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Salt-induced subcellular kinase relocation and seedling susceptibility caused by overexpression of Medicago SIMKK in Arabidopsis

Dual-specificity mitogen-activated protein kinases kinases (MAPKKs) are the immediate upstream activators of MAPKs. They simultaneously phosphorylate the TXY motif within the activation loop of MAPKs, allowing them to interact with and regulate multiple substrates. Often, the activation of MAPKs tri...

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Autores principales: Ovečka, Miroslav, Takáč, Tomáš, Komis, George, Vadovič, Pavol, Bekešová, Slávka, Doskočilová, Anna, Smékalová, Veronika, Luptovčiak, Ivan, Šamajová, Olga, Schweighofer, Alois, Meskiene, Irute, Jonak, Claudia, Křenek, Pavel, Lichtscheidl, Irene, Škultéty, Ľudovít, Hirt, Heribert, Šamaj, Jozef
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4036504/
https://www.ncbi.nlm.nih.gov/pubmed/24648569
http://dx.doi.org/10.1093/jxb/eru115
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author Ovečka, Miroslav
Takáč, Tomáš
Komis, George
Vadovič, Pavol
Bekešová, Slávka
Doskočilová, Anna
Smékalová, Veronika
Luptovčiak, Ivan
Šamajová, Olga
Schweighofer, Alois
Meskiene, Irute
Jonak, Claudia
Křenek, Pavel
Lichtscheidl, Irene
Škultéty, Ľudovít
Hirt, Heribert
Šamaj, Jozef
author_facet Ovečka, Miroslav
Takáč, Tomáš
Komis, George
Vadovič, Pavol
Bekešová, Slávka
Doskočilová, Anna
Smékalová, Veronika
Luptovčiak, Ivan
Šamajová, Olga
Schweighofer, Alois
Meskiene, Irute
Jonak, Claudia
Křenek, Pavel
Lichtscheidl, Irene
Škultéty, Ľudovít
Hirt, Heribert
Šamaj, Jozef
author_sort Ovečka, Miroslav
collection PubMed
description Dual-specificity mitogen-activated protein kinases kinases (MAPKKs) are the immediate upstream activators of MAPKs. They simultaneously phosphorylate the TXY motif within the activation loop of MAPKs, allowing them to interact with and regulate multiple substrates. Often, the activation of MAPKs triggers their nuclear translocation. However, the spatiotemporal dynamics and the physiological consequences of the activation of MAPKs, particularly in plants, are still poorly understood. Here, we studied the activation and localization of the Medicago sativa stress-induced MAPKK (SIMKK)–SIMK module after salt stress. In the inactive state, SIMKK and SIMK co-localized in the cytoplasm and in the nucleus. Upon salt stress, however, a substantial part of the nuclear pool of both SIMKK and SIMK relocated to cytoplasmic compartments. The course of nucleocytoplasmic shuttling of SIMK correlated temporally with the dual phosphorylation of the pTEpY motif. SIMKK function was further studied in Arabidopsis plants overexpressing SIMKK–yellow fluorescent protein (YFP) fusions. SIMKK–YFP plants showed enhanced activation of Arabidopsis MPK3 and MPK6 kinases upon salt treatment and exhibited high sensitivity against salt stress at the seedling stage, although they were salt insensitive during seed germination. Proteomic analysis of SIMKK–YFP overexpressors indicated the differential regulation of proteins directly or indirectly involved in salt stress responses. These proteins included catalase, peroxiredoxin, glutathione S-transferase, nucleoside diphosphate kinase 1, endoplasmic reticulum luminal-binding protein 2, and finally plasma membrane aquaporins. In conclusion, Arabidopsis seedlings overexpressing SIMKK–YFP exhibited higher salt sensitivity consistent with their proteome composition and with the presumptive MPK3/MPK6 hijacking of the salt response pathway.
