Intergenomic gene transfer in diploid and allopolyploid Gossypium
Abstract Background Intergenomic gene transfer (IGT) between nuclear and organellar genomes is a common phenomenon during plant evolution. Gossypium is a useful model to evaluate the genomic consequences of IGT for both diploid and polyploid species. Here, we explore IGT among nuclear, mitochondrial...
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doaj-e8462efa504d4154bfa0faf73cbda4212020-11-25T04:09:42ZengBMCBMC Plant Biology1471-22292019-11-0119111810.1186/s12870-019-2041-2Intergenomic gene transfer in diploid and allopolyploid GossypiumNan Zhao0Corrinne E. Grover1Zhiwen Chen2Jonathan F. Wendel3Jinping Hua4Laboratory of Cotton Genetics, Genomics and Breeding /Joint Laboratory for International Cooperation in Crop Molecular Breeding, Ministry of Education / Key Laboratory of Crop Heterosis and Utilization of Ministry of Education, College of Agronomy and Biotechnology, China Agricultural UniversityDepartment of Ecology, Evolution and Organismal Biology, Iowa State UniversityLaboratory of Cotton Genetics, Genomics and Breeding /Joint Laboratory for International Cooperation in Crop Molecular Breeding, Ministry of Education / Key Laboratory of Crop Heterosis and Utilization of Ministry of Education, College of Agronomy and Biotechnology, China Agricultural UniversityDepartment of Ecology, Evolution and Organismal Biology, Iowa State UniversityLaboratory of Cotton Genetics, Genomics and Breeding /Joint Laboratory for International Cooperation in Crop Molecular Breeding, Ministry of Education / Key Laboratory of Crop Heterosis and Utilization of Ministry of Education, College of Agronomy and Biotechnology, China Agricultural UniversityAbstract Background Intergenomic gene transfer (IGT) between nuclear and organellar genomes is a common phenomenon during plant evolution. Gossypium is a useful model to evaluate the genomic consequences of IGT for both diploid and polyploid species. Here, we explore IGT among nuclear, mitochondrial, and plastid genomes of four cotton species, including two allopolyploids and their model diploid progenitors (genome donors, G. arboreum: A2 and G. raimondii: D5). Results Extensive IGT events exist for both diploid and allotetraploid cotton (Gossypium) species, with the nuclear genome being the predominant recipient of transferred DNA followed by the mitochondrial genome. The nuclear genome has integrated 100 times more foreign sequences than the mitochondrial genome has in total length. In the nucleus, the integrated length of chloroplast DNA (cpDNA) was between 1.87 times (in diploids) to nearly four times (in allopolyploids) greater than that of mitochondrial DNA (mtDNA). In the mitochondrion, the length of nuclear DNA (nuDNA) was typically three times than that of cpDNA. Gossypium mitochondrial genomes integrated three nuclear retrotransposons and eight chloroplast tRNA genes, and incorporated chloroplast DNA prior to divergence between the diploids and allopolyploid formation. For mitochondrial chloroplast-tRNA genes, there were 2-6 bp conserved microhomologies flanking their insertion sites across distantly related genera, which increased to 10 bp microhomologies for the four cotton species studied. For organellar DNA sequences, there are source hotspots, e.g., the atp6-trnW intergenic region in the mitochondrion and the inverted repeat region in the chloroplast. Organellar DNAs in the nucleus were rarely expressed, and at low levels. Surprisingly, there was asymmetry in the survivorship of ancestral insertions following allopolyploidy, with most numts (nuclear mitochondrial insertions) decaying or being lost whereas most nupts (nuclear plastidial insertions) were retained. Conclusions This study characterized and compared intracellular transfer among nuclear and organellar genomes within two cultivated allopolyploids and their ancestral diploid cotton species. A striking asymmetry in the fate of IGTs in allopolyploid cotton was discovered, with numts being preferentially lost relative to nupts. Our results connect intergenomic gene transfer with allotetraploidy and provide new insight into intracellular genome evolution.http://link.springer.com/article/10.1186/s12870-019-2041-2Intergenomic gene transferAllopolyploidizationGossypiumMitochondrial genomeChloroplast genomeNumt |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Nan Zhao Corrinne E. Grover Zhiwen Chen Jonathan F. Wendel Jinping Hua |
