Abstract
The first single-nucleotide polymorphism (SNP) maps for watermelon [Citrullus lanatus (Thunb.) Matsum. et Nakai] were constructed and compared. Three populations were developed from crosses between two elite cultivars, Klondike Black Seeded × New Hampshire Midget (KBS × NHM), an elite cultivar and wild egusi accession, Strain II × PI 560023 (SII × Egusi) and an elite cultivar and a wild citron accession, ZWRM50 × PI 244019 (ZWRM × Citroides). The SII × Egusi and ZWRM × Citroides F2 populations consisted of 187 and 182 individuals respectively while the KBS × NHM recombinant inbred line (RIL) population consisted of 164 lines. The length of the genetic maps were 1,438, 1,514 and 1,144 cM with average marker distances of 3.8, 4.2, and 3.4 cM for the KBS × NHM, SII × Egusi and ZWRM × Citroides populations, respectively. Shared markers were used to align the three maps so that the linkage groups (LGs) represented the 11 chromosomes of the species. Marker segregation distortion were observed in all three populations, but was highest (12.7 %) in the ZWRM × Citroides population, where Citroides alleles were favored. The three maps were used to construct a consensus map containing 378 SNP markers with an average distance of 5.1 cM between markers. Phenotypic data was collected for fruit weight (FWT), fruit length (FL), fruit width (FWD), fruit shape index (FSI), rind thickness (RTH) and Brix (BRX) and analyzed for quantitative trait loci (QTL) associated with these traits. A total of 40 QTL were identified in the three populations, including major QTL for fruit size and shape that were stable across genetic backgrounds and environments. The present study reports the first SNP maps for Citrullus and the first map constructed using two elite parents. We also report the first stable QTL associated with fruit size and shape in Citrullus lanatus. These maps, QTL and SNPs should be useful for the watermelon community and represent a significant step towards the potential use of molecular tools in watermelon breeding.
Similar content being viewed by others
References
Arcade A, Labourdette A, Falque M, Mangin B, Chardon F, Charcosset A, Joets J (2004) BioMercator: integrating genetic maps and QTL towards discovery of candidate genes. Bioinformatics 20:2324–2326
Blanc G, Charcosset A, Mangin B, Gallais A, Moreau L (2006) Connected populations for detecting quantitative trait loci and testing for epistasis: an application in maize. Theor Appl Genet 113:206–224
Buckler ES, Phelps-Durr TL, Buckler CSK, Dawe RK, Doebley JF, Holtsford TP (1999) Meiotic drive of chromosomal knobs reshaped the maize genome. Genetics 153:415–426
Che K-P, Liang C-Y, Wang Y-G, Jin D-M, Wang B, Xu Y, Kang G-B, Zhang H-Y (2003) Genetic assessment of watermelon germplasm using the AFLP technique. HortScience 38:81–84
Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971
Dane F, Lang P (2004) Sequence variation at cpDNA regions of watermelons and related wild species: implications for evolution of Citrullus haplotypes. Am J Bot 91:1922–1929
Dane F, Liu J (2007) Diversity and origin of cultivated and citron type watermelon (Citrullus lanatus). Genet Resour Crop Evol 54:1255–1265
Deleu W, Esteras C, Roig C, Gonzalez-To M, Fernandez-Silva I, Gonzalez-Ibeas D, Blanca J, Aranda M, Arus P, Nuez F, Monforte A, Pico M, Garcia-Mas J (2009) A set of EST-SNPs for map saturation and cultivar identification in melon. BMC Plant Biol 9:90
Demir I, Mavi K (2004) The effect of priming on seedling emergence of differentially matured watermelon (Citrullus lanatus (Thunb.) Matsum and Nakai) seeds. Sci Horticult 102:467–473
deVicente MC, Tanksley SD (1993) QTL analysis of transgressive segregation in an interspecific tomato cross. Genetics 134:585–596
Doerge RW, Churchill GA (1996) Permutation tests for multiple loci affecting a quantitative character. Genet Mol Biol 142:285–294
Esteras C, Gomez P, Monforte AJ, Blanca J, Vicente-Dolera N, Roig C, Nuez F, Pico B (2012) High-throughput SNP genotyping in Cucurbita pepo for map construction and quantitative trait loci mapping. BMC Genomics 13:80
Fernandez-Silva I, Moreno E, Essafi A, Fergany M, Garcia-Mas J, Martín-Hernandez A, Álvarez J, Monforte A (2010) Shaping melons: agronomic and genetic characterization of QTLs that modify melon fruit morphology. Theor Appl Genet 121:931–940
Food and Agriculture Organization of the United Nations (2011) Crop production. http://www.faostat.fao.org/site/567/default.aspx#ancor. Accessed 18 July 2011
