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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...

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Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
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.
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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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