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Ankyrin domain encoding genes from an ancient horizontal transfer are functionally integrated into Nasonia developmental gene regulatory networks

BACKGROUND: How regulatory networks incorporate additional components and how novel genes are functionally integrated into well-established developmental processes are two important and intertwined questions whose answers have major implications for understanding the evolution of development. We rec...

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Autores principales: Pers, Daniel, Lynch, Jeremy A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6161386/
https://www.ncbi.nlm.nih.gov/pubmed/30266092
http://dx.doi.org/10.1186/s13059-018-1526-x
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author Pers, Daniel
Lynch, Jeremy A.
author_facet Pers, Daniel
Lynch, Jeremy A.
author_sort Pers, Daniel
collection PubMed
description BACKGROUND: How regulatory networks incorporate additional components and how novel genes are functionally integrated into well-established developmental processes are two important and intertwined questions whose answers have major implications for understanding the evolution of development. We recently discovered a set of lineage-restricted genes with strong and specific expression patterns along the dorsal-ventral (DV) axis of the embryo of the wasp Nasonia that may serve as a powerful system for addressing these questions. We sought to both understand the evolutionary history of these genes and to determine their functions in the Nasonia DV patterning system. RESULTS: We have found that the novel DV genes are part of a large family of rapidly duplicating and diverging ankyrin domain-encoding genes that originated most likely by horizontal transfer from a prokaryote in a common ancestor of the wasp superfamily Chalcidoidea. We tested the function of those ankyrin-encoding genes expressed along the DV axis and found that they participate in early embryonic DV patterning. We also developed a new wasp model system (Melittobia) and found that some functional integration of ankyrin genes have been preserved for over 90 million years. CONCLUSIONS: Our results indicate that regulatory networks can incorporate novel genes that then become necessary for stable and repeatable outputs. Even a modest role in developmental networks may be enough to allow novel or duplicate genes to be maintained in the genome and become fully integrated network components. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13059-018-1526-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-61613862018-10-01 Ankyrin domain encoding genes from an ancient horizontal transfer are functionally integrated into Nasonia developmental gene regulatory networks Pers, Daniel Lynch, Jeremy A. Genome Biol Research BACKGROUND: How regulatory networks incorporate additional components and how novel genes are functionally integrated into well-established developmental processes are two important and intertwined questions whose answers have major implications for understanding the evolution of development. We recently discovered a set of lineage-restricted genes with strong and specific expression patterns along the dorsal-ventral (DV) axis of the embryo of the wasp Nasonia that may serve as a powerful system for addressing these questions. We sought to both understand the evolutionary history of these genes and to determine their functions in the Nasonia DV patterning system. RESULTS: We have found that the novel DV genes are part of a large family of rapidly duplicating and diverging ankyrin domain-encoding genes that originated most likely by horizontal transfer from a prokaryote in a common ancestor of the wasp superfamily Chalcidoidea. We tested the function of those ankyrin-encoding genes expressed along the DV axis and found that they participate in early embryonic DV patterning. We also developed a new wasp model system (Melittobia) and found that some functional integration of ankyrin genes have been preserved for over 90 million years. CONCLUSIONS: Our results indicate that regulatory networks can incorporate novel genes that then become necessary for stable and repeatable outputs. Even a modest role in developmental networks may be enough to allow novel or duplicate genes to be maintained in the genome and become fully integrated network components. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13059-018-1526-x) contains supplementary material, which is available to authorized users. BioMed Central 2018-09-28 /pmc/articles/PMC6161386/ /pubmed/30266092 http://dx.doi.org/10.1186/s13059-018-1526-x 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
Pers, Daniel
Lynch, Jeremy A.
Ankyrin domain encoding genes from an ancient horizontal transfer are functionally integrated into Nasonia developmental gene regulatory networks
title Ankyrin domain encoding genes from an ancient horizontal transfer are functionally integrated into Nasonia developmental gene regulatory networks
title_full Ankyrin domain encoding genes from an ancient horizontal transfer are functionally integrated into Nasonia developmental gene regulatory networks
title_fullStr Ankyrin domain encoding genes from an ancient horizontal transfer are functionally integrated into Nasonia developmental gene regulatory networks
title_full_unstemmed Ankyrin domain encoding genes from an ancient horizontal transfer are functionally integrated into Nasonia developmental gene regulatory networks
title_short Ankyrin domain encoding genes from an ancient horizontal transfer are functionally integrated into Nasonia developmental gene regulatory networks
title_sort ankyrin domain encoding genes from an ancient horizontal transfer are functionally integrated into nasonia developmental gene regulatory networks
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6161386/
https://www.ncbi.nlm.nih.gov/pubmed/30266092
http://dx.doi.org/10.1186/s13059-018-1526-x
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