Skip to main content
SpringerLink
Log in

Grapevine powdery mildew resistance and susceptibility loci identified on a high-resolution SNP map

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Improved efficacy and durability of powdery mildew resistance can be enhanced via knowledge of the genetics of resistance and susceptibility coupled with the development of high-resolution maps to facilitate the stacking of multiple resistance genes and other desirable traits. We studied the inheritance of powdery mildew (Erysiphe necator) resistance and susceptibility of wild Vitis rupestris B38 and cultivated V. vinifera ‘Chardonnay’, finding evidence for quantitative variation. Molecular markers were identified using genotyping-by-sequencing, resulting in 16,833 single nucleotide polymorphisms (SNPs) based on alignment to the V. vinifera ‘PN40024’ reference genome sequence. With an average density of 36 SNPs/Mbp and uniform coverage of the genome, this 17K set was used to identify 11 SNPs on chromosome 7 associated with a resistance locus from V. rupestris B38 and ten SNPs on chromosome 9 associated with a locus for susceptibility from ‘Chardonnay’ using single marker association and linkage disequilibrium analysis. Linkage maps for V. rupestris B38 (1,146 SNPs) and ‘Chardonnay’ (1,215 SNPs) were constructed and used to corroborate the ‘Chardonnay’ locus named Sen1 (Susceptibility to Erysiphe necator 1), providing the first insight into the genetics of susceptibility to powdery mildew from V. vinifera. The identification of markers associated with a susceptibility locus in a V. vinifera background can be used for negative selection among breeding progenies. This work improves our understanding of the nature of powdery mildew resistance in V. rupestris B38 and ‘Chardonnay’, while applying next-generation sequencing tools to advance grapevine genomics and breeding.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adam-Blondon AF, Roux C, Claux D, Butterlin G, Merdinoglu D, This P (2004) Mapping 245 SSR markers on the Vitis vinifera genome: a tool for grape genetics. Theor Appl Genet 109(5):1017–1027

    Article  CAS  PubMed  Google Scholar 

  • Alleweldt G, Spiegel-Roy P, Reisch B (1991) Grapes (Vitis). In: vol 290. Acta Hort (ISHS), pp 291–330

  • Barbazuk WB, Bedell JA, Rabinowicz PD (2005) Reduced representation sequencing: a success in maize and a promise for other plant genomes. Bioessays 27(8):839–848

    Article  CAS  PubMed  Google Scholar 

  • Boubals D (1961) Étude des causes de la résistance des Vitacées à l’Oïdium de la vigne (Uncinula necator (Schw.) Burr.) et de leur mode de transmission héréditaire. Ann Amélior Plant 11:401–500

    Google Scholar 

  • 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(19):2633–2635

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cadle-Davidson L, Mahanil S, Gadoury DM, Kozma P, Reisch BI (2011) Natural infection of Run1-positive vines by naïve genotypes of Erysiphe necator. Vitis 50:173–175

    Google Scholar 

  • Coleman C, Copetti D, Cipriani G, Hoffman S, Kozman P, Kovacs L, Morgante M, Testolin R, Di Gaspero G (2009) The powdery mildew resistance gene REN1 co-segregates with an NBS-LRR gene cluster in two Central Asian grapevines. BMC Genet. 10. doi:10.1186/1471-2156-10-89

  • Dalbó MA, Ye GN, Weeden NF, Wilcox WF, Reisch BI (2001) Marker-assisted selection for powdery mildew resistance in grapes. J Am Soc Hortic Sci 126(1):83–89

    Google Scholar 

  • Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12(7):499–510

    Article  CAS  PubMed  Google Scholar 

  • Deulvot C, Charrel H, Marty A, Jacquin F, Donnadieu C, Lejeune-Henaut I, Burstin J, Aubert G (2010) Highly-multiplexed SNP genotyping for genetic mapping and germplasm diversity studies in pea. BMC Genomics 11:468

    Article  PubMed Central  PubMed  Google Scholar 

  • Di Gaspero G, Cattonaro F (2009) Application of genomics to grapevine improvement. Aust J Grape Wine Res 16:122–130

