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Molecular Breeding

, Volume 33, Issue 1, pp 61–74 | Cite as

Development of novel EST-derived resistance gene markers in hop (Humulus lupulus L.)

  • Aljaz Majer
  • Branka Javornik
  • Andreja Cerenak
  • Jernej Jakse
Article

Abstract

Although sources of resistance to major pathogens exist in cultivated hop germplasm, little effort has been invested to date in developing resistance-linked markers. The aim of this study was to design and evaluate resistance gene analogs (RGAs) potentially useful for marker-assisted selection towards novel resistant hop cultivars. A set of 34 putative hop RGAs was retrieved by screening publicly available hop expressed sequence tags (ESTs) for conserved sequence motifs of common resistance protein domains. Seventeen of these were identified as putative RGAs by BLAST analyses. Exon/intron boundary prediction enabled re-sequencing of 24 EST-RGAs, allowing the acquisition of approximately 5 kbp of novel intronic sequence and 8 kbp of re-sequenced exons. Fifteen EST-RGAs exhibited polymorphisms and were added to a framework linkage map of hop. In addition to providing EST-derived markers potentially useful for resistant hop cultivar development, this study provides valuable insights into the utility of targeting hop introns for marker development.

Keywords

Humulus lupulus Resistance gene analogs EST SNP Exon/intron boundary prediction 

Notes

Acknowledgments

The authors acknowledge financial support from the Slovenian Research Agency, grant number P4-0077, and the support of A.M. by Grant Number 1000-09-310205.

Supplementary material

11032_2013_9934_MOESM1_ESM.doc (56 kb)
Supplementary material 1 (DOC 56 kb)
11032_2013_9934_MOESM2_ESM.docx (12 kb)
Supplementary material 2 (DOCX 12 kb)
11032_2013_9934_MOESM3_ESM.doc (44 kb)
Supplementary material 3 (DOC 43 kb)

