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Characterization of transcriptomic response in ovules derived from inter-subgeneric hybridization in Prunus (Rosaceae) species

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Abstract

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Characterization of hybrid seed failure in Prunus provides insight into conserved or lineage-specific hybrid incompatibility mechanisms in plant species.

Abstract

Postzygotic hybrid incompatibility resulting from a cross between different species involves complex mechanisms occurring at various developmental stages. Embryo arrest, followed by seed abortion, is the first stage of such incompatibility reactions and inhibits hybrid seed development. In Prunus, a rosaceous woody species, some interspecific crosses result in fruit drop during the early stage of fruit development, in which inferior seed development may be accounted for the observed hybrid incompatibility. In this study, we investigated ovule development and the transcriptomes of developing ovules in inter-subgeneric crosses of Prunus. We conducted a cross of Prunus mume (subgenus Prunus), pollinated by P. persica (subgenus Amygdalus), and found that ovule and seed coat degeneration occurs before fruit drop. Transcriptome analysis identified differentially expressed genes enriched in several GO pathways, including organelle development, stimulus response, and signaling. Among these pathways, the organelle-related genes were actively regulated during ovule development, as they showed higher expression in the early stage of interspecific crosses and declined in the later stage, suggesting that the differential regulation of organelle function may induce the degeneration of hybrid ovules. Additionally, genes related to ovule and seed coat development, such as genes encoding AGL-like and auxin response, were differentially regulated in Prunus interspecific crosses. Our results provide histological and molecular information on hybrid seed abortion in Prunus that could be utilized to develop new hybrid crops. Additionally, we compared and discussed transcriptome responses to hybrid seed failure in Prunus and other plant species, which provides insight into conserved or lineage-specific hybrid incompatibility mechanisms in some plant species.

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Availability of data and material

RNA-Seq data obtained from this study have been prepared to deposit in DNA Data Bank of Japan.

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Acknowledgements

We appreciated Drs. Fabrizio Costa and Takashi Akagi for providing valuable comments to the research and for providing financial support (the Japan Society for the Promotion of Science JSPS, Grants-in-Aids for Challenging Exploratory Research No. 17K19265 to Takashi Akagi). This work was also supported by the JSPS Grants-in-Aids for Young Scientists No. 19K15834 to TM.

Funding

This work was supported by the Japan Society for the Promotion of Science JSPS, Grants-in-Aids for Young Scientists No. 19K15834 to TM. This work was also supported by the JSPS, Grants-in-Aids for Challenging Exploratory Research No. 17K19265 to Takashi Akagi, associate professor at Okayama University, Japan.

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Authors

Contributions

TM conceived and designed research. YK and KN conducted experiments. TM analyzed data. TM and AI wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Takuya Morimoto.

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The authors declare that they have no competing interests.

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Communicated by JS Pat Heslop-Harrison.

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Supplementary Information

Below is the link to the electronic supplementary material. Fig. S1 Principal component analysis of transcriptome data. Three biological replicates were analyzed using 1,129 differentially expressed genes. Percentages on axes indicate values explained by each principal component. Fig. S2 Proportion of Prunus persica allele in genes expressed in hybrid tissues. (A) 2 WAP) (B) 4 WAP (C) 5 WAP. WAP: weeks after pollination.

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Morimoto, T., Kitamura, Y., Numaguchi, K. et al. Characterization of transcriptomic response in ovules derived from inter-subgeneric hybridization in Prunus (Rosaceae) species. Plant Reprod 34, 255–266 (2021). https://doi.org/10.1007/s00497-021-00423-2

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