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Upregulation of defense-related gene expressions associated with lethal growth failure in the hybrid seedlings of Japanese flowering cherry

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Abstract

Knowledge of post-zygotic hybrid incompatibility is essential to understand speciation. Although the genes and molecular mechanisms involved in hybrid incompatibility are being elucidated in model plants and crops, the information on woody non-model plants is lacking. In the seedlings of a cross between the most famous ornamental cherry cultivar Cerasus × yedoensis ‘Somei-yoshino’ and its closely related wild species Cerasus itosakura, we discovered a hybrid incompatibility characterized by a phenotype in which growth stops after the expansion of the first true leaves and the seedling eventually dies. To elucidate the molecular mechanisms related to this seedling necrosis, we performed a comprehensive expressed gene analysis on normal-growth and necrotic weak-growth (SW) hybrid seedlings. The RNA-seq results showed over 1500 differentially expressed genes (DEGs) specified for the SW. Numerous genes associated with plant defense response, such as pathogenesis-related genes, and several receptor-like protein kinases were included in SW-specific upregulated DEGs. The Gene Ontology enrichment analysis also showed the significant association of “defense response” in SW seedlings. These upregulated defense-related gene expressions were particularly observed in the hypocotyls. On the contrary, the reduction of photosynthesis-related gene expression and reduction in the gene expressions of cell division and cell cycle at specific parts of seedlings were also observed in the SW. Our results suggest that an upregulated defense-related gene expression suppresses the meristem growth and deviation, resulting in growth failure as an autoimmune response in hybrid cherry seedlings.

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  • 22 July 2022

    Handling editor name correction.

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Acknowledgements

We would like to thank the staff of the University of Tokyo Tanashi Forest for providing the cherry trees for artificial pollination; Dr. S-I. Miyazawa, Senior Researcher of FFPRI, for the advising in qPCR analysis; and Dr. D. Tsugama, Associate Professor of ARC-BRES, the University of Tokyo, for the kind support in the first step of next-generation sequencing analysis.

Funding

This work was supported by the JSPS KAKENHI Grant Number JP18K14489.

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M.T. designed and carried out the experiments and wrote draft manuscripts. C.L. and Y.M. provided critical advice for experiments and analysis. All authors discussed the results and approved the final manuscript.

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Correspondence to Momi Tsuruta.

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The authors declare no competing interests.

Data Archiving Statement

The raw sequence data of RNA-seqs were deposited in the DDBJ Sequence Read Archive (DRA) with accession numbers DRA 011866 and DRA011867.

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Communicated by: C. Dardick

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Tsuruta, M., Lian, C. & Mukai, Y. Upregulation of defense-related gene expressions associated with lethal growth failure in the hybrid seedlings of Japanese flowering cherry. Tree Genetics & Genomes 18, 21 (2022). https://doi.org/10.1007/s11295-022-01552-z

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  • DOI: https://doi.org/10.1007/s11295-022-01552-z

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