Skip to main content
Log in

Breeding for grapevine downy mildew resistance: a review of “omics” approaches

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

Downy mildew (DM) is one of the most destructive diseases affecting viticulture, especially in temperate-humid climates. This pathogen is able to differentially attack leaves and grapes, and is currently controlled with repeated applications of fungicides that lead to environmental pollution, development of resistant strains, residual toxicity, and pathogen pressure. The use of resistant grapevine varieties, obtained through breeding programs, represents a potential alternative to control grapevine DM, although this approach is constrained by the limits of natural resistance. In this review, we describe the latest breakthroughs achieved in the exploitation of the host–pathogen interaction, which have led to the identification of DM resistance loci, with associated molecular markers, that can be employed to efficiently screen hybrid grapevines and improve (pre-)breeding programs. The development of controlled infection protocols and contemporary “omics” approaches (next generation sequencing/genomics, QTLomics, transcriptomics, proteomics and metabolomics) integrated with comparative studies are shedding light onto the early host responses to DM attack and the complex plant defence mechanisms that are triggered.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Adam-Blondon AF, Roux C, Claux D et al (2004) Mapping 245 SSR markers on the Vitis vinifera genome: a tool for grape genetics. Theor Appl Genet 109:1017–1027. doi:10.1007/s00122-004-1704-y

    Article  CAS  PubMed  Google Scholar 

  • Algarra Alarcon A, Lazazzara V, Cappellin L et al (2015) Emission of volatile sesquiterpenes and monoterpenes in grapevine genotypes following Plasmopara viticola inoculation in vitro. J Mass Spectrom 50:1013–1022. doi:10.1002/jms.3615

    Article  CAS  PubMed  Google Scholar 

  • Ali K, Maltese F, Figueiredo A et al (2012) Alterations in grapevine leaf metabolism upon inoculation with Plasmopara viticola in different time-points. Plant Sci 191–192:100–107. doi:10.1016/j.plantsci.2012.04.014

    Article  PubMed  CAS  Google Scholar 

  • Antolín MC, Santesteban H, Ayari M et al (2010) Grapevine fruiting cuttings: an experimental system to study grapevine physiology under water deficit conditions. In: Delrot S, Medrano H, Or E et al (eds) Methodologies and results in grapevine research. Springer, Netherlands, pp 151–163

    Chapter  Google Scholar 

  • Bacilieri R, Lacombe T, Le Cunff L et al (2013) Genetic structure in cultivated grapevines is linked to geography and human selection. BMC Plant Biol 13:25. doi:10.1186/1471-2229-13-25

    Article  PubMed  PubMed Central  Google Scholar 

  • Banani H, Roatti B, Ezzahi B et al (2014) Characterization of resistance mechanisms activated by Trichoderma harzianum T39 and benzothiadiazole to downy mildew in different grapevine cultivars. Plant Pathol 63:334–343. doi:10.1111/ppa.12089

    Article  CAS  Google Scholar 

  • Barabaschi D, Tondelli A, Desiderio F et al (2016) Next generation breeding. Plant Sci 242:3–13. doi:10.1016/j.plantsci.2015.07.010

    Article  CAS  PubMed  Google Scholar 

  • Bashir Z, Ahmad A, Shafique S et al (2013) Hypersensitive response—a biophysical phenomenon of producers. Eur J Microbiol Immunol 3:105–110. doi:10.1556/EuJMI.3.2013.2.3

    Article  Google Scholar 

  • Basler P, Pfenninger H (2003) Disease-resistant cultivars as a solution for organic viticulture. Acta Hortic 603:681–685. doi:10.17660/ActaHortic.2003.603.94

    Article  Google Scholar 

  • Batovska DI, Todorova IT, Nedelcheva DV et al (2008) Preliminary study on biomarkers for the fungal resistance in Vitis vinifera leaves. J Plant Physiol 165:791–795. doi:10.1016/j.jplph.2007.09.005

    Article  CAS  PubMed  Google Scholar 

  • Batovska DI, Todorova IT, Parushev SP et al (2009) Biomarkers for the prediction of the resistance and susceptibility of grapevine leaves to downy mildew. J Plant Physiol 166:781–785. doi:10.1016/j.jplph.2008.08.008

    Article  CAS  PubMed  Google Scholar 

  • Baudoin A, Olaya G, Delmotte F et al (2008) QoI resistance of Plasmopara viticola and Erysiphe necator in the mid-atlantic United States. Plant Heal Prog. doi:10.1094/PHP-2008-0211-02-RS.Abstract

    Google Scholar 

  • Becker L, Poutaraud A, Hamm G et al (2013) Metabolic study of grapevine leaves infected by downy mildew using negative ion electrospray—Fourier transform ion cyclotron resonance mass spectrometry. Anal Chim Acta 795:44–51. doi:10.1016/j.aca.2013.07.068

    Article  CAS  PubMed  Google Scholar 

  • Bellin D, Peressotti E, Merdinoglu D et al (2009) Resistance to Plasmopara viticola in grapevine “Bianca” is controlled by a major dominant gene causing localised necrosis at the infection site. Theor Appl Genet 120:163–176. doi:10.1007/s00122-009-1167-2

    Article  PubMed  Google Scholar 

  • Blasi P, Blanc S, Wiedemann-Merdinoglu S et al (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. doi:10.1007/s00122-011-1565-0

    Article  PubMed  Google Scholar 

  • Blum M, Waldner M, Gisi U (2010) A single point mutation in the novel PvCesA3 gene confers resistance to the carboxylic acid amide fungicide mandipropamid in Plasmopara viticola. Fungal Genet Biol 47:499–510. doi:10.1016/j.fgb.2010.02.009

    Article  CAS  PubMed  Google Scholar 

  • Boso S, Kassemeyer HH (2008) Different susceptibility of European grapevine cultivars for downy mildew. Vitis - J Grapevine Res 47:39–49

    Google Scholar 

  • Boso S, Santiago JL, Martínez MC (2004) Resistance of eight different clones of the grape cultivar Albariño to Plasmopara viticola. Plant Dis 88:741–744. doi:10.1094/PDIS.2004.88.7.741

