The pangenome enhances the understanding of the genetic diversity of papaya

Abstract

Papaya (Carica papaya L.) is a nutritionally and medicinally important tropical fruit crop, yet its genetic improvement has been limited by insufficient genomic resources. In this study, we constructed chromosome-level genomes for three key varieties (Zhufeng, T3, and T5) and integrated them with three existing assemblies to build a comprehensive pangenome, including graph-based, linear, and syntelog-based representations. The syntelog-based pangenome revealed 24 453 syntelog groups (SGs). Leveraging resequencing data from 222 accessions aligned to the graph-based pangenome, we identified 26 173 structural variations (SVs), including a functionally relevant 94-bp deletion in the RETARDED ROOT GROWTH (RRG) gene in the T3 genome. This deletion affects the expression of the RRG, resulting in a reduction in its expression level in T3. Further phenotypic analysis showed that RRG can influence papaya root length by promoting the proliferation of root meristem cells and inhibiting cell elongation. Additionally, the linear pangenome uncovered 5273 translocations and 1440 inversions, significantly expanding the known SV repertoire in papaya. This study provides a critical genomic resource for deciphering domestication-related traits and accelerating marker-assisted breeding, ultimately advancing the genetic improvement of papaya.

Acknowledgements

This work was supported by the General Program of the National Natural Science Foundation of China (grant 32572974), the ‘Young and Middle-aged Academic Leaders’ training fund project of Guangdong Academy of Agricultural Sciences (grant R2023PY-JX005), the Cultivation Project of Fruit Tree Research Institute, Guangdong Academy of Agricultural Sciences (grant 23107), and the Guangdong Province Rural Revitalization Strategy Special Fund-Seed Industry Revitalization Action Project (grant 2024-NPY-00-028), and the Guangzhou Municipal Science and Technology Project (grant 2024A04J6951).

Authors contributions

M.Y. and Y.W. planned and designed the research. M.Y. and C.Z. performed most of the experiments and bioinformatics analyses. X.K., R.K., X.W., C.L., Z.X., and H.H. assisted with data analysis, sample collection, and extraction of total RNA or DNA. M.Y. and Y.W. wrote the manuscript. All authors contributed to the article and approved the submitted version.

Data availability

All sequencing data generated in this study were deposited at the National Center for Biotechnology Information (NCBl) under BioProject ID PRJNA1154410. The sequencing data of Zihui were downloaded from the NCBI (BioProject: PRJNA968045). The whole-genome resequencing was downloaded from the National Centre for Biotechnology Information (NCBI) under BioProject ID PRJNA970517.

Conflicts 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 material

Supplementary material is available at Horticulture Research online.

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