Construction of a high-density linkage map and QTL detection of downy mildew resistance in Vitis aestivalis-derived ‘Norton’

Abstract

Key message

A major QTL for downy mildew resistance was detected on chromosome 18 (Rpv27) in Vitis aestivalis-derived ‘Norton’ based on a high-resolution linkage map with SNP and SSR markers as well as 2 years of field and laboratory phenotyping data.

Abstract

Grapevine downy mildew caused by the oomycete Plasmopara viticola is one of the most widespread and destructive diseases, particularly in humid viticultural areas where it damages green tissues and defoliates vines. Traditional Vitis vinifera wine grape cultivars are susceptible to downy mildew whereas several North American and a few Asian cultivars possess various levels of resistance to this disease. To identify genetic determinants of downy mildew resistance in V. aestivalis-derived ‘Norton,’ a mapping population with 182 genotypes was developed from a cross between ‘Norton’ and V. vinifera ‘Cabernet Sauvignon’ from which a consensus map was constructed via 411 simple sequence repeat (SSR) markers. Using genotyping-by-sequencing, 3825 single nucleotide polymorphism (SNP) markers were also generated. Of these, 1665 SNP and 407 SSR markers were clustered into 19 linkage groups in 159 genotypes, spanning a genetic distance of 2203.5 cM. Disease progression in response to P. viticola was studied in this population for 2 years under both laboratory and field conditions, and strong correlations were observed among data sets (Spearman correlation coefficient = 0.57–0.79). A quantitative trait loci (QTL) analysis indicated a resistance locus on chromosome 18, here named Rpv27, explaining 33.8% of the total phenotypic variation. Flanking markers closely linked with the trait can be further used for marker-assisted selection in the development of new cultivars with resistance to downy mildew.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Adhikari P, Chen L-L, Chen X, Sapkota SD, Hwang C-F (2014) Interspecific hybrid identification of Vitis aestivalis-derived ‘Norton’-based populations using microsatellite markers. Sci Hort 179:363–366

    CAS  Article  Google Scholar 

  2. Akkurt M, Welter L, Maul E, Töpfer R, Zyprian E (2007) Development of SCAR markers linked to powdery mildew (Uncinula necator) resistance in grapevine (Vitis vinifera L. and Vitis sp.). Mol Breed 19:103–111

    CAS  Article  Google Scholar 

  3. Ambers CP (2013) A historical hypothesis on the origin of the Norton grape. J Wine Res 24:85–95

    Article  Google Scholar 

  4. Ball AD, Stapley J, Dawson DA, Birkhead TR, Burke T, Slate J (2010) A comparison of SNPs and microsatellites as linkage mapping markers: lessons from the zebra finch (Taeniopygia guttata). BMC Genom 11:218

    Article  Google Scholar 

  5. Barba P, Cadle-Davidson L, Harriman J, Glaubitz JC, Brooks S, Hyma K, Reisch B (2014) Grapevine powdery mildew resistance and susceptibility loci identified on a high-resolution SNP map. Theor Appl Genet 127:73–84

    CAS  Article  Google Scholar 

  6. Bellin D, Peressotti E, Merdinoglu D, Wiedemann-Merdinoglu S, Adam-Blondon A-F, Cipriani G, Morgante M, Testolin R, Di Gaspero G (2009) Resistance to Plasmopara viticola in grapevine ‘Bianca’ is controlled by a major dominant gene causing localized necrosis at the infection site. Theor Appl Genet 120:163–176

    Article  Google Scholar 

  7. Bernet GP, Fernandez Ribacoba J, Carbonell EA, Asins MJ (2010) Comparative genome-wide segregation analysis and map construction using a reciprocal cross design to facilitate citrus germplasm utilization. Mol Breed 25:659–673

    Article  Google Scholar 

  8. Bielenberg DG, Rauh B, Fan S, Gasic K, Abbott AG, Reighard GL, Okie WR, Wells CE (2015) Genotyping by sequencing for SNP-based linkage map construction and QTL analysis of chilling requirement and bloom date in peach [Prunus persica (L.) Batsch]. PLoS One 10:e0139406

    Article  Google Scholar 

  9. Blanc S, Wiedemann-Merdinoglu S, Dumas V, Mestre P, Merdinoglu D (2012) A reference genetic map of Muscadinia rotundifolia and identification of Ren5, a new major locus for resistance to grapevine powdery mildew. Theor Appl Genet 125:1663–1675

    CAS  Article  Google Scholar 

  10. Blasi P, Blanc S, Wiedemann-Merdinoglu S, Prado E, Rühl EH, Mestre P, Merdinoglu D (2011) Construction of a reference linkage map of Vitis amurensis and genetic mapping of Rpv8, a locus conferring resistance to grapevine downy mildew. Theor Appl Genet 123:43–53

    Article  Google Scholar 

  11. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

    CAS  Article  Google Scholar 

  12. Broman KW, Wu H, Sen Ś, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890

    CAS  Article  Google Scholar 

  13. Brown MV, Moore JN, Fenn P, McNew RW (1999) Comparison of leaf disk, greenhouse, and field screening procedures for evaluation of grape seedlings for downy mildew resistance. HortScience 34:331–333

    Google Scholar 

  14. Cadle-Davidson L (2008) Variation within and between Vitis spp. for foliar resistance to the downy mildew pathogen Plasmopara viticola. Plant Dis 92:1577–1584

    Article  Google Scholar 

  15. Cadle-Davidson L, Gadoury D, Fresnedo-Ramírez J, Yang S, Barba P, Sun Q, Kasinathan H (2016) Lessons from a phenotyping center revealed by the genome-guided mapping of powdery mildew resistance loci. Phytopathology 106:1159–1169

    CAS  Article  Google Scholar 

  16. Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nature Rev Genet 12:499

    CAS  Article  Google Scholar 

  17. Di Gaspero G, Copetti D, Coleman C, Castellarin SD, Eibach R, Kozma P, Kovács L (2012) Selective sweep at the Rpv3 locus during grapevine breeding for downy mildew resistance. Theor Appl Genet 124:277–286

    Article  Google Scholar 

  18. Diez-Navajas AM, Wiedemann-Merdinoglu S, Greif C, Merdinoglu D (2008) Nonhost versus host resistance to the grapevine downy mildew, Plasmopara viticola, studied at the tissue level. Phytopathology 98:776–780

    CAS  Article  Google Scholar 

  19. Divilov K, Barba P, Cadle-Davidson L, Reisch RI (2018) Single and multiple phenotype QTL analyses of downy mildew resistance in interspecific grapevines. Theor Appl Genet 131:1133–1143

    Article  Google Scholar 

  20. Doligez A, Adam-Blondon A-F, Cipriani G, Di Gaspero G, Laucou V, Merdinoglu D, Meredith C, Riaz S, Roux C, This P (2006) An integrated SSR map of grapevine based on five mapping populations. Theor Appl Genet 113:369–382

    CAS  Article  Google Scholar 

  21. Edwards D, Forster JW, Cogan NOI, Batley J, Chagné D (2007) Chapter 4: single nucleotide polymorphism discovery in plants. In: Oraguzie NC, Rikkerink E, Gardiner SE, De Silva NH (eds) Association mapping in plants. Springer, New York, pp 53–76

    Google Scholar 

  22. Einset J, Pratt C (1975) Grapes. In: Janick J, Moore JN (eds) Advances in fruit breeding. Purdue University Press, West Lafayette, pp 130–153

    Google Scholar 

  23. Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379

    CAS  Article  Google Scholar 

  24. Fischer BM, Salakhutdinov I, Akkurt M, Eibach R, Edwards KJ, Töpfer R, Zyprian EM (2004) Quantitative trait locus analysis of fungal disease resistance factors on a molecular map of grapevine. Theor Appl Genet 108:501–515

    CAS  Article  Google Scholar 

  25. Ganal MW, Polley A, Graner EM, Plieske J, Wieseke R, Luerssen H, Durstewitz G (2012) Large SNP arrays for genotyping in crop plants. J Biol Sci 37:821–828

    CAS  Google Scholar 

  26. Hammers M, Sapkota S, Chen L-L, Hwang C-F (2017) Constructing a genetic linkage map of Vitis aestivalis-derived “Norton” and its use in comparing Norton and Cynthiana. Mol Breed 37:64

    Article  Google Scholar 

  27. He J, Zhao X, Laroche A, Lu Z-X, Liu H, Li Z (2014) Genotyping-by-sequencing (GBS), an ultimate marker-assisted selection (MAS) tool to accelerate plant breeding. Front Plant Sci 5:484

    Article  Google Scholar 

  28. Heath MC, Skalamera D (1997) Cellular interactions between plants and biotrophic fungal parasites. Adv Bot Res 24:195–225

    CAS  Article  Google Scholar 

  29. Huang Y-F, Poland JA, Wight CP, Jackson EW, Tinker NA (2014) Using genotyping-by-sequencing (GBS) for genomic discovery in cultivated oat. PLoS ONE 9:e102448

