Genetic differentiation and historical dynamics of the endemic species Rheum pumilum on the Qinghai-Tibetan Plateau inferred from phylogeography implications

Abstract Background Rheum pumilum, an endemic species on the Qinghai-Tibetan Plateau (QTP), serves as an ideal material for investigating the phylogeography of alpine plants. This study employs chloroplast DNA fragments (trnL-F, trnS-G, and matK) to delve into how Rh. pumilum adapted to the extreme...

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Main Authors: Shuliang Liu, Jianxin Gao, Bo Xiao, Wenjie Guo, Qiushi Yu, Ailan Wang, Weiwei Li
Format: Article
Language:English
Published: BMC 2025-02-01
Series:BMC Plant Biology
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Online Access:https://doi.org/10.1186/s12870-025-06164-y
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author Shuliang Liu
Jianxin Gao
Bo Xiao
Wenjie Guo
Qiushi Yu
Ailan Wang
Weiwei Li
author_facet Shuliang Liu
Jianxin Gao
Bo Xiao
Wenjie Guo
Qiushi Yu
Ailan Wang
Weiwei Li
author_sort Shuliang Liu
collection DOAJ
description Abstract Background Rheum pumilum, an endemic species on the Qinghai-Tibetan Plateau (QTP), serves as an ideal material for investigating the phylogeography of alpine plants. This study employs chloroplast DNA fragments (trnL-F, trnS-G, and matK) to delve into how Rh. pumilum adapted to the extreme environmental changes on the QTP, during its evolutionary process through phylogenetic geographical analysis, revealing its population differentiation and historical dynamics. Results The examination of 39 haplotypes across 26 populations of Rh. pumilum reveals distinct regional distribution, reflecting a phylogeographic pattern resembling “alpine-island”. The total genetic diversity of Rh. pumilum is remarkably high (Ht = 0.910), with the majority of genetic variation primarily occurred among populations (84.5%) with limited gene flow, indicating geographic isolation influenced by diverse habitats of plateau. The geographic isolation model is further supported by various analytical methods, including AMOVA analysis, UPGMA dendrogram, PCoA, Structure analysis, and Mantel test. Micro-refugia for Rh. pumilum during the Quaternary ice ages are supported by haplotype network and genetic diversity analysis. The absence of a typical “star-shape” pattern in the overall haplotype network suggests that Rh. pumilum likely maintains a stable state without experiencing rapid expansion, which has been supported by mismatch distribution analysis. Ecological Niche Modeling (ENM) indicates sensitivity of Rh. pumilum to humidity, temperature and altitude, aligning with a historical distribution resembling a “displacement refugia” model during the Quaternary ice ages. The involvement of Rh. kialense and Rh. sublanceolatum in the origin and gene introgression of Rh. pumilum is suggested, possibly as maternal ancestors of closely related haplotypes. Haplotype divergence of Rh. pumilum approximately 11 million years ago, with notable divergence peaks observed during the late Miocene, as well as the Pliocene, Pleistocene and Holocene. Conclusion These findings suggest a correlation between genetic diversity, haplotype lineage divergence and key geological and climatic events, notably the uplift of the QTP, monsoon climate changes, and the climatic oscillations during the Quaternary ice ages. This study might provide valuable insights into the formation mechanisms of plant diversity on the QTP, crucial for biodiversity conservation and sustainable species development in extreme environments.
