Damage Signaling by Extracellular Nucleotides: A Role for Cyclic Nucleotides in Elevating Cytosolic Free Calcium?

Jian Sun,Youzheng Ning,Limin Wang,Julia M Davies,Katie A Wilkins

doi:10.3389/fpls.2021.788514

Abstract

Extracellular ATP (eATP) is now held to be a constitutive damage-associated molecular pattern (DAMP) that is released by wounding, herbivory or pathogen attack. The concentration of eATP must be tightly regulated as either depletion or overload leads to cell death. In Arabidopsis thaliana, sensing of eATP is by two plasma membrane legume-like lectin serine–threonine receptor kinases (P2K1 and P2K2), although other receptors are postulated. The transcriptional response to eATP is dominated by wound- and defense-response genes. Wounding and pathogen attack can involve the cyclic nucleotides cyclic AMP (cAMP) and cyclic GMP (cGMP) which, in common with eATP, can increase cytosolic-free Ca2+ as a second messenger. This perspective on DAMP signaling by eATP considers the possibility that the eATP pathway involves production of cyclic nucleotides to promote opening of cyclic nucleotide-gated channels and so elevates cytosolic-free Ca2+. In silico analysis of P2K1 and P2K2 reveals putative adenylyl and guanylyl kinase sequences that are the hallmarks of “moonlighting” receptors capable of cAMP and cGMP production. Further, an Arabidopsis loss of function cngc mutant was found to have an impaired increase in cytosolic-free Ca2+ in response to eATP. A link between eATP, cyclic nucleotides, and Ca2+ signaling therefore appears credible.

Highlights

Extracellular ATP is recognized as a plant cell regulator, with the ability to affect growth, development, and stress responses
Damage Signaling by Extracellular Nucleotides B. Clearly at both Extracellular ATP (eATP) concentrations loss of CNGC2 Overall these results show that CNGC2 could be involved in function allows the majority of the [Ca2+]cyt increase to occur. an eATP-induced [Ca2+]cyt increase in leaf tissue. It can only be inferred from existing studies that eATP could increase cyclic AMP (cAMP) or cyclic GMP (cGMP) synthesis to act as second messengers in [Ca2+]cyt-based damage-associated molecular pattern (DAMP) signaling
It is timely to assess experimentally whether eATP does elicit an increase in cyclic nucleotides and whether this is driven by known eATP receptors

Summary

INTRODUCTION

Extracellular ATP (eATP) is recognized as a plant cell regulator, with the ability to affect growth, development, and stress responses (reviewed by Matthus et al, 2019a). Annexin (which supports a hydroxyl radical-activated Ca2+ channel activity; Laohavisit et al, 2012) is implicated in eATP-induced [Ca2+]cyt increase of Arabidopsis roots and transcriptional regulation of wound- and defense-response genes, but its mode of action has not been determined (Mohammad-Sidik et al, 2021). Wu et al (2021) reported that eATP (0.1 mM) failed to elicit a plasma membrane Ca2+-permeable influx conductance in Arabidopsis pollen grain protoplasts of a cngc mutant This concentration of eATP stimulated pollen germination in the wild type but not cngc (Wu et al, 2021), but it remains unknown whether activation of CNGC2 by eATP would increase [Ca2+]cyt. Clearly at both eATP concentrations loss of CNGC2 Overall these results show that CNGC2 could be involved in function allows the majority of the [Ca2+]cyt increase to occur. an eATP-induced [Ca2+]cyt increase in leaf tissue

DISCUSSION

Findings

DATA AVAILABILITY STATEMENT