Jonathan H Bethke, Jeffrey Kimbrel, Yongqin Jiao, Dante Ricci
Bacterial evolution through horizontal gene transfer (HGT) reflects their community interactions. In this way, HGT networks do well at mapping community interactions, but offer little toward controlling them-an important step in the translation of synthetic strains into natural contexts. Toxin-antitoxin (TA) systems serve as ubiquitous and diverse agents of selection; however, their utility is limited by their erratic distribution in hosts. Here we examine the heterogeneous distribution of TAs as a consequence of their mobility. By systematically mapping TA systems across a 10,000 plasmid network, we find HGT communities have unique and predictable TA signatures. We propose these TA signatures arise from plasmid competition and have further potential to signal the degree to which plasmids, hosts, and phage interact. To emphasize these relationships, we construct an HGT network based solely on TA similarity, framing specific selection markers in the broader context of bacterial communities. This work both clarifies the evolution of TA systems and unlocks a common framework for manipulating community interactions through TA compatibility.
细菌通过水平基因转移(HGT)实现的进化反映了其群落间的相互作用。因此,HGT 网络能很好地绘制群落相互作用的图谱,但在控制群落相互作用方面却无能为力--而这正是将合成菌株转化为自然菌株的重要一步。毒素-抗毒素(TA)系统是无处不在、多种多样的选择媒介;然而,由于它们在宿主体内的分布不稳定,它们的作用受到了限制。在这里,我们研究了TA的异质性分布是其流动性的结果。通过系统地绘制 10,000 个质粒网络中的 TA 系统图,我们发现 HGT 群体具有独特且可预测的 TA 特征。我们认为这些TA特征源于质粒竞争,并有可能进一步表明质粒、宿主和噬菌体之间的相互作用程度。为了强调这些关系,我们仅根据 TA 相似性构建了一个 HGT 网络,在细菌群落的大背景下构建了特定的选择标记。这项工作既阐明了TA系统的进化,又为通过TA兼容性操纵群落相互作用打开了一个共同的框架。
{"title":"Toxin-Antitoxin Systems Reflect Community Interactions Through Horizontal Gene Transfer.","authors":"Jonathan H Bethke, Jeffrey Kimbrel, Yongqin Jiao, Dante Ricci","doi":"10.1093/molbev/msae206","DOIUrl":"10.1093/molbev/msae206","url":null,"abstract":"<p><p>Bacterial evolution through horizontal gene transfer (HGT) reflects their community interactions. In this way, HGT networks do well at mapping community interactions, but offer little toward controlling them-an important step in the translation of synthetic strains into natural contexts. Toxin-antitoxin (TA) systems serve as ubiquitous and diverse agents of selection; however, their utility is limited by their erratic distribution in hosts. Here we examine the heterogeneous distribution of TAs as a consequence of their mobility. By systematically mapping TA systems across a 10,000 plasmid network, we find HGT communities have unique and predictable TA signatures. We propose these TA signatures arise from plasmid competition and have further potential to signal the degree to which plasmids, hosts, and phage interact. To emphasize these relationships, we construct an HGT network based solely on TA similarity, framing specific selection markers in the broader context of bacterial communities. This work both clarifies the evolution of TA systems and unlocks a common framework for manipulating community interactions through TA compatibility.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":" ","pages":""},"PeriodicalIF":11.0,"publicationDate":"2024-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11523183/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142470142","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Zihao Zhu, Jana Trenner, Carolin Delker, Marcel Quint
Plants have evolved mechanisms to anticipate and adjust their growth and development in response to environmental changes. Understanding the key regulators of plant performance is crucial to mitigate the negative influence of global climate change on crop production. EARLY FLOWERING 3 (ELF3) is one such regulator playing a critical role in the circadian clock and thermomorphogenesis. In Arabidopsis thaliana, ELF3 contains a prion-like domain (PrLD) that acts as a thermosensor, facilitating liquid-liquid phase separation at high ambient temperatures. To assess the conservation of this function across the plant kingdom, we traced the evolutionary emergence of ELF3, with a focus on the presence of PrLDs. We found that the PrLD, primarily influenced by the length of polyglutamine (polyQ) repeats, is most prominent in Brassicales. Analyzing 319 natural A. thaliana accessions, we confirmed the previously described wide range of polyQ length variation in AtELF3, but found it to be only weakly associated with geographic origin, climate conditions, and classic temperature-responsive phenotypes. Interestingly, similar polyQ length variation was not observed in several other investigated Bassicaceae species. Based on these findings, available prediction tools and limited experimental evidence, we conclude that the emergence of PrLD, and particularly polyQ length variation, is unlikely to be a key driver of environmental adaptation. Instead, it likely adds an additional layer to ELF3's role in thermomorphogenesis in A. thaliana, with its relevance in other species yet to be confirmed.
