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Stress-responsive pathways and small RNA changes distinguish variable developmental phenotypes caused by MSH1 loss

BACKGROUND: Proper regulation of nuclear-encoded, organelle-targeted genes is crucial for plastid and mitochondrial function. Among these genes, MutS Homolog 1 (MSH1) is notable for generating an assortment of mutant phenotypes with varying degrees of penetrance and pleiotropy. Stronger phenotypes h...

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Autores principales: Shao, Mon-Ray, Kumar Kenchanmane Raju, Sunil, Laurie, John D., Sanchez, Robersy, Mackenzie, Sally A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5319189/
https://www.ncbi.nlm.nih.gov/pubmed/28219335
http://dx.doi.org/10.1186/s12870-017-0996-4
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author Shao, Mon-Ray
Kumar Kenchanmane Raju, Sunil
Laurie, John D.
Sanchez, Robersy
Mackenzie, Sally A.
author_facet Shao, Mon-Ray
Kumar Kenchanmane Raju, Sunil
Laurie, John D.
Sanchez, Robersy
Mackenzie, Sally A.
author_sort Shao, Mon-Ray
collection PubMed
description BACKGROUND: Proper regulation of nuclear-encoded, organelle-targeted genes is crucial for plastid and mitochondrial function. Among these genes, MutS Homolog 1 (MSH1) is notable for generating an assortment of mutant phenotypes with varying degrees of penetrance and pleiotropy. Stronger phenotypes have been connected to stress tolerance and epigenetic changes, and in Arabidopsis T-DNA mutants, two generations of homozygosity with the msh1 insertion are required before severe phenotypes begin to emerge. These observations prompted us to examine how msh1 mutants contrast according to generation and phenotype by profiling their respective transcriptomes and small RNA populations. RESULTS: Using RNA-seq, we analyze pathways that are associated with MSH1 loss, including abiotic stresses such as cold response, pathogen defense and immune response, salicylic acid, MAPK signaling, and circadian rhythm. Subtle redox and environment-responsive changes also begin in the first generation, in the absence of strong phenotypes. Using small RNA-seq we further identify miRNA changes, and uncover siRNA trends that indicate modifications at the chromatin organization level. In all cases, the magnitude of changes among protein-coding genes, transposable elements, and small RNAs increases according to generation and phenotypic severity. CONCLUSION: Loss of MSH1 is sufficient to cause large-scale regulatory changes in pathways that have been individually linked to one another, but rarely described all together within a single mutant background. This study enforces the recognition of organelles as critical integrators of both internal and external cues, and highlights the relationship between organelle and nuclear regulation in fundamental aspects of plant development and stress signaling. Our findings also encourage further investigation into potential connections between organelle state and genome regulation vis-á-vis small RNA feedback. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-017-0996-4) contains supplementary material, which is available to authorized users.
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spelling pubmed-53191892017-02-24 Stress-responsive pathways and small RNA changes distinguish variable developmental phenotypes caused by MSH1 loss Shao, Mon-Ray Kumar Kenchanmane Raju, Sunil Laurie, John D. Sanchez, Robersy Mackenzie, Sally A. BMC Plant Biol Research Article BACKGROUND: Proper regulation of nuclear-encoded, organelle-targeted genes is crucial for plastid and mitochondrial function. Among these genes, MutS Homolog 1 (MSH1) is notable for generating an assortment of mutant phenotypes with varying degrees of penetrance and pleiotropy. Stronger phenotypes have been connected to stress tolerance and epigenetic changes, and in Arabidopsis T-DNA mutants, two generations of homozygosity with the msh1 insertion are required before severe phenotypes begin to emerge. These observations prompted us to examine how msh1 mutants contrast according to generation and phenotype by profiling their respective transcriptomes and small RNA populations. RESULTS: Using RNA-seq, we analyze pathways that are associated with MSH1 loss, including abiotic stresses such as cold response, pathogen defense and immune response, salicylic acid, MAPK signaling, and circadian rhythm. Subtle redox and environment-responsive changes also begin in the first generation, in the absence of strong phenotypes. Using small RNA-seq we further identify miRNA changes, and uncover siRNA trends that indicate modifications at the chromatin organization level. In all cases, the magnitude of changes among protein-coding genes, transposable elements, and small RNAs increases according to generation and phenotypic severity. CONCLUSION: Loss of MSH1 is sufficient to cause large-scale regulatory changes in pathways that have been individually linked to one another, but rarely described all together within a single mutant background. This study enforces the recognition of organelles as critical integrators of both internal and external cues, and highlights the relationship between organelle and nuclear regulation in fundamental aspects of plant development and stress signaling. Our findings also encourage further investigation into potential connections between organelle state and genome regulation vis-á-vis small RNA feedback. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-017-0996-4) contains supplementary material, which is available to authorized users. BioMed Central 2017-02-20 /pmc/articles/PMC5319189/ /pubmed/28219335 http://dx.doi.org/10.1186/s12870-017-0996-4 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Shao, Mon-Ray
Kumar Kenchanmane Raju, Sunil
Laurie, John D.
Sanchez, Robersy
Mackenzie, Sally A.
Stress-responsive pathways and small RNA changes distinguish variable developmental phenotypes caused by MSH1 loss
title Stress-responsive pathways and small RNA changes distinguish variable developmental phenotypes caused by MSH1 loss
title_full Stress-responsive pathways and small RNA changes distinguish variable developmental phenotypes caused by MSH1 loss
title_fullStr Stress-responsive pathways and small RNA changes distinguish variable developmental phenotypes caused by MSH1 loss
title_full_unstemmed Stress-responsive pathways and small RNA changes distinguish variable developmental phenotypes caused by MSH1 loss
title_short Stress-responsive pathways and small RNA changes distinguish variable developmental phenotypes caused by MSH1 loss
title_sort stress-responsive pathways and small rna changes distinguish variable developmental phenotypes caused by msh1 loss
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5319189/
https://www.ncbi.nlm.nih.gov/pubmed/28219335
http://dx.doi.org/10.1186/s12870-017-0996-4
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