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Differential retention and expansion of the ancestral genes associated with the paleopolyploidies in modern rosid plants, as revealed by analysis of the extensins super-gene family

BACKGROUND: All modern rosids originated from a common hexapolyploid ancestor, and the genomes of some rosids have undergone one or more cycles of paleopolyploidy. After the duplication of the ancient genome, wholesale gene loss and gene subfunctionalization has occurred. Using the extensin super-ge...

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Autores principales: Guo, Lianhua, Chen, Yingnan, Ye, Ning, Dai, Xiaogang, Yang, Wanxu, Yin, Tongming
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4117974/
https://www.ncbi.nlm.nih.gov/pubmed/25047956
http://dx.doi.org/10.1186/1471-2164-15-612
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author Guo, Lianhua
Chen, Yingnan
Ye, Ning
Dai, Xiaogang
Yang, Wanxu
Yin, Tongming
author_facet Guo, Lianhua
Chen, Yingnan
Ye, Ning
Dai, Xiaogang
Yang, Wanxu
Yin, Tongming
author_sort Guo, Lianhua
collection PubMed
description BACKGROUND: All modern rosids originated from a common hexapolyploid ancestor, and the genomes of some rosids have undergone one or more cycles of paleopolyploidy. After the duplication of the ancient genome, wholesale gene loss and gene subfunctionalization has occurred. Using the extensin super-gene family as an example, we tracked the differential retention and expansion of ancestral extensin genes in four modern rosids, Arabidopsis, Populus, Vitis and Carica, using several analytical methods. RESULTS: The majority of extensin genes in each of the modern rosids were found to originate from different ancestral genes. In Arabidopsis and Populus, almost half of the extensins were paralogous duplicates within the genome of each species. By contrast, no paralogous extensins were detected in Vitis and Carica, which have only undergone the common γ-triplication event. It was noteworthy that a group of extensins containing the IPR006706 domain had actively duplicated in Arabidopsis, giving rise to a neo-extensin around every 3 million years. However, such extensins were absent from, or rare in, the other three rosids. A detailed examination revealed that this group of extensins had proliferated significantly in the genomes of a number of species in the Brassicaceae. We propose that this group of extensins might play important roles in the biology and in the evolution of the Brassicaceae. Our analyses also revealed that nearly all of the paralogous and orthologous extensin-pairs have been under strong purifying selection, leading to the strong conservation of the function of extensins duplicated from the same ancestral gene. CONCLUSIONS: Our analyses show that extensins originating from a common ancestor have been differentially retained and expanded among four modern rosids. Our findings suggest that, if Arabidopsis is used as the model plant, we can only learn a limited amount about the functions of a particular gene family. These results also provide an example of how it is essential to learn the origination of a gene when analyzing its function across different plant species. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-612) contains supplementary material, which is available to authorized users.
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spelling pubmed-41179742014-08-05 Differential retention and expansion of the ancestral genes associated with the paleopolyploidies in modern rosid plants, as revealed by analysis of the extensins super-gene family Guo, Lianhua Chen, Yingnan Ye, Ning Dai, Xiaogang Yang, Wanxu Yin, Tongming BMC Genomics Research Article BACKGROUND: All modern rosids originated from a common hexapolyploid ancestor, and the genomes of some rosids have undergone one or more cycles of paleopolyploidy. After the duplication of the ancient genome, wholesale gene loss and gene subfunctionalization has occurred. Using the extensin super-gene family as an example, we tracked the differential retention and expansion of ancestral extensin genes in four modern rosids, Arabidopsis, Populus, Vitis and Carica, using several analytical methods. RESULTS: The majority of extensin genes in each of the modern rosids were found to originate from different ancestral genes. In Arabidopsis and Populus, almost half of the extensins were paralogous duplicates within the genome of each species. By contrast, no paralogous extensins were detected in Vitis and Carica, which have only undergone the common γ-triplication event. It was noteworthy that a group of extensins containing the IPR006706 domain had actively duplicated in Arabidopsis, giving rise to a neo-extensin around every 3 million years. However, such extensins were absent from, or rare in, the other three rosids. A detailed examination revealed that this group of extensins had proliferated significantly in the genomes of a number of species in the Brassicaceae. We propose that this group of extensins might play important roles in the biology and in the evolution of the Brassicaceae. Our analyses also revealed that nearly all of the paralogous and orthologous extensin-pairs have been under strong purifying selection, leading to the strong conservation of the function of extensins duplicated from the same ancestral gene. CONCLUSIONS: Our analyses show that extensins originating from a common ancestor have been differentially retained and expanded among four modern rosids. Our findings suggest that, if Arabidopsis is used as the model plant, we can only learn a limited amount about the functions of a particular gene family. These results also provide an example of how it is essential to learn the origination of a gene when analyzing its function across different plant species. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-612) contains supplementary material, which is available to authorized users. BioMed Central 2014-07-21 /pmc/articles/PMC4117974/ /pubmed/25047956 http://dx.doi.org/10.1186/1471-2164-15-612 Text en © Guo et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. 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 credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Guo, Lianhua
Chen, Yingnan
Ye, Ning
Dai, Xiaogang
Yang, Wanxu
Yin, Tongming
Differential retention and expansion of the ancestral genes associated with the paleopolyploidies in modern rosid plants, as revealed by analysis of the extensins super-gene family
title Differential retention and expansion of the ancestral genes associated with the paleopolyploidies in modern rosid plants, as revealed by analysis of the extensins super-gene family
title_full Differential retention and expansion of the ancestral genes associated with the paleopolyploidies in modern rosid plants, as revealed by analysis of the extensins super-gene family
title_fullStr Differential retention and expansion of the ancestral genes associated with the paleopolyploidies in modern rosid plants, as revealed by analysis of the extensins super-gene family
title_full_unstemmed Differential retention and expansion of the ancestral genes associated with the paleopolyploidies in modern rosid plants, as revealed by analysis of the extensins super-gene family
title_short Differential retention and expansion of the ancestral genes associated with the paleopolyploidies in modern rosid plants, as revealed by analysis of the extensins super-gene family
title_sort differential retention and expansion of the ancestral genes associated with the paleopolyploidies in modern rosid plants, as revealed by analysis of the extensins super-gene family
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4117974/
https://www.ncbi.nlm.nih.gov/pubmed/25047956
http://dx.doi.org/10.1186/1471-2164-15-612
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