Theoretical and Applied Genetics

, Volume 127, Issue 3, pp 731–748 | Cite as

Identification of agronomically important QTL in tetraploid potato cultivars using a marker–trait association analysis

  • Björn B. D’hoop
  • Paul L. C. Keizer
  • M. João Paulo
  • Richard G. F. Visser
  • Fred A. van Eeuwijk
  • Herman J. van EckEmail author
Original Paper


Key message

Nineteen tuber quality traits in potato were phenotyped in 205 cultivars and 299 breeder clones. Association analysis using 3364 AFLP loci and 653 SSR-alleles identified QTL for these traits.


Two association mapping panels were analysed for marker–trait associations to identify quantitative trait loci (QTL). The first panel comprised 205 historical and contemporary tetraploid potato cultivars that were phenotyped in field trials at two locations with two replicates (the academic panel). The second panel consisted of 299 potato cultivars and included recent breeds obtained from five Dutch potato breeding companies and reference cultivars (the industrial panel). Phenotypic data for the second panel were collected during subsequent clonal selection generations at the individual breeding companies. QTL were identified for 19 agro-morphological and quality traits. Two association mapping models were used: a baseline model without, and a more advanced model with correction for population structure and genetic relatedness. Correction for population structure and genetic relatedness was performed with a kinship matrix estimated from marker information. The detected QTL partly not only confirmed previous studies, e.g. for tuber shape and frying colour, but also new QTL were found like for after baking darkening and enzymatic browning. Pleiotropic effects could be discerned for several QTL.


Quantitative Trait Locus Association Mapping Phenotypic Analysis Flesh Colour Trait Association 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Agrico Research B. V. (Bant, Netherlands), Averis Seeds B. V. (Valthermond, Netherlands), C. Meijer B. V. (Rilland, Netherlands), HZPC Holland B. V. (Metslawier, Netherlands) and KWS Potato B. V. (Emmeloord, Netherlands) for providing tuber material, sharing phenotypic data and for their help in the academic trial. We acknowledge the genebanks Agriculture and Agri-Food (Canada), Arche Noah (Austria), IPK Gatersleben (Germany), INRA (France), SASA (Scotland), Teagasc (Ireland) and USDA-ARS (USA) for providing scarce heirloom potato cultivars. This study was financed as project P8 and PP2 by the Centre for BioSystems Genomics (CBSG), which is part of the Netherlands Genomics Initiative, Netherlands Organization for Scientific Research for financing this study. Fred van Eeuwijk and Paul Keizer worked wholly and João Paulo partially on this paper within the context of the CBSG projects BB9 and BB12.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

122_2013_2254_MOESM1_ESM.xls (44 kb)
Table S1. Marker–trait associations detected with the academic panel and 720 mapped AFLPs. In the left part, the associations identified with the baseline model are listed and to the right the ones found with the advanced model. The observed significance “-10logp”, the chromosome, the map position in cM and the marker name are presented as well. (XLS 44 kb)
122_2013_2254_MOESM2_ESM.xls (72 kb)
Table S2. Marker–trait associations detected with the industrial panel and 720 mapped AFLPs. In the left part, the associations identified with the baseline model are listed, and to the right the ones found with the advanced model. The observed significance “-10logp”, the chromosome, the map position in cM and the marker name are presented as well. (XLS 72 kb)
