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[Display omitted] • Key volatile organic compounds associated with watermelon aroma were identified. • Key aroma compounds are closely related to the sugar content and flesh color. • Linkage markers and candidate genes of key aroma compounds were obtained. A range of volatile organic compounds played an important role in the formation of watermelon fruit aroma, while due to the low content and difficulty in detection, it is often neglected in watermelon breeding programs, resulting in a decline in fruit flavor. VOCs in the flesh of 194 watermelon accessions and seven cultivars at four developmental stages were determined by SPME-GC–MS. Ten metabolites with significant differences in the natural population and positive accumulation during fruit development are considered to be the key metabolite related to watermelon fruit aroma. And the link between metabolite and, flesh color and sugar content by correlation analysis was established. The results of the genome-wide association study showed that (5E)-6,10-dimethylundeca-5,9-dien-2-one, and 1-(4-methylphenyl) ethanone were colocalized with watermelon flesh color on chromosome 4, which may be regulated by LCYB and CCD. (E)-4-(2,6,6-trimethylcyclohexen-1-yl)but-3-en-2-one is the VOC produced by the cleavage of carotenoids, which has a positive correlation with the sugar content of the fruit, and the candidate gene Cla97C05G092490 on chromosome 5 may interact with PSY to influence the accumulation of this metabolite. In addition, Cla97C02G049790 (enol reductase), Cla97C03G051490 (omega-3 fatty acid desaturase gene), LOX , and ADH may play important roles in the synthesis of fatty acids and their derived VOCs. Taken together, our findings provide molecular insights into the accumulation and natural variation of VOCs in watermelon, and give data support for breeding watermelon cultivars with better flavor. [ABSTRACT FROM AUTHOR]

• Bitterness of watermelon fruit is a dominant trait and controlled by a single gene. • A candidate region of 116.7 kb was obtained by fine mapping with 4 candidate genes. • qRT-PCR indicated Cla011508 might be a candidate gene for watermelon fruit bitterness. • Cla011508 mutation site and qRT-PCR were verified in sixteen germplasms. The bitterness of the fruit seriously affects the taste of watermelon. Therefore, genetic research on bitterness is of great significance to improve watermelon fruit quality. However, there is no research on fine mapping of watermelon fruit bitterness. In the present study, an F 2 population was developed, and two inbred lines, '9904' (bitter flesh) and 'Handel' (non-bitter flesh) as parental materials. Genetic analysis indicated that the bitterness of watermelon was a dominant trait. The initial mapping revealed a 6.16 Mb region on chromosome 1. SNP and CAPS markers were used to narrowed the candidate region to 116.7 kb with four candidate genes (Cla011507, Cla011508, Cla011509 , and Cla011510). Notably, Cla011508 , and Cla011510 have high homology with gene Csa5G156220 and Csa5G157230 , which regulate the bitterness trait in cucumber, and the mutation base at the locus 3,168,882 on chromosome 1 of Cla011508 led to the premature termination of the translation process; at the same time, a non-synonymous mutation caused the amino acid sequence change of Cla011510. The results of qRT-PCR showed that Cla011508 was highly expressed in watermelon flesh of '9904', while no such significant difference was found in Cla011510. Furthermore, the analysis of 16 watermelon accessions showed that 8 bitterness accessions with base C at the locus 3,168,882 had higher gene expression level of Cla011508 , which was significantly different from that of the 8 non-bitter accessions with base T. In conclusion, the bitterness of watermelon fruit may be controlled by Cla011508 , and the important mutation loucs in this gene provide molecular insights for marker-assisted breeding of target trait. [ABSTRACT FROM AUTHOR]

• Combine BSA-Seq and comparative transcriptomic unveiled a candidate gene AUX/IAA related to the flesh firmness trait of watermelon. • AUX/IAA involved in synergistic regulation of various endogenous hormones on flesh firmness in watermelon. • AUX/IAA and ERF1 crosstalk in watermelon flesh firmness. • ABA associated with the flesh firmness of watermelon increased with exogenous ethylene. Fruit flesh firmness is the key trait of watermelon (Citrullus lanatus) that affects fruit texture, commerciality, and shelf life. However, the knowledge about the underlying molecular mechanisms responsible for variations in fruit flesh firmness is still limited. We constructed a near-isogenic line HWF with high fruit flesh firmness by crossing a wild watermelon PI 271769 as the donor parent and an inbred line 203Z as the recurrent parent. An F 2 sub-segregation population was developed by crossing 203Z and HWF for bulked segregant analysis (BSA-seq). The results revealed a candidate region of 6.1Mb (Chr6: 11557845–17658672) containing the genes related to watermelon flesh firmness. RNA Sequencing (RNA-Seq) analysis of the candidate region led to the identification of a candidate gene, Cla004102 (Aux/IAA), an auxin-responsive protein. The expression of Aux/IAA decreased with fruit developmental stages and a reduction in fruit flesh firmness was observed. Moreover, correlation analysis showed a high positive correlation of Aux/IAA with Cla004120, an ethylene-responsive factor1 (ERF1). The RT-qPCR analysis revealed a higher expression of Aux/IAA and ERF1 consistent with flesh firmness. Higher contents of abscisic acid (ABA) were observed in soft fleshed fruits than hard fleshed fruits. Further, applying exogenous ethylene to watermelon fruit reduced flesh firmness, and ABA content was increased much faster in ethylene-treated fruits than in the control. Interestingly, Aux/IAA expression was also decreased with the reduction in flesh firmness and inclined ABA contents. These findings add considerably to the existing knowledge about watermelon fruit flesh firmness. A more in-depth study would better understand watermelon's genetic mechanisms underlying flesh firmness. [ABSTRACT FROM AUTHOR]