Activation of indolic glucosinolate pathway by extracellular ATP in Arabidopsis.

Abstract

Dear Editor, Extracellular ATP (eATP) is a purinergic signal recognized by plasma membrane-localized transmembrane receptors, such as P2X or P2Y receptors found in mammals (Verkhratsky and Burnstock, 2014), and the P2K receptors found in plants (Choi et al., 2014; Pham et al., 2020). In mammals, eATP and purinoceptors are the basis of intercellular signaling used to regulate diverse processes including neuronal signaling, apoptosis, and inflammation (Verkhratsky and Burnstock, 2014). In plants, eATP and P2K1 appear to influence root growth (Weerasinghe et al., 2009; Zhu et al., 2017), but are currently best characterized as a damage associated molecular pattern signal and recognition system contributing to plant defense (Tanaka et al., 2014). In this study, we found that the indolic glucosinolate pathway is induced by eATP in Arabidopsis (Arabidopsis thaliana) and may play a role as a biochemical defense when plants are damaged by pathogens and herbivores. Accumulating evidence from our group and others suggests that eATP is released to trigger plant responses to various biotic stresses and touch/wounding (Dark et al., 2011; Ramachandran et al., 2019). Recently, the P2K1 overexpression line OxP2K1 was reported to enhance plant resistance against various foliar pathogens, such as Phytophthora brassicae (biotrophic oomycete), Pseudomonas syringae (hemibiotrophic bacterium), Botrytis cinerea (necrotrophic fungus), and Rhizoctonia solani (necrotrophic root fungus), whereas a knockout mutant line of P2K1, dorn1-3, showed increased susceptibility (Bouwmeester et al., 2011; Wang et al., 2014, 2016; Balagué et al., 2017; Chen et al., 2017; Tripathi et al., 2018; Kumar et al., 2020). As shown in Table 1 and Supplemental Figures S1–S4, a similar trend was observed with Sclerotinia sclerotiorum (necrotrophic fungus) and Phytophthora capsici (hemi-biotrophic oomycete), overexpression of P2K1 made the plants more resistant to the parasitic nematode Meloidogyne javanica, and, interestingly, pre-treatment of Arabidopsis with eATP made the plants more resistant to the turnip mosaic virus (TuMV). These data suggest that eATP plays an important role in plant defense against a broad range of pathogens. Furthermore, OxP2K1 showed enhanced resistance against Pieris rapae (specialist) and Spodoptera exigua (generalist) (Supplemental Figure S5), suggesting that eATP also plays an important role in the plant defense response against wounding caused by herbivorous insects. How eATP signaling contributes to defense against varied pests is not well understood.