Genomic insights into the domestication and genetic basis of yield in papaya

Abstract

Papaya (Carica papaya L.) is an important tropical and subtropical fruit crop, and understanding its genome is essential for breeding. In this study, we assembled a high-quality genome of 344.17 Mb for the newly cultivated papaya ‘Zihui’, which contains 22 250 protein-coding genes. By integrating 201 resequenced papaya genomes, we identified four distinct papaya groups and a 34 Mb genomic region with strong domestication selection signals. Within these regions, two key genes associated with papaya yield were discovered: Cp_zihui06549, encoding a leucine-rich receptor-like protein kinase, and Cp_zihui06768, encoding the accumulation of photosystem one 1 (APO1) protein. Heterologous expression of Cp_zihui06549 in tomato confirmed that the total number of fruits in transgenic lines more than doubled compared to wild-type plants, resulting in a significant yield increase. Furthermore, we constructed a pan-genome of papaya and obtained a 77.41 Mb nonreference sequence containing 1543 genes. Within this pan-genome, 2483 variable genes, we detected, including four genes annotated as the ‘terpene synthase activity’ Gene Ontology term, which were lost in cultivars during domestication. Finally, gene retention analyses were performed using gene presence and absence variation data and differentially expressed genes across various tissues and organs. This study provides valuable insights into the genes and loci associated with phenotypes and domestication processes, laying a solid foundation for future papaya breeding efforts.

Acknowledgements

This work was supported by the ‘Young and Middle-aged Academic Leaders’ Training Fund Project of Guangdong Academy of Agricultural Sciences (Grant no. R2023PY-JX005), the Guangdong Basic and Applied Basic Research Foundation (Grant no. 2022A1515010697), the Cultivation Project of Fruit Tree Research Institute, Guangdong Academy of Agricultural Sciences (Grant no. 23107), and the Guangzhou Science and Technology Planning Project (Grant no. 2023B03J1369).

Author Contributions

M.Y. and Y.W. planned and designed the research. M.Y. and X.K. performed most of the experiments and all bioinformatics analyses. C.Z., R.K., X.W., C.L., H.H., and Z.X. helped collect the samples and extracted total RNAs or DNAs. M.Y., X.K., and Y.W. wrote the manuscript. All authors contributed to the article and approved the submitted version.

Data Availability

The Hi-C, HiFi, RNA-Seq and genome assembly data were deposited in the National Centre for Biotechnology Information (NCBI) under BioProject ID PRJNA968045. The whole-genome resequencing was deposited in the National Centre for Biotechnology Information (NCBI) under BioProject ID PRJNA970517. The nonreference contigs of Carica papaya pangenome and annotation are available at Figshare database.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Supplementary data

Supplementary data is available at Horticulture Research online.

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