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Biochemical Properties and Physiological Roles of Plant Inositol Hexakisphosphate Kinases

Subject Area Plant Physiology
Term from 2017 to 2023
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 361089095
 
Final Report Year 2023

Final Report Abstract

Inositol pyrophosphates are high-energy molecular messengers that regulate several cellular processes in eukaryotes. While inositol pyrophosphates InsP7 and InsP8 are present in different plant species, both the identity of enzymes responsible for InsP7 synthesis and the isomer identity of plant InsP7 remained unknown at the onset of this DFG proposal. In the initial phase of the project, we developed and optimized various methods to analyze inositol poly- and pyrophosphates, mostly in collaboration with the labs of Henning Jessen and Adolfo Saiardi. The employment of those methods led to a number of findings, including the identification of the bacterial effector XopH as a 1-phytase, the discovery of novel inositol pyrophosphate phosphatases, and the identification of previously undetected 4/6-InsP7 and a PP-InsP4 isomer in plants. We also contributed to a study by the Hothorn lab showing that VIH1/2 are bifunctional enzymes able to generate and break-down inositol pyrophosphates, and that InsP8 serves as a proxy for intracellular P. The main focus of our activities was on characterizing ITPK1 and ITPK2, previously shown by us to catalyze in vitro the phosphorylation of phytic acid (InsP6) to the symmetric 5-InsP7 isomer. We discovered an important role of these enzymes in phosphate signaling and found that InsP8 is very responsive to the plant P status and that its synthesis critically depends on ITPK1. Importantly, ITPK1 can work in both directions, i.e. as a kinase to generate 5-InsP7 (thus allowing InsP8 synthesis) and as a phosphotransferase to deplete cellular 5-InsP7 and to locally produce ATP thereby functioning as an energy sensor regulating phosphate starvation responses. In a follow-up study, we discovered a critical role of ITPK1 also in auxin-related processes, including primary root elongation, root hair development, leaf venation, thermomorphogenic and gravitropic responses, and sensitivity to exogenously applied auxin. We further found that a recombinant auxin receptor complex binds to anionic inositol polyphosphates with high affinity and identified a physical interaction between ITPK1 and the auxin receptor component TIR1, suggesting a localized production of ITPK1-dependent 5-InsP7 to activate auxin signaling. Finally, we contributed to mostly collaborative projects investigating lipid-dependent processes upstream of inositol polyphosphate synthesis, in particular work on SEC14-type phospholipid transfer proteins in yeast and plants, as well as on phospholipase C-dependent regulation of lateral root initiation and ABA responses during seed germination and stomatal closure.

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