122_2013_2254_MOESM3_ESM.xls (80 kb)
Table S3. Marker–trait associations detected with the academic panel and the comprehensive set. In the left part, the associations identified with the baseline model are listed, and to the right the ones found with the advanced model. The observed significance “- 10logp”, the marker number and the marker name are presented as well. (XLS 80 kb)
122_2013_2254_MOESM4_ESM.xls (227 kb)
Table S4. Marker–trait associations detected with the industrial panel and the comprehensive set. In the left part, the associations identified with the baseline model are listed, and to the right the ones found with the advanced model. The observed significance “- 10logp”, the marker number and the marker name are presented as well. (XLS 227 kb)
122_2013_2254_MOESM5_ESM.docx (14 kb)
Table S5. Marker–trait associations found with 53 microsatellites. (DOCX 13 kb)


  1. Alonso-Blanco C, Blankestijn de Vries H, Hanhart CJ, Koornneef M (1999) Natural allelic variation at seed size loci in relation to other life history traits of Arabidopsis thaliana. Proc Natl Acad Sci USA 96:4710–4717PubMedCrossRefGoogle Scholar
  2. Aranzana MJ, Kim S, Zhao K, Bakker E, Horton M et al (2005) Genome-wide association mapping in Arabidopsis identifies previously known flowering time and pathogen resistance genes. PLoS Genet 1:e60PubMedCentralPubMedCrossRefGoogle Scholar
  3. Bachem CWB, Speckmann G-J, van der Linde PCG, Verheggen FTM, Hunt MD et al (1994) Antisense expression of polyphenol oxidase genes inhibits enzymatic browning in potato tubers. Nat Biotechnol 12:1101–1105CrossRefGoogle Scholar
  4. Bonierbale MW, Plaisted RL, Tanksley SD (1988) RFLP maps based on a common set of clones reveal modes of chromosomal evolution in potato and tomato. Genetics 120:1095–1103PubMedGoogle Scholar
  5. Bradshaw JE, Pande B, Bryan GJ, Hackett CA, McLean K et al (2004) Interval mapping of quantitative trait loci for resistance to late blight [Phytophthora infestans (Mont.) de Bary], height and maturity in a tetraploid population of potato (Solanum tuberosum subsp tuberosum). Genetics 168:983–995PubMedCrossRefGoogle Scholar
  6. Bradshaw JE, Hackett CA, Pande B, Waugh R, Bryan GJ (2008) QTL mapping of yield, agronomic and quality traits in tetraploid potato (Solanum tuberosum subsp tuberosum). Theor Appl Genet 116:193–211PubMedCrossRefGoogle Scholar
  7. Breseghello F, Sorrells ME (2006a) Association analysis as a strategy for improvement of quantitative traits in plants. CropSci 46:1323–1330Google Scholar
  8. Breseghello F, Sorrells ME (2006b) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1177PubMedCrossRefGoogle Scholar
  9. Caldwell KS, Russell J, Langridge P, Powell W (2006) Extreme population-dependent linkage disequilibrium detected in an inbreeding plant species, Hordeum vulgare. Genetics 172:557–567PubMedCrossRefGoogle Scholar
  10. Chen X, Salamini F, Gebhardt C (2001) A potato molecular-function map for carbohydrate metabolism and transport. Theor Appl Genet 102:284–295CrossRefGoogle Scholar
  11. Cockram J, White J, Leigh FJ, Lea VJ, Chiapparino E et al (2008) Association mapping of partitioning loci in barley. BMC Genet 9:16PubMedCentralPubMedCrossRefGoogle Scholar
  12. Collins A, Milbourne D, Ramsay L, Meyer R, Chatot-Balandras C, Oberhagemann P, De Jong W, Gebhardt C, Bonnel E, Waugh R (1999) QTL for field resistance to late blight in potato are strongly correlated with maturity and vigour. Mol Breed 5:387–398CrossRefGoogle Scholar
