Pullagurla Naga Jyothi, Shome Supritam, Liu Guizhen, Jessen Henning J, Laha Debabrata
Department of Biochemistry, Division of Biological Sciences, Indian Institute of Science (IISc), Bengaluru 560012, India.
Institute of Organic Chemistry & CIBSS-Centre for Integrative Biological Signalling Studies, University of Freiburg, Freiburg 79104, Germany.
Plant Physiol. 2025 Feb 7;197(2). doi: 10.1093/plphys/kiae454.
Land plants have evolved sophisticated sensing mechanisms and signaling pathways to adapt to phosphate-limited environments. While molecular players contributing to these adaptations in flowering plants have been described, how nonvascular bryophytes regulate phosphate (Pi) homeostasis remained largely unknown. In this study, we present findings that both male and female plants of the liverwort Marchantia polymorpha respond to altered phosphate availability through substantial developmental changes. We show that the second messenger inositol pyrophosphates (PP-InsPs) respond more quickly to changes in cellular Pi status than the lower inositol phosphates, highlighting a functional relationship between PP-InsP and Pi homeostasis in M. polymorpha. To further corroborate the possible involvement of PP-InsP in Pi homeostasis, we characterized M. polymorpha INOSITOL (1,3,4) TRIPHOSPHATE 5/6 KINASE1 (MpITPK1) that phosphorylates InsP6 to generate InsP7 both in vitro and in vivo. Consistent with the role of PP-InsPs in Pi homeostasis, M. polymorpha lines with enhanced MpITPK1 expression leading to the accumulation of 5-InsP7 and an InsP8 isomer, exhibit altered expression of phosphate starvation induced (PSI) genes and display attenuated responses to low phosphate. The characterization of MpPHO1-deficient plants with dramatically increased levels of 1,5-InsP8 further supports the role of PP-InsP in Pi homeostasis in this liverwort species. Notably, our study unveiled that MpITPK1 rescues the deregulated Pi homeostasis in Arabidopsis (Arabidopsis thaliana) ITPK1-deficient plants, suggesting that liverwort and eudicots share a functional ITPK1 homolog. In summary, our study provides insights into the regulation of Pi homeostasis by ITPK1-derived PP-InsPs in M. polymorpha.
陆地植物已经进化出复杂的感知机制和信号通路，以适应磷酸盐有限的环境。虽然已经描述了开花植物中促成这些适应性的分子成分，但非维管苔藓植物如何调节磷酸盐（Pi）稳态在很大程度上仍然未知。在这项研究中，我们展示了地钱多形苔（Marchantia polymorpha）的雄株和雌株都通过显著的发育变化来响应磷酸盐可利用性的改变。我们表明，第二信使肌醇焦磷酸（PP-InsPs）比低肌醇磷酸更快地响应细胞内Pi状态的变化，突出了PP-InsP与多形苔Pi稳态之间的功能关系。为了进一步证实PP-InsP可能参与Pi稳态，我们鉴定了多形苔肌醇（1,3,4）三磷酸5/6激酶1（MpITPK1），其在体外和体内都能将InsP6磷酸化生成InsP7。与PP-InsPs在Pi稳态中的作用一致，MpITPK1表达增强导致5-InsP7和一种InsP8异构体积累的多形苔株系，表现出磷酸盐饥饿诱导（PSI）基因表达的改变，并对低磷酸盐表现出减弱的反应。MpPHO1缺陷型植物中1,5-InsP8水平显著增加的特征进一步支持了PP-InsP在这种苔类植物Pi稳态中的作用。值得注意的是，我们的研究揭示MpITPK1拯救了拟南芥（Arabidopsis thaliana）ITPK1缺陷型植物中失调的Pi稳态，表明苔类植物和真双子叶植物共享一个功能性的ITPK1同源物。总之，我们的研究为ITPK1衍生的PP-InsPs在多形苔中调节Pi稳态提供了见解。
