Skip to main content
SpringerLink
Log in

Histological responses to downy mildew in resistant and susceptible grapevines

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Downy mildew in grapevines, caused by Plasmopara viticola, is a very serious disease throughout the grape-producing nations, especially in more humid climates. Downy mildew mainly affects the cultivated varieties of Vitis vinifera. A promising way to minimize or eliminate P. viticola infections is by the adoption of resistant cultivars. Chinese wild grapevines are reported to possess resistance to many fungal diseases. In this study, three Chinese wild grapevines (Vitis pseudoreticulata Baihe-35-1, Vitis davidii var. cyanocarpa Langao-5, and Vitis piasezkii Liuba-8) and a European cultivated variety (V. vinifera cv. Pinot noir) were inoculated with P. viticola, and a histological survey was undertaken. Macroscopic observations revealed no sporulation in V. piasezkii Liuba-8, little sporulation in V. pseudoreticulata Baihe-35-1 and V. davidii var. cyanocarpa Langao-5, but serious sporulation in V. vinifera cv. Pinot noir. Aniline blue staining indicated callose deposition in V. pseudoreticulata Baihe-35-1, V. davidii var. cyanocarpa Langao-5, and V. piasezkii Liuba-8. Cells with distinctive fluorescence were also observed in V. pseudoreticulata Baihe-35-1. After staining with 3,3-diaminobenzidine, production of H2O2 was observed early on, after infection in V. davidii var. cyanocarpa Langao-5 and V. piasezkii Liuba-8. No H2O2 accumulation was observed in V. vinifera cv. Pinot noir. It is concluded that V. piasezkii Liuba-8 should be classified as “highly resistant” to downy mildew, V. pseudoreticulata Baihe-35-1 and V. davidii var. cyanocarpa Langao-5 as “resistant,” and V. vinifera Pinot noir as “susceptible.” The possible roles of stomatal callose deposition in the defense r6eactions of the mildew-resistant grapevines are discussed.

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
Fig. 6

Similar content being viewed by others

References

  • Allegre M, Heloir MC, Trouvelot S, Daire X, Pugin A, Wendehenne D, Adrian M (2009) Are grapevine stomata involved in the elicitor-induced protection against downy mildew? Mol Plant Microbe Interact 22:977–986

    Article  CAS  PubMed  Google Scholar 

  • Alleweldt G, Possingham JV (1988) Progress in grapevine breeding. Theor Appl Genet 75:669–673

    Article  Google Scholar 

  • Alonso-Villaverde V, Voinesco F, Viret O, Spring JL, Gindro K (2011) The effectiveness of stilbenes in resistant Vitaceae: ultrastructural and biochemical events during Plasmopara viticola infection process. Plant Physiol Biochem 49:265–274

    Article  CAS  PubMed  Google Scholar 

  • Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773–784

    Article  CAS  PubMed  Google Scholar 

  • Asai S, Mase K, Yoshioka H (2010) A key enzyme for flavin synthesis is required for nitric oxide and reactive oxygen species production in disease resistance. Plant J 62:911–924

    CAS  PubMed  Google Scholar 

  • Bennett M, Gallagher M, Fagg J, Bestwick C, Paul T, Beale M, Mansfield J (1996) The hypersensitive reaction, membrane damage and accumulation of autofluorescent phenolics in lettuce cells challenged by Bremia lactucae. Plant J 9:851–865

    Article  CAS  Google Scholar 

  • Bolwell GP, Wojtaszek P (1997) Mechanisms for the generation of reactive oxygen species in plant defence—a broad perspective. Physiol Mol Plant Pathol 51:347–366

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Boubakri H, Wahab MA, Chong J, Bertsch C, Mliki A, Soustre-Gacougnolle I (2012) Thiamine induced resistance to Plasmopara viticola in grapevine and elicited host–defense responses, including HR like-cell death. Plant Physiol Biochem 57:120–133

    Article  CAS  PubMed  Google Scholar 

  • Cavalier-Smith T (1998) A revised six-kingdom system of life. Biol Rev Cambridge Philos Soc 73:203–266

