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Effect of paleopolyploidy and allopolyploidy on gene expression in banana

BACKGROUND: Bananas (Musa spp.) are an important crop worldwide. Most modern cultivars resulted from a complex polyploidization history that comprised three whole genome duplications (WGDs) shaping the haploid Musa genome, followed by inter- and intra-specific crosses between Musa acuminata and M. b...

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Autores principales: Cenci, Alberto, Hueber, Yann, Zorrilla-Fontanesi, Yasmin, van Wesemael, Jelle, Kissel, Ewaut, Gislard, Marie, Sardos, Julie, Swennen, Rony, Roux, Nicolas, Carpentier, Sebastien Christian, Rouard, Mathieu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6438041/
https://www.ncbi.nlm.nih.gov/pubmed/30917780
http://dx.doi.org/10.1186/s12864-019-5618-0
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author Cenci, Alberto
Hueber, Yann
Zorrilla-Fontanesi, Yasmin
van Wesemael, Jelle
Kissel, Ewaut
Gislard, Marie
Sardos, Julie
Swennen, Rony
Roux, Nicolas
Carpentier, Sebastien Christian
Rouard, Mathieu
author_facet Cenci, Alberto
Hueber, Yann
Zorrilla-Fontanesi, Yasmin
van Wesemael, Jelle
Kissel, Ewaut
Gislard, Marie
Sardos, Julie
Swennen, Rony
Roux, Nicolas
Carpentier, Sebastien Christian
Rouard, Mathieu
author_sort Cenci, Alberto
collection PubMed
description BACKGROUND: Bananas (Musa spp.) are an important crop worldwide. Most modern cultivars resulted from a complex polyploidization history that comprised three whole genome duplications (WGDs) shaping the haploid Musa genome, followed by inter- and intra-specific crosses between Musa acuminata and M. balbisiana (A and B genome, respectively). Unresolved hybridizations finally led to banana diversification into several autotriploid (AAA) and allotriploid cultivars (AAB and ABB). Using transcriptomic data, we investigated the impact of the genome structure on gene expression patterns in roots of 12 different triploid genotypes covering AAA, AAB and ABB subgenome constitutions. RESULTS: We demonstrate that (i) there are different genome structures, (ii) expression patterns go beyond the predicted genomic groups, and (iii) the proportion of the B genome influences the gene expression. The presence of the B genome is associated with a higher expression of genes involved in flavonoid biosynthesis, fatty acid metabolism, amino sugar and nucleotide sugar metabolism and oxidative phosphorylation. There are cultivar-specific chromosome regions with biased B:A gene expression ratios that demonstrate homoeologous exchanges (HE) between A and B sub-genomes. In two cultivars, aneuploidy was detected. We identified 3674 genes with a different expression level between allotriploid and autotriploid with ~ 57% having recently duplicated copies (paralogous). We propose a Paralog Inclusive Expression (PIE) analysis that appears to be suitable for genomes still in a downsizing and fractionation process following whole genome duplications. Our approach allows highlighting the genes with a maximum likelihood to affect the plant phenotype. CONCLUSIONS: This study on banana is a good case to investigate the effects of alloploidy in crops. We conclude that allopolyploidy triggered changes in the genome structure of a crop and it clearly influences the gene. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5618-0) contains supplementary material, which is available to authorized users.
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spelling pubmed-64380412019-04-08 Effect of paleopolyploidy and allopolyploidy on gene expression in banana Cenci, Alberto Hueber, Yann Zorrilla-Fontanesi, Yasmin van Wesemael, Jelle Kissel, Ewaut Gislard, Marie Sardos, Julie Swennen, Rony Roux, Nicolas Carpentier, Sebastien Christian Rouard, Mathieu BMC Genomics Research Article BACKGROUND: Bananas (Musa spp.) are an important crop worldwide. Most modern cultivars resulted from a complex polyploidization history that comprised three whole genome duplications (WGDs) shaping the haploid Musa genome, followed by inter- and intra-specific crosses between Musa acuminata and M. balbisiana (A and B genome, respectively). Unresolved hybridizations finally led to banana diversification into several autotriploid (AAA) and allotriploid cultivars (AAB and ABB). Using transcriptomic data, we investigated the impact of the genome structure on gene expression patterns in roots of 12 different triploid genotypes covering AAA, AAB and ABB subgenome constitutions. RESULTS: We demonstrate that (i) there are different genome structures, (ii) expression patterns go beyond the predicted genomic groups, and (iii) the proportion of the B genome influences the gene expression. The presence of the B genome is associated with a higher expression of genes involved in flavonoid biosynthesis, fatty acid metabolism, amino sugar and nucleotide sugar metabolism and oxidative phosphorylation. There are cultivar-specific chromosome regions with biased B:A gene expression ratios that demonstrate homoeologous exchanges (HE) between A and B sub-genomes. In two cultivars, aneuploidy was detected. We identified 3674 genes with a different expression level between allotriploid and autotriploid with ~ 57% having recently duplicated copies (paralogous). We propose a Paralog Inclusive Expression (PIE) analysis that appears to be suitable for genomes still in a downsizing and fractionation process following whole genome duplications. Our approach allows highlighting the genes with a maximum likelihood to affect the plant phenotype. CONCLUSIONS: This study on banana is a good case to investigate the effects of alloploidy in crops. We conclude that allopolyploidy triggered changes in the genome structure of a crop and it clearly influences the gene. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5618-0) contains supplementary material, which is available to authorized users. BioMed Central 2019-03-27 /pmc/articles/PMC6438041/ /pubmed/30917780 http://dx.doi.org/10.1186/s12864-019-5618-0 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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
Cenci, Alberto
Hueber, Yann
Zorrilla-Fontanesi, Yasmin
van Wesemael, Jelle
Kissel, Ewaut
Gislard, Marie
Sardos, Julie
Swennen, Rony
Roux, Nicolas
Carpentier, Sebastien Christian
Rouard, Mathieu
Effect of paleopolyploidy and allopolyploidy on gene expression in banana
title Effect of paleopolyploidy and allopolyploidy on gene expression in banana
title_full Effect of paleopolyploidy and allopolyploidy on gene expression in banana
title_fullStr Effect of paleopolyploidy and allopolyploidy on gene expression in banana
title_full_unstemmed Effect of paleopolyploidy and allopolyploidy on gene expression in banana
title_short Effect of paleopolyploidy and allopolyploidy on gene expression in banana
title_sort effect of paleopolyploidy and allopolyploidy on gene expression in banana
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6438041/
https://www.ncbi.nlm.nih.gov/pubmed/30917780
http://dx.doi.org/10.1186/s12864-019-5618-0
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