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Ca(2+)-dependent phosphorylation of NRAMP1 by CPK21 and CPK23 facilitates manganese uptake and homeostasis in Arabidopsis
Homeostasis of the essential micronutrient manganese (Mn) is crucially determined through availability and uptake efficiency in all organisms. Mn deficiency of plants especially occurs in alkaline and calcareous soils, seriously restricting crop yield. However, the mechanisms underlying the sensing...
Autores principales: | , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9546541/ https://www.ncbi.nlm.nih.gov/pubmed/36161952 http://dx.doi.org/10.1073/pnas.2204574119 |
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author | Fu, Dali Zhang, Zhenqian Wallrad, Lukas Wang, Zhangqing Höller, Stefanie Ju, ChuanFeng Schmitz-Thom, Ina Huang, Panpan Wang, Lei Peiter, Edgar Kudla, Jörg Wang, Cun |
author_facet | Fu, Dali Zhang, Zhenqian Wallrad, Lukas Wang, Zhangqing Höller, Stefanie Ju, ChuanFeng Schmitz-Thom, Ina Huang, Panpan Wang, Lei Peiter, Edgar Kudla, Jörg Wang, Cun |
author_sort | Fu, Dali |
collection | PubMed |
description | Homeostasis of the essential micronutrient manganese (Mn) is crucially determined through availability and uptake efficiency in all organisms. Mn deficiency of plants especially occurs in alkaline and calcareous soils, seriously restricting crop yield. However, the mechanisms underlying the sensing and signaling of Mn availability and conferring regulation of Mn uptake await elucidation. Here, we uncover that Mn depletion triggers spatiotemporally defined long-lasting Ca(2+) oscillations in Arabidopsis roots. These Ca(2+) signals initiate in individual cells, expand, and intensify intercellularly to transform into higher-order multicellular oscillations. Furthermore, through an interaction screen we identified the Ca(2+)-dependent protein kinases CPK21 and CPK23 as Ca(2+) signal-decoding components that bring about translation of these signals into regulation of uptake activity of the high-affinity Mn transporter natural resistance associated macrophage proteins 1 (NRAMP1). Accordingly, a cpk21/23 double mutant displays impaired growth and root development under Mn-limiting conditions, while kinase overexpression confers enhanced tolerance to low Mn supply to plants. In addition, we define Thr498 phosphorylation within NRAMP1 as a pivot mechanistically determining NRAMP1 activity, as revealed by biochemical assays and complementation of yeast Mn uptake and Arabidopsis nramp1 mutants. Collectively, these findings delineate the Ca(2+)-CPK21/23-NRAMP1 axis as key for mounting plant Mn homeostasis. |
format | Online Article Text |
id | pubmed-9546541 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-95465412023-03-26 Ca(2+)-dependent phosphorylation of NRAMP1 by CPK21 and CPK23 facilitates manganese uptake and homeostasis in Arabidopsis Fu, Dali Zhang, Zhenqian Wallrad, Lukas Wang, Zhangqing Höller, Stefanie Ju, ChuanFeng Schmitz-Thom, Ina Huang, Panpan Wang, Lei Peiter, Edgar Kudla, Jörg Wang, Cun Proc Natl Acad Sci U S A Biological Sciences Homeostasis of the essential micronutrient manganese (Mn) is crucially determined through availability and uptake efficiency in all organisms. Mn deficiency of plants especially occurs in alkaline and calcareous soils, seriously restricting crop yield. However, the mechanisms underlying the sensing and signaling of Mn availability and conferring regulation of Mn uptake await elucidation. Here, we uncover that Mn depletion triggers spatiotemporally defined long-lasting Ca(2+) oscillations in Arabidopsis roots. These Ca(2+) signals initiate in individual cells, expand, and intensify intercellularly to transform into higher-order multicellular oscillations. Furthermore, through an interaction screen we identified the Ca(2+)-dependent protein kinases CPK21 and CPK23 as Ca(2+) signal-decoding components that bring about translation of these signals into regulation of uptake activity of the high-affinity Mn transporter natural resistance associated macrophage proteins 1 (NRAMP1). Accordingly, a cpk21/23 double mutant displays impaired growth and root development under Mn-limiting conditions, while kinase overexpression confers enhanced tolerance to low Mn supply to plants. In addition, we define Thr498 phosphorylation within NRAMP1 as a pivot mechanistically determining NRAMP1 activity, as revealed by biochemical assays and complementation of yeast Mn uptake and Arabidopsis nramp1 mutants. Collectively, these findings delineate the Ca(2+)-CPK21/23-NRAMP1 axis as key for mounting plant Mn homeostasis. National Academy of Sciences 2022-09-26 2022-10-04 /pmc/articles/PMC9546541/ /pubmed/36161952 http://dx.doi.org/10.1073/pnas.2204574119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | Biological Sciences Fu, Dali Zhang, Zhenqian Wallrad, Lukas Wang, Zhangqing Höller, Stefanie Ju, ChuanFeng Schmitz-Thom, Ina Huang, Panpan Wang, Lei Peiter, Edgar Kudla, Jörg Wang, Cun Ca(2+)-dependent phosphorylation of NRAMP1 by CPK21 and CPK23 facilitates manganese uptake and homeostasis in Arabidopsis |
title | Ca(2+)-dependent phosphorylation of NRAMP1 by CPK21 and CPK23 facilitates manganese uptake and homeostasis in Arabidopsis |
title_full | Ca(2+)-dependent phosphorylation of NRAMP1 by CPK21 and CPK23 facilitates manganese uptake and homeostasis in Arabidopsis |
title_fullStr | Ca(2+)-dependent phosphorylation of NRAMP1 by CPK21 and CPK23 facilitates manganese uptake and homeostasis in Arabidopsis |
title_full_unstemmed | Ca(2+)-dependent phosphorylation of NRAMP1 by CPK21 and CPK23 facilitates manganese uptake and homeostasis in Arabidopsis |
title_short | Ca(2+)-dependent phosphorylation of NRAMP1 by CPK21 and CPK23 facilitates manganese uptake and homeostasis in Arabidopsis |
title_sort | ca(2+)-dependent phosphorylation of nramp1 by cpk21 and cpk23 facilitates manganese uptake and homeostasis in arabidopsis |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9546541/ https://www.ncbi.nlm.nih.gov/pubmed/36161952 http://dx.doi.org/10.1073/pnas.2204574119 |
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