Genetic Resources and Crop Evolution

, Volume 60, Issue 2, pp 427–440 | Cite as

High frequency oligonucleotides: targeting active gene (HFO-TAG) markers revealed wide genetic diversity among Citrullus spp. accessions useful for enhancing disease or pest resistance in watermelon cultivars

  • Amnon Levi
  • Judy A. Thies
  • W. Patrick Wechter
  • Howard F. Harrison
  • Alvin M. Simmons
  • Umesh K. Reddy
  • Padma Nimmakayala
  • Zhangjun Fei
Research Article

Abstract

There is a continuous need to enhance watermelon cultivars for disease and pest resistance. Different U.S. Plant Introductions (PIs) of Citrullus lanatus subsp. lanatus var. lanatus [also known as C. lanatus (Thunb.) Matsum. et Nakai subsp. lanatus var. citroides (Bailey) Mansf. ex Greb.] (CLC) collected in southern Africa are a useful source for enhancing disease or pest resistance in watermelon cultivars. They are also valuable as rootstocks for grafted watermelon, particularly in fields infested with root-knot nematodes or Fusarium wilt. However, there is little information about genetic relationships among these PIs. In this study, genetic diversity was examined among 74 CLC PIs collected from their center of origin in southern Africa. Also, 15 Citrullus lanatus subsp. lanatus (CLL) PIs and the American heirloom cultivars Charleston Gray and Black Diamond (Citrullus lanatus subsp. vulgaris (Schrader ex Eckl. et Zeyh.) Fursa) (CLV) and five Citrullus colocynthis (L.) Schrader (CC) PIs collected in different locations throughout the world were used as out-groups in the phylogenetic analysis for the CLC PIs. Twenty-three high frequency oligonucleotides—targeting active gene (HFO-TAG) primers were used in polymerase chain reaction (PCR) experiments to produce a total of 562 polymorphic markers among the Citrullus PIs and cultivars. Cluster and multidimensional scaling plot analysis produced distinct groups of CLC, CLL, and CC PIs. Several PIs that were designated as CLC or CLL were in transitional positions, indicating that they are the result of gene flow between the major Citrullus groups or subgroups. Population structure analysis indicated that CLC comprises two subgroups; each containing a set of unique alleles. Also, unique alleles exist in the CLL and the CC genotypes. Overall, broad genetic diversity exists among the Citrullus PIs. The data in this study should be useful for identifying PIs with a wide genetic distance between them that could be used in breeding programs aiming to develop heterotic F1 hybrid rootstock lines for grafted watermelon.