{"title":"Tracing the Evolutionary History of the Temperature-Sensing Prion-like Domain in EARLY FLOWERING 3 Highlights the Uniqueness of AtELF3.","authors":"Zihao Zhu, Jana Trenner, Carolin Delker, Marcel Quint","doi":"10.1093/molbev/msae205","DOIUrl":"10.1093/molbev/msae205","url":null,"abstract":"<p><p>Plants have evolved mechanisms to anticipate and adjust their growth and development in response to environmental changes. Understanding the key regulators of plant performance is crucial to mitigate the negative influence of global climate change on crop production. EARLY FLOWERING 3 (ELF3) is one such regulator playing a critical role in the circadian clock and thermomorphogenesis. In Arabidopsis thaliana, ELF3 contains a prion-like domain (PrLD) that acts as a thermosensor, facilitating liquid-liquid phase separation at high ambient temperatures. To assess the conservation of this function across the plant kingdom, we traced the evolutionary emergence of ELF3, with a focus on the presence of PrLDs. We found that the PrLD, primarily influenced by the length of polyglutamine (polyQ) repeats, is most prominent in Brassicales. Analyzing 319 natural A. thaliana accessions, we confirmed the previously described wide range of polyQ length variation in AtELF3, but found it to be only weakly associated with geographic origin, climate conditions, and classic temperature-responsive phenotypes. Interestingly, similar polyQ length variation was not observed in several other investigated Bassicaceae species. Based on these findings, available prediction tools and limited experimental evidence, we conclude that the emergence of PrLD, and particularly polyQ length variation, is unlikely to be a key driver of environmental adaptation. Instead, it likely adds an additional layer to ELF3's role in thermomorphogenesis in A. thaliana, with its relevance in other species yet to be confirmed.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":" ","pages":""},"PeriodicalIF":11.0,"publicationDate":"2024-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11523139/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142400759","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Marieke S van de Loosdrecht, Nicholaas M Pinas, Evanne Dongstra, Jerry R Tjoe Awie, Frank F M Becker, Harro Maat, Robin van Velzen, Tinde van Andel, Michael Eric Schranz
Maroons in Suriname and French Guiana descend from enslaved Africans who escaped the plantations during colonial times. Maroon farmers still cultivate a large diversity of rice, their oldest staple crop. The oral history and written records of Maroons by colonial authorities provide contrasting perspectives on the origins of Maroon rice. Here, we analyzed the genomic ancestry of 136 newly sequenced Maroon rice varieties and found seven genomic groups that differ in their geographical associations. We interpreted these findings in light of ethnobotanical and archival investigations to reconstruct the historical contexts associated with the introduction of rice varieties to the Guianas. We found that two rice groups trace to West Africa, which we propose are linked to the transatlantic slave trade (c. 1526 to 1825). We posit that the Maroon rice stock additionally contains varieties that derive from rice introduced by indentured laborers from Java (1890 onwards), USA rice breeders (1932 onwards), and Hmong refugees who fled the Vietnam War (1991). Furthermore, on the Maroon fields, we found rice types never documented before that were derived from crosses. Overall, our results demonstrate that the Maroon farmers prioritize maintenance of a high stock diversity, which we posit reflects the expertise they inherited from their (African) ancestors. Ignored by agricultural modernization initiatives, Maroon farmers today are custodians of a unique cultural heritage. Notably, the genomic findings underline many Maroon stories about their past. We anticipate that a similar study approach can be applied to other heirloom crops of (Indigenous) communities that may have preserved their history on their farms to reconstruct, acknowledge, and honor the past.
