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

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Abstract

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.

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References

  • Analytica EBC/European brewery convention (2000) Nuernberg, EBC Analysis Committe–Nuernberg, Carl, Hans, Getränke–Fadverl. Grundwerk: Section 7

  • Araki S, Tsuchiya Y, Takashio M, Tamaki T, Shinotsuka K (1998) Identification of hop cultivars by DNA marker analysis. J Am Soc Brew Chem 56:93–98

    CAS  Google Scholar 

  • Bae J, Halterman D, Jansky S (2008) Development of a molecular marker associated with Verticillium wilt resistance in diploid interspecific potato hybrids. Mol Breed 22:61–69

    Article  CAS  Google Scholar 

  • 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 168:1581–1590

    Article  CAS  Google Scholar 

  • 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 91:277–284

    Article  CAS  Google Scholar 

  • 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 49:485–494

    Article  PubMed  CAS  Google Scholar 

  • 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 170:141–154

    Article  CAS  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    PubMed  CAS  Google Scholar 

  • Clarkson JM, Heale JB (1985) Pathogenicity and colonization studies on wild-type and auxotrophic isolates of Verticillium-albo-atrum from hop. Plant Pathol 34:119–128

    Article  Google Scholar 

  • 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 40:356–359

    Article  PubMed  CAS  Google Scholar 

  • 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 76–80

    Google Scholar 

  • 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 109:5110–5115

    Article  PubMed  Google Scholar 

  • 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 98:315–319

    Article  CAS  Google Scholar 

  • 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 150:320–332

    Article  PubMed  CAS  Google Scholar 

  • 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 41:82–87

    Google Scholar 

  • Grattapaglia D, Sederoff R (1994) Genetic-linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:1121–1137

    PubMed  CAS  Google Scholar 

  • 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 92:1616–1624

    Article  CAS  Google Scholar 

  • 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 4:280–282

    Article  CAS  Google Scholar 

  • 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 123:509–517

    Article  PubMed  CAS  Google Scholar 

  • 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 180:411–420

    Article  Google Scholar 

  • Isaac I, Keyworth WG (1948) Verticillium wilt of the hop (Humulus lupulus). Ann Appl Biol 35:243–249

    Article  Google Scholar 

  • Jakse J, Bandelj D, Javornik B (2002) Eleven new microsatellites for hop (Humulus lupulus L.). Mol Ecol Notes 2:544–546

    Article  CAS  Google Scholar 

  • Jakse J, Luthar Z, Javornik B (2008a) New polymorphic dinucleotide and trinucleotide microsatellite loci for hop Humulus lupulus L. Mol Ecol Resour 8:769–772

    Article  PubMed  CAS  Google Scholar 

  • 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 21:139–148

    Article  CAS  Google Scholar 

  • 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 28:227–239

    Article  Google Scholar 

  • Jansen RC, Stam P (1994) High-resolution of quantitative traits into multiple loci via interval mapping. Genetics 136:1447–1455

    PubMed  CAS  Google Scholar 

  • Jansky S, Rouse DI, Kauth PJ (2004) Inheritance of resistance to Verticillium dahliae in diploid interspecific potato hybrids. Plant Dis 88:1075–1078

    Article  Google Scholar 

  • 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 52:872–884

    Article  Google Scholar 

  • Kanai D, Kirita M, Sakamoto K (2006) Method for judging kind of hop using microsatellite DNA. Japan Patent 2006-034142. Asahi Breweries LTD, Japan

  • 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 98:6511–6515

    Article  PubMed  CAS  Google Scholar 

  • Keyworth WG (1942) Verticillium wilt of the hop (Humulus lupulus). Ann Appl Biol 29:346–357

    Article  CAS  Google Scholar 

  • 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 94:810–820

    Article  Google Scholar 

  • 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 59–66

  • 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 176:775–782

    Article  CAS  Google Scholar 

  • Kump B, Javornik B (1996) Evaluation of genetic variability among common buckwheat (Fagopyrum esculentum Moench) populations by RAPD markers. Plant Sci 114:149–158

    Article  CAS  Google Scholar 

  • Lander ES, Botstein D (1989) Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199

    PubMed  CAS  Google Scholar 

  • Lu H, Romero-Severson J, Bernardo R (2002) Chromosomal regions associated with segregation distortion in maize. Theor Appl Genet 105:622–628

