Nian Zhou, Ke Miao, Luxiao Hou, Haiyang Liu, Jiahui Chen, Yunheng Ji
{"title":"系统转录组学分析揭示了巴黎木属(Melanthiaceae)的进化复杂性,该属形态独特,具有重要的药用价值。","authors":"Nian Zhou, Ke Miao, Luxiao Hou, Haiyang Liu, Jiahui Chen, Yunheng Ji","doi":"10.1093/aob/mcae156","DOIUrl":null,"url":null,"abstract":"<p><strong>Background and aims: </strong>Previous phylogenetic studies on the pharmaceutically significant genus Paris (Melanthiaceae) have consistently revealed substantial cytonuclear discordance, yet the underlying mechanism responsible for this phenomenon remains elusive. This study aims to reconstruct a robust nuclear backbone phylogeny and elucidate the potential evolutionarily complex events contributing to previously observed cytonuclear discordance within Paris.</p><p><strong>Methods: </strong>Based on a comprehensive set of nuclear low-copy orthologous genes obtained from transcriptomic data, the intrageneric phylogeny of Paris, along with its phylogenetic relationships to allied genera were inferred, using coalescent and concatenated approaches. The analysis of gene tree discordance and reticulate evolution, in conjunction with an incomplete lineage sorting (ILS) simulation, was conducted to explore potential hybridization and ILS events in the evolutionary history of Paris and assess their contribution to the discordance of gene trees.</p><p><strong>Key results: </strong>The nuclear phylogeny unequivocally confirmed the monophyly of Paris and its sister relationship with Trillium, while widespread incongruences in gene trees were observed at the majority of internal nodes within Paris. The reticulate evolution analysis identified five instances of hybridization events in Paris, indicating that hybridization events might have recurrently occurred throughout the evolutionary history of Paris. In contrast, the ILS simulations revealed that only two internal nodes within sect. Euthyra experienced ILS events.</p><p><strong>Conclusions: </strong>Our data suggest that the previously observed cytonuclear discordance in the phylogeny of Paris can primarily be attributed to recurrent hybridization events, with secondary contributions from infrequent ILS events. The recurrent hybridization events in the evolutionary history of Paris not only drove lineage diversification and speciation but also facilitated morphological innovation, and enhanced ecological adaptability. Therefore, artificial hybridization has great potential for breeding medicinal Paris species. These findings significantly contribute to our comprehensive understanding of the evolutionary complexity of this pharmaceutically significant plant lineage, thereby facilitating effective exploration and conservation efforts.</p>","PeriodicalId":8023,"journal":{"name":"Annals of botany","volume":null,"pages":null},"PeriodicalIF":3.6000,"publicationDate":"2024-09-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Phylotranscriptomic analyses reveal the evolutionary complexity of Paris L. 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This study aims to reconstruct a robust nuclear backbone phylogeny and elucidate the potential evolutionarily complex events contributing to previously observed cytonuclear discordance within Paris.</p><p><strong>Methods: </strong>Based on a comprehensive set of nuclear low-copy orthologous genes obtained from transcriptomic data, the intrageneric phylogeny of Paris, along with its phylogenetic relationships to allied genera were inferred, using coalescent and concatenated approaches. The analysis of gene tree discordance and reticulate evolution, in conjunction with an incomplete lineage sorting (ILS) simulation, was conducted to explore potential hybridization and ILS events in the evolutionary history of Paris and assess their contribution to the discordance of gene trees.</p><p><strong>Key results: </strong>The nuclear phylogeny unequivocally confirmed the monophyly of Paris and its sister relationship with Trillium, while widespread incongruences in gene trees were observed at the majority of internal nodes within Paris. The reticulate evolution analysis identified five instances of hybridization events in Paris, indicating that hybridization events might have recurrently occurred throughout the evolutionary history of Paris. In contrast, the ILS simulations revealed that only two internal nodes within sect. 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引用次数: 0
