Understanding the physiological role of ITPK1-type inositol phosphate kinase in embryophytes

Abstract

Land plants have evolved sophisticated mechanisms to adapt to phosphate (Pi) limitation, yet such regulatory networks in nonvascular bryophytes remain poorly understood. Here, we show that both male and female liverworts (Marchantia polymorpha) undergo developmental changes in response to Pi availability. Inositol pyrophosphates (PP-InsPs), acting as second messengers, respond more rapidly to cellular Pi fluctuations than lower inositol phosphates, underscoring their critical role in Pi homeostasis. To dissect this link, we characterized the kinase INOSITOL (1,3,4) TRIPHOSPHATE 5/6 KINASE1 (MpITPK1), which phosphorylates InsP₆ to generate InsP₇ both in vitro and in vivo. Consistent with the regulatory role of PP-InsPs in Pi homeostasis, M. polymorpha lines overexpressing MpITPK1 exhibited elevated levels of 5-InsP₇ and an InsP₈ isomer, altered phosphate starvation-induced gene expression, and reduced sensitivity to Pi deficiency. Importantly, MpITPK1 complemented the Arabidopsis thaliana itpk1 mutant associated phenotype, highlighting an evolutionarily conserved function of ITPK1 and its role in Pi regulatory module. Beyond Pi regulation, we also establish a role for ITPK1 and its dependent PP-InsPs in jasmonic acid (JA) signaling. We demonstrate that ITPK1 regulates jasmonic acid (JA)-dependent developmental processes. ITPK1-deficient plants exhibited enhanced root growth inhibition and increased lateral root density upon JA treatment, without changes in ITPK1 protein abundance or JA biosynthetic gene expression. Instead, genes encoding JAZ repressor proteins were markedly down-regulated in itpk1 plants, linking ITPK1 activity to JA-responsive transcriptional regulation. Together, our findings establish ITPK1-derived PP-InsPs as versatile signaling molecules that integrate nutrient availability with JA mediated developmental and stress responses in land plants.