ITPK1 is an InsP 6 /ADP phosphotransferase that controls phosphate signaling in Arabidopsis

In plants, phosphate (P ) homeostasis is regulated by the interaction of PHR transcription factors with stand-alone SPX proteins, which act as sensors for inositol pyrophosphates. In this study, we combined different methods to obtain a comprehensive picture of how inositol (pyro)phosphate metabolis...

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Bibliographic Details
Published in:Molecular plant 2021-11, Vol.14 (11), p.1864
Main Authors: Riemer, Esther, Qiu, Danye, Laha, Debabrata, Harmel, Robert K, Gaugler, Philipp, Gaugler, Verena, Frei, Michael, Hajirezaei, Mohammad-Reza, Laha, Nargis Parvin, Krusenbaum, Lukas, Schneider, Robin, Saiardi, Adolfo, Fiedler, Dorothea, Jessen, Henning J, Schaaf, Gabriel, Giehl, Ricardo F H
Format: Article
Language:English
Subjects:
Adenosine Triphosphatases - metabolism
Arabidopsis - enzymology
Arabidopsis - metabolism
Arabidopsis Proteins - metabolism
Inositol Phosphates - metabolism
Phosphates - metabolism
Phosphotransferases (Alcohol Group Acceptor) - metabolism
Signal Transduction
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Summary:In plants, phosphate (P ) homeostasis is regulated by the interaction of PHR transcription factors with stand-alone SPX proteins, which act as sensors for inositol pyrophosphates. In this study, we combined different methods to obtain a comprehensive picture of how inositol (pyro)phosphate metabolism is regulated by P and dependent on the inositol phosphate kinase ITPK1. We found that inositol pyrophosphates are more responsive to P than lower inositol phosphates, a response conserved across kingdoms. Using the capillary electrophoresis electrospray ionization mass spectrometry (CE-ESI-MS) we could separate different InsP isomers in Arabidopsis and rice, and identify 4/6-InsP and a PP-InsP isomer hitherto not reported in plants. We found that the inositol pyrophosphates 1/3-InsP , 5-InsP , and InsP increase several fold in shoots after P resupply and that tissue-specific accumulation of inositol pyrophosphates relies on ITPK1 activities and MRP5-dependent InsP compartmentalization. Notably, ITPK1 is critical for P -dependent 5-InsP and InsP synthesis in planta and its activity regulates P starvation responses in a PHR-dependent manner. Furthermore, we demonstrated that ITPK1-mediated conversion of InsP to 5-InsP requires high ATP concentrations and that Arabidopsis ITPK1 has an ADP phosphotransferase activity to dephosphorylate specifically 5-InsP under low ATP. Collectively, our study provides new insights into P -dependent changes in nutritional and energetic states with the synthesis of regulatory inositol pyrophosphates.
ISSN:1752-9867