    Article  Google Scholar 

  • Boso S, Alonso-Villaverde V, Santiago JL et al (2010) Macro- and microscopic leaf characteristics of six grapevine genotypes (Vitis spp.) with different susceptibilities to grapevine downy mildew. Vitis - J Grapevine Res 49:43–50

    Google Scholar 

  • Boso S, Alonso-Villaverde V, Gago P et al (2011) Susceptibility of 44 grapevine (Vitis vinifera L.) varieties to downy mildew in the field. Aust J Grape Wine Res 17:394–400. doi:10.1111/j.1755-0238.2011.00157.x

    Article  Google Scholar 

  • Boso S, Alonso-Villaverde V, Gago P et al (2014) Susceptibility to downy mildew (Plasmopara viticola) of different Vitis varieties. Crop Prot 63:26–35. doi:10.1016/j.cropro.2014.04.018

    Article  Google Scholar 

  • Bowers JE, Dangl GS, Meredith CP (1999) Development and characterization of additional microsatellite DNA markers for grape. Am J Enol Vitic 50:243–246

    CAS  Google Scholar 

  • Bozkurt TO, Schornack S, Banfield MJ, Kamoun S (2012) Oomycetes, effectors, and all that jazz. Curr Opin Plant Biol 15:483–492. doi:10.1016/j.pbi.2012.03.008

    Article  PubMed  Google Scholar 

  • Breitling R, Li Y, Tesson BM et al (2008) Genetical genomics: spotlight on QTL hotspots. PLoS Genet 4(10):e1000232. doi:10.1371/journal.pgen.1000232

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 

  • Buonassisi D, Cappellin L, Dolzani C, et al (submitted) Development of a novel phenotyping method to assess downy mildew symptoms on grapevine inflorescences

  • Buonassisi D, Perazzolli M, Tadiello A, et al (in preparation) Grapevine downy mildew dual epidemics: a leaf and inflorescence transcriptomics study

  • 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. doi:10.1094/PDIS-92-11-1577

    Article  Google Scholar 

  • Calonnec A, Wiedemann-Merdinoglu S, Delière L et al (2013) The reliability of leaf bioassays for predicting disease resistance on fruit: a case study on grapevine resistance to downy and powdery mildew. Plant Pathol 62:533–544. doi:10.1111/j.1365-3059.2012.02667.x

    Article  Google Scholar 

  • Casagrande K, Falginella L, Castellarin SD et al (2011) Defence responses in Rpv3-dependent resistance to grapevine downy mildew. Planta 234:1097–1109. doi:10.1007/s00425-011-1461-5

    Article  CAS  PubMed  Google Scholar 

  • Chin C-S, Peluso P, Sedlazeck FJ et al (2016) Phased diploid genome assembly with single-molecule real-time sequencing. Nat Methods 13:1050–1054. doi:10.1038/nmeth.4035

    Article  CAS  PubMed  Google Scholar 

  • Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host–microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814. doi:10.1016/j.cell.2006.02.008

    Article  CAS  PubMed  Google Scholar 

  • Cindric P, Korac N, Kovac V (2003) Grape breeding for resistance. Acta Hortic 603:385–391. doi:10.17660/ActaHortic.2003.603.49

    Article  Google Scholar 

  • Costa F (2015) MetaQTL analysis provides a compendium of genomic loci controlling fruit quality traits in apple. Tree Genet Genomes 11:819. doi:10.1007/s11295-014-0819-9

    Article  Google Scholar 

  • Crespan M (2003) The parentage of Muscat of Hamburg. Vitis - J Grapevine Res 42:193–197

    CAS  Google Scholar 

  • Cui H, Tsuda K, Parker JE (2015) Effector-triggered immunity: from pathogen perception to robust defense. Annu Rev Plant Biol 66:487–511. doi:10.1146/annurev-arplant-050213-040012

    Article  CAS  PubMed  Google Scholar 

  • Dèglene-Benbrahim L, Wiedemann-Merdinoglu S, Merdinoglu D, Walter B (2010) Evaluation of downy mildew resistance in grapevine by leaf disc bioassay with in vitro- and greenhouse-grown plants. Am J Enol Vitic 61:521–528. doi:10.5344/ajev.2010.10009

    Article  Google Scholar 

  • Delmotte F, Chen WJ, Richard-Cervera S et al (2006) Microsatellite DNA markers for Plasmopara viticola, the causal agent of downy mildew of grapes. Mol Ecol Notes 6:379–381. doi:10.1111/j.1471-8286.2005.01240.x

    Article  CAS  Google Scholar 

  • Delmotte F, Machefer V, Giresse X et al (2011) Characterization of single-nucleotide-polymorphism markers for Plasmopara viticola, the causal agent of grapevine downy mildew. Appl Environ Microbiol 77:7861–7863. doi:10.1128/AEM.05782-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Demaree JB, Dix IW, Magoon CA (1937) Observations on the resistance of grape varieties to black rot and downy mildew. Proc Am Soc Hortic Sci 35:451–460

    Google Scholar 

  • Deschamps S, Llaca V, May GD (2012) Genotyping-by-Sequencing in plants. Biology 1:460–483. doi:10.3390/biology1030460

    PubMed  Google Scholar 

  • Di Gaspero G, Foria S (2015) Molecular grapevine breeding techniques. In: Elsevier (ed) Grapevine breeding programs for the wine industry. Elsevier, New York, pp 23–37

  • Di Gaspero G, Copetti D, Coleman C et al (2012) Selective sweep at the Rpv3 locus during grapevine breeding for downy mildew resistance. Theor Appl Genet 124:277–286. doi:10.1007/s00122-011-1703-8

    Article  PubMed  Google Scholar 

  • Díez-Navajas AM, Greif C, Poutaraud A, Merdinoglu D (2007) Two simplified fluorescent staining techniques to observe infection structures of the oomycete Plasmopara viticola in grapevine leaf tissues. Micron 38:680–683. doi:10.1016/j.micron.2006.09.009

    Article  PubMed  CAS  Google Scholar 

  • Díez-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. doi:10.1094/PHYTO-98-7-0776

    Article  PubMed  Google Scholar 

  • Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11:539–548. doi:10.1038/nrg2812

