Bee-mediated pollination enhances fruit set and seed yield in Paeonia ostii ‘Fengdan’: insights into physiological and molecular mechanisms

Abstract

Bee pollination enhances crop productivity and food security globally. However, its impact on pollen performance within pistil tissues and the underlying regulatory mechanisms remain unclear. In this study, artificial self-pollination yielded the highest pollen deposition on stigmas (119879.33 ± 43037.92 grains), followed by bee pollination (95464.60 ± 3985.01 grains). Conversely, bee pollination achieved the highest seed set rate (55.21% ± 1.84%), significantly exceeding the artificial self-pollination rate (7.27% ± 1.87%). A positive correlation was observed between pollen load on the stigmatic pollination band and seed set rate. Bee pollination delivers ample high-quality pollen to the stigmas of oil tree peony, enhancing seed production. Moreover, a trend high correlation was observed between pollen deposition on the stigmatic pollination band and seed set rate. Fluorescence microscopy and endogenous hormone analyses revealed that bee pollination stimulated a rapid increase in ZR, IAA, and GA₃ levels in the pistil tissues, promoting pollen germination and pollen tube growth. Transcriptome analysis identified PoFAR2, a key candidate gene involved in pollen development, in the pistil tissues after bee pollination. This gene exhibits high homology with genes found in other crops. The PoFAR2 gene localizes to the cell membrane, validating earlier predictions, and exhibits strong transcriptional activity. Silencing PoFAR2 disrupts pollen development in Paeonia ostii ‘Fengdan’ manifesting as structural defects in pollen walls and significantly reduces pollen viability. In conclusion, bees enhance fertilization in oil tree peony by delivering high-quality pollen that promotes germination and pollen tube growth. Crucially, we identified PoFAR2, a membrane-localized key gene regulating pollen development. This study establishes a crucial foundation for deciphering the molecular mechanisms by which bee pollination and phytohormone signaling mediate pollen development.

Acknowledgements

We sincerely thank our team leader, Dr. Xiao-Gai Hou, for her outstanding contributions, support, and guidance throughout this work. This research was funded by grants from Central Plains Scholars Fund of Henan Province (212101510003), the Henan Province Central Guidance for Local Science and Technology Development Fund Project (Z20231811104), and the Zhongyuan Scholar Workstation Funded Project (234400510018). We also extend our gratitude to graduate students Rui-Ya Li and Ding-Ding Zuo from Henan University of Science and Technology for their valuable assistance in the experiments.

Author contributions

K.-Y.Z. contributed to the material preparation, phenotype investigation, methodology, data curation, writing, reviewing, and editing. Y.-Y.L. conducted experiments and analyzed data. J.-Y.B. and X.-N.H. contributed to experiments and data investigation. L.-F.C. performed experiments and analyzed data. L.-L.G., D.-L.G. and C.-W.S. performed editing. C.-L.H. contributed to conceptualization, experimental design, manuscript review, and editing. X.-G.H. led conceptualization, experimental design, supervision and funding acquisition. All authors critically reviewed the manuscript and approved the final version for publication.

Data availability

The data underlying this article are available in the manuscript and in its online supplementary material.

Conflict of interest statement

The authors declare that no competing interests exist.

Supplementary Data

Supplementary data is available at Horticulture Research online.

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