High-quality genome assembly and genetic mapping reveal a gene regulating flesh color in watermelon (Citrullus lanatus)

Abstract

The unique color and type characteristics of watermelon fruits are regulated by many molecular mechanisms. However, it still needs to be combined with more abundant genetic data to fine-tune the positioning. We assembled genomes of two Korean inbred watermelon lines (cv. 242-1 and 159-1) with unique color and fruit-type characteristics and identified 23,921 and 24,451 protein-coding genes in the two genomes, respectively. To obtain more precise results for further study, we resequenced one individual of each parental line and an F2 population composed of 87 individuals. This identified 1,539 single-nucleotide polymorphisms (SNPs) and 80 InDel markers that provided a high-density genetic linkage map with a total length of 3,036.9 cM. Quantitative trait locus mapping identified 15 QTLs for watermelon fruit quality-related traits, including β-carotene and lycopene content in fruit flesh, fruit shape index, skin thickness, flesh color, and rind color. By investigating the mapping intervals, we identified 33 candidate genes containing variants in the coding sequence. Among them, Cla97C01G008760 was annotated as a phytoene synthase with a single-nucleotide variant (A → G) in the first exon at 9,539,129 bp of chromosome 1 that resulted in the conversion of a lysine to glutamic acid, indicating that this gene might regulate flesh color changes at the protein level. These findings not only prove the importance of a phytoene synthase gene in pigmentation but also explain an important reason for the color change of watermelon flesh.

Development of a Gene-Based Marker Set for Orange-Colored Watermelon Flesh with a High β-Carotene Content

“…2. The non-synonymous SNP (A>G) in ClPSY1 was also detected by Nie et al [ 4 ]. In higher plants, RCCR is essential for chlorophyll degradation during leaf senescence and fruit ripening.…”

“…Song et al [ 19 ] conducted a comparative analysis of the whole-genome sequence of 24 watermelon inbred lines (six orange-, nine red-, and nine yellow-fleshed) and reported that the non-synonymous SNP (A>G) in the first exon of ClPSY1 , which is the same SNP discovered in our study, exhibited an 87.5% matching rate to flesh color; the SNP (G) for orange color was present in all six orange-fleshed lines, two red-, and one yellow-fleshed lines. In addition, by performing a high-resolution genetic mapping of an F 2 population derived from red- and orange-β-fleshed inbreds, Nie et al [ 4 ] identified two carotenoid biosynthesis genes in the QTL intervals: ClPSY1 on Chr. 1 and RCCR encoding red chlorophyll catabolite reductase (RCCR) on Chr.…”

“…Fruit color is an essential breeding trait that significantly affects consumer preference and the market value of the fruit in relation to visual appeal and the associated health benefits. Watermelon flesh ranges in color, including white, light yellow, canary-yellow, salmon yellow, orange, pink, red (scarlet or coral), and green [ 3 , 4 ], and the color is primarily attributed to the composition of carotenoids that accumulate in the chromoplasts [ 5 ]. For instance, the predominant red flesh of cultivated watermelons results from the accumulation of all-trans-lycopene, while the orange flesh primarily arises from the accumulation of either ζ-carotene and β-carotene or prolycopene (7,9,7’,9’-tetra-cis-lycopene) [ 3 , 4 ], and the canary-yellow flesh results from the synthesis of xanthophyll, including neoxanthin, violaxanthin, and zeaxanthin, from carotene via the carotenoid biosynthesis pathway [ 4 , 6 , 7 ].…”

From Sequencing to Genome Editing in Cucurbitaceae: Application of Modern Genomic Techniques to Enhance Plant Traits

“…Another important species in relation to a high cultivation rate worldwide is watermelon (Citrullus lanatus). The referenced genome of 242-1 isolate was published in 2023 [88], where the authors utilised Oxford Nanopore MinION and Illumina HiSeq 2500 systems and described the genome size of 361.7 Mb with 22.0x data coverage and 23,921 proteincoding genes. Due to the existence of a huge number of watermelon varieties, the genome sequencing of other subspecies and species has also been attempted several times by other researchers.…”

“…Due to the existence of a huge number of watermelon varieties, the genome sequencing of other subspecies and species has also been attempted several times by other researchers. DNA sequences for the Korean cultivar 159-1 [88], as well as for Charleston Gray [89], a dessert watermelon cultivar, have also been obtained. Moreover, in 2013 the genome of C. lanatus subsp.…”