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spelling pubmed-40365042014-05-28 Salt-induced subcellular kinase relocation and seedling susceptibility caused by overexpression of Medicago SIMKK in Arabidopsis Ovečka, Miroslav Takáč, Tomáš Komis, George Vadovič, Pavol Bekešová, Slávka Doskočilová, Anna Smékalová, Veronika Luptovčiak, Ivan Šamajová, Olga Schweighofer, Alois Meskiene, Irute Jonak, Claudia Křenek, Pavel Lichtscheidl, Irene Škultéty, Ľudovít Hirt, Heribert Šamaj, Jozef J Exp Bot Research Paper Dual-specificity mitogen-activated protein kinases kinases (MAPKKs) are the immediate upstream activators of MAPKs. They simultaneously phosphorylate the TXY motif within the activation loop of MAPKs, allowing them to interact with and regulate multiple substrates. Often, the activation of MAPKs triggers their nuclear translocation. However, the spatiotemporal dynamics and the physiological consequences of the activation of MAPKs, particularly in plants, are still poorly understood. Here, we studied the activation and localization of the Medicago sativa stress-induced MAPKK (SIMKK)–SIMK module after salt stress. In the inactive state, SIMKK and SIMK co-localized in the cytoplasm and in the nucleus. Upon salt stress, however, a substantial part of the nuclear pool of both SIMKK and SIMK relocated to cytoplasmic compartments. The course of nucleocytoplasmic shuttling of SIMK correlated temporally with the dual phosphorylation of the pTEpY motif. SIMKK function was further studied in Arabidopsis plants overexpressing SIMKK–yellow fluorescent protein (YFP) fusions. SIMKK–YFP plants showed enhanced activation of Arabidopsis MPK3 and MPK6 kinases upon salt treatment and exhibited high sensitivity against salt stress at the seedling stage, although they were salt insensitive during seed germination. Proteomic analysis of SIMKK–YFP overexpressors indicated the differential regulation of proteins directly or indirectly involved in salt stress responses. These proteins included catalase, peroxiredoxin, glutathione S-transferase, nucleoside diphosphate kinase 1, endoplasmic reticulum luminal-binding protein 2, and finally plasma membrane aquaporins. In conclusion, Arabidopsis seedlings overexpressing SIMKK–YFP exhibited higher salt sensitivity consistent with their proteome composition and with the presumptive MPK3/MPK6 hijacking of the salt response pathway. Oxford University Press 2014-06 2014-03-19 /pmc/articles/PMC4036504/ /pubmed/24648569 http://dx.doi.org/10.1093/jxb/eru115 Text en © The Author 2014. Published by Oxford University Press on behalf of the Society for Experimental Biology. http://creativecommons.org/licenses/by/3.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Paper
Ovečka, Miroslav
Takáč, Tomáš
Komis, George
Vadovič, Pavol
Bekešová, Slávka
Doskočilová, Anna
Smékalová, Veronika
Luptovčiak, Ivan
Šamajová, Olga
Schweighofer, Alois
Meskiene, Irute
Jonak, Claudia
Křenek, Pavel
Lichtscheidl, Irene
Škultéty, Ľudovít
Hirt, Heribert
Šamaj, Jozef
Salt-induced subcellular kinase relocation and seedling susceptibility caused by overexpression of Medicago SIMKK in Arabidopsis
title Salt-induced subcellular kinase relocation and seedling susceptibility caused by overexpression of Medicago SIMKK in Arabidopsis
title_full Salt-induced subcellular kinase relocation and seedling susceptibility caused by overexpression of Medicago SIMKK in Arabidopsis
title_fullStr Salt-induced subcellular kinase relocation and seedling susceptibility caused by overexpression of Medicago SIMKK in Arabidopsis
title_full_unstemmed Salt-induced subcellular kinase relocation and seedling susceptibility caused by overexpression of Medicago SIMKK in Arabidopsis
title_short Salt-induced subcellular kinase relocation and seedling susceptibility caused by overexpression of Medicago SIMKK in Arabidopsis
title_sort salt-induced subcellular kinase relocation and seedling susceptibility caused by overexpression of medicago simkk in arabidopsis
topic Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4036504/
https://www.ncbi.nlm.nih.gov/pubmed/24648569
http://dx.doi.org/10.1093/jxb/eru115
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