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

Abstract

Summary Years of selection for desirable fruit quality traits in dessert watermelon (Citrullus lanatus) has resulted in a narrow genetic base in modern 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, to complement the existing reference genome from ‘97103’, an East Asian cultivar. Comparative analyses between genomes of ‘Charleston Gray’ and ‘97103’ revealed genomic variants that may underlie phenotypic differences between the two cultivars. We then genotyped 1365 watermelon plant introduction (PI) lines maintained at the U.S. National Plant Germplasm System using genotyping‐by‐sequencing (GBS). These PI lines were collected throughout the world and belong to three Citrullus species, C. lanatus, C. mucosospermus and C. amarus. Approximately 25 000 high‐quality single nucleotide polymorphisms (SNPs) were derived from the GBS data using the ‘Charleston Gray’ genome as the reference. Population genomic analyses using these SNPs discovered a close relationship between C. lanatus and C. mucosospermus and identified four major groups in these two species correlated to their geographic locations. Citrullus amarus was found to have a distinct genetic makeup compared to C. lanatus and C. mucosospermus. The SNPs also enabled identification of genomic regions associated with important fruit quality and disease resistance traits through genome‐wide association studies. The high‐quality ‘Charleston Gray’ genome and the genotyping data of this large collection of watermelon accessions provide valuable resources for facilitating watermelon research, breeding and improvement.

Resequencing of 414 cultivated and wild watermelon accessions identifies selection for fruit quality traits

“…Two C. lanatus accessions collected in Sudan (PI 481871 and PI 254622) were placed in the deepest branch of the C. lanatus clade (Fig. 1b), supporting the idea that the primitive watermelons from Sudan and neighboring countries of northeastern Africa may be the closest to the progenitor of the sweet watermelon 2,5,10 . Twelve accessions were clustered into unexpected species groups and were therefore excluded from downstream analyses (Supplementary Table 5).…”

Ethylene‐responsive factor 4 is associated with the desirable rind hardness trait conferring cracking resistance in fresh fruits of watermelon

“…To date, there have been two sequenced reference genomes for the watermelon accessions of 'Charleston Gray' and '97103'. In the present study, we discovered that the American dessert watermelon 'Charleston Gray' (Wu et al, 2019), which has a thick and tough rind, showed the aa genotype in the ClERF4 locus. The Chinese elite line '97103' (Guo et al, 2013) showed the bb type in the ClERF4 locus.…”

Comparative genomics of muskmelon reveals a potential role for retrotransposons in the modification of gene expression

“…Both protein BUSCO benchmark analysis 32 (ver. 3.0) and an InterProScan search 33 indicated that the Harukei-3 genome annotation represents a highly comprehensive dataset of plant protein-coding genes compared with published cucurbit genomes [26][27][28][34][35][36][37][38][39][40] (complete BUSCO = 1372 [95.3%] and InterPro ID count = 5607; Table 2 and Supplementary Data 1). In addition, we observed that our ONT-based gene prediction method gave accurate insights into exon-intron gene structure, whereas other methods (e.g., AUGUSTUS and Braker2) gave incorrect assessments of structure in some genes ( Supplementary Fig.…”

“…1.1) 36 32,205 1333 (92.6%) 37 70 627 841 200 5546 Citrullus lanatus (97103 ver. 2) 27 22,596 1313 (91.2%) 40 87 623 836 199 5498 Citrullus lanatus (Charleston Gray, v2) 37 22,545 1298 (90.1%) 44 98 611 823 196 5418 Benincasa hispida var. B227 28 27,467 1321 (91.7%) 43 76 632 841 197 5505 Cucurbita maxima (Rimu ver.…”