Role of Ca2+ in Mediating Plant Responses to Extracellular ATP and ADP

Abstract

Among the most recently discovered chemical regulators of plant growth and development are extracellular nucleotides, especially extracellular ATP (eATP) and extracellular ADP (eADP). Plant cells release ATP into their extracellular matrix under a variety of different circumstances, and this eATP can then function as an agonist that binds to a specific receptor and induces signaling changes, the earliest of which is an increase in the concentration of cytosolic calcium ([Ca²⁺]_cyt). This initial change is then amplified into downstream-signaling changes that include increased levels of reactive oxygen species and nitric oxide, which ultimately lead to major changes in the growth rate, defense responses, and leaf stomatal apertures of plants. This review presents and discusses the evidence that links receptor activation to increased [Ca²⁺]_cyt and, ultimately, to growth and diverse adaptive changes in plant development. It also discusses the evidence that increased [Ca²⁺]_cyt also enhances the activity of apyrase (nucleoside triphosphate diphosphohydrolase) enzymes that function in multiple subcellular locales to hydrolyze ATP and ADP, and thus limit or terminate the effects of these potent regulators.

Keywords: NADPH oxidase; apyrase; calmodulin; nitric oxide; reactive oxygen species.

Figure 1

Model of two hypothetical signaling pathways whereby eATP could induce an increase in [Ca²⁺]_cyt. In this model, two potential receptors could initiate the signaling pathway. The one starting with P2K1 is much better documented and supported by published data, whereas the one starting with a postulated (and as yet unknown) receptor is supported only by indirect evidence. The sequence of signaling steps initiated by P2K1 would include: 1, the binding of ATP to the plasma membrane-localized P2K1 receptor, thus activating its protein kinase activity; 2, the receptor-induced phosphorylation and activation of the RBOHD subunit of NADPH oxidase; 3, increased accumulation of reactive oxygen species (ROS) in the extracellular matrix (ECM); 4, ROS-induced opening of calcium channels; 5, increase in the [Ca²⁺]_cyt. This increase could then further activate RBOHD to synthesize more ROS (Steps 6 and 7). The sequence of signaling steps initiated by the postulated unknown receptor would include: 1′, the binding of ATP to the receptor; 2′, activation of G_α; 3′, the direct or indirect induction of Ca²⁺ channel activity by G_α; and 4′, increase in the [Ca²⁺]_cyt. There is also evidence for an as-yet unidentified pathway whereby receptor activation leads to the release of Ca²⁺ from internal stores, such as vacuoles and mitochondria. Dotted lines indicate steps mediated by as-yet unknown mechanisms.