    Article  Google Scholar 

  • Di Gaspero G, Cipriani G, Adam-Blondon AF, Testolin R (2007) Linkage maps of grapevine displaying the chromosomal locations of 420 microsatellite markers and 82 markers for R-gene candidates. Theor Appl Genet 114(7):1249–1263

    Article  PubMed  Google Scholar 

  • Doligez A, Adam-Blondon A, 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(3):369–382

    Article  CAS  PubMed  Google Scholar 

  • Eibach R, Zyprian E, Welter LJ, Topfer R (2007) The use of molecular markers for pyramiding resistance genes in grapevine breeding. Vitis 46(3):120–125

    CAS  Google Scholar 

  • Elshire R, Glaubitz J, Sun Q, Poland J, Kawamoto K, Buckler E, Mitchell S (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE. doi:10.1371/journal.pone.0019379

    PubMed Central  PubMed  Google Scholar 

  • Feechan A, Kabbara S, Dry IB (2010) Mechanisms of powdery mildew resistance in the Vitaceae family. Mol Plant Path doi. doi:10.1111/j.1364-3703.2010.00668.x

    Google Scholar 

  • Ganal MW, Durstewitz G, Polley A, Bérard A, Buckler ES, Charcosset A, Clarke JD, Graner E-M, Hansen M, Joets J, Le Paslier M-C, McMullen MD, Montalent P, Rose M, Schön C-C, Sun Q, Walter H, Martin OC, Falque M (2011) A large maize (Zea mays L.) SNP genotyping array: Development and germplasm genotyping, and genetic mapping to compare with the B73 reference genome. PLoS ONE. doi:10.1371/journal.pone.0028334

  • Glaubitz J, Casstevens T, Elshire R, Harriman J, Casstevens T (2012) TASSEL 3.0 genotyping by sequencing (GBS) pipeline documentation. http://www.maizegenetics.net/tassel/docs/TasselPipelineGBS.pdf. Accessed 23 November 2012

  • IPGRI, UPOV, OIV (1997) Descriptors for grapevine (Vitis spp.). International Union for the Protection of New Varieties of Plants, Geneva, Switzerland/Office International de la Vigne et du Vin, Paris, France/International Plant Genetic Resources Institute, Rome, Italy

  • Jaillon O, Aury J-M, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyère C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Fabbro CD, Alaux M, Gaspero GD, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Clainche IL, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pè ME, Valle G, Morgante M, Caboche M, Adam-Blondon A-F, Weissenbach J, Quétier F, Wincker P (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449(7161):463–467

    Article  CAS  PubMed  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444(7117):323–329

    Article  CAS  PubMed  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25(14):1754–1760

    Article  CAS  PubMed  Google Scholar 

  • Lu F, Lipka AE, Glaubitz J, Elshire R, Cherney JH, Casler MD, Buckler ES, Costish DE (2013) Switchgrass genomic diversity, ploidy, and evolution: novel insights from a network-based SNP discovery protocol. PLoS Genet 9(1):e1003215

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mahanil S, Ramming DW, Cadle-Davidson M, Owens CL, Garris A, Myles S, Cadle-Davidson L (2011) Development of marker sets useful in the early selection of Ren4 powdery mildew resistance and seedlessness for table and raisin grape breeding. Theor Appl Genet. doi:10.1007/s00122-011-1684-7

  • Moroldo M, Paillard S, Marconi R, Fabrice L, Canaguier A, Cruaud C, De Berardinis V, Guichard C, Brunaud V, Le Clainche I, Scalabrin S, Testolin R, Di Gaspero G, Morgante M, Adam-Blondon A (2008) A physical map of the heterozygous grapevine ‘Cabernet Sauvignon’ allows mapping candidate genes for disease resistance. BMC Plant Biol. doi:10.1186/1471-2229-8-66

  • Morrell PL, Buckler ES, Ross-Ibarra J (2012) Crop genomics: advances and applications. Nat Rev Genet 13(2):85–96

    CAS  Google Scholar 

  • Myles S, Chia J-M, Hurwitz B, Simon C, Zhong GY, Buckler E, Ware D (2010) Rapid genomic characterization of the genus Vitis. PLoS ONE. e8219. doi:10.1371/journal.pone.0008219