spellingShingle |
Nan Zhao Corrinne E. Grover Zhiwen Chen Jonathan F. Wendel Jinping Hua Intergenomic gene transfer in diploid and allopolyploid Gossypium BMC Plant Biology Intergenomic gene transfer Allopolyploidization Gossypium Mitochondrial genome Chloroplast genome Numt |
author_facet |
Nan Zhao Corrinne E. Grover Zhiwen Chen Jonathan F. Wendel Jinping Hua |
author_sort |
Nan Zhao |
title |
Intergenomic gene transfer in diploid and allopolyploid Gossypium |
title_short |
Intergenomic gene transfer in diploid and allopolyploid Gossypium |
title_full |
Intergenomic gene transfer in diploid and allopolyploid Gossypium |
title_fullStr |
Intergenomic gene transfer in diploid and allopolyploid Gossypium |
title_full_unstemmed |
Intergenomic gene transfer in diploid and allopolyploid Gossypium |
title_sort |
intergenomic gene transfer in diploid and allopolyploid gossypium |
publisher |
BMC |
series |
BMC Plant Biology |
issn |
1471-2229 |
publishDate |
2019-11-01 |
description |
Abstract Background Intergenomic gene transfer (IGT) between nuclear and organellar genomes is a common phenomenon during plant evolution. Gossypium is a useful model to evaluate the genomic consequences of IGT for both diploid and polyploid species. Here, we explore IGT among nuclear, mitochondrial, and plastid genomes of four cotton species, including two allopolyploids and their model diploid progenitors (genome donors, G. arboreum: A2 and G. raimondii: D5). Results Extensive IGT events exist for both diploid and allotetraploid cotton (Gossypium) species, with the nuclear genome being the predominant recipient of transferred DNA followed by the mitochondrial genome. The nuclear genome has integrated 100 times more foreign sequences than the mitochondrial genome has in total length. In the nucleus, the integrated length of chloroplast DNA (cpDNA) was between 1.87 times (in diploids) to nearly four times (in allopolyploids) greater than that of mitochondrial DNA (mtDNA). In the mitochondrion, the length of nuclear DNA (nuDNA) was typically three times than that of cpDNA. Gossypium mitochondrial genomes integrated three nuclear retrotransposons and eight chloroplast tRNA genes, and incorporated chloroplast DNA prior to divergence between the diploids and allopolyploid formation. For mitochondrial chloroplast-tRNA genes, there were 2-6 bp conserved microhomologies flanking their insertion sites across distantly related genera, which increased to 10 bp microhomologies for the four cotton species studied. For organellar DNA sequences, there are source hotspots, e.g., the atp6-trnW intergenic region in the mitochondrion and the inverted repeat region in the chloroplast. Organellar DNAs in the nucleus were rarely expressed, and at low levels. Surprisingly, there was asymmetry in the survivorship of ancestral insertions following allopolyploidy, with most numts (nuclear mitochondrial insertions) decaying or being lost whereas most nupts (nuclear plastidial insertions) were retained. Conclusions This study characterized and compared intracellular transfer among nuclear and organellar genomes within two cultivated allopolyploids and their ancestral diploid cotton species. A striking asymmetry in the fate of IGTs in allopolyploid cotton was discovered, with numts being preferentially lost relative to nupts. Our results connect intergenomic gene transfer with allotetraploidy and provide new insight into intracellular genome evolution. |
topic |
Intergenomic gene transfer Allopolyploidization Gossypium Mitochondrial genome Chloroplast genome Numt |
url |
http://link.springer.com/article/10.1186/s12870-019-2041-2 |
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