摘要
背景和目的:以前对具有重要药用价值的巴黎属(Melanthiaceae)进行的系统发育研究一直揭示了大量的胞核不一致性,但造成这种现象的潜在机制仍然难以捉摸。本研究旨在重建一个强大的核骨干系统发育,并阐明导致之前观察到的巴黎属细胞核不一致的潜在复杂进化事件:方法:基于从转录组数据中获得的一整套核低拷贝直向同源基因,利用聚合和连接方法推断了巴黎属的属内系统发育及其与同属的系统发育关系。结合不完全世系分类(ILS)模拟,对基因树的不一致性和网状进化进行了分析,以探索巴黎属进化史中潜在的杂交和 ILS 事件,并评估它们对基因树不一致性的影响:主要结果:核系统进化明确证实了巴黎树的单系性及其与三叶草的姊妹关系,而在巴黎树的大部分内部节点上观察到了基因树的广泛不一致性。网状进化分析在巴黎中发现了五次杂交事件,表明杂交事件可能在巴黎的整个进化历史中反复发生。与此相反,ILS模拟显示,在Euthyra科中只有两个内部节点经历了ILS事件。结论:我们的数据表明,之前观察到的巴黎龙系统发育中的细胞核不一致性主要归因于反复发生的杂交事件,其次才是不经常发生的 ILS 事件。巴黎鱼进化史中反复发生的杂交事件不仅推动了鱼系的多样化和物种的分化,还促进了形态创新,增强了生态适应性。因此,人工杂交在培育药用巴黎树种方面具有巨大潜力。这些发现大大有助于我们全面了解这一具有重要药用价值的植物品系的进化复杂性,从而促进有效的探索和保护工作。
Phylotranscriptomic analyses reveal the evolutionary complexity of Paris L. (Melanthiaceae), a morphologically distinctive genus with significant pharmaceutical importance.
Background and aims: Previous phylogenetic studies on the pharmaceutically significant genus Paris (Melanthiaceae) have consistently revealed substantial cytonuclear discordance, yet the underlying mechanism responsible for this phenomenon remains elusive. This study aims to reconstruct a robust nuclear backbone phylogeny and elucidate the potential evolutionarily complex events contributing to previously observed cytonuclear discordance within Paris.
Methods: Based on a comprehensive set of nuclear low-copy orthologous genes obtained from transcriptomic data, the intrageneric phylogeny of Paris, along with its phylogenetic relationships to allied genera were inferred, using coalescent and concatenated approaches. The analysis of gene tree discordance and reticulate evolution, in conjunction with an incomplete lineage sorting (ILS) simulation, was conducted to explore potential hybridization and ILS events in the evolutionary history of Paris and assess their contribution to the discordance of gene trees.
Key results: The nuclear phylogeny unequivocally confirmed the monophyly of Paris and its sister relationship with Trillium, while widespread incongruences in gene trees were observed at the majority of internal nodes within Paris. The reticulate evolution analysis identified five instances of hybridization events in Paris, indicating that hybridization events might have recurrently occurred throughout the evolutionary history of Paris. In contrast, the ILS simulations revealed that only two internal nodes within sect. Euthyra experienced ILS events.
Conclusions: Our data suggest that the previously observed cytonuclear discordance in the phylogeny of Paris can primarily be attributed to recurrent hybridization events, with secondary contributions from infrequent ILS events. The recurrent hybridization events in the evolutionary history of Paris not only drove lineage diversification and speciation but also facilitated morphological innovation, and enhanced ecological adaptability. Therefore, artificial hybridization has great potential for breeding medicinal Paris species. These findings significantly contribute to our comprehensive understanding of the evolutionary complexity of this pharmaceutically significant plant lineage, thereby facilitating effective exploration and conservation efforts.
期刊介绍:
Annals of Botany is an international plant science journal publishing novel and rigorous research in all areas of plant science. It is published monthly in both electronic and printed forms with at least two extra issues each year that focus on a particular theme in plant biology. The Journal is managed by the Annals of Botany Company, a not-for-profit educational charity established to promote plant science worldwide.
The Journal publishes original research papers, invited and submitted review articles, ''Research in Context'' expanding on original work, ''Botanical Briefings'' as short overviews of important topics, and ''Viewpoints'' giving opinions. All papers in each issue are summarized briefly in Content Snapshots , there are topical news items in the Plant Cuttings section and Book Reviews . A rigorous review process ensures that readers are exposed to genuine and novel advances across a wide spectrum of botanical knowledge. All papers aim to advance knowledge and make a difference to our understanding of plant science.