ITPK1 is an InsP6/ADP phosphotransferase that controls phosphate signaling in Arabidopsis
2021
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.
In plants, phosphate (Pᵢ) 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 Pᵢ and dependent on the inositol phosphate kinase ITPK1. We found that inositol pyrophosphates are more responsive to Pᵢ than lower inositol phosphates, a response conserved across kingdoms. Using the capillary electrophoresis electrospray ionization mass spectrometry (CE-ESI-MS) we could separate different InsP₇ isomers in Arabidopsis and rice, and identify 4/6-InsP₇ and a PP-InsP₄ isomer hitherto not reported in plants. We found that the inositol pyrophosphates 1/3-InsP₇, 5-InsP₇, and InsP₈ increase several fold in shoots after Pᵢ resupply and that tissue-specific accumulation of inositol pyrophosphates relies on ITPK1 activities and MRP5-dependent InsP₆ compartmentalization. Notably, ITPK1 is critical for Pᵢ-dependent 5-InsP₇ and InsP₈ synthesis in planta and its activity regulates Pᵢ starvation responses in a PHR-dependent manner. Furthermore, we demonstrated that ITPK1-mediated conversion of InsP₆ to 5-InsP₇ requires high ATP concentrations and that Arabidopsis ITPK1 has an ADP phosphotransferase activity to dephosphorylate specifically 5-InsP₇ under low ATP. Collectively, our study provides new insights into Pᵢ-dependent changes in nutritional and energetic states with the synthesis of regulatory inositol pyrophosphates.
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