Skip to main content
SpringerLink
Log in

Histopathology of infection and colonisation of Elsinoë ampelina on grapevine leaves

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Elsinoë ampelina, the causal agent of grapevine anthracnose, infects all aboveground succulent parts of the plant, causing serious yield losses. There are no histopathological reports on this pathogen interaction with grapevine tissues. This study aimed at understanding the infection and colonisation processes of E. ampelina on Vitis labrusca cv. Niagara Rosada leaves by light, transmission and scanning microscopy. From one to five germ tubes per conidia were formed during conidia germination, predominantly one or two. Cuticle degradation was observed on plant surface underneath germ tubes and appressorium-like structures were rare. Monilioid and branched hyphae were observed 48 h post inoculation. Direct penetration occurred only on the adaxial leaf surface due to high trichome density on the abaxial leaf surface and conidia trapped on trichomes were frequently observed. The colonisation process was similar in the leaf blade, veins and petiole with the formation of inter- and intracellular hyphae. Phenolic compounds accumulated in infected areas; however, they did not prevent the colonisation progress. Tissues of foliar blade were totally changed by cell collapse and conidiogenous cells were observed on the surface of necrotic lesions. Ascus-like structures were observed within deeply unstructured tissues of leaf veins and necrotic areas of the petiole.

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

Similar content being viewed by others

References

  • Agrios, G. N. (2005). Plant pathology (5th ed.). Burlington: Elsevier Academic Press.

    Google Scholar 

  • Amorim, L., Spósito, M. B., & Kuniyuki, H. (2016). Doenças da videira. In L. Amorim, J. A. M. Rezende, A. Bergamin Filho, & L. E. A. Camargo (Eds.), Manual de Fitopatologia: Doenças das Plantas Cultivadas (pp. 745–758). São Paulo: Editora Agronômica Ceres.

    Google Scholar 

  • Barros, L. B., Biasi, L. A., Carisse, O., & De Mio, L. L. M. (2015). Incidence of grape anthracnose on different Vitis labrusca and hybrid cultivars and rootstocks combination under humid subtropical climate. Australasian Plant Pathology, 44, 397–403.

    Article  Google Scholar 

  • Brook, P. J. (1973). Epidemiology of grapevine anthracnose, caused by Elsinoe ampelina. New Zealand Journal of Agricultural Research, 16, 333–342.

    Article  Google Scholar 

  • Camargo, U. A., Tonietto, J., & Hoffmann, A. (2011). Progressos na viticultura brasileira. Revista Brasileira de Fruticultura, 33, 144–149.

    Article  Google Scholar 

  • Carisse, O., & Lefebvre, A. (2011). A model to estimate the amount of primary inoculum of Elsinoë ampelina. Plant Disease, 95, 1167–1171.

    Article  PubMed  Google Scholar 

  • Carisse, O., & Morissette-Thomas, V. (2013). Epidemiology of grape anthracnose: Factors associated with defoliation of grape leaves infected by Elsinoë ampelina. Plant Disease, 97, 222–230.

    Article  PubMed  Google Scholar 

  • EPPO (European and Mediterranean Plant Protection Organization) (2016). Elsinoë ampelina. https://gd.eppo.int/taxon/ELSIAM/distribution. Accessed 5 Jun 2018.

  • Fan, X. L., Barreto, R. W., Groenewald, J. Z., Bezerra, J. D. P., Pereira, O. L., Cheewangkoon, R., & Crous, P. W. (2017). Phylogeny and taxonomy of the scab and spot anthracnose fungus Elsinoë (Myriangiales, Dothideomycetes). Studies in Mycology, 87, 1–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feder, N. E. D., & O'Brien, T. P. (1968). Plant microtechnique: Some principles and new methods. American Journal of Botany, 55, 123–142.