Keywords

Citrullus DNA Genetic structure Resistance Grafting Nematodes Fusarium 

References

  1. Barata C, Carena MJ (2006) Classification of North Dakota maize inbred lines into heterotic groups based on molecular and testcross data. Euphytica 151:339–349CrossRefGoogle Scholar
  2. Bates DM, Robinson RW (1995) Cucumbers melon and watermelons. In: Smart J, Simmonds NW (eds) Evolution of crop plants, 2nd edn. Longman, London, UK, pp 89–96Google Scholar
  3. Boyhan GE, Norton JD, Abrahams BR, Wen NH (1994) A new source of resistance to anthracnose (Race 2) in watermelon. HortScience 29:111–112Google Scholar
  4. Buckler ES IV, Phelps-Durr TL, Keith Buckler CS, Dawe RK, Doebley JF, Holtsford TP (1999) Meiotic drive of chromosomal knobs reshaped the maize genome. Genetics 153:415–426PubMedGoogle Scholar
  5. Burkill HM (1985) The useful plants of west tropical Africa, 2nd edn, vol 1. Royal Botanic Gardens, KewGoogle Scholar
  6. Cheres MT, Miller JF, Crane JM, Knapp SJ (2000) Genetic distance as a predictor of heterosis and hybrid performance within and between heterotic groups in sunflower. Theor Appl Genet 100:889–894CrossRefGoogle Scholar
  7. Cohen R, Burger Y, Horev C, Koren A, Edelstein M (2007) Introducing grafted cucurbits to modern agriculture: the Israeli experience. Plant Dis 91:916–923CrossRefGoogle Scholar
  8. Dahl Jensen B, Touré FM, Hamattal MA, Touré FA, Nantoumé AD (2011) Watermelons in the Sand of Sahara: cultivation and use of indigenous landraces in the Tombouctou Region of Mali. Ethnobotany Research & Applications 9:151–162Google Scholar
  9. Dane F, Lang P (2004) Sequence variation at cpDNA regions of watermelon and related species: implications for the evolution of Citrullus haplotypes. Am J Bot 91:1922–1929PubMedCrossRefGoogle Scholar
  10. Dane F, Liu J (2007) Diversity and origin of cultivated and citron type watermelon (Citrullus lanatus). Genet Resour Crop Evol 54:1255–1265CrossRefGoogle Scholar
  11. Dane F, Hawkins LK, Norton JD (1998) New resistance to race 2 of Fusarium oxysporum f. sp. niveum in watermelon. Cucurbit Genet Coop Report 21:37–39Google Scholar
  12. Davis AR, Levi A, Tetteh A, Wehner T, Russo V, Pitrat M (2007) Evaluation of watermelon and related species for resistance to race 1 W powdery mildew. J Amer Hort Sci 132:790–795Google Scholar
  13. De Winter B (1990) A new species of Citrullus (Benincaseae) from the Namib desert, Namibia. Bothalia 20:209–211Google Scholar
  14. Dhliwayo T, Pixley K, Menkir A, Warburton M (2009) Combining ability, genetic distances, and heterosis among elite CIMMYT and IITA tropical maize inbred lines. Crop Sci 49:1301–1310CrossRefGoogle Scholar
  15. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578PubMedCrossRefGoogle Scholar
  16. FAOSTAT (2012) Food and Agriculture Organization of the United Nations http://faostat.fao.org
  17. Fursa TB (1972) On the taxonomy of the genus Citrullus Schad. Botanicheskij Zhurnal 57:31–34Google Scholar
  18. Gillaspie AG Jr, Wright JM (1993) Evaluation of Citrullus sp. germplasm for resistance to watermelon Mosaic Virus 2. Plant Dis 77:352–354CrossRefGoogle Scholar
  19. Gusmini G, Song R, Wehner TC (2005) New sources of resistance to gummy stem blight in watermelon. Crop Sci 45:582–588CrossRefGoogle Scholar
  20. Harris KR, Wechter WP, Levi A (2009a) Isolation, sequence analysis, and linkage mapping of NBS-LRR disease resistance gene homologs in watermelon. J Amer Soc Hort Sci 134:649–657Google Scholar
  21. Harris KR, Ling K, Levi A, Wechter WP (2009b) Identification and utility of markers linked to the zucchini yellow mosaic virus resistance gene in watermelon. J Amer Soc Hort Sci 134:529–534Google Scholar
