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Natural variation in the maternal and zygotic mRNA complements of the early embryo in Drosophila melanogaster

BACKGROUND: Maternal gene products supplied to the egg during oogenesis drive the earliest events of development in all metazoans. After the initial stages of embryogenesis, maternal transcripts are degraded as zygotic transcription is activated; this is known as the maternal to zygotic transition (...

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Autores principales: Feitzinger, Anna A., Le, Anthony, Thompson, Ammon, Haseeb, Mehnoor, Murugesan, Mohan Koumar, Tang, Austin M., Lott, Susan E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9461177/
https://www.ncbi.nlm.nih.gov/pubmed/36076188
http://dx.doi.org/10.1186/s12864-022-08839-4
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author Feitzinger, Anna A.
Le, Anthony
Thompson, Ammon
Haseeb, Mehnoor
Murugesan, Mohan Koumar
Tang, Austin M.
Lott, Susan E.
author_facet Feitzinger, Anna A.
Le, Anthony
Thompson, Ammon
Haseeb, Mehnoor
Murugesan, Mohan Koumar
Tang, Austin M.
Lott, Susan E.
author_sort Feitzinger, Anna A.
collection PubMed
description BACKGROUND: Maternal gene products supplied to the egg during oogenesis drive the earliest events of development in all metazoans. After the initial stages of embryogenesis, maternal transcripts are degraded as zygotic transcription is activated; this is known as the maternal to zygotic transition (MZT). Recently, it has been shown that the expression of maternal and zygotic transcripts have evolved in the Drosophila genus over the course of 50 million years. However, the extent of natural variation of maternal and zygotic transcripts within a species has yet to be determined. We asked how the maternal and zygotic pools of mRNA vary within and between populations of D. melanogaster. In order to maximize sampling of genetic diversity, African lines of D. melanogaster originating from Zambia as well as DGRP lines originating from North America were chosen for transcriptomic analysis. RESULTS: Generally, we find that maternal transcripts are more highly conserved, and zygotic transcripts evolve at a higher rate. We find that there is more within-population variation in transcript abundance than between populations and that expression variation is highest post- MZT between African lines. CONCLUSIONS: Determining the natural variation of gene expression surrounding the MZT in natural populations of D. melanogaster gives insight into the extent of how a tightly regulated process may vary within a species, the extent of developmental constraint at both stages and on both the maternal and zygotic genomes, and reveals expression changes allowing this species to adapt as it spread across the world. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08839-4.
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spelling pubmed-94611772022-09-10 Natural variation in the maternal and zygotic mRNA complements of the early embryo in Drosophila melanogaster Feitzinger, Anna A. Le, Anthony Thompson, Ammon Haseeb, Mehnoor Murugesan, Mohan Koumar Tang, Austin M. Lott, Susan E. BMC Genomics Research Article BACKGROUND: Maternal gene products supplied to the egg during oogenesis drive the earliest events of development in all metazoans. After the initial stages of embryogenesis, maternal transcripts are degraded as zygotic transcription is activated; this is known as the maternal to zygotic transition (MZT). Recently, it has been shown that the expression of maternal and zygotic transcripts have evolved in the Drosophila genus over the course of 50 million years. However, the extent of natural variation of maternal and zygotic transcripts within a species has yet to be determined. We asked how the maternal and zygotic pools of mRNA vary within and between populations of D. melanogaster. In order to maximize sampling of genetic diversity, African lines of D. melanogaster originating from Zambia as well as DGRP lines originating from North America were chosen for transcriptomic analysis. RESULTS: Generally, we find that maternal transcripts are more highly conserved, and zygotic transcripts evolve at a higher rate. We find that there is more within-population variation in transcript abundance than between populations and that expression variation is highest post- MZT between African lines. CONCLUSIONS: Determining the natural variation of gene expression surrounding the MZT in natural populations of D. melanogaster gives insight into the extent of how a tightly regulated process may vary within a species, the extent of developmental constraint at both stages and on both the maternal and zygotic genomes, and reveals expression changes allowing this species to adapt as it spread across the world. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08839-4. BioMed Central 2022-09-08 /pmc/articles/PMC9461177/ /pubmed/36076188 http://dx.doi.org/10.1186/s12864-022-08839-4 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Feitzinger, Anna A.
Le, Anthony
Thompson, Ammon
Haseeb, Mehnoor
Murugesan, Mohan Koumar
Tang, Austin M.
Lott, Susan E.
Natural variation in the maternal and zygotic mRNA complements of the early embryo in Drosophila melanogaster
title Natural variation in the maternal and zygotic mRNA complements of the early embryo in Drosophila melanogaster
title_full Natural variation in the maternal and zygotic mRNA complements of the early embryo in Drosophila melanogaster
title_fullStr Natural variation in the maternal and zygotic mRNA complements of the early embryo in Drosophila melanogaster
title_full_unstemmed Natural variation in the maternal and zygotic mRNA complements of the early embryo in Drosophila melanogaster
title_short Natural variation in the maternal and zygotic mRNA complements of the early embryo in Drosophila melanogaster
title_sort natural variation in the maternal and zygotic mrna complements of the early embryo in drosophila melanogaster
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9461177/
https://www.ncbi.nlm.nih.gov/pubmed/36076188
http://dx.doi.org/10.1186/s12864-022-08839-4
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