Rapid diversification of St-genome-sharing species in wheat grasses (Triticeae: Poaceae) accompanied by diversifying selection of chloroplast genes

Abstract Background The St-genome-sharing taxa are highly complex group of the species with the St nuclear genome and monophyletic origin in maternal lineages within the Triticeae, which contains more than half of polyploid species that distributed in a wide range of ecological habitats. While high...

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Main Authors: Li-Na Sha, Ning Chen, Shi-Yong Chen, Yue Zhang, Yi-Ran Cheng, Dan-Dan Wu, Yi Wang, Hou-Yang Kang, Hai-Qin Zhang, Xiao Ma, Yong-Hong Zhou, Xing Fan
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Language:English
Published: BMC 2025-01-01
Series:BMC Plant Biology
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Online Access:https://doi.org/10.1186/s12870-025-06051-6
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author Li-Na Sha
Ning Chen
Shi-Yong Chen
Yue Zhang
Yi-Ran Cheng
Dan-Dan Wu
Yi Wang
Hou-Yang Kang
Hai-Qin Zhang
Xiao Ma
Yong-Hong Zhou
Xing Fan
author_facet Li-Na Sha
Ning Chen
Shi-Yong Chen
Yue Zhang
Yi-Ran Cheng
Dan-Dan Wu
Yi Wang
Hou-Yang Kang
Hai-Qin Zhang
Xiao Ma
Yong-Hong Zhou
Xing Fan
author_sort Li-Na Sha
collection DOAJ
description Abstract Background The St-genome-sharing taxa are highly complex group of the species with the St nuclear genome and monophyletic origin in maternal lineages within the Triticeae, which contains more than half of polyploid species that distributed in a wide range of ecological habitats. While high level of genetic heterogeneity in plastome DNA due to a reticulate evolutionary event has been considered to link with the richness of the St-genome-sharing taxa, the relationship between the dynamics of diversification and molecular evolution is lack of understanding. Results Here, integrating 106 previously and 12 newly sequenced plastomes representing almost all previously recognized genomic types and genus of the Triticeae, this study applies phylogenetic reconstruction methods in combination with lineage diversification analyses, estimate of sequence evolution, and gene expression to investigate the dynamics of diversification in the tribe. Phylogenomic analysis confirmed previous phylogenetic relationships, with the St/E/V lineages (Pseudoroegneria/Lophopyrum + Thinopyrum/Dasypyrum) being suffered from a chloroplast capture event prior to polyploidization events. Analyses of diversification rates detected a significant acceleration approximately five million years ago in the St-genome-sharing taxa. Molecular tests of evolution and gene expression further indicated that radiation within the accelerated group has been accompanied by adaptive genetic changes in a few chloroplast-encoded genes directly or indirectly related to photosynthesis. Conclusions Our results support an important role for adaptive evolution in plastomes during accelerated diversification. In combination with plastome data, further investigations using other genomes, such as the nuclear genome, are urgently needed to enhance our understanding of the evolutionary history of the St-genome-sharing taxa, especially to determine whether adaptive changes in the nuclear genome are accelerated as well because plastome represents the maternal inheritation in angiosperms.
