The mechanism of tetraploidization in tree peony, and its implications for speciation and evolution of genus Paeonia L.

IntroductionPolyploidization is not only an important driving force for plant speciation and evolution, but also an effective approach for plant domestication and improvement. Polyploid taxa are quite common in Paeonia section Paeonia (herbaceous peonies), but very rare in section Moutan (tree peoni...

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Main Authors: Yuan Zhong, Ming-jie Du, Run-ze Ji, Fang-yun Cheng
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-05-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2025.1586225/full
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author Yuan Zhong
Yuan Zhong
Ming-jie Du
Ming-jie Du
Run-ze Ji
Run-ze Ji
Fang-yun Cheng
Fang-yun Cheng
author_facet Yuan Zhong
Yuan Zhong
Ming-jie Du
Ming-jie Du
Run-ze Ji
Run-ze Ji
Fang-yun Cheng
Fang-yun Cheng
author_sort Yuan Zhong
collection DOAJ
description IntroductionPolyploidization is not only an important driving force for plant speciation and evolution, but also an effective approach for plant domestication and improvement. Polyploid taxa are quite common in Paeonia section Paeonia (herbaceous peonies), but very rare in section Moutan (tree peonies), which are known as the ‘king of flowers’.MethodsIn this paper, we studied the origination of a tetraploid tree peony, P. × lemoinei ‘Golden Era’ (‘GE’, AABB), by comparing its karyotype with its seed parent, P. × lemoinei ‘Golden Isles’ (‘GI’, AB), based on genomic in situ hybridization (GISH) and rDNA fluorescence in situ hybridization (FISH). The meiosis behaviors of ‘GI’ were observed to make clear the cytogenetic process of unreduced (2n) gamete generation.ResultsFour chromosomes with inter-genome translocations were identified in ‘GE’, two of which might be reciprocal translocations. The 2n female gametes via first division restitution (FDR) from ‘GI’ might play an important role in tetraploidization of ‘GE’.DisucssionThe distant hybridization between intersterile species from different subsections of section Moutan probably promotes the tetraploidization of tree peonies by facilitating 2n gamete production. The mechanism of tetraploidization in section Moutan is highly consistent with that in section Paeonia, but is inseparable with the assist from mankind. The divergence of life history between tree peonies and herbaceous peonies is speculated to contribute to the different level of polyploidization, and distinct tempo of speciation and evolution, between section Moutan and section Paeonia in genus Paeonia. These findings bring new insights to polyploid breeding, speciation and evolution in genus Paeonia.
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spelling doaj-art-d2be302bf4bf4d0384205d62945d0e542025-08-20T03:09:41ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-05-011610.3389/fpls.2025.15862251586225The mechanism of tetraploidization in tree peony, and its implications for speciation and evolution of genus Paeonia L.Yuan Zhong0Yuan Zhong1Ming-jie Du2Ming-jie Du3Run-ze Ji4Run-ze Ji5Fang-yun Cheng6Fang-yun Cheng7State Key Laboratory of Efficient Production of Forest Resources, National Engineering Research Center for Floriculture, Peony International Institute, School of Landscape Architecture, Beijing Forestry University, Beijing, ChinaBeijing Key Laboratory of Ornamental Plants Germplasm Innovation & Molecular Breeding, National Engineering Research Center for Floriculture, Peony International Institute, School of Landscape Architecture, Beijing Forestry University, Beijing, ChinaState Key Laboratory of Efficient Production of Forest Resources, National Engineering Research Center for Floriculture, Peony International Institute, School of Landscape Architecture, Beijing Forestry University, Beijing, ChinaBeijing Key Laboratory of Ornamental Plants Germplasm Innovation & Molecular Breeding, National Engineering Research Center for Floriculture, Peony International Institute, School of Landscape Architecture, Beijing Forestry University, Beijing, ChinaState Key Laboratory of Efficient Production of Forest Resources, National Engineering Research Center for Floriculture, Peony International Institute, School of Landscape Architecture, Beijing Forestry University, Beijing, ChinaBeijing Key Laboratory of Ornamental Plants Germplasm Innovation & Molecular Breeding, National Engineering Research Center for Floriculture, Peony International Institute, School of Landscape Architecture, Beijing Forestry University, Beijing, ChinaState Key Laboratory of Efficient Production of Forest Resources, National Engineering Research Center for Floriculture, Peony International Institute, School of Landscape Architecture, Beijing Forestry University, Beijing, ChinaBeijing Key Laboratory of Ornamental Plants Germplasm Innovation & Molecular Breeding, National Engineering Research Center for Floriculture, Peony International Institute, School of Landscape Architecture, Beijing Forestry University, Beijing, ChinaIntroductionPolyploidization is not only an important driving force for plant speciation and evolution, but also an effective approach for plant domestication and improvement. Polyploid taxa are quite common in Paeonia section Paeonia (herbaceous peonies), but very rare in section Moutan (tree peonies), which are known as the ‘king of flowers’.MethodsIn this paper, we studied the origination of a tetraploid tree peony, P. × lemoinei ‘Golden Era’ (‘GE’, AABB), by comparing its karyotype with its seed parent, P. × lemoinei ‘Golden Isles’ (‘GI’, AB), based on genomic in situ hybridization (GISH) and rDNA fluorescence in situ hybridization (FISH). The meiosis behaviors of ‘GI’ were observed to make clear the cytogenetic process of unreduced (2n) gamete generation.ResultsFour chromosomes with inter-genome translocations were identified in ‘GE’, two of which might be reciprocal translocations. The 2n female gametes via first division restitution (FDR) from ‘GI’ might play an important role in tetraploidization of ‘GE’.DisucssionThe distant hybridization between intersterile species from different subsections of section Moutan probably promotes the tetraploidization of tree peonies by facilitating 2n gamete production. The mechanism of tetraploidization in section Moutan is highly consistent with that in section Paeonia, but is inseparable with the assist from mankind. The divergence of life history between tree peonies and herbaceous peonies is speculated to contribute to the different level of polyploidization, and distinct tempo of speciation and evolution, between section Moutan and section Paeonia in genus Paeonia. These findings bring new insights to polyploid breeding, speciation and evolution in genus Paeonia.https://www.frontiersin.org/articles/10.3389/fpls.2025.1586225/fullkaryotypemeiosisGISHFISHhybridpolypoid
spellingShingle Yuan Zhong
Yuan Zhong
Ming-jie Du
Ming-jie Du
Run-ze Ji
Run-ze Ji
Fang-yun Cheng
Fang-yun Cheng
The mechanism of tetraploidization in tree peony, and its implications for speciation and evolution of genus Paeonia L.
Frontiers in Plant Science
karyotype
meiosis
GISH
FISH
hybrid
polypoid
title The mechanism of tetraploidization in tree peony, and its implications for speciation and evolution of genus Paeonia L.
title_full The mechanism of tetraploidization in tree peony, and its implications for speciation and evolution of genus Paeonia L.
title_fullStr The mechanism of tetraploidization in tree peony, and its implications for speciation and evolution of genus Paeonia L.
title_full_unstemmed The mechanism of tetraploidization in tree peony, and its implications for speciation and evolution of genus Paeonia L.
title_short The mechanism of tetraploidization in tree peony, and its implications for speciation and evolution of genus Paeonia L.
title_sort mechanism of tetraploidization in tree peony and its implications for speciation and evolution of genus paeonia l
topic karyotype
meiosis
GISH
FISH
hybrid
polypoid
url https://www.frontiersin.org/articles/10.3389/fpls.2025.1586225/full
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