{"title":"Maroon Rice Genomic Diversity Reflects 350 Years of Colonial History.","authors":"Marieke S van de Loosdrecht, Nicholaas M Pinas, Evanne Dongstra, Jerry R Tjoe Awie, Frank F M Becker, Harro Maat, Robin van Velzen, Tinde van Andel, Michael Eric Schranz","doi":"10.1093/molbev/msae204","DOIUrl":"10.1093/molbev/msae204","url":null,"abstract":"<p><p>Maroons in Suriname and French Guiana descend from enslaved Africans who escaped the plantations during colonial times. Maroon farmers still cultivate a large diversity of rice, their oldest staple crop. The oral history and written records of Maroons by colonial authorities provide contrasting perspectives on the origins of Maroon rice. Here, we analyzed the genomic ancestry of 136 newly sequenced Maroon rice varieties and found seven genomic groups that differ in their geographical associations. We interpreted these findings in light of ethnobotanical and archival investigations to reconstruct the historical contexts associated with the introduction of rice varieties to the Guianas. We found that two rice groups trace to West Africa, which we propose are linked to the transatlantic slave trade (c. 1526 to 1825). We posit that the Maroon rice stock additionally contains varieties that derive from rice introduced by indentured laborers from Java (1890 onwards), USA rice breeders (1932 onwards), and Hmong refugees who fled the Vietnam War (1991). Furthermore, on the Maroon fields, we found rice types never documented before that were derived from crosses. Overall, our results demonstrate that the Maroon farmers prioritize maintenance of a high stock diversity, which we posit reflects the expertise they inherited from their (African) ancestors. Ignored by agricultural modernization initiatives, Maroon farmers today are custodians of a unique cultural heritage. Notably, the genomic findings underline many Maroon stories about their past. We anticipate that a similar study approach can be applied to other heirloom crops of (Indigenous) communities that may have preserved their history on their farms to reconstruct, acknowledge, and honor the past.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":"41 10","pages":""},"PeriodicalIF":11.0,"publicationDate":"2024-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11495330/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142504321","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Polyploids arise from whole-genome duplication (WGD) events, which have played important roles in genome evolution across eukaryotes. WGD can increase genome complexity, yield phenotypic novelty, and influence adaptation. Neo-polyploids have been reported to often show seemingly stochastic epigenetic and transcriptional changes, but this leaves open the question whether these changes persist in evolved polyploids. A powerful approach to address this is to compare diploids, neo-polyploids, and evolved polyploids of the same species. Arabidopsis arenosa is a species that allows us to do this-natural diploid and autotetraploid populations exist, while neo-tetraploids can be artificially generated. Here, we use ATAC-seq to assay local chromatin accessibility, and RNA-seq to study gene expression on matched leaf and petal samples from diploid, neo-tetraploid and evolved tetraploid A. arenosa. We found over 8,000 differentially accessible chromatin regions across all samples. These are largely tissue specific and show distinct trends across cytotypes, with roughly 70% arising upon WGD. Interestingly, only a small proportion is associated with expression changes in nearby genes. However, accessibility variation across cytotypes associates strongly with the number of nearby transposable elements. Relatively few genes were differentially expressed upon genome duplication, and ∼60% of these reverted to near-diploid levels in the evolved tetraploid, suggesting that most initial perturbations do not last. Our results provide new insights into how epigenomic and transcriptional mechanisms jointly respond to genome duplication and subsequent evolution of autopolyploids, and importantly, show that one cannot be directly predicted from the other.
