Cargando…

Whole-genome Duplications and the Long-term Evolution of Gene Regulatory Networks in Angiosperms

Angiosperms have a complex history of whole-genome duplications (WGDs), with varying numbers and ages of WGD events across clades. These WGDs have greatly affected the composition of plant genomes due to the biased retention of genes belonging to certain functional categories following their duplica...

Descripción completa

Detalles Bibliográficos
Autores principales: Almeida-Silva, Fabricio, Van de Peer, Yves
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10321489/
https://www.ncbi.nlm.nih.gov/pubmed/37405949
http://dx.doi.org/10.1093/molbev/msad141
_version_ 1785068624741924864
author Almeida-Silva, Fabricio
Van de Peer, Yves
author_facet Almeida-Silva, Fabricio
Van de Peer, Yves
author_sort Almeida-Silva, Fabricio
collection PubMed
description Angiosperms have a complex history of whole-genome duplications (WGDs), with varying numbers and ages of WGD events across clades. These WGDs have greatly affected the composition of plant genomes due to the biased retention of genes belonging to certain functional categories following their duplication. In particular, regulatory genes and genes encoding proteins that act in multiprotein complexes have been retained in excess following WGD. Here, we inferred protein–protein interaction (PPI) networks and gene regulatory networks (GRNs) for seven well-characterized angiosperm species and explored the impact of both WGD and small-scale duplications (SSDs) in network topology by analyzing changes in frequency of network motifs. We found that PPI networks are enriched in WGD-derived genes associated with dosage-sensitive intricate systems, and strong selection pressures constrain the divergence of WGD-derived genes at the sequence and PPI levels. WGD-derived genes in network motifs are mostly associated with dosage-sensitive processes, such as regulation of transcription and cell cycle, translation, photosynthesis, and carbon metabolism, whereas SSD-derived genes in motifs are associated with response to biotic and abiotic stress. Recent polyploids have higher motif frequencies than ancient polyploids, whereas WGD-derived network motifs tend to be disrupted on the longer term. Our findings demonstrate that both WGD and SSD have contributed to the evolution of angiosperm GRNs, but in different ways, with WGD events likely having a more significant impact on the short-term evolution of polyploids.
format Online
Article
Text
id pubmed-10321489
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Oxford University Press
record_format MEDLINE/PubMed
spelling pubmed-103214892023-07-06 Whole-genome Duplications and the Long-term Evolution of Gene Regulatory Networks in Angiosperms Almeida-Silva, Fabricio Van de Peer, Yves Mol Biol Evol Discoveries Angiosperms have a complex history of whole-genome duplications (WGDs), with varying numbers and ages of WGD events across clades. These WGDs have greatly affected the composition of plant genomes due to the biased retention of genes belonging to certain functional categories following their duplication. In particular, regulatory genes and genes encoding proteins that act in multiprotein complexes have been retained in excess following WGD. Here, we inferred protein–protein interaction (PPI) networks and gene regulatory networks (GRNs) for seven well-characterized angiosperm species and explored the impact of both WGD and small-scale duplications (SSDs) in network topology by analyzing changes in frequency of network motifs. We found that PPI networks are enriched in WGD-derived genes associated with dosage-sensitive intricate systems, and strong selection pressures constrain the divergence of WGD-derived genes at the sequence and PPI levels. WGD-derived genes in network motifs are mostly associated with dosage-sensitive processes, such as regulation of transcription and cell cycle, translation, photosynthesis, and carbon metabolism, whereas SSD-derived genes in motifs are associated with response to biotic and abiotic stress. Recent polyploids have higher motif frequencies than ancient polyploids, whereas WGD-derived network motifs tend to be disrupted on the longer term. Our findings demonstrate that both WGD and SSD have contributed to the evolution of angiosperm GRNs, but in different ways, with WGD events likely having a more significant impact on the short-term evolution of polyploids. Oxford University Press 2023-07-05 /pmc/articles/PMC10321489/ /pubmed/37405949 http://dx.doi.org/10.1093/molbev/msad141 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Discoveries
Almeida-Silva, Fabricio
Van de Peer, Yves
Whole-genome Duplications and the Long-term Evolution of Gene Regulatory Networks in Angiosperms
title Whole-genome Duplications and the Long-term Evolution of Gene Regulatory Networks in Angiosperms
title_full Whole-genome Duplications and the Long-term Evolution of Gene Regulatory Networks in Angiosperms
title_fullStr Whole-genome Duplications and the Long-term Evolution of Gene Regulatory Networks in Angiosperms
title_full_unstemmed Whole-genome Duplications and the Long-term Evolution of Gene Regulatory Networks in Angiosperms
title_short Whole-genome Duplications and the Long-term Evolution of Gene Regulatory Networks in Angiosperms
title_sort whole-genome duplications and the long-term evolution of gene regulatory networks in angiosperms
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10321489/
https://www.ncbi.nlm.nih.gov/pubmed/37405949
http://dx.doi.org/10.1093/molbev/msad141
work_keys_str_mv AT almeidasilvafabricio wholegenomeduplicationsandthelongtermevolutionofgeneregulatorynetworksinangiosperms
AT vandepeeryves wholegenomeduplicationsandthelongtermevolutionofgeneregulatorynetworksinangiosperms