Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Watermelon [Citrullus lanatus (Thunb.) Matsum. & Nakai] is an economically important vegetable crop grown extensively worldwide. To facilitate the identification of agronomically important traits and provide new information for genetic and genomic research on this species, a high-density genetic linkage map of watermelon was constructed using an F2 population derived from a cross between elite watermelon cultivar K3 and wild watermelon germplasm PI 189225. Based on a sliding window approach, a total of 1,161 bin markers representing 3,465 SNP markers were mapped onto 11 linkage groups corresponding to the chromosome pair number of watermelon. The total length of the genetic map is 1,099.2 cM, with an average distance between bins of 1.0 cM. The number of markers in each chromosome varies from 62 in chromosome 07 to 160 in chromosome 05. The length of individual chromosomes ranged between 61.8 cM for chromosome 07 and 140.2 cM for chromosome 05. A total of 616 SNP bin markers showed significant (P < 0.05) segregation distortion across all 11 chromosomes, and 513 (83.3 %) of these distorted loci showed distortion in favor of the elite watermelon cultivar K3 allele and 103 were skewed toward PI 189225. The number of SNPs and InDels per Mb varied considerably across the segregation distorted regions (SDRs) on each chromosome, and a mixture of dense and sparse SNPs and InDel SDRs coexisted on some chromosomes suggesting that SDRs were randomly distributed throughout the genome. Recombination rates varied greatly among each chromosome, from 2.0 to 4.2 centimorgans per megabase (cM/Mb). An inconsistency was found between the genetic and physical positions on the map for a segment on chromosome 11. The high-density genetic map described in the present study will facilitate fine mapping of quantitative trait loci, the identification of candidate genes, map-based cloning, as well as marker-assisted selection (MAS) in watermelon breeding programs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Akhunov E, Nicolet C, Dvorak J (2009) Single nucleotide polymorphism genotyping in polyploid wheat with the Illumina GoldenGate assay. Theor Appl Genet 119:507–517

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Altshuler D, Pollara VJ, Cowles CR, Van Etten WJ, Baldwin J, Linton L, Lander ES (2000) An SNP map of the human genome generated by reduced representation shotgun sequencing. Nature 407:513–516

    Article  CAS  PubMed  Google Scholar 

  • Arumuganathan K, Earle E (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Report 9:208–218

    Article  CAS  Google Scholar 

  • Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Selker EU, Cresko WA, Johnson EA (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3:e3376

    Article  PubMed Central  PubMed  Google Scholar 

  • Boyhan G, Norton J, Abrahams B, Wen H (1994) A new source of resistance to anthracnose (Race 2) in watermelon. HortScience 29:111–112

    Google Scholar 

  • Brookes AJ (1999) The essence of SNPs. Gene 234:177–186

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Xie W, He H, Yu H, Chen W, Li J, Yu R, Yao Y, Zhang W, He Y, Tang X, Zhou F, Deng XW, Zhang Q (2014) A high-density SNP genotyping array for rice biology and molecular breeding. Mol Plant 7:541–553

    Article  CAS  PubMed  Google Scholar 

  • Courtois B, Audebert A, Dardou A, Roques S, Ghneim-Herrera T, Droc G, Frouin J, Rouan L, Gozé E, Kilian A (2013) Genome-wide association mapping of root traits in a japonica rice panel. PLoS One 8:e78037

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cruz VM, Kilian A, Dierig DA (2013) Development of DArT marker platforms and genetic diversity assessment of the U.S. collection of the new oilseed crop lesquerella and related species. PLoS One 8:e64062

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Deleu W, Esteras C, Roig C, Gonzalez-To M, Fernandez-Silva I, Gonzalez-Ibeas D, Blanca J, Aranda MA, Arus P, Nuez F, Monforte AJ, Pico MB, Garcia-Mas J (2009) A set of EST-SNPs for map saturation and cultivar identification in melon. BMC Plant Biol 9:90

    Article  PubMed Central  PubMed  Google Scholar 

  • Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6:e19379

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 Genom 13:80

    Article  CAS  Google Scholar 

  • Ganal MW, Altmann T, Röder MS (2009) SNP identification in crop plants. Curr Opin Plant Biol 12:211–217

