Whole genome resequencing of watermelons to identify single nucleotide polymorphisms related to flesh color and lycopene content


Autoři: Saminathan Subburaj aff001;  Kayoun Lee aff001;  Yongsam Jeon aff001;  Luhua Tu aff001;  Gilwoo Son aff002;  SuBok Choi aff003;  Yong-Pyo Lim aff001;  Cecilia McGregor aff004;  Geung-Joo Lee aff001
Působiště autorů: Department of Horticulture, Chungnam National University, Daejeon, Republic of Korea aff001;  Breeding Institute, Hyundai Seed Co Ltd., Yeoju, Gyeonggi, Republic of Korea aff002;  Asia Seed, Co., Ltd., Seoul, Republic of Korea aff003;  Department of Horticulture, University of Georgia, Athens, GA, United States of America aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223441

Souhrn

Cultivated watermelon (Citrullus lanatus) is one of the most important food crops in the Cucurbitaceae family. Diversification after domestication has led cultivated watermelons to exhibit diverse fruit flesh colors, including red, yellow, and orange. Recently, there has been increased interest in red-fleshed watermelons because they contain the antioxidant cis-isomeric lycopene. We performed whole genome resequencing (WGRS) of 24 watermelons with different flesh colors to identify single-nucleotide polymorphisms (SNPs) related to high lycopene content. The resequencing data revealed 203,894–279,412 SNPs from read mapping between inbred lines and the 97103 reference genome. In total, 295,065 filtered SNPs were identified, which had an average polymorphism information content of 0.297. Most of these SNPs were intergenic (90.1%) and possessed a transversion (Tv) rate of 31.64%. Overall, 2,369 SNPs were chosen at 0.5 Mb physical intervals to analyze genetic diversity across the 24 inbred lines. A neighbor-joining dendrogram and principal coordinate analysis (PCA) based on the 2,369 SNPs revealed that the 24 inbred lines could be grouped into high and low lycopene-type watermelons. In addition, we analyzed SNPs that could discriminate high lycopene content, red-fleshed watermelon from low lycopene, yellow or orange watermelon inbred lines. For validation, 19 SNPs (designated as WMHL1–19) were chosen randomly, and cleavage amplified polymorphic sequence (CAPS) markers were designed. Genotyping of the above 24 lines and 12 additional commercial cultivars using WMHL1–19 CAPS markers resulted in match rates of over 0.92 for most validated markers in correlation with the flesh color phenotypes. Our results provide valuable genomic information regarding the high lycopene content phenotype of red-fleshed cultivated watermelons, and the identified SNPs will be useful for the development of molecular markers in the marker-assisted breeding of watermelons with high lycopene content.

Klíčová slova:

Fruits – Chromosome mapping – Inbred strains – Introns – Invertebrate genomics – Molecular genetics – Seeds – Carotenoids


Zdroje

1. Chomicki G, Renner SS. Watermelon origin solved with molecular phylogenetics including Linnaean material: another example of museomics. New Phytol. 2015;205(2): 526–532. doi: 10.1111/nph.13163 25358433

2. Paris HS. Origin and emergence of the sweet dessert watermelon, Citrullus Lanatus. Ann Bot. 2015;116(2): 133–148. doi: 10.1093/aob/mcv077 26141130

3. Levi A, Thomas CE, Keinath AP and Wehner TC. Genetic diversity among watermelon (Citrullus lanatus and Citrullus colocynthis) accessions. Genet Resour Crop Evol. 2001a;48(6): 559–566. https://doi.org/10.1023/A:1013888418442

4. Levi A, Thomas CE, Wehner TC and Zhang X. Low genetic diversity indicates the need to broaden the genetic base of cultivated watermelon. HortScience. 2001b;36(6): 1096–1101.

5. Levi A, Thomas CE, Newman M, Reddy OUK, Zhang X, Xu Y. ISSR and AFLP markers differ among American watermelon cultivars with limited genetic diversity. Amer Soc Hort Sci. 2004;129(4): 553–558.

6. Beckmann JS, Soller M. Restriction fragment length polymorphisms and genetic improvement of agricultural species. Euphytica. 1986;35(1): 111–24. https://doi.org/10.1007/BF00028548

7. Powell W, Morgante M, Andre C, Hanafey M, Vogel J, Tingey S and Rafalski A. The comparison of RFLP, RAPD, AFLP and SSR (microsatellite) markers for genotype analysis. Mol breeding. 1996;2(3): 225–238. https://doi.org/10.1007/BF00564200

8. Liu S, Gao P, Zhu Q, Luan F, Davis AR, Wang X. Development of cleaved amplified polymorphic sequence markers and a CAPS-based genetic linkage map in watermelon (Citrullus lanatus [Thunb.] Matsum. and Nakai) constructed using whole-genome re-sequencing data. Breed Sci. 2016;66(2): 244–259. doi: 10.1270/jsbbs.66.244 27162496

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

10. Guo SG, Zhang JG, Sun HH, Salse J, Lucas WJ, Zhang H, Zheng Y, Mao LY, Ren Y, et al. The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nat Genet. 2013;45(1): 51–58. doi: 10.1038/ng.2470 23179023

