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Plant Cell, Vol. 11, 2379-2392, December 1999, Copyright © 1999, American Society of Plant Physiologists

Phosphorylation of Thr-948 at the C Terminus of the Plasma Membrane H+-ATPase Creates a Binding Site for the Regulatory 14-3-3 Protein

Fredrik Svennelida, Anne Olssona, Markus Piotrowskib, Magnus Rosenquista, Cristian Ottmanb, Christer Larssona, Claudia Oeckingb, and Marianne Sommarina
a Department of Plant Biochemistry, Lund University, P.O. Box 117, SE-221 00 Lund, Sweden
b Lehrstuhl für Pflanzenphysiologie, Ruhr-Universität, D-44780 Bochum, Germany

Correspondence to: Anne Olsson, Anne.Olsson{at}plantbio.lu.se (E-mail), 46-462224116 (fax)

The plant plasma membrane H+-ATPase is activated by the binding of 14-3-3 protein to the C-terminal region of the enzyme, thus forming an H+-ATPase–14-3-3 complex that can be stabilized by the fungal toxin fusicoccin. A novel 14-3-3 binding motif, QQXYpT948V, at the C terminus of the H+-ATPase is identified and characterized, and the protein kinase activity in the plasma membrane fraction that phosphorylates this threonine residue in the H+-ATPase is identified. A synthetic peptide that corresponds to the C-terminal 16 amino acids of the H+-ATPase and that is phosphorylated on Thr-948 prevents the in vitro activation of the H+-ATPase that is obtained in the presence of recombinant 14-3-3 and fusicoccin. Furthermore, binding of 14-3-3 to the H+-ATPase in the absence of fusicoccin is absolutely dependent on the phosphorylation of Thr-948, whereas binding of 14-3-3 in the presence of fusicoccin occurs independently of phosphorylation but still involves the C-terminal motif YTV. Finally, by complementing yeast that lacks its endogenous H+-ATPase with wild-type and mutant forms of the Nicotiana plumbaginifolia H+-ATPase isoform PMA2, we provide physiological evidence for the importance of the phosphothreonine motif in 14-3-3 binding and, hence, in the activation of the H+-ATPase in vivo. Indeed, replacing Thr-948 in the plant H+-ATPase with alanine is lethal because this mutant fails to functionally replace the yeast H+-ATPase. Considering the importance of the motif QQXYpTV for 14-3-3 binding and yeast growth, this motif should be of vital importance for regulating H+-ATPase activity in the plant and thus for plant growth.




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