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Using RNA sequencing to characterize female reproductive genes between Z and E Strains of European Corn Borer moth (Ostrinia nubilalis)

BACKGROUND: Reproductive proteins often evolve rapidly and are thought to be subject to strong sexual selection, and thus may play a key role in reproductive isolation and species divergence. However, our knowledge of reproductive proteins has been largely limited to males and model organisms with s...

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Autores principales: Al-Wathiqui, Nooria, Lewis, Sara M, Dopman, Erik B
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4007636/
https://www.ncbi.nlm.nih.gov/pubmed/24621199
http://dx.doi.org/10.1186/1471-2164-15-189
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author Al-Wathiqui, Nooria
Lewis, Sara M
Dopman, Erik B
author_facet Al-Wathiqui, Nooria
Lewis, Sara M
Dopman, Erik B
author_sort Al-Wathiqui, Nooria
collection PubMed
description BACKGROUND: Reproductive proteins often evolve rapidly and are thought to be subject to strong sexual selection, and thus may play a key role in reproductive isolation and species divergence. However, our knowledge of reproductive proteins has been largely limited to males and model organisms with sequenced genomes. With advances in sequencing technology, Lepidoptera are emerging models for studies of sexual selection and speciation. By profiling the transcriptomes of the bursa copulatrix and bursal gland from females of two incipient species of moth, we characterize reproductive genes expressed in the primary reproductive tissues of female Lepidoptera and identify candidate genes contributing to a one-way gametic incompatibility between Z and E strains of the European corn borer (Ostrinia nubilalis). RESULTS: Using RNA sequencing we identified transcripts from ~37,000 and ~36,000 loci that were expressed in the bursa copulatrix or the bursal gland respectively. Of bursa copulatrix genes, 8% were significantly differentially expressed compared to the female thorax, and those that were up-regulated or specific to the bursa copulatrix showed functional biases toward muscle activity and/or organization. In the bursal gland, 9% of genes were differentially expressed compared to the thorax, with many showing reproduction or gamete production functions. Of up-regulated bursal gland genes, 46% contained a transmembrane region and 16% possessed secretion signal peptides. Divergently expressed genes in the bursa copulatrix were exclusively biased toward protease-like functions and 51 proteases or protease inhibitors were divergently expressed overall. CONCLUSIONS: This is the first comprehensive characterization of female reproductive genes in any lepidopteran system. The transcriptome of the bursa copulatrix supports its role as a muscular sac that is the primary site for disruption of the male ejaculate. We find that the bursal gland acts as a reproductive secretory body that might also interact with male ejaculate. In addition, differential expression of proteases between strains supports a potential role for these tissues in contributing to reproductive isolation. Our study provides new insight into how male ejaculate is processed by female Lepidoptera, and paves the way for future work on interactions between post-mating sexual selection and speciation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-189) contains supplementary material, which is available to authorized users.
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spelling pubmed-40076362014-05-03 Using RNA sequencing to characterize female reproductive genes between Z and E Strains of European Corn Borer moth (Ostrinia nubilalis) Al-Wathiqui, Nooria Lewis, Sara M Dopman, Erik B BMC Genomics Research Article BACKGROUND: Reproductive proteins often evolve rapidly and are thought to be subject to strong sexual selection, and thus may play a key role in reproductive isolation and species divergence. However, our knowledge of reproductive proteins has been largely limited to males and model organisms with sequenced genomes. With advances in sequencing technology, Lepidoptera are emerging models for studies of sexual selection and speciation. By profiling the transcriptomes of the bursa copulatrix and bursal gland from females of two incipient species of moth, we characterize reproductive genes expressed in the primary reproductive tissues of female Lepidoptera and identify candidate genes contributing to a one-way gametic incompatibility between Z and E strains of the European corn borer (Ostrinia nubilalis). RESULTS: Using RNA sequencing we identified transcripts from ~37,000 and ~36,000 loci that were expressed in the bursa copulatrix or the bursal gland respectively. Of bursa copulatrix genes, 8% were significantly differentially expressed compared to the female thorax, and those that were up-regulated or specific to the bursa copulatrix showed functional biases toward muscle activity and/or organization. In the bursal gland, 9% of genes were differentially expressed compared to the thorax, with many showing reproduction or gamete production functions. Of up-regulated bursal gland genes, 46% contained a transmembrane region and 16% possessed secretion signal peptides. Divergently expressed genes in the bursa copulatrix were exclusively biased toward protease-like functions and 51 proteases or protease inhibitors were divergently expressed overall. CONCLUSIONS: This is the first comprehensive characterization of female reproductive genes in any lepidopteran system. The transcriptome of the bursa copulatrix supports its role as a muscular sac that is the primary site for disruption of the male ejaculate. We find that the bursal gland acts as a reproductive secretory body that might also interact with male ejaculate. In addition, differential expression of proteases between strains supports a potential role for these tissues in contributing to reproductive isolation. Our study provides new insight into how male ejaculate is processed by female Lepidoptera, and paves the way for future work on interactions between post-mating sexual selection and speciation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-189) contains supplementary material, which is available to authorized users. BioMed Central 2014-03-12 /pmc/articles/PMC4007636/ /pubmed/24621199 http://dx.doi.org/10.1186/1471-2164-15-189 Text en © Al-Wathiqui 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
Al-Wathiqui, Nooria
Lewis, Sara M
Dopman, Erik B
Using RNA sequencing to characterize female reproductive genes between Z and E Strains of European Corn Borer moth (Ostrinia nubilalis)
title Using RNA sequencing to characterize female reproductive genes between Z and E Strains of European Corn Borer moth (Ostrinia nubilalis)
title_full Using RNA sequencing to characterize female reproductive genes between Z and E Strains of European Corn Borer moth (Ostrinia nubilalis)
title_fullStr Using RNA sequencing to characterize female reproductive genes between Z and E Strains of European Corn Borer moth (Ostrinia nubilalis)
title_full_unstemmed Using RNA sequencing to characterize female reproductive genes between Z and E Strains of European Corn Borer moth (Ostrinia nubilalis)
title_short Using RNA sequencing to characterize female reproductive genes between Z and E Strains of European Corn Borer moth (Ostrinia nubilalis)
title_sort using rna sequencing to characterize female reproductive genes between z and e strains of european corn borer moth (ostrinia nubilalis)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4007636/
https://www.ncbi.nlm.nih.gov/pubmed/24621199
http://dx.doi.org/10.1186/1471-2164-15-189
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