Euphytica

, 213:98 | Cite as

QTL analysis of resistance to powdery mildew in hop (Humulus lupulus L.)

  • J. A. Henning
  • D. H. Gent
  • M. S. Townsend
  • J. L. Woods
  • S. T. Hill
  • D. Hendrix
Article
  • 287 Downloads

Abstract

Hop with powdery mildew [HPM: caused by Podosphaera macularis (Wallr.) U. Braun & S. Takam.] results in significant losses in hop production by reducing yield and quality. One means of increasing yield and quality is the production of resistant hop lines. Breeding for resistance can be significantly improved and accelerated by use of marker-assisted selection. The objective of this preliminary study was to identify QTLs and markers for genetic resistance to HPM. A bi-parental mapping population between the resistant line “Newport” and susceptible line ‘21110M’. Phenotypic data was scored under controlled greenhouse conditions. Significant differences among offspring were observed and disease resistance did not follow a distinct binomial distribution, suggesting quantitative genetic control. Genotyping-by-sequencing resulted in approximately 375 K SNP markers, which were filtered down to 2263 markers mapped to 10 linkage groups. Interval Mapping identified four QTLs with one on linkage group 1 and three located on linkage group 6. Composite interval mapping identified three QTLs, all located on linkage group 6. Mixed linear models identified 15 markers associated with expression of resistance to HPM. Three of these 15 SNPs were also identified in QTL-CIM analysis. Evaluation of the scaffolds containing the significant SNP markers identified seven putative genes—several of which appear involved in disease resistance in other plant species. The SNP markers identified in this study still require validation in unrelated populations prior to implementation in breeding programs.

Keywords

Disease resistance Genetic mapping Genome Hop Humulus Powdery Mildew QTL 

Supplementary material

10681_2017_1849_MOESM1_ESM.xlsx (828 kb)
Supplementary material 1 (XLSX 828 kb)
10681_2017_1849_MOESM2_ESM.docx (13 kb)
Supplementary material 2 (DOCX 13 kb)
10681_2017_1849_MOESM3_ESM.xls (32 kb)
Supplementary material 3 (XLS 33 kb)

References

  1. Allard R (1999) Principles of plant breeding. Wiley: Hoboken. ISBN: 978-0-471-02309-8Google Scholar
  2. Austin MB, Noel JP (2003) The chalcone synthase superfamily of type III polyketide synthases. Nat Prod Rep 20:79–110CrossRefPubMedGoogle Scholar
  3. Ben-Ari G, Lavi U (2012) 11-marker-assisted selection in plant breeding A2—Altman, Arie. In: Hasegawa PM (ed) Plant biotechnology and agriculture. Academic Press, San Diego, pp 163–184CrossRefGoogle Scholar
  4. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57 (1): 289–300. MR 1325392Google Scholar
  5. Bernardo R (2008) Molecular markers and selection for complex traits in plants: learning from the last 20 years. Crop Sci 48:1649–1664CrossRefGoogle Scholar
  6. Bernardo R (2010) Breeding for quantitative traits in plants. Stemma Press, WoodburyGoogle Scholar
  7. Bonferroni CE (1936) “Teoria statistica delle classi e calcolo delle probabilità.”. Pubblicazioni del R Istituto Superiore di Scienze Economiche e Commerciali di Firenze 8: 3–62,Google Scholar
  8. Borner GH, Lilley KS, Stevens TJ, Dupree P (2003) Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A proteomic and genomic analysis. Plant Physiol 132:568–577CrossRefPubMedPubMedCentralGoogle Scholar
  9. Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890CrossRefPubMedGoogle Scholar
  10. Castro CB, Whittock LD, Whittock SP, Leggett G, Koutoulis A (2008) DNA sequence and expression variation of Hop (Humulus lupulus) valerophenone synthase (VPS), a key gene in bitter acid biosynthesis. Ann Bot 102:265–273CrossRefPubMedPubMedCentralGoogle Scholar
  11. Čerenak A, Šatović Z, Jakše J, Luthar Z, Carović-Stanko K, Javornik B (2009) Identification of QTLs for alpha acid content and yield in hop (Humulus lupulus L.). Euphytica 170(1–2):141–154. doi:10.1007/s10681-009-9920-9 CrossRefGoogle Scholar
  12. Dao TTH, Linthorst HJM, Verpoorte R (2011) Chalcone synthase and its functions in plant resistance. Phytochem Rev 10:397–412CrossRefPubMedPubMedCentralGoogle Scholar
  13. Djian-Caporalino C, Palloix A, Fazari A, Marteu N, Barbary A, Abad P, Sage-Palloix A-M, Mateille T, Risso S, Lanza R et al (2014) Pyramiding, alternating or mixing: comparative performances of deployment strategies of nematode resistance genes to promote plant resistance efficiency and durability. BMC Plant Biol 14:1–13CrossRefGoogle Scholar
  14. Dudley JW (2007) From means to QTL: the Illinois long-term selection experiment as a case study in quantitative genetics. Crop Sci 47(S3):S20–S31Google Scholar
  15. Flor HH (1971) Current status of the gene-for-gene concept. Ann Rev Phytopathol 9:275–296CrossRefGoogle Scholar
  16. Gent DH, Nelson ME, George AE, Grove GG, Mahaffee WF, Ocamb CM, Barbour JD, Peetz A, Turechek WW (2008) A decade of hop powdery mildew in the pacific northwest. Plant Health Prog. doi:10.1094/PHP-2008-0314-01-RV Google Scholar
  17. Godwin JR, Mansfield JW, Darby P (1987) Microscopical studies of resistance to powdery mildew disease in the hop cultivar Wye Target. Plant Pathol 36:21–32CrossRefGoogle Scholar
  18. Hallauer AR (2007) History, contribution, and future of quantitative genetics in plant breeding: lessons from maize. Crop Sci 47(S3):S4–S19Google Scholar
  19. Henning JA, Townsend MS, Mahaffee WF, Kenny S, Haunold A (2004) Registration of ‘Newport’ hop. Crop Sci 44:1018–1019CrossRefGoogle Scholar
  20. Henning J, Townsend MS, Gent D, 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. Henning JA, Gent DH, Twomey MC, Townsend MS, Pitra NJ, Matthews PD (2015) Precision QTL mapping of downy mildew resistance in hop (Humulus lupulus L.). Euphytica 202:487–498CrossRefGoogle Scholar
  22. Henning JA, Gent DH, Twomey MC, Townsend MS, Pitra NJ, Matthews PD (2016). Genotyping-by-sequencing of a bi-parental mapping population segregating for downy mildew resistance in hop (Humulus lupulus L.). Euphytica 208:545–559. doi:10.1007/s10681-015-1600-3 CrossRefGoogle Scholar
  23. Hill, ST, JA. Henning, R Sudarsanam, and D Hendrix. (2016). HopBase: A unified resource for Humulus Genomics. J. Database (Submitted)Google Scholar
  24. Lander ES, Botstein D (1989) Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics. 121:185–199PubMedPubMedCentralGoogle Scholar
  25. Li F, Zhang H, Wang S, Xiao W, Ding C, Liu W, Guo H (2016) Identification of topping responsive proteins in tobacco roots. Front Plant Sci 7:582PubMedPubMedCentralGoogle Scholar
  26. Lu F, Lipka AE, Glaubitz J, Elshire R, Cherney JH et al (2013) Switchgrass genomic diversity, ploidy, and evolution: novel insights from a network-based SNP discovery protocol. PLoS Genet 9(1):e1003215. doi:10.1371/journal.pgen.1003215 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Mahaffee WF, Thomas CS, Turechek WW, Ocamb CM, Nelson ME, Fox A, Gubler WD (2003) Responding to an introduced pathogen: Podosphaera macularis (hop powdery mildew) in the Pacific Northwest. Plant Health Prog. doi:10.1094/PHP-2003-1113-07-RV Google Scholar
  28. Mahaffee WF, Engelhard B, Gent DH, Groves GG (2009) Powdery mildew. In: Mahaffee WF, Pethybridge SJ, Gent DH (eds) Compendium of hop diseases and pests. American Phytopathological Society Press, St. PaulGoogle Scholar
  29. McAdam EL, Freeman JS, Whittock SP, Buck EJ, Jakse J, Cerenak A, Javornik B, Kilian A, Wang C-H, Andersen D et al (2013) Quantitative trait loci in hop (Humulus lupulus L.) reveal complex genetic architecture underlying variation in sex, yield and cone chemistry. BMC Genom 14:1–27CrossRefGoogle Scholar
  30. Nambiar M, Smith GR (2016) Repression of harmful meiotic recombination in centromeric regions. Semin Cell Dev Biol 54:188–197CrossRefPubMedGoogle Scholar
  31. Natsume S, Takagi H, Shiraishi A, Murata J, Toyonaga H, Patzak J, Takagi M, Yaegashi H, Uemura A, Mitsuoka C et al (2015) The draft genome of hop (Humulus lupulus), an essence for brewing. Plant Cell Physiol 56:428–441CrossRefPubMedGoogle Scholar
  32. Neve RA (1991) Hops. Chapman & Hall, LondonCrossRefGoogle Scholar
  33. Ocamb CM, Gent DH (2016) Hop (Humulus lupulus)-Powdery mildew. In: Pscheidt JW, Ocamb CM (eds.) Pacific northwest plant disease management handbook . Corvallis, OR: Oregon State University. http://pnwhandbooks.org/plantdisease/hop-humulus-lupulus-abiotic-wilt. Accessed 31 March 2016
  34. Poland J, Rutkoski J (2016) Advances and challenges in genomic selection for disease resistance. Annu Rev Phytopathol 54:79–98CrossRefPubMedGoogle Scholar
  35. Reilly JF, Martinez SD, Mickey G, Maher PA (2002) A novel role for farnesyl pyrophosphate synthase in fibroblast growth factor-mediated signal transduction. Biochem J 366:501–510. doi:10.1042/bj20020560 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Sallam AH, Smith KP (2016) Genomic selection performs similarly to phenotypic selection in barley. Crop Sci 56:2871–2881. doi:10.2135/cropsci2015.09.0557 CrossRefGoogle Scholar
  37. St. Clair DA (2010) Quantitative disease resistance and quantitative resistance loci in breeding. Annu Rev Phytopathol 48:247–268CrossRefPubMedGoogle Scholar
  38. Van Ooijen J (2011) Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genet Res 93(5):343–349CrossRefGoogle Scholar
  39. Wang S, Basten CJ, Zeng ZB (2012) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC. http://statgen.ncsu.edu/qtlcart/WQTLCart.htm. Accessed 9 Oct 2016
  40. Wolfenbarger SN, Eck EB, Gent DH (2014) Characterization of resistance to powdery mildew in the hop cultivars “Newport” and “Comet”. Plant Health Prog. doi:10.1094/PHP-BR-13-0129 Google Scholar
  41. Zimmermann CE, Likens ST, Haunold A, Homer CE, Roberts DD (1975) Registration of “Comet” hop (Registration No. 3). Crop Sci 15:98CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht (outside the USA) 2017

Authors and Affiliations

  1. 1.USDA-ARSCorvallisUSA
  2. 2.Department of Crop and Soil SciencesOregon State UniversityCorvallisUSA
  3. 3.Department of Botany and Plant PathologyOregon State UniversityCorvallisUSA
  4. 4.Department of Computer SciencesOregon State UniversityCorvallisUSA
  5. 5.Department of Biochemistry and BiophysicsOregon State UniversityCorvallisUSA

Personalised recommendations