Cara L Brand, Genevieve T Oliver, Isabella Z Farkas, Michael Buszczak, Mia T Levine
{"title":"果蝇中一个重要 DNA 修复基因家族的重复和多样化。","authors":"Cara L Brand, Genevieve T Oliver, Isabella Z Farkas, Michael Buszczak, Mia T Levine","doi":"10.1093/molbev/msae113","DOIUrl":null,"url":null,"abstract":"<p><p>Maintaining genome integrity is vital for organismal survival and reproduction. Essential, broadly conserved DNA repair pathways actively preserve genome integrity. However, many DNA repair proteins evolve adaptively. Ecological forces like UV exposure are classically cited drivers of DNA repair evolution. Intrinsic forces like repetitive DNA, which also imperil genome integrity, have received less attention. We recently reported that a Drosophila melanogaster-specific DNA satellite array triggered species-specific, adaptive evolution of a DNA repair protein called Spartan/MH. The Spartan family of proteases cleave hazardous, covalent crosslinks that form between DNA and proteins (\"DNA-protein crosslink repair\"). Appreciating that DNA satellites are both ubiquitous and universally fast-evolving, we hypothesized that satellite DNA turnover spurs adaptive evolution of DNA-protein crosslink repair beyond a single gene and beyond the D. melanogaster lineage. This hypothesis predicts pervasive Spartan gene family diversification across Drosophila species. To study the evolutionary history of the Drosophila Spartan gene family, we conducted population genetic, molecular evolution, phylogenomic, and tissue-specific expression analyses. We uncovered widespread signals of positive selection across multiple Spartan family genes and across multiple evolutionary timescales. We also detected recurrent Spartan family gene duplication, divergence, and gene loss. Finally, we found that ovary-enriched parent genes consistently birthed functionally diverged, testis-enriched daughter genes. To account for Spartan family diversification, we introduce a novel mechanistic model of antagonistic coevolution that links DNA satellite evolution and adaptive regulation of Spartan protease activity. This framework promises to accelerate our understanding of how DNA repeats drive recurrent evolutionary innovation to preserve genome integrity.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":null,"pages":null},"PeriodicalIF":11.0000,"publicationDate":"2024-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11210505/pdf/","citationCount":"0","resultStr":"{\"title\":\"Recurrent Duplication and Diversification of a Vital DNA Repair Gene Family Across Drosophila.\",\"authors\":\"Cara L Brand, Genevieve T Oliver, Isabella Z Farkas, Michael Buszczak, Mia T Levine\",\"doi\":\"10.1093/molbev/msae113\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Maintaining genome integrity is vital for organismal survival and reproduction. Essential, broadly conserved DNA repair pathways actively preserve genome integrity. However, many DNA repair proteins evolve adaptively. Ecological forces like UV exposure are classically cited drivers of DNA repair evolution. Intrinsic forces like repetitive DNA, which also imperil genome integrity, have received less attention. We recently reported that a Drosophila melanogaster-specific DNA satellite array triggered species-specific, adaptive evolution of a DNA repair protein called Spartan/MH. The Spartan family of proteases cleave hazardous, covalent crosslinks that form between DNA and proteins (\\\"DNA-protein crosslink repair\\\"). Appreciating that DNA satellites are both ubiquitous and universally fast-evolving, we hypothesized that satellite DNA turnover spurs adaptive evolution of DNA-protein crosslink repair beyond a single gene and beyond the D. melanogaster lineage. This hypothesis predicts pervasive Spartan gene family diversification across Drosophila species. To study the evolutionary history of the Drosophila Spartan gene family, we conducted population genetic, molecular evolution, phylogenomic, and tissue-specific expression analyses. We uncovered widespread signals