Extracellular ATP acts as a damage-associated molecular pattern (DAMP) signal in plants.

Kiwamu Tanaka,Yangrong Cao,Jeongmin Choi,Gary Stacey

doi:10.3389/fpls.2014.00446

Abstract

As sessile organisms, plants have evolved effective mechanisms to protect themselves from environmental stresses. Damaged (i.e., wounded) plants recognize a variety of endogenous molecules as danger signals, referred to as damage-associated molecular patterns (DAMPs). ATP is among the molecules that are released by cell damage, and recent evidence suggests that ATP can serve as a DAMP. Although little studied in plants, extracellular ATP is well known for its signaling roles in animals, including acting as a DAMP during the inflammatory response and wound healing. If ATP acts outside the cell, then it is reasonable to expect that it is recognized by a plasma membrane-localized receptor. Recently, DORN1, a lectin receptor kinase, was shown to recognize extracellular ATP in Arabidopsis. DORN1 is the founding member of a new purinoceptor subfamily, P2K (P2 receptor kinase), which is plant-specific. P2K1 (DORN1) is required for ATP-induced cellular responses (e.g., cytosolic Ca2+ elevation, MAPK phosphorylation, and gene expression). Genetic analysis of loss-of-function mutants and overexpression lines showed that P2K1 participates in the plant wound response, consistent with the role of ATP as a DAMP. In this review, we summarize past research on the roles and mechanisms of extracellular ATP signaling in plants, and discuss the direction of future research on extracellular ATP as a DAMP signal.

Highlights

ENDOGENOUS DANGER SIGNALS, damage-associated molecular patterns (DAMPs) IN PLANTS Multicellular organisms have assembled complex signaling networks that mediate specific and dynamic responses following various environmental stimuli
Endogenous molecules and fragments from damaged cells and tissues can be recognized as danger signals, referred to as damage-associated molecular patterns (DAMPs)
Plants have evolved a large number of receptor kinases (e.g., >600 genes in Arabidopsis), most of which are likely involved in the response to different stresses, based on the observation that many duplication events have occurred in the genes involved in defense responses and disease resistance (Shiu et al, 2004)

Summary

Saccharides Volatile organic compounds Peptides

ATP NAD(P)H DNA Sucrose Oligogalacturonic acid (OGA) Green leaf volatiles Systemin* Pep914/890** Subtilase peptide (SubPep)** Hydroxyproline-rich glycopeptides Elicitor peptides (Peps). Detailed analysis of ATP-induced genes by Cao et al (2014) suggested that extracellular ATP signaling, mediated by P2K1, was involved in plant responses to a variety of stresses. Cell breakage is a simple mechanism for ATP release that could be caused by herbivore attack (i.e., wounding) or pathogeninduced cell lysis (i.e., necrosis) This released ATP would be expected to act as a DAMP. Given the high affinity of P2K1 for ATP recognition (Kd ∼46 nM), these levels of extracellular ATP would be sufficient to trigger P2K1-mediated ATP signaling This finding suggests that extracellular ATP released during wounding acts as a DAMP signal and is recognized by the P2K1 receptor (Figure 2).

Germinating pollen

Findings

ROLE OF EXTRACELLULAR ATP AS A DAMP