Genomic and pangenomic analyses provide insights into the population history and genomic diversification of bottle gourd

Authors: ZHAO, XUEBO - Boyce Thompson Institute; YU, JINGYIN - Boyce Thompson Institute; Chanda, Bidisha; ZHOA, JIANTAO - Boyce Thompson Institute; WU, SHAN - Boyce Thompson Institute; ZHENG, YI - Boyce Thompson Institute; SUN, HONGHE - (NCE, CECR)networks Of Centres Of Exellence Of Canada, Centres Of Excellence For Commercilization A; Levi, Amnon; Ling, Kai-Shu; FEI, ZHANGJUN - Boyce Thompson Institute

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/27/2024
Publication Date: 5/9/2024
Citation: Zhao, X., Yu, J., Chanda, B., Zhoa, J., Wu, S., Zheng, Y., Sun, H., Levi, A., Ling, K., Fei, Z. 2024. Genomic and pangenomic analyses provide insights into the population history and genomic diversification of bottle gourd. New Phytologist. 242:2285–2300. https://doi.org/10.1111/nph.19673.
DOI: https://doi.org/10.1111/nph.19673

Interpretive Summary: Bottle gourd in the Cucurbitaceae family is one of the most ancient domesticated crops widely grown in tropical and subtropical regions worldwide. Its fruits have diverse uses for food, medicines, ornaments, containers and musical instruments. Its seedlings could serve as rootstocks for other cucurbit crops such as watermelon, mainly to improve disease resistance and stress tolerance. However, the demographic history and genomic diversity of large-scale bottle gourd populations have yet to be comprehensively investigated. In this study, USDA scientists in Charleston, SC collaborated with Boyce Thompson Institute researchers to construct a high-resolution genome variation map of bottle gourd from genome resequencing data of 197 worldwide representative accessions, which empowers the identification of genomic regions associated with zucchini yellow mosaic virus resistance. Our high-density genome variation map facilitates the characterization of the genetic diversity captured in the bottle gourd germplasm and the constructed pangenome provides a useful resource for future functional studies and breeding of bottle gourd.

Technical Abstract: Bottle gourd [Lagenaria siceraria (Mol.) Strandl.] is an economically important vegetable crop and one of the earliest domesticated crops. However, the population history and genomic diversification of bottle gourd has not been extensively studied. We generate a comprehensive bottle gourd genome variation map from genome sequences of 197 worldwide representative accessions, which enables a genome-wide association study for identifying genomic loci associated with resistance to zucchini yellow mosaic virus, and construct a bottle gourd pangenome that harbors 1,534 protein-coding genes absent in the reference genome. Demographic analyses uncover that bottle gourd originated in Southern Africa approximately 12,500 years ago, and subsequently radiated to the New World via the Atlantic drift and to Eurasia through the efforts of early farmers in the initial Holocene. The identified highly differentiated genomic regions among different bottle gourd populations harbor many genes contributing to their local adaptations such as those related to disease resistance and stress tolerance. Presence/absence variation analysis of genes in the pangenome reveals numerous genes including those involved in abiotic/biotic stress responses that have been under selection during the worldwide expansion of bottle gourds. The bottle gourd variation map and pangenome provide valuable resources for future functional studies and genomics-assisted breeding.