References

  1. Birney E, Durbin R (1997) Wise2. http://www.sanger.ac.uk/Software/Wise2. Accessed 10 March 2013
  2. 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
  3. 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
  4. Chee PW, Rong J, Williams-Coplin D, Schulze SR, Paterson AH (2004) EST derived PCR-based markers for functional gene homologues in cotton. Genome 47:449–462PubMedCrossRefGoogle Scholar
  5. Collard BC, Mackill DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Phil Trans R Soc B 363:557–572PubMedCrossRefGoogle Scholar
  6. 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 86–90Google Scholar
  7. Dilbirligi M, Gill KS (2003) Identification and analysis of expressed resistance gene sequences in wheat. Plant Mol Biol 53:771–787PubMedCrossRefGoogle Scholar
  8. Duvick J, Fu A, Muppirala U, Sabharwal M, Wilkerson MD, Lawrence CJ, Lushbough C, Brendel V (2008) PlantGDB: a resource for comparative plant genomics. Nucleic Acids Res. doi: 10.1093/nar/gkm1041 PubMedCentralPubMedGoogle Scholar
  9. Eitas TK, Dangl JL (2010) NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Curr Opin Plant Biol 13:472–477PubMedCentralPubMedCrossRefGoogle Scholar
  10. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunesekaran P, Ceric G, Forslund K, Holm L, Sonnhammer EL, Eddy SR, Bateman A (2010) The Pfam protein families database. Nucleic Acids Res. doi: 10.1093/nar/gkp985 Google Scholar
  11. Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. doi: 10.1093/nar/gkr367
  12. Fradin EF, Zhang Z, Ayala JCJ, Castroverde CD, Nazar RN, Robb J, Liu CM, Thomma BP (2009) Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol 150:320–332PubMedCentralPubMedCrossRefGoogle Scholar
  13. Goese M, Kammhuber K, Bacher A, Zenk MH, Eisenreich W (1999) Biosynthesis of bitter acids in hops. Eur J Biochem 263:447–454PubMedCrossRefGoogle Scholar
  14. Grattapaglia D, Sederoff R (1994) Genetic linkage mapping in Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross mapping strategy and RAPD markers. Genetics 137:1121–1137PubMedGoogle Scholar
  15. Hartl L, Seefelder S (1998) Diversity of selected hop cultivars detected by fluorescent AFLPs. Theor Appl Genet 96:112–116CrossRefGoogle Scholar
  16. 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
  17. Howard EL, Whittock SP, Jakse J, Carling J, Matthews PD, Probasco G, Henning JA, Darby P, Cerenak A, Javornik B, Killian A, Koutoulis A (2011) High-throughput genotyping of hop (Humulus lupulus L.) utilising diversity arrays technology (DArT). Theor Appl Genet 122:1265–1280PubMedCrossRefGoogle Scholar
  18. IHGC (2011) International hop growers’ convention economic commission summary reports. http://www.hmelj-giz.si/ihgc/doc/IHGC%20hop%20supply.pdf. Accessed 3 Feb 2013
  19. Jakse J, Kindlhofer K, Javornik B (2001) Assessment of genetic variation and differentiation of hop genotypes by microsatellite and AFLP markers. Genome 44:773–782PubMedCrossRefGoogle Scholar
  20. Jakse J, Stajner N, Kozjak P, Cerenak A, Javornik B (2008) Trinucleotide microsatellite repeat is tightly linked to male sex in hop (Humulus lupulus L.). Mol Breed 21:139–148CrossRefGoogle Scholar
  21. 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
  22. Jakse J, Cerenak A, Radisek S, Satovic Z, Luthar Z, Javornik B (2013) Identification of quantitative trait loci for resistance to Verticillium wilt and yield parameters in hop (Humulus lupulus L.). Theor Appl Genet. doi: 10.1007/s00122-013-2062-4 PubMedGoogle Scholar
  23. Judd WS, Olmstead RG (2004) A survey of tricolpate (eudicot) phylogenetic relationships. Am J Bot 91:1627–1644PubMedCrossRefGoogle Scholar
  24. Kohler A, Rinaldi C, Duplessis S, Baucher M, Geelen D, Duchaussoy F, Meyers BC, Boerjan W, Martin F (2008) Genome-wide identification of NBS resistance genes in Populus trichocarpa. Plant Mol Biol 66:619–636PubMedCrossRefGoogle Scholar
  25. 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
  26. 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
  27. Leister D, Ballvora A, Salamini F, Gebhardt C (1996) A PCR–based approach for isolating pathogen resistance genes from potato with potential for wide application in plants. Nat Genet 14:421–429PubMedCrossRefGoogle Scholar
  28. Li D, Xia Z, Deng Z, Liu X, Dong J, Feng F (2012) Development and characterization of intron-flanking EST-PCR markers in rubber tree (Hevea brasiliensis Muell. Arg.). Mol Biotechnol 51:148–159PubMedCrossRefGoogle Scholar
  29. Liu H, Lin Y, Chen G, Shen Y, Liu J, Zhang S (2012) Genome-scale identification of resistance gene analogs and the development of their intron length polymorphism markers in maize. Mol Breed 29:437–447Google Scholar
