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

Abstract 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...

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Main Authors: Daniel Pers, Jeremy A. Lynch
Format: Article
Language:English
Published: BMC 2018-09-01
Series:Genome Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13059-018-1526-x
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spelling doaj-488b8a76ea3945be801f6bc0651656ee2020-11-24T21:50:21ZengBMCGenome Biology1474-760X2018-09-0119112010.1186/s13059-018-1526-xAnkyrin domain encoding genes from an ancient horizontal transfer are functionally integrated into Nasonia developmental gene regulatory networksDaniel Pers0Jeremy A. Lynch1Department of Biological Sciences, University of Illinois at ChicagoDepartment of Biological Sciences, University of Illinois at ChicagoAbstract 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.http://link.springer.com/article/10.1186/s13059-018-1526-xRegulatory networksDevelopmentEvoDevoAnkyrinChalcidoideaNasonia
collection DOAJ
language English
format Article
sources DOAJ
author Daniel Pers
Jeremy A. Lynch
spellingShingle Daniel Pers
Jeremy A. Lynch
Ankyrin domain encoding genes from an ancient horizontal transfer are functionally integrated into Nasonia developmental gene regulatory networks
Genome Biology
Regulatory networks
Development
EvoDevo
Ankyrin
Chalcidoidea
Nasonia
author_facet Daniel Pers
Jeremy A. Lynch
author_sort Daniel Pers
title 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_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_sort ankyrin domain encoding genes from an ancient horizontal transfer are functionally integrated into nasonia developmental gene regulatory networks
publisher BMC
series Genome Biology
issn 1474-760X
publishDate 2018-09-01
description Abstract 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.
topic Regulatory networks
Development
EvoDevo
Ankyrin
Chalcidoidea
Nasonia
url http://link.springer.com/article/10.1186/s13059-018-1526-x
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