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Ancient eudicot hexaploidy meets ancestral eurosid gene order

BACKGROUND: A hexaploidization event over 125 Mya underlies the evolutionary lineage of the majority of flowering plants, including very many species of agricultural importance. Half of these belong to the rosid subgrouping, containing severals whose genome sequences have been published. Although mo...

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Autores principales: Zheng, Chunfang, Chen, Eric, Albert, Victor A, Lyons, Eric, Sankoff, David
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3817805/
https://www.ncbi.nlm.nih.gov/pubmed/24564362
http://dx.doi.org/10.1186/1471-2164-14-S7-S3
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author Zheng, Chunfang
Chen, Eric
Albert, Victor A
Lyons, Eric
Sankoff, David
author_facet Zheng, Chunfang
Chen, Eric
Albert, Victor A
Lyons, Eric
Sankoff, David
author_sort Zheng, Chunfang
collection PubMed
description BACKGROUND: A hexaploidization event over 125 Mya underlies the evolutionary lineage of the majority of flowering plants, including very many species of agricultural importance. Half of these belong to the rosid subgrouping, containing severals whose genome sequences have been published. Although most duplicate and triplicate genes have been lost in all descendants, clear traces of the original chromosome triples can be discerned, their internal contiguity highly conserved in some genomes and very fragmented in others. To understand the particular evolutionary patterns of plant genomes, there is a need to systematically survey the fate of the subgenomes of polyploids, including the retention of a small proportion of the duplicate and triplicate genes and the reconstruction of putative ancestral intermediates between the original hexaploid and modern species, in this case the ancestor of the eurosid clade. RESULTS: We quantitatively trace the fate of gene triples originating in the hexaploidy across seven core eudicot flowering plants, and fit this to a two-stage model, pre- and post-radiation. We also measure the simultaneous dynamics of duplicate orthologous gene loss in three rosids, as influenced by biological functional class. We propose a new protocol for reconstructing ancestral gene order using only gene adjacency data from pairwise genomic analyses, based on repeating MAXIMUM WEIGHT MATCHING at two levels of resolution, an approach designed to transcend limitations on reconstructed contig size, while still avoiding the ambiguities of a multiplicity of solutions. Applied to three high-quality rosid genomes without subsequent polyploidy events, our automated procedure reconstructs the ancestor of the eurosid clade. CONCLUSIONS: The gene loss analysis and the ancestor reconstruction present complementary assessments of post-hexaploidization evolution, the first at the level of individual gene families within and across sister genomes and the second at the chromosome level. Despite the loss of more than 95% of gene duplicates and triplicates, and despite major structural rearrangement, our reconstructed eurosid ancestor clearly identifies the three regions corresponding to each of the seven original chromosomes of the earlier pre-hexaploid ancestor. Functional analysis confirmed trends reported for more recent plant polyploidy events: genes involved with regulation and responses were retained in multiple copies, while genes involved with metabolic processes were lost.
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spelling pubmed-38178052013-11-07 Ancient eudicot hexaploidy meets ancestral eurosid gene order Zheng, Chunfang Chen, Eric Albert, Victor A Lyons, Eric Sankoff, David BMC Genomics Research BACKGROUND: A hexaploidization event over 125 Mya underlies the evolutionary lineage of the majority of flowering plants, including very many species of agricultural importance. Half of these belong to the rosid subgrouping, containing severals whose genome sequences have been published. Although most duplicate and triplicate genes have been lost in all descendants, clear traces of the original chromosome triples can be discerned, their internal contiguity highly conserved in some genomes and very fragmented in others. To understand the particular evolutionary patterns of plant genomes, there is a need to systematically survey the fate of the subgenomes of polyploids, including the retention of a small proportion of the duplicate and triplicate genes and the reconstruction of putative ancestral intermediates between the original hexaploid and modern species, in this case the ancestor of the eurosid clade. RESULTS: We quantitatively trace the fate of gene triples originating in the hexaploidy across seven core eudicot flowering plants, and fit this to a two-stage model, pre- and post-radiation. We also measure the simultaneous dynamics of duplicate orthologous gene loss in three rosids, as influenced by biological functional class. We propose a new protocol for reconstructing ancestral gene order using only gene adjacency data from pairwise genomic analyses, based on repeating MAXIMUM WEIGHT MATCHING at two levels of resolution, an approach designed to transcend limitations on reconstructed contig size, while still avoiding the ambiguities of a multiplicity of solutions. Applied to three high-quality rosid genomes without subsequent polyploidy events, our automated procedure reconstructs the ancestor of the eurosid clade. CONCLUSIONS: The gene loss analysis and the ancestor reconstruction present complementary assessments of post-hexaploidization evolution, the first at the level of individual gene families within and across sister genomes and the second at the chromosome level. Despite the loss of more than 95% of gene duplicates and triplicates, and despite major structural rearrangement, our reconstructed eurosid ancestor clearly identifies the three regions corresponding to each of the seven original chromosomes of the earlier pre-hexaploid ancestor. Functional analysis confirmed trends reported for more recent plant polyploidy events: genes involved with regulation and responses were retained in multiple copies, while genes involved with metabolic processes were lost. BioMed Central 2013-11-05 /pmc/articles/PMC3817805/ /pubmed/24564362 http://dx.doi.org/10.1186/1471-2164-14-S7-S3 Text en Copyright © 2013 Zheng et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research
Zheng, Chunfang
Chen, Eric
Albert, Victor A
Lyons, Eric
Sankoff, David
Ancient eudicot hexaploidy meets ancestral eurosid gene order
title Ancient eudicot hexaploidy meets ancestral eurosid gene order
title_full Ancient eudicot hexaploidy meets ancestral eurosid gene order
title_fullStr Ancient eudicot hexaploidy meets ancestral eurosid gene order
title_full_unstemmed Ancient eudicot hexaploidy meets ancestral eurosid gene order
title_short Ancient eudicot hexaploidy meets ancestral eurosid gene order
title_sort ancient eudicot hexaploidy meets ancestral eurosid gene order
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3817805/
https://www.ncbi.nlm.nih.gov/pubmed/24564362
http://dx.doi.org/10.1186/1471-2164-14-S7-S3
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