{"title":"Chromatin Accessibility and Gene Expression Vary Between a New and Evolved Autopolyploid of Arabidopsis arenosa.","authors":"Thanvi Srikant, Adrián Gonzalo, Kirsten Bomblies","doi":"10.1093/molbev/msae213","DOIUrl":"10.1093/molbev/msae213","url":null,"abstract":"<p><p>Polyploids arise from whole-genome duplication (WGD) events, which have played important roles in genome evolution across eukaryotes. WGD can increase genome complexity, yield phenotypic novelty, and influence adaptation. Neo-polyploids have been reported to often show seemingly stochastic epigenetic and transcriptional changes, but this leaves open the question whether these changes persist in evolved polyploids. A powerful approach to address this is to compare diploids, neo-polyploids, and evolved polyploids of the same species. Arabidopsis arenosa is a species that allows us to do this-natural diploid and autotetraploid populations exist, while neo-tetraploids can be artificially generated. Here, we use ATAC-seq to assay local chromatin accessibility, and RNA-seq to study gene expression on matched leaf and petal samples from diploid, neo-tetraploid and evolved tetraploid A. arenosa. We found over 8,000 differentially accessible chromatin regions across all samples. These are largely tissue specific and show distinct trends across cytotypes, with roughly 70% arising upon WGD. Interestingly, only a small proportion is associated with expression changes in nearby genes. However, accessibility variation across cytotypes associates strongly with the number of nearby transposable elements. Relatively few genes were differentially expressed upon genome duplication, and ∼60% of these reverted to near-diploid levels in the evolved tetraploid, suggesting that most initial perturbations do not last. Our results provide new insights into how epigenomic and transcriptional mechanisms jointly respond to genome duplication and subsequent evolution of autopolyploids, and importantly, show that one cannot be directly predicted from the other.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":" ","pages":""},"PeriodicalIF":11.0,"publicationDate":"2024-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11518924/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142470119","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Julius Wiegert, Dimitri Höhler, Julia Haag, Alexandros Stamatakis
Estimating the statistical robustness of the inferred tree(s) constitutes an integral part of most phylogenetic analyses. Commonly, one computes and assigns a branch support value to each inner branch of the inferred phylogeny. The still most widely used method for calculating branch support on trees inferred under maximum likelihood (ML) is the Standard, nonparametric Felsenstein bootstrap support (SBS). Due to the high computational cost of the SBS, a plethora of methods has been developed to approximate it, for instance, via the rapid bootstrap (RB) algorithm. There have also been attempts to devise faster, alternative support measures, such as the SH-aLRT (Shimodaira-Hasegawa-like approximate likelihood ratio test) or the UltraFast bootstrap 2 (UFBoot2) method. Those faster alternatives exhibit some limitations, such as the need to assess model violations (UFBoot2) or unstable behavior in the low support interval range (SH-aLRT). Here, we present the educated bootstrap guesser (EBG), a machine learning-based tool that predicts SBS branch support values for a given input phylogeny. EBG is on average 9.4 (σ=5.5) times faster than UFBoot2. EBG-based SBS estimates exhibit a median absolute error of 5 when predicting SBS values between 0 and 100. Furthermore, EBG also provides uncertainty measures for all per-branch SBS predictions and thereby allows for a more rigorous and careful interpretation. EBG can, for instance, predict SBS support values on a phylogeny comprising 1,654 SARS-CoV2 genome sequences within 3 h on a mid-class laptop. EBG is available under GNU GPL3.