of positive selection across multiple Spartan family genes and across multiple evolutionary timescales. We also detected recurrent Spartan family gene duplication, divergence, and gene loss. Finally, we found that ovary-enriched parent genes consistently birthed functionally diverged, testis-enriched daughter genes. To account for Spartan family diversification, we introduce a novel mechanistic model of antagonistic coevolution that links DNA satellite evolution and adaptive regulation of Spartan protease activity. This framework promises to accelerate our understanding of how DNA repeats drive recurrent evolutionary innovation to preserve genome integrity.</p>\",\"PeriodicalId\":18730,\"journal\":{\"name\":\"Molecular biology and evolution\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":11.0000,\"publicationDate\":\"2024-06-01\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11210505/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Molecular biology and evolution\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1093/molbev/msae113\",\"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}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Molecular biology and evolution","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1093/molbev/msae113","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
摘要
保持基因组的完整性对生物的生存和繁殖至关重要。基本的、广泛保守的 DNA 修复途径可积极维护基因组的完整性。然而,许多 DNA 修复蛋白是适应性进化的。紫外线照射等生态力量是DNA修复进化的经典驱动力。像重复 DNA 这样的内在力量也会危及基因组的完整性,但却较少受到关注。我们最近报告说,黑腹果蝇特异的DNA卫星阵列引发了一种名为Spartan/MH的DNA修复蛋白的物种特异性适应性进化。Spartan蛋白酶家族能裂解DNA与蛋白质之间形成的危险的共价交联("DNA-蛋白质交联修复")。由于 DNA 卫星无处不在,而且进化速度极快,我们假设卫星 DNA 的更替会促进 DNA 蛋白交联修复的适应性进化,使其超越单个基因,超越黑腹蝇系。这一假设预测了果蝇物种间普遍的斯巴达基因家族多样化。为了研究果蝇斯巴达基因家族的进化历史,我们进行了群体遗传学、分子进化、系统发生学和组织特异性表达分析。我们在多个斯巴达家族基因和多个进化时间尺度上发现了广泛的正选择信号。我们还发现了斯巴达家族基因的重复、分化和基因丢失。最后,我们发现,富含卵巢的父基因始终孕育着功能上分化的、富含睾丸的子基因。为了解释斯巴达家族的多样化,我们引入了一个新的拮抗共同进化机制模型,该模型将DNA卫星进化与斯巴达蛋白酶活性的适应性调控联系起来。这一框架有望加速我们对DNA重复序列如何推动反复进化创新以保持基因组完整性的理解。
Recurrent Duplication and Diversification of a Vital DNA Repair Gene Family Across Drosophila.
Maintaining genome integrity is vital for organismal survival and reproduction. Essential, broadly conserved DNA repair pathways actively preserve genome integrity. However, many DNA repair proteins evolve adaptively. Ecological forces like UV exposure are classically cited drivers of DNA repair evolution. Intrinsic forces like repetitive DNA, which also imperil genome integrity, have received less attention. We recently reported that a Drosophila melanogaster-specific DNA satellite array triggered species-specific, adaptive evolution of a DNA repair protein called Spartan/MH. The Spartan family of proteases cleave hazardous, covalent crosslinks that form between DNA and proteins ("DNA-protein crosslink repair"). Appreciating that DNA satellites are both ubiquitous and universally fast-evolving, we hypothesized that satellite DNA turnover spurs adaptive evolution of DNA-protein crosslink repair beyond a single gene and beyond the D. melanogaster lineage. This hypothesis predicts pervasive Spartan gene family diversification across Drosophila species. To study the evolutionary history of the Drosophila Spartan gene family, we conducted population genetic, molecular evolution, phylogenomic, and tissue-specific expression analyses. We uncovered widespread signals of positive selection across multiple Spartan family genes and across multiple evolutionary timescales. We also detected recurrent Spartan family gene duplication, divergence, and gene loss. Finally, we found that ovary-enriched parent genes consistently birthed functionally diverged, testis-enriched daughter genes. To account for Spartan family diversification, we introduce a novel mechanistic model of antagonistic coevolution that links DNA satellite evolution and adaptive regulation of Spartan protease activity. This framework promises to accelerate our understanding of how DNA repeats drive recurrent evolutionary innovation to preserve genome integrity.
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.