  13. D’hoop BB, Paulo MJ, Mank R, van Eck HJ, van Eeuwijk FA (2008) Association mapping of quality traits in potato (Solanum tuberosum L.). Euphytica 161:47–60CrossRefGoogle Scholar
  14. D’hoop BB, Paulo MJ, Kowitwanich K, Sengers M, Visser RGF et al (2010) Population structure and linkage disequilibrium unravelled in tetraploid potato. Theor Appl Genet 121:1151–1170PubMedCentralPubMedCrossRefGoogle Scholar
  15. D’hoop BB, Paulo MJ, Visser RGF, van Eck HJ, van Eeuwijk FA (2011) Phenotypic analyses of multi-environment data for two diverse tetraploid potato collections; comparing an academic panel with an industrial panel. Potato Res 54:157–181CrossRefGoogle Scholar
  16. Douches DS, Freyre R (1994) Identification of genetic factors influencing chip color in diploid potato (Solanum spp). Am Potato J 71:581–590CrossRefGoogle Scholar
  17. Ersoz ES, Yu J, Buckler ES (2007) Applications of linkage disequilibrium and association mapping in crop plants. In: Varshney RK, Tuberosa R (eds) Genomics-assisted crop improvement. Springer Verlag, Germany, pp 97–119CrossRefGoogle Scholar
  18. Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374PubMedCrossRefGoogle Scholar
  19. Fischer M, Schreiber L, Colby T, Kuckenberg M, Tacke E, Hofferbert H-R, Schmidt J, Gebhardt C (2013) Novel candidate genes influencing natural variation in potato tuber cold sweetening identified by comparative proteomics and association mapping. BMC Plant Biol 13(1):113PubMedCentralPubMedCrossRefGoogle Scholar
  20. Gebhardt C, Ballvora A, Walkemeier B, Oberhagemann P, Schuler K (2004) Assessing genetic potential in germplasm collections of crop plants by marker–trait association: a case study for potatoes with quantitative variation of resistance to late blight and maturity type. Mol Breed 13:93–102CrossRefGoogle Scholar
  21. Gebhardt C, Menendez CM, Chen X, Li L, Schäfer-Pregl R et al (2005) Genomic approaches for the improvement of tuber quality traits in potato. Acta Hortic 684:85–92Google Scholar
  22. Goddard ME, Hayes BJ (2009) Mapping genes for complex traits in domestic animals and their use in breeding programmes. Nat Rev Genet 10:381–391PubMedCrossRefGoogle Scholar
  23. Gupta PK, Rustgi S, Kulwal PL (2005) Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Mol Biol 57:461–485PubMedCrossRefGoogle Scholar
  24. Haase N (2003) Estimation of dry matter and starch concentration in potatoes by determination of underwater weight and near infrared spectroscopy. Potato Res 46:117–127CrossRefGoogle Scholar
  25. Jacobs JME, van Eck HJ, Arens P, Verkerk-Bakker B, Lintel Hekkert B et al (1995) A genetic map of potato (Solanum tuberosum) integrating molecular markers, including transposons, and classical markers. Theor Appl Genet 91:289–300PubMedCrossRefGoogle Scholar
  26. Jannink JL, Walsh B (2002) Association mapping in plant populations. In: Kang MS (ed) Quantitative genetics, genomics and plant breeding, chap 5. CABI, UK, pp 59–68 Google Scholar
  27. Kang HM, Zaitlen NA, Wade CM, Kirby A, Heckerman D et al (2008) Efficient control of population structure in model organism association mapping. Genetics 178:1709–1723PubMedCrossRefGoogle Scholar
  28. Khu DM, Lorenzen J, Hackett CA, Love SL (2008) Interval mapping of quantitative trait loci for corky ringspot disease resistance in a tetraploid population of potato (Solanum tuberosum subsp tuberosum). Am J Potato Res 85:129–139CrossRefGoogle Scholar
  29. Kloosterman B, Oortwijn M, Uitdewilligen J, America T, de Vos R et al (2010) From QTL to candidate gene: genetical genomics of simple and complex traits in potato using a pooling strategy. BMC Genom 11:158CrossRefGoogle Scholar