    Article  CAS  PubMed  Google Scholar 

  • Ganal MW, Durstewitz G, Polley A, Berard A, Buckler ES, Charcosset A, Clarke JD, Graner EM, Hansen M, Joets J, Le Paslier MC, McMullen MD, Montalent P, Rose M, Schon CC, Sun Q, Walter H, Martin OC, Falque M (2011) A large maize (Zea mays L.) SNP genotyping array: development and germplasm genotyping, and genetic mapping to compare with the B73 reference genome. PLoS ONE 6:e28334

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ganal MW, Polley A, Graner E-M, Plieske J, Wieseke R, Luerssen H, Durstewitz G (2012) Large SNP arrays for genotyping in crop plants. J Biosci 37:821–828

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Mas J, Benjak A, Sanseverino W, Bourgeois M, Mir G, Gonzalez VM, Henaff E, Camara F, Cozzuto L, Lowy E, Alioto T, Capella-Gutierrez S, Blanca J, Canizares J, Ziarsolo P, Gonzalez-Ibeas D, Rodriguez-Moreno L, Droege M, Du L, Alvarez-Tejado M, Lorente-Galdos B, Mele M, Yang L, Weng Y, Navarro A, Marques-Bonet T, Aranda MA, Nuez F, Pico B, Gabaldon T, Roma G, Guigo R, Casacuberta JM, Arus P, Puigdomenech P (2012) The genome of melon (Cucumis melo L.). Proc Natl Acad Sci U S A 109:11872–11877

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guo S, Liu J, Zheng Y, Huang M, Zhang H, Gong G, He H, Ren Y, Zhong S, Fei Z, Xu Y (2011) Characterization of transcriptome dynamics during watermelon fruit development: sequencing, assembly, annotation and gene expression profiles. BMC Genom 12:454

    Article  CAS  Google Scholar 

  • Guo S, Zhang J, Sun H, Salse J, Lucas WJ, Zhang H, Zheng Y, Mao L, Ren Y, Wang Z (2013) The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nat Genet 45:51–58

    Article  CAS  PubMed  Google Scholar 

  • Gusmini G, Song R, Wehner TC (2005) New sources of resistance to gummy stem blight in watermelon. Crop Sci 45:582–588

    Article  Google Scholar 

  • Harel-Beja R, Tzuri G, Portnoy V, Lotan-Pompan M, Lev S, Cohen S, Dai N, Yeselson L, Meir A, Libhaber SE, Avisar E, Melame T, van Koert P, Verbakel H, Hofstede R, Volpin H, Oliver M, Fougedoire A, Stalh C, Fauve J, Copes B, Fei Z, Giovannoni J, Ori N, Lewinsohn E, Sherman A, Burger J, Tadmor Y, Schaffer AA, Katzir N (2010) A genetic map of melon highly enriched with fruit quality QTLs and EST markers, including sugar and carotenoid metabolism genes. Theor Appl Genet 121:511–533

    Article  CAS  PubMed  Google Scholar 

  • Harushima Y, Nakagahra M, Yano M, Sasaki T, Kurata N (2001) A genome-wide survey of reproductive barriers in an intraspecific hybrid. Genetics 159:883–892

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  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 106:779–785

    CAS  PubMed  Google Scholar 

  • 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 Hortic Sci 126:344–350

    CAS  Google Scholar 

  • Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, Lucas WJ, Wang X, Xie B, Ni P, Ren Y, Zhu H, Li J, Lin K, Jin W, Fei Z, Li G, Staub J, Kilian A, van der Vossen EA, Wu Y, Guo J, He J, Jia Z, Ren Y, Tian G, Lu Y, Ruan J, Qian W, Wang M, Huang Q, Li B, Xuan Z, Cao J, Asan WuZ, Zhang J, Cai Q, Bai Y, Zhao B, Han Y, Li Y, Li X, Wang S, Shi Q, Liu S, Cho WK, Kim JY, Xu Y, Heller-Uszynska K, Miao H, Cheng Z, Zhang S, Wu J, Yang Y, Kang H, Li M, Liang H, Ren X, Shi Z, Wen M, Jian M, Yang H, Zhang G, Yang Z, Chen R, Liu S, Li J, Ma L, Liu H, Zhou Y, Zhao J, Fang X, Li G, Fang L, Li Y, Liu D, Zheng H, Zhang Y, Qin N, Li Z, Yang G, Yang S, Bolund L, Kristiansen K, Zheng H, Li S, Zhang X, Yang H, Wang J, Sun R, Zhang B, Jiang S, Wang J, Du Y, Li S (2009) The genome of the cucumber, Cucumis sativus L. Nat Genet 41:1275–1281

