The plant plasma membrane proton pump ATPase: a highly regulated P-type ATPase with multiple physiological roles

Abstract

Around 40 P-type ATPases have been identified in Arabidopsis and rice, for which the genomes are known. None seems to exchange sodium and potassium, as does the animal Na(+)/K(+)-ATPase. Instead, plants, together with fungi, possess a proton pumping ATPase (H(+)-ATPase), which couples ATP hydrolysis to proton transport out of the cell, and so establishes an electrochemical gradient across the plasma membrane, which is dissipated by secondary transporters using protons in symport or antiport, as sodium is used in animal cells. Additional functions, such as stomata opening, cell growth, and intracellular pH homeostasis, have been proposed. Crystallographic data and homology modeling suggest that the H(+)-ATPase has a broadly similar structure to the other P-type ATPases but has an extended C-terminal region, which is involved in enzyme regulation. Phosphorylation of the penultimate residue, a Thr, and the subsequent binding of regulatory 14-3-3 proteins result in the formation of a dodecamer (six H(+)-ATPase and six 14-3-3 molecules) and enzyme activation. This type of regulation is unique to the P-type ATPase family. However, the recent identification of additional phosphorylated residues suggests further regulatory features.

Phytosulfokine Regulates Growth in Arabidopsis through a Response Module at the Plasma Membrane That Includes CYCLIC NUCLEOTIDE-GATED CHANNEL17, H+-ATPase, and BAK1

“…Irreversible cell growth further depends on altered cell wall properties that allow for controlled yielding of the cell wall. Acidification of the apoplast via activation of the P-type PM-localized H + -ATPase (termed AHA in Arabidopsis) by auxin (Duby and Boutry, 2009) or brassinosteroids (Caesar et al, 2011) activates cell wall loosening protein activities that allow for cell expansion commonly referred to as acid growth. Apoplast acidification also changes the ion equilibrium across the PM, favoring cation influx.…”

Cytosolic Nucleotides Block and Regulate the Arabidopsis Vacuolar Anion Channel AtALMT9

“…Indeed, during stomatal opening AtALMT9 drives the influx of anions into the vacuole. The influx of anion via AtALMT9 is driven by hyperpolarized vacuolar membrane potentials that are maintained through H ϩ -ATPases (27)(28)(29). During stomatal opening the high hydrolytic activity of the proton pump consumes ATP, decreasing its concentration in the cytosol.…”

A Phosphorylation in the C-terminal Auto-inhibitory Domain of the Plant Plasma Membrane H+-ATPase Activates the Enzyme with No Requirement for Regulatory 14-3-3 Proteins

“…Recently, several studies in Arabidopsis thaliana, O. sativa, and N. plumbaginifolia have led to the identification of new phosphorylation sites in the C-terminal region of the H ϩ -ATPase (for review, see Ref,1). Two of these, corresponding to PMA2 Thr-931 (14) and to PMA2 Ser-938 (14) or AHA2 931 (15), have been shown to negatively regulate the enzyme by impairing the binding of 14-3-3 proteins.…”

“…The H ϩ -ATPase is thus involved in many physiological roles, such as solute transport inside the cell and in the plant, cell pH homeostasis and elongation, stomatal opening, and salt stress tolerance. Because of the key role of this enzyme in plant cell function, multiple mechanisms have evolved to regulate H ϩ -ATPase expression and activity (1,2). The H ϩ -ATPase is encoded by a family of ϳ10 genes (3,4).…”