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Dissecting the Role of SAL1 in Metabolizing the Stress Signaling Molecule 3′-Phosphoadenosine 5′-Phosphate in Different Cell Compartments

Plants possess the most highly compartmentalized eukaryotic cells. To coordinate their intracellular functions, plastids and the mitochondria are dependent on the flow of information to and from the nuclei, known as retrograde and anterograde signals. One mobile retrograde signaling molecule is the...

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Autores principales: Ashykhmina, Natallia, Chan, Kai Xun, Frerigmann, Henning, Van Breusegem, Frank, Kopriva, Stanislav, Flügge, Ulf-Ingo, Gigolashvili, Tamara
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8815814/
https://www.ncbi.nlm.nih.gov/pubmed/35127814
http://dx.doi.org/10.3389/fmolb.2021.763795
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author Ashykhmina, Natallia
Chan, Kai Xun
Frerigmann, Henning
Van Breusegem, Frank
Kopriva, Stanislav
Flügge, Ulf-Ingo
Gigolashvili, Tamara
author_facet Ashykhmina, Natallia
Chan, Kai Xun
Frerigmann, Henning
Van Breusegem, Frank
Kopriva, Stanislav
Flügge, Ulf-Ingo
Gigolashvili, Tamara
author_sort Ashykhmina, Natallia
collection PubMed
description Plants possess the most highly compartmentalized eukaryotic cells. To coordinate their intracellular functions, plastids and the mitochondria are dependent on the flow of information to and from the nuclei, known as retrograde and anterograde signals. One mobile retrograde signaling molecule is the monophosphate 3′-phosphoadenosine 5′-phosphate (PAP), which is mainly produced from 3′-phosphoadenosine 5′-phosphosulfate (PAPS) in the cytosol and regulates the expression of a set of nuclear genes that modulate plant growth in response to biotic and abiotic stresses. The adenosine bisphosphate phosphatase enzyme SAL1 dephosphorylates PAP to AMP in plastids and the mitochondria, but can also rescue sal1 Arabidopsis phenotypes (PAP accumulation, leaf morphology, growth, etc.) when expressed in the cytosol and the nucleus. To understand better the roles of the SAL1 protein in chloroplasts, the mitochondria, nuclei, and the cytosol, we have attempted to complement the sal1 mutant by specifically cargoing the transgenic SAL1 protein to these four cell compartments. Overexpression of SAL1 protein targeted to the nucleus or the mitochondria alone, or co-targeted to chloroplasts and the mitochondria, complemented most aspects of the sal1 phenotypes. Notably, targeting SAL1 to chloroplasts or the cytosol did not effectively rescue the sal1 phenotypes as these transgenic lines accumulated very low levels of SAL1 protein despite overexpressing SAL1 mRNA, suggesting a possibly lower stability of the SAL1 protein in these compartments. The diverse transgenic SAL1 lines exhibited a range of PAP levels. The latter needs to reach certain thresholds in the cell for its impacts on different processes such as leaf growth, regulation of rosette morphology, sulfate homeostasis, and glucosinolate biosynthesis. Collectively, these findings provide an initial platform for further dissection of the role of the SAL1–PAP pathway in different cellular processes under stress conditions.
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spelling pubmed-88158142022-02-05 Dissecting the Role of SAL1 in Metabolizing the Stress Signaling Molecule 3′-Phosphoadenosine 5′-Phosphate in Different Cell Compartments Ashykhmina, Natallia Chan, Kai Xun Frerigmann, Henning Van Breusegem, Frank Kopriva, Stanislav Flügge, Ulf-Ingo Gigolashvili, Tamara Front Mol Biosci Molecular Biosciences Plants possess the most highly compartmentalized eukaryotic cells. To coordinate their intracellular functions, plastids and the mitochondria are dependent on the flow of information to and from the nuclei, known as retrograde and anterograde signals. One mobile retrograde signaling molecule is the monophosphate 3′-phosphoadenosine 5′-phosphate (PAP), which is mainly produced from 3′-phosphoadenosine 5′-phosphosulfate (PAPS) in the cytosol and regulates the expression of a set of nuclear genes that modulate plant growth in response to biotic and abiotic stresses. The adenosine bisphosphate phosphatase enzyme SAL1 dephosphorylates PAP to AMP in plastids and the mitochondria, but can also rescue sal1 Arabidopsis phenotypes (PAP accumulation, leaf morphology, growth, etc.) when expressed in the cytosol and the nucleus. To understand better the roles of the SAL1 protein in chloroplasts, the mitochondria, nuclei, and the cytosol, we have attempted to complement the sal1 mutant by specifically cargoing the transgenic SAL1 protein to these four cell compartments. Overexpression of SAL1 protein targeted to the nucleus or the mitochondria alone, or co-targeted to chloroplasts and the mitochondria, complemented most aspects of the sal1 phenotypes. Notably, targeting SAL1 to chloroplasts or the cytosol did not effectively rescue the sal1 phenotypes as these transgenic lines accumulated very low levels of SAL1 protein despite overexpressing SAL1 mRNA, suggesting a possibly lower stability of the SAL1 protein in these compartments. The diverse transgenic SAL1 lines exhibited a range of PAP levels. The latter needs to reach certain thresholds in the cell for its impacts on different processes such as leaf growth, regulation of rosette morphology, sulfate homeostasis, and glucosinolate biosynthesis. Collectively, these findings provide an initial platform for further dissection of the role of the SAL1–PAP pathway in different cellular processes under stress conditions. Frontiers Media S.A. 2022-01-21 /pmc/articles/PMC8815814/ /pubmed/35127814 http://dx.doi.org/10.3389/fmolb.2021.763795 Text en Copyright © 2022 Ashykhmina, Chan, Frerigmann, Van Breusegem, Kopriva, Flügge and Gigolashvili. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Molecular Biosciences
Ashykhmina, Natallia
Chan, Kai Xun
Frerigmann, Henning
Van Breusegem, Frank
Kopriva, Stanislav
Flügge, Ulf-Ingo
Gigolashvili, Tamara
Dissecting the Role of SAL1 in Metabolizing the Stress Signaling Molecule 3′-Phosphoadenosine 5′-Phosphate in Different Cell Compartments
title Dissecting the Role of SAL1 in Metabolizing the Stress Signaling Molecule 3′-Phosphoadenosine 5′-Phosphate in Different Cell Compartments
title_full Dissecting the Role of SAL1 in Metabolizing the Stress Signaling Molecule 3′-Phosphoadenosine 5′-Phosphate in Different Cell Compartments
title_fullStr Dissecting the Role of SAL1 in Metabolizing the Stress Signaling Molecule 3′-Phosphoadenosine 5′-Phosphate in Different Cell Compartments
title_full_unstemmed Dissecting the Role of SAL1 in Metabolizing the Stress Signaling Molecule 3′-Phosphoadenosine 5′-Phosphate in Different Cell Compartments
title_short Dissecting the Role of SAL1 in Metabolizing the Stress Signaling Molecule 3′-Phosphoadenosine 5′-Phosphate in Different Cell Compartments
title_sort dissecting the role of sal1 in metabolizing the stress signaling molecule 3′-phosphoadenosine 5′-phosphate in different cell compartments
topic Molecular Biosciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8815814/
https://www.ncbi.nlm.nih.gov/pubmed/35127814
http://dx.doi.org/10.3389/fmolb.2021.763795
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