    Article  CAS  PubMed  Google Scholar 

  • Dai GH, Andary C, Mondolot-Cosson L, Boubals D (1995) Histochemical studies on the interaction between three species of grapevine, Vitis vinifera, V. rupestris and V. rotundifolia and the downy mildew fungus, Plasmopara viticola. Physiol Mol Plant Pathol 46:177–188

    Article  Google Scholar 

  • Dercks W, Creasy LL (1989) The significance of stilbene phytoalexins in the Plasmopara viticola-grapevine interaction. Physiol Mol Plant Pathol 34:189–202

    Article  CAS  Google Scholar 

  • Díez-Navajas AM, Greif C, 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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Gindro K, Pezet R, Viret O (2003) Histological study of the responses of two Vitis vinifera cultivars (resistant and susceptible) to Plasmopara viticola infections. Plant Physiol Biochem 41:846–853

    Article  CAS  Google Scholar 

  • Gisi U, Sierotzki H (2008) Fungicide modes of action and resistance in downy mildews. Eur J Plant Pathol 122:157–167

    Article  CAS  Google Scholar 

  • He PC (1999) Viticulture. China Agriculture Press, Beijing

    Google Scholar 

  • Hood ME, Shew HD (1996) Applications of KOH aniline blue fluorescence in the study of plant–fungal interactions. Phytopathology 86:704–708

    Article  Google Scholar 

  • Ingram DS (1981) Physiology and biochemistry of host–parasite interaction. In: Spencer DM (ed) The downy mildews: 143–161

  • 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  PubMed  Google Scholar 

  • Kiefer B, Riemann M, Büche C, Kassemeyer HH, Nick P (2002) The host guides morphogenesis and stomatal targeting in the grapevine pathogen Plasmopara viticola. Planta 215:387–393

    Article  CAS  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

    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

  • Kortekamp A, Wind R, Zvprian E (1997) The role of callose deposits during infection of two downy mildew-tolerant and two-susceptible Vitis cultivars. Vitis 36:103–104

    Google Scholar 

  • Lafon R, Bulit J (1981) Downy mildew of the vine. In: Spencer DM (ed) The downy mildews, pp 601–614

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

    Google Scholar 

  • Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593

    Article  CAS  PubMed  Google Scholar 

  • Mellersh DG, Foulds IV, Higgins VJ, Heath MC (2002) H2O2 plays different roles in determining penetration failure in three diverse plant–fungal interactions. Plant J 29:257–268

    Article  CAS  PubMed  Google Scholar 

  • Palmieri MC, Perazzolli M, Matafora V, Moretto M, Bachi A, Pertot I (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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pugin A, Frachisse JM, Tavernier E, Bligny R, Gout E, Laurière C, Guern J (1997) Early events induced by the elicitor cryptogein in tobacco cells: involvement of a plasma membrane NADPH oxidase and activation of glycolysis and the pentose phosphate pathway. Plant Cell 9:2077–2091

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Richter H, Pezet R, Viret O, Gindro K (2006) Characterization of 3 new partial stilbene synthase genes out of over 20 expressed in Vitis vinifera during the interaction with Plasmopara viticola. Physiol Mol Plant Pathol 67:248–260

    Article  Google Scholar 

  • Riemann M, Büche C, Kassemeyer HH, Nick P (2002) Cytoskeletal response during early development of the downy mildew of grapevine (Plasmopara viticola). Protoplasma 219:13–22

    Article  CAS  PubMed  Google Scholar 

  • Shetty NP, Lyngs Jørgensen HJ, Jensen JD, Collinge DB, Shekar Shetty H (2008) Roles of reactive oxygen species in interactions between plants and pathogens. Eur J Plant Pathol 121:267–280

    Article  CAS  Google Scholar 

  • Slaughter AR, Hamiduzzaman MM, Gindro K, Neuhaus JM, Mauch-Mani B (2008) Beta-aminobutyric acid-induced resistance in grapevine against downy mildew: involvement of pterostilbene. Eur J Plant Pathol 122:185–195

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • This P, Lacombe T, Thomas MR (2006) Historical origins and genetic diversity of wine grapes. Trends Genet 22:511–519