11. Nimmakayala P, Abburi VL, Bhandary A, Abburi L, Vajja VG, Reddy R, et al. Use of VeraCode 384-plex assays for watermelon diversity analysis and integrated genetic map of watermelon with single nucleotide polymorphisms and simple sequence repeats. Mol Breed. 2014;34(2): 537–548. https://doi.org/10.1007/s11032-014-0056-9

12. Reddy UK, Nimmakayala P, Levi A, Abburi VL, Saminathan T, Tomason YR et al. High-resolution genetic map for understanding the effect of genome-wide recombination rate on nucleotide diversity in watermelon. G3 (Bethesda). 2014;4(11): 2219–2230. doi: 10.1534/g3.114.012815 25227227

13. Ren R, Ray R, Li P, Xu J, Zhang M, Liu G, et al. Construction of a high-density DArTseq SNP-based genetic map and identification of genomic regions with segregation distortion in a genetic population derived from a cross between feral and cultivated-type watermelon. Mol Genet Genomics. 2015;290(4): 1457–1470. doi: 10.1007/s00438-015-0997-7 25702268

14. Yang X, Ren R, Ray R, Xu J, Li P, Zhang M, et al. Genetic diversity and population structure of core watermelon (Citrullus lanatus) genotypes using DArTseq-based SNPs. Plant Genet Res. 2016;14(3): 226–233. https://doi.org/10.1017/S1479262115000659

15. Bramley PM. Regulation of carotenoid formation during tomato fruit ripening and development. J Exp Bot. 2002;53(377): 2107–2113. doi: 10.1093/jxb/erf059 12324534

16. Alque´zar B, Rodrigo MJ, Zacarı´as L. Regulation of carotenoid biosynthesis during fruit maturation in the red-fleshed orange mutant Cara Cara. Phytochemistry. 2008;69(10): 1997–2007. doi: 10.1016/j.phytochem.2008.04.020 18538806.

17. Gusmini G, Wehner TC. Qualitative inheritance of rind pattern and flesh color in watermelon. J Hered. 2006;97(2): 177–185. doi: 10.1093/jhered/esj023 16489140

18. Tadmor Y, King S, Levi A, Davis A, Meir A, Wasserman B et al. Comparative fruit colouration in watermelon and tomato. Food Res Int. 2005;38(8–9): 837–841. https://doi.org/10.1016/j.foodres.2004.07.011

19. Bang H, Davis AR, Kim S, Leskovar DI, King SR. Flesh color inheritance and gene interactions among canary yellow, pale yellow, and red watermelon. J Am Soc Hortic Sci. 2010;135(4): 362–368

20. Perkins-Veazie P, Collins JK, Davis AR, Roberts W. Carotenoid content of 50 watermelon cultivars. J Agric Food Chem. 2006;54(7): 2593–2597. doi: 10.1021/jf052066p 16569049

21. Mohanty NK, Saxena S, Singh UP, Goyal NK, Arora RP. Lycopene as a chemopreventive agent in the treatment of high-grade prostate intraepithelial neoplasia. Urol Oncol. 2005;23(6): 383–385. doi: 10.1016/j.urolonc.2005.05.012 16301113

22. Feng D, Ling WH, Duan RD. Lycopene suppresses LPS induced NO and IL-6 production by inhibiting the activation of ERK, p38MAPK, and NF-k B in macrophages. Inflamm. Res. 2010;59(2): 115–121. doi: 10.1007/s00011-009-0077-8 19693648

23. Reddy UK, Abburi L, Abburi VL, Saminathan T, Cantrell R, Vajja VG, Reddy R, Tomason YR, Levi A, Wehner TC, et al. A genome-wide scan of selective sweeps and association mapping of fruit traits using microsatellite markers in watermelon. J Hered. 2015;106(2): 166–76. doi: 10.1093/jhered/esu077 25425675

24. Park G, Kim J, Jin B, Yang HB, Park SW, Yang HB, et al. Genome-wide sequence variation in watermelon inbred Lines and its implication for marker-assisted breeding. Korean J Hortic Sci Technol. 2018;36(2): 280–291. https://doi.org/10.12972/kjhst.20180028

25. Branham S, Vexler L, Meir A, Tzuri G, Frieman Z, Levi A et al. Genetic mapping of a major codominant QTL associated with β-carotene accumulation in watermelon. Mol Breeding. 2017;37: 146. https://doi.org/10.1007/s11032-017-0747-0

26. Poole CF. Genetics of cultivated cucurbits. J Hered. 1994;35(4): 122–128. https://doi.org/10.1093/oxfordjournals.jhered.a105364

27. Henderson WR. Inheritance of orange flesh color in watermelon. Cucurbit Genet Coop Rpt. 1989;12: 59–63.

28. Henderson WR, Scott GH, Wehner TC. Interaction of flesh color genes in watermelon. J Hered. 1998;89(1): 50–53. https://doi.org/10.1093/jhered/89.1.50

29. Bang H, Kim S, Leskovar D, King S. 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. 2007;20(1): 63–72. https://doi.org/10.1007/s11032-006-9076-4