    Article  CAS  PubMed  Google Scholar 

  • Dussert Y, Gouzy J, Richart-Cervera S et al (2016) Draft genome sequence of Plasmopara viticola, the grapevine downy mildew pathogen. Genome Announc 4:e00987. doi:10.1128/genomeA.00987-16

    Article  PubMed  PubMed Central  Google Scholar 

  • Ehrhardt C, Arapitsas P, Stefanini M et al (2014) Analysis of the phenolic composition of fungus-resistant grape varieties cultivated in Italy and Germany using UHPLC-MS/MS. J Mass Spectrom 49:860–869. doi:10.1002/jms.3440

    Article  CAS  PubMed  Google Scholar 

  • Eibach R, Töpfer R (2003) Success in resistance breeding: “Regent” and its steps into the market. Acta Hortic 603:687–691

    Article  Google Scholar 

  • Eibach R, Töpfer R (2015) Traditional grapevine breeding techniques. Grapevine breeding programs for the wine industry. Elsevier Ltd, New York, pp 3–22

    Chapter  Google Scholar 

  • Eibach R, Diehl H, Alleweldt G (1989) Untersuchungen zur Vererbung von Resistenzeigenschaften bei Reben gegen Oidium tuckeri, Plasmopara viticola und Botrytis cinerea. Vitis - J Grapevine Res 28:209–228

    Google Scholar 

  • Emanuelli F, Lorenzi S, Grzeskowiak L et al (2013) Genetic diversity and population structure assessed by SSR and SNP markers in a large germplasm collection of grape. BMC Plant Biol 13:39. doi:10.1186/1471-2229-13-39

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan JJ, Wang P, Xu X et al (2015) Characterization of a TIR-NBS-LRR gene associated with downy mildew resistance in grape. Genet Mol Res 14:7964–7975. doi:10.4238/2015.July.17.4

    Article  CAS  PubMed  Google Scholar 

  • Fawke S, Doumane M, Schornack S (2015) Oomycete interactions with plants: infection strategies and resistance principles. Microbiol Mol Biol Rev 79:263–280. doi:10.1128/MMBR.00010-15

    Article  PubMed  PubMed Central  Google Scholar 

  • Feau N, Taylor G, Dale AL et al (2016) Genome sequences of six Phytophthora species threatening forest ecosystems. Genom Data 10:85–88. doi:10.1016/j.gdata.2016.09.013

    Article  PubMed  PubMed Central  Google Scholar 

  • Figueiredo A, Fortes AM, Ferreira S et al (2008) Transcriptional and metabolic profiling of grape (Vitis vinifera L.) leaves unravel possible innate resistance against pathogenic fungi. J Exp Bot 59:3371–3381. doi:10.1093/jxb/ern187

    Article  CAS  PubMed  Google Scholar 

  • Figueiredo A, Monteiro F, Fortes AM et al (2012) Cultivar-specific kinetics of gene induction during downy mildew early infection in grapevine. Funct Integr Genom 12:379–386. doi:10.1007/s10142-012-0261-8

    Article  CAS  Google Scholar 

  • Figueiredo A, Martins J, Sebastiana M et al (2017) Specific adjustments in grapevine leaf proteome discriminating resistant and susceptible grapevine genotypes to Plasmopara viticola. J Proteom 152:48–57. doi:10.1016/j.jprot.2016.10.012

    Article  CAS  Google Scholar 

  • Fischer BM, Salakhutdinov I, Akkurt M et al (2004) Quantitative trait locus analysis of fungal disease resistance factors on a molecular map of grapevine. Theor Appl Genet 108:501–515. doi:10.1007/s00122-003-1445-3

    Article  CAS  PubMed  Google Scholar 

  • Gauthier A, Trouvelot S, Kelloniemi J et al (2014) The sulfated laminarin triggers a stress transcriptome before priming the SA- and ROS-dependent defenses during grapevine’s induced resistance against Plasmopara viticola. PLoS ONE 9:e88145. doi:10.1371/journal.pone.0088145

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gessler C, Pertot I, Perazzolli M (2011) Plasmopara viticola: a review of knowledge on downy mildew of grapevine and effective disease management. Phytopathol Mediterr 50:3–44. doi:10.14601/Phytopathol_Mediterr-9360

    Google Scholar 

  • Gindro K, Spring JL, Pezet R et al (2006) Histological and biochemical criteria for objective and early selection of grapevine cultivars resistant to Plasmopara viticola. Vitis - J Grapevine Res 45:191–196

    Google Scholar 

  • Gindro K, Alonso-Villaverde V, Voinesco F et al (2012) Susceptibility to downy mildew in grape clusters: new microscopical and biochemical insights. Plant Physiol Biochem 52:140–146. doi:10.1016/j.plaphy.2011.12.009

    Article  CAS  PubMed  Google Scholar 

  • Gisi U, Waldner M, Kraus N et al (2007) Inheritance of resistance to carboxylic acid amide (CAA) fungicides in Plasmopara viticola. Plant Pathol 56:199–208. doi:10.1111/j.1365-3059.2006.01512.x

    Article  CAS  Google Scholar 

  • Gobbin D, Pertot I, Gessler C (2003a) Genetic structure of a Plasmopara viticola population in an isolated Italian mountain vineyard. J Phytopathol 151:636–646. doi:10.1046/j.0931-1785.2003.00779.x

    Article  CAS  Google Scholar 

  • Gobbin D, Pertot I, Gessler C (2003b) Identification of microsatellite markers for Plasmopara viticola and establishment of high throughput method for SSR analysis. Eur J Plant Pathol 109:153–164. doi:10.1023/A:1022565405974

    Article  CAS  Google Scholar 

  • Gobbin D, Jermini M, Loskill B et al (2005) Importance of secondary inoculum of Plasmopara viticola to epidemics of grapevine downy mildew. Plant Pathol 54:522–534. doi:10.1111/j.1365-3059.2005.01208.x

    Article  Google Scholar 

  • Gobbin D, Rumbou A, Linde CC, Gessler C (2006) Population genetic structure of Plasmopara viticola after 125 years of colonization in European vineyards. Mol Plant Pathol 7:519–531. doi:10.1111/j.1364-3703.2006.00357.x

