Genome of ‘Charleston Gray’, the principal American watermelon cultivar, and genetic characterization of 1,365 accessions in the U.S. National Plant Germplasm System watermelon collection

Authors: WU, SHAN - Boyce Thompson Institute; WANG, XIN - Boyce Thompson Institute; REDDY, UMESH - West Virginia State University; SUN, HONGHE - Boyce Thompson Institute; BAO, KAN - Boyce Thompson Institute; PATEL, TAKSHAY - North Carolina State University; ORITZ, CARLOS - West Virginia State University; ABBURI, LAKSHMI - West Virginia State University; NIMMAKAYALA, PADMA - West Virginia State University; Branham, Sandra; Wechter, William - Pat; Massey, Laura; Ling, Kai-Shu; Kousik, Chandrasekar - Shaker; HAMMAR, SUE - Michigan State University; TADMOR, YAAKOV - Israel Agricultural Research Organization (ARO); PORTNOY, VITALY - Israel Agricultural Research Organization (ARO); GUR, AMIT - Israel Agricultural Research Organization (ARO); KATZIR, NURIT - Israel Agricultural Research Organization (ARO); GUNER, NIHAT - Sakata Seed America, Inc; DAVIS, ANGELA - Sakata Seed America, Inc; HERNANDEZ, ALVARO - University Of Illinois; WRIGHT, CHRIS - University Of Illinois; MCGREGOR, CECILIA - University Of Georgia; Jarret, Robert - Bob; XU, YONG - National Engineering Center For Vegetables; ZHANG, XINGPING - Syngenta; WEHNER, TODD - North Carolina State University; GRUMET, REBECCA - Michigan State University; Levi, Amnon; FEI, ZHANGJUN - Boyce Thompson Institute

Submitted to: Plant Biotechnology Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/19/2019
Publication Date: 4/25/2019
Citation: Wu, S., Wang, X., Reddy, U., Sun, H., Bao, K., Patel, T., Oritz, C., Abburi, L., Nimmakayala, P., Branham, S., Wechter, W.P., Massey, L.M., Ling, K., Kousik, C.S., Hammar, S.A., Tadmor, Y., Portnoy, V., Gur, A., Katzir, N., Guner, N., Davis, A., Hernandez, A.G., Wright, C.L., McGregor, C., Jarret, R.L., Xu, Y., Zhang, X., Wehner, T.C., Grumet, R., Levi, A., Fei, Z. 2019. Genome of ‘Charleston Gray’, the principal American watermelon cultivar, and genetic characterization of 1,365 accessions in the U.S. National Plant Germplasm System watermelon collection. Plant Biotechnology Journal. https://doi.org/10.1111/pbi.13136.
DOI: https://doi.org/10.1111/pbi.13136

Interpretive Summary: Watermelon is an important vegetable fruit crop in the USA and throughout the world. Years of selection for desirable fruit quality traits has narrowed the genetic base in modern watermelon cultivars and diminished their ability to combat a wide range of diseases and pests. In this study, ARS scientists collaborated with scientists at several universities on developing a high-quality genome sequence of the principle American watermelon cultivar ‘Charleston Gray’. In addition, the genomes of 1,365 watermelon plant introduction (PI) lines collected throughout the world and maintained by the USDA, National Plant Germplasm System (NPGS) were sequenced. The genomic analyses here elucidated the genetic diversity among watermelon PIs and facilitated the identification of gene loci associated with important fruit quality and disease resistance traits. The genome sequencing data in this study provide a valuable resource for genetic research and discovery of genes and for breeding and improvement of watermelon.

Technical Abstract: Watermelon (Citrullus lanatus) is a popular vegetable fruit crop. Years of selection for desirable fruit quality traits has resulted in a narrow genetic base in modern dessert watermelon cultivars. Development of novel genomic and genetic resources offers great potential to expand genetic diversity and improve important traits in watermelon. Here we report a high-quality genome sequence of watermelon cultivar ‘Charleston Gray’, a principal American dessert watermelon that has been used in numerous breeding programs to develop improved cultivars. Comparative analyses between genomes of ‘Charleston Gray’ and ‘97103’, an East Asian watermelon cultivar, revealed genomic variants that may underlie phenotypic differences between the two cultivars. We then genotyped 1,365 watermelon plant introduction (PI) lines maintained at the United States National Plant Germplasm System using genotyping-by-sequencing (GBS). These PI lines are collected throughout the world and belong to three Citrullus species, C. lanatus, C. mucosospermus and C. amarus. Approximately 25,000 high-quality single-nucleotide polymorphism (SNP) markers were derived from the GBS data using the high-quality ‘Charleston Gray’ genome as the reference. Comprehensive population genomic analyses using these SNP markers have allowed assessment of genetic diversity within different species and geographic groups, and provided insights into their phylogenetic relationships and the domestication and distribution history of watermelons. The SNP markers also enabled identification of genomic regions associated with important fruit quality traits and disease resistances through genome-wide association studies (GWAS). The high-quality ‘Charleston Gray’ genome and genotyping data of this large collection of watermelon accessions provide a valuable resource for facilitating watermelon research, breeding and improvement.