  30. Mahaffee WF, Pethybridge SJ, Gent DH (2009) Compendium of hop diseases and pests. American Phytopathological Society, St. Paul, MNGoogle Scholar
  31. Mbanjo EGN, Tchoumbougnang F, Mouelle AS, Oben JE, Nyine M, Dochez C, Ferguson ME, Lorenzen J (2012) Molecular marker-based genetic linkage map of a diploid banana population (Musa acuminata Colla). Euphytica 188:369–386CrossRefGoogle Scholar
  32. McHale L, Xiaoping T, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7:212. doi: 10.1186/gb-2006-7-4-212 PubMedCentralPubMedCrossRefGoogle Scholar
  33. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR–encoding genes in Arabidopsis. Plant Cell 15:809–834PubMedCentralPubMedCrossRefGoogle Scholar
  34. Milligan S, Kalita J, Pocock V, Heyerick A, De Cooman L, Rong H, De Keukeleire D (2002) Oestrogenic activity of the hop phytooestrogen, 8-prenylnaringenin. Reproduction 123:235–242PubMedCrossRefGoogle Scholar
  35. Nagel J, Culley LK, Liu YLE, Matthews PD, Stevens JF, Page JE (2008) EST analysis of hop glandular trichomes identifies an O-methyltransferase that catalyzes the biosynthesis of xanthohumol. Plant Cell 20:186–200PubMedCentralPubMedCrossRefGoogle Scholar
  36. Neve RA (1991) Hops. Chapman and Hall, LondonCrossRefGoogle Scholar
  37. Patzak J (2001) Comparison of RAPD, STS, ISSR and AFLP molecular methods used for assessment of genetic diversity in hop (Humulus lupulus L.). Euphytica 121:9–18CrossRefGoogle Scholar
  38. Patzak J, Vrba L, Matousek J (2007) New STS molecular markers for assessment of genetic diversity and DNA fingerprinting in hop (Humulus lupulus L.). Genome 50:15–25PubMedCrossRefGoogle Scholar
  39. Polley A, Ganal MW, Seigner E (1997) Identification of sex in hop (Humulus lupulus) using molecular markers. Genome 40:357–361PubMedCrossRefGoogle Scholar
  40. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org
  41. Rambaldi D, Ciccarelli FD (2009) FancyGene: dynamic visualization of gene structures and protein domain architectures on genomic loci. Bioinformatics 25:2281–2282PubMedCrossRefGoogle Scholar
  42. Rossi M, Araujo PG, Paulet F, Garsmeur O, Dias VM, Chen H, Van Sluys MA, D’Hont A (2003) Genomic distribution and characterization of EST-derived resistance gene analogs (RGAs) in sugarcane. Mol Genet Genomics 269:406–419PubMedCrossRefGoogle Scholar
  43. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386PubMedGoogle Scholar
  44. 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
  45. Shang W, Zhou R, Jia J, Gao L (2010) RGA-ILP, a new type of functional molecular markers in bread wheat. Euphytica 172:263–273CrossRefGoogle Scholar
  46. Stajner N, Satovic Z, Cerenak A, Javornik B (2008) Genetic structure and differentiation in hop (Humulus lupulus L.) as inferred from microsatellites. Euphytica 161:301–311CrossRefGoogle Scholar
  47. 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
  48. Takken FL, Albrecht M, Tameling WI (2006) Resistance proteins: molecular switches of plant defence. Curr Opin Plant Biol 9:383–390PubMedCrossRefGoogle Scholar
  49. Valkonen JPT, Wiegmann K, Hämäläinen JH, Marczewski W, Watanabe KN (2008) Evidence for utility of the same PCR-based markers for selection of extreme resistance to Potato virus Y controlled by Rysto of Solanum stoloniferum derived from different sources. Ann Appl Biol 152:121–130CrossRefGoogle Scholar
  50. Van Ooijen JW, Voorrips RE (2001) JoinMap version 3.0: software for the calculation of genetic linkage maps. Plant Research International, WageningenGoogle Scholar
  51. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78PubMedCrossRefGoogle Scholar
  52. Wang G, Tian L, Aziz N, Broun P, Dai X, He J, King A, Zhao PX, Dixon RA (2008) Terpene biosynthesis in glandular trichomes of hop. Plant Physiol 148:1254–1266PubMedCentralPubMedCrossRefGoogle Scholar
  53. Wang Y, Chen J, Francis DM, Shen H, Wu T, Yang W (2010) Discovery of intron polymorphisms in cultivated tomato using both tomato and Arabidopsis genomic information. Theor Appl Genet 121:1199–1207PubMedCrossRefGoogle Scholar
  54. Wei H, Fu Y, Arora R (2005) Intron-flanking EST–PCR markers: from genetic marker development to gene structure analysis in Rhododendron. Theor Appl Genet 111:1347–1356PubMedCrossRefGoogle Scholar
  55. Zhou T, Wang Y, Chen JQ, Araki H, Jing Z, Jiang K, Shen J, Tian D (2004) Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol Genet Genomics 271:402–415PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Aljaz Majer
    • 1
  • Branka Javornik
    • 1
  • Andreja Cerenak
    • 2
  • Jernej Jakse
    • 1
  1. 1.Agronomy Department, Biotechnical FacultyUniversity of LjubljanaLjubljanaSlovenia
  2. 2.Slovenian Institute for Hop Research and BrewingŽalecSlovenia

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