Extracellular ATP plays an important role in systemic wound response activation

Ronald J. Myers, Yosef Fichman, Gary Stacey, Ron Mittler*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

Mechanical wounding occurs in plants during biotic or abiotic stresses and is associated with the activation of long-distance signaling pathways that trigger wound responses in systemic tissues. Among the different systemic signals activated by wounding are electric signals, calcium, hydraulic, and reactive oxygen species (ROS) waves. The release of glutamate (Glu) from cells at the wounded tissues was recently proposed to trigger systemic signal transduction pathways via GLU-LIKE RECEPTORs (GLRs). However, the role of another important compound released from cells during wounding (extracellular ATP [eATP]) in triggering systemic responses is not clear. Here, we show in Arabidopsis (Arabidopsis thaliana) that wounding results in the accumulation of nanomolar levels of eATP and that these levels are sufficient to trigger the systemic ROS wave. We further show that the triggering of the ROS wave by eATP during wounding requires the PURINORECEPTOR 2 KINASE (P2K) receptor. Application of eATP to unwounded leaves triggered the ROS wave, and the activation of the ROS wave by wounding or eATP application was suppressed in mutants deficient in P2Ks (e.g. p2k1-3, p2k2, and p2k1-3p2k2). In addition, expression of systemic wound response (SWR) transcripts was suppressed in mutants deficient in P2Ks during wounding. Interestingly, the effect of Glu and eATP application on ROS wave activation was not additive, suggesting that these two compounds function in the same pathway to trigger the ROS wave. Our findings reveal that in addition to sensing Glu via GLRs, eATP sensed by P2Ks plays a key role in the triggering of SWRs in plants.

Original languageEnglish
Pages (from-to)1314-1325
Number of pages12
JournalPlant Physiology
Volume189
Issue number3
DOIs
StatePublished - Jul 2022
Externally publishedYes

Funding

FundersFunder number
Next-Generation BioGreen 21 Program Systems and Synthetic Agrobiotech Center
National Science FoundationIOS-1932639, IOS-1353886, IOS1826803, MCB-1936590, IOS-2110017
National Institutes of Health
National Institute of General Medical SciencesR01GM121445
University of Missouri
Rural Development AdministrationPJ01325403

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