Submitted to: Plant Journal
Publication Type: Peer reviewed journal
Publication Acceptance Date: 8/27/2014
Publication Date: 9/7/2014
Citation: Desai, M., Rangarajan, P., Donahue, J.X., Williams, S.P., Land, E.S., Mandal, M.K., Phillippy, B.Q., Perera, I., Raboy, V., Gillaspy, G.E. 2014. Two inositol hexakisphosphate kinases drive inositol pyrophosphate synthesis in plants. Plant Journal. 80(4):642-653. Interpretive Summary: Plants possess mechanisms to sense their environment and if needed respond to environmental stresses such as drought, heat or cold and nutrient deficiencies, referred together as “abiotic stresses”. An important component of this “sensing/signaling” machinery involves a class of compounds called “inositol phosphates”. When plant cells sense that they are in trouble, they synthesize these compounds which then function as signals to the plant that it needs to adapt and respond to the stress it is experiencing. The work described in this research article, conducted as an NSF-funded collaboration between the scientists in the USDA-ARS and two Universities, North Carolina State University and Virginia Tech, identifies for the first time in studies of plants a new and important sub-class of inositol phosphates called “inositol pyrophosphates”. These compounds are believed to be critically important to how plants sense and respond to their environment, but before this work had not yet been observed or studied in plants. Therefore this work establishes a base to support future studies of inositol pyrophosphates in plants and their role in the important process of “abiotic stress response”.
Technical Abstract: Inositol pyrophosphates are novel cellular signaling molecules with newly discovered roles in energy sensing and metabolic control. Studies in eukaryotes have revealed that these compounds turn over rapidly, 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 the first 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 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 signaling in plants and will lay a foundation for understanding the energy signaling role of InsP7 and InsP8.