The plastidial glucan, water dikinase (GWD) catalyses multiple phosphotransfer reactions

FEBS J. 2012 Jun;279(11):1953-66. doi: 10.1111/j.1742-4658.2012.08576.x. Epub 2012 Apr 25.

Abstract

The plant genome encodes at least two distinct and evolutionary conserved plastidial starch-related dikinases that phosphorylate a low percentage of glucosyl residues at the starch granule surface. Esterification of starch favours the transition of highly ordered α-glucans to a less ordered state and thereby facilitates the cleavage of interglucose bonds by hydrolases. Metabolically most important is the phosphorylation at position C6, which is catalysed by the glucan, water dikinase (GWD). The reactions mediated by recombinant wild-type GWD from Arabidopsis thaliana (AtGWD) and from Solanum tuberosum (StGWD) were studied. Two mutated proteins lacking the conserved histidine residue that is indispensible for glucan phosphorylation were also included. The wild-type GWDs consume approximately 20% more ATP than is required for glucan phosphorylation. Similarly, although incapable of phosphorylating α-glucans, the two mutated dikinase proteins are capable of degrading ATP. Thus, consumption of ATP and phosphorylation of α-glucans are not strictly coupled processes but, to some extent, occur as independent phosphotransfer reactions. As revealed by incubation of the GWDs with [γ-(33) P]ATP, the consumption of ATP includes the transfer of the γ-phosphate group to the GWD protein but this autophosphorylation does not require the conserved histidine residue. Thus, the GWD proteins possess two vicinal phosphorylation sites, both of which are transiently phosphorylated. Following autophosphorylation at both sites, native dikinases flexibly use various terminal phosphate acceptors, such as water, α-glucans, AMP and ADP. A model is presented describing the complex phosphotransfer reactions of GWDs as affected by the availability of the various acceptors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Diphosphate / metabolism
  • Adenosine Monophosphate / metabolism
  • Adenosine Triphosphate / metabolism
  • Arabidopsis / enzymology*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Biocatalysis
  • Glucans / metabolism*
  • Histidine / metabolism
  • Kinetics
  • Phosphorylation
  • Phosphotransferases (Paired Acceptors) / genetics
  • Phosphotransferases (Paired Acceptors) / metabolism*
  • Plastids / enzymology*
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Solanum tuberosum / enzymology*
  • Water / metabolism

Substances

  • Arabidopsis Proteins
  • Glucans
  • Recombinant Proteins
  • Water
  • Adenosine Monophosphate
  • Histidine
  • Adenosine Diphosphate
  • Adenosine Triphosphate
  • Phosphotransferases (Paired Acceptors)
  • alpha-glucan, water dikinase, Arabidopsis
  • alpha-glucan, water dikinase, Solanum tuberosum