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QTLs associated with flesh quality traits in an elite × elite watermelon population

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Abstract

Consumers prefer watermelon with sweet, red flesh, and the presence of lycopene, citrulline and arginine phytochemicals helpful for human health is an additional bonus. Breeders often select fruit with desirable flesh characteristics based on soluble solids content (Brix) and visual flesh color. Although marker assisted selection (MAS) of flesh traits would advance germplasm selection efficiency, the low heritability of Brix and lycopene content in red fleshed watermelon has hampered marker development. Here we describe the identification of QTLs associated with lycopene content, the amino acids citrulline and arginine, and the content of individual sugar (sucrose, glucose, fructose) in an elite × elite recombinant inbred line (RIL) population. Brix was most highly correlated with total sugars and glucose content, lycopene content was correlated with sucrose content, and citrulline and arginine content showed no correlation. A region on chromosome 5 was associated with sucrose, glucose, and fructose accumulation, while stable arginine content QTLs were identified on chromosomes 2 and 5.

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References

  • Akashi K, Miyakel C, Yokota A (2001) Citrulline, a novel compatible solute in drought-tolerant wild watermelon leaves, is an efficient hydroxyl radical scavenger. Fed Eur Biomed Soc 508(3):438–442

    Article  CAS  Google Scholar 

  • Akashi K, Mifune Y, Morita K, Ishitsuka S, Tsujimoto H, Ishihara T (2017) Spatial accumulation pattern of citrulline and other nutrients in immature and mature watermelon fruits. J Sci Agric 97:479–487

    Article  CAS  Google Scholar 

  • Baldwin EA (2008) Flavor. In: Gross K (ed) Agriculture handbook, vol 66. USDA. Beltsville, Maryland, pp 126–148

    Google Scholar 

  • Bang H, Kim S, Leskovar D, King S (2007) Development of a codominant CAPS marker for allelic selection between canary yellow and red watermelon based on SNP in lycopene β-cyclase (LCYB) gene. Mol Breed 20(1):63–72. https://doi.org/10.1007/s11032-006-9076-4

    Article  CAS  Google Scholar 

  • Bogdan M, Doerge RW (2005) Biased estimators of quantitative trait locus heritability and location in interval mapping. Hered 95:476–484

    Article  CAS  Google Scholar 

  • Brandt S, Pék Z, Barna É, Lugasi A, Helyes L (2006) Lycopene content and colour of ripening tomatoes as affected by environmental conditions. J Sci Food Agric 86(4):568–572. https://doi.org/10.1002/jsfa.2390

    Article  CAS  Google Scholar 

  • Broman KW, Wu H, Sen Ś, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890

    Article  CAS  Google Scholar 

  • Brown AC Jr, Summers WL (1985) Carbohydrate accumulation and color development in watermelon. J Am Soc Hort 11(5):683–687

    Google Scholar 

  • Brueckner B, Schonhof I, Schroedter R, Kornelson C (2007) ) Improved flavour acceptability of cherry tomatoes. Target group: children. Food Qual Prefer 18(1):152–160. https://doi.org/10.1016/j.foodqual.2005.09.011

    Article  Google Scholar 

  • Cheng Y, Luan F, Wang X et al (2016) Construction of a genetic linkage map of watermelon (Citrullus lanatus) using CAPS and SSR markers and QTL analysis for fruit quality traits. Sci Hortic 202:25–31. https://doi.org/10.1016/j.scienta.2016.01.004

    Article  CAS  Google Scholar 

  • Cheng HM, Koutsidis G, Lodge JK, Ashor A, Siervo M, Lara J (2017) Tomato and lycopene supplementation and cardiovascular risk factors: a systematic review and meta-analysis. Atherosclerosis 257:100–108. https://doi.org/10.1016/j.atherosclerosis.2017.01.009

    Article  CAS  PubMed  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    CAS  PubMed  PubMed Central  Google Scholar 

  • Corey KA, Schlimme DV (1988) Relationship of rind gloss and groundspot color to flesh quality of watermelon fruits during maturation. Sci Hortic 34:211–218

    Article  Google Scholar 

  • Davis AR, Fish WW, Perkins-Veazie P (2003) A rapid hexane-free method for analyzing lycopene content in watermelon. J Food Sci 68:328–332

