Regulation of Plant Growth and Development by Extracellular Nucleotides - Communication in Plants: Neuronal Aspects of Plant Life - page 221

15 Regulation of Plant Growth

and Development
by Extracellular Nucleotides

Stanley J. Roux, Charlotte Song, Collene Jeter

Abstract 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. How-
ever, recent findings, first in animals and then in plants, indicate that ATP and ADP can have
significantrolesoutsidetheplasmamembraneasagoniststhatdonothavetobehydrolyzed
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 produc-
tion 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, La 3+ ,Gd 3+ , 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 millimo-
lar 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 un-
wounded 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.

15.1
Introduction
Although most biologists think of ATP as the principal energy currency of
the cell, functioning entirely inside of cells, there is a significant literature
documenting an extracellular function of ATP as an agonist that does not
have to be hydrolyzed to activate responses in cells (Burnstock and Knight
2004). This literature originally was restricted to studies of animal cells,
where adenine nucleoside triphosphate and diphosphate mediate a wide
variety of biological processes in the extracellular matrix (ECM) at special-
ized receptors known as P2 purinoceptors. The main types of these multi-
gene family receptors in animals are P2X, 2-pass transmembrane (TM)
subunits which oligomerize to form ligand-gated ion channels, and P2Y,