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Geoffrey Meru and Cecilia McGregor

Seed oil percentage (SOP) and fatty acid composition of watermelon (Citrullus lanatus) seeds are important traits in Africa, the Middle East, and Asia where the seeds provide a significant source of nutrition and income. Oil yield from watermelon seed exceeds 50% (w/w) and is high in unsaturated fatty acids, a profile comparable to that of sunflower (Helianthus annuus) and soybean (Glycine max) oil. As a result of novel non-food uses of plant-derived oils, there is an increasing need for more sources of vegetable oil. To improve the nutritive value of watermelon seed and position watermelon as a potential oil crop, it is critical to understand the genetic factors associated with SOP and fatty acid composition. Although the fatty acid composition of watermelon seed is well documented, the underlying genetic basis has not yet been studied. Therefore, the current study aimed to elucidate the quality of watermelon seed oil and identify genomic regions and candidate genes associated with fatty acid composition. Seed from an F2 population developed from a cross between an egusi type (PI 560023), known for its high SOP, and Strain II (PI 279261) was phenotyped for palmitic acid (16:0), stearic acid (18:0), oleic acid (18:1), and linoleic acid (18:2). Significant (P < 0.05) correlations were found between palmitic and oleic acid (0.24), palmitic and linoleic acid (–0.37), stearic and linoleic acid (–0.21), and oleic and linoleic acid (–0.92). A total of eight quantitative trait loci (QTL) were associated with fatty acid composition with a QTL for oleic and linoleic acid colocalizing on chromosome (Chr) 6. Eighty genes involved in fatty biosynthesis including those modulating the ratio of saturated and unsaturated fatty acids were identified from the functionally annotated genes on the watermelon draft genome. Several fatty acid biosynthesis genes were found within and in close proximity to the QTL identified in this study. A gene (Cla013264) homolog to fatty acid elongase (FAE) was found within the 1.5-likelihood-odds (LOD) interval of the QTL for palmitic acid (R 2 = 7.6%) on Chr 2, whereas Cla008157, a homolog to omega-3-fatty acid desaturase and Cla008263, a homolog to FAE, were identified within the 1.5-LOD interval of the QTL for palmitic acid (R 2 = 24.7%) on Chr 3. In addition, the QTL for palmitic acid on Chr 3 was located ≈0.60 Mbp from Cla002633, a gene homolog to fatty acyl- [acyl carrier protein (ACP)] thioesterase B. A gene (Cla009335) homolog to ACP was found within the flanking markers of the QTL for oleic acid (R 2 = 17.9%) and linoleic acid (R 2 = 21.5%) on Chr 6, whereas Cla010780, a gene homolog to acyl-ACP desaturase was located within the QTL for stearic acid (R 2 = 10.2%) on Chr 7. On Chr 8, another gene (Cla013862) homolog to acyl-ACP desaturase was found within the 1.5-LOD interval of the QTL for oleic acid (R 2 = 13.5%). The genes identified in this study are possible candidates for the development of functional markers for application in marker-assisted selection for fatty acid composition in watermelon seed. To the best of our knowledge, this is the first study that aimed to elucidate genetic control of the fatty acid composition of watermelon seed.

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Geoffrey Meru and Cecilia McGregor

Egusi watermelon [Citrullus lanatus (Thunb.) Matsum. & Nakai subsp. mucosospermus var. egusi (C. Jeffrey) Mansf.] is known for its distinctive fleshy-pericarp seed phenotype and high seed oil percentage (SOP). The seed is part of the daily diet in West Africa where it is used in soups and stews or processed for cooking oil. Genetic mapping studies have revealed that most of the variation in SOP between egusi and normal, non-egusi seed is explained by the egusi (eg) locus, which is also associated with the unique seed phenotype. However, variation in SOP is also observed within egusi and normal seed types although the basis of this variation remains to be elucidated. A high correlation between kernel percentage (KP) and SOP has been observed in watermelon and other crops, and recent data also suggest an association between seed size and SOP in watermelon. The aim of this study was to elucidate the relationship among SOP, KP, and seed size traits in watermelon and to identify quantitative trait loci (QTL) associated with the latter traits to facilitate marker-assisted selection (MAS) for traits correlated with SOP. KP showed a significant (α = 0.05) positive correlation with SOP in both egusi and normal seed types, whereas seed size traits showed significant negative correlations with SOP. QTL associated with KP and seed size traits in normal seed were colocalized with a previously mapped locus for SOP on linkage group (LG) 2, but in egusi seed, a QTL explaining 33% of phenotypic variation in KP was localized on LG 7. The results of this study show that SOP in watermelon is correlated with KP and seed size, but KP is associated with different loci in normal and egusi seed phenotypes.

