Regulation of plant growth and development by extracellular nucleotides

The traditionally emphasized roles of ATP and other nucleotides are in energy metabolism, and they all happen within the borders of the plasma membrane of cells. However, recent findings, first in animals and then in plants, indicate that ATP and ADP can have significant roles outside the plasma membrane as agonists that do not have to be hydrolyzed to induce diverse signaling responses in cells. This chapter reviews results obtained mainly in Arabidopsis that point to a likely role of extracellular nucleotides as regulators of plant growth and development. Concentrations of ATP in the 40-60-μM range are released from cells into intercellular spaces of plant tissues by wounds, and lower levels of applied ATP, but not AMP or phosphate, can induce increases in the concentration of cytoplasmic calcium ions and such calcium-dependent downstream responses as increased superoxide production and increased levels of messenger RNAs associated with wound responses such as lipoxygenase and 1-aminocyclopropane-1-carboxylic acid synthase. Inhibitors of calcium signaling (calcium chelators, La³⁺, Gd³⁺, calmodulin antagonists) and inhibitors of animal purinoceptors suppress the inductive effects of ATP in plants. Because growth zones of plants are regions of high secretory activity and because secretory vesicles contain millimolar levels of ATP that are delivered to the plant extracellular matrix when they fuse with the plasma membrane, extracellular ATP could also play a signaling role during growth of unwounded tissues, and published evidence for this is reviewed and discussed here. Although extracellular nucleotides are well-established agonists in animal cells, the evidence for their role in plants is thus far only indirect. The discovery and characterization of purinoceptors was the breakthrough that confirmed extracellular nucleotides were signaling agents in animals, and a similar identification of ATP-/ADP-responsive receptors in plants will be required to confirm that these agents are extracellular regulators of plant metabolism.