    Article  CAS  PubMed  Google Scholar 

  • Goffinet B, Gerber S (2000) Quantitative trait loci: a meta-analysis. Genetics 155:463–473

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grenville-Briggs LJ, Anderson VL, Fugelstad J et al (2008) Cellulose synthesis in Phytophthora infestans is required for normal appressorium formation and successful infection of potato. Plant Cell 20:720–738. doi:10.1105/tpc.107.052043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grimplet J, Cramer GR, Dickerson JA et al (2009) VitisNet: “Omics” integration through grapevine molecular networks. PLoS ONE 4:1–11. doi:10.1371/journal.pone.0008365

    Article  CAS  Google Scholar 

  • Guedes de Pinho P, Bertrand A (1995) Analytical determination of furaneol (2,5-dimethyl1-4-hydroxy-3(2H)-furanone). Application to differentiation of white wines from hybrid and various Vitis vinifera cultivars. Am J Enol Vitic 46:181–186

    CAS  Google Scholar 

  • Guillier C, Gamm M, Lucchi G et al (2015) Toward the identification of two glycoproteins involved in the stomatal deregulation of downy mildew-infected grapevine leaves. Mol Plant-Microbe Interact 28:1227–1236. doi:10.1094/MPMI-05-15-0115-R

    Article  CAS  PubMed  Google Scholar 

  • Haas BJ, Kamoun S, Zody MC et al (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:393–398. doi:10.1038/nature08358

    Article  CAS  PubMed  Google Scholar 

  • He M, Xu Y, Cao J et al (2013) Subcellular localization and functional analyses of a PR10 protein gene from Vitis pseudoreticulata in response to Plasmopara viticola infection. Protoplasma 250:129–140. doi:10.1007/s00709-012-0384-8

    Article  CAS  PubMed  Google Scholar 

  • He J, Zhao X, Laroche A et al (2014) Genotyping-by-sequencing (GBS), an ultimate marker-assisted selection (MAS) tool to accelerate plant breeding. Front Plant Sci 5:484. doi:10.3389/fpls.2014.00484

    Article  PubMed  PubMed Central  Google Scholar 

  • Heath MC (2000) Nonhost resistance and nonspecific plant defenses. Curr Opin Plant Biol 3:315–319. doi:10.1016/S1369-5266(00)00087-X

    Article  CAS  PubMed  Google Scholar 

  • Herman M, Williams M (2012) Fighting for their lives: plants and pathogens. Plant Cell 24:1–15. doi:10.1105/tpc.112.tt0612

    Article  CAS  Google Scholar 

  • Hood ME, Shew HD (1996) Applications of KOH-aniline blue fluorescence in the study of plant–fungal interactions. Phytopathology 86:704. doi:10.1094/Phyto-86-704

    Article  Google Scholar 

  • Jaillon O, Aury J-M, Noel B et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467. doi:10.1038/nature06148

    Article  CAS  PubMed  Google Scholar 

  • Jansen RC, Nap J-P (2001) Genetical genomics: the added value from segregation. Trends Genet 17:388–391. doi:10.1016/S0168-9525(01)02310-1

    Article  CAS  PubMed  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329. doi:10.1038/nature05286

    Article  CAS  PubMed  Google Scholar 

  • Jürges G, Kassemeyer H-H, Dürrenberger M et al (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. doi:10.1111/j.1438-8677.2008.00182.x

    Article  PubMed  Google Scholar 

  • Katula-Debreceni D, Lencsés AK, Szőke A et al (2010) Marker-assisted selection for two dominant powdery mildew resistance genes introgressed into a hybrid grape population. Sci Hortic (Amsterdam) 126:448–453. doi:10.1016/j.scienta.2010.08.012

    Article  CAS  Google Scholar 

  • Kennelly MM, Gadoury DM, Wilcox WF et al (2005) Seasonal development of ontogenic resistance to downy mildew in grape berries and rachises. Phytopathology 95:1445–1452. doi:10.1094/PHYTO-95-1445

    Article  PubMed  Google Scholar 

  • Kiefer B, Riemann M, Büche C et al (2002) The host guides morphogenesis and stomatal targeting in the grapevine pathogen Plasmopara viticola. Planta 215:387–393. doi:10.1007/s00425-002-0760-2

    Article  CAS  PubMed  Google Scholar 

  • Kim Khiook IL, Schneider C, Heloir M-C et al (2013) Image analysis methods for assessment of H2O2 production and Plasmopara viticola development in grapevine leaves: application to the evaluation of resistance to downy mildew. J Microbiol Methods 95:235–244. doi:10.1016/j.mimet.2013.08.012

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Koopman T, Linde CC, Fourie PH, MCLeod A (2007) Population genetic structure of Plasmopara viticola in the Western Cape Province of South Africa. Mol Plant Pathol 8:723–736. doi:10.1111/j.1364-3703.2007.00429.x

    Article  PubMed  Google Scholar 

  • Kortekamp A (2006) Expression analysis of defence-related genes in grapevine leaves after inoculation with a host and a non-host pathogen. Plant Physiol Biochem 44:58–67. doi:10.1016/j.plaphy.2006.01.008

    Article  CAS  PubMed  Google Scholar 

  • Kortekamp A, Zyprian E (2003) Characterization of Plasmopara-resistance in grapevine using in vitro plants. J Plant Physiol 160:1393–1400. doi:10.1078/0176-1617-01021

    Article  CAS  PubMed  Google Scholar 

  • Lafon R, Clerjeau M (1988) Downy mildew. In: Pearson RC, Goheen AC (eds) Compendium of grape diseases. APS Press, St. Paul, pp 11–13

    Google Scholar 

  • Langcake P, Pryce RJ (1977) Oxidative dimerisation of 4-hydroxystilbenes in vitro: production of a grapevine phytoalexin mimic. J Chem Soc Chem Commun. doi:10.1039/c39770000208

    Google Scholar 

  • Latouche G, Bellow S, Poutaraud A et al (2013) Influence of constitutive phenolic compounds on the response of grapevine (Vitis vinifera L.) leaves to infection by Plasmopara viticola. Planta 237:351–361. doi:10.1007/s00425-012-1776-x

