Theoretical and Applied Genetics

, Volume 126, Issue 6, pp 1431–1443 | Cite as

Identification of quantitative trait loci for resistance to Verticillium wilt and yield parameters in hop (Humulus lupulus L.)

  • Jernej Jakse
  • Andreja Cerenak
  • Sebastjan Radisek
  • Zlatko Satovic
  • Zlata Luthar
  • Branka JavornikEmail author
Original Paper


Verticillium wilt (VW) can cause substantial yield loss in hop particularly with the outbreaks of the lethal strain of Verticillium albo-atrum. To elucidate genetic control of VW resistance in hop, an F1 mapping population derived from a cross of cultivar Wye Target, with the predicted genetic basis of resistance, and susceptible male breeding line BL2/1 was developed to assess wilting symptoms and to perform QTL mapping. The genetic linkage map, constructed with 203 markers of various types using a pseudo-testcross strategy, formed ten major linkage groups (LG) of the maternal and paternal maps, covering 552.98 and 441.1 cM, respectively. A significant QTL for VW resistance was detected at LOD 7 on a single chromosomal region on LG03 of both parental maps, accounting for 24.2–26.0 % of the phenotypic variance. QTL analysis for alpha-acid content and yield parameters was also performed on this map. QTLs for these traits were also detected and confirmed our previously detected QTLs in a different pedigree and environment. The work provides the basis for exploration of QTL flanking markers for possible use in marker-assisted selection.


Quantitative Trait Locus Quantitative Trait Locus Analysis Harvest Index Verticillium Wilt Flank Marker 
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.



The authors acknowledge funding by the Slovenian Research Agency, research program Grant no. P4-0077. We thank Dr. Stefan Seefelder from Bayerische Landesanstalt für Landwirtschaft, Institut für Pflanzenbau und Pflanzenzüchtung, Freising, for kindly providing primer sequences for microsatellite markers of the Ho series.


