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Coevolution in Hybrid Genomes: Nuclear-Encoded Rubisco Small Subunits and Their Plastid-Targeting Translocons Accompanying Sequential Allopolyploidy Events in Triticum

The Triticum/Aegilops complex includes hybrid species resulting from homoploid hybrid speciation and allopolyploid speciation. Sequential allotetra- and allohexaploidy events presumably result in two challenges for the hybrids, which involve 1) cytonuclear stoichiometric disruptions caused by combin...

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Autores principales: Li, Changping, Wang, Xiaofei, Xiao, Yaxian, Sun, Xuhan, Wang, Jinbin, Yang, Xuan, Sun, Yuchen, Sha, Yan, Lv, Ruili, Yu, Yanan, Ding, Baoxu, Zhang, Zhibin, Li, Ning, Wang, Tianya, Wendel, Jonathan F, Liu, Bao, Gong, Lei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7743682/
https://www.ncbi.nlm.nih.gov/pubmed/32602899
http://dx.doi.org/10.1093/molbev/msaa158
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author Li, Changping
Wang, Xiaofei
Xiao, Yaxian
Sun, Xuhan
Wang, Jinbin
Yang, Xuan
Sun, Yuchen
Sha, Yan
Lv, Ruili
Yu, Yanan
Ding, Baoxu
Zhang, Zhibin
Li, Ning
Wang, Tianya
Wendel, Jonathan F
Liu, Bao
Gong, Lei
author_facet Li, Changping
Wang, Xiaofei
Xiao, Yaxian
Sun, Xuhan
Wang, Jinbin
Yang, Xuan
Sun, Yuchen
Sha, Yan
Lv, Ruili
Yu, Yanan
Ding, Baoxu
Zhang, Zhibin
Li, Ning
Wang, Tianya
Wendel, Jonathan F
Liu, Bao
Gong, Lei
author_sort Li, Changping
collection PubMed
description The Triticum/Aegilops complex includes hybrid species resulting from homoploid hybrid speciation and allopolyploid speciation. Sequential allotetra- and allohexaploidy events presumably result in two challenges for the hybrids, which involve 1) cytonuclear stoichiometric disruptions caused by combining two diverged nuclear genomes with the maternal inheritance of the cytoplasmic organellar donor; and 2) incompatibility of chimeric protein complexes with diverged subunits from nuclear and cytoplasmic genomes. Here, we describe coevolution of nuclear rbcS genes encoding the small subunits of Rubisco (ribulose 1,5-bisphosphate carboxylase/oxygenase) and nuclear genes encoding plastid translocons, which mediate recognition and translocation of nuclear-encoded proteins into plastids, in allopolyploid wheat species. We demonstrate that intergenomic paternal-to-maternal gene conversion specifically occurred in the genic region of the homoeologous rbcS3 gene from the D-genome progenitor of wheat (abbreviated as rbcS3D) such that it encodes a maternal-like or B-subgenome-like SSU3D transit peptide in allohexaploid wheat but not in allotetraploid wheat. Divergent and limited interaction between SSU3D and the D-subgenomic TOC90D translocon subunit is implicated to underpin SSU3D targeting into the chloroplast of hexaploid wheat. This implicates early selection favoring individuals harboring optimal maternal-like organellar SSU3D targeting in hexaploid wheat. These data represent a novel dimension of cytonuclear evolution mediated by organellar targeting and transportation of nuclear proteins.
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spelling pubmed-77436822020-12-21 Coevolution in Hybrid Genomes: Nuclear-Encoded Rubisco Small Subunits and Their Plastid-Targeting Translocons Accompanying Sequential Allopolyploidy Events in Triticum Li, Changping Wang, Xiaofei Xiao, Yaxian Sun, Xuhan Wang, Jinbin Yang, Xuan Sun, Yuchen Sha, Yan Lv, Ruili Yu, Yanan Ding, Baoxu Zhang, Zhibin Li, Ning Wang, Tianya Wendel, Jonathan F Liu, Bao Gong, Lei Mol Biol Evol Discoveries The Triticum/Aegilops complex includes hybrid species resulting from homoploid hybrid speciation and allopolyploid speciation. Sequential allotetra- and allohexaploidy events presumably result in two challenges for the hybrids, which involve 1) cytonuclear stoichiometric disruptions caused by combining two diverged nuclear genomes with the maternal inheritance of the cytoplasmic organellar donor; and 2) incompatibility of chimeric protein complexes with diverged subunits from nuclear and cytoplasmic genomes. Here, we describe coevolution of nuclear rbcS genes encoding the small subunits of Rubisco (ribulose 1,5-bisphosphate carboxylase/oxygenase) and nuclear genes encoding plastid translocons, which mediate recognition and translocation of nuclear-encoded proteins into plastids, in allopolyploid wheat species. We demonstrate that intergenomic paternal-to-maternal gene conversion specifically occurred in the genic region of the homoeologous rbcS3 gene from the D-genome progenitor of wheat (abbreviated as rbcS3D) such that it encodes a maternal-like or B-subgenome-like SSU3D transit peptide in allohexaploid wheat but not in allotetraploid wheat. Divergent and limited interaction between SSU3D and the D-subgenomic TOC90D translocon subunit is implicated to underpin SSU3D targeting into the chloroplast of hexaploid wheat. This implicates early selection favoring individuals harboring optimal maternal-like organellar SSU3D targeting in hexaploid wheat. These data represent a novel dimension of cytonuclear evolution mediated by organellar targeting and transportation of nuclear proteins. Oxford University Press 2020-06-30 /pmc/articles/PMC7743682/ /pubmed/32602899 http://dx.doi.org/10.1093/molbev/msaa158 Text en © The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Discoveries
Li, Changping
Wang, Xiaofei
Xiao, Yaxian
Sun, Xuhan
Wang, Jinbin
Yang, Xuan
Sun, Yuchen
Sha, Yan
Lv, Ruili
Yu, Yanan
Ding, Baoxu
Zhang, Zhibin
Li, Ning
Wang, Tianya
Wendel, Jonathan F
Liu, Bao
Gong, Lei
Coevolution in Hybrid Genomes: Nuclear-Encoded Rubisco Small Subunits and Their Plastid-Targeting Translocons Accompanying Sequential Allopolyploidy Events in Triticum
title Coevolution in Hybrid Genomes: Nuclear-Encoded Rubisco Small Subunits and Their Plastid-Targeting Translocons Accompanying Sequential Allopolyploidy Events in Triticum
title_full Coevolution in Hybrid Genomes: Nuclear-Encoded Rubisco Small Subunits and Their Plastid-Targeting Translocons Accompanying Sequential Allopolyploidy Events in Triticum
title_fullStr Coevolution in Hybrid Genomes: Nuclear-Encoded Rubisco Small Subunits and Their Plastid-Targeting Translocons Accompanying Sequential Allopolyploidy Events in Triticum
title_full_unstemmed Coevolution in Hybrid Genomes: Nuclear-Encoded Rubisco Small Subunits and Their Plastid-Targeting Translocons Accompanying Sequential Allopolyploidy Events in Triticum
title_short Coevolution in Hybrid Genomes: Nuclear-Encoded Rubisco Small Subunits and Their Plastid-Targeting Translocons Accompanying Sequential Allopolyploidy Events in Triticum
title_sort coevolution in hybrid genomes: nuclear-encoded rubisco small subunits and their plastid-targeting translocons accompanying sequential allopolyploidy events in triticum
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7743682/
https://www.ncbi.nlm.nih.gov/pubmed/32602899
http://dx.doi.org/10.1093/molbev/msaa158
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