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Cecilia E. McGregor and Vickie Waters

The past 10 years has seen a steep increase in production of seedless watermelon (Citrullus lanatus) in the United States. Seedless fruit is produced on triploid plants that require pollination from diploid pollenizers for fruit set. Synchronization of the staminate flowers on the pollenizers with the appearance of pistillate flowers on the triploids is a fundamental requirement for this production system. Previous research suggested that pistillate flowers reach peak production early in the season, but data are only available for a small number of triploid cultivars. We compared the flowering patterns of 29 triploid cultivars and 20 pollenizers, including 10 harvested pollenizers, during the first 6 weeks after transplanting over 2 years. The average number of days from transplanting (DAT) to the first staminate flower was between 5.3 days and 19.1 days in 2012 and 9.7 days and 24.4 days in 2013 for the pollenizers and between 18.7 days and 27.6 days and 22.1 days and 32.7 days for the pistillate triploid flowers in the 2 years, respectively. K-means clustering of the weekly percentage of plants with staminate and pistillate flowers for the different cultivars shows that different triploid and pollenizer cultivars have different flowering patterns and that some combinations have better synchronized flowering than others. Growers should take particular care when choosing pollenizers for early-flowering triploid cultivars. Harvested pollenizers are better suited to late-flowering triploids and growers should choose triploid and pollenizer cultivar combinations with flowering patterns that best satisfy their specific production goals.

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Cecilia E. McGregor and Vickie Waters

Crop wild relatives (CWRs) are important sources of variation for domesticated crops like watermelon (Citrullus lanatus) where cultivated varieties have a very narrow genetic base. The use of CWRs in plant breeding can be hampered by low fertility, chromosomal rearrangements, marker distortion, and linkage drag in the progeny. Pollen viability can be a quick and easy way to estimate male fertility, which can be a cause of marker distortion and an indicator of chromosomal rearrangements. Pollen viability was determined for F1 hybrids between cultivars and resistant citron and egusi types and the data were used to determine whether the parental cultivars/lines used or the directionality of the cross play a role in pollen viability. F1 hybrids between cultivars and the egusi type showed no reduction in pollen viability compared with parental lines, whereas pollen viability of hybrids with citron types varied between 61.8% and 91.7%. Significant main effects were observed for the cultivar and donor lines used, but the directionality of the cross did not affect pollen viability. F1 hybrids with ‘Crimson Sweet’ as the cultivar parent had significantly higher pollen viability than those with ‘Sugar Baby’ or ‘Charleston Gray’. Our results indicate that the directionality of the crosses between watermelon cultivars and infraspecific CWRs does not affect pollen viability but that the specific cultivars and donor lines used can have a significant effect. The high pollen viability of cultivar–egusi hybrids is supported by previous genetic data and strongly suggests that it should be easier to introgress traits from egusi types than citron types.

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Geoffrey Meru and Cecilia E. McGregor

Fusarium wilt of watermelon (Citrullus lanatus), caused by Fusarium oxysporum f. sp. niveum (FON), is a devastating soil-borne disease limiting watermelon production across the world. Although many watermelon cultivars have been bred for resistance to FON races 0 and 1, the only released cultivars that are resistant to FON 2 are nonharvested pollenizers. The lack of FON 2–resistant edible cultivars is thought to be associated with linkage drag and/or preferential inheritance patterns observed when crossing the resistant, wild source (Citrullus amarus), with edible watermelon. A potential way to overcome these obstacles is to use a resistant C. lanatus as the source of resistance and to develop molecular markers to increase the efficiency of selection. Here we describe the identification of a quantitative trait locus (QTL) associated with FON 2 resistance in watermelon. The genotyping by sequencing (GBS) platform was used to generate single nucleotide polymorphisms (SNPs) in an F2 population (n = 178) developed from a cross between UGA147 (resistant) and ‘Charleston Gray’ (susceptible). Five hundred and one SNPs were placed on the watermelon physical map and used in the mapping of QTL. F3 lines were phenotyped for resistance to FON 2 in the greenhouse. An intermediate QTL associated with resistance to FON 2 was identified on chromosome 11 (Qfon11). This QTL is a potential target for marker-assisted selection (MAS) for FON 2 resistance in watermelon.

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Cecilia E. McGregor and Don R. LaBonte

`White Jewel' is a yellow-and-orange fleshed spontaneous mutant of the orange-flesh sweetpotato [Ipomoea batatas (L.) Lam.] cultivar Jewel. Mutations in storage root flesh color, and other traits are common in sweetpotato. The orange flesh color of sweetpotato is due to β-carotene stored in chromoplasts of root cells. β-carotene is important because of its role in human health. In an effort to elucidate biosynthesis and storage of β-carotene in sweetpotato roots, microarray analysis was used to investigate genes differentially expressed between `White Jewel' and `Jewel' storage roots. β-carotene content calculated from a* color values of `Jewel' and `White Jewel' were 20.66 mg/100 g fresh weight (FW) and 1.68 mg/100 g FW, respectively. Isopentenyl diphosphate isomerase (IPI) was down-regulated in `White Jewel', but farnesyl-diphosphate synthase (FPPS), geranylgeranyl diphosphate synthase (GGPS), and lycopene β-cyclase (LCY-b) were not differentially expressed. Several genes associated with chloroplasts were differentially expressed, indicating probable differences in chromoplast development of `White Jewel' and `Jewel'. Sucrose Synthase was down-regulated in `White Jewel' and fructose and glucose levels in `White Jewel' were lower than in `Jewel' while sucrose levels were higher in `White Jewel'. No differences were observed between dry weight or alcohol insoluble solids of the two cultivars. This study represents the first effort to elucidate β-carotene synthesis and storage in sweetpotato through large-scale gene expression analysis.

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Suzanne Stone, George Boyhan and Cecilia McGregor

Watermelon [Citrullus lanatus (Thunb.) Matsum. & Nakai] cultivars exhibit diverse phenotypic traits, yet are derived from a narrow genetic base. Heirloom cultivars, and to a lesser extent modern open-pollinated (OP) cultivars, are perceived to contain vital genetic variation that is critical for biodiversity conservation and crop improvement. The objective of this study was to characterize the diversity of six heirloom and open-pollinated watermelon cultivars that are popular among U.S. organic, direct-market, and home gardeners. An additional evaluation was conducted to determine whether significant phenotypic and genotypic variation existed among seed lots sourced from different commercial seed vendors. Important horticultural traits such as days to germination, days to first flower, yield, and fruit quality were measured over two field seasons. Genetic diversity was estimated using 32 simple sequence repeat (SSR) markers. Significant differences in horticultural traits among seed lots in both years were observed only in days to germination and first male flower, which may be a consequence of vendor differences in seed storage and quality control. Heirloom ‘Moon and Stars’ and modern OP ‘Sugar Baby’ were the most genetically distinct from the other cultivars and heirloom ‘Georgia Rattlesnake’ was determined to be highly related to the modern OP ‘Charleston Gray’. The two heirloom cultivars were observed to have lower average gene diversity than the modern cultivars. Heirloom ‘Moon and Stars’ contained significant genetic variation among seed lots, yet heirloom ‘Georgia Rattlesnake’ contained none. These findings suggest that genetic variation can be more accurately attributed to pedigree and foundation seed maintenance practices than to the “heirloom” designation per se. The variation reported in this study can be used to inform conservation and breeding efforts.

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Cecilia E. McGregor, Vickie Waters, Tripti Vashisth and Hussein Abdel-Haleem

U.S. watermelon (Citrullus lanatus) production is worth ≈$0.5 billion annually to growers and nearly all of them are dependent on reliable synchronized flowering time of triploid cultivars and diploid pollenizers in their production fields. One aspect of this synchronization is time to flowering, the change from the vegetative to reproductive phase of a plant. Flowering time has emerged as one of the key traits in horticultural and agronomic crops to breed for escape from biotic and abiotic stresses. However, very little is known about the control of flowering time in watermelon. The number of genes involved, mode of inheritance, heritability, and the possible candidate genes are all unknown. In this study, quantitative trait loci (QTL) associated with days to first male flower (DMF), days to first female flower (DFF), and the female-male flower interval (FMI) were identified in a ‘Klondike Black Seeded’ × ‘New Hampshire Midget’ recombinant inbred line population over 2 years. Heritability for DMF, DFF, and FMI were 0.43, 0.23, and 0.10, respectively. Control of flowering time was oligogenic with a major, stable, colocalized QTL on chromosome 3 responsible for ≈50% of the phenotypic variation observed for DMF and DFF. This region of the draft genome sequence contains 172 genes, including homologs of the flowering locus T (Cla009504) and tempranillo 1 (Cla000855) genes associated with flowering time in other species. Cla009504 and Cla000855 represent excellent candidate genes toward the development of a functional marker for marker-assisted selection of flowering time in watermelon. In addition to the major QTL on chromosome 3, two other QTL were identified for DMF (chromosomes 2 and 3) and DFF (chromosomes 3 and 11) and one for FMI on chromosome 2. Understanding the genes involved in this trait and the ability to select efficiently for flowering time phenotypes is expected to accelerate the development of new watermelon cultivars in changing environmental conditions.

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Cecilia McGregor, Vickie Waters, Savithri Nambeesan, Dan MacLean, Byron L. Candole and Patrick Conner

Developing high levels of resistance to Phytophthora blight (Phytophthora capsici Leonian) of pepper (Capsicum annuum L.) is a goal of many pepper breeding programs. Genetic diversity and plant characteristics were evaluated on 21 pepper accessions previously identified as having high levels of Phytophthora root rot resistance. Accessions were evaluated for plant height, fruit size and shape, pericarp thickness, and pungency. Accessions varied widely from very unadapted material to those with more obvious breeding potential. Genetic diversity among the accessions was estimated using 22 simple sequence repeat (SSR) loci. Phytophthora capsici resistant accessions were identified that were not closely related to previously described sources of resistance. This information will allow breeders and researchers to further identify and incorporate novel sources of resistance to P. capsici into breeding programs. Accessions PI 201237 and PI 640532 appear to have the most potential for introgressing P. capcisi resistance into bell pepper.

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Jason Prothro, Katherine Sandlin, Hussein Abdel-Haleem, Eleni Bachlava, Victoria White, Steven Knapp and Cecilia McGregor

Watermelon (Citrullus lanatus) is an important crop grown for both its edible flesh and seeds. Seed size is an important trait in watermelon breeding, with large seeds preferred for planting and edible seeds but small seeds preferred in fruit sold for consumption. Large, medium, and small seed sizes are thought to be controlled by two genes with epistatic interaction. A ‘Klondike Black Seeded’ × ‘New Hampshire Midget’ (KBS × NHM) recombinant inbred line population and a ZWRM 50 × PI 244019 (ZWRM × Citroides) F2 population were used to identify main effect quantitative trait loci (M-QTL) and epistatic QTL (E-QTL) associated with 100 seed weight (100SWT), seed length (SL), and seed width (SWD). Thirteen M-QTL were identified on four linkage groups (LGs) for the three traits in the two populations. Major M-QTL (R 2 = 26.9% to 73.6%) were identified at the same location on LG 2 in both populations for all three traits. M-QTL for all three traits also colocalized on LG 9 in the ZWRM × Citroides population and on LG 4 for 100SWT and SL in the KBS × NHM population. Significant epistatic effects were found between the M-QTL on LG 2 and LG 4 in the KBS × NHM population and between LG 2 and LG 9 in the ZWRM × Citroides population. The phenotypic variance explained by the E-QTL was generally small. The stable, major M-QTL on LG 2 is a candidate for marker-assisted selection for seed size in watermelon.