  1. Analytica EBC/European brewery convention (2000) Nuernberg, EBC Analysis Committe–Nuernberg, Carl, Hans, Getränke–Fadverl. Grundwerk: Section 7Google Scholar
  2. Araki S, Tsuchiya Y, Takashio M, Tamaki T, Shinotsuka K (1998) Identification of hop cultivars by DNA marker analysis. J Am Soc Brew Chem 56:93–98Google Scholar
  3. Bae J, Halterman D, Jansky S (2008) Development of a molecular marker associated with Verticillium wilt resistance in diploid interspecific potato hybrids. Mol Breed 22:61–69CrossRefGoogle Scholar
  4. Bolek Y, El-Zik KM, Pepper AE, Bell AA, Magill CW, Thaxton PM, Reddy OUK (2005) Mapping of verticillium wilt resistance genes in cotton. Plant Sci 168:1581–1590CrossRefGoogle Scholar
  5. Brady JL, Scott NS, Thomas MR (1996) DNA typing of hops (Humulus lupulus) through application of RAPD and microsatellite marker sequences converted to sequence tagged sites (STS). Euphytica 91:277–284CrossRefGoogle Scholar
  6. Cerenak A, Satovic Z, Javornik B (2006) Genetic mapping of hop (Humulus lupulus L.) applied to the detection of QTLs for alpha-acid content. Genome 49:485–494PubMedCrossRefGoogle Scholar
  7. Cerenak A, Satovic Z, Jakse J, Luthar Z, Carovic-Stanko K, Javornik B (2009) Identification of QTLs for alpha acid content and yield in hop (Humulus lupulus L.). Euphytica 170:141–154CrossRefGoogle Scholar
  8. Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971PubMedGoogle Scholar
  9. Clarkson JM, Heale JB (1985) Pathogenicity and colonization studies on wild-type and auxotrophic isolates of Verticillium-albo-atrum from hop. Plant Pathol 34:119–128CrossRefGoogle Scholar
  10. Conneally PM, Edwards JH, Kidd KK, Lalouel JM, Morton NE, Ott J, White R (1985) Report of the committee on methods of linkage analysis and reporting. Cytogenet Cell Genet 40:356–359PubMedCrossRefGoogle Scholar
  11. Darby P (2001) Single gene traits in hop breeding. In: Seigner E (ed) Scientific Commission of the International Hop Growers Convention IHGC. Canterbury, UK, pp 76–80Google Scholar
  12. de Jonge R, van Esse HP, Maruthachalam K, Bolton MD, Santhanam P, Saber MK, Zhang Z, Usami T, Lievens B, Subbarao KV, Thomma B (2012) Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc Natl Acad Sci USA 109:5110–5115PubMedCrossRefGoogle Scholar
  13. Diwan N, Fluhr R, Eshed Y, Zamir D, Tanksley SD (1999) Mapping of Ve in tomato: a gene conferring resistance to the broad-spectrum pathogen, Verticillium dahliae race 1. Theor Appl Genet 98:315–319CrossRefGoogle Scholar
  14. Fradin EF, Zhang Z, Ayala JCJ, Castroverde CDM, Nazar RN, Robb J, Liu CM, Thomma B (2009) Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol 150:320–332PubMedCrossRefGoogle Scholar
  15. Gillet E, Gregorius HR (1992) What can be inferred from open-pollination progenies about the source of observed segregation distortion? A case-study in Castanea sativa Mill. Silvae Genet 41:82–87Google Scholar
  16. Grattapaglia D, Sederoff R (1994) Genetic-linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:1121–1137PubMedGoogle Scholar
  17. Gril T, Celar F, Munda A, Javornik B, Jakse J (2008) AFLP analysis of intraspecific variation between Monilinia laxa isolates from different hosts. Plant Dis 92:1616–1624CrossRefGoogle Scholar
  18. Hadonou AM, Walden R, Darby P, Darby W (2004) Isolation and characterization of polymorphic microsatellites for assessment of genetic variation of hops (Humulus lupulus L.). Mol Ecol Notes 4:280–282CrossRefGoogle Scholar
  19. Hayes RJ, McHale LK, Vallad GE, Truco MJ, Michelmore RW, Klosterman SJ, Maruthachalam K, Subbarao KV (2011) The inheritance of resistance to Verticillium wilt caused by race 1 isolates of Verticillium dahliae in the lettuce cultivar La Brillante. Theor Appl Genet 123:509–517PubMedCrossRefGoogle Scholar
  20. Henning JA, Townsend MS, Gent DH, Bassil N, Matthews P, Buck E, Beatson R (2011) QTL mapping of powdery mildew susceptibility in hop (Humulus lupulus L.). Euphytica 180:411–420CrossRefGoogle Scholar
  21. Isaac I, Keyworth WG (1948) Verticillium wilt of the hop (Humulus lupulus). Ann Appl Biol 35:243–249CrossRefGoogle Scholar
