Extracellular ATP: a modulator of cell death and pathogen defense in plants

Abstract

Living organisms acquire or synthesize high energy molecules, which they frugally conserve and use to meet their cellular metabolic demands. Therefore, it is surprising that ATP, the most accessible and commonly utilized chemical energy carrier, is actively secreted to the extracellular matrix of cells. It is now becoming clear that in plants this extracellular ATP (eATP) is not wasted, but harnessed at the cell surface to signal across the plasma membrane of the secreting cell and neighboring cells to control gene expression and influence plant development. Identification of the gene/protein networks regulated by eATP-mediated signaling should provide insight into the physiological roles of eATP in plants. By disrupting eATP-mediated signaling, we have identified pathogen defense genes as part of the eATP-regulated gene circuitry, leading us to the discovery that eATP is a negative regulator of pathogen defense in plants.(1) Previously, we reported that eATP is a key signal molecule that modulates programmed cell death in plants.(2) A complex picture is now emerging, in which eATP-mediated signaling cross-talks with signaling mediated by the major plant defense hormone, salicylic acid, in the regulation of pathogen defense and cell death.

Figure 1

Model of how eATP- and SA-mediated signaling interconnect. Under normal growth conditions, basal SA levels do not deplete eATP. Basal eATP negatively regulates cell death and defense gene expression through eARP^via and eARP^def activity, respectively (blue lines). The red lines represent signaling activated by increases in tissue SA levels, caused by either exogenous application or elicitor/pathogen-induced biosynthesis. Inhibition of cell death by SA could involve signaling through eARP^via activity or another independent pathway (represented by dotted red lines). Black lines represent the outcome in response to addition of the non-hydrolysable ATP analogue, AMP-PCP. Cell death occurs in the presence of high light (∼200 µmol.m⁻².s⁻¹). Pointed arrows denote activation; blunt-ending lines denote downregulation.

Figure 2

Gene expression in response to SA and ATP treatments. (A) RT-PCR analysis of putative Arabidopsis eARPs in cell culture samples treated with 1 mM ATP or 200 µM SA for 30 minutes or 24 h, respectively. (B) RT-PCR analysis of a putative eARP^def and PR1, an archetypal SA-inducible defense gene. Arabidopsis cell cultures were treated with 200 µM SA for the indicated time. Actin 2 served as a constitutive reference gene.