  30. Kloosterman B, Abelenda JA, del Mar Carretero Gomez M, Oortwijn M, de Boer JM, Kowitwanich K, Horvath BM, van Eck HJ, Smaczniak C, Prat S, Visser RGF, Bachem CWB (2013) Naturally occurring allele diversity allows potato cultivation in northern latitudes. Nature 495(7440):246–250PubMedCrossRefGoogle Scholar
  31. Kraakman ATW, Niks RE, van den Berg PMMM, Stam P, van Eeuwijk FA (2004) Linkage disequilibrium mapping of yield and yield stability in modern spring barley cultivars. Genetics 168:435–446PubMedCrossRefGoogle Scholar
  32. Kraft T, Hansen M, Nilsson N-O (2000) Linkage disequilibrium and fingerprinting in sugar beet. Theor Appl Genet 101:323–326CrossRefGoogle Scholar
  33. Lærke PE, Christiansen J, Veierskov B (2002) Colour of blackspot bruises in potato tubers during growth and storage compared to their discolouration potential. Postharvest Biol Technol 26:99–111CrossRefGoogle Scholar
  34. Li L, Strahwald J, Hofferbert HR, Lubeck J, Tacke E et al (2005) DNA variation at the invertase locus invGE/GF is associated with tuber quality traits in populations of potato breeding clones. Genetics 170:813–821PubMedCrossRefGoogle Scholar
  35. Li L, Paulo MJ, Strahwald J, Lübeck J, Hofferbert HR et al (2008) Natural DNA variation at candidate loci is associated with potato chip color, tuber starch content, yield and starch yield. Theor Appl Genet 116:1167–1181PubMedCentralPubMedCrossRefGoogle Scholar
  36. Li L, Tacke E, Hofferbert H-R, Lübeck J, Strahwald J, Draffehn AM, Walkemeier B, Gebhardt C (2013) Validation of candidate gene markers for marker-assisted selection of potato cultivars with improved tuber quality. Theor Appl Genet 126(4):1039–1052PubMedCentralPubMedCrossRefGoogle Scholar
  37. Lindhout P, Meijer D, Schotte T, Hutten RCB, Visser RGF, van Eck HJ (2011) Towards F1 hybrid seed potato breeding. Potato Res 54(4):301–312Google Scholar
  38. Lu H, Redus MA, Coburn JR, Rutger JN, McCouch SR et al (2005) Population structure and breeding patterns of 145 US rice cultivars based on SSR marker analysis. CropSci 45:66–76Google Scholar
  39. Maccaferri M, Sanguineti MC, Noli E, Tuberosa R (2005) Population structure and long-range linkage disequilibrium in a durum wheat elite collection. Mol Breed 15:271–289CrossRefGoogle Scholar
  40. Mackay I, Powell W (2007) Methods for linkage disequilibrium mapping in crops. Trends Plant Sci 12:57–63PubMedCrossRefGoogle Scholar
  41. Malosetti M, van der Linden CG, Vosman B, van Eeuwijk FA (2007) A mixed-model approach to association mapping using pedigree information with an illustration of resistance to Phytophthora infestans in potato. Genetics 175:879–889PubMedCrossRefGoogle Scholar
  42. Maris B (1969) Studies on maturity, yield, underwater weight and some other characters of potato progenies. Euphytica 18:297–319CrossRefGoogle Scholar
  43. Mather KA, Caicedo AL, Polato NR, Olsen KM, McCouch S et al (2007) The extent of linkage disequilibrium in rice (Oryza sativa L.). Genetics 177:2223–2232PubMedCrossRefGoogle Scholar
  44. Menendez CM, Ritter E, Schäfer-Pregl R, Walkemeier B, Kalde A et al (2002) Cold sweetening in diploid potato: mapping quantitative trait loci and candidate genes. Genetics 162:1423–1434PubMedGoogle Scholar
  45. Montgomery DC, Peck EA, Vining GG (2001) Introduction to linear regression analysis. John Wiley & Sons Inc., New York, p 641Google Scholar
  46. Nordborg M, Tavare S (2002) Linkage disequilibrium: what history has to tell us. Trends Genet 18:83–90PubMedCrossRefGoogle Scholar
  47. Nordborg M, Borevitz JO, Bergelson J, Berry CC, Chory J et al (2002) The extent of linkage disequilibrium in Arabidopsis thaliana. Nat Genet 30:190–193PubMedCrossRefGoogle Scholar