    Article  CAS  Google Scholar 

  • Davis AR, Webber CLI, Fish WW, Wehner TC, King S, Perkins-Veazie P (2011) L-citrulline levels in watermelon cultigens tested in two environments. Hort Sci 46(12):1572–1575

    CAS  Google Scholar 

  • Di Mascio P, Kaiser S, Sies H (1989) Lycopene as the most effective biological carotenoid singlet oxygen quencher. Arch Biochem Biophys 274:532–538

    Article  Google Scholar 

  • Dirlewanger E, Moing A, Rothan C et al (1999) Mapping QTLs controlling fruit quality in peach (Prunus persica (L.) Batsch). Theor Appl Genet 98:18–31

    Article  CAS  Google Scholar 

  • Elmstrom GW, Davis PL (1981) Sugars in developing and mature fruits of several watermelon cultivars. J Amer Soc Hort Sci 106:330–333

    CAS  Google Scholar 

  • Evans CB (2008) Consumer preferences for watermelons: a conjoint analysis. Thesis, Auburn University

  • Fish WW (2014) The expression of citrulline and other members of the arginine metabolic family in developing watermelon fruit. International J Agric Innovations Res 2(5):665–672

    Google Scholar 

  • Fulton TM, Bucheli P, Voirol E, Lopez J, Petiard V, Tanksley SD (2002) Quantitative trait loci (QTL) affecting sugars, organic acids and other biochemical properties possibly contributing to flavor, identified in four advanced backcross populations of tomato. Euphytica 127:163–177

    Article  CAS  Google Scholar 

  • Goubel F, Vanhoutte C, Allaf O, Verleye M, Gillardin JM (1997) Citrulline malate limits increase in muscle fatigue induced by bacterial endotoxins. J Physiol Pharmacology 75:205–207

    Article  CAS  Google Scholar 

  • Guan Y, Peace C, Rudell D, Verma S, Evans K (2015) QTLs detected for individual sugars and soluble solids content in apple. Mol Breeding 35(6):1–13. https://doi.org/10.1007/s11032-015-0334-1

    Article  CAS  Google Scholar 

  • Guo S, Zhang J, Sun H et al (2013) The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nature Genet 45(1):51–58. https://doi.org/10.1038/ng.2470

    Article  CAS  PubMed  Google Scholar 

  • Hashizume T, Shimamoto I, Hirai M (2003) Construction of a linkage map and QTL analysis of horticultural traits for watermelon [Citrullus lanatus (THUNB.) MATSUM & NAKAI] using RAPD, RFLP and ISSR markers. Theor Appl Genet 106(5):779–785. https://doi.org/10.1007/s00122-002-1030-1

    Article  CAS  PubMed  Google Scholar 

  • Henderson WR, Scott GH, Wehner TC (1998) Interaction of flesh color genes in watermelon. J Hered 89:50–53

    Article  Google Scholar 

  • Holland JB, Nyquist WE, Cervantes-Martinez CT (2003) Estimating and interpreting heritability for plant breeding: an update. Plant Breed Rev 22:9–111

    Google Scholar 

  • Jayaprakasha GK, Murthy KNC, Patil BS (2011) Rapid HPLC-UV method for quantification of L-citrulline in watermelon and its potential role on smooth muscle relaxation markers. Food Chem 127:240–248

    Article  CAS  Google Scholar 

  • Jeffrey C (1978) Further notes on Cucurbitaceae IV: some new-world taxa. Kew Bull 33:347–380

    Article  Google Scholar 

  • Joshi V, Fernie AR (2017) Citrulline metabolism in plants. Amino Acids. https://doi.org/10.1007/s00726-017-2468-4

    Article  PubMed  Google Scholar 

  • Kader AA (2008) Flavor quality of fruits and vegetables. J Sci Food Agric 88(11):1863–1868. https://doi.org/10.1002/jsfa.3293

    Article  CAS  Google Scholar 

  • Kang B, Zhao W, Hou Y, Tian P (2010) Expression of carotenogenic genes during the development and ripening of watermelon fruit. Scientia Hort 124(3):368–375. https://doi.org/10.1016/j.scienta.2010.01.027

    Article  CAS  Google Scholar 

  • Kuti JO, Konuru HB (2005) Effects of genotype and cultivation environment on lycopene content in red-ripe tomatoes. J Sci Food Agric 85(12):2021–2026. https://doi.org/10.1002/jsfa.2205