    Article  Google Scholar 

  • Feng, J., Wang, F., Hughes, G. R., Kaminskyj, S., & Wei, Y. (2011). An important role for secreted esterase in disease establishment of the wheat powdery mildew fungus Blumeria graminis f. sp. tritici. Canadian Journal of Microbiology, 57, 211–216.

  • Gabel, A. W., & Tiffany, L. H. (1987). Host-parasite relations and development of Elsinoë panici. Mycologia, 79, 737–744.

    Google Scholar 

  • Gregory, M., & Baas, P. (1989). A survey of mucilage cells in vegetative organs of the dicotyledons. Israel Journal of Botany, 38, 125–174.

    Google Scholar 

  • Horridge, G., & Tamm, S. (1969). Critical point drying for scanning electron microscopic study of ciliary motion. Science, 163, 817–818.

    Article  CAS  PubMed  Google Scholar 

  • Hughes, J., & McCully, M. E. (1975). The use of an optical brightener in the study of plant structure. Stain Technology, 50, 319–329.

    Article  CAS  PubMed  Google Scholar 

  • IBGE (Instituto Brasileiro de Geografia e Estatística) (2019). Levantamento sistemático da produção agrícola. https://sidra.ibge.gov.br/tabela/6588#resultado. Accessed 20 Feb 2019.

  • Karnovsky, J. M. (1965). A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. Journal of Cell Biology, 27, 137–138.

    Google Scholar 

  • Kim, K. W., Hyun, J. W., & Park, E. W. (2004). Cytology of cork layer formation of citrus and limited growth of Elsinoe fawcettii in scab lesions. European Journal of Plant Pathology, 110, 129–138.

    Article  Google Scholar 

  • Kono, A., Sato, A., Ban, Y., & Mitani, N. (2013). Resistance of Vitis germplasm to Elsinoë ampelina (de Bary) Shear evaluated by lesion number and diameter. HortScience, 48, 1433–1439.

    Article  Google Scholar 

  • Kortekamp, A., & Zyprian, E. (1999). Leaf hairs as a basic protective barrier against downy mildew of grape. Journal of Phytopathology, 147, 453–459.

    Article  Google Scholar 

  • Kubicek, C. P., Starr, T. L., & Glass, N. L. (2014). Plant cell wall–degrading enzymes and their secretion in plant-pathogenic fungi. Annual Review of Phytopathology, 52, 427–451.

    Article  CAS  PubMed  Google Scholar 

  • Li, Z., Dang, H., Yuan, X., He, J., Hu, Z., & Wang, X. (2018). Morphological characterization and optimization of conditions for conidial production of Elsinoë ampelina, the causal organism of grapevine anthracnose. Journal of Phytopathology, 166, 420–428.

    Article  Google Scholar 

  • Maia, J. D. G., Camargo, U. A., Tonietto, J., Zanus, M. C., Quecini, V., Ferreira, M. E., & Ritschel, P. (2015). Grapevine breeding programs in Brazil. In G. A. Reynolds (Ed.), Grapevine breeding programs for the wine industry (pp. 247–271). Cambridge: Elsevier.

    Chapter  Google Scholar 

  • Marques, J. P. R., Spósito, M. B., Mello, A. F. S., Amorim, L., Mondin, M., & Appezzato-da-Glória, B. (2012). Histopathology of black spot symptoms in sweet oranges. European Journal of Plant Pathology, 133, 439–448.

    Article  Google Scholar 

  • Marques, J. P. R., Amorim, L., Spósito, M. B., & Appezzato-da-Glória, B. (2013a). Histopathology of postbloom fruit drop caused by Colletotrichum acutatum in citrus flowers. European Journal of Plant Pathology, 135, 783–790.

    Article  CAS  Google Scholar 

  • Marques, J. P. R., Soares, M. K. M., & Appezzato-Da-Gloria, B. (2013b). New staining technique for fungal-infected plant tissues. Turkish Journal of Botany, 37, 784–787.

    Google Scholar 

  • Mason, D. L., & Backus, