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Watermelons, Citrullus species (Cucurbitaceae), are native to Africa and have been cultivated since ancient times. The fruit flesh of wild watermelons is watery, but typically hard-textured, pale-coloured and bland or bitter. The familiar sweet dessert watermelons, C. lanatus, featuring non-bitter, tender, well-coloured flesh, have a narrow genetic base, suggesting that they originated from a series of selection events in a single ancestral population. The objective of the present investigation was to determine where dessert watermelons originated and the time frame during which sweet dessert watermelons emerged. Archaeological remains of watermelons, mostly seeds, that date from 5000 years ago have been found in northeastern Africa. An image of a large, striped, oblong fruit on a tray has been found in an Egyptian tomb that dates to at least 4000 years ago. The Greek word pepon, Latin pepo and Hebrew avattiah of the first centuries CE were used for the same large, thick-rinded, wet fruit which, evidently, was the watermelon. Hebrew literature from the end of the second century CE and Latin literature from the beginning of the sixth century CE present watermelons together with three sweet fruits: figs, table grapes and pomegranates. Wild and primitive watermelons have been observed repeatedly in Sudan and neighbouring countries of northeastern Africa. The diverse evidence, combined, indicates that northeastern Africa is the centre of origin of the dessert watermelon, that watermelons were domesticated for water and food there over 4000 years ago, and that sweet dessert watermelons emerged in Mediterranean lands by approximately 2000 years ago. Next-generation ancient-DNA sequencing and state-of-the-art genomic analysis offer opportunities to rigorously assess the relationships among ancient and living wild and primitive watermelons from northeastern Africa, modern sweet dessert watermelons and other Citrullus taxa.

Some of the World’s most valuable crops, including watermelon, honey melon, cucumber, squash, zucchini and pumpkin, belong to the family Cucurbitaceae. We review insights on their domestication from new phylogenies, archaeology and genomic studies. Ancestral state estimation on the most complete Cucurbitaceae phylogeny to date suggests that an annual life cycle may have contributed to domestication. Domestication started c. 11 000 years ago in the New World and Asia, and apparently more recently in Africa. Some cucurbit crops were domesticated only once, others multiple times (e.g. melon from different Asian and African populations). Most wild cucurbit fruits are bitter and nonpalatable to humans, and nonbitterness of the pulp apparently was a trait favoured early during domestication, with genomic data showing how bitterness loss was achieved convergently. The genetic pathways underlying lycopene accumulation, red or orange pulp colour, and fruit size and shape are only just beginning to be understood. The study of cucurbit domestication in recent years has benefitted from the increasing integration of archaeological and genomic data with insights from herbarium collections, the most efficient way to understand species’ natural geographic ranges and climate adaptations.

Watermelon produces many byproducts (watermelon rind and skin) even though those components contain various bioactive compounds, including citrulline. This study evaluated the citrulline concentration, total phenolic content, and antioxidant activity (DPPH and FRAP assays) of different parts of watermelon and investigated the bioavailability of citrulline from different parts of watermelon using an in vitro human intestinal epithelial Caco-2 cell monolayer model. Solid-phase extracted watermelon flesh, rind, and skin samples were treated on a Caco-2 cell monolayer for 1, 2, and 4 h. The collected basolateral solution at each time point was analyzed for the percentage of citrulline transport. Watermelon flesh had the highest citrulline content, but the watermelon skin had the highest total phenolic content and antioxidant activity compared to other watermelon parts. The citrulline bioavailability showed greater % transport in watermelon skin than in watermelon flesh, rind, and L-citrulline standard. It may be due to the different food matrices of watermelon parts. This suggests that the utilization of watermelon by-products such as skin would help develop value-added products with better bioavailability of citrulline. However, since this study was conducted with an in vitro cell model, more extensive research with in vivo studies will be needed.

