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Inositol Trisphosphate Kinase and Diphosphoinositol Pentakisphosphate Kinase Enzymes Constitute the Inositol Pyrophosphate Synthesis Pathway in Plants

Olusegun Adepoju, Sarah P. Williams, Branch Craige, Caitlin A. Cridland, Amanda K. Sharpe, Anne M. Brown, Eric Land, Imara Y. Perera, Didier Mena, Pablo Sobrado, View ORCID ProfileGlenda E. Gillaspy
doi: https://doi.org/10.1101/724914
Olusegun Adepoju
1Department of Biochemistry, Virginia Tech, Blacksburg, VA
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Sarah P. Williams
2Department of Biology, College of William and Mary, Williamsburg, VA
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Branch Craige
1Department of Biochemistry, Virginia Tech, Blacksburg, VA
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Caitlin A. Cridland
1Department of Biochemistry, Virginia Tech, Blacksburg, VA
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Amanda K. Sharpe
1Department of Biochemistry, Virginia Tech, Blacksburg, VA
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Anne M. Brown
1Department of Biochemistry, Virginia Tech, Blacksburg, VA
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Eric Land
3Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC
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Imara Y. Perera
3Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC
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Didier Mena
1Department of Biochemistry, Virginia Tech, Blacksburg, VA
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Pablo Sobrado
1Department of Biochemistry, Virginia Tech, Blacksburg, VA
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Glenda E. Gillaspy
1Department of Biochemistry, Virginia Tech, Blacksburg, VA
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  • ORCID record for Glenda E. Gillaspy
  • For correspondence: gillaspy@vt.edu
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ABSTRACT

Inositol pyrophosphates (PP-InsPs) are an emerging class of “high-energy” intracellular signaling molecules containing one or two diphosphate groups attached to an inositol ring, with suggested roles in bioenergetic homeostasis and inorganic phosphate (Pi) sensing. Information regarding the biosynthesis of these unique class of signaling molecules in plants is scarce, however the enzymes responsible for their biosynthesis in other eukaryotes have been well described. Here we report the characterization of the two Arabidopsis VIP kinase domains, a newly discovered activity of the Arabidopsis ITPK1 and ITPK2 enzymes, and the subcellular localization of the enzymes involved in the synthesis of InsP6 and PP-InsPs. Our data indicate that AtVIP1-KD and AtVIP2-KD act primarily as 1PP-specific Diphosphoinositol Pentakisphosphate Kinases (PPIP5) Kinases. The AtITPK enzymes, in contrast, can function as InsP6 kinases, and thus are the missing enzyme in the plant PP-InsP synthesis pathway. Together, these enzyme classes can function in plants to produce PP-InsPs, which have been implicated in signal transduction and Pi sensing pathways. We measured a higher InsP7 level (increased InsP7/InsP8 ratio) in vip1/vip2 double loss-of-function mutants, and an accumulation of InsP8 (decreased InsP7/InsP8 ratio) in the 35S:VIP2 overexpression line relative to wild-type plants. We also report that enzymes involved in the synthesis of InsPs and PP-InsPs accumulate within the nucleus and cytoplasm of plant cells. Our work defines a molecular basis for understanding how plants synthesize PP-InsPs which is crucial for determining the roles of these signaling molecules in processes such as Pi sensing.

SIGNIFICANCE STATEMENT Inositol pyrophosphate signaling molecules are of agronomic importance as they can control complex responses to the limited nutrient, phosphate. This work fills in the missing steps in the inositol pyrophosphate synthesis pathway and points to a role for these molecules in the plant cell nucleus. This is an important advance that can help us design future strategies to increase phosphate efficiency in plants.

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Posted August 05, 2019.
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Inositol Trisphosphate Kinase and Diphosphoinositol Pentakisphosphate Kinase Enzymes Constitute the Inositol Pyrophosphate Synthesis Pathway in Plants
Olusegun Adepoju, Sarah P. Williams, Branch Craige, Caitlin A. Cridland, Amanda K. Sharpe, Anne M. Brown, Eric Land, Imara Y. Perera, Didier Mena, Pablo Sobrado, Glenda E. Gillaspy
bioRxiv 724914; doi: https://doi.org/10.1101/724914
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Inositol Trisphosphate Kinase and Diphosphoinositol Pentakisphosphate Kinase Enzymes Constitute the Inositol Pyrophosphate Synthesis Pathway in Plants
Olusegun Adepoju, Sarah P. Williams, Branch Craige, Caitlin A. Cridland, Amanda K. Sharpe, Anne M. Brown, Eric Land, Imara Y. Perera, Didier Mena, Pablo Sobrado, Glenda E. Gillaspy
bioRxiv 724914; doi: https://doi.org/10.1101/724914

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