Pangenomics and single-cell transcriptomics uncover the genetic basis of continuous bearing trait in grapevine

Abstract

Grapevine (Vitis vinifera) is economically important for fresh consumption, winemaking, and drying. The circadian systems of flowering and fruit development are crucial for viticulture and yield formation. However, the genetic basis of continuous flowering and bearing has been rarely elucidated. Here, we integrate pan-genomics, comparative genomics, single-cell transcriptomics, and bulk transcriptomics to investigate the continuous flowering and bearing trait (CFB) in the ‘Julian’ grape, which bears fruits at different development stages from flower to mature berries simultaneously. Pan-genomics and comparative genomics discovered 558 unique structural variations (SVs) and eight genes enriched in flowering pathways exclusively in Julian, based on the newly generated haplotype-resolved near telomere-to-telomere (T2T) genome of ‘Julian’ and 15 previously published genomes of grapevine, which bears fruits in the same developmental stage (i.e., seasonal flowering and bearing, SFB). Single-cell transcriptomes of flowering buds for CFB ‘Julian’ and SFB ‘Muscat Hamburg’ detected seven distinct cell types, which provide detailed cell-type-specific gene expression profiles for both cultivars, with differential gene expression (DEG) insights highlighting growth, metabolism, and hormonal regulation pathways in ‘Julian’. Integrating SVs and DEG data, we pinpoint 37 candidate genes potentially associated with CFB, including Auxin/IAA, Cytochrome P450, Vicilin-like antimicrobial peptides (AMP) and respiratory burst oxidase homolog protein B (RBOH) related genes. This study provides insights into the genetic basis of CFB in grapevine, facilitating grapevine breeding with continuous flowering and bearing.

Acknowledgements

We thank members of the Zhou lab at Agricultural Genomics Institute at Shenzhen (AGIS) for discussions and comments on the project. This work was supported by the Key Research and Development Plan of Shandong Province (2024LZGC033 and 2023TZXD015), the National Natural Science Foundation of China (NSFC) (32372646， 32572969), the Qingdao Natural Science Foundation (24-4-4-zrjj-135-jch), the Project of National Key Laboratory for Tropical Crop Breeding (SKLTCBYWF202507), the Science Fund Program for Distinguished Young Scholars of the National Natural Science Foundation of China (Overseas) to Yongfeng Zhou and Hainan Province Key Research and Development Project (ZDYF2024XDNY156).

Author contributions

X.L. and Y.P. conceived and designed the study; Y.C. and X.L. collected the plant materials; Y.L., Y.D., and X.F. assembled and annotated the haplotype-resolved T2T genomes; Y.L., X.W., J.L., T.Z., and Q.L. jointly constructed the pan-genome; Y.L., Y.D., Y.S., X.S., X.N.S.,Y.C.Z.,Y.R., P.W., X.J., and T.H. jointly conducted single-cell transcriptome analysis; M.D., S.Y., and S.F.Y. jointly conducted bulk transcriptomics analysis; Y.L. and Y.D. wrote the manuscript; All authors provided critical feedback and approved the final manuscript.

Data availability

The raw sequencing data, comprising PacBio HiFi long-reads, Illumina Hi-C reads, RNA-seq reads, and snRNA-seq reads, is accessible on NCBI under BioProject ID PRJNA192950 and on the National Genomics Data Center (NGDC) under BioProject ID PRJCA033121. The genome assembly and their annotations have been deposited into in Zenodo:10.5281/zenodo.14263262.

Conflict of interest statement

The authors declare no competing interests.

Supplementary data

Supplementary data is available at Horticulture Research online.

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