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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Main Authors: Shengqian Xia, Nicholas W VanKuren, Chunyan Chen, Li Zhang, Clause Kemkemer, Yi Shao, Hangxing Jia, UnJin Lee, Alexander S Advani, Andrea Gschwend, Maria D Vibranovski, Sidi Chen, Yong E Zhang, Manyuan Long
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-07-01
Series:PLoS Genetics
Online Access:https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009654&type=printable
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author Shengqian Xia
Nicholas W VanKuren
Chunyan Chen
Li Zhang
Clause Kemkemer
Yi Shao
Hangxing Jia
UnJin Lee
Alexander S Advani
Andrea Gschwend
Maria D Vibranovski
Sidi Chen
Yong E Zhang
Manyuan Long
author_facet Shengqian Xia
Nicholas W VanKuren
Chunyan Chen
Li Zhang
Clause Kemkemer
Yi Shao
Hangxing Jia
UnJin Lee
Alexander S Advani
Andrea Gschwend
Maria D Vibranovski
Sidi Chen
Yong E Zhang
Manyuan Long
author_sort Shengqian Xia
collection DOAJ
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 doaj-art-1311e241fdee4679af4e4a31677aca392025-08-20T02:01:00ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042021-07-01177e100965410.1371/journal.pgen.1009654Genomic analyses of new genes and their phenotypic effects reveal rapid evolution of essential functions in Drosophila development.Shengqian XiaNicholas W VanKurenChunyan ChenLi ZhangClause KemkemerYi ShaoHangxing JiaUnJin LeeAlexander S AdvaniAndrea GschwendMaria D VibranovskiSidi ChenYong E ZhangManyuan LongIt 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.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009654&type=printable
spellingShingle Shengqian Xia
Nicholas W VanKuren
Chunyan Chen
Li Zhang
Clause Kemkemer
Yi Shao
Hangxing Jia
UnJin Lee
Alexander S Advani
Andrea Gschwend
Maria D Vibranovski
Sidi Chen
Yong E Zhang
Manyuan Long
Genomic analyses of new genes and their phenotypic effects reveal rapid evolution of essential functions in Drosophila development.
PLoS Genetics
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
url https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009654&type=printable
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