    Article  CAS  PubMed  Google Scholar 

  • Le Cunff L, Fournier-Level A, Laucou V et al (2008) Construction of nested genetic core collections to optimize the exploitation of natural diversity in Vitis vinifera L. subsp sativa. BMC Plant Biol 8:31. doi:10.1186/1471-2229-8-31

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Legay G, Marouf E, Berger D et al (2011) Identification of genes expressed during the compatible interaction of grapevine with Plasmopara viticola through suppression subtractive hybridization (SSH). Eur J Plant Pathol 129:281–301. doi:10.1007/s10658-010-9676-z

    Article  Google Scholar 

  • Lemaître-Guillier C, Hovasse A, Schaeffer-Reiss C et al (2017) Proteomics towards the understanding of elicitor induced resistance of grapevine against downy mildew. J Proteom 156:113–125. doi:10.1016/j.jprot.2017.01.016

    Article  CAS  Google Scholar 

  • Li X, Wu J, Yin L et al (2015) Comparative transcriptome analysis reveals defense-related genes and pathways against downy mildew in Vitis amurensis grapevine. Plant Physiol Biochem 95:1–14. doi:10.1016/j.plaphy.2015.06.016

    Article  PubMed  CAS  Google Scholar 

  • Liu R, Wang L, Zhu J et al (2014) Histological responses to downy mildew in resistant and susceptible grapevines. Protoplasma 252:259–270. doi:10.1007/s00709-014-0677-1

    Article  PubMed  CAS  Google Scholar 

  • Lodhi MA, Ye G-NN, Weeden NF et al (1995) A molecular marker based linkage map of Vitis. Genome 38:786–794. doi:10.1139/g95-100

    Article  CAS  PubMed  Google Scholar 

  • Luis P, Gauthier A, Trouvelot S et al (2013) Identification of Plasmopara viticola genes potentially involved in pathogenesis on grapevine suggests new similarities between oomycetes and true fungi. Phytopathology 103:1035–1044. doi:10.1094/PHYTO-06-12-0121-R

    Article  CAS  PubMed  Google Scholar 

  • Malacarne G, Vrhovsek U, Zulini L et al (2011) Resistance to Plasmopara viticola in a grapevine segregating population is associated with stilbenoid accumulation and with specific host transcriptional responses. BMC Plant Biol 11:114. doi:10.1186/1471-2229-11-114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malacarne G, Perazzolli M, Cestaro A et al (2012) Deconstruction of the (paleo) polyploid grapevine genome based on the analysis of transposition events involving NBS resistance genes. PLoS ONE. doi:10.1371/journal.pone.0029762

    PubMed  PubMed Central  Google Scholar 

  • Marguerit E, Boury C, Manicki A et al (2009) Genetic dissection of sex determinism, inflorescence morphology and downy mildew resistance in grapevine. Theor Appl Genet 118:1261–1278. doi:10.1007/s00122-009-0979-4

    Article  PubMed  Google Scholar 

  • Matasci CL, Gobbin D, Schärer H-J et al (2008) Selection for fungicide resistance throughout a growing season in populations of Plasmopara viticola. Eur J Plant Pathol 120:79–83. doi:10.1007/s10658-007-9190-0

    Article  CAS  Google Scholar 

  • Maul E, Sudharma KN, Kecke S et al (2012) The European vitis database (www.eu-vitis.de)—a technical innovation through an online uploading and interactive modification system. Vitis - J Grapevine Res 51:79–85

    Google Scholar 

  • Merdinoglu D, Wiedemann-Merdinoglu S, Coste P et al (2003) Genetic analysis of downy mildew resistance derived from Muscadinia rotundifolia. Acta Hortic 603:451–456

    Article  CAS  Google Scholar 

  • Mestre P, Piron M-C, Merdinoglu D (2012) Identification of effector genes from the phytopathogenic oomycete Plasmopara viticola through the analysis of gene expression in germinated zoospores. Fungal Biol 116:825–835. doi:10.1016/j.funbio.2012.04.016

    Article  CAS  PubMed  Google Scholar 

  • Mestre P, Carrere S, Gouzy J et al (2016) Comparative analysis of expressed CRN and RXLR effectors from two Plasmopara species causing grapevine and sunflower downy mildew. Plant Pathol 65:767–781. doi:10.1111/ppa.12469

    Article  CAS  Google Scholar 

  • Milli A, Cecconi D, Bortesi L et al (2012) Proteomic analysis of the compatible interaction between Vitis vinifera and Plasmopara viticola. J Proteom 75:1284–1302. doi:10.1016/j.jprot.2011.11.006

    Article  CAS  Google Scholar 

  • Mochizuki M, Aoki Y, Suzuki S (2012) Detection and analysis of genetic variations in GOB locus of Plasmopara viticola by DNA sequence analysis. J Gen Plant Pathol 78:170–175. doi:10.1007/s10327-012-0368-8

    Article  CAS  Google Scholar 

  • Moreira FM, Madini A, Marino R et al (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. doi:10.1007/s11295-010-0322-x

    Article  Google Scholar 

  • Moroldo M, Paillard S, Marconi R et al (2008) A physical map of the heterozygous grapevine “Cabernet Sauvignon” allows mapping candidate genes for disease resistance. BMC Plant Biol 8:66. doi:10.1186/1471-2229-8-66

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mullins MG (1966) Test-plants for investigations of the physiology of fruiting in Vitis vinifera L. Nature 209:419–420. doi:10.1038/209419a0

    Article  Google Scholar 

  • Mullins MG, Rajasekaran K (1981) Fruiting cuttings: revides method for producing test plants of grapevine cultivars. Am J Enol Vitic 32:35–40

    Google Scholar 

  • Musetti R, Stringher L, Borselli S et al (2005) Ultrastructural analysis of Vitis vinifera leaf tissues showing atypical symptoms of Plasmopara viticola. Micron 36:73–80. doi:10.1016/j.micron.2004.05.002

    Article  CAS  PubMed  Google Scholar 

  • Musetti R, Vecchione A, Stringher L et al (2006) Inhibition of sporulation and ultrastructural alterations of grapevine downy mildew by the endophytic fungus Alternaria alternata. Phytopathology 96:689–698. doi:10.1094/PHYTO-96-0689

