Identification and Characterization of the Heat-Induced Plastidial Stress Granules Reveal New Insight Into Arabidopsis Stress Response

Plants exhibit different physiological and molecular responses to adverse changes in their environment. One such molecular response is the sequestration of proteins, RNAs, and metabolites into cytoplasmic bodies called stress granules (cSGs). Here we report that, in addition to cSGs, heat stress als...

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Main Authors: Monika Chodasiewicz, Ewelina Maria Sokolowska, Anna C. Nelson-Dittrich, Aleksandra Masiuk, Juan Camilo Moreno Beltran, Andrew D. L. Nelson, Aleksandra Skirycz
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-10-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2020.595792/full
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spelling doaj-182d0fc01168470f8b20d350b5a25a592020-11-25T04:08:36ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-10-011110.3389/fpls.2020.595792595792Identification and Characterization of the Heat-Induced Plastidial Stress Granules Reveal New Insight Into Arabidopsis Stress ResponseMonika Chodasiewicz0Monika Chodasiewicz1Ewelina Maria Sokolowska2Anna C. Nelson-Dittrich3Aleksandra Masiuk4Juan Camilo Moreno Beltran5Andrew D. L. Nelson6Aleksandra Skirycz7Aleksandra Skirycz8Max Planck Institute of Molecular Plant Physiology, Golm, GermanyCenter for Desert Agriculture, Biological and Environmental Science and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaMax Planck Institute of Molecular Plant Physiology, Golm, GermanyBoyce Thompson Institute, Cornell University, Ithaca, NY, United StatesMax Planck Institute of Molecular Plant Physiology, Golm, GermanyMax Planck Institute of Molecular Plant Physiology, Golm, GermanyBoyce Thompson Institute, Cornell University, Ithaca, NY, United StatesMax Planck Institute of Molecular Plant Physiology, Golm, GermanyBoyce Thompson Institute, Cornell University, Ithaca, NY, United StatesPlants exhibit different physiological and molecular responses to adverse changes in their environment. One such molecular response is the sequestration of proteins, RNAs, and metabolites into cytoplasmic bodies called stress granules (cSGs). Here we report that, in addition to cSGs, heat stress also induces the formation of SG-like foci (cGs) in the chloroplasts of the model plant Arabidopsis thaliana. Similarly to the cSGs, (i) cpSG assemble rapidly in response to stress and disappear when the stress ceases, (ii) cpSG formation is inhibited by treatment with a translation inhibitor (lincomycin), and (iii) cpSG are composed of a stable core and a fluid outer shell. A previously published protocol for cSG extraction was successfully adapted to isolate cpSG, followed by protein, metabolite, and RNA analysis. Analogously to the cSGs, cpSG sequester proteins essential for SG formation, dynamics, and function, also including RNA-binding proteins with prion-like domain, ATPases and chaperones, and the amino acids proline and glutamic acid. However, the most intriguing observation relates to the cpSG localization of proteins, such as a complete magnesium chelatase complex, which is involved in photosynthetic acclimation to stress. These data suggest that cpSG have a role in plant stress tolerance.https://www.frontiersin.org/articles/10.3389/fpls.2020.595792/fullstress granulesplastidprotomechlorophyll biosynthesismetabolites
collection DOAJ
language English
format Article
sources DOAJ
author Monika Chodasiewicz
Monika Chodasiewicz
Ewelina Maria Sokolowska
Anna C. Nelson-Dittrich
Aleksandra Masiuk
Juan Camilo Moreno Beltran
Andrew D. L. Nelson
Aleksandra Skirycz
Aleksandra Skirycz
spellingShingle Monika Chodasiewicz
Monika Chodasiewicz
Ewelina Maria Sokolowska
Anna C. Nelson-Dittrich
Aleksandra Masiuk
Juan Camilo Moreno Beltran
Andrew D. L. Nelson
Aleksandra Skirycz
Aleksandra Skirycz
Identification and Characterization of the Heat-Induced Plastidial Stress Granules Reveal New Insight Into Arabidopsis Stress Response
Frontiers in Plant Science
stress granules
plastid
protome
chlorophyll biosynthesis
metabolites
author_facet Monika Chodasiewicz
Monika Chodasiewicz
Ewelina Maria Sokolowska
Anna C. Nelson-Dittrich
Aleksandra Masiuk
Juan Camilo Moreno Beltran
Andrew D. L. Nelson
Aleksandra Skirycz
Aleksandra Skirycz
author_sort Monika Chodasiewicz
title Identification and Characterization of the Heat-Induced Plastidial Stress Granules Reveal New Insight Into Arabidopsis Stress Response
title_short Identification and Characterization of the Heat-Induced Plastidial Stress Granules Reveal New Insight Into Arabidopsis Stress Response
title_full Identification and Characterization of the Heat-Induced Plastidial Stress Granules Reveal New Insight Into Arabidopsis Stress Response
title_fullStr Identification and Characterization of the Heat-Induced Plastidial Stress Granules Reveal New Insight Into Arabidopsis Stress Response
title_full_unstemmed Identification and Characterization of the Heat-Induced Plastidial Stress Granules Reveal New Insight Into Arabidopsis Stress Response
title_sort identification and characterization of the heat-induced plastidial stress granules reveal new insight into arabidopsis stress response
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2020-10-01
description Plants exhibit different physiological and molecular responses to adverse changes in their environment. One such molecular response is the sequestration of proteins, RNAs, and metabolites into cytoplasmic bodies called stress granules (cSGs). Here we report that, in addition to cSGs, heat stress also induces the formation of SG-like foci (cGs) in the chloroplasts of the model plant Arabidopsis thaliana. Similarly to the cSGs, (i) cpSG assemble rapidly in response to stress and disappear when the stress ceases, (ii) cpSG formation is inhibited by treatment with a translation inhibitor (lincomycin), and (iii) cpSG are composed of a stable core and a fluid outer shell. A previously published protocol for cSG extraction was successfully adapted to isolate cpSG, followed by protein, metabolite, and RNA analysis. Analogously to the cSGs, cpSG sequester proteins essential for SG formation, dynamics, and function, also including RNA-binding proteins with prion-like domain, ATPases and chaperones, and the amino acids proline and glutamic acid. However, the most intriguing observation relates to the cpSG localization of proteins, such as a complete magnesium chelatase complex, which is involved in photosynthetic acclimation to stress. These data suggest that cpSG have a role in plant stress tolerance.
topic stress granules
plastid
protome
chlorophyll biosynthesis
metabolites
url https://www.frontiersin.org/articles/10.3389/fpls.2020.595792/full
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