Most Pleiotropic Effects of Gene Knockouts Are Evolutionarily Transient in Yeasts.

IF 11 1区 生物学 Q1 BIOCHEMISTRY & MOLECULAR BIOLOGY Molecular biology and evolution Pub Date : 2024-09-04 DOI:10.1093/molbev/msae189
Li Liu, Yao Liu, Lulu Min, Zhenzhen Zhou, Xingxing He, YunHan Xie, Waifang Cao, Shuyun Deng, Xiaoju Lin, Xionglei He, Xiaoshu Chen
{"title":"Most Pleiotropic Effects of Gene Knockouts Are Evolutionarily Transient in Yeasts.","authors":"Li Liu, Yao Liu, Lulu Min, Zhenzhen Zhou, Xingxing He, YunHan Xie, Waifang Cao, Shuyun Deng, Xiaoju Lin, Xionglei He, Xiaoshu Chen","doi":"10.1093/molbev/msae189","DOIUrl":null,"url":null,"abstract":"<p><p>Pleiotropy, the phenomenon in which a single gene influences multiple traits, is a fundamental concept in genetics. However, the evolutionary mechanisms underlying pleiotropy require further investigation. In this study, we conducted parallel gene knockouts targeting 100 transcription factors in 2 strains of Saccharomyces cerevisiae. We systematically examined and quantified the pleiotropic effects of these knockouts on gene expression levels for each transcription factor. Our results showed that the knockout of a single gene generally affected the expression levels of multiple genes in both strains, indicating various degrees of pleiotropic effects. Strikingly, the pleiotropic effects of the knockouts change rapidly between strains in different genetic backgrounds, and ∼85% of them were nonconserved. Further analysis revealed that the conserved effects tended to be functionally associated with the deleted transcription factors, while the nonconserved effects appeared to be more ad hoc responses. In addition, we measured 184 yeast cell morphological traits in these knockouts and found consistent patterns. In order to investigate the evolutionary processes underlying pleiotropy, we examined the pleiotropic effects of standing genetic variations in a population consisting of ∼1,000 hybrid progenies of the 2 strains. We observed that newly evolved expression quantitative trait loci impacted the expression of a greater number of genes than did old expression quantitative trait loci, suggesting that natural selection is gradually eliminating maladaptive or slightly deleterious pleiotropic responses. Overall, our results show that, although being prevalent for new mutations, the majority of pleiotropic effects observed are evolutionarily transient, which explains how evolution proceeds despite complicated pleiotropic effects.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":null,"pages":null},"PeriodicalIF":11.0000,"publicationDate":"2024-09-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11414406/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Molecular biology and evolution","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1093/molbev/msae189","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Pleiotropy, the phenomenon in which a single gene influences multiple traits, is a fundamental concept in genetics. However, the evolutionary mechanisms underlying pleiotropy require further investigation. In this study, we conducted parallel gene knockouts targeting 100 transcription factors in 2 strains of Saccharomyces cerevisiae. We systematically examined and quantified the pleiotropic effects of these knockouts on gene expression levels for each transcription factor. Our results showed that the knockout of a single gene generally affected the expression levels of multiple genes in both strains, indicating various degrees of pleiotropic effects. Strikingly, the pleiotropic effects of the knockouts change rapidly between strains in different genetic backgrounds, and ∼85% of them were nonconserved. Further analysis revealed that the conserved effects tended to be functionally associated with the deleted transcription factors, while the nonconserved effects appeared to be more ad hoc responses. In addition, we measured 184 yeast cell morphological traits in these knockouts and found consistent patterns. In order to investigate the evolutionary processes underlying pleiotropy, we examined the pleiotropic effects of standing genetic variations in a population consisting of ∼1,000 hybrid progenies of the 2 strains. We observed that newly evolved expression quantitative trait loci impacted the expression of a greater number of genes than did old expression quantitative trait loci, suggesting that natural selection is gradually eliminating maladaptive or slightly deleterious pleiotropic responses. Overall, our results show that, although being prevalent for new mutations, the majority of pleiotropic effects observed are evolutionarily transient, which explains how evolution proceeds despite complicated pleiotropic effects.

查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
在酵母菌中,基因敲除的大多数多效作用在进化过程中都是短暂的。
多效性(Pleiotropy)是一个基因影响多个性状的现象,是遗传学中的一个基本概念。然而,多效性背后的进化机制还需要进一步研究。在这项研究中,我们在两株酿酒酵母中针对 100 个转录因子进行了平行基因敲除。我们系统地检测并量化了这些基因敲除对每个转录因子基因表达水平的多效性影响。结果表明,在两个菌株中,单个基因的敲除通常会影响多个基因的表达水平,这表明存在不同程度的多效应。引人注目的是,基因敲除的多效应在不同遗传背景的菌株之间变化迅速,其中85%是非保守效应。进一步分析发现,保守效应往往与被删除的转录因子在功能上相关,而非保守效应似乎更多是临时反应。此外,我们还测量了这些基因敲除的 184 种酵母细胞形态特征,并发现了一致的模式。为了研究多效性背后的进化过程,我们在由这两个菌株的 1000 个杂交后代组成的群体中考察了常存遗传变异的多效性效应。我们观察到,新进化的表达量性状位点(eQTL)比旧的eQTL对更多基因的表达产生了影响,这表明自然选择正在逐渐消除不适应的或轻微有害的多生物效应。总之,我们的研究结果表明,虽然新的突变很普遍,但观察到的大多数多向效应在进化过程中都是短暂的,这也解释了为什么尽管多向效应很复杂,进化仍在继续。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 去求助
来源期刊
Molecular biology and evolution
Molecular biology and evolution 生物-进化生物学
CiteScore
19.70
自引率
3.70%
发文量
257
审稿时长
1 months
期刊介绍: Molecular Biology and Evolution Journal Overview: Publishes research at the interface of molecular (including genomics) and evolutionary biology Considers manuscripts containing patterns, processes, and predictions at all levels of organization: population, taxonomic, functional, and phenotypic Interested in fundamental discoveries, new and improved methods, resources, technologies, and theories advancing evolutionary research Publishes balanced reviews of recent developments in genome evolution and forward-looking perspectives suggesting future directions in molecular evolution applications.
期刊最新文献
Conjugation mediates large-scale chromosomal transfer in Streptomyces driving diversification of antibiotic biosynthetic gene clusters. Multiple-wave admixture and adaptive evolution of the Pamirian Wakhi people. Integrating contact tracing data to enhance outbreak phylodynamic inference: a deep learning approach. Rewiring of uric acid metabolism in the intestine promotes high-altitude hypoxia adaptation in humans. Specialization restricts the evolutionary paths available to yeast sugar transporters.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术
文献互助 智能选刊 最新文献 互助须知 联系我们:info@booksci.cn
Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。
Copyright © 2023 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1