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Reduced pollen activity in peanut (Arachis hypogaea L.) by long-term monocropping is linked to flower water deficit

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Abstract

Background and aims

Long-term monocultures seriously compromise crop productivity, which is known as replanting obstacle. Flowers are the most valuable tissue in annual plants and closely associated with pollen production, fertilization and seed set, however, their roles in replanting obstacle are unknown. We here explored how long-term monocropping impacts flowers, and revealed the potential acclimation mechanisms employing by flowers to monocropping.

Methods

Field trial and pot experiments with peanut monocropped and rotated regimes were performed to study the response of peanut flowers to monocropping with physiological, transcriptomic and fungal community analyses.

Results

Long-term monocropping reduced flower formation, pollen viability, pollen germination and tube growth, thereby reducing seed set in peanut. The transcriptome of flowers revealed that genes associated with the anther dehiscence, heat stress response, flavonoid biosynthesis, glutathione metabolism and potassium uptake were enriched by monocropping, which indicated that flowers experienced water deficit and oxidative stress. Inhibition of reactive oxygen species (ROS) synthesis or scavenging excess ROS rescued pollen activity decline under monocropping. By screening flower physiology and soil physicochemical properties, combined with drought and soil aggregate composition mimic experiments, we confirmed that flower water deficit and oxidative stress under monocropping were mediated by the soil structure alterations, especially large macro-aggregates (> 2 mm) reduction.

Conclusion

Long-term monocropping alters soil structures, resulting in a water deficit and ROS accumulation in the flowers, which decreases pollen activity, and a multi-faceted actions including accelerated anther dehiscence, enhanced potassium absorption and better ROS scavenging capacity, are taken by flowers to acclimate to monocropping.

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Data availability

The raw sequence data of flower fungal community and RNA-seq reads were deposited in the Sequence Read Archive (SRA) service of the GenBank database under the accession numbers SUB11087554 and SUB11084279, respectively. All other data supporting the findings of this study are available within the article and its supplement.

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Acknowledgements

We thank Drs. Ying-Chun Du, Cheng-Yu Ma and Hui-Jun Jiang (Nanjing Normal University) for providing assistance for plant sample collection and managing the field. This work was supported by the National Natural Science Foundation of China (grant no. 32101277, 31870478), China Postdoctoral Science Foundation (2020 M681657), a project funded by the Priority Academic Program Development (PAPD) of the Jiangsu Higher Education Institutions of China.

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Authors and Affiliations

Authors

Contributions

W.Z. and C.C.D. conceived the original research plans, designed the experiments and wrote the manuscript. X.L. and W.Z. performed the experiments, created the figures and wrote the manuscript. Y.N.B. and K.S performed the experiments, created the figs. C.C.D. supervised the research and provided laboratory infrastructures. W.Z. and C.C.D. provided funding. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Wei Zhang or Chuan-Chao Dai.

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The authors declare no conflict of interest.

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Responsible Editor: Hans Lambers.

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Luo, X., Bai, YN., Sun, K. et al. Reduced pollen activity in peanut (Arachis hypogaea L.) by long-term monocropping is linked to flower water deficit. Plant Soil 482, 427–450 (2023). https://doi.org/10.1007/s11104-022-05699-5

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  • DOI: https://doi.org/10.1007/s11104-022-05699-5

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