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa S, Komatsu H, Yuda E (1980) A study of micro-morphology of grape berry surface during their development with speciai reference to stoma. J Japanese Soc Hortic Sci 49:1–7. doi:10.2503/jjshs.49.1

    Article  Google Scholar 

  • Nascimento-Gavioli MCA, Agapito-Tenfen SZ, Nodari RO et al (2016) Proteome of Plasmopara viticola-infected Vitis vinifera provides insights into grapevine Rpv1/Rpv3 pyramided resistance to downy mildew. J Proteom. doi:10.1016/j.jprot.2016.05.024

    Google Scholar 

  • Newman M-A, Sundelin T, Nielsen JT, Erbs G (2013) MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front Plant Sci 4:139. doi:10.3389/fpls.2013.00139

    Article  PubMed  PubMed Central  Google Scholar 

  • Nicolas SD, Péros J-P, Lacombe T et al (2016) Genetic diversity, linkage disequilibrium and power of a large grapevine (Vitis vinifera L) diversity panel newly designed for association studies. BMC Plant Biol 16:74. doi:10.1186/s12870-016-0754-z

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ochssner I, Hausmann L, Töpfer R (2016) Rpv14, a new genetic source for Plasmopara viticola resistance conferred by Vitis cinerea. Vitis - J Grapevine Res 55:79–81. doi:10.5073/vitis.2016.55.79-81

    Google Scholar 

  • OEPP/EPPO 2001. Guidelines for the efficacy evaluation of fungicides. OEPP/EPPO Bullettin, 31, 313–317

  • OIV (2009) Descriptor list for grape varieties and Vitis species, 2nd edn. Office International de la Vigne et du Vin, Paris

    Google Scholar 

  • Ollat N, Geny L, Soyer JP (1998) Grapevine fruiting cuttings: validation of an experimental system to study grapevine physiology. I. Main vegetative characteristics. OENO One 32:1–9. doi:10.20870/oeno-one.1998.32.1.1061

    Article  Google Scholar 

  • Pacifico D, Gaiotti F, Giusti M, Tomasi D (2013) Performance of interspecific grapevine varieties in north-east Italy. Agric Sci 04:91–101. doi:10.4236/as.2013.42015

    Google Scholar 

  • Palmieri MC, Perazzolli M, Matafora V et al (2012) Proteomic analysis of grapevine resistance induced by Trichoderma harzianum T39 reveals specific defence pathways activated against downy mildew. J Exp Bot 63:6237–6251. doi:10.1093/jxb/ers279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pavloušek P (2012) Evaluation of foliar resistance of grapevine genetic resources to downy mildew (Plasmopara viticola). Acta Univ Agric Silvic Mendelianae Brun 60:191–198. doi:10.11118/actaun201260080191

    Article  Google Scholar 

  • Pedneault K, Provost C (2016) Fungus resistant grape varieties as a suitable alternative for organic wine production: benefits, limits, and challenges. Sci Hortic (Amsterdam) 208:57–77. doi:10.1016/j.scienta.2016.03.016

    Article  CAS  Google Scholar 

  • Perazzolli M, Moretto M, Fontana P et al (2012) Downy mildew resistance induced by Trichoderma harzianum T39 in susceptible grapevines partially mimics transcriptional changes of resistant genotypes. BMC Genom 13:660. doi:10.1186/1471-2164-13-660

    Article  CAS  Google Scholar 

  • Perazzolli M, Palmieri MC, Matafora V et al (2016) Phosphoproteomic analysis of induced resistance reveals activation of signal transduction processes by beneficial and pathogenic interaction in grapevine. J Plant Physiol 195:59–72. doi:10.1016/j.jplph.2016.03.007

    Article  CAS  PubMed  Google Scholar 

  • Peressotti E, Wiedemann-Merdinoglu S, Delmotte F et al (2010) Breakdown of resistance to grapevine downy mildew upon limited deployment of a resistant variety. BMC Plant Biol 10:147. doi:10.1186/1471-2229-10-147

    Article  PubMed  PubMed Central  Google Scholar 

  • Peressotti E, Duchêne E, Merdinoglu D, Mestre P (2011) A semi-automatic non-destructive method to quantify grapevine downy mildew sporulation. J Microbiol Methods 84:265–271. doi:10.1016/j.mimet.2010.12.009

    Article  PubMed  Google Scholar 

  • Peressotti E, Dolzani C, Poles L et al (2015) First pedigree-based analysis (PBA) approach for the dissection of disease resistance traits in grapevine hybrids. Acta Hortic 1082:113–121. doi:10.17660/ActaHortic.2015.1082.15

    Article  Google Scholar 

  • Pezet R, Perret C, Jean-Denis JB et al (2003) δ-viniferin, a resveratrol dehydrodimer: one of the major stilbenes synthesized by stressed grapevine leaves. J Agric Food Chem 51:5488–5492. doi:10.1021/jf030227o

    Article  CAS  PubMed  Google Scholar 

  • Pimentel D (2005) Environmental and economic costs of the application of pesticides primarily in the United States’. Environ Dev Sustain 7:229–252. doi:10.1007/s10668-005-7314-2

    Article  Google Scholar 

  • Polesani M, Desario F, Ferrarini A et al (2008) cDNA-AFLP analysis of plant and pathogen genes expressed in grapevine infected with Plasmopara viticola. BMC Genom 9:142. doi:10.1186/1471-2164-9-142

    Article  CAS  Google Scholar 

  • Polesani M, Bortesi L, Ferrarini A et al (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. doi:10.1186/1471-2164-11-117

    Article  CAS  Google Scholar 

  • Prajongjai T, Poolsawat O, Pombungkerd P et al (2014) Evaluation of grapevines for resistance to downy mildew (Plasmopara viticola) under laboratory and field conditions. S Afr J Enol Vitic 35:43–50

    Google Scholar 

  • Raaymakers TM, Van Den Ackerveken G, Van den Ackerveken G (2016) Extracellular recognition of oomycetes during biotrophic infection of plants. Front Plant Sci 7:1–12. doi:10.3389/fpls.2016.00906

    Article  Google Scholar 

  • Reuveni M (1998) Relationships between leaf age, peroxidase and β-1,3-glucanase activity, and resistance to downy mildew in grapevines. J Phytopathol 146:525–530. doi:10.1111/j.1439-0434.1998.tb04615.x