    Article  CAS  Google Scholar 

  • Li X, Quigg RJ, Zhou J, Xu S, Masinde G, Mohan S, Baylink D (2006) A critical evaluation of the effect of population size and phenotypic measurement on QTL detection and localization using a large F2 murine mapping population. Genet Mol Biol 29:166–173

    Article  CAS  Google Scholar 

  • Li H, Hearne S, Banziger M, Li Z, Wang J (2010) Statistical properties of QTL linkage mapping in biparental genetic populations. Hered 105:257–267

    Article  CAS  Google Scholar 

  • Liu Q, Xu J, Liu Y, Zhao X, Deng X, Guo L, Gu J (2007) A novel bud mutation that confers abnormal patterns of lycopene accumulation in sweet orange fruit (Citrus sinensis L. Osbeck). J Exper Bot 58(15):4161–4171. https://doi.org/10.1093/jxb/erm273

    Article  CAS  Google Scholar 

  • Liu S, Gao P, Wang X, Davis A, Baloch AM, Luan F (2015) Mapping of quantitative trait loci for lycopene content and fruit traits in Citrullus lanatus. Euphytica 202:411–426. https://doi.org/10.1007/s10681-014-1308-9

    Article  CAS  Google Scholar 

  • Ma C, Sun Z, Chen C, Zhang L, Zhu S (2014) Simultaneous separation and determination of fructose, sorbitol, glucose and sucrose in fruits by HPLC–ELSD. Food Chem 145:784–788. https://doi.org/10.1016/j.foodchem.2013.08.135

    Article  CAS  PubMed  Google Scholar 

  • Maynard DN (2001) An introduction to the watermelon. In: Maynard DN (ed) Characteristics, production and marketing. ASHS Press, Alexandria, pp 9–20

    Google Scholar 

  • McKnight JR, Satterfield MC, Jobgen WS et al (2010) Beneficial effects of l-arginine on reducing obesity: potential mechanisms and important implications for human health. Amino Acids 39:349–357. https://doi.org/10.1007/s00726-010-0598-z

    Article  CAS  PubMed  Google Scholar 

  • Mitcham B, Cantwell M, Kader A (1996) Methods for determining quality of fresh commodities. Perishables Handling Newsletter 85:1–5

    Google Scholar 

  • NASS (2015) Vegetables 2016 summary. United States Department of Agriculture, Wasington

    Google Scholar 

  • Nyquist WE, Baker R (1991) Estimation of heritability and prediction of selection response in plant populations. Crit Rev Plant Sci 10:235–322

    Article  Google Scholar 

  • Pangborn RM (1963) Relative taste intensities of selected sugars and organic acids. Food Science 28:726–733

    Article  Google Scholar 

  • Pardo JE, Gomez R, Tardaguila J, Amo A, Varon R (1997) Quality evaluation of watermelon varieties (Citrullus vulgaris S.). J Food Quality 20:547–557

    Article  Google Scholar 

  • Parris GK (1949) Watermelon breeding. Econ Bot 3:193–212

    Article  Google Scholar 

  • Perkins-Veazie P, Collins JK, Pair SD, Roberts W (2001) Lycopene content differs among red-fleshed watermelon cultivars. J Sci Food Agric 81:983–987

    Article  CAS  Google Scholar 

  • Perkins-Veazie P, Collins J, Hassell R et al (2005) Lycopene content of mini watermelon varieties grown at four locations. Hort Sci 40(4):1091

    Google Scholar 

  • Poole CF (1944) Genetics of cultivated cucurbits. J Hered 35:122–128

    Article  Google Scholar 

  • Pratt HK (1971) The biochemistry of fruits and their products. In: Hulme AC (ed) Melons, vol 2. Academic Press, London, pp 207–232

    Google Scholar 

  • Rekha C, Poornima G, Manasa M, Abhipsa V, Pavithra Devi J, Vijay Kumar HT, Prashith Kekuda TR (2012) Ascorbic acid, total phenol content and antioxidant acitivity of fresh juices of four ripe and unripe citrus fruits. Chem Sci Trans 1(2):303–310