估计推断树的统计稳健性是大多数系统发生学分析不可或缺的一部分。通常,我们会计算并给推断出的系统发生的每个内部分支分配一个分支支持度值。在最大似然法(ML)下计算推断树的分支支持度时,目前最广泛使用的方法是标准非参数费尔森斯坦引导支持法(SBS)。由于 SBS 的计算成本较高,人们开发了大量方法来近似 SBS,例如通过快速引导(RB)算法。此外,还有人尝试设计更快的替代支持度量,如 SH-aLRT(下平-长谷川类近似似然比检验)或超快速引导 2(UFBoot2)方法。这些更快的替代方法有一些局限性,比如需要评估模型违反情况(UFBoot2)或在低支持区间范围内的不稳定行为(SH-aLRT)。在此,我们介绍了教育引导猜测器(EBG),这是一种基于机器学习的工具,可预测给定输入系统发生的 SBS 分支支持值。EBG 比 UFBoot2 平均快 9.4 (σ = 5.5) 倍。在预测 0 到 100 之间的 SBS 值时,基于 EBG 的 SBS 估计值的中位绝对误差为 5。此外,EBG 还为所有每个分支的 SBS 预测提供了不确定性度量,因此可以进行更严格、更仔细的解释。例如,EBG 可以在一台中档笔记本电脑上,在 3 小时内预测由 1654 美元 SARS-CoV2 基因组序列组成的系统发生的 SBS 支持值。EBG 在 GNU GPL3 下提供。
{"title":"Predicting Phylogenetic Bootstrap Values via Machine Learning.","authors":"Julius Wiegert, Dimitri Höhler, Julia Haag, Alexandros Stamatakis","doi":"10.1093/molbev/msae215","DOIUrl":"10.1093/molbev/msae215","url":null,"abstract":"<p><p>Estimating the statistical robustness of the inferred tree(s) constitutes an integral part of most phylogenetic analyses. Commonly, one computes and assigns a branch support value to each inner branch of the inferred phylogeny. The still most widely used method for calculating branch support on trees inferred under maximum likelihood (ML) is the Standard, nonparametric Felsenstein bootstrap support (SBS). Due to the high computational cost of the SBS, a plethora of methods has been developed to approximate it, for instance, via the rapid bootstrap (RB) algorithm. There have also been attempts to devise faster, alternative support measures, such as the SH-aLRT (Shimodaira-Hasegawa-like approximate likelihood ratio test) or the UltraFast bootstrap 2 (UFBoot2) method. Those faster alternatives exhibit some limitations, such as the need to assess model violations (UFBoot2) or unstable behavior in the low support interval range (SH-aLRT). Here, we present the educated bootstrap guesser (EBG), a machine learning-based tool that predicts SBS branch support values for a given input phylogeny. EBG is on average 9.4 (σ=5.5) times faster than UFBoot2. EBG-based SBS estimates exhibit a median absolute error of 5 when predicting SBS values between 0 and 100. Furthermore, EBG also provides uncertainty measures for all per-branch SBS predictions and thereby allows for a more rigorous and careful interpretation. EBG can, for instance, predict SBS support values on a phylogeny comprising 1,654 SARS-CoV2 genome sequences within 3 h on a mid-class laptop. EBG is available under GNU GPL3.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":" ","pages":""},"PeriodicalIF":11.0,"publicationDate":"2024-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11523138/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142470138","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ziyue Yang, Yongtao Shan, Xue Liu, Guowei Chen, Yuanfei Pan, Qinyu Gou, Jie Zou, Zilong Chang, Qiang Zeng, Chunhui Yang, Jianbin Kong, Yanni Sun, Shaochuan Li, Xu Zhang, Wei-Chen Wu, Chunmei Li, Hong Peng, Edward C Holmes, Deyin Guo, Mang Shi
RNA viruses exhibit vast phylogenetic diversity and can significantly impact public health and agriculture. However, current bioinformatics tools for viral discovery from metagenomic data frequently generate false positive virus results, overestimate viral diversity, and misclassify virus sequences. Additionally, current tools often fail to determine virus-host associations, which hampers investigation of the potential threat posed by a newly detected virus. To address these issues we developed VirID, a software tool specifically designed for the discovery and characterization of RNA viruses from metagenomic data. The basis of VirID is a comprehensive RNA-dependent RNA polymerase database to enhance a workflow that includes RNA virus discovery, phylogenetic analysis, and phylogeny-based virus characterization. Benchmark tests on a simulated data set demonstrated that VirID had high accuracy in profiling viruses and estimating viral richness. In evaluations with real-world samples, VirID was able to identify RNA viruses of all types, but also provided accurate estimations of viral genetic diversity and virus classification, as well as comprehensive insights into virus associations with humans, animals, and plants. VirID therefore offers a robust tool for virus discovery and serves as a valuable resource in basic virological studies, pathogen surveillance, and early warning systems for infectious disease outbreaks.
