is a process intended for the maintenance of cellular homeostasis by eliminating old, damaged, or unwanted cells. In plants, PCD takes place during developmental processes and in response to biotic and abiotic stresses. In contrast to the field of animal studies, PCD is not well understood in plants. Calcium (Ca²⁺) is a universal cell signaling entity and regulates numerous physiological activities across all the kingdoms of life. The cytosolic increase in Ca²⁺ is a prerequisite for the induction of PCD in plants. Although over the past years, we have witnessed significant progress in understanding the role of Ca²⁺ in the regulation of PCD, it is still unclear how the upstream stress perception leads to the Ca²⁺ elevation and how the signal is further propagated to result in the onset of PCD. In this review article, we discuss recent advancements in the field, and compare the role of Ca²⁺ signaling in PCD in biotic and abiotic stresses. Moreover, we discuss the upstream and downstream components of Ca²⁺ signaling and its crosstalk with other signaling pathways in PCD. The review is expected to provide new insights into the role of Ca²⁺ signaling in PCD and to identify gaps for future research efforts.

Keywords: abiotic stress; calcium signal; development; hypersensitive response; programmed cell death; signal crosstalk.

Figure 1

The role of calcium signal in biotic stress-induced PCD. Ca²⁺ channel, sensor and relative gene and protein are presented. PTI: pattern-triggered immunity; ETI: effector-triggered immunity; flg22: a 22 amino acid PAMP derived from bacterial flagellin; FB1: Fumonisins B1; FLS2: Flagellin-sensitive 2; CNGCs: Cyclic nucleotide gated channel; BAK1: brassinosteroid insensitive 1-associated receptor kinase 1; SERK4: Somatic embryogenesis receptor kinase 4; BIK1: botrytis-induced kinase 1; BIR1: BAK1-interacting receptor-like kinase 1; SOBIR1: suppressor of BIR1-1; Peps: plant elicitor peptide; PEPRs: extracellular Pep receptors; CaM: calmodulin; CML: CaM-like protein; CDPK(CPK): Ca²⁺-dependent protein kinase; CBL: calcineurin B-like protein; CIPK: CBL-interacting protein kinase; cAMP: 3’-5’-cyclic adenosine monophosphate; cGMP: cyclic guanosine monophosphate; AC: adenylate cyclase; PDE: phosphodiesterase; PHS: phytosphingosine; MC4: metacaspase 4; 14-3-3: 14-3-3 proteins; SERCA: sarco-endoplasmic reticulum Ca²⁺-ATPase; ACA: autoinhibited Ca²⁺-ATPase; RPM1: resistance to Pseudomonas syringae pv. Maculicola 1; AvrRpm1: Pseudomonas syringae type III effector; MAPK: Mitogen activated protein kinase (based on [10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62]).

Figure 2

The role of calcium signal in abiotic stress-induced PCD. Salt, temperature, anoxic, heavy metal and mechanic damage stresses are depicted. OSCA1: hyperosmolality-induced [Ca²⁺](i) increase 1; MCA1: mechanosensitive channel 1; GLRs: glutamate receptor-like channels; AtHMA1: heavy metal transporting ATPase 1; NSCC: nonselective cation channel; CAX: H⁺/Ca²⁺ antiporters; COLD1: chilling-tolerance divergence 1; AtANN1: Ca²⁺- permeable transporter ANNEXIN1; OST1: open stomata 1; RGA1: rice G-protein a subunit 1; VPE: vacuole processing enzymes; JJW: JAV1-JAZ8-WRKY51 complex; JA: jasmonic acid; GIPCs: glycosyl inositol phosphoryl ceramides (based on [63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108,109,110,111,112,113,114,115]).

Figure 3

Ca²⁺ participates in the PCD during plant development and postharvest.

Figure 4

Crosstalk between calcium signal and ROS-, NO-, phytohormone-induced PCD. HPCA1: hydrogen peroxide sensor; PAMPs: pathogen associated molecular pattern; PRR: pattern recognition receptor; RBOHD: respiratory burst oxidase homolog protein; SA: salicylic acid; GA: gibberellin. (based on [145,146,147,148,149,150,151,152,153,154,155,156,157,158,159,160,161]).