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

Summary

Emerging studies have implicated a close link between inositol phosphate (InsP) metabolism and cellular phosphate (P_i) homeostasis in eukaryotes; however, whether a common InsP species is deployed as an evolutionarily conserved metabolic messenger to mediate P_i signaling remains unknown. Here, using genetics and InsP profiling combined with P_i starvation response (PSR) analysis in Arabidopsis 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 P_i homeostasis under P_i-replete conditions, and inositol 1,3,4-trisphosphate 5/6-kinase 1 (ITPK1) plays an equivalent role. Although both ipk1-1 and itpk1 mutants exhibited decreased levels of InsP₆ and diphosphoinositol pentakisphosphate (PP-InsP₅; InsP₇), disruption of another ITPK family enzyme, ITPK4, which correspondingly caused depletion of InsP₆ and InsP₇, did not display similar P_i-related phenotypes, which precludes these InsP species as effectors. Notably, the level of D/L-Ins(3,4,5,6)P₄ was concurrently elevated in both ipk1-1 and itpk1 mutants, which implies a potential role for InsP₄ in regulating P_i homeostasis. However, the level of D/L-Ins(3,4,5,6)P₄ is not responsive to P_i starvation that instead manifests a shoot-specific increase in InsP₇ level. This study demonstrates a more nuanced picture of intersection of InsP metabolism and P_i homeostasis and PSR than has previously been elaborated, and additionally establishes intermediate steps to phytate biosynthesis in plant vegetative tissues.