{"title":"VirID: Beyond Virus Discovery-An Integrated Platform for Comprehensive RNA Virus Characterization.","authors":"Ziyue Yang, Yongtao Shan, Xue Liu, Guowei Chen, Yuanfei Pan, Qinyu Gou, Jie Zou, Zilong Chang, Qiang Zeng, Chunhui Yang, Jianbin Kong, Yanni Sun, Shaochuan Li, Xu Zhang, Wei-Chen Wu, Chunmei Li, Hong Peng, Edward C Holmes, Deyin Guo, Mang Shi","doi":"10.1093/molbev/msae202","DOIUrl":"10.1093/molbev/msae202","url":null,"abstract":"<p><p>RNA viruses exhibit vast phylogenetic diversity and can significantly impact public health and agriculture. However, current bioinformatics tools for viral discovery from metagenomic data frequently generate false positive virus results, overestimate viral diversity, and misclassify virus sequences. Additionally, current tools often fail to determine virus-host associations, which hampers investigation of the potential threat posed by a newly detected virus. To address these issues we developed VirID, a software tool specifically designed for the discovery and characterization of RNA viruses from metagenomic data. The basis of VirID is a comprehensive RNA-dependent RNA polymerase database to enhance a workflow that includes RNA virus discovery, phylogenetic analysis, and phylogeny-based virus characterization. Benchmark tests on a simulated data set demonstrated that VirID had high accuracy in profiling viruses and estimating viral richness. In evaluations with real-world samples, VirID was able to identify RNA viruses of all types, but also provided accurate estimations of viral genetic diversity and virus classification, as well as comprehensive insights into virus associations with humans, animals, and plants. VirID therefore offers a robust tool for virus discovery and serves as a valuable resource in basic virological studies, pathogen surveillance, and early warning systems for infectious disease outbreaks.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":" ","pages":""},"PeriodicalIF":11.0,"publicationDate":"2024-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11523140/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142350256","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Understanding the main determinants of protein evolution is a fundamental challenge in biology. Despite many decades of active research, the molecular and cellular mechanisms underlying the substantial variability of evolutionary rates across cellular proteins are not currently well understood. It also remains unclear how protein molecular function is optimized in the context of multicellular species and why many proteins, such as enzymes, are only moderately efficient on average. Our analysis of genomics and functional datasets reveals in multiple organisms a strong inverse relationship between the optimality of protein molecular function and the rate of protein evolution. Furthermore, we find that highly expressed proteins tend to be substantially more functionally optimized. These results suggest that cellular expression costs lead to more pronounced functional optimization of abundant proteins and that the purifying selection to maintain high levels of functional optimality significantly slows protein evolution. We observe that in multicellular species both the rate of protein evolution and the degree of protein functional efficiency are primarily affected by expression in several distinct cell types and tissues, specifically, in developed neurons with upregulated synaptic processes in animals and in young and fast-growing tissues in plants. Overall, our analysis reveals how various constraints from the molecular, cellular, and species' levels of biological organization jointly affect the rate of protein evolution and the level of protein functional adaptation.
{"title":"Functional Optimization in Distinct Tissues and Conditions Constrains the Rate of Protein Evolution.","authors":"Dinara R Usmanova, Germán Plata, Dennis Vitkup","doi":"10.1093/molbev/msae200","DOIUrl":"10.1093/molbev/msae200","url":null,"abstract":"<p><p>Understanding the main determinants of protein evolution is a fundamental challenge in biology. Despite many decades of active research, the molecular and cellular mechanisms underlying the substantial variability of evolutionary rates across cellular proteins are not currently well understood. It also remains unclear how protein molecular function is optimized in the context of multicellular species and why many proteins, such as enzymes, are only moderately efficient on average. Our analysis of genomics and functional datasets reveals in multiple organisms a strong inverse relationship between the optimality of protein molecular function and the rate of protein evolution. Furthermore, we find that highly expressed proteins tend to be substantially more functionally optimized. These results suggest that cellular expression costs lead to more pronounced functional optimization of abundant proteins and that the purifying selection to maintain high levels of functional optimality significantly slows protein evolution. We observe that in multicellular species both the rate of protein evolution and the degree of protein functional efficiency are primarily affected by expression in several distinct cell types and tissues, specifically, in developed neurons with upregulated synaptic processes in animals and in young and fast-growing tissues in plants. Overall, our analysis reveals how various constraints from the molecular, cellular, and species' levels of biological organization jointly affect the rate of protein evolution and the level of protein functional adaptation.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":" ","pages":""},"PeriodicalIF":11.0,"publicationDate":"2024-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11523136/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142470122","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Twinkle Biswas, Cassie Sims, Jothi Kumar Yuvaraj, Rebecca E Roberts, Christer Löfstedt, Martin N Andersson
Chemical communication using pheromones is thought to have contributed to the diversification and speciation of insects. The species-specific pheromones are detected by specialized pheromone receptors. Whereas the evolution and function of pheromone receptors have been extensively studied in Lepidoptera, only a few pheromone receptors have been identified in beetles, which limits our understanding of their evolutionary histories and physiological functions. To shed light on these questions, we aimed to functionally characterize potential pheromone receptors in the spruce bark beetle Ips typographus (‘Ityp’) and explore their evolutionary origins and molecular interactions with ligands. Males of this species release an aggregation pheromone comprising 2-methyl-3-buten-2-ol and (4S)-cis-verbenol, which attracts both sexes to attacked trees. Using two systems for functional characterization, we show that the highly expressed odorant receptor (OR) ItypOR41 responds specifically to (4S)-cis-verbenol, with structurally similar compounds eliciting minor responses. We next targeted the closely related ItypOR40 and ItypOR45. Whereas ItypOR40 was unresponsive, ItypOR45 showed an overlapping response profile with ItypOR41, but a broader tuning. Our phylogenetic analysis shows that these ORs are present in a different OR clade as compared to all other known beetle pheromone receptors, suggesting multiple evolutionary origins of pheromone receptors in bark beetles. Next, using computational analyses and experimental validation, we reveal two amino acid residues (Gln179 and Trp310) that are important for ligand binding and pheromone specificity of ItypOR41 for (4S)-cis-verbenol, possibly via hydrogen bonding to Gln179. Collectively, our results shed new light on the origins, specificity, and ligand binding mechanisms of pheromone receptors in beetles.