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institution Kabale University
issn 1471-2229
language English
publishDate 2025-01-01
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series BMC Plant Biology
spelling doaj-art-08e0bb06317948b5b6ae9c1d326f23132025-01-12T12:14:18ZengBMCBMC Plant Biology1471-22292025-01-0125111210.1186/s12870-025-06051-6Rapid diversification of St-genome-sharing species in wheat grasses (Triticeae: Poaceae) accompanied by diversifying selection of chloroplast genesLi-Na Sha0Ning Chen1Shi-Yong Chen2Yue Zhang3Yi-Ran Cheng4Dan-Dan Wu5Yi Wang6Hou-Yang Kang7Hai-Qin Zhang8Xiao Ma9Yong-Hong Zhou10Xing Fan11College of Grassland Science and Technology, Sichuan Agricultural UniversityTriticeae Research Institute, Sichuan Agricultural UniversityTriticeae Research Institute, Sichuan Agricultural UniversityTriticeae Research Institute, Sichuan Agricultural UniversityTriticeae Research Institute, Sichuan Agricultural UniversityTriticeae Research Institute, Sichuan Agricultural UniversityTriticeae Research Institute, Sichuan Agricultural UniversityTriticeae Research Institute, Sichuan Agricultural UniversityTriticeae Research Institute, Sichuan Agricultural UniversityCollege of Grassland Science and Technology, Sichuan Agricultural UniversityTriticeae Research Institute, Sichuan Agricultural UniversityTriticeae Research Institute, Sichuan Agricultural UniversityAbstract Background The St-genome-sharing taxa are highly complex group of the species with the St nuclear genome and monophyletic origin in maternal lineages within the Triticeae, which contains more than half of polyploid species that distributed in a wide range of ecological habitats. While high level of genetic heterogeneity in plastome DNA due to a reticulate evolutionary event has been considered to link with the richness of the St-genome-sharing taxa, the relationship between the dynamics of diversification and molecular evolution is lack of understanding. Results Here, integrating 106 previously and 12 newly sequenced plastomes representing almost all previously recognized genomic types and genus of the Triticeae, this study applies phylogenetic reconstruction methods in combination with lineage diversification analyses, estimate of sequence evolution, and gene expression to investigate the dynamics of diversification in the tribe. Phylogenomic analysis confirmed previous phylogenetic relationships, with the St/E/V lineages (Pseudoroegneria/Lophopyrum + Thinopyrum/Dasypyrum) being suffered from a chloroplast capture event prior to polyploidization events. Analyses of diversification rates detected a significant acceleration approximately five million years ago in the St-genome-sharing taxa. Molecular tests of evolution and gene expression further indicated that radiation within the accelerated group has been accompanied by adaptive genetic changes in a few chloroplast-encoded genes directly or indirectly related to photosynthesis. Conclusions Our results support an important role for adaptive evolution in plastomes during accelerated diversification. In combination with plastome data, further investigations using other genomes, such as the nuclear genome, are urgently needed to enhance our understanding of the evolutionary history of the St-genome-sharing taxa, especially to determine whether adaptive changes in the nuclear genome are accelerated as well because plastome represents the maternal inheritation in angiosperms.https://doi.org/10.1186/s12870-025-06051-6TriticeaeRadiationChloroplast genomeAdaptive evolutionSelection
spellingShingle Li-Na Sha
Ning Chen
Shi-Yong Chen
Yue Zhang
Yi-Ran Cheng
Dan-Dan Wu
Yi Wang
Hou-Yang Kang
Hai-Qin Zhang
Xiao Ma
Yong-Hong Zhou
Xing Fan
Rapid diversification of St-genome-sharing species in wheat grasses (Triticeae: Poaceae) accompanied by diversifying selection of chloroplast genes
BMC Plant Biology
Triticeae
Radiation
Chloroplast genome
Adaptive evolution
Selection
title Rapid diversification of St-genome-sharing species in wheat grasses (Triticeae: Poaceae) accompanied by diversifying selection of chloroplast genes
title_full Rapid diversification of St-genome-sharing species in wheat grasses (Triticeae: Poaceae) accompanied by diversifying selection of chloroplast genes
title_fullStr Rapid diversification of St-genome-sharing species in wheat grasses (Triticeae: Poaceae) accompanied by diversifying selection of chloroplast genes
title_full_unstemmed Rapid diversification of St-genome-sharing species in wheat grasses (Triticeae: Poaceae) accompanied by diversifying selection of chloroplast genes
title_short Rapid diversification of St-genome-sharing species in wheat grasses (Triticeae: Poaceae) accompanied by diversifying selection of chloroplast genes
title_sort rapid diversification of st genome sharing species in wheat grasses triticeae poaceae accompanied by diversifying selection of chloroplast genes
topic Triticeae
Radiation
Chloroplast genome
Adaptive evolution
Selection
url https://doi.org/10.1186/s12870-025-06051-6
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