Abstract
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 NUCLEOTIDES1 (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: PEROXIDASE52, SUBTILASE-LIKE SERINE PROTEASE1.7 and PHOSPHOLIPASEC-LIKE1. In wild-type Arabidopsis, the expression of genes encoding all three proteins responded to fumonisinB1, a cell death-activating mycotoxin. The expression of PEROXIDASE52 and PHOSPHOLIPASEC-LIKE1 was altered in fumonisinB1-resistant salicylic acid induction-deficient (sid2) mutants. Exposure to fumonisinB1 suppressed PHOSPHOLIPASEC-LIKE1 expression in sid2 mutants, suggesting that the inactivation of this gene might provide mycotoxin tolerance. Accordingly, gene knockout mutants of PHOSPHOLIPASEC-LIKE1 were resistant to fumonisinB1-induced death. The activation of PHOSPHOLIPASEC-LIKE1 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, PHOSPHOLIPASEC-LIKE1 serves as a convergence point for fumonisinB1 and extracellular ATP signalling, and functions in the Arabidopsis stress response to fumonisinB1.
Highlights
When secreted into the extracellular matrix, the highenergy molecule adenosine 50-triphosphate (ATP) functions as an important signalling molecule
We have previously reported that extracellular ATP regulates plant cell death (Chivasa et al, 2005)
Proteins secreted into the growth medium of Arabidopsis cell suspension cultures were analysed using liquid chromatography and tandem mass spectrometry
Summary
When secreted into the extracellular matrix, the highenergy molecule adenosine 50-triphosphate (ATP) functions as an important signalling molecule In plants this extracellular ATP activates an influx of Ca2+ into the cytosol (Demidchik et al, 2003; Jeter et al, 2004; Tanaka et al, 2010) and biosynthesis of second messenger molecules, such as reactive oxygen species (Demidchik et al, 2009; Song et al, 2006; Wu et al, 2008), nitric oxide (Foresi et al, 2007; Reichler et al, 2009; Tonon et al, 2010; Wu and Wu, 2008) and phosphatidic acid (Sueldo et al, 2010). The inhibition of Ca2+ influx (Jeter et al, 2004; Wu and Wu, 2008) or blocking the accumulation of second messenger signal molecules (Hao et al, 2012; Tonon et al, 2010; Wu and Wu, 2008) prevents extracellular ATP-induced plant responses, indicating that ATP is sensed at the external cell surface to activate intracellular signalling through classical signalling intermediates.
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