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A New Hope: A Hermaphroditic Nematode Enables Analysis of a Recent Whole Genome Duplication Event

Whole genome duplication (WGD) is often considered a major driver of evolution that leads to phenotypic novelties. However, the importance of WGD for evolution is still controversial because most documented WGD events occurred anciently and few experimental systems amenable to genetic analysis are a...

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Autores principales: Wighard, Sara S, Athanasouli, Marina, Witte, Hanh, Rödelsperger, Christian, Sommer, Ralf J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9763058/
https://www.ncbi.nlm.nih.gov/pubmed/36461901
http://dx.doi.org/10.1093/gbe/evac169
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author Wighard, Sara S
Athanasouli, Marina
Witte, Hanh
Rödelsperger, Christian
Sommer, Ralf J
author_facet Wighard, Sara S
Athanasouli, Marina
Witte, Hanh
Rödelsperger, Christian
Sommer, Ralf J
author_sort Wighard, Sara S
collection PubMed
description Whole genome duplication (WGD) is often considered a major driver of evolution that leads to phenotypic novelties. However, the importance of WGD for evolution is still controversial because most documented WGD events occurred anciently and few experimental systems amenable to genetic analysis are available. Here, we report a recent WGD event in the hermaphroditic nematode Allodiplogaster sudhausi and present a comparison with a gonochoristic (male/female) sister species that did not undergo WGD. Self-fertilizing reproduction of A. sudhausi makes it amenable to functional analysis and an ideal system to study WGD events. We document WGD in A. sudhausi through karyotype analysis and whole genome sequencing, the latter of which allowed us to 1) identify functional bias in retention of protein domains and metabolic pathways, 2) show most duplicate genes are under evolutionary constraint, 3) show a link between sequence and expression divergence, and 4) characterize differentially expressed duplicates. We additionally show WGD is associated with increased body size and an abundance of repeat elements (36% of the genome), including a recent expansion of the DNA-hAT/Ac transposon family. Finally, we demonstrate the use of CRISPR/Cas9 to generate mutant knockouts, whereby two WGD-derived duplicate genes display functional redundancy in that they both need to be knocked out to generate a phenotype. Together, we present a novel experimental system that is convenient for examining and characterizing WGD-derived genes both computationally and functionally.
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spelling pubmed-97630582022-12-20 A New Hope: A Hermaphroditic Nematode Enables Analysis of a Recent Whole Genome Duplication Event Wighard, Sara S Athanasouli, Marina Witte, Hanh Rödelsperger, Christian Sommer, Ralf J Genome Biol Evol Research Article Whole genome duplication (WGD) is often considered a major driver of evolution that leads to phenotypic novelties. However, the importance of WGD for evolution is still controversial because most documented WGD events occurred anciently and few experimental systems amenable to genetic analysis are available. Here, we report a recent WGD event in the hermaphroditic nematode Allodiplogaster sudhausi and present a comparison with a gonochoristic (male/female) sister species that did not undergo WGD. Self-fertilizing reproduction of A. sudhausi makes it amenable to functional analysis and an ideal system to study WGD events. We document WGD in A. sudhausi through karyotype analysis and whole genome sequencing, the latter of which allowed us to 1) identify functional bias in retention of protein domains and metabolic pathways, 2) show most duplicate genes are under evolutionary constraint, 3) show a link between sequence and expression divergence, and 4) characterize differentially expressed duplicates. We additionally show WGD is associated with increased body size and an abundance of repeat elements (36% of the genome), including a recent expansion of the DNA-hAT/Ac transposon family. Finally, we demonstrate the use of CRISPR/Cas9 to generate mutant knockouts, whereby two WGD-derived duplicate genes display functional redundancy in that they both need to be knocked out to generate a phenotype. Together, we present a novel experimental system that is convenient for examining and characterizing WGD-derived genes both computationally and functionally. Oxford University Press 2022-12-03 /pmc/articles/PMC9763058/ /pubmed/36461901 http://dx.doi.org/10.1093/gbe/evac169 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Research Article
Wighard, Sara S
Athanasouli, Marina
Witte, Hanh
Rödelsperger, Christian
Sommer, Ralf J
A New Hope: A Hermaphroditic Nematode Enables Analysis of a Recent Whole Genome Duplication Event
title A New Hope: A Hermaphroditic Nematode Enables Analysis of a Recent Whole Genome Duplication Event
title_full A New Hope: A Hermaphroditic Nematode Enables Analysis of a Recent Whole Genome Duplication Event
title_fullStr A New Hope: A Hermaphroditic Nematode Enables Analysis of a Recent Whole Genome Duplication Event
title_full_unstemmed A New Hope: A Hermaphroditic Nematode Enables Analysis of a Recent Whole Genome Duplication Event
title_short A New Hope: A Hermaphroditic Nematode Enables Analysis of a Recent Whole Genome Duplication Event
title_sort new hope: a hermaphroditic nematode enables analysis of a recent whole genome duplication event
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9763058/
https://www.ncbi.nlm.nih.gov/pubmed/36461901
http://dx.doi.org/10.1093/gbe/evac169
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