  22. Jarret RL, Merrick LC, Holms T, Evans J, Aradhya MK (1997) Simple sequence repeats in watermelon [Citrullus lanatus (Thunb.) Matsum. & Nakai]. Genome 40:433–441PubMedCrossRefGoogle Scholar
  23. Jeffrey C (2001) Cucurbitaceae. In: Hanelt P, Institute of Plant Genetics and Crop Plant Research (eds) Mansfeld’s encyclopedia of agricultural and horticultural crops, vol 3. Springer, Berlin, pp 1510–1557Google Scholar
  24. Jones RM (1965) Analysis of variance of the half diallel table. Heredity 20:117–121CrossRefGoogle Scholar
  25. Laghetti G, Hammer K (2007) The Corsican citron melon (Citrullus lanatus (Thunb.) Matsum. et Nakai subsp. lanatus var. citroides (Bailey) Mansf. ex Greb.) a traditional and neglected crop. G. Genet Resour Crop Evol 54:913–916CrossRefGoogle Scholar
  26. Levi A, Thomas CE (1999) An improved procedure for isolation of high quality DNA from watermelon and melon leaves. Cucurbit Genet Coop Rep 22:41–42Google Scholar
  27. Levi A, Thomas CE, Keinath AP, Wehner TC (2001a) Genetic diversity among watermelon (Citrullus lanatus and Citrullus colocynthis) accessions. Genet Resour Crop Evol 48:559–566CrossRefGoogle Scholar
  28. Levi A, Thomas CE, Wehner TC, Zhang X (2001b) Low genetic diversity indicates the need to broaden the genetic base of cultivated watermelon. HortScience 36:1096–1101Google Scholar
  29. Levi A, Davis A, Hernandez A, Wechter P, Thimmapuram J, Tadmor Y, Katzir N, Trebitsh T, King S (2006) Genes expressed during the development and ripening of watermelon fruit. Plant Cell Rep 25:1233–1245PubMedCrossRefGoogle Scholar
  30. Levi A, Wechter P, Davis A (2009) EST-PCR markers representing watermelon fruit genes are polymorphic among watermelon heirloom cultivars sharing a narrow genetic base. Plant Genet Resour 7:16–32CrossRefGoogle Scholar
  31. Levi A, Wechter WP, Harris-Shultz KR, Davis AR, Fie Z (2010) High-frequency oligonucleotides in watermelon expressed sequenced tag-unigenes are useful in producing polymorphic polymerase chain reaction markers among watermelon genotypes. J Amer Hort Sci 135:369–378Google Scholar
  32. Levi A, Wechter WP, Massey LM, Carter L, Hopkins D (2011) Genetic linkage map of Citrullus lanatus var. citroides chromosomal segments introgressed into the watermelon cultivar Crimson Sweet (Citrullus lanatus var. lanatus) genome. American Journal of Plant Sciences 2:93–110CrossRefGoogle Scholar
  33. Luan F, Sheng Y, Wang Y, Staub JE (2010) Performance of melon hybrids derived from parents of diverse geographic origins. Euphytica 173:1–16CrossRefGoogle Scholar
  34. Martyn RD, Netzer D (1991) Resistance to races 0, 1 and 2 of Fusarium wilt of watermelon in Citrullus sp. PI-296341-FR. HortScience 26:429–432Google Scholar
  35. Meeuse AD (1962) The Cucurbitaceae of Southern Africa. Bothalia 8:1–111Google Scholar
  36. Melchinger AE, Gumber RK (1998) Overview of heterosis and heterotic groups in agronomic crops. In: Lamkey KR, Staub JE (eds) Concepts and breeding of heterosis in crop plants. CSSA Spec. Publ. 25. CSSA, Madison, WI, pp. 29–44Google Scholar
  37. Mujaju C, Fatih M (2011) Distribution patterns of cultivated watermelon forms in Zimbabwe using DIVA-GIS. International Journal of Biodiversity and Conservation 39:474–481Google Scholar
  38. Mujaju C, Sehic J, Werlemark G, Garkava-Gustavsson L, Faith M, Nybom H (2010) Genetic diversity in watermelon (Citrullus lanatus) landraces from Zimbabwe revealed by RAPD and SSR markers. Hereditas 147:142–153PubMedCrossRefGoogle Scholar
  39. Mujaju C, Zborowska A, Werlemark G, Garkava-Gustavsson L, Andersen SB, Nybom H (2011) Genetic diversity among and within watermelon (Citrullus lanatus) landraces in southern Africa. Journal of Horticultural Science & Biotechnology 86:353–358Google Scholar