    Article  Google Scholar 

  • Ren Y, McGregor C, Zhang Y et al (2014) An integrated genetic map based on four mapping populations and quantitative trait loci associated with economically important traits in watermelon (Citrullus lanatus). BMC Plant Biol 14(33):1–11

    Google Scholar 

  • Rimando AM, Perkins-Veazie PM (2005) Determination of citrulline in watermelon rind. J Chromatography A 1078(1–2):196–200. https://doi.org/10.1016/j.chroma.2005.05.009

    Article  CAS  Google Scholar 

  • Sandlin K, Prothro J, Heesacker A et al (2012) Comparative mapping in watermelon [Citrullus lanatus (Thunb.) Matsum. et Nakai]. Theor Appl Genet 125(8):1603–1618. https://doi.org/10.1007/s00122-012-1938-z

    Article  PubMed  Google Scholar 

  • Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52(3):591–611. https://doi.org/10.2307/2333709

    Article  Google Scholar 

  • Telef N, Stammitti B, Mortain-Bertrand A, Maucourt M, Carde JP, Rolin D, Gallusci P (2006) Sucrose deficiency delays lycopene accumulation in tomato fruit pericarp discs. Plant Mol Biol 62:453–469. https://doi.org/10.1007/s11103-006-9033-y

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Basten CJ, Zeng ZB (2011) Windows QTL cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh

    Google Scholar 

  • Waugh WH, Daeschner CWI, Files BA, McConnell ME, Strandjord SE (2001) Oral citrulline as arginine precursor may be beneficial in sickle cell disease: early phase two results. J Natl Medical Assn 93(10):363–371

    CAS  Google Scholar 

  • Wehner TC, Naegele RP, Perkins-Veazie P (2017) Heritability and genetic variance components associated with citrulline, arginine, and lycopene content in diverse watermelon cultigens. Hort Sci 52(7):936–940. https://doi.org/10.21273/HORTSCI11255-16

    Article  CAS  Google Scholar 

  • Wu G, Bazer FW, Kim SW (2007) New developments in amino acid research. In: Rosati A, Tewolde A, Mosconi C (eds) Animal production and animal science worldwide. Wageningen Academic Publishers, Wageningen, pp 299–315

    Google Scholar 

  • Wu G, Bazer FW, Davis TA et al (2009) Arginine metabolism and nutrition in growth, health and disease. Amino Acids 37(1):153–168. https://doi.org/10.1007/s00726-008-0210-y

    Article  CAS  PubMed  Google Scholar 

  • Xu Y, Guo S, Zhang H, Gong G (2006) QTL analysis of soluble solids content in watermelon under different environments. In: Paper presented at the Cucurbitaceae, Asheville, North Carolina, 17–21 Sept 2006

  • Xu Q, Yu K, Zhu A, Ye J, Liu Q, Zhang J, Deng X (2009) Comparative transcripts profiling reveals new insight into molecular processes regulating lycopene accumulation in a sweet orange (Citrus sinensis) red-flesh mutant. BMC Genom. https://doi.org/10.1186/1471-2164-10-540

    Article  Google Scholar 

  • Yativ M, Harary I, Wolf S (2010) Sucrose accumulation in watermelon fruits: genetic variation and biochemical analysis. J Plant Physiol 167(8):589–596. https://doi.org/10.1016/j.jplph.2009.11.009

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Ge Y (2016) Dynamics of sugar-metabolic enzymes and sugars accumulation during watermelon (Citrullus lanatus) fruit development. Pak J Bot 48(6):2535–2538

    CAS  Google Scholar 

  • Zhu Q, Gao P, Liu S, Zhu Z, Amanullah S, Davis AR, Luan F (2017) Comparative transcriptome analysis of two contrasting watermelon genotypes during fruit development and ripening. BMC Genom. https://doi.org/10.1186/s12864-016-3442-3

    Article  Google Scholar 

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Acknowledgements

The authors thank Yihua Chen, Kristin Adams, Jessica Norton, and Daniel Powell for their invaluable help during harvest, collection, and preparation of samples.

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Correspondence to Cecilia McGregor.

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Fall, L.A., Perkins-Veazie, P., Ma, G. et al. QTLs associated with flesh quality traits in an elite × elite watermelon population. Euphytica 215, 30 (2019). https://doi.org/10.1007/s10681-019-2356-y

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