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Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels

Mitochondrial and plastid functions depend on coordinated expression of proteins encoded by genomic compartments that have radical differences in copy number of organellar and nuclear genomes. In polyploids, doubling of the nuclear genome may add challenges to maintaining balanced expression of prot...

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Autores principales: Forsythe, Evan S., Grover, Corrinne E., Miller, Emma R., Conover, Justin L., Arick, Mark A., Chavarro, M. Carolina F., Leal-Bertioli, Soraya C. M., Peterson, Daniel G., Sharbrough, Joel, Wendel, Jonathan F., Sloan, Daniel B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9335225/
https://www.ncbi.nlm.nih.gov/pubmed/35858449
http://dx.doi.org/10.1073/pnas.2204187119
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author Forsythe, Evan S.
Grover, Corrinne E.
Miller, Emma R.
Conover, Justin L.
Arick, Mark A.
Chavarro, M. Carolina F.
Leal-Bertioli, Soraya C. M.
Peterson, Daniel G.
Sharbrough, Joel
Wendel, Jonathan F.
Sloan, Daniel B.
author_facet Forsythe, Evan S.
Grover, Corrinne E.
Miller, Emma R.
Conover, Justin L.
Arick, Mark A.
Chavarro, M. Carolina F.
Leal-Bertioli, Soraya C. M.
Peterson, Daniel G.
Sharbrough, Joel
Wendel, Jonathan F.
Sloan, Daniel B.
author_sort Forsythe, Evan S.
collection PubMed
description Mitochondrial and plastid functions depend on coordinated expression of proteins encoded by genomic compartments that have radical differences in copy number of organellar and nuclear genomes. In polyploids, doubling of the nuclear genome may add challenges to maintaining balanced expression of proteins involved in cytonuclear interactions. Here, we use ribo-depleted RNA sequencing (RNA-seq) to analyze transcript abundance for nuclear and organellar genomes in leaf tissue from four different polyploid angiosperms and their close diploid relatives. We find that even though plastid genomes contain <1% of the number of genes in the nuclear genome, they generate the majority (69.9 to 82.3%) of messenger RNA (mRNA) transcripts in the cell. Mitochondrial genes are responsible for a much smaller percentage (1.3 to 3.7%) of the leaf mRNA pool but still produce much higher transcript abundances per gene compared to nuclear genome. Nuclear genes encoding proteins that functionally interact with mitochondrial or plastid gene products exhibit mRNA expression levels that are consistently more than 10-fold lower than their organellar counterparts, indicating an extreme cytonuclear imbalance at the RNA level despite the predominance of equimolar interactions at the protein level. Nevertheless, interacting nuclear and organellar genes show strongly correlated transcript abundances across functional categories, suggesting that the observed mRNA stoichiometric imbalance does not preclude coordination of cytonuclear expression. Finally, we show that nuclear genome doubling does not alter the cytonuclear expression ratios observed in diploid relatives in consistent or systematic ways, indicating that successful polyploid plants are able to compensate for cytonuclear perturbations associated with nuclear genome doubling.
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spelling pubmed-93352252023-01-19 Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels Forsythe, Evan S. Grover, Corrinne E. Miller, Emma R. Conover, Justin L. Arick, Mark A. Chavarro, M. Carolina F. Leal-Bertioli, Soraya C. M. Peterson, Daniel G. Sharbrough, Joel Wendel, Jonathan F. Sloan, Daniel B. Proc Natl Acad Sci U S A Biological Sciences Mitochondrial and plastid functions depend on coordinated expression of proteins encoded by genomic compartments that have radical differences in copy number of organellar and nuclear genomes. In polyploids, doubling of the nuclear genome may add challenges to maintaining balanced expression of proteins involved in cytonuclear interactions. Here, we use ribo-depleted RNA sequencing (RNA-seq) to analyze transcript abundance for nuclear and organellar genomes in leaf tissue from four different polyploid angiosperms and their close diploid relatives. We find that even though plastid genomes contain <1% of the number of genes in the nuclear genome, they generate the majority (69.9 to 82.3%) of messenger RNA (mRNA) transcripts in the cell. Mitochondrial genes are responsible for a much smaller percentage (1.3 to 3.7%) of the leaf mRNA pool but still produce much higher transcript abundances per gene compared to nuclear genome. Nuclear genes encoding proteins that functionally interact with mitochondrial or plastid gene products exhibit mRNA expression levels that are consistently more than 10-fold lower than their organellar counterparts, indicating an extreme cytonuclear imbalance at the RNA level despite the predominance of equimolar interactions at the protein level. Nevertheless, interacting nuclear and organellar genes show strongly correlated transcript abundances across functional categories, suggesting that the observed mRNA stoichiometric imbalance does not preclude coordination of cytonuclear expression. Finally, we show that nuclear genome doubling does not alter the cytonuclear expression ratios observed in diploid relatives in consistent or systematic ways, indicating that successful polyploid plants are able to compensate for cytonuclear perturbations associated with nuclear genome doubling. National Academy of Sciences 2022-07-19 2022-07-26 /pmc/articles/PMC9335225/ /pubmed/35858449 http://dx.doi.org/10.1073/pnas.2204187119 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
Forsythe, Evan S.
Grover, Corrinne E.
Miller, Emma R.
Conover, Justin L.
Arick, Mark A.
Chavarro, M. Carolina F.
Leal-Bertioli, Soraya C. M.
Peterson, Daniel G.
Sharbrough, Joel
Wendel, Jonathan F.
Sloan, Daniel B.
Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels
title Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels
title_full Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels
title_fullStr Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels
title_full_unstemmed Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels
title_short Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels
title_sort organellar transcripts dominate the cellular mrna pool across plants of varying ploidy levels
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9335225/
https://www.ncbi.nlm.nih.gov/pubmed/35858449
http://dx.doi.org/10.1073/pnas.2204187119
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