The role of extracellular ATP in plant abiotic stress signaling

Abstract

Adenosine 5'-triphosphate (ATP) is one of the most important molecules in living cells. ATP is majorly produced in the mitochondria by the processes of oxidative phosphorylation by the enzyme ATP synthase. It is known as the energy currency of the cell due to its ability to store energy and distribute it to various cells as and when required; thus it is crucial for diverse cellular processes. ATP is normally present inside the cell; however, in animals it was established that ATP can come out of the plasma membrane and into the extracellular spaces (Burnstock and Knight, 2004), and this ATP is referred to as extracellular ATP (eATP). In plants, the presence of ATP in extracellular space and its effect on plant processes were studied long ago (Jaffe, 1973); however, evidence for eATP acting as a signaling molecule in plants to regulate growth and development is relatively recent (Demidchik et al., 2003; Jeter et al., 2004). The identifcation of ATPs in the extracellular spaces posed the important question of what could be specifc stimulus for the release of ATPs from within the cell to intercellular spaces in plants. To answer this question different study concluded that external stimuli like wounding, pathogen attack, touch or mechanical stimulus or abiotic stresses may cause the release of cellular ATPs to the extracellular matrix (Choi et al., 2014). In animals, ATP exodus into the extracellular matrix mainly occurs through anion channels, gap junctions, ATP binding cassettes (ABC) transporters and vesicular exocytosis (Feng et al., 2015). In addition, eATP could also be produced by a plasma membrane-localized F0F1-ATP synthase complex in animal cells (Mangiullo et al., 2008). On the other hand, the eATP pool in plants is accumulated mainly by the release of intracellular ATP through ABC transporters or by exocytosis, as an ATP synthase complex is not found at the plasma membrane of plant cells (Feng et al., 2015; Kim et al., 2006). In addition, a plasma membrane-localized transporter PM-ANT1 mediates ATP release from the pollen tube during its maturation (Rieder and Neuhaus, 2011), and its variable expression levels in a wide variety of plant tissues hint towards a vital role of ATP transport into extracellular space in plants (Clark and Roux, 2011). eATP is widely accepted as a signaling molecule in animal cells as it could stimulate an increase in vital signaling components, including cytosolic free calcium (Ca2+), nitric oxide (NO) and reactive oxygen species (ROS) (Silva et al., 2006). Moreover, eATP is essential for several crucial physiological processes such as cell growth and cell death, neurotransmission, muscle contraction and immune response in animals (Khakh and Burnstock, 2009). Several recent studies have shown signifcant involvement of eATP in crucial cellular and physiological processes in plants such as root hair growth, vegetative growth, biotic and abiotic stress responses, pollen tube growth, gravitropism and cell viability (Tanaka et al., 2010, 2014; Cao et al., 2014; Chen et al., 2017; Tripathi et and Tanaka, 2018; Hou et al., 2018). The role of eATP in different processes in animal cells could be established due to knowledge of their cognitive receptors. Two types of membrane-associated purinergic receptors are known in animal cells: P2X, the ligand gated ion channels, and P2Y, G-protein coupled receptors (Khakh and Burnstock, 2009). However, the functional role of eATP as a signaling molecule in plants could be established only recently, because a membrane-associated purinoreceptor was unknown in plants until the recent identifcation of Does not Respond to Nucleotides (DORN1), a lectin receptor kinase, by Choi et al. (2014). The DORN1 gene was identifed through a large-scale mutant screening in Arabidopsis, where it was shown to mediate some eATP-related processes (Choi et al., 2014). Identifcation of this purinoreceptor in plants has led to several interesting studies which shed the light on some important physiological roles of eATP. Thus, here we elaborate, update and provide new insights in eATP signaling, regulation and functional roles in abiotic stress signaling in plants (Figure 13.1).