ORCID IDs: 0000-0002-7823-5489 (D.L.); 0000-0002-4512-9508 (P.J.); 0000-0002-1025-9484 (H.J.J.); 0000-0001-9022-4515 (G.S.)Diphosphorylated inositol polyphosphates, also referred to as inositol pyrophosphates, are important signaling molecules that regulate critical cellular activities in many eukaryotic organisms, such as membrane trafficking, telomere maintenance, ribosome biogenesis, and apoptosis. In mammals and fungi, two distinct classes of inositol phosphate kinases mediate biosynthesis of inositol pyrophosphates: Kcs1/IP6K-and Vip1/PPIP5K-like proteins. Here, we report that PPIP5K homologs are widely distributed in plants and that Arabidopsis thaliana VIH1 and VIH2 are functional PPIP5K enzymes. We show a specific induction of inositol pyrophosphate InsP 8 by jasmonate and demonstrate that steady state and jasmonate-induced pools of InsP 8 in Arabidopsis seedlings depend on VIH2. We identify a role of VIH2 in regulating jasmonate perception and plant defenses against herbivorous insects and necrotrophic fungi. In silico docking experiments and radioligand binding-based reconstitution assays show highaffinity binding of inositol pyrophosphates to the F-box protein COI1-JAZ jasmonate coreceptor complex and suggest that coincidence detection of jasmonate and InsP 8 by COI1-JAZ is a critical component in jasmonate-regulated defenses.
In plants, phosphate (P i ) 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 i and dependent on the inositol phosphate kinase ITPK1. We found that inositol pyrophosphates are more responsive to P i 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 7 isomers in Arabidopsis and rice, and identify 4/6-InsP 7 and a PP-InsP 4 isomer hitherto not reported in plants. We found that the inositol pyrophosphates 1/3-InsP 7 , 5-InsP 7 , and InsP 8 increase several fold in shoots after P i resupply and that tissue-specific accumulation of inositol pyrophosphates relies on ITPK1 activities and MRP5-dependent InsP 6 compartmentalization. Notably, ITPK1 is critical for P i -dependent 5-InsP 7 and InsP 8 synthesis in planta and its activity regulates P i starvation responses in a PHRdependent manner. Furthermore, we demonstrated that ITPK1-mediated conversion of InsP 6 to 5-InsP 7 requires high ATP concentrations and that Arabidopsis ITPK1 has an ADP phosphotransferase activity to dephosphorylate specifically 5-InsP 7 under low ATP. Collectively, our study provides new insights into P i -dependent changes in nutritional and energetic states with the synthesis of regulatory inositol pyrophosphates.
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