Inositol pyrophosphate catabolism by three families of phosphatases regulates plant growth and development

• DOI: 10.1371/journal.pgen.1011468
• Publication Date: 2024-11-12T18:37:47Z
• Authors: Florian Laurent; Simon M. Bartsch; Anuj Shukla; Felix Rico-Resendiz; Daniel Couto; Christelle Fuchs; Joël Nicolet; Sylvain Loubéry; Henning J. Jessen; Dorothea Fiedler; Michael Hothorn
• Keywords: 580; 570; 0303 health sciences; Pyrophosphatases / metabolism; Plant Development / genetics; Phosphotransferases (Phosphate Group Acceptor) / metabolism; info:eu-repo/classification/ddc/580; Phosphoric Monoester Hydrolases / metabolism; 547; Phosphoric Monoester Hydrolases / genetics; Arabidopsis Proteins / metabolism; QH426-470; Pyrophosphatases / genetics; 03 medical and health sciences; Arabidopsis / genetics; Arabidopsis Proteins / genetics; Gene Expression Regulation, Plant; Genetics; Phosphotransferases (Phosphate Group Acceptor) / genetics; Arabidopsis / growth & development; Arabidopsis / metabolism; Inositol Phosphates / metabolism; Research Article

Inositol pyrophosphates (PP-InsPs) are nutrient messengers whose cellular levels are precisely regulated. Diphosphoinositol pentakisphosphate kinases (PPIP5Ks) generate the active signaling molecule 1,5-InsP8. PPIP5Ks harbor phosphatase domains that hydrolyze PP-InsPs. Plant and Fungi Atypical Dual Specificity Phosphatases (PFA-DSPs) and NUDIX phosphatases (NUDTs) are also involved in PP-InsP degradation. Here, we analyze the relative contributions of the three different phosphatase families to plant PP-InsP catabolism. We report the biochemical characterization of inositol pyrophosphate phosphatases from Arabidopsis and Marchantia polymorpha. Overexpression of different PFA-DSP and NUDT enzymes affects PP-InsP levels and leads to stunted growth phenotypes in Arabidopsis. nudt17/18/21 knock-out mutants have altered PP-InsP pools and gene expression patterns, but no apparent growth defects. In contrast, Marchantia polymorpha Mppfa-dsp1ge, Mpnudt1ge and Mpvip1ge mutants display severe growth and developmental phenotypes and associated changes in cellular PP-InsP levels. Analysis of Mppfa-dsp1geand Mpvip1ge mutants supports a role for PP-InsPs in Marchantia phosphate signaling, and additional functions in nitrate homeostasis and cell wall biogenesis. Simultaneous elimination of two phosphatase activities enhanced the observed growth phenotypes. Taken together, PPIP5K, PFA-DSP and NUDT inositol pyrophosphate phosphatases regulate growth and development by collectively shaping plant PP-InsP pools.