  48. Parisseaux B, Bernardo R (2004) In silico mapping of quantitative trait loci in maize. Theor Appl Genet 109:508–514PubMedCrossRefGoogle Scholar
  49. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  50. Raboin L-M, Pauquet J, Butterfield M, D’Hont A, Glaszmann J-C (2008) Analysis of genome wide linkage disequilibrium in the highly polyploid sugarcane. Theor Appl Genet 116:701–714PubMedCrossRefGoogle Scholar
  51. Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR et al (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci USA 98:11479–11484PubMedCrossRefGoogle Scholar
  52. Simko I, Costanzo S, Haynes KG, Christ BJ, Jones RW (2004a) Linkage disequilibrium mapping of a Verticillium dahliae resistance quantitative trait locus in tetraploid potato (Solanum tuberosum) through a candidate gene approach. Theor Appl Genet 108:217–224PubMedCrossRefGoogle Scholar
  53. Simko I, Haynes KG, Ewing EE, Costanzo S, Christ BJ et al (2004b) Mapping genes for resistance to Verticillium albo-atrum in tetraploid and diploid potato populations using haplotype association tests and genetic linkage analysis. Mol Genet Genomics 271:522–531PubMedCrossRefGoogle Scholar
  54. Sliwka J, Wasilewicz-Flis I, Jakuczun H, Gebhardt C (2008) Tagging quantitative trait loci for dormancy, tuber shape, regularity of tuber shape, eye depth and flesh colour in diploid potato originated from six Solanum species. Plant Breed 127:49–55CrossRefGoogle Scholar
  55. Sørensen KK, Madsen MH, Kirk HG, Madsen DK, Torp AM (2006) Linkage and quantitative trait locus mapping of foliage late blight resistance in the wild species Solanum vernei. Plant Breed 125:268–276CrossRefGoogle Scholar
  56. Stich B, Melchinger A, Heckenberger M, Möhring J, Schechert A, Piepho H-P (2008a) Association mapping in multiple segregating populations of sugar beet (Beta vulgaris L.). Theor Appl Genet 117:1167–1179PubMedCrossRefGoogle Scholar
  57. Stich B, Möhring J, Piepho H-P, Heckenberger M, Buckler ES et al (2008b) Comparison of mixed-model approaches for association mapping. Genetics 178:1745–1754PubMedCrossRefGoogle Scholar
  58. Stich B, Piepho H-P, Schulz B, Melchinger A (2008c) Multi-trait association mapping in sugar beet (Beta vulgaris L.). Theor Appl Genet 117:947–954PubMedCrossRefGoogle Scholar
  59. Thomas WTB, Powell W, Waugh R, Chalmers KJ, Barua UM, Jack P, Lea V, Forster BP, Swanston JS, Ellis RP, Hanson PR, Lance RCM (1995) Detection of quantitative trait loci for agronomic, yield, grain and disease characters in spring barley (Hordeum vulgare L.). Theor Appl Genet 91:1037–1047PubMedGoogle Scholar
  60. Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D et al (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286–289PubMedCrossRefGoogle Scholar
  61. Urbany C, Stich B, Schmidt L, Simon L, Berding H, Junghans H, Niehoff K-H, Braun A, Tacke E, Hofferbert H-R, Lübeck J, Strahwald J, Gebhardt C (2011) Association genetics in Solanum tuberosum provides new insights into potato tuber bruising and enzymatic tissue discoloration. BMC Genom 12:7CrossRefGoogle Scholar
  62. Van der Beek JG, Verkerk R, Zabel P, Lindhout P (1992) Mapping strategy for resistance genes in tomato based on RFLPs between cultivars: Cf9 (resistance to Cladosporium fulvum) on chromosome 1. Theor Appl Genet 84:106–112PubMedCrossRefGoogle Scholar
  63. Van Eck HJ, Jacobs JME, Stam P, Ton J, Stiekema WJ et al (1994a) Multiple alleles for tuber shape in diploid potato detected by qualitative and quantitative genetic analysis using RFLPs. Genetics 137:303–309PubMedGoogle Scholar