  22. Jakse J, Bandelj D, Javornik B (2002) Eleven new microsatellites for hop (Humulus lupulus L.). Mol Ecol Notes 2:544–546CrossRefGoogle Scholar
  23. Jakse J, Luthar Z, Javornik B (2008a) New polymorphic dinucleotide and trinucleotide microsatellite loci for hop Humulus lupulus L. Mol Ecol Resour 8:769–772PubMedCrossRefGoogle Scholar
  24. Jakse J, Stajner N, Kozjak P, Cerenak A, Javornik B (2008b) Trinucleotide microsatellite repeat is tightly linked to male sex in hop (Humulus lupulus L.). Mol Breed 21:139–148CrossRefGoogle Scholar
  25. Jakse J, Stajner N, Luthar Z, Jeltsch JM, Javornik B (2011) Development of transcript-associated microsatellite markers for diversity and linkage mapping studies in hop (Humulus lupulus L.). Mol Breed 28:227–239CrossRefGoogle Scholar
  26. Jansen RC, Stam P (1994) High-resolution of quantitative traits into multiple loci via interval mapping. Genetics 136:1447–1455PubMedGoogle Scholar
  27. Jansky S, Rouse DI, Kauth PJ (2004) Inheritance of resistance to Verticillium dahliae in diploid interspecific potato hybrids. Plant Dis 88:1075–1078CrossRefGoogle Scholar
  28. Jiang F, Zhao J, Zhou L, Guo WZ, Zhang TZ (2009) Molecular mapping of Verticillium wilt resistance QTL clustered on chromosomes D7 and D9 in upland cotton. Sci China Life Sci 52:872–884CrossRefGoogle Scholar
  29. Kanai D, Kirita M, Sakamoto K (2006) Method for judging kind of hop using microsatellite DNA. Japan Patent 2006-034142. Asahi Breweries LTD, JapanGoogle Scholar
  30. Kawchuk LM, Hachey J, Lynch DR, Kulcsar F, van Rooijen G, Waterer DR, Robertson A, Kokko E, Byers R, Howard RJ, Fischer R, Prufer D (2001) Tomato Ve disease resistance genes encode cell surface-like receptors. Proc Natl Acad Sci USA 98:6511–6515PubMedCrossRefGoogle Scholar
  31. Keyworth WG (1942) Verticillium wilt of the hop (Humulus lupulus). Ann Appl Biol 29:346–357CrossRefGoogle Scholar
  32. Knott SA, Neale DB, Sewell MM, Haley CS (1997) Multiple marker mapping of quantitative trait loci in an outbred pedigree of loblolly pine. Theor Appl Genet 94:810–820CrossRefGoogle Scholar
  33. Koie K, Inaba A, Okada Y, Kaneko T, Ito K (2005) Construction of the genetic linkage map and QTL analysis on hop (Humulus lupulus L.) In: Hummer KE, Henning JA (eds) ISHS Acta Horticulturae 668: I International Humulus Symposium. ISHS, Corvallis (Oregon), USA, pp 59–66Google Scholar
  34. Kozjak P, Jakse J, Javornik B (2009) Isolation and sequence analysis of NBS-LRR disease resistance gene analogues from hop Humulus lupulus L. Plant Sci 176:775–782CrossRefGoogle Scholar
  35. Kump B, Javornik B (1996) Evaluation of genetic variability among common buckwheat (Fagopyrum esculentum Moench) populations by RAPD markers. Plant Sci 114:149–158CrossRefGoogle Scholar
  36. Lander ES, Botstein D (1989) Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199PubMedGoogle Scholar
  37. Lu H, Romero-Severson J, Bernardo R (2002) Chromosomal regions associated with segregation distortion in maize. Theor Appl Genet 105:622–628PubMedCrossRefGoogle Scholar
  38. Matousek J, Kocabek T, Patzak J, Fussy Z, Prochazkova J, Heyerick A (2012) Combinatorial analysis of lupulin gland transcription factors from R2R3Myb, bHLH and WDR families indicates a complex regulation of chs_H1 genes essential for prenylflavonoid biosynthesis in hop (Humulus Lupulus L.). BMC Plant Biol 12:27PubMedCrossRefGoogle Scholar
  39. Mert M, Kurt S, Gencer O, Akiscan Y, Boyaci K, Tok FM (2005) Inheritance of resistance to Verticillium wilt (Verticillium dahliae) in cotton (Gossypium hirsutum L.). Plant Breed 124:102–104CrossRefGoogle Scholar
  40. Neve RA (1991) Hops. Chapman and Hall, LondonGoogle Scholar
  41. Novak P, Matousek J, Briza J (2003) Valerophenone synthase-like chalcone synthase homologues in Humulus lupulus. Biol Plant 46:375–381CrossRefGoogle Scholar
  42. Okada Y, Sugimoto M, Ito K (2001) Molecular cloning and expression of farnesyl pyrophosphate synthase gene responsible for essential oil biosynthesis in hop (Humulus lupulus). J Plant Physiol 158:1183–1188CrossRefGoogle Scholar
