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Homoeolog expression bias in allopolyploid oleaginous marine diatom Fistulifera solaris

BACKGROUND: Allopolyploidy is a genomic structure wherein two or more sets of chromosomes derived from divergent parental species coexist within an organism. It is a prevalent genomic configuration in plants, as an important source of genetic variation, and also frequently confers environmental adap...

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Autores principales: Nomaguchi, Tatsuhiro, Maeda, Yoshiaki, Yoshino, Tomoko, Asahi, Toru, Tirichine, Leila, Bowler, Chris, Tanaka, Tsuyoshi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5935921/
https://www.ncbi.nlm.nih.gov/pubmed/29728068
http://dx.doi.org/10.1186/s12864-018-4691-0
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author Nomaguchi, Tatsuhiro
Maeda, Yoshiaki
Yoshino, Tomoko
Asahi, Toru
Tirichine, Leila
Bowler, Chris
Tanaka, Tsuyoshi
author_facet Nomaguchi, Tatsuhiro
Maeda, Yoshiaki
Yoshino, Tomoko
Asahi, Toru
Tirichine, Leila
Bowler, Chris
Tanaka, Tsuyoshi
author_sort Nomaguchi, Tatsuhiro
collection PubMed
description BACKGROUND: Allopolyploidy is a genomic structure wherein two or more sets of chromosomes derived from divergent parental species coexist within an organism. It is a prevalent genomic configuration in plants, as an important source of genetic variation, and also frequently confers environmental adaptability and increased crop productivity. We previously reported the oleaginous marine diatom Fistulifera solaris JPCC DA0580 to be a promising host for biofuel production and that its genome is allopolyploid, which had never previously been reported in eukaryotic microalgae. However, the study of allopolyploidy in F. solaris was hindered by the difficulty in classifying the homoeologous genes based on their progenitor origins, owing to the shortage of diatom genomic references. RESULTS: In this study, the allopolyploid genome of F. solaris was tentatively classified into two pseudo-parental subgenomes using sequence analysis based on GC content and codon frequency in each homoeologous gene pair. This approach clearly separated the genome into two distinct fractions, subgenome Fso_h and Fso_l, which also showed the potency of codon usage analysis to differentiate the allopolyploid subgenome. Subsequent homoeolog expression bias analysis revealed that, although both subgenomes appear to contribute to global transcription, there were subgenomic preferences in approximately 61% of homoeologous gene pairs, and the majority of these genes showed continuous bias towards a specific subgenome during lipid accumulation. Additional promoter analysis indicated the possibility of promoter motifs involved in biased transcription of homoeologous genes. Among these subgenomic preferences, genes involved in lipid metabolic pathways showed interesting patterns in that biosynthetic and degradative pathways showed opposite subgenomic preferences, suggesting the possibility that the oleaginous characteristics of F. solaris derived from one of its progenitors. CONCLUSIONS: We report the detailed genomic structure and expression patterns in the allopolyploid eukaryotic microalga F. solaris. The allele-specific patterns reported may contribute to the oleaginous characteristics of F. solaris and also suggest the robust oleaginous characteristics of one of its progenitors. Our data reveal novel aspects of allopolyploidy in a diatom that is not only important for evolutionary studies but may also be advantageous for biofuel production in microalgae. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4691-0) contains supplementary material, which is available to authorized users.
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spelling pubmed-59359212018-05-11 Homoeolog expression bias in allopolyploid oleaginous marine diatom Fistulifera solaris Nomaguchi, Tatsuhiro Maeda, Yoshiaki Yoshino, Tomoko Asahi, Toru Tirichine, Leila Bowler, Chris Tanaka, Tsuyoshi BMC Genomics Research Article BACKGROUND: Allopolyploidy is a genomic structure wherein two or more sets of chromosomes derived from divergent parental species coexist within an organism. It is a prevalent genomic configuration in plants, as an important source of genetic variation, and also frequently confers environmental adaptability and increased crop productivity. We previously reported the oleaginous marine diatom Fistulifera solaris JPCC DA0580 to be a promising host for biofuel production and that its genome is allopolyploid, which had never previously been reported in eukaryotic microalgae. However, the study of allopolyploidy in F. solaris was hindered by the difficulty in classifying the homoeologous genes based on their progenitor origins, owing to the shortage of diatom genomic references. RESULTS: In this study, the allopolyploid genome of F. solaris was tentatively classified into two pseudo-parental subgenomes using sequence analysis based on GC content and codon frequency in each homoeologous gene pair. This approach clearly separated the genome into two distinct fractions, subgenome Fso_h and Fso_l, which also showed the potency of codon usage analysis to differentiate the allopolyploid subgenome. Subsequent homoeolog expression bias analysis revealed that, although both subgenomes appear to contribute to global transcription, there were subgenomic preferences in approximately 61% of homoeologous gene pairs, and the majority of these genes showed continuous bias towards a specific subgenome during lipid accumulation. Additional promoter analysis indicated the possibility of promoter motifs involved in biased transcription of homoeologous genes. Among these subgenomic preferences, genes involved in lipid metabolic pathways showed interesting patterns in that biosynthetic and degradative pathways showed opposite subgenomic preferences, suggesting the possibility that the oleaginous characteristics of F. solaris derived from one of its progenitors. CONCLUSIONS: We report the detailed genomic structure and expression patterns in the allopolyploid eukaryotic microalga F. solaris. The allele-specific patterns reported may contribute to the oleaginous characteristics of F. solaris and also suggest the robust oleaginous characteristics of one of its progenitors. Our data reveal novel aspects of allopolyploidy in a diatom that is not only important for evolutionary studies but may also be advantageous for biofuel production in microalgae. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4691-0) contains supplementary material, which is available to authorized users. BioMed Central 2018-05-04 /pmc/articles/PMC5935921/ /pubmed/29728068 http://dx.doi.org/10.1186/s12864-018-4691-0 Text en © The Author(s). 2018 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
Nomaguchi, Tatsuhiro
Maeda, Yoshiaki
Yoshino, Tomoko
Asahi, Toru
Tirichine, Leila
Bowler, Chris
Tanaka, Tsuyoshi
Homoeolog expression bias in allopolyploid oleaginous marine diatom Fistulifera solaris
title Homoeolog expression bias in allopolyploid oleaginous marine diatom Fistulifera solaris
title_full Homoeolog expression bias in allopolyploid oleaginous marine diatom Fistulifera solaris
title_fullStr Homoeolog expression bias in allopolyploid oleaginous marine diatom Fistulifera solaris
title_full_unstemmed Homoeolog expression bias in allopolyploid oleaginous marine diatom Fistulifera solaris
title_short Homoeolog expression bias in allopolyploid oleaginous marine diatom Fistulifera solaris
title_sort homoeolog expression bias in allopolyploid oleaginous marine diatom fistulifera solaris
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5935921/
https://www.ncbi.nlm.nih.gov/pubmed/29728068
http://dx.doi.org/10.1186/s12864-018-4691-0
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