{"title":"Functional characterization supports multiple evolutionary origins of pheromone receptors in bark beetles","authors":"Twinkle Biswas, Cassie Sims, Jothi Kumar Yuvaraj, Rebecca E Roberts, Christer Löfstedt, Martin N Andersson","doi":"10.1093/molbev/msae196","DOIUrl":"https://doi.org/10.1093/molbev/msae196","url":null,"abstract":"Chemical communication using pheromones is thought to have contributed to the diversification and speciation of insects. The species-specific pheromones are detected by specialized pheromone receptors. Whereas the evolution and function of pheromone receptors have been extensively studied in Lepidoptera, only a few pheromone receptors have been identified in beetles, which limits our understanding of their evolutionary histories and physiological functions. To shed light on these questions, we aimed to functionally characterize potential pheromone receptors in the spruce bark beetle Ips typographus (‘Ityp’) and explore their evolutionary origins and molecular interactions with ligands. Males of this species release an aggregation pheromone comprising 2-methyl-3-buten-2-ol and (4S)-cis-verbenol, which attracts both sexes to attacked trees. Using two systems for functional characterization, we show that the highly expressed odorant receptor (OR) ItypOR41 responds specifically to (4S)-cis-verbenol, with structurally similar compounds eliciting minor responses. We next targeted the closely related ItypOR40 and ItypOR45. Whereas ItypOR40 was unresponsive, ItypOR45 showed an overlapping response profile with ItypOR41, but a broader tuning. Our phylogenetic analysis shows that these ORs are present in a different OR clade as compared to all other known beetle pheromone receptors, suggesting multiple evolutionary origins of pheromone receptors in bark beetles. Next, using computational analyses and experimental validation, we reveal two amino acid residues (Gln179 and Trp310) that are important for ligand binding and pheromone specificity of ItypOR41 for (4S)-cis-verbenol, possibly via hydrogen bonding to Gln179. Collectively, our results shed new light on the origins, specificity, and ligand binding mechanisms of pheromone receptors in beetles.","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":"2 1","pages":""},"PeriodicalIF":10.7,"publicationDate":"2024-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142248019","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Identifying soft selective sweeps using genomic data is a challenging yet crucial task in population genetics. In this study, we present HaploSweep, a novel method for detecting and categorizing soft and hard selective sweeps based on haplotype structure. Through simulations spanning a broad range of selection intensities, softness levels, and demographic histories, we demonstrate that HaploSweep outperforms iHS, nSL, and H12 in detecting soft sweeps. HaploSweep achieves high classification accuracy—0.9247 for CHB, 0.9484 for CEU, and 0.9829 YRI—when applied to simulations in line with the human Out-of-Africa demographic model. We also observe that the classification accuracy remains consistently robust across different demographic models. Additionally, we introduce a refined method to accurately distinguish soft shoulders adjacent to hard sweeps from soft sweeps. Application of HaploSweep to genomic data of CHB, CEU, and YRI populations from the 1000 genomes project has led to the discovery of several new genes that bear strong evidence of population-specific soft sweeps (HRNR, AMBRA1, BFA2T2, DYNC2H1, and RANBP2 etc), with prevalent associations to immune functions and metabolic processes. The validated performance of HaploSweep, demonstrated through both simulated and real data, underscores its potential as a valuable tool for detecting and comprehending the role of soft sweeps in adaptive evolution.