  • Myles S, Boyko AR, Owens CL, Brown PJ, Grassi F, Aradhya MK, Prins B, Reynolds A, Chia J-M, Ware D, Bustamante CD, Buckler ES (2011) Genetic structure and domestication history of the grape. Proc Natl Acad Sci USA 108(9):3530–3535

    Article  CAS  PubMed  Google Scholar 

  • Nielsen R, Paul JS, Albrechtsen A, Song YS (2011) Genotype and SNP calling from next-generation sequencing data. Nat Rev Genet 12(6):443–451

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pearson R (1988) Compendium of grape diseases. American Phytopathological Society (APS), Minnesota

    Google Scholar 

  • Peressotti E, Wiedemann-Merdinoglu S, Delmotte F, Bellin D, Di Gaspero G, Testolin R, Merdinoglu D, Mestre P (2010) Breakdown of resistance to grapevine downy mildew upon limited deployment of a resistant variety. BMC Plant Biol. doi:10.1186/1471-2229-10-147

  • Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ (2009) Shades of gray: the world of quantitative disease resistance. Trends Plant Sci 14(1):21–29

    Article  CAS  PubMed  Google Scholar 

  • Poland JA, Brown PJ, Sorrells ME, Jannink J-L (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS ONE. doi:10.1371/journal.pone.0032253

  • Pollard KS, Gilbert HN, Ge Y, Taylor S, Dudoit (2004) S multtest: resampling-based multiple hypothesis testing. R package version 2.12.0

  • Riaz S, Dangl GS, Edwards KJ, Meredith CP (2004) A microsatellite marker based framework linkage map of Vitis vinifera L. Theor Appl Genet 108(5):864–872

    Article  CAS  PubMed  Google Scholar 

  • Troggio M, Malacarne G, Coppola G, Segala C, Cartwright DA, Pindo M, Stefanini M, Mank R, Moroldo M, Morgante M, Grando MS, Velasco R (2007) A dense single-nucleotide polymorphism-based genetic linkage map of grapevine (Vitis vinifera L.) anchoring Pinot Noir Bacterial Artificial Chromosome contigs. Genetics 176(4):2637–2650

    Article  CAS  PubMed  Google Scholar 

  • Van Ooijen JW (2006). JoinMap® 4, Software for the calculation of genetic linkage maps in experimental populations. Kyazma, Wageningen, The Netherlands

  • Van Tassell CP, Smith TPL, Matukumalli LK, Taylor JF, Schnabel RD, Lawley CT, Haudenschild CD, Moore SS, Warren WC, Sonstegard TS (2008) SNP discovery and allele frequency estimation by deep sequencing of reduced representation libraries. Nat Meth 5(3):247–252

    Article  Google Scholar 

  • Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D, Pindo M, FitzGerald LM, Vezzulli S, Reid J, Malacarne G, Iliev D, Coppola G, Wardell B, Micheletti D, Macalma T, Facci M, Mitchell JT, Perazzolli M, Eldredge G, Gatto P, Oyzerski R, Moretto M, Gutin N, Stefanini M, Chen Y, Segala C, Davenport C, Demattè L, Mraz A, Battilana J, Stormo K, Costa F, Tao Q, Si-Ammour A, Harkins T, Lackey A, Perbost C, Taillon B, Stella A, Solovyev V, Fawcett JA, Sterck L, Vandepoele K, Grando SM, Toppo S, Moser C, Lanchbury J, Bogden R, Skolnick M, Sgaramella V, Bhatnagar SK, Fontana P, Gutin A, Van de Peer Y, Salamini F, Viola R (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS ONE. doi:10.1371/journal.pone.0001326

  • Wang N, Fang L, Xin H, Wang L, Li S (2012) Construction of a high-density genetic map for grape using next generation restriction-site associated DNA sequencing. BMC Plant Biol. doi:10.1186/1471-2229-12-148

  • Ward JA, Bhangoo J, Fernández-Fernández F, Moore P, Swanson JD, 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 Genomics. doi:10.1186/1471-2164-14-2

  • Wiedmann R, Smith T, Nonneman D (2008) SNP discovery in swine by reduced representation and high throughput pyrosequencing. BMC Genet. doi:10.1186/1471-2156-9-81