    Article  Google Scholar 

  30. Hyma KE, Barba P, Wang M, Londo JP, Acharya CB, Mitchell SE, Sun Q, Reisch B, Cadle-Davidson L (2015) Heterozygous mapping strategy (HetMappS) for high resolution genotyping-by-sequencing markers: a case study in grapevine. PLoS ONE 10:e0134880

    Article  Google Scholar 

  31. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Vezzi A (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463

    CAS  Article  Google Scholar 

  32. Jürges G, Kassemeyer HH, Dürrenberger M, Düggelin M, Nick P (2009) The mode of interaction between Vitis and Plasmopara viticola Berk. & Curt. Ex de Bary depends on the host species. Plant Biol 11:886–898

    Article  Google Scholar 

  33. Kono A, Sato A, Reisch B, Cadle-Davidson L (2015) Effect of detergent on the quantification of grapevine downy mildew sporangia from leaf discs. HortScience 50:656–660

    CAS  Google Scholar 

  34. Kortekamp A, Zyprian E (1999) Leaf hairs as a basic protective barrier against downy mildew of grape. J Phytopathol 147:453–459

    Article  Google Scholar 

  35. Langcake P, Lovell E (1980) Light and electron microscopical studies of the infection of Vitis spp. by Plasmopara viticola, the downy mildew pathogen. Vitis 19:321–337

    Google Scholar 

  36. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760

    CAS  Article  Google Scholar 

  37. Marguerit E, Boury C, Manicki A, Donnart M, Butterlin G, Némorin A, Wiedemann-Merdinoglu S, Merdinoglu D, Ollat N, Decroocq S (2009) Genetic dissection of sex determinism, inflorescence morphology and downy mildew resistance in grapevine. Theor Appl Genet 118:1261–1278

    Article  Google Scholar 

  38. Merdinoglu D, Wiedeman-Merdinoglu S, Coste P, Dumas V, Haetty S, Butterlin G, Greif C (2003) Genetic analysis of downy mildew resistance derived from Muscadinia rotundifolia. Acta Hort 603:451–456

    CAS  Article  Google Scholar 

  39. Moreira FM, Madini A, Marino R, Zulini L, Stefanini M, Velasco R, Kozma P, Grando MS (2011) Genetic linkage maps of two interspecific grape crosses (Vitis spp.) used to localize quantitative trait loci for downy mildew resistance. Tree Genet Genomes 7:153–167

    Article  Google Scholar 

  40. Ochssner I, Hausmann L, Töpfer R (2016) Rpv14, a new genetic source for Plasmopara viticola resistance conferred by Vitis cinerea. Vitis 55:79–81

    CAS  Google Scholar 

  41. Ollitrault P, Terol J, Chen C, Federici CT, Lotfy S, Hippolyte I, Costantino G (2012) A reference genetic map of C. clementina hort. ex Tan,; citrus evolution inferences from comparative mapping. BMC Genom 13:593

    CAS  Article  Google Scholar 

  42. Polesani M, Bortesi L, Ferrarini A, Zamboni A, Fasoli M, Zadra C, Lovato A, Pezzotti M, Delledonne M, Polverari A (2010) General and species-specific transcriptional responses to downy mildew infection in a susceptible (Vitis vinifera) and a resistant (V. riparia) grapevine species. BMC Genom 11:117

    Article  Google Scholar 

  43. Pootakham W, Ruang-Areerate P, Jomchai N, Sonthirod C, Sangsrakru D, Yoocha T, Theerawattanasuk K, Nirapathpongporn K, Romruensukharom P, Tragoonrung S (2015) Construction of a high-density integrated genetic linkage map of rubber tree (Hevea brasiliensis) using genotyping-by-sequencing (GBS). Front Plant Sci 6:367

    Article  Google Scholar 

  44. Sawler J, Reisch B, Aradhya MK, Prins B, Zhong GY, Schwaninger H, Simon C, Buckler E, Myles S (2013) Genomics assisted ancestry deconvolution in grape. PLoS ONE 8:e80791

    CAS  Article  Google Scholar 

  45. Schwander F, Eibach R, Fechter I, Hausmann L, Zyprian E, Töpfer R (2012) Rpv10: a new locus from the Asian Vitis gene pool for pyramiding downy mildew resistance loci in grapevine. Theor Appl Genet 124:163–176

    CAS  Article  Google Scholar 

  46. Spindel J, Wright M, Chen C, Cobb J, Gage J, Harrington S, McCouch S (2013) Bridging the genotyping gap: using genotyping by sequencing (GBS) to add high-density SNP markers and new value to traditional bi-parental mapping and breeding populations. Theor Appl Genet 126:2699–2716