  64. Van Eck HJ, Jacobs JME, van den Berg PMMM, Stiekema WJ, Jacobsen E (1994b) The inheritance of anthocyanin pigmentation in potato (Solanum tuberosum L.) and mapping of tuber skin colour loci using RFLPs. Heredity 73:410–421CrossRefGoogle Scholar
  65. Van Os H, Andrzejewski S, Bakker E, Barrena I, Bryan GJ et al (2006) Construction of a 10,000-marker ultradense genetic recombination map of potato: providing a framework for accelerated gene isolation and a genomewide physical map. Genetics 173:1075–1087PubMedCrossRefGoogle Scholar
  66. Van Zanten M, Snoek LB, Proveniers MCG, Peeters AJM (2009) The many functions of ERECTA. Trends Plant Sci 14:214–218PubMedCrossRefGoogle Scholar
  67. Verbeke G, Molenberghs G (2000) Mixed models for longitudinal data. Springer, Berlin, p 568Google Scholar
  68. Visker MHPW, Keizer LCP, van Eck HJ, Jacobsen E, Colon LT et al (2003) Can the QTL for late blight resistance on potato chromosome 5 be attributed to foliage maturity type? Theor Appl Genet 106:317–325PubMedGoogle Scholar
  69. Visker MHPW, Heilersig HJB, Kodde LP, van de Weg WE, Voorrips RE et al (2005) Genetic linkage of QTLs for late blight resistance and foliage maturity type in six related potato progenies. Euphytica 143:189–199CrossRefGoogle Scholar
  70. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T et al (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414PubMedCentralPubMedCrossRefGoogle Scholar
  71. Wang J, McClean PE, Lee R, Goos RJ, Helms T (2008) Association mapping of iron deficiency chlorosis loci in soybean (Glycine max L. Merr.) advanced breeding lines. Theor Appl Genet 116:777–787PubMedCrossRefGoogle Scholar
  72. Wang-Pruski G, Nowak J (2004) Potato after-cooking darkening. Am J Potato Res 81:7–16CrossRefGoogle Scholar
  73. Werij JS, Kloosterman B, Celis-Gamboa C, de Vos CHR, America T et al (2007) Unravelling enzymatic discolouration in potato through a combined approach of candidate genes, QTL, and expression analysis. Theor Appl Genet 115:245–252PubMedCentralPubMedCrossRefGoogle Scholar
  74. Wolters A-M, Uitdewilligen J, Kloosterman B, Hutten RCB, Visser RGF et al (2010) Identification of alleles of carotenoid pathway genes important for zeaxanthin accumulation in potato tubers. Plant Mol Biol 73:659–671PubMedCentralPubMedCrossRefGoogle Scholar
  75. Yu J, Pressoir G, Briggs WH, Vroh BI, Yamasaki M et al (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208PubMedCrossRefGoogle Scholar
  76. Zhao J, Paulo MJ, Jamar D, Lou P, van Eeuwijk FA et al (2007a) Association mapping of leaf traits, flowering time, and phytate content in Brassica rapa. Genome 50:963–973PubMedCrossRefGoogle Scholar
  77. Zhao KY, Aranzana MJ, Kim S, Lister C, Shindo C et al (2007b) An Arabidopsis example of association mapping in structured samples. PLoS Genet 3:e4PubMedCentralPubMedCrossRefGoogle Scholar
  78. Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. Plant Genome 1:5–20CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Björn B. D’hoop
    • 1
    • 2
    • 3
  • Paul L. C. Keizer
    • 4
  • M. João Paulo
    • 1
    • 3
    • 4
  • Richard G. F. Visser
    • 1
    • 2
    • 3
  • Fred A. van Eeuwijk
    • 3
    • 4
  • Herman J. van Eck
    • 1
    • 2
    • 3
    Email author
  1. 1.Plant BreedingWageningen University and Research CentreWageningenThe Netherlands
  2. 2.Graduate School of Experimental Plant SciencesWageningenThe Netherlands
  3. 3.Centre for BioSystems Genomics (CBSG)WageningenThe Netherlands
  4. 4.BiometrisWageningen University and Research CentreWageningenThe Netherlands

Personalised recommendations