During plant evolution, there is genetic communication between organelle and nuclear genomes. A comparative analysis was performed on the organelle and nuclear genomes of the watermelon and melon. In the watermelon, chloroplast-derived sequences accounted for 7.6% of the total length of the mitochondrial genome. In the melon, chloroplast-derived sequences accounted for approximately 2.73% of the total mitochondrial genome. In watermelon and melon, the chloroplast-derived small-fragment sequences are either a subset of large-fragment sequences or appeared multiple times in the mitochondrial genome, indicating that these fragments may have undergone multiple independent migration integrations or emerged in the mitochondrial genome after migration, replication, and reorganization. There was no evidence of migration from the mitochondria to chloroplast genome. A sequence with a total length of about 73 kb (47%) in the watermelon chloroplast genome was homologous to a sequence of about 313 kb in the nuclear genome. About 33% of sequences in the watermelon mitochondrial genome was homologous with a 260 kb sequence in the nuclear genome. A sequence with a total length of about 38 kb (25%) in the melon chloroplast genome was homologous with 461 sequences in the nuclear genome, with a total length of about 301 kb. A 3.4 Mb sequence in the nuclear genome was homologous with a melon mitochondrial sequence. These results indicate that, during the evolution of watermelon and melon, a large amount of genetic material was exchanged between the nuclear genome and the two organelle genomes in the cytoplasm.

The plant compact and dwarf growth habit is an important agronomic trait when breeding watermelon ( Citrullus lanatus ) cultivars because of their reduced vine length, high-density planting, and better land utilization; however, the genetic basis of the dwarf growth habit is not well-known. In this study, the plant population of six generations, P1, P2, F1, F2, BC1P1, and BC1P2, were studied. A genetic segregation analysis demonstrated that dwarfism is mainly controlled by a single recessive Cldw gene. Furthermore, whole-genome sequencing of two distinct watermelon cultivars, W1-1 (P1) and 812 (P2), was performed and preliminarily mapped through a bulked segregant analysis of F2 individuals that revealed the Cldw gene locus on chromosome 9. Two candidate genes, Cla015407 and Cla015408 , were discovered at the delimited region of 43.2 kb by fine mapping, and gene annotation exposed that the Cla015407 gene encodes gibberellic acid 3β-hydroxylase protein. In addition, a comparative analysis of gene sequence and cultivars sequences across the reference genome of watermelon revealed the splice site mutation in the intron region of the Cldw gene in dwarf-type cultivar 812. The quantitative real-time polymerase chain reaction exhibited a significantly higher expression of the Cla015407 gene in cultivar W1-1 compared with 812. There was no significant difference in the vine length of both cultivars after gibberellic acid treatment. In brief, our fine mapping demonstrated that Cla015407 is a candidate gene controlling dwarfism of watermelon plants.

Phytoene synthase (PSY) plays an essential role in carotenoid biosynthesis. In this study, three ClPSY genes were identified through the watermelon genome, and their full-length cDNA sequences were cloned. The deduced proteins of the three ClPSY genes were ranged from 355 to 421 amino acid residues. Phylogenetic analysis suggested that the ClPSYs are highly conserved with bottle gourd compared to other cucurbit crops PSY proteins. Variation in ClPSY1 expression in watermelon with different flesh colors was observed; ClPSY1 was most highly expressed in fruit flesh and associated with the flesh color formation. ClPSY1 expression was much lower in the white-fleshed variety than the colored fruits. Gene expression analysis of ClPSY genes in root, stem, leaf, flower, ovary and flesh of watermelon plants showed that the levels of ClPSY2 transcripts found in leaves was higher than other tissues; ClPSY3 was dominantly expressed in roots. Functional complementation assays of the three ClPSY genes suggested that all of them could encode functional enzymes to synthesize the phytoene from Geranylgeranyl Pyrophosphate (GGPP). Some of the homologous genes clustered together in the phylogenetic tree and located in the synteny chromosome region seemed to have similar expression profiles among different cucurbit crops. The findings provide a foundation for watermelon flesh color breeding with regard to carotenoid synthesis and also provide an insight for the further research of watermelon flesh color formation.