    Article  PubMed  CAS  Google Scholar 

  • 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 12:27

    Article  PubMed  CAS  Google Scholar 

  • 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 124:102–104

    Article  Google Scholar 

  • Neve RA (1991) Hops. Chapman and Hall, London

  • Novak P, Matousek J, Briza J (2003) Valerophenone synthase-like chalcone synthase homologues in Humulus lupulus. Biol Plant 46:375–381

    Article  CAS  Google Scholar 

  • 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 158:1183–1188

    Article  CAS  Google Scholar 

  • 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 262:612–616

    Article  PubMed  CAS  Google Scholar 

  • 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 48:318–321

    Google Scholar 

  • Polley A, Seigner E, Ganal MW (1997) Identification of sex in hop (Humulus lupulus) using molecular markers. Genome 40:357–361

    Article  PubMed  CAS  Google Scholar 

  • Radisek S, Jakse J, Simoncic A, Javornik B (2003) Characterization of Verticillium albo-atrum field isolates using pathogenicity data and AFLP analysis. Plant Dis 87:633–638

    Article  CAS  Google Scholar 

  • Radisek S, Jakse J, Javornik B (2006) Genetic variability and virulence among Verticillium albo-atrum isolates from hop. Eur J Plant Pathol 116:301–314

    Article  Google Scholar 

  • 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 98:215–221

    Article  PubMed  CAS  Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    Article  PubMed  CAS  Google Scholar 

  • Seefelder S, Ehrmaier H, Schweizer G, Seigner E (2000) Male and female genetic linkage map of hops, Humulus lupulus. Plant Breed 119:249–255

    Article  CAS  Google Scholar 

  • Seefelder S, Lutz A, Seigner E (2006) Development of molecular markers for powdery mildew resistance to support breeding for high quality hops. Monatsschrift Brauwiss 59:100–104

    Google Scholar 

  • 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 67–69

    Google Scholar 

  • 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 49:545–555

    Article  PubMed  CAS  Google Scholar 

  • Sewell GWF, Wilson JF (1984) The nature and distribution of Verticillium albo-atrum strains highly pathogenic to the hop. Plant Pathol 33:39–51

    Article  Google Scholar 

  • Stajner N, Jakse J, Kozjak P, Javornik B (2005) The isolation and characterisation of microsatellites in hop (Humulus lupulus L.). Plant Sci 168:213–221

    Article  CAS  Google Scholar 

  • Sustar-Vozlic J, Javornik B (1999) Genetic relationships in cultivars of hop, Humulus lupulus L., determined by RAPD analysis. Plant Breed 118:175–181

    Article  Google Scholar 

  • Van Ooijen J (2004) MapQTL® 5, Software for the mapping of quantitative trait loci in experimental populations, 5th edn. Kyazma B.V, Wageningen

    Google Scholar 

  • Van Ooijen J (2006) JoinMap® 4, Software for the calculation of genetic linkage maps in experimental populations, 4th edn. Kyazma B.V, Wageningen

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 23:4407–4414

    Article  PubMed  CAS  Google Scholar 

  • 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 174:290–298

    Article  CAS  Google Scholar 

  • Zamir D, Tadmor Y (1986) Unequal segregation of nuclear genes in plants. Bot Gazette 147:355–358

    Article  Google Scholar 

Download references

Acknowledgments

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.

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Authors and Affiliations

  1. University of Ljubljana, Biotechnical Faculty, Jamnikarjeva 101, 1000, Ljubljana, Slovenia

    Jernej Jakse, Zlata Luthar & Branka Javornik

  2. Slovenian Institute for Hop Research and Brewing, Zalskega Tabora 2, 3300, Ljubljana, Slovenia

    Andreja Cerenak & Sebastjan Radisek

  3. University of Zagreb, Faculty of Agriculture, Svetosimunska 25, 10000, Zagreb, Croatia

    Zlatko Satovic

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  1. Jernej Jakse
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  2. Andreja Cerenak
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  3. Sebastjan Radisek
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  4. Zlatko Satovic
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  5. Zlata Luthar
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  6. Branka Javornik
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Correspondence to Branka Javornik.

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Communicated by C. Gebhardt.

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Jakse, J., Cerenak, A., Radisek, S. et al. Identification of quantitative trait loci for resistance to Verticillium wilt and yield parameters in hop (Humulus lupulus L.). Theor Appl Genet 126, 1431–1443 (2013). https://doi.org/10.1007/s00122-013-2062-4

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