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Genomic analyses of new genes and their phenotypic effects reveal rapid evolution of essential functions in Drosophila development

It is a conventionally held dogma that the genetic basis underlying development is conserved in a long evolutionary time scale. Ample experiments based on mutational, biochemical, functional, and complementary knockdown/knockout approaches have revealed the unexpectedly important role of recently ev...

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Autores principales: Xia, Shengqian, VanKuren, Nicholas W., Chen, Chunyan, Zhang, Li, Kemkemer, Clause, Shao, Yi, Jia, Hangxing, Lee, UnJin, Advani, Alexander S., Gschwend, Andrea, Vibranovski, Maria D., Chen, Sidi, Zhang, Yong E., Long, Manyuan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8270118/
https://www.ncbi.nlm.nih.gov/pubmed/34242211
http://dx.doi.org/10.1371/journal.pgen.1009654
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author Xia, Shengqian
VanKuren, Nicholas W.
Chen, Chunyan
Zhang, Li
Kemkemer, Clause
Shao, Yi
Jia, Hangxing
Lee, UnJin
Advani, Alexander S.
Gschwend, Andrea
Vibranovski, Maria D.
Chen, Sidi
Zhang, Yong E.
Long, Manyuan
author_facet Xia, Shengqian
VanKuren, Nicholas W.
Chen, Chunyan
Zhang, Li
Kemkemer, Clause
Shao, Yi
Jia, Hangxing
Lee, UnJin
Advani, Alexander S.
Gschwend, Andrea
Vibranovski, Maria D.
Chen, Sidi
Zhang, Yong E.
Long, Manyuan
author_sort Xia, Shengqian
collection PubMed
description It is a conventionally held dogma that the genetic basis underlying development is conserved in a long evolutionary time scale. Ample experiments based on mutational, biochemical, functional, and complementary knockdown/knockout approaches have revealed the unexpectedly important role of recently evolved new genes in the development of Drosophila. The recent progress in the genome-wide experimental testing of gene effects and improvements in the computational identification of new genes (< 40 million years ago, Mya) open the door to investigate the evolution of gene essentiality with a phylogenetically high resolution. These advancements also raised interesting issues in techniques and concepts related to phenotypic effect analyses of genes, particularly of those that recently originated. Here we reported our analyses of these issues, including reproducibility and efficiency of knockdown experiment and difference between RNAi libraries in the knockdown efficiency and testing of phenotypic effects. We further analyzed a large data from knockdowns of 11,354 genes (~75% of the Drosophila melanogaster total genes), including 702 new genes (~66% of the species total new genes that aged < 40 Mya), revealing a similarly high proportion (~32.2%) of essential genes that originated in various Sophophora subgenus lineages and distant ancestors beyond the Drosophila genus. The transcriptional compensation effect from CRISPR knockout were detected for highly similar duplicate copies. Knockout of a few young genes detected analogous essentiality in various functions in development. Taken together, our experimental and computational analyses provide valuable data for detection of phenotypic effects of genes in general and further strong evidence for the concept that new genes in Drosophila quickly evolved essential functions in viability during development.
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spelling pubmed-82701182021-07-21 Genomic analyses of new genes and their phenotypic effects reveal rapid evolution of essential functions in Drosophila development Xia, Shengqian VanKuren, Nicholas W. Chen, Chunyan Zhang, Li Kemkemer, Clause Shao, Yi Jia, Hangxing Lee, UnJin Advani, Alexander S. Gschwend, Andrea Vibranovski, Maria D. Chen, Sidi Zhang, Yong E. Long, Manyuan PLoS Genet Research Article It is a conventionally held dogma that the genetic basis underlying development is conserved in a long evolutionary time scale. Ample experiments based on mutational, biochemical, functional, and complementary knockdown/knockout approaches have revealed the unexpectedly important role of recently evolved new genes in the development of Drosophila. The recent progress in the genome-wide experimental testing of gene effects and improvements in the computational identification of new genes (< 40 million years ago, Mya) open the door to investigate the evolution of gene essentiality with a phylogenetically high resolution. These advancements also raised interesting issues in techniques and concepts related to phenotypic effect analyses of genes, particularly of those that recently originated. Here we reported our analyses of these issues, including reproducibility and efficiency of knockdown experiment and difference between RNAi libraries in the knockdown efficiency and testing of phenotypic effects. We further analyzed a large data from knockdowns of 11,354 genes (~75% of the Drosophila melanogaster total genes), including 702 new genes (~66% of the species total new genes that aged < 40 Mya), revealing a similarly high proportion (~32.2%) of essential genes that originated in various Sophophora subgenus lineages and distant ancestors beyond the Drosophila genus. The transcriptional compensation effect from CRISPR knockout were detected for highly similar duplicate copies. Knockout of a few young genes detected analogous essentiality in various functions in development. Taken together, our experimental and computational analyses provide valuable data for detection of phenotypic effects of genes in general and further strong evidence for the concept that new genes in Drosophila quickly evolved essential functions in viability during development. Public Library of Science 2021-07-09 /pmc/articles/PMC8270118/ /pubmed/34242211 http://dx.doi.org/10.1371/journal.pgen.1009654 Text en © 2021 Xia et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Xia, Shengqian
VanKuren, Nicholas W.
Chen, Chunyan
Zhang, Li
Kemkemer, Clause
Shao, Yi
Jia, Hangxing
Lee, UnJin
Advani, Alexander S.
Gschwend, Andrea
Vibranovski, Maria D.
Chen, Sidi
Zhang, Yong E.
Long, Manyuan
Genomic analyses of new genes and their phenotypic effects reveal rapid evolution of essential functions in Drosophila development
title Genomic analyses of new genes and their phenotypic effects reveal rapid evolution of essential functions in Drosophila development
title_full Genomic analyses of new genes and their phenotypic effects reveal rapid evolution of essential functions in Drosophila development
title_fullStr Genomic analyses of new genes and their phenotypic effects reveal rapid evolution of essential functions in Drosophila development
title_full_unstemmed Genomic analyses of new genes and their phenotypic effects reveal rapid evolution of essential functions in Drosophila development
title_short Genomic analyses of new genes and their phenotypic effects reveal rapid evolution of essential functions in Drosophila development
title_sort genomic analyses of new genes and their phenotypic effects reveal rapid evolution of essential functions in drosophila development
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8270118/
https://www.ncbi.nlm.nih.gov/pubmed/34242211
http://dx.doi.org/10.1371/journal.pgen.1009654
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