  • Xie W, Feng Q, Yu H, Huang X, Zhao Q, Xing Y, Yu S, Han B, Zhang Q (2010) Parent-independent genotyping for constructing an ultrahigh-density linkage map based on population sequencing. Proc Natl Acad Sci USA. doi:10.1073/pnas.1005931107

Download references

Acknowledgments

We thank Edward Buckler and Qi Sun for support with GBS procedures and genetic analysis; Alex Lipka for statistical advice; and Laura Shannon for her help in R/QTL use and linkage map construction. This research was supported by BecasChile, the USDA Viticulture Consortium—East, the New York Wine & Grape Foundation, and the Lake Erie Regional Grape Processors Fund. Partial funding was also provided by a USDA-National Institute of Food and Agriculture—Specialty Crop Research Initiative Competitive Grant, Award No. 2011-51181-30635.

Author information

Authors and Affiliations

  1. Department of Plant Breeding, Cornell University, Ithaca, NY, 14853, USA

    Paola Barba

  2. USDA/ARS Grape Genetics Research Unit, Geneva, NY, 14456, USA

    Lance Cadle-Davidson & Siraprapa Brooks

  3. Institute for Genomic Diversity, Cornell University, Ithaca, NY, 14853, USA

    James Harriman & Jeffrey C. Glaubitz

  4. Computational Biology Service Unit, Cornell University, Ithaca, NY, 14853, USA

    Katie Hyma

  5. Department of Horticulture, New York State Agricultural Experiment Station, Cornell University, Geneva, NY, 14456, USA

    Bruce Reisch

Authors
  1. Paola Barba
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lance Cadle-Davidson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. James Harriman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jeffrey C. Glaubitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Siraprapa Brooks
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Katie Hyma
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bruce Reisch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bruce Reisch.

Additional information

Communicated by R. Töpfer.

Electronic supplementary material

Below is the link to the electronic supplementary material.

122_2013_2202_MOESM1_ESM.tif

Suppl. S1 Number of crossovers per individual as a function of percentage of missing data. Individuals 2, 36, 45, 50, 55, 62, 66, 70, 74 and 76 showing an increased proportion of crossing over were discarded from the linkage analysis (TIFF 81 kb)

122_2013_2202_MOESM2_ESM.pdf

Suppl. S2 The allelic state of each significant SNP in each of the parents and progeny. For each progeny, ‘Chardonnay’ (Ch) and Vitis rupestris B38 (R), each of these biallelic SNPs is coded as dark red or light red, with a blank for missing data. Marker name corresponds with chromosome location in the PN40024 reference genome. S20 markers have not been assigned to a chromosome, and S27 corresponds to unassembled portions of chromosome 7. Locus LD reports the reference chromosome to which the marker was in linkage disequilibrium. S10_16893872 was not in LD with any PN40024 reference chromosome (PDF 36 kb)

122_2013_2202_MOESM3_ESM.pdf

Suppl. S3 Linkage disequilibrium of single SNPs with whole genome SNPs from the corresponding parent, measured as D′. X axis indicates SNP position based on alignment to the physical map (PN40024). Additional information for each of these significant SNPs is provided in Table 2 (PDF 1072 kb)

122_2013_2202_MOESM4_ESM.tif

Suppl. S4 Linkage disequilibrium (LD) analysis based on D′ calculations for a full matrix of selected chromosomes of V. rupestris B38 (A) and ‘Chardonnay’ (B). Chromosomes 7 and 9 contain SNPs associated with powdery mildew resistance and chromosomes 6 and 16 are representative of the pattern observed among the remaining chromosomes. X- and Y-axes indicate SNP positions based on alignment to the physical map (PN40024). Markers with high D′ values are in LD (red to purple) as commonly seen by the within chromosome comparisons. Panel (C) represents an enlargement of the comparison between chromosomes 9 and 16 of ‘Chardonnay’. The arrow shows the position of significant marker S16_11260816. Alignment to the physical map placed this marker in chromosome 16, but LD analysis and the linkage map placed it on chromosome 9. (TIFF 586 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barba, P., Cadle-Davidson, L., Harriman, J. et al. Grapevine powdery mildew resistance and susceptibility loci identified on a high-resolution SNP map. Theor Appl Genet 127, 73–84 (2014). https://doi.org/10.1007/s00122-013-2202-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-013-2202-x

Keywords

Search

Navigation