Two inositol hexakisphosphate kinases drive inositol pyrophosphate synthesis in plants

Plant J. 2014 Nov;80(4):642-53. doi: 10.1111/tpj.12669.

Abstract

Inositol pyrophosphates are unique cellular signaling molecules with recently discovered roles in energy sensing and metabolism. Studies in eukaryotes have revealed that these compounds have a rapid turnover, and thus only small amounts accumulate. Inositol pyrophosphates have not been the subject of investigation in plants even though seeds produce large amounts of their precursor, myo-inositol hexakisphosphate (InsP6 ). Here, we report that Arabidopsis and maize InsP6 transporter mutants have elevated levels of inositol pyrophosphates in their seed, providing unequivocal identification of their presence in plant tissues. We also show that plant seeds store a little over 1% of their inositol phosphate pool as InsP7 and InsP8 . Many tissues, including, seed, seedlings, roots and leaves accumulate InsP7 and InsP8 , thus synthesis is not confined to tissues with high InsP6 . We have identified two highly similar Arabidopsis genes, AtVip1 and AtVip2, which are orthologous to the yeast and mammalian VIP kinases. Both AtVip1 and AtVip2 encode proteins capable of restoring InsP7 synthesis in yeast mutants, thus AtVip1 and AtVip2 can function as bonafide InsP6 kinases. AtVip1 and AtVip2 are differentially expressed in plant tissues, suggesting non-redundant or non-overlapping functions in plants. These results contribute to our knowledge of inositol phosphate metabolism and will lay a foundation for understanding the role of InsP7 and InsP8 in plants.

Keywords: Arabidopsis thaliana; At3g01310; At5g15070; InsP6; inositol kinase; inositol pyrophosphate.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Chromatography, High Pressure Liquid
  • Genetic Complementation Test
  • Inositol Phosphates / metabolism*
  • Mutation
  • Phosphotransferases (Alcohol Group Acceptor) / genetics
  • Phosphotransferases (Alcohol Group Acceptor) / metabolism
  • Phosphotransferases (Phosphate Group Acceptor) / genetics
  • Phosphotransferases (Phosphate Group Acceptor) / metabolism*
  • Phylogeny
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Seeds / metabolism*
  • Transcription Factors, General / genetics
  • Transcription Factors, General / metabolism*
  • Yeasts / genetics
  • Zea mays / genetics
  • Zea mays / metabolism

Substances

  • Arabidopsis Proteins
  • Inositol Phosphates
  • Plant Proteins
  • Transcription Factors, General
  • VIP1 protein, Arabidopsis
  • VIP2 protein, Arabidopsis
  • inositol heptakisphosphate
  • inositol-1-pyrophosphate
  • Phosphotransferases (Alcohol Group Acceptor)
  • Phosphotransferases (Phosphate Group Acceptor)
  • VIP1 InsP6 kinase, Arabidopsis
  • VIP2 InsP6 kinase, Arabidopsis
  • inositol hexakisphosphate kinase