Fursa TB (1972) K sistematic roda Citrullus Schrad. [On the taxonomy of genus Citrullus Schrad.]. Botanicheski Zhurnal 57:31–41
Guner N, Wehner TC (2004) The genes of watermelon. HortScience 39:1175–1182
Gusmini G, Wehner TC (2005) Foundations of yield improvement in watermelon. Crop Sci 45:141–146
Gusmini G, Wehner TC (2007) Heritability and genetic variance estimates for fruit weight in watermelon. HortScience 42:1332–1336
Hackett CA, Broadfoot LB (2003) Effects of genotyping errors, missing values and segregation distortion in molecular marker data on the construction of linkage maps. Heredity 90:33–38
Hashizume T, Shimamoto I, Harushima Y, Yui M, Sato T, Imai T, Hirai M (1996) Construction of a linkage map for watermelon (Citrullus lanatus (Thunb.) Matsum & Nakai) using random amplified polymorphic DNA (RAPD). Euphytica 90:265–273
Hashizume T, Shimamoto I, Hirai M (2003) Construction of a linkage map and QTL analysis of horticultural traits for watermelon [Citrullus lanatus (Thumb.) Matsum & Nakai] using RAPD, RFLP and ISSR markers. Theor Appl Genet 106:779–785
Hawkins LK, Dane F, Kubisiak TL, Rhodes BB, Jarret RL (2001) Linkage mapping in a watermelon population segregating for Fusarium wilt resistance. J Am Soc Hort Sci 126:344–350
Henry RJ (2008) Plant genotyping II: SNP technology. CABI, Wallingford
Holland JB, Nyquist WE, Cervantes-Martinez CT (2003) Estimating and interpreting heritability for plant breeding: an update. Plant Breed Rev 22:9–111
Jarret RL, Merrick LC, Holms T, Evans J, Aradhya MK (1997) Simple sequence repeats in watermelon (Citrullus lanatus (Thunb.) Matsum. & Nakai). Genome 40:433–441
JMP Version 8.0.2 (2009) SAS Institute Inc., Cary, NC, 1989–2009
Kole C, Abbott AG (2008) Principles and practices of plant genomics, vol 1. Genome mapping Science Publishers, Enfield
Kumar R (2009) Inheritance of fruit yield and other horticulturally important traits in watermelon [Citrullus lanatus (Thunb.) Matsum. & Nakai]. North Carolina State University, Raleigh
Levi A, Thomas CE (2005) Polymorphisms among chloroplast and mitochondrial geneomes of Citrullus species and subspecies. Genet Resour Crop Evol 52:609–617
Levi A, Thomas CE, Keinath AP, Wehner TC (2001a) Genetic diversity among watermelon (Citrullus lanatus and Citrullus colocynthis) accessions. Genet Resour Crop Evol 48:559–566
Levi A, Thomas CE, XP XPZ, Joobeur T, Dean RE, Wehner TC, Carle BR (2001b) A genetic linkage map for watermelon based on randomly ampliWed polymorphic DNA markers. J Hort Sci 126:730–737
Levi A, Thomas C, Joobeur T, Zhang X, Davis A (2002) A genetic linkage map for watermelon derived from a testcross population: (Citrullus lanatus var. citroides × C. lanatus var. lanatus) × Citrullus colocynthis. Theor Appl Genet 105:555–563
Levi A, Thomas CE, Trebitsh T, Salman A, King J, Karalius J, Newman M, Reddy OUK, Xu Y, Zhang X (2006) An extended linkage map for watermelon based on SRAP, AFLP, SSR, ISSR, and RAPD markers. J Am Soc Hort Sci 131:393–402
Levi A, Wechter P, Massey L, Carter L, Hopkins D (2011) An extended genetic linkage map for watermelon based on a testcross and a BC2F2 population. Am J Plant Sci 2:93–110
MacGillivray JH (1947) Soluble solids content of different regions of watermelon. Plant Physiol 22:637–640
Maynard DN (2001) An introduction to the watermelon. In: Maynard DN (ed) Watermelon characteristics, production and marketing. ASHS Press, Alexandria, pp 9–20
McGregor CE (2011) Citrullus lanatus germplasm of Southern Africa. Isr J Plant Sci (in press)
Monforte AJ, Oliver M, Gonzalo MJ, Alvarez JM, Dolcet-Sanjuan R, Arús P (2004) Identification of quantitative trait loci involved in fruit quality traits in melon (Cucumis melo L.). Theor Appl Genet 108:750–758
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Resour 8:4321–4325
Navot N, Sarfatti M, Zamir D (1990) Linkage relationships of genes affecting bitterness and flesh color in watermelon. J Hered 81:162–165
Nerson H (2002) Effects of seed maturity, extraction practices and storage duration on germinability in watermelon. Sci Horticult 93:245–256
Nimmakayala P, Tomason YR, Jeong J, Ponniah SK, Karunathilake A, Levi A, Perumal R, Reddy UK (2010) Genetic reticulation and interrelationships among Citrullus species as revealed by joint analysis of shared AFLPs and species-specific SSR alleles. Plant Genetic Resour 8:16–25
