Non-Target Metabolomics Reveals Changes in Metabolite Profiles in Distant Hybrid Incompatibility Between <i>Paeonia</i> sect. <i>Moutan </i>and<i> P. lactiflora</i>

Peonies are globally renowned ornamental plants, and distant hybridization is a key method for breeding new varieties, though it often faces cross-incompatibility challenges. The metabolic mechanisms underlying the crossing barrier between tree peony (<i>Paeonia</i> sect<i>. Moutan...

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Main Authors: Wenqing Jia, Yingyue Yu, Zhaorong Mi, Yan Zhang, Guodong Zhao, Yingzi Guo, Zheng Wang, Erqiang Wang, Songlin He
Format: Article
Language:English
Published: MDPI AG 2025-05-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/14/9/1381
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author Wenqing Jia
Yingyue Yu
Zhaorong Mi
Yan Zhang
Guodong Zhao
Yingzi Guo
Zheng Wang
Erqiang Wang
Songlin He
author_facet Wenqing Jia
Yingyue Yu
Zhaorong Mi
Yan Zhang
Guodong Zhao
Yingzi Guo
Zheng Wang
Erqiang Wang
Songlin He
author_sort Wenqing Jia
collection DOAJ
description Peonies are globally renowned ornamental plants, and distant hybridization is a key method for breeding new varieties, though it often faces cross-incompatibility challenges. The metabolic mechanisms underlying the crossing barrier between tree peony (<i>Paeonia</i> sect<i>. Moutan</i>) and herbaceous peony (<i>P. lactiflora</i>) remain unclear. To identify key metabolites involved in cross-incompatibility, we performed a cross between <i>P. ostii</i> ‘Fengdanbai’ (female parent) and <i>P. lactiflora</i> ‘Red Sara’ (male parent) and analyzed metabolites in the stigma 12 h after pollination using UPLC-MS. We identified 1242 differential metabolites, with 433 up-regulated and 809 down-regulated, including sugars, nucleotides, amino acids, lipids, organic acids, benzenoids, flavonoids, and alkaloids. Most differential metabolites were down-regulated in hybrid stigmas, potentially affecting pollen germination and pollen tube growth. Cross-pollinated stigma exhibited lower levels of high-energy nutrients (such as amino acids, nucleotides, and tricarboxylic acid cycle metabolites) compared to self-pollinated stigma, which suggests that energy deficiency is a contributing factor to the crossing barrier. Additionally, cross-pollination significantly impacted KEGG pathways such as nucleotide metabolism, purine metabolism, and vitamin B6 metabolism, with most metabolites in these pathways being down-regulated. These findings provide new insights into the metabolic basis of cross-incompatibility between tree and herbaceous peonies, offering a foundation for overcoming hybridization barriers in peony breeding.
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spelling doaj-art-ee6bf37e3a804b87a30e5c8e6d1a887c2025-08-20T02:31:03ZengMDPI AGPlants2223-77472025-05-01149138110.3390/plants14091381Non-Target Metabolomics Reveals Changes in Metabolite Profiles in Distant Hybrid Incompatibility Between <i>Paeonia</i> sect. <i>Moutan </i>and<i> P. lactiflora</i>Wenqing Jia0Yingyue Yu1Zhaorong Mi2Yan Zhang3Guodong Zhao4Yingzi Guo5Zheng Wang6Erqiang Wang7Songlin He8School of Horticulture and Landscape Architecture, Henan Institute of Science and Technology, Xinxiang 453003, ChinaSchool of Horticulture and Landscape Architecture, Henan Institute of Science and Technology, Xinxiang 453003, ChinaSchool of Horticulture and Landscape Architecture, Henan Institute of Science and Technology, Xinxiang 453003, ChinaSchool of Horticulture and Landscape Architecture, Henan Institute of Science and Technology, Xinxiang 453003, ChinaLuoyang National Peony Gene Bank, Luoyang 471011, ChinaCollege of Landscape Architecture and Art, Henan