Cargando…

Variation in cytonuclear expression accommodation among allopolyploid plants

Cytonuclear coevolution is a common feature among plants, which coordinates gene expression and protein products between the nucleus and organelles. Consequently, lineage-specific differences may result in incompatibilities between the nucleus and cytoplasm in hybrid taxa. Allopolyploidy is also a c...

Descripción completa

Detalles Bibliográficos
Autores principales: Grover, Corrinne E, Forsythe, Evan S, Sharbrough, Joel, Miller, Emma R, Conover, Justin L, DeTar, Rachael A, Chavarro, Carolina, Arick, Mark A, Peterson, Daniel G, Leal-Bertioli, Soraya C M, Sloan, Daniel B, Wendel, Jonathan F
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9526054/
https://www.ncbi.nlm.nih.gov/pubmed/35951749
http://dx.doi.org/10.1093/genetics/iyac118
_version_ 1784800794996899840
author Grover, Corrinne E
Forsythe, Evan S
Sharbrough, Joel
Miller, Emma R
Conover, Justin L
DeTar, Rachael A
Chavarro, Carolina
Arick, Mark A
Peterson, Daniel G
Leal-Bertioli, Soraya C M
Sloan, Daniel B
Wendel, Jonathan F
author_facet Grover, Corrinne E
Forsythe, Evan S
Sharbrough, Joel
Miller, Emma R
Conover, Justin L
DeTar, Rachael A
Chavarro, Carolina
Arick, Mark A
Peterson, Daniel G
Leal-Bertioli, Soraya C M
Sloan, Daniel B
Wendel, Jonathan F
author_sort Grover, Corrinne E
collection PubMed
description Cytonuclear coevolution is a common feature among plants, which coordinates gene expression and protein products between the nucleus and organelles. Consequently, lineage-specific differences may result in incompatibilities between the nucleus and cytoplasm in hybrid taxa. Allopolyploidy is also a common phenomenon in plant evolution. The hybrid nature of allopolyploids may result in cytonuclear incompatibilities, but the massive nuclear redundancy created during polyploidy affords additional avenues for resolving cytonuclear conflict (i.e. cytonuclear accommodation). Here we evaluate expression changes in organelle-targeted nuclear genes for 6 allopolyploid lineages that represent 4 genera (i.e. Arabidopsis, Arachis, Chenopodium, and Gossypium) and encompass a range in polyploid ages. Because incompatibilities between the nucleus and cytoplasm could potentially result in biases toward the maternal homoeolog and/or maternal expression level, we evaluate patterns of homoeolog usage, expression bias, and expression-level dominance in cytonuclear genes relative to the background of noncytonuclear expression changes and to the diploid parents. Although we find subsets of cytonuclear genes in most lineages that match our expectations of maternal preference, these observations are not consistent among either allopolyploids or categories of organelle-targeted genes. Our results indicate that cytonuclear expression evolution may be subtle and variable among genera and genes, likely reflecting a diversity of mechanisms to resolve nuclear-cytoplasmic incompatibilities in allopolyploid species.
format Online
Article
Text
id pubmed-9526054
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Oxford University Press
record_format MEDLINE/PubMed
spelling pubmed-95260542022-10-03 Variation in cytonuclear expression accommodation among allopolyploid plants Grover, Corrinne E Forsythe, Evan S Sharbrough, Joel Miller, Emma R Conover, Justin L DeTar, Rachael A Chavarro, Carolina Arick, Mark A Peterson, Daniel G Leal-Bertioli, Soraya C M Sloan, Daniel B Wendel, Jonathan F Genetics Investigation Cytonuclear coevolution is a common feature among plants, which coordinates gene expression and protein products between the nucleus and organelles. Consequently, lineage-specific differences may result in incompatibilities between the nucleus and cytoplasm in hybrid taxa. Allopolyploidy is also a common phenomenon in plant evolution. The hybrid nature of allopolyploids may result in cytonuclear incompatibilities, but the massive nuclear redundancy created during polyploidy affords additional avenues for resolving cytonuclear conflict (i.e. cytonuclear accommodation). Here we evaluate expression changes in organelle-targeted nuclear genes for 6 allopolyploid lineages that represent 4 genera (i.e. Arabidopsis, Arachis, Chenopodium, and Gossypium) and encompass a range in polyploid ages. Because incompatibilities between the nucleus and cytoplasm could potentially result in biases toward the maternal homoeolog and/or maternal expression level, we evaluate patterns of homoeolog usage, expression bias, and expression-level dominance in cytonuclear genes relative to the background of noncytonuclear expression changes and to the diploid parents. Although we find subsets of cytonuclear genes in most lineages that match our expectations of maternal preference, these observations are not consistent among either allopolyploids or categories of organelle-targeted genes. Our results indicate that cytonuclear expression evolution may be subtle and variable among genera and genes, likely reflecting a diversity of mechanisms to resolve nuclear-cytoplasmic incompatibilities in allopolyploid species. Oxford University Press 2022-08-11 /pmc/articles/PMC9526054/ /pubmed/35951749 http://dx.doi.org/10.1093/genetics/iyac118 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of Genetics Society of America. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (https://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Investigation
Grover, Corrinne E
Forsythe, Evan S
Sharbrough, Joel
Miller, Emma R
Conover, Justin L
DeTar, Rachael A
Chavarro, Carolina
Arick, Mark A
Peterson, Daniel G
Leal-Bertioli, Soraya C M
Sloan, Daniel B
Wendel, Jonathan F
Variation in cytonuclear expression accommodation among allopolyploid plants
title Variation in cytonuclear expression accommodation among allopolyploid plants
title_full Variation in cytonuclear expression accommodation among allopolyploid plants
title_fullStr Variation in cytonuclear expression accommodation among allopolyploid plants
title_full_unstemmed Variation in cytonuclear expression accommodation among allopolyploid plants
title_short Variation in cytonuclear expression accommodation among allopolyploid plants
title_sort variation in cytonuclear expression accommodation among allopolyploid plants
topic Investigation
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9526054/
https://www.ncbi.nlm.nih.gov/pubmed/35951749
http://dx.doi.org/10.1093/genetics/iyac118
work_keys_str_mv AT grovercorrinnee variationincytonuclearexpressionaccommodationamongallopolyploidplants
AT forsytheevans variationincytonuclearexpressionaccommodationamongallopolyploidplants
AT sharbroughjoel variationincytonuclearexpressionaccommodationamongallopolyploidplants
AT milleremmar variationincytonuclearexpressionaccommodationamongallopolyploidplants
AT conoverjustinl variationincytonuclearexpressionaccommodationamongallopolyploidplants
AT detarrachaela variationincytonuclearexpressionaccommodationamongallopolyploidplants
AT chavarrocarolina variationincytonuclearexpressionaccommodationamongallopolyploidplants
AT arickmarka variationincytonuclearexpressionaccommodationamongallopolyploidplants
AT petersondanielg variationincytonuclearexpressionaccommodationamongallopolyploidplants
AT lealbertiolisorayacm variationincytonuclearexpressionaccommodationamongallopolyploidplants
AT sloandanielb variationincytonuclearexpressionaccommodationamongallopolyploidplants
AT wendeljonathanf variationincytonuclearexpressionaccommodationamongallopolyploidplants