Arabidopsis inositol phosphate kinases, IPK1 and ITPK1, constitute a metabolic pathway in maintaining phosphate homeostasis

Abstract

SummaryEmerging studies have implicated a close link between inositol phosphate (InsP) metabolism and cellular phosphate (Pi) homeostasis in eukaryotes; however, whether a common InsPspecies is deployed as an evolutionarily conserved metabolic messenger to mediate Pisignaling remains unknown. Here, using genetics and InsPprofiling combined with Pistarvation response (PSR) analysis inArabidopsis thaliana, we showed that the kinase activity of inositol pentakisphosphate 2-kinase (IPK1), an enzyme required for phytate (inositol hexakisphosphates; InsP6) synthesis, is indispensable for maintaining Pihomeostasis under Pi-replete conditions, and inositol 1,3,4-trisphosphate 5/6-kinase 1 (ITPK1) plays an equivalent role. Although bothipk1-1anditpk1mutants exhibited decreased levels of InsP6and diphosphoinositol pentakisphosphate (PP-InsP5; InsP7), disruption of another ITPK family enzyme, ITPK4, which correspondingly caused depletion of InsP6and InsP7, did not display similar Pi-related phenotypes, which precludes these InsPspecies as effectors. Notably, the level of D/L-Ins(3,4,5,6)P4was concurrently elevated in bothipk1-1anditpk1mutants, which implies a potential role for InsP4in regulating Pihomeostasis. However, the level of D/L-Ins(3,4,5,6)P4is not responsive to Pistarvation that instead manifests a shoot-specific increase in InsP7level. This study demonstrates a more nuanced picture of intersection of InsPmetabolism and Pihomeostasis and PSR than has previously been elaborated, and additionally establishes intermediate steps to phytate biosynthesis in plant vegetative tissues.Significance StatementRegulation of phosphate homeostasis and adaptive responses to phosphate limitation is critical for plant growth and crop yield. Accumulating studies implicate inositol phosphates as regulators of phosphate homeostasis in eukaryotes; however, the relationship between inositol phosphate metabolism and phosphate signaling in plants remain elusive. This study dissected the step where inositol phosphate metabolism intersects with phosphate homeostasis regulation and phosphate starvation responses.