Viral infections on cucurbit plants cause substantial quality and yield losses on their crops. The diseased plants can often be infected by multiple viruses, and their epidemiology may depend, in addition to the agro-ecological management practices, on the combination of these viral infections. Watermelon mosaic virus (WMV) is one of the most prevalent viruses in cucurbit crops, and Moroccan watermelon mosaic virus (MWMV) emerged as a related species that threatens these crops. The occurrence of WMV and MWMV was monitored in a total of 196 apical-leaf samples of watermelon and pumpkin plants that displayed mosaic symptoms. The samples were collected from 49 fields in three major cucurbit-producing areas in Spain (Castilla La-Mancha, Alicante, and Murcia) for three consecutive (2018–2020) seasons. A molecular hybridization dot-blot method revealed that WMV was mainly (53%) found in both cultivated plants, with an unadvertised occurrence of MWMV. To determine the extent of cultivated plant species and mixed infections on viral dynamics, two infectious cDNA clones were constructed from a WMV isolate (MeWM7), and an MWMV isolate (ZuM10). Based on the full-length genomes, both isolates were grouped phylogenetically with the Emergent and European clades, respectively. Five-cucurbit plant species were infected steadily with either WMV or MWMV cDNA clones, showing variations on symptom expressions. Furthermore, the viral load varied depending on the plant species and infection type. In single infections, the WMV isolate showed a higher viral load than the MWMV isolate in melon and pumpkin, and MWMV only showed higher viral load than the WMV isolate in zucchini plants. However, in mixed infections, the viral load of the WMV isolate was greater than MWMV isolate in melon, watermelon and zucchini, whereas MWMV isolate was markedly reduced in zucchini. These results suggest that the impaired distribution of MWMV in cucurbit crops may be due to the cultivated plant species, in addition to the high prevalence of WMV.

The molecular mode controlling cucumber green mottle mosaic virus (CGMMV)‐induced watermelon blood flesh disease (WBFD) is largely unknown. In this study, we have found that application of exogenous boron suppressed CGMMV infection in watermelon fruit and alleviated WBFD symptoms. Our transcriptome analysis showed that the most up‐regulated differentially expressed genes (DEGs) were associated with polyamine and auxin biosynthesis, abscisic acid catabolism, defence‐related pathways, cell wall modification, and energy and secondary metabolism, while the down‐regulated DEGs were mostly involved in ethylene biosynthesis, cell wall catabolism, and plasma membrane functions. Our virus‐induced gene silencing results showed that silencing of SPDS expression in watermelon resulted in a higher putrescine content and an inhibited CGMMV infection correlating with no WBFD symptoms. SBT and TUBB1 were also required for CGMMV infection. In contrast, silencing of XTH23 and PE/PEI7 (low‐level lignin, cellulose and pectin) and ATPS1 (low‐level glutathione) promoted CGMMV accumulation. Furthermore, RAP2‐3, MYB6, WRKY12, H2A, and DnaJ11 are likely to participate in host antiviral resistance. In addition, a higher (spermidine + spermine):putrescine ratio, malondialdehyde content, and lactic acid content were responsible for fruit decay and acidification. Our results provide new knowledge on the roles of boron in watermelon resistance to CGMMV‐induced WBFD. This new knowledge can be used to design better control methods for CGMMV in the field and to breed CGMMV resistant watermelon and other cucurbit crops. Boron inhibits CGMMV infection in watermelon fruits, probably though regulating the expression of SPDS, SBT, TUBB1, RAP2‐3, MYB6, WRKY12, H2A, XTH23, PE/PEI7, DnaJ11, and ATPS1 in various physiological and biochemical pathways.

• Unloading sugar from sink phloem by transporters is complex and much remains to be understood about this phenomenon in the watermelon fruit. • Here, we report a novel vacuolar sugar transporter (ClVST1) identified through map-based cloning and association study, whose expression in fruit phloem is associated with accumulation of sucrose (Suc) in watermelon fruit. ClVST197 knockout lines show decreased sugar content and total biomass, whereas overexpression of ClVST197 increases Suc content. • Population genomic and subcellular localization analyses strongly suggest a single-base change at the coding region of ClVST197 as a major molecular event during watermelon domestication, which results in the truncation of 45 amino acids and shifts the localization of ClVST197 to plasma membranes in sweet watermelons. Molecular, biochemical and phenotypic analyses indicate that ClVST197 is a novel sugar transporter for Suc and glucose efflux and unloading. • Functional characterization of ClVST1 provides a novel strategy to increase sugar sink potency during watermelon domestication.