    Article  Google Scholar 

  • Rossin G, Villalta D, Martelli P et al (2015) Grapevine downy mildew Plasmopara viticola infection elicits the expression of allergenic pathogenesis-related proteins. Int Arch Allergy Immunol 168:90–95. doi:10.1159/000441792

    Article  CAS  PubMed  Google Scholar 

  • Rouxel M, Papura D, Nogueira M et al (2012) Microsatellite markers for characterization of native and introduced populations of Plasmopara viticola, the causal agent of grapevine downy mildew. Appl Environ Microbiol 78:6337–6340. doi:10.1128/AEM.01255-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rouxel M, Mestre P, Comont G et al (2013) Phylogenetic and experimental evidence for host-specialized cryptic species in a biotrophic oomycete. New Phytol 197:251–263. doi:10.1111/nph.12016

    Article  PubMed  Google Scholar 

  • Rouxel M, Mestre P, Baudoin A et al (2014) Geographic distribution of cryptic species of Plasmopara viticola causing downy mildew on wild and cultivated grape in Eastern North America. Phytopathology 104:692–701. doi:10.1094/PHYTO-08-13-0225-R

    Article  PubMed  Google Scholar 

  • Ruehl E, Schmid J, Eibach R, Töpfer R (2015) Grapevine breeding programmes in Germany. In: Reynolds AG (Elsevier) Grapevine breeding programs for the wine industry, 1st edn. Woodhead Publishing, Cambridge, 5:77–101

  • Rumbou A, Gessler C (2004) Genetic dissection of Plasmopara viticola population from a Greek vineyard in two consecutive years. Eur J Plant Pathol 110:379–392. doi:10.1023/B:EJPP.0000021061.38154.22

    Article  CAS  Google Scholar 

  • Salvi S, Tuberosa R (2015) The crop QTLome comes of age. Curr Opin Biotechnol 32:179–185. doi:10.1016/j.copbio.2015.01.001

    Article  CAS  PubMed  Google Scholar 

  • Savary S, Delbac L, Rochas A et al (2009) Analysis of nonlinear relationships in dual epidemics, and its application to the management of grapevine downy and powdery mildews. Phytopathology 99:930–942. doi:10.1094/PHYTO-99-8-0930

    Article  PubMed  Google Scholar 

  • Scalabrin S, Troggio M, Moroldo M et al (2010) Physical mapping in highly heterozygous genomes: a physical contig map of the Pinot Noir grapevine cultivar. BMC Genom 11:204. doi:10.1186/1471-2164-11-204

    Article  CAS  Google Scholar 

  • Schwander F, Eibach R, Fechter I et al (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. doi:10.1007/s00122-011-1695-4

    Article  CAS  PubMed  Google Scholar 

  • Seehalak W, Moonsom S, Metheenukul P, Tantasawat P (2011) Isolation of resistance gene analogs from grapevine resistant and susceptible to downy mildew and anthracnose. Sci Hortic (Amsterdam) 128:357–363. doi:10.1016/j.scienta.2011.01.003

    Article  CAS  Google Scholar 

  • Sharma R, Xia X, Cano LM et al (2015) Genome analyses of the sunflower pathogen Plasmopara halstedii provide insights into effector evolution in downy mildews and Phytophthora. BMC Genom 16:1–23. doi:10.1186/s12864-015-1904-7

    Article  CAS  Google Scholar 

  • Sotolář R (2007) Comparison of grape seedlings population against downy mildew by using different provocation methods. Vitis - J Grapevine Res 35:61–68

    Google Scholar 

  • Staudt G, Kassemeyer H (1995) Evaluation of downy mildew resistance in various accessions of wild Vitis species. Vitis - J Grapevine Res 34:225–228

    Google Scholar 

  • Steimetz E, Trouvelot S, Gindro K et al (2012) Influence of leaf age on induced resistance in grapevine against Plasmopara viticola. Physiol Mol Plant Pathol 79:89–96. doi:10.1016/j.pmpp.2012.05.004

    Article  CAS  Google Scholar 

  • Tena G, Boudsocq M, Sheen J (2011) Protein kinase signaling networks in plant innate immunity. Curr Opin Plant Biol 14:519–529. doi:10.1016/j.pbi.2011.05.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • This P, Jung A, Boccacci P et al (2004) Development of a standard set of microsatellite reference alleles for identification of grape cultivars. Theor Appl Genet 109:1448–1458. doi:10.1007/s00122-004-1760-3

    Article  CAS  PubMed  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley–powdery mildew interaction. Plant J 11:1187–1194. doi:10.1046/j.1365-313X.1997.11061187.x

    Article  CAS  Google Scholar 

  • Toffolatti S, Venturini G, Maffi D, Vercesi A (2012) Phenotypic and histochemical traits of the interaction between Plasmopara viticola and resistant or susceptible grapevine varieties. BMC Plant Biol 12:124. doi:10.1186/1471-2229-12-124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trouvelot S, Varnier A-L, Allègre M et al (2008) A β-1,3 glucan sulfate induces resistance in grapevine against Plasmopara viticola through priming of defense responses, including HR-like cell death. Mol Plant-Microbe Interact 21:232–243. doi:10.1094/MPMI-21-2-0232

    Article  CAS  PubMed  Google Scholar 

  • Tyler BM, Tripathy S, Zhang X, Dehal P (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313:1261–1266. doi:10.1126/science.1128796

    Article  CAS  PubMed  Google Scholar 

  • Unger S, Büche C, Boso S, Kassemeyer H-H (2007) The course of colonization of two different vitis genotypes by Plasmopara viticola indicates compatible and incompatible host-pathogen interactions. Phytopathology 97:780–786. doi:10.1094/PHYTO-97-7-0780

    Article  PubMed  Google Scholar 

  • 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. doi:10.1007/s10681-014-1167-4

    Article  CAS  Google Scholar 

  • Vannozzi A, Dry IB, Fasoli M et al (2012) Genome-wide analysis of the grapevine stilbene synthase multigenic family: genomic organization and expression profiles upon biotic and abiotic stresses. BMC Plant Biol 12:130. doi:10.1186/1471-2229-12-130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Velasco R, Zharkikh A, Troggio M et al (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS ONE 2:e1326. doi:10.1371/journal.pone.0001326