    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

    Article  CAS  Google Scholar 

  • Toffolatti SL, 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Torres AT, Jones JDG, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373–378

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Trouvelot S, Varnier AL, Allegre M, Mercier L, Baillieul F, Arnould C, Gianinazzi-Pearson V, Klarzynski O, Joubert JM, Pugin A, Daire X (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

    Article  CAS  PubMed  Google Scholar 

  • Unger S, Büche C, Boso S, Kassemeyer HH (2007) The course of colonization of two different Vitis genotypes by Plasmopara viticola indicates compatible and incompatible host–pathogen interactions. Phytopathology 97:780–786

    Article  PubMed  Google Scholar 

  • Vercesi A, Tornaghi R, Sant S, Burruano S, Faoro F (1999) A cytological and ultrastructural study on the maturation and germination of oospores of Plasmopara viticola from overwintering vine leaves. Mycol Res 103:193–202

    Article  Google Scholar 

  • Voigt CA, Somerville SC (2009) Callose in biotic stress (pathogenesis) biology, biochemistry and molecular biology of callose in plant defence: callose deposition and turnover in plant-pathogen interactions. In: Bacic A, Fincher GB, Stone BA (eds) Chemistry, biochemistry, and biology of 1–3 beta glucans and related polysaccharides. A. Academic Press, London, pp 525–562

    Chapter  Google Scholar 

  • Wan YZ, Schwaniniger H, He PC, Wang YJ (2007) Comparison of resistance to powdery mildew and downy mildew in Chinese wild grapes. Vitis 46:132–136

    Google Scholar 

  • Wang YJ, Liu Y, He PC, Che J, Lamikanra OLJ (1995) Evaluation of foliar resistance to Uncinula necator in Chinese wild Vitis species. Vitis 34:159–164

    Google Scholar 

  • Wang YJ, Liu Y, He PC, Lamikanra O, Lu J (1998) Resistance of Chinese Vitis species to Elsinoe ampelina (de Bary) Shear. HortSci 33:123–126

    Google Scholar 

  • Yu Y, Zhang Y, Yin L, Lu J (2012) The mode of host resistance to Plasmopara viticola infection of grapevines. Phytopathology 102:1094–1101

    Article  PubMed  Google Scholar 

  • Zhang HC, Wang CF, Cheng YL, Wang XJ, Li F, Han QM, Xu JR, Chen XM, Huang LL, Wei GR, Kang ZS (2011) Histological and molecular studies of the non-host interaction between wheat and Uromyces fabae. Planta 234:979–991

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (Grant No. 31272125). Support was also received from the Program for Innovative Research Team of Grape Germplasm Resource and Breeding (2013KCT-25) and from the Program for Young Talents in Northwest A&F University (NCET-10-0692, QN2011052) to Yan Xu.

Author information

Authors and Affiliations

  1. State Key Laboratory of Crop Stress Biology in Arid Areas, Northwest A&F University, Yangling, Shaanxi, People’s Republic of China

    Ruiqi Liu, Lan Wang, Jiali Zhu, Tingting Chen, Yuejin Wang & Yan Xu

  2. College of Horticulture, Northwest A&F University, Yangling, Shaanxi, People’s Republic of China

    Ruiqi Liu, Lan Wang, Jiali Zhu, Tingting Chen, Yuejin Wang & Yan Xu

  3. Key Laboratory of Horticultural Plant Biology and Germplasm Innovation in Northwest China, Ministry of Agriculture, Yangling, Shaanxi, People’s Republic of China

    Ruiqi Liu, Lan Wang, Jiali Zhu, Tingting Chen, Yuejin Wang & Yan Xu

Authors
  1. Ruiqi Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiali Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tingting Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuejin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yan Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yan Xu.

Additional information

Handling Editor: Hanns H. Kassemeyer

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, R., Wang, L., Zhu, J. et al. Histological responses to downy mildew in resistant and susceptible grapevines. Protoplasma 252, 259–270 (2015). https://doi.org/10.1007/s00709-014-0677-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-014-0677-1

Keywords

Search

Navigation