    CAS  Article  Google Scholar 

  47. van Heerden CJ, Burger P, Vermeulen A, Prins R (2014) Detection of downy and powdery mildew resistance QTL in a ‘Regent’ × ‘RedGlobe’ population. Euphytica 200:281–295

    Article  Google Scholar 

  48. van Ooijen JW (2006) JoinMap 4, software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen

    Google Scholar 

  49. van Ooijen JW (2009) MapQTL 6, software for the mapping of quantitative trait loci in experimental populations of diploid species. Kyazma BV, Wageningen

    Google Scholar 

  50. Venuti S, Copetti D, Foria S, Falginella L, Hoffmann S, Bellin D, Cindrić P, Kozma P, Scalabrin S, Morgante M (2013) Historical introgression of the downy mildew resistance gene Rpv12 from the Asian species Vitis amurensis into grapevine varieties. PLoS ONE 8:e61228

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  52. VIVC (2018) Table of Loci for Traits in Grapevine Relevant for Breeding and Genetics. http://www.vivc.de/docs/dataonbreeding/20181001_Table%20of%20Loci%20for%20Traits%20in%20Grapevine.pdf

  53. Wang H, Misztal I, Aguilar I, Legarra A, Muir WM (2012) Genome-wide association mapping including phenotypes from relatives without genotypes. Genet Res 94:73–83

    CAS  Article  Google Scholar 

  54. Wang L, Wan ZY, Bai B, Huang SQ, Chua E, Lee M, Pang HY, Wen YF, Liu P, Liu F, Sun F, Lin G, Ye BQ, Yue GH (2015) Construction of a high-density linkage map and fine mapping of QTL for growth in Asian seabass. Sci Rep 5:16358

    CAS  Article  Google Scholar 

  55. Ward JA, Bhangoo J, Fernández-Fernández F, Moore P, Swanson J, Viola R, Velasco R, Bassil N, Weber CA, Sargent DJ (2013) Saturated linkage map construction in Rubus idaeus using genotyping by sequencing and genome-independent imputation. BMC Genom 14:2

    CAS  Article  Google Scholar 

  56. Welter LJ, Göktürk-Baydar N, Akkurt M, Maul E, Eibach R, Töpfer R, Zyprian EM (2007) Genetic mapping and localization of quantitative trait loci affecting fungal disease resistance and leaf morphology in grapevine (Vitis vinifera L). Mol Breed 20:359–374

    CAS  Article  Google Scholar 

  57. Wiedemann-Merdinoglu S, Prado E, Coste P, Dumas V, Butterlin G, Bouquet A, Merdinoglu D (2006) Genetic analysis of resistance to downy mildew from Muscadinia rotundifolia. In: 9th international conference on grape genetics and breeding 2006

  58. Zhang Y, Wang L, Xin H, Li D, Ma C, Ding X, Hong W, Zhang X (2013) Construction of a high-density genetic map for sesame based on large scale marker development by specific length amplified fragment (SLAF) sequencing. BMC Plant Biol 13:141

    Article  Google Scholar 

  59. Zhou X, Xia Y, Ren X, Chen Y, Huang L, Huang S, Liao B, Lei Y, Yan L, Jiang H (2014) Construction of a SNP-based genetic linkage map in cultivated peanut based on large scale marker development using next-generation double-digest restriction-site-associated DNA sequencing (ddRADseq). BMC Genom 15:351

    Article  Google Scholar 

  60. Zyprian E, Ochssner I, Schwander F, Šimon S, Hausmann L, Bonow-Rex M, Moreno-Sanz P, Grando MS, Wiedemann-Merdinoglu S, Merdinoglu D, Eibach R, Töpfer R (2016) Quantitative trait loci affecting pathogen resistance and ripening of grapevines. Mol Genet Genomics 291:1573–1594

    CAS  Article  Google Scholar 

Download references

Acknowledgements

The authors thank S. Jacob Schneider, Marilyn Odneal and Kevin Fort for valuable discussions and constructive comments on the manuscript. This project was supported by Agriculture and Food Research Initiative Competitive Grant, Award No. 2013-67014-21360, and Specialty Crop Research Initiative Competitive Grant, Award No. 2011-51181-30635, of the USDA National Institute of Food and Agriculture.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Chin-Feng Hwang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Communicated by Reinhard Toepfer.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sapkota, S., Chen, L., Yang, S. et al. Construction of a high-density linkage map and QTL detection of downy mildew resistance in Vitis aestivalis-derived ‘Norton’. Theor Appl Genet 132, 137–147 (2019). https://doi.org/10.1007/s00122-018-3203-6

Download citation