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spelling doaj-art-332060c61b934d3582fc7e1e7cc9d5452025-02-09T12:27:52ZengBMCBMC Plant Biology1471-22292025-02-0125111710.1186/s12870-025-06164-yGenetic differentiation and historical dynamics of the endemic species Rheum pumilum on the Qinghai-Tibetan Plateau inferred from phylogeography implicationsShuliang Liu0Jianxin Gao1Bo Xiao2Wenjie Guo3Qiushi Yu4Ailan Wang5Weiwei Li6School of Life Sciences, Ludong UniversitySchool of Life Sciences, Ludong UniversitySchool of Life Sciences, Ludong UniversitySchool of Life Sciences, Ludong UniversityGansu Academy of ForestrySchool of Life Sciences, Ludong UniversitySchool of Life Sciences, Ludong UniversityAbstract Background Rheum pumilum, an endemic species on the Qinghai-Tibetan Plateau (QTP), serves as an ideal material for investigating the phylogeography of alpine plants. This study employs chloroplast DNA fragments (trnL-F, trnS-G, and matK) to delve into how Rh. pumilum adapted to the extreme environmental changes on the QTP, during its evolutionary process through phylogenetic geographical analysis, revealing its population differentiation and historical dynamics. Results The examination of 39 haplotypes across 26 populations of Rh. pumilum reveals distinct regional distribution, reflecting a phylogeographic pattern resembling “alpine-island”. The total genetic diversity of Rh. pumilum is remarkably high (Ht = 0.910), with the majority of genetic variation primarily occurred among populations (84.5%) with limited gene flow, indicating geographic isolation influenced by diverse habitats of plateau. The geographic isolation model is further supported by various analytical methods, including AMOVA analysis, UPGMA dendrogram, PCoA, Structure analysis, and Mantel test. Micro-refugia for Rh. pumilum during the Quaternary ice ages are supported by haplotype network and genetic diversity analysis. The absence of a typical “star-shape” pattern in the overall haplotype network suggests that Rh. pumilum likely maintains a stable state without experiencing rapid expansion, which has been supported by mismatch distribution analysis. Ecological Niche Modeling (ENM) indicates sensitivity of Rh. pumilum to humidity, temperature and altitude, aligning with a historical distribution resembling a “displacement refugia” model during the Quaternary ice ages. The involvement of Rh. kialense and Rh. sublanceolatum in the origin and gene introgression of Rh. pumilum is suggested, possibly as maternal ancestors of closely related haplotypes. Haplotype divergence of Rh. pumilum approximately 11 million years ago, with notable divergence peaks observed during the late Miocene, as well as the Pliocene, Pleistocene and Holocene. Conclusion These findings suggest a correlation between genetic diversity, haplotype lineage divergence and key geological and climatic events, notably the uplift of the QTP, monsoon climate changes, and the climatic oscillations during the Quaternary ice ages. This study might provide valuable insights into the formation mechanisms of plant diversity on the QTP, crucial for biodiversity conservation and sustainable species development in extreme environments.https://doi.org/10.1186/s12870-025-06164-yRheum pumilumPhylogeographycpDNAThe Qinghai-Tibetan PlateauEcological niche
spellingShingle Shuliang Liu
Jianxin Gao
Bo Xiao
Wenjie Guo
Qiushi Yu
Ailan Wang
Weiwei Li
Genetic differentiation and historical dynamics of the endemic species Rheum pumilum on the Qinghai-Tibetan Plateau inferred from phylogeography implications
BMC Plant Biology
Rheum pumilum
Phylogeography
cpDNA
The Qinghai-Tibetan Plateau
Ecological niche
title Genetic differentiation and historical dynamics of the endemic species Rheum pumilum on the Qinghai-Tibetan Plateau inferred from phylogeography implications
title_full Genetic differentiation and historical dynamics of the endemic species Rheum pumilum on the Qinghai-Tibetan Plateau inferred from phylogeography implications
title_fullStr Genetic differentiation and historical dynamics of the endemic species Rheum pumilum on the Qinghai-Tibetan Plateau inferred from phylogeography implications
title_full_unstemmed Genetic differentiation and historical dynamics of the endemic species Rheum pumilum on the Qinghai-Tibetan Plateau inferred from phylogeography implications
title_short Genetic differentiation and historical dynamics of the endemic species Rheum pumilum on the Qinghai-Tibetan Plateau inferred from phylogeography implications
title_sort genetic differentiation and historical dynamics of the endemic species rheum pumilum on the qinghai tibetan plateau inferred from phylogeography implications
topic Rheum pumilum
Phylogeography
cpDNA
The Qinghai-Tibetan Plateau
Ecological niche
url https://doi.org/10.1186/s12870-025-06164-y
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