Scientia Agricultura Sinica ›› 2025, Vol. 58 ›› Issue (23): 5013-5030.doi: 10.3864/j.issn.0578-1752.2025.23.016

• HYBRIDIZATION BREEDING AND GERMPLASM INNOVATION IN PAEONIA • Previous Articles     Next Articles

Integrated Transcriptomic and Metabolomic Analysis of Pre- Fertilization Barriers in Distant Hybridization of Paeonia ostii × P. ludlowii

JIA WenQing1(), HE YaLin1, DUAN HuiLin1, YU YingYue1, WANG Zheng2, ZHAO GuoDong3, GUO YingZi2, WANG ErQiang4, MU JinYan1, ZHANG Yan1, WANG YanLi1, HE SongLin2,*()   

  1. 1 College of Horticulture and Landscape Architecture, Henan Institute of Science and Technology, Xinxiang 453003, Henan
    2 College of Landscape Architecture, Henan Agricultural University, Zhengzhou 450002
    3 National Peony Gene Bank, Luoyang 471009, Henan
    4 Luoyang Academy of Agricultural and Forestry Sciences, Luoyang 471023, Henan
  • Received:2025-06-05 Accepted:2025-07-22 Online:2025-12-01 Published:2025-12-09
  • Contact: HE SongLin

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Abstract:

【Objective】 Paeonia ludlowii, an endemic wild tree peony species in Tibet, possesses superior characteristics including tall plant stature, pure yellow flowers, and scarlet autumn foliage. However, the distant hybridization barrier with cultivated peonies has prevented the effective utilization of its superior genes. This study aims to elucidate the molecular mechanisms underlying the stigma response to distant hybridization after pollination, clarify the regulatory network of pollen-stigma recognition barriers, and provide a theoretical basis for overcoming pre-fertilization barriers in distant hybridization of peonies. 【Method】 Hybridization experiments were conducted using the cultivated variety Paeonia ostii Fengdan as the maternal parent and Paeonia ludlowii as the paternal parent. Three experimental groups were established: self-pollination of Fengdan (CK), ‘Fengdan’ × P. ludlowii (DH), and Fengdan × P. ludlowii with stigmas pretreated with 2 mg·L-1 KCl (KH). Fluorescence microscopy was used to dynamically observe pollen germination and pollen tube growth from 0 to 4 h after pollination. Stigma transcriptome analysis (RNA-seq) was performed using the Illumina high-throughput sequencing platform, combined with UPLC-QTOF-MS-based untargeted metabolomics to systematically identify differentially expressed genes (DEGs) and differentially accumulated metabolites (DAMs). Key metabolic pathways were further analyzed through KEGG and GO enrichment. 【Result】 Phenotypic observations revealed that in the CK group, a large number of pollen germination occurred at 2 h after pollination, polar growth of pollen tubes was observed at 4 h. Only a few pollen grains germinated 4 h after pollination in the DH group, while the KH group exhibited significantly higher pollen germination rates than the DH group. During pollen-pistil interactions, high concentrations of O2- and H2O2 were found to inhibit pollen germination. KEGG enrichment indicated that DEGs and DAMs were primarily involved in sugar metabolism, cell wall organization or biogenesis, and flavonoid biosynthesis. In interspecific hybridization of tree peony, the widespread downregulation of carbohydrates results in insufficient energy supply, while the reduction in flavonoid compounds disrupts reactive oxygen species (ROS) homeostasis these constitute the key inhibitory factors for pollen germination. 【Conclusion】 Reactive oxygen species (ROS) dynamic imbalance mediated by Rboh, insufficient energy supply induced by glucose metabolism disorder, abnormal flavonoid metabolism, and disrupted hormone signal transduction collectively impede pollen germination in the distant hybridization of Paeonia ludlowii, ultimately resulting in the formation of prezygotic barriers.

Key words: tree peony, distant hybridization, prezygotic barriers, aniline blue staining, extension of pollen tube

Fig. 1

Pollen germination at 2 and 4 hours after pollination A: At 2 h after pollination in CK; B: At 2 h after pollination in KH; C: At 2 h after pollination in DH; D: At 4 h after pollination in CK; E: At 4 h after pollination in KH; F: At 4 h after pollination in DH. pg: Pollen grain; pt: Pollen tube. CK: Refers to the self-pollination of P. ostii. KH: Refers to the cross between P. ostii (with KCl-treated stigma) and P. ludlowii. DH: Refers to the conventional cross between P. ostii and P. ludlowii. The same as below"

Fig. 2

Changes in H2O2, O2-, and ·OH content in the stigmas of CK, DH, and KH"

Fig. 3

Venn diagram of differentially expressed genes"

Fig. 4

OPLS-DA statistical analysis plot of metabolomic samples"

Fig. 5

Comprehensive functional/pathway clustering analysis plot of differential metabolites in stigmas A: DH vs CK; B: DH vs KH; C: KH vs CK. Each node in the figure represents a differential metabolite annotated through the KEGG pathway. The diameter of the circle is directly proportional to the difference multiple (FC value) of metabolites. Red indicates significant upregulation of metabolites (log2FC>0), dark blue indicates significant downregulation of metabolites (log2FC<0), and light blue indicates classification information of metabolites"

Fig. 6

KEGG enrichment differential metabolite pathways"

Fig. 7

The effect of distant hybridization on the metabolic pathway of stigma The blue indicates differential metabolites, and the solid and dashed lines between the arrows indicate direct or indirect responses, respectively"

Fig. 8

GO enrichment of differentially expressed genes"

Fig. 9

KEGG enrichment of differentially expressed genes"

Fig. 10

Combined transcriptome and proteome analysis in CK, DH, and KH A: DH vs CK; B: DH vs KH; C: KH vs CK. The horizontal axis represents the IDs of differentially expressed genes, and the vertical axis represents differentially expressed metabolites"

Fig. 11

Validation of ROS-related gene expression levels by qRT-PCR (A) and RNA-Seq expression patterns (B)"

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