30. Bang H, Yi G, Kim S, Leskovar D, Patil BS. Watermelon lycopene β-cyclase: promoter characterization leads to the development of a PCR marker for allelic selection. Euphytica. 2014;200(3): 363–378. https://doi.org/10.1007/s10681-014-1158-5

31. Zhu Q, Gao P, Liu S, Zhu Z, Amanullah S, Davis AR et al. Comparative transcriptome analysis of two contrasting watermelon genotypes during fruit development and ripening. BMC Genomics. 2017;18: 3. doi: 10.1186/s12864-016-3442-3 28049426

32. Hashizume T, Shimamoto I, Hirai M. 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. 2003;106(5): 779–785. doi: 10.1007/s00122-002-1030-1 12647050

33. Liu S, Gao P, Wang X, Davis AR, Baloch AM, Luan F. Mapping of quantitative trait loci for lycopene content and fruit traits in Citrullus lanatus. Euphytica. 2015;202(3): 411–426. https://doi.org/10.1007/s10681-014-1308-9

34. UPOV (International union for the protection of new varieties of plants). Watermelon-guidelines for the conduct of tests for distinctness, uniformity and stability. 2013;TG 142/5: 1–39

35. Murray MG, Thompson WF. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 1980;8: 4321–4325. doi: 10.1093/nar/8.19.4321 7433111.

36. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14): 1754–1760. doi: 10.1093/bioinformatics/btp324 19451168

37. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R; 1000 Genome Project Data Processing Subgroup. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25(16): 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943

38. Hildebrand CE, David C, Torney C, Wagner P. Informativeness of polymorphic DNA markers. In: Cooper NG, ed. Human genome project: deciphering the blueprint of heredity. University Science Books, Sausalito, CA, USA; 1992. pp. 100–102.

39. Zheng X, Levine D, Shen J, Gogarten SM, Laurie C, Weir BS: A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics. 2012;28(24): 3326–3328. doi: 10.1093/bioinformatics/bts606 23060615

40. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, et al. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics. 2007;23(19): 2633–2635. doi: 10.1093/bioinformatics/btm308 17586829

41. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol. 2016;33(7): 1870–1874. doi: 10.1093/molbev/msw054 27004904

42. Ren Y, McGregor C, Zhang Y, Gong G, Zhang H, Guo S, Sun H, Cai W, Zhang J, Xu Y: 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. 2014;14: 33. doi: 10.1186/1471-2229-14-33 24443961

43. Sandlin K, Prothro J, Heesacker A, Khalilian N, Okashah R, Xiang W, Bachlava E, Caldwell DG, Taylor CA, et al. Comparative mapping in watermelon [Citrullus lanatus (Thunb.) Matsum. et Nakai]. Theor Appl Genet. 2012;125(8): 1603–1618. doi: 10.1007/s00122-012-1938-z 22875176

44. Dia M, Wehner TC, Perkins-Veazie P, Hassell R, Price DS, Boyhan GE, Olson SM, King SR, Davis AR, Tolla GE, Bernier J, Juarez B. Stability of fruit quality traits in diverse watermelon cultivars tested in multiple environments. Hortic Res. 2016;3: 16066. doi: 10.1038/hortres.2016.66 28066557

45. Thiel T, Kota R, Grosse I, Stein N, Graner A. SNP2CAPS: a SNP and INDEL analysis tool for CAPS marker development. Nucleic Acids Res. 2004;32(1): e5. doi: 10.1093/nar/gnh006 14704362

46. Carrillo-López A, Yahia EM. Changes in color-related compounds in tomato fruit exocarp and mesocarp during ripening using HPLC-APcI(+)-mass Spectrometry. J Food Sci Technol. 2014;51(10): 2720–2726. doi: 10.1007/s13197-012-0782-0 25328217

47. Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML. Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet. 2011;12(7): 499–510. doi: 10.1038/nrg3012 21681211

48. Edwards D, Batley J. Plant genome sequencing: applications for crop improvement. Plant Biotechnol J. 2010;8(1): 2–9. doi: 10.1111/j.1467-7652.2009.00459.x 19906089

49. Poole CF, Grimball PC. Interaction of sex, shape, and weight genes in watermelon. J Agric Res. 1945;71: 533–552. 21004938

50. Kumar R, Wehner TC. Discovery of second gene for solid dark green versus light green rind pattern in watermelon. J Hered. 2011;102(4): 489–493. doi: 10.1093/jhered/esr025 21566001

51. Yang HB, Park SW, Park Y, Lee GP, Kang SC, Kim YK. Linkage analysis of the three loci determining rind color and stripe pattern in watermelon. Korean J Hortic Sci. 2015;33(4): 559–565.

52. Kim KH, Hwang JH, Han DY, Park M, Kim S, Choi D, Park YH. Major quantitative trait loci and putative candidate genes for powdery mildew resistance and fruit-related traits revealed by an intraspecific genetic map for watermelon (Citrullus lanatus var. lanatus). PLOS ONE. 2015;10(12): e0145665. doi: 10.1371/journal.pone.0145665 26700647


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