Agricultural University, Zhengzhou 450002, ChinaCollege of Landscape Architecture and Art, Henan Agricultural University, Zhengzhou 450002, ChinaLuoyang Academy of Agricultural and Forestry Sciences, Luoyang 471099, ChinaCollege of Landscape Architecture and Art, Henan Agricultural University, Zhengzhou 450002, ChinaPeonies are globally renowned ornamental plants, and distant hybridization is a key method for breeding new varieties, though it often faces cross-incompatibility challenges. The metabolic mechanisms underlying the crossing barrier between tree peony (<i>Paeonia</i> sect<i>. Moutan</i>) and herbaceous peony (<i>P. lactiflora</i>) remain unclear. To identify key metabolites involved in cross-incompatibility, we performed a cross between <i>P. ostii</i> ‘Fengdanbai’ (female parent) and <i>P. lactiflora</i> ‘Red Sara’ (male parent) and analyzed metabolites in the stigma 12 h after pollination using UPLC-MS. We identified 1242 differential metabolites, with 433 up-regulated and 809 down-regulated, including sugars, nucleotides, amino acids, lipids, organic acids, benzenoids, flavonoids, and alkaloids. Most differential metabolites were down-regulated in hybrid stigmas, potentially affecting pollen germination and pollen tube growth. Cross-pollinated stigma exhibited lower levels of high-energy nutrients (such as amino acids, nucleotides, and tricarboxylic acid cycle metabolites) compared to self-pollinated stigma, which suggests that energy deficiency is a contributing factor to the crossing barrier. Additionally, cross-pollination significantly impacted KEGG pathways such as nucleotide metabolism, purine metabolism, and vitamin B6 metabolism, with most metabolites in these pathways being down-regulated. These findings provide new insights into the metabolic basis of cross-incompatibility between tree and herbaceous peonies, offering a foundation for overcoming hybridization barriers in peony breeding.https://www.mdpi.com/2223-7747/14/9/1381stigma metabolitenucleotide metabolismpurine metabolismnucleotide sugar metabolismmetabolite analysis
spellingShingle Wenqing Jia
Yingyue Yu
Zhaorong Mi
Yan Zhang
Guodong Zhao
Yingzi Guo
Zheng Wang
Erqiang Wang
Songlin He
Non-Target Metabolomics Reveals Changes in Metabolite Profiles in Distant Hybrid Incompatibility Between <i>Paeonia</i> sect. <i>Moutan </i>and<i> P. lactiflora</i>
Plants
stigma metabolite
nucleotide metabolism
purine metabolism
nucleotide sugar metabolism
metabolite analysis
title Non-Target Metabolomics Reveals Changes in Metabolite Profiles in Distant Hybrid Incompatibility Between <i>Paeonia</i> sect. <i>Moutan </i>and<i> P. lactiflora</i>
title_full Non-Target Metabolomics Reveals Changes in Metabolite Profiles in Distant Hybrid Incompatibility Between <i>Paeonia</i> sect. <i>Moutan </i>and<i> P. lactiflora</i>
title_fullStr Non-Target Metabolomics Reveals Changes in Metabolite Profiles in Distant Hybrid Incompatibility Between <i>Paeonia</i> sect. <i>Moutan </i>and<i> P. lactiflora</i>
title_full_unstemmed Non-Target Metabolomics Reveals Changes in Metabolite Profiles in Distant Hybrid Incompatibility Between <i>Paeonia</i> sect. <i>Moutan </i>and<i> P. lactiflora</i>
title_short Non-Target Metabolomics Reveals Changes in Metabolite Profiles in Distant Hybrid Incompatibility Between <i>Paeonia</i> sect. <i>Moutan </i>and<i> P. lactiflora</i>
title_sort non target metabolomics reveals changes in metabolite profiles in distant hybrid incompatibility between i paeonia i sect i moutan i and i p lactiflora i
topic stigma metabolite
nucleotide metabolism
purine metabolism
nucleotide sugar metabolism
metabolite analysis
url https://www.mdpi.com/2223-7747/14/9/1381
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