Apyrase Suppression Raises Extracellular ATP Levels and Induces Gene Expression and Cell Wall Changes Characteristic of Stress Responses      

Abstract

Plant cells release ATP into their extracellular matrix as they grow, and extracellular ATP (eATP) can modulate the rate of cell growth in diverse tissues. Two closely related apyrases (APYs) in Arabidopsis (Arabidopsis thaliana), APY1 and APY2, function, in part, to control the concentration of eATP. The expression of APY1/APY2 can be inhibited by RNA interference, and this suppression leads to an increase in the concentration of eATP in the extracellular medium and severely reduces growth. To clarify how the suppression of APY1 and APY2 is linked to growth inhibition, the gene expression changes that occur in seedlings when apyrase expression is suppressed were assayed by microarray and quantitative real-time-PCR analyses. The most significant gene expression changes induced by APY suppression were in genes involved in biotic stress responses, which include those genes regulating wall composition and extensibility. These expression changes predicted specific chemical changes in the walls of mutant seedlings, and two of these changes, wall lignification and decreased methyl ester bonds, were verified by direct analyses. Taken together, the results are consistent with the hypothesis that APY1, APY2, and eATP play important roles in the signaling steps that link biotic stresses to plant defense responses and growth changes.

Extracellular ATP: a potential molecule regulating the defence response of plants to biotic stresses - a review

“…Choi et al (2014) revealed that treatment with exogenous 100 µm ATP for 5-60 min increased the expression of mitogenactivated protein kinases, which have been reported to be induced by wounding, herbivore attack, or pathogen infection and be involved in herbivore and pathogen resistance (Zhang & Klessig 1998;Menke et al 2004;Heinrich et al 2011). Correspondingly, by suppressing the expression of apyrase that functions in hydrolysing eATP, it is found that a slight enhancement of the eATP concentration for 3-6 days induced the accumulation of ROS, biosynthesis of lignin, and expression of several genes that are involved in the defence responses to insect herbivores or pathogens (Lim et al 2014).…”

“…As mentioned above, short-term or slight enhancements of eATP level seem to induce some physiological responses that are also induced by or are associated with the defence responses to pathogen (Song et al 2006;Lim et al 2014). Thus, eATP could serve as an early signal of plant defence responses to pathogen infection.…”

“…Treatments of the plant with exogenous ATP can increase the contents of cytosolic free calcium ([Ca 2+ ] cyt ), ROS, and NO, all of which are well known as important intracellular signalling molecules (Kim et al 2006;Song et al 2006;Foresi et al 2007;Demidchik et al 2009;Reichler et al 2009;Clark et al 2010;Tanaka et al 2010b;Sun et al 2012a;Lim et al 2014;Möhlmann et al 2014). The increase of [Ca 2+ ] cyt induced by eATP is considered to come from an influx of Ca 2+ from the extracellular Ca 2+ and a release of Ca 2+ from the intracellular Ca 2+ storages including the vacuole, endoplasmic reticulum or mitochondria (Demidchik et al 2009;Tanaka et al 2010b).…”

“…Previous studies have shown that calcium (Ca 2+ ), nitric oxide (NO), reactive oxygen species (ROS), salicylic acid (SA), jasmonates (JA), cyclic nucleotides, polyphosphoinositides, sugars, abscisic acid (ABA), and polyamines play important roles as central signalling molecules during a variety of plant stress responses (Tuteja & Sopory 2008). An elevation of eATP levels can induce the expression of many genes involved in stress responses (Lim et al 2014). And, exogenous application of ATP can obviously affect the production of Ca 2+ , NO, ROS, and SA (see details below).…”

Extracellular ATP Acts on Jasmonate Signaling to Reinforce Plant Defense

“…A dozen studies showed that extracellular ATP signaling is associated with second messengers-cytosolic calcium (Ca 2+ ), reactive oxygen species (ROS), and nitric oxide (NO; Demidchik et al, 2003;Jeter et al, 2004;Song et al, 2006;Foresi et al, 2007;Wu and Wu, 2008;Reichler et al, 2009;Tanaka et al, 2010b;Tonón et al, 2010;Clark et al, 2011;Sun et al, 2012;Lim et al, 2014). Some of them are suggested to be mediated by cellular components in the plasma membrane, including Ca 2+ channels, heterotrimeric G Proteins, and NADPH oxidase (Song et al, 2006;Demidchik et al, 2009;Weerasinghe et al, 2009;Tanaka et al, 2010b;Hao et al, 2012;Wang et al, 2014).…”