  43. Paniego NB, Zuurbier KWM, Fung SY, van der Heijden R, Scheffer JJC, Verpoorte R (1999) Phlorisovalerophenone synthase, a novel polyketide synthase from hop (Humulus lupulus L.) cones. Eur J Biochem 262:612–616PubMedCrossRefGoogle Scholar
  44. Patzak J, Vejl P, Skupinova S, Newadba V (2002) Identification of sex in F1 progenies of hop (Humulus lupulus L.) by molecular marker. Rost Vyroba 48:318–321Google Scholar
  45. Polley A, Seigner E, Ganal MW (1997) Identification of sex in hop (Humulus lupulus) using molecular markers. Genome 40:357–361PubMedCrossRefGoogle Scholar
  46. Radisek S, Jakse J, Simoncic A, Javornik B (2003) Characterization of Verticillium albo-atrum field isolates using pathogenicity data and AFLP analysis. Plant Dis 87:633–638CrossRefGoogle Scholar
  47. Radisek S, Jakse J, Javornik B (2006) Genetic variability and virulence among Verticillium albo-atrum isolates from hop. Eur J Plant Pathol 116:301–314CrossRefGoogle Scholar
  48. Rygulla W, Snowdon RJ, Friedt W, Happstadius I, Cheung WY, Chen D (2008) Identification of quantitative trait loci for resistance against Verticillium longisporum in oilseed rape (Brassica napus). Phytopathology 98:215–221PubMedCrossRefGoogle Scholar
  49. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234PubMedCrossRefGoogle Scholar
  50. Seefelder S, Ehrmaier H, Schweizer G, Seigner E (2000) Male and female genetic linkage map of hops, Humulus lupulus. Plant Breed 119:249–255CrossRefGoogle Scholar
  51. Seefelder S, Lutz A, Seigner E (2006) Development of molecular markers for powdery mildew resistance to support breeding for high quality hops. Monatsschrift Brauwiss 59:100–104Google Scholar
  52. Seefelder S, Seigner E, Niedermeier E, Radišek S, Javornik B (2009) Genotyping of Verticillium pathotypes in the Hallertau: Basic findings to assess the risk of Verticillium infections. In: Seigner E (ed) CICH—IHB—IHGC International Hop Growers` Convention. Leon, Spain, pp 67–69Google Scholar
  53. Semagn K, Bjornstad A, Skinnes H, Maroy AG, Tarkegne Y, William M (2006) Distribution of DArT, AFLP, and SSR markers in a genetic linkage map of a doubled-haploid hexaploid wheat population. Genome 49:545–555PubMedCrossRefGoogle Scholar
  54. Sewell GWF, Wilson JF (1984) The nature and distribution of Verticillium albo-atrum strains highly pathogenic to the hop. Plant Pathol 33:39–51CrossRefGoogle Scholar
  55. Stajner N, Jakse J, Kozjak P, Javornik B (2005) The isolation and characterisation of microsatellites in hop (Humulus lupulus L.). Plant Sci 168:213–221CrossRefGoogle Scholar
  56. Sustar-Vozlic J, Javornik B (1999) Genetic relationships in cultivars of hop, Humulus lupulus L., determined by RAPD analysis. Plant Breed 118:175–181CrossRefGoogle Scholar
  57. Van Ooijen J (2004) MapQTL® 5, Software for the mapping of quantitative trait loci in experimental populations, 5th edn. Kyazma B.V, WageningenGoogle Scholar
  58. Van Ooijen J (2006) JoinMap® 4, Software for the calculation of genetic linkage maps in experimental populations, 4th edn. Kyazma B.V, WageningenGoogle Scholar
  59. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78PubMedCrossRefGoogle Scholar
  60. Vos P, Hogers R, Bleeker M, Reijans M, Vandelee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP—a new technique for DNA-fingerprinting. Nucleic Acids Res 23:4407–4414PubMedCrossRefGoogle Scholar
  61. Yang C, Guo WZ, Li GY, Gao F, Lin SS, Zhang TZ (2008) QTLs mapping for Verticillium wilt resistance at seedling and maturity stages in Gossypium barbadense L. Plant Sci 174:290–298CrossRefGoogle Scholar
  62. Zamir D, Tadmor Y (1986) Unequal segregation of nuclear genes in plants. Bot Gazette 147:355–358CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Jernej Jakse
    • 1
  • Andreja Cerenak
    • 2
  • Sebastjan Radisek
    • 2
  • Zlatko Satovic
    • 3
  • Zlata Luthar
    • 1
  • Branka Javornik
    • 1
    Email author
  1. 1.University of Ljubljana, Biotechnical FacultyLjubljanaSlovenia
  2. 2.Slovenian Institute for Hop Research and BrewingLjubljanaSlovenia
  3. 3.University of Zagreb, Faculty of AgricultureZagrebCroatia

Personalised recommendations