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Multi-tissue RNA-Seq Analysis and Long-read-based Genome Assembly Reveal Complex Sex-specific Gene Regulation and Molecular Evolution in the Manila Clam
The molecular factors and gene regulation involved in sex determination and gonad differentiation in bivalve molluscs are unknown. It has been suggested that doubly uniparental inheritance (DUI) of mitochondria may be involved in these processes in species such as the ubiquitous and commercially rel...
Autores principales: | , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9803972/ https://www.ncbi.nlm.nih.gov/pubmed/36508337 http://dx.doi.org/10.1093/gbe/evac171 |
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author | Xu, Ran Martelossi, Jacopo Smits, Morgan Iannello, Mariangela Peruzza, Luca Babbucci, Massimiliano Milan, Massimo Dunham, Joseph P Breton, Sophie Milani, Liliana Nuzhdin, Sergey V Bargelloni, Luca Passamonti, Marco Ghiselli, Fabrizio |
author_facet | Xu, Ran Martelossi, Jacopo Smits, Morgan Iannello, Mariangela Peruzza, Luca Babbucci, Massimiliano Milan, Massimo Dunham, Joseph P Breton, Sophie Milani, Liliana Nuzhdin, Sergey V Bargelloni, Luca Passamonti, Marco Ghiselli, Fabrizio |
author_sort | Xu, Ran |
collection | PubMed |
description | The molecular factors and gene regulation involved in sex determination and gonad differentiation in bivalve molluscs are unknown. It has been suggested that doubly uniparental inheritance (DUI) of mitochondria may be involved in these processes in species such as the ubiquitous and commercially relevant Manila clam, Ruditapes philippinarum. We present the first long-read-based de novo genome assembly of a Manila clam, and a RNA-Seq multi-tissue analysis of 15 females and 15 males. The highly contiguous genome assembly was used as reference to investigate gene expression, alternative splicing, sequence evolution, tissue-specific co-expression networks, and sexual contrasting SNPs. Differential expression (DE) and differential splicing (DS) analyses revealed sex-specific transcriptional regulation in gonads, but not in somatic tissues. Co-expression networks revealed complex gene regulation in gonads, and genes in gonad-associated modules showed high tissue specificity. However, male gonad-associated modules showed contrasting patterns of sequence evolution and tissue specificity. One gene set was related to the structural organization of male gametes and presented slow sequence evolution but high pleiotropy, whereas another gene set was enriched in reproduction-related processes and characterized by fast sequence evolution and tissue specificity. Sexual contrasting SNPs were found in genes overrepresented in mitochondrial-related functions, providing new candidates for investigating the relationship between mitochondria and sex in DUI species. Together, these results increase our understanding of the role of DE, DS, and sequence evolution of sex-specific genes in an understudied taxon. We also provide resourceful genomic data for studies regarding sex diagnosis and breeding in bivalves. |
format | Online Article Text |
id | pubmed-9803972 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-98039722023-01-03 Multi-tissue RNA-Seq Analysis and Long-read-based Genome Assembly Reveal Complex Sex-specific Gene Regulation and Molecular Evolution in the Manila Clam Xu, Ran Martelossi, Jacopo Smits, Morgan Iannello, Mariangela Peruzza, Luca Babbucci, Massimiliano Milan, Massimo Dunham, Joseph P Breton, Sophie Milani, Liliana Nuzhdin, Sergey V Bargelloni, Luca Passamonti, Marco Ghiselli, Fabrizio Genome Biol Evol Research Article The molecular factors and gene regulation involved in sex determination and gonad differentiation in bivalve molluscs are unknown. It has been suggested that doubly uniparental inheritance (DUI) of mitochondria may be involved in these processes in species such as the ubiquitous and commercially relevant Manila clam, Ruditapes philippinarum. We present the first long-read-based de novo genome assembly of a Manila clam, and a RNA-Seq multi-tissue analysis of 15 females and 15 males. The highly contiguous genome assembly was used as reference to investigate gene expression, alternative splicing, sequence evolution, tissue-specific co-expression networks, and sexual contrasting SNPs. Differential expression (DE) and differential splicing (DS) analyses revealed sex-specific transcriptional regulation in gonads, but not in somatic tissues. Co-expression networks revealed complex gene regulation in gonads, and genes in gonad-associated modules showed high tissue specificity. However, male gonad-associated modules showed contrasting patterns of sequence evolution and tissue specificity. One gene set was related to the structural organization of male gametes and presented slow sequence evolution but high pleiotropy, whereas another gene set was enriched in reproduction-related processes and characterized by fast sequence evolution and tissue specificity. Sexual contrasting SNPs were found in genes overrepresented in mitochondrial-related functions, providing new candidates for investigating the relationship between mitochondria and sex in DUI species. Together, these results increase our understanding of the role of DE, DS, and sequence evolution of sex-specific genes in an understudied taxon. We also provide resourceful genomic data for studies regarding sex diagnosis and breeding in bivalves. Oxford University Press 2022-12-12 /pmc/articles/PMC9803972/ /pubmed/36508337 http://dx.doi.org/10.1093/gbe/evac171 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Research Article Xu, Ran Martelossi, Jacopo Smits, Morgan Iannello, Mariangela Peruzza, Luca Babbucci, Massimiliano Milan, Massimo Dunham, Joseph P Breton, Sophie Milani, Liliana Nuzhdin, Sergey V Bargelloni, Luca Passamonti, Marco Ghiselli, Fabrizio Multi-tissue RNA-Seq Analysis and Long-read-based Genome Assembly Reveal Complex Sex-specific Gene Regulation and Molecular Evolution in the Manila Clam |
title | Multi-tissue RNA-Seq Analysis and Long-read-based Genome Assembly Reveal Complex Sex-specific Gene Regulation and Molecular Evolution in the Manila Clam |
title_full | Multi-tissue RNA-Seq Analysis and Long-read-based Genome Assembly Reveal Complex Sex-specific Gene Regulation and Molecular Evolution in the Manila Clam |
title_fullStr | Multi-tissue RNA-Seq Analysis and Long-read-based Genome Assembly Reveal Complex Sex-specific Gene Regulation and Molecular Evolution in the Manila Clam |
title_full_unstemmed | Multi-tissue RNA-Seq Analysis and Long-read-based Genome Assembly Reveal Complex Sex-specific Gene Regulation and Molecular Evolution in the Manila Clam |
title_short | Multi-tissue RNA-Seq Analysis and Long-read-based Genome Assembly Reveal Complex Sex-specific Gene Regulation and Molecular Evolution in the Manila Clam |
title_sort | multi-tissue rna-seq analysis and long-read-based genome assembly reveal complex sex-specific gene regulation and molecular evolution in the manila clam |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9803972/ https://www.ncbi.nlm.nih.gov/pubmed/36508337 http://dx.doi.org/10.1093/gbe/evac171 |
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