Nyquist WE, Baker R (1991) Estimation of heritability and prediction of selection response in plant populations. Crit Rev Plant Sci 10:235–322
Perin C, Hagen S, De Conto V, Katzir N, Danin-Poleg Y, Portnoy V, Baudracco-Arnas S, Chadoeuf J, Dogimont C, Pitrat M (2002) A reference map of Cucumis melo based on two recombinant inbred line populations. Theor Appl Genet 104:1017–1034
Périn C, Hagen L, Giovinazzo N, Besombes D, Dogimont C, Pitrat M (2002) Genetic control of fruit shape acts prior to anthesis in melon (Cucumis melo L.). Mol Genet Genomics 266:933–941
Poole CF, Grimball PC (1945) Interaction of sex, shape, and weight genes in watermelon. J Agric Res 71:533–552
Porter DR (1933) Watermelon breeding. Hilgardia 7:533–552
Porter DR (1937) Inheritance of certain fruit and seed characters in watermelons. Hilgardia 10:489–509
Porter DR, Bission CS, Allinger HW (1940) Factors affecting the total soluble solids, reducing sugars, and sucrose in watermelons. Hilgardia 13:31–66
Ren Y, Zhao H, Kou Q, Jiang J, Guo S, Zhang H, Hou W, Zou X, Sun H, Gong G, Levi A, Xu Y (2012) A high resolution genetic map anchoring scaffolds of the sequenced watermelon genome. PLoS One 7:e29453
Rieseberg LH, Archer MA, Wayne RK (1999) Transgressive segregation, adaptation and speciation. Heredity 83:363–372
Robinson RW, Decker-Walters DS (1997) Cucurbits. CAB International Publishing, Oxon
Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611
Showalter RK (1961) Specific gravity, weight, and solids relationships in watermelons. Florida St Hort Soc 74:268–271
Tang S, Okashah R, Knapp S, Arnold M, Martin N (2010) Transmission ratio distortion results in asymmetric introgression in Louisiana Iris. BMC Plant Biol 10:48
Tanksley SD (2004) The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. Plant Cell 16:S181–S189
United States Department of Agriculture—National Agricultural Statistics Service (2011) 2010 Agricultural Statistics. http://www.nass.usda.gov/Publications/Ag_Statistics/2010/index.asp. Accessed 09 July 2011
Van Ooijen JW (2006) JoinMap®4 Software for the calculation of genetic linkage maps in experimental populations. Kyazma B.V, Wageningen
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Wang S, Basten CJ, Zeng ZB (2011) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh
Weetman LM (1937) Inheritance and correlation of shape, size and color in the watermelon Citrullus vulgaris Schrad. Iowa Agric Exp Station Ann Bull 228:224–256
Wehner T (2008) Watermelon. In: Prohens J, Nuez F (eds) Vegetables I: Asteraceae, Brassicaceae, Chenopodicaceae, and Cucurbitaceae. Springer, New York, pp 381–418
Wehner TC, Shetty NV, Elmstron GW (2001) Breeding and seed production. In: Maynard DN (ed) Watermelons: characteristics, production, and marketing. ASHS Press, Alexandria, pp 27–73
Yuan X, Pan J, Cai R, Guan Y, Liu L, Zhang W, Li Z, He H, Zhang C, Si L, Zhu L (2008a) Genetic mapping and QTL analysis of fruit and flower related traits in cucumber (Cucumis sativus L.) using recombinant inbred lines. Euphytica 164:473–491
Yuan XJ, Li XZ, Pan JS, Wang G, Jiang S, Li XH, Deng SL, He HL, Si MX, Lai L, Wu AZ, Zhu LH, Cai R (2008b) Genetic linkage map construction and location of QTLs for fruit-related traits in cucumber. Plant Breed 127:180–188
Zalapa J, Staub J, McCreight J, Chung S, Cuevas H (2007) Detection of QTL for yield-related traits using recombinant inbred lines derived from exotic and elite US Western Shipping melon germplasm. Theor Appl Genet 114:1185–1201
Zeng ZB (1993) Theoretical basis of separation of multiple linked gene effects on mapping quantitative trait loci. PNAS 90:10972–10976
Zeng ZB (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468
Zhang R, Xu Y, Yi K, Zhang H, Liu L, Gong G, Levi A (2004) A genetic linkage map for watermelon derived from recombinant inbred lines. J Am Soc Hort Sci 129:237–243
Zraidi A, Stift G, Pachner M, Shojaeiyan A, Gong L, Lelley T (2007) A consensus map for Cucurbita pepo. Mol Breed 20:375–388
Acknowledgments
This research was funded by Monsanto. The authors thank Hussein Abdel-Haleem for assistance with heritability calculations.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Havey.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sandlin, K., Prothro, J., Heesacker, A. et al. Comparative mapping in watermelon [Citrullus lanatus (Thunb.) Matsum. et Nakai]. Theor Appl Genet 125, 1603–1618 (2012). https://doi.org/10.1007/s00122-012-1938-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-012-1938-z