    Article  CAS  PubMed  Google Scholar 

  • Jansen J, De Jong A, Van Ooijen J (2001) Constructing dense genetic linkage maps. Theor Appl Genet 102:1113–1122

    Article  CAS  Google Scholar 

  • Jones N, Ougham H, Thomas H, Pasakinskiene I (2009) Markers and mapping revisited: finding your gene. New Phytol 183:935–966

    Article  CAS  PubMed  Google Scholar 

  • Joobeur T, Gusmini G, Zhang X, Levi A, Xu Y, Wehner TC, Oliver M, Dean RA (2006) Construction of a watermelon BAC library and identification of SSRs anchored to melon or Arabidopsis genomes. Theor Appl Genet 112:1553–1562

    Article  CAS  PubMed  Google Scholar 

  • Kianian S, Quiros C (1992) Generation of a Brassica oleracea composite RFLP map: linkage arrangements among various populations and evolutionary implications. Theor Appl Genet 84:544–554

    CAS  PubMed  Google Scholar 

  • Kilian A, Wenzl P, Huttner E, Carling J, Xia L, Blois H, Caig V, Heller-Uszynska K, Jaccoud D, Hopper C (2012) Diversity arrays technology: a generic genome profiling technology on open platforms. In: Data production and analysis in population genomics. Springer, pp 67–89

  • Kosambi D (1943) The estimation of map distances from recombination values. Annal Eugen 12:172–175

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Levi A, Davis A, Hernandez A, Wechter P, Thimmapuram J, Trebitsh T, Tadmor Y, Katzir N, Portnoy V, King S (2006a) Genes expressed during the development and ripening of watermelon fruit. Plant Cell Rep 25:1233–1245

    Article  CAS  PubMed  Google Scholar 

  • Levi A, Thomas C, Trebitsh T, Salman A, King J, Karalius J, Newman M, Reddy O, Xu Y, Zhang X (2006b) An extended linkage map for watermelon based on SRAP, AFLP, SSR, ISSR, and RAPD markers. J Am Soc Hortic Sci 131:393–402

    CAS  Google Scholar 

  • Li X, Wang X, Wei Y, Brummer EC (2011) Prevalence of segregation distortion in diploid alfalfa and its implications for genetics and breeding applications. Theor Appl Genet 123:667–679

    Article  PubMed  Google Scholar 

  • Lorieux M, Perrier X, Goffinet B, Lanaud C, De León DG (1995) Maximum-likelihood models for mapping genetic markers showing segregation distortion. 2. F2 populations. Theor Appl Genet 90:81–89

    Article  CAS  PubMed  Google Scholar 

  • Lyttle TW (1991) Segregation distorters. Annu Rev Genet 25:511–581

    Article  CAS  PubMed  Google Scholar 

  • Rafalski JA (2002) Novel genetic mapping tools in plants: SNPs and LD-based approaches. Plant Sci 162:329–333

    Article  CAS  Google Scholar 

  • Raman H, Raman R, Kilian A, Detering F, Carling J, Coombes N, Diffey S, Kadkol G, Edwards D, McCully M, Ruperao P, Parkin IA, Batley J, Luckett DJ, Wratten N (2014) Genome-wide delineation of natural variation for pod shatter resistance in Brassica napus. PLoS ONE 9:e101673

    Article  PubMed Central  PubMed  Google Scholar 

  • Ren R, Wang M, Chen X, Zhang Z (2012a) Characterization and molecular mapping of Yr52 for high-temperature adult-plant resistance to stripe rust in spring wheat germplasm PI 183527. Theor Appl Genet 125:847–857

    Article  CAS  PubMed  Google Scholar 

  • Ren Y, Zhao H, Kou Q, Jiang J, Guo S, Zhang H, Hou W, Zou X, Sun H, Gong G, Levi A, Xu Y (2012b) A high resolution genetic map anchoring scaffolds of the sequenced watermelon genome. PLoS One 7:e29453