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Venuti S, Copetti D, Foria S et al (2013) Historical introgression of the downy mildew resistance gene Rpv12 from the asian species Vitis amurensis into grapevine varieties. PLoS ONE 8:e61228. doi:10.1371/journal.pone.0061228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Veyrieras JB, Goffinet B, Charcosset A (2007) MetaQTL: a package of new computational methods for the meta-analysis of QTL mapping experiments. BMC Bioinform 8:49. doi:10.1186/1471-2105-8-49

    Article  CAS  Google Scholar 

  • Vezzulli S, Troggio M, Coppola G et al (2008) A reference integrated map for cultivated grapevine (Vitis vinifera L.) from three crosses, based on 283 SSR and 501 SNP-based markers. Theor Appl Genet 117:499–511. doi:10.1007/s00122-008-0794-3

    Article  CAS  PubMed  Google Scholar 

  • Vezzulli S, Malacarne G, Vecchione A, Dolzani C, Masuero D, Haile Mehari Z, Franceschi P, Banchi E, Velasco R, Stefanini M, Wehrens R, Vhrovsek U, Zulini L, Moser C (in preparation) Rpv3 locus and stilbenoid induction mediate downy mildew resistance in the Merzling × Teroldego segregating population

  • Vezzulli S, Vecchione A, Stefanini M, Zulini L (submitted) Downy mildew resistance evaluation in 28 grapevine hybrids promising for breeding programs in Trentino region (Italy)

  • Viret O, Siegfried W, Bloesch B et al (2001) Prévision et gestion des infections du mildiou de la vigne (Plasmopara viticola) basées sur des stations d’avertissement. Rev suisse Vitic Arboric Hortic 33(2):1–12

    Google Scholar 

  • Vitulo N, Forcato C, Carpinelli E et al (2014) A deep survey of alternative splicing in grape reveals changes in the splicing machinery related to tissue, stress condition and genotype. BMC Plant Biol 14:99. doi:10.1186/1471-2229-14-99

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wan Y, Schwaninger H, He P, Wang Y (2007) Comparison of resistance to powdery mildew and downy mildew in Chinese wild grapes. Vitis - J Grapevine Res 46:132–136

    Google Scholar 

  • Welter LJ, Göktürk-Baydar N, Akkurt M et al (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. doi:10.1007/s11032-007-9097-7

    Article  CAS  Google Scholar 

  • Werner S, Steiner U, Becher R et al (2002) Chitin synthesis during in planta growth and asexual propagation of the cellulosic oomycete and obligate biotrophic grapevine pathogen Plasmopara viticola. FEMS Microbiol Lett 208:169–173. doi:10.1016/S0378-1097(01)00456-6

    Article  CAS  PubMed  Google Scholar 

  • 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, Udine, Italy, July 2–6

  • Wilson C, Tisdell C (2001) Why farmers continue to use pesticides despite environmental, health and sustainability costs. Ecol Econ 39:449–462. doi:10.1016/S0921-8009(01)00238-5

    Article  Google Scholar 

  • Wu J, Zhang Y, Zhang H et al (2010) Whole genome wide expression profiles of Vitis amurensis grape responding to downy mildew by using Solexa sequencing technology. BMC Plant Biol 10:234. doi:10.1186/1471-2229-10-234

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xiang J, Li X, Wu J et al (2016) Studying the mechanism of Plasmopara viticola RxLR effectors on suppressing plant immunity. Front Microbiol 7:1–12. doi:10.3389/fmicb.2016.00709

    Article  Google Scholar 

  • Xu P, Liu Y, Qin H et al (2015) Proteomic analysis of the resistant responses of two Vitis amurensis cultivars to Plasmopara viticola infections. Curr Proteom 12:63–68

    Article  CAS  Google Scholar 

  • Yin L, Zhang Y, Hao Y, Lu J (2014) Genetic diversity and population structure of Plasmopara viticola in China. Eur J Plant Pathol 140:365–376. doi:10.1007/s10658-014-0470-1

    Article  Google Scholar 

  • Yin L, Li X, Xiang J et al (2015) Characterization of the secretome of Plasmopara viticola by de novo transcriptome analysis. Physiol Mol Plant Pathol 91:1–10. doi:10.1016/j.pmpp.2015.05.002

    Article  CAS  Google Scholar 

  • Yu Y, Jiao L, Fu S et al (2016) Callose synthase family genes involved in the grapevine defense response to downy mildew disease. Phytopathology 106:56–64. doi:10.1094/PHYTO-07-15-0166-R

    Article  CAS  PubMed  Google Scholar 

  • Zyprian E, Ochßner I, Schwander F et al (2016) Quantitative trait loci affecting pathogen resistance and ripening of grapevines. Mol Genet Genom 291:1573–1594. doi:10.1007/s00438-016-1200-5

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors apologize to the scientists that are not cited because of space limitation. They wish to thank Marco Stefanini (FEM) for helpful discussions and Elena Zini (Laimburg Institute) for useful suggestions on Table 2. Daniele Buonassisi acknowledges funding from a FEM PhD fellowship at University of Udine, Monica Colombo from the Cariplo foundation (project GrAptaResistance, Integrated research on industrial biotechnologies 2015), and Michele Perazzolli from the European Unions Seventh Framework Programme for research, technological development and demonstration under Grant agreement No. 324416 (project INNOVA, theme FP7-PEOPLE-2012-IAPP).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Silvia Vezzulli.

Additional information

This article is part of the Topical Collection on Plant Breeding: the Art of Bringing Science to Life. Highlights of the 20th EUCARPIA General Congress, Zurich, Switzerland, 29 August–1 September 2016

Edited by Roland Kölliker, Richard G. F. Visser, Achim Walter & Beat Boller

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Buonassisi, D., Colombo, M., Migliaro, D. et al. Breeding for grapevine downy mildew resistance: a review of “omics” approaches. Euphytica 213, 103 (2017). https://doi.org/10.1007/s10681-017-1882-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10681-017-1882-8

Keywords

Navigation