{"title":"HaploSweep: detecting and distinguishing recent soft and hard selective sweeps through haplotype structure","authors":"Shilei Zhao, Lianjiang Chi, Mincong Fu, Hua Chen","doi":"10.1093/molbev/msae192","DOIUrl":"https://doi.org/10.1093/molbev/msae192","url":null,"abstract":"Identifying soft selective sweeps using genomic data is a challenging yet crucial task in population genetics. In this study, we present HaploSweep, a novel method for detecting and categorizing soft and hard selective sweeps based on haplotype structure. Through simulations spanning a broad range of selection intensities, softness levels, and demographic histories, we demonstrate that HaploSweep outperforms iHS, nSL, and H12 in detecting soft sweeps. HaploSweep achieves high classification accuracy—0.9247 for CHB, 0.9484 for CEU, and 0.9829 YRI—when applied to simulations in line with the human Out-of-Africa demographic model. We also observe that the classification accuracy remains consistently robust across different demographic models. Additionally, we introduce a refined method to accurately distinguish soft shoulders adjacent to hard sweeps from soft sweeps. Application of HaploSweep to genomic data of CHB, CEU, and YRI populations from the 1000 genomes project has led to the discovery of several new genes that bear strong evidence of population-specific soft sweeps (HRNR, AMBRA1, BFA2T2, DYNC2H1, and RANBP2 etc), with prevalent associations to immune functions and metabolic processes. The validated performance of HaploSweep, demonstrated through both simulated and real data, underscores its potential as a valuable tool for detecting and comprehending the role of soft sweeps in adaptive evolution.","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":"33 1","pages":""},"PeriodicalIF":10.7,"publicationDate":"2024-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142248020","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Cate B Quinn, Sophie Preckler-Quisquater, Michael R Buchalski, Benjamin N Sacks
A few iconic examples have proven the value of facilitated gene flow for counteracting inbreeding depression and staving off extinction, yet the practice is often not implemented for fear of causing outbreeding depression. Using genomic sequencing, climatic niche modeling, and demographic reconstruction, we sought to assess the risks and benefits of using translocations as a tool for recovery of endangered montane red fox (Vulpes vulpes) populations in the western United States. We demonstrated elevated inbreeding and homozygosity of deleterious alleles across all populations, but especially those isolated in the Cascade and Sierra Nevada ranges. Consequently, translocations would be expected to increase population growth by masking deleterious recessive alleles. Demographic reconstructions further indicated shallow divergences of less than a few thousand years among montane populations, suggesting low risk of outbreeding depression. These genomic-guided findings set the stage for future management, the documentation of which will provide a roadmap for recovery of other data-deficient taxa.
{"title":"Whole genomes inform genetic rescue strategy for montane red foxes in North America","authors":"Cate B Quinn, Sophie Preckler-Quisquater, Michael R Buchalski, Benjamin N Sacks","doi":"10.1093/molbev/msae193","DOIUrl":"https://doi.org/10.1093/molbev/msae193","url":null,"abstract":"A few iconic examples have proven the value of facilitated gene flow for counteracting inbreeding depression and staving off extinction, yet the practice is often not implemented for fear of causing outbreeding depression. Using genomic sequencing, climatic niche modeling, and demographic reconstruction, we sought to assess the risks and benefits of using translocations as a tool for recovery of endangered montane red fox (Vulpes vulpes) populations in the western United States. We demonstrated elevated inbreeding and homozygosity of deleterious alleles across all populations, but especially those isolated in the Cascade and Sierra Nevada ranges. Consequently, translocations would be expected to increase population growth by masking deleterious recessive alleles. Demographic reconstructions further indicated shallow divergences of less than a few thousand years among montane populations, suggesting low risk of outbreeding depression. These genomic-guided findings set the stage for future management, the documentation of which will provide a roadmap for recovery of other data-deficient taxa.","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":"2 1","pages":""},"PeriodicalIF":10.7,"publicationDate":"2024-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142248017","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}