  40. Nei M, Li W (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273PubMedCrossRefGoogle Scholar
  41. Pavlicek A, Hrda S, Flegr J (1999) FreeTree-Freeware program for construction of phylogenetic trees on the basis of distance data and bootstrap/jackknife analysis of the tree robustness. Application in the RAPD analysis of the genus Frenkelia. Folia Biol 45:97–99Google Scholar
  42. Rohlf FJ (1998) NTSYS-PC numerical taxonomy and multivariate analysis system, ver. 2.2. Exeter Publishing, Ltd., Setauket, NYGoogle Scholar
  43. Sowell G, Pointer GR (1962) Gummy stem blight resistance in introduced watermelons. Plant Dis Rep 46:883–885Google Scholar
  44. Sowell G Jr, Rhodes BB, Norton JD (1980) New sources of resistance to watermelon anthracnose. J Am Soc Hort Sci 105:197–199Google Scholar
  45. Teklewold A, Becker HC (2006) Comparison of phenotypic and molecular distances to predict heterosis and F1 performance in Ethiopean mustard (Brassica carinata A. Braun). Theor Appl Genet 112:752–759PubMedCrossRefGoogle Scholar
  46. Tetteh AY, Wehner TC, Davis AR (2010) Identifying resistance to powdery mildew race 2 W in the USDA-ARS watermelon germplasm collection. Crop Sci 50:933–939CrossRefGoogle Scholar
  47. Thies JA, Levi A (2003) Resistance of watermelon (Citrullus spp.) germplasm to the peanut root-knot nematode (Meloidogyne arenaria race 1). HortScience 38:1417–1421Google Scholar
  48. Thies JA, Levi A (2007) Characterization of watermelon (Citrullus lanatus var. citroides) germplasm for resistance to root-knot nematodes. J Nematol 42:1530–1533Google Scholar
  49. Thies J, Ariss J, Hassell R, Kousik C, Olson S, Levi A (2010) Grafting for managing southern root-knot nematode, Meloidogyne incognita, in watermelon. Plant Dis 94:1195–1199CrossRefGoogle Scholar
  50. USDA, NASS (2009) Watermelons, vegetables, potatoes, and melons harvested for sale: 2007 and 2002, 2007 Census of Agriculture-State Data, National Agricultural Statistics Service, USDAGoogle Scholar
  51. van der Vossen HAM, Denton OA, El Tahir IM (2004) Citrullus lanatus. In: Grubben GJH, Denton OA (eds) Plant resources of tropical Africa, vol 2. Vegetables. Backhuys Publishers, Wageningen, pp 185–191Google Scholar
  52. Wechter WP, Levi A, Harris KR, Davis AR, Fei ZJ, Katzir N, Giovannoni JJ, Salman A, Hernandez A, Thimmapuram J, Tadmor V, Portnoy V, Trebitsh T (2008) Gene expression in developing watermelon fruit. BMC-Genomics 9:275–282PubMedCrossRefGoogle Scholar
  53. Wechter WP, Kousik C, McMillan M, Levi A (2012) Identification of resistance to Fusarium oxysporum f. sp. niveum race 2 in Citrullus lanatus var. citroides Plant Introductions. HortScience 47:334–338Google Scholar
  54. Wehner TC (2008) Watermelon. In: Prohens J, Nuez F (eds) Handbook of plant breeding; vegetables I: Asteraceae, Brassicaceae, Chenopodiaceae, and Cucurbitaceae. Springer Science + Business LLC, New York, pp 381–418Google Scholar
  55. Whitaker TW, Bemis WB (1976) Cucurbits. In: Simmonds NW (ed) Evolution of crop plants. Longman, London, pp 64–69Google Scholar
  56. Whitaker TW, Davis GN (1962) Cucurbits: botany, cultivation, and utilization. Interscience Publishers, Inc., New YorkGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. (outside the USA) 2012

Authors and Affiliations

  • Amnon Levi
    • 1
  • Judy A. Thies
    • 1
  • W. Patrick Wechter
    • 1
  • Howard F. Harrison
    • 1
  • Alvin M. Simmons
    • 1
  • Umesh K. Reddy
    • 2
  • Padma Nimmakayala
    • 2
  • Zhangjun Fei
    • 3
  1. 1.USDA, ARSCharlestonUSA
  2. 2.Department of Biology, Douglass Land-grant InstituteWest Virginia State UniversityInstituteUSA
  3. 3.Boyce Thompson Institute for Plant ResearchIthacaUSA

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