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

Article Article scientifique Article Inositol pyrophosphate catabolism by three families of phosphatases regulates plant growth and development eng 2024-11-12 2024-11 author Laurent Florian Structural Plant Biology Laboratory, Department of Plant Sciences, University of Geneva, Geneva, Switzerland. 919363 author Bartsch Simon M 0000-0002-2215-7901 Department of Chemical Biology, Leibniz-Forschungsinstitut für Molekulare Pharmakologie, Berlin, Germany.,Institute of Chemistry, Humboldt-Universität zu Berlin, Berlin, Germany. author Shukla Anuj 0000-0002-4154-689X Institute of Organic Chemistry, University of Freiburg, Freiburg, Germany.,CIBSS-Centre for Integrative Biological Signalling Studies, University of Freiburg, Freiburg, Germany. author Rico Resendiz Félix Edgardo Structural Plant Biology Laboratory, Department of Plant Sciences, University of Geneva, Geneva, Switzerland. 962981 Département des sciences végétales (BIVEG) author Couto Daniel Structural Plant Biology Laboratory, Department of Plant Sciences, University of Geneva, Geneva, Switzerland. 869297 author Fuchs Christelle 0000-0001-8181-2294 Plant Imaging Unit, Department of Plant Sciences, University of Geneva, Geneva, Switzerland. 823460 Département des sciences végétales (BIVEG) author Nicolet Joël Structural Plant Biology Laboratory, Department of Plant Sciences, University of Geneva, Geneva, Switzerland. 114592 Département des sciences végétales (BIVEG) author Loubery Sylvain Philippe 0000-0001-7061-9456 Plant Imaging Unit, Department of Plant Sciences, University of Geneva, Geneva, Switzerland. 669207 Département des sciences végétales (BIVEG) author Jessen Henning J Institute of Organic Chemistry, University of Freiburg, Freiburg, Germany.,CIBSS-Centre for Integrative Biological Signalling Studies, University of Freiburg, Freiburg, Germany. author Fiedler Dorothea Department of Chemical Biology, Leibniz-Forschungsinstitut für Molekulare Pharmakologie, Berlin, Germany.,Institute of Chemistry, Humboldt-Universität zu Berlin, Berlin, Germany. author Hothorn Michael 0000-0002-3597-5698 Structural Plant Biology Laboratory, Department of Plant Sciences, University of Geneva, Geneva, Switzerland. 826130 Département des sciences végétales (BIVEG) e1011468 10.1371/journal.pgen.1011468 39531477 1553-7390 PMC11611267 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. Arabidopsis / genetics Arabidopsis / growth & development Arabidopsis / metabolism Inositol Phosphates / metabolism Phosphoric Monoester Hydrolases / genetics Phosphoric Monoester Hydrolases / metabolism Plant Development / genetics Gene Expression Regulation, Plant Arabidopsis Proteins / genetics Arabidopsis Proteins / metabolism Phosphotransferases (Phosphate Group Acceptor) / genetics Phosphotransferases (Phosphate Group Acceptor) / metabolism Pyrophosphatases / genetics Pyrophosphatases / metabolism Dewey 580 European Commission System-wide discovery and analysis of inositol pyrophosphate signaling networks in plants 818696 INSPIRE EU H2020 Swiss National Science Foundation Illuminating the functions, cellular locations and regulation of inositol pyrophosphate nutrient messengers 209412 CH Programmes 45 Département des sciences végétales 163 false 830 Groupe Hothorn PLOS genetics 20 11 6aeb18fb-a363-43a5-8614-7bb57bcb7a54 Article (Published version) Public Article_scientifique_from_europePmc.pdf 4702767 application/pdf CC BY c1f3aabc3cf3f98ccd31a21eacc522ec39e7dfbfcff3956b47a18d885e541b51 25dad8b6-cb6e-4d9d-92ae-caa7b25611fe Appendix Public pgen.1011468.s011.xlsx 8163 application/vnd.openxmlformats-officedocument.spreadsheetml.sheet 5c8bdc46ba15d005af27789eb7c39497c315ca663e285065ecdc954092419baf 116b4a32-d1b8-4873-acff-a098a60010f2 Appendix Public pgen.1011468.s008.eps 202868 application/postscript 7f80a17d430415d9cf478baa919dccbbcf47f343efe920c2c058244994d1f49c 9a78c3ba-6ce2-4a75-bdec-2bc2680831bf Appendix Public pgen.1011468.s009.eps 1913996 application/postscript 98ec44a5e43cb4ad25145ea83ae555902fcfbfd526138f9774fee03087d28a4e 70e83900-f4d6-4ff8-ab1e-c5a3e87ddf8a Appendix Public pgen.1011468.s012.zip 13445331 application/zip e043147816839ee8627a840b718fef3c0df64d7864768bba2bcd779b736826a7 6ec17486-50f8-456a-84be-8c1d81a600c3 Appendix Public pgen.1011468.s003.eps 55571 application/postscript 7c60468e38400989f90a561d013321219a83ae3d405f5e4541d54bb030169e13 5a9c63c4-08ec-4aca-a472-e6a1c545cae4 Appendix Public pgen.1011468.s013.pdf 759146 application/pdf f19012730291a31d71ac63b1b608dcd85372a62c8cdbfb7d4aadf3e686e103a8 5ffd827c-ea5c-4526-83cc-f1320f5ff36b Appendix Public pgen.1011468.s010.eps 560575 application/postscript 9bdeca89ca401604da882944ddf1931b10870e6ac6e808fc1681ed1dfd03281e f294c999-6d76-4529-b7b5-a6555068bef7 Appendix Public pgen.1011468.s007.eps 80320 application/postscript 42a9194a0b2ca7c8058540fbac88aa22da425423b298ff3af6b7a9c00950d824 dfd9717c-eb39-4f2d-a1f6-8dc70b29008d Appendix Public pgen.1011468.s002.eps 1367127 application/postscript 2bde8c80605e40c6f804a8c6f0ef68de1cdbf1d3da62cb30e73bf6725373c443 08be7f0d-093a-4222-a6cd-d9ae09732bfd Appendix Public pgen.1011468.s006.eps 1684750 application/postscript db26fa0301eacd8cc1ac164d9abbb8983b93772b9592163c75eb2d4c886791a5 0fe31d0b-de61-41ba-9f25-57b5a315aa4d Appendix Public pgen.1011468.s005.eps 149772 application/postscript 15d3fa593b28053ecaecb5a78bd5a3a09d29b5527bb4a0e829482f684ef2d0b5 51c93835-8b5f-4f0d-b4a9-2a4460806934 Appendix Public pgen.1011468.s001.eps 1219185 application/postscript 27cc699234e55aa3d92131be1bb839cf6d5489238d1015945a8f642806815e27 3bca9318-9494-4a24-b38e-db249a16965c Appendix Public pgen.1011468.s004.eps 2384607 application/postscript 13fd7b07eb7a7e029a9f1544e9c88ad4544c44430b80b038f0cc798f94582f31 openAccess Faculté des sciences / Section de biologie / Département des sciences végétales

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