Color and pigment contents are important aspects of fruit quality and consumer acceptance of cucurbit crops. Here, we describe the independent mapping and cloning of a common causative APRR2 gene regulating pigment accumulation in melon and watermelon. We initially show that the APRR2 transcription factor is causative for the qualitative difference between dark and light green rind in both crops. Further analyses establish the link between sequence or expression level variations in the CmAPRR2 gene and pigment content in the rind and flesh of mature melon fruits. A genome-wide association study (GWAS) of young fruit rind color in a panel composed of 177 diverse melon accessions did not result in any significant association, leading to an earlier assumption that multiple genes are involved in shaping the overall phenotypic variation in this trait. Through resequencing of 25 representative accessions and allelism tests between light rind accessions, we show that multiple independent single nucleotide polymorphisms in the CmAPRR2 gene are causative of the light rind phenotype. The multi-haplotypic nature of this gene explains the lack of detection power obtained through genotyping by sequencing-based GWAS and confirms the pivotal role of this gene in shaping fruit color variation in melon. This study demonstrates the power of combining bi- and multi-allelic designs with deep sequencing, to resolve lack of power due to high haplotypic diversity and low allele frequencies. Due to its central role and broad effect on pigment accumulation in fruits, the APRR2 gene is an attractive target for carotenoid bio-fortification of cucurbit crops.

Background: An adverse stimulus's biological reaction is inflammation and a key factor in the pathogenesis of various diseases. Lycopene, a potent antioxidant found abundantly in watermelon (Citrullus lanatus), has demonstrated significant anti-inflammatory properties. This study aims to formulate a lycopene-based emulgel from watermelon and assess its anti-inflammatory properties in Wistar rats. Materials and methods: Lycopene was extracted from watermelon. A stable emulgel formulation was developed, combining the benefits of emulsions and gels for effective topical delivery. Using well-established experimental models, the emulgel's anti-inflammatory effectiveness was accessed. Results and discussion: Results indicated that the lycopene-based emulgel significantly reduced inflammation in treated rats, as evidenced by decreased edema and reduced levels of pro-inflammatory cytokines. The mechanisms underlying these effects include the antioxidant activity of lycopene, inhibition of pro-inflammatory cytokines, suppression of the NF-κB pathway, and modulation of enzymatic activity. Additionally, the emulgel formulation ensured enhanced skin penetration and localized action, maximizing therapeutic efficacy while minimizing systemic exposure. Conclusion: In conclusion, the lycopene-based emulgel formulated from watermelon exhibits promising anti-inflammatory activity and offers a potential therapeutic approach for managing inflammatory conditions. Further studies are warranted to explore its clinical applications and long-term safety.

Key message CRISPR/Cas9 system can precisely edit genomic sequence and effectively create knockout mutations in T0 generation watermelon plants. Genome editing offers great advantage to reveal gene function and generate agronomically important mutations to crops. Recently, RNA-guided genome editing system using the type II clustered regularly interspaced short palindromic repeats (CRISPR)-associated protein 9 (Cas9) has been applied to several plant species, achieving successful targeted mutagenesis. Here, we report the genome of watermelon, an important fruit crop, can also be precisely edited by CRISPR/Cas9 system. ClPDS , phytoene desaturase in watermelon, was selected as the target gene because its mutant bears evident albino phenotype. CRISPR/Cas9 system performed genome editing, such as insertions or deletions at the expected position, in transfected watermelon protoplast cells. More importantly, all transgenic watermelon plants harbored ClPDS mutations and showed clear or mosaic albino phenotype, indicating that CRISPR/Cas9 system has technically 100% of genome editing efficiency in transgenic watermelon lines. Furthermore, there were very likely no off-target mutations, indicated by examining regions that were highly homologous to sgRNA sequences. Our results show that CRISPR/Cas9 system is a powerful tool to effectively create knockout mutations in watermelon.

Type specimens are permanently preserved biological specimens that fix the usage of species names. This method became widespread from 1935 onwards and is now obligatory. We used DNA sequencing of types and more recent collections of wild and cultivated melons to reconstruct the evolutionary history of the genus Citrullus and the correct names for its species. We discovered that the type specimen of the name Citrullus lanatus, prepared by a Linnaean collector in South Africa in 1773, is not the species now thought of as watermelon. Instead, it is a representative of another species that is sister to C. ecirrhosus, a tendril‐less South African endemic. The closest relative of the watermelon instead is a West African species. Our nuclear and plastid data furthermore reveal that there are seven species of Citrullus, not four as assumed. Our study implies that sweet watermelon originates from West, not southern Africa as previously believed, and that the South African citron melon has been independently domesticated. These findings affect and explain numerous studies on the origin of these two crops that led to contradictory results because of the erroneous merging of several distinct species.