Genome resequencing reveals the evolutionary history of garlic reproduction traits

Abstract

The propagation of cultivated garlic relies on vegetative cloves, thus flowers become non-essential for reproduction in this species, driving the evolution of reproductive feature-derived traits. To obtain insights into the evolutionary alteration of reproductive traits in the clonally propagated garlic, the evolutionary histories of two main reproduction-related traits, bolting and flower differentiation, were explored by genome analyses using 134 accessions displaying wide diversity in these two traits. Resequencing identified 272.8 million variations in the garlic genome, 198.0 million of which represent novel variants. Population analysis identified five garlic groups that have evolved into two clades. Gene expression, single-cell transcriptome sequencing, and genome-wide trait association analyses have identified numerous candidates that correlate with reproductive transition and flower development, some of which display distinct selection signatures. Selective forces acting on the B-box zinc finger protein-encoding Asa2G00291.1, the global transcription factor group E protein-encoding Asa5G01527.1, and VERNALIZATION INSENSITIVE 3-like Asa3G03399.1 appear to be representative of the evolution of garlic bolting. Plenty of novel genomic variations and trait-related candidates represent valuable resources for biological studies of garlic. Numerous selective signatures from genes associated with the two chosen reproductive traits provide important insights into the evolutionary history of reproduction in this clonally propagated crop.

Acknowledgements

This research was supported by grants from the National Natural Science Foundation of China (31872946, 32172566 to H.W., 32372689 to T.L.), the Scientific Research Foundation of Yangzhou University (5018/137012867 to T.L.), the Shandong Provincial Key Research and Development Program (2023CXPT045 to T.L.), and the China Agriculture Research System of MOF and MARA (CARS-24-01 to H.W.).

Author Contributions

E.S. and Y.W. collected the samples. H.W., J.Z., Z.Y., H.J., Z.Z., and S.G. performed the experiments and data analysis. Xu.Z., J.S., Xi.Z., W.Y. and Q.H. managed the fieldwork and measured traits. T.L. wrote the manuscript. A.S., L.L., and R.K. revised the manuscript. All authors read and approved the final manuscript.

Data availability statement

The reported variation data from whole-genome sequencing have been deposited in the Genome Variation Map (GVM) in the Big Data Center, Beijing Institute of Genomics (BIG), Chinese Academy of Science, under the project accession numbers PRJCA006629 and PRJCA012274. The sequence reads of single-cell RNA sequencing have been deposited in the Genome Sequence Archive in the National Genomics Data Center, China National Center for Bioinformation/Beijing Institute of Genomics, Chinese Academy of Sciences (GSA: CRA009173).

Conflict of interests

The authors declare no competing interests.

Supplementary information

Supplementary data is available at Horticulture Research online.

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