Summary ATP is secreted to the extracellular matrix, where it activates plasma membrane receptors for controlling plant growth and stress‐adaptive processes. DOES NOT RESPOND TO NUCLEOTIDES 1 (DORN1), was the first plant ATP receptor to be identified but key downstream proteins remain sought after. Here, we identified 120 proteins secreted by Arabidopsis cell cultures and screened them for putative stress‐responsive proteins using ATP‐affinity purification. We report three Arabidopsis proteins isolated by ATP‐affinity: PEROXIDASE 52, SUBTILASE‐LIKE SERINE PROTEASE 1.7 and PHOSPHOLIPASE C‐LIKE 1. In wild‐type Arabidopsis, the expression of genes encoding all three proteins responded to fumonisin B1, a cell death‐activating mycotoxin. The expression of PEROXIDASE 52 and PHOSPHOLIPASE C‐LIKE 1 was altered in fumonisin B1‐resistant salicylic acid induction‐deficient (sid2) mutants. Exposure to fumonisin B1 suppressed PHOSPHOLIPASE C‐LIKE 1 expression in sid2 mutants, suggesting that the inactivation of this gene might provide mycotoxin tolerance. Accordingly, gene knockout mutants of PHOSPHOLIPASE C‐LIKE 1 were resistant to fumonisin B1‐induced death. The activation of PHOSPHOLIPASE C‐LIKE 1 gene expression by exogenous ATP was not blocked in dorn1 loss‐of‐function mutants, indicating that DORN1 is not required. Furthermore, exogenous ATP rescued both the wild type and the dorn1 mutants from fumonisin‐B1 toxicity, suggesting that different ATP receptor(s) are operational in this process. Our results point to the existence of additional plant ATP receptor(s) and provide crucial downstream targets for use in designing screens to identify these receptors. Finally, PHOSPHOLIPASE C‐LIKE 1 serves as a convergence point for fumonisin B1 and extracellular ATP signalling, and functions in the Arabidopsis stress response to fumonisin B1.

Summary Despite having a network of cytoplasmic interconnections (plasmodesmata) facilitating rapid exchange of metabolites and signal molecules, plant cells use the extracellular matrix as an alternative route for cell–cell communication. The need for extracellular signalling in plasmodesmata‐networked tissues is baffling. A hypothesis is proposed that this phenomenon defines the plant extracellular matrix as a ‘democratic space’ for collective decision‐making in a decentralized system, similar to quorum‐sensing in bacteria. Extracellular communication enables signal integration and coordination across several cell layers through ligand‐activated plasma membrane receptors. Recent results from drought stress‐adaptive responses and light‐mediated signalling in cell death activation show operational utility of this decision‐making process. Opportunities are discussed for new innovations in drought gene discovery using platforms targeting the extracellular matrix.

Extracellular ATP is a purinergic signal with important functions in regulating plant growth and stress-adaptive responses, including programmed cell death. While signalling events proximate to receptor activation at the plasma membrane have been characterised, downstream protein targets and the mechanism of cell death activation/regulation are unknown.We designed a proteomic screen to identify ATP-responsive proteins in Arabidopsis cell cultures exposed to mycotoxin stress via fumonisin B1 (FB1) application.Arabidopsis RIBONUCLEASE 1 (RNS1) was identified by the screen, and transgenic plants overexpressing native RNS1 showed greater susceptibility to FB1, while a gene knockout rns1 mutant and antisense RNS1 transgenic plants were resistant to FB1-induced cell death. Native RNS1 complemented rns1 mutants and restored the cell death response to FB1, while a catalytically inactive version of the ribonuclease could not. The FB1 resistance of salicylic acid (SA)-depleted nahG-expressing plants was abolished by transformation with native RNS1, but not the catalytically dead version.The mechanism of FB1-induced cell death is activation of RNS1-dependent RNA cleavage, which is blocked by ATP via RNS1 suppression, or enhanced by SA through induction of RNS1 expression. Our study reveals RNS1 as a previously unknown convergence point of ATP and SA signalling in the regulation of stress-induced cell death.