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Maternal patterns of inheritance alter transcript expression in eggs

BACKGROUND: Modifications to early development can lead to evolutionary diversification. The early stages of development are under maternal control, as mothers produce eggs loaded with nutrients, proteins and mRNAs that direct early embryogenesis. Maternally provided mRNAs are the only expressed gen...

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Autores principales: Harry, Nathan D., Zakas, Christina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10084599/
https://www.ncbi.nlm.nih.gov/pubmed/37038099
http://dx.doi.org/10.1186/s12864-023-09291-8
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author Harry, Nathan D.
Zakas, Christina
author_facet Harry, Nathan D.
Zakas, Christina
author_sort Harry, Nathan D.
collection PubMed
description BACKGROUND: Modifications to early development can lead to evolutionary diversification. The early stages of development are under maternal control, as mothers produce eggs loaded with nutrients, proteins and mRNAs that direct early embryogenesis. Maternally provided mRNAs are the only expressed genes in initial stages of development and are tightly regulated. Differences in maternal mRNA provisioning could lead to phenotypic changes in embryogenesis and ultimately evolutionary changes in development. However, the extent that maternal mRNA expression in eggs can vary is unknown for most developmental models. Here, we use a species with dimorphic development— where females make eggs and larvae of different sizes and life-history modes—to investigate the extent of variation in maternal mRNA provisioning to the egg. RESULTS: We find that there is significant variation in gene expression across eggs of different development modes, and that there are both qualitative and quantitative differences in mRNA expression. We separate parental effects from allelic effects, and find that both mechanisms contribute to mRNA expression differences. We also find that offspring of intraspecific crosses differentially provision their eggs based on the parental cross direction (a parental effect), which has not been previously demonstrated in reproductive traits like oogenesis. CONCLUSION: We find that maternally controlled initiation of development is functionally distinct between eggs of different sizes and maternal genotypes. Both allele-specific effects and parent-of-origin effects contribute to gene expression differences in eggs. The latter indicates an intergenerational effect where a parent’s genotype can affect gene expression in an egg made by the next generation. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09291-8.
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spelling pubmed-100845992023-04-11 Maternal patterns of inheritance alter transcript expression in eggs Harry, Nathan D. Zakas, Christina BMC Genomics Research BACKGROUND: Modifications to early development can lead to evolutionary diversification. The early stages of development are under maternal control, as mothers produce eggs loaded with nutrients, proteins and mRNAs that direct early embryogenesis. Maternally provided mRNAs are the only expressed genes in initial stages of development and are tightly regulated. Differences in maternal mRNA provisioning could lead to phenotypic changes in embryogenesis and ultimately evolutionary changes in development. However, the extent that maternal mRNA expression in eggs can vary is unknown for most developmental models. Here, we use a species with dimorphic development— where females make eggs and larvae of different sizes and life-history modes—to investigate the extent of variation in maternal mRNA provisioning to the egg. RESULTS: We find that there is significant variation in gene expression across eggs of different development modes, and that there are both qualitative and quantitative differences in mRNA expression. We separate parental effects from allelic effects, and find that both mechanisms contribute to mRNA expression differences. We also find that offspring of intraspecific crosses differentially provision their eggs based on the parental cross direction (a parental effect), which has not been previously demonstrated in reproductive traits like oogenesis. CONCLUSION: We find that maternally controlled initiation of development is functionally distinct between eggs of different sizes and maternal genotypes. Both allele-specific effects and parent-of-origin effects contribute to gene expression differences in eggs. The latter indicates an intergenerational effect where a parent’s genotype can affect gene expression in an egg made by the next generation. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09291-8. BioMed Central 2023-04-10 /pmc/articles/PMC10084599/ /pubmed/37038099 http://dx.doi.org/10.1186/s12864-023-09291-8 Text en © The Author(s) 2023 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
Harry, Nathan D.
Zakas, Christina
Maternal patterns of inheritance alter transcript expression in eggs
title Maternal patterns of inheritance alter transcript expression in eggs
title_full Maternal patterns of inheritance alter transcript expression in eggs
title_fullStr Maternal patterns of inheritance alter transcript expression in eggs
title_full_unstemmed Maternal patterns of inheritance alter transcript expression in eggs
title_short Maternal patterns of inheritance alter transcript expression in eggs
title_sort maternal patterns of inheritance alter transcript expression in eggs
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10084599/
https://www.ncbi.nlm.nih.gov/pubmed/37038099
http://dx.doi.org/10.1186/s12864-023-09291-8
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