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ren Y, McGregor C, Zhang Y, Gong G, Zhang H, Guo S, Sun H, Cai W, Zhang J, Xu Y (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

    Article  PubMed Central  PubMed  Google Scholar 

  • Sandlin K, Prothro J, Heesacker A, Khalilian N, Okashah R, Xiang W, Bachlava E, Caldwell DG, Taylor CA, Seymour DK, White V, Chan E, Tolla G, White C, Safran D, Graham E, Knapp S, McGregor C (2012) Comparative mapping in watermelon [Citrullus lanatus (Thunb.) Matsum. et Nakai]. Theor Appl Genet 125:1603–1618

    Article  PubMed  Google Scholar 

  • Sansaloni C, Petroli C, Jaccoud D, Carling J, Detering F, Grattapaglia D, Kilian A (2011) Diversity Arrays Technology (DArT) and next-generation sequencing combined: genome-wide, high throughput, highly informative genotyping for molecular breeding of Eucalyptus. In: BMC Proceedings. BioMed Central Ltd, pp P54

  • Taylor DR, Ingvarsson PK (2003) Common features of segregation distortion in plants and animals. Genetica 117:27–35

    Article  CAS  PubMed  Google Scholar 

  • Team RC (2012) R: A language and environment for statistical computing

  • Tetteh AY, Wehner TC, Davis AR (2010) Identifying resistance to powdery mildew race 2W in the USDA-ARS Watermelon Germplasm Collection. Crop Sci 50:933

    Article  Google Scholar 

  • Tetteh AY, Wehner TC, Davis AR (2013) Inheritance of resistance to powdery mildew race 2 in Citrullus lanatus var. lanatus. HortScience 48:1227–1230

    Google Scholar 

  • Van Ooijen J (2011) Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genet Res 93:343–349

    Article  Google Scholar 

  • Voorrips R (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  CAS  PubMed  Google Scholar 

  • Wechter WP, Levi A, Harris KR, Davis AR, Fei Z, Katzir N, Giovannoni JJ, Salman-Minkov A, Hernandez A, Thimmapuram J, Tadmor Y, Portnoy V, Trebitsh T (2008) Gene expression in developing watermelon fruit. BMC Genom 9:275

    Article  Google Scholar 

  • 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 Hortic Sci 129:237–243

    CAS  Google Scholar 

  • Zraidi A, Stift G, Pachner M, Shojaeiyan A, Gong L, Lelley T (2007) A consensus map for Cucurbita pepo. Mol Breed 20:375–388

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Damian Jaccoud and Haitao Xiang for providing the SNP data and answering questions about data analysis. This research was supported by Grants from the China Postdoctoral Science Foundation (2013M541624), Jiangsu Province Postdoctoral Science Foundation (1301068B) and the Jiangsu Provincial Major Support Program for Agriculture (BE2012323).

Author information

Authors and Affiliations

  1. Institute of Vegetable Crops, Jiangsu Academy of Agricultural Sciences, 50 Zhongling Street, Nanjing, 210014, China

    Runsheng Ren, Pingfang Li, Jinhua Xu, Man Zhang, Guang Liu, Xiefeng Yao & Xingping Yang

  2. Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, LE12 5RD, UK

    Runsheng Ren & Rumiana Ray

  3. DArT P/L, PO Box 7141, Yarralumla, Canberra, ACT, 2600, Australia

    Andrzej Kilian

Authors
  1. Runsheng Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rumiana Ray
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pingfang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jinhua Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Man Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Guang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiefeng Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Andrzej Kilian
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Xingping Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xingping Yang.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Table 1. The number of SNP in each bin marker (XLS) (XLSX 32 kb)

438_2015_997_MOESM2_ESM.xlsx

Supplementary Table 2. Bin markers used to construct the genetic map of watermelon. Their chromosome, bin position, genetic distance, marker name, bin marker start, bin marker end and bin marker length are listed.(XLS) (XLSX 58 kb)

Supplementary Table 3. The genetic map of K3 × PI 189225 144 individuals F2 population.(XLS) (XLSX 42 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ren, R., Ray, R., Li, P. 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 290, 1457–1470 (2015). https://doi.org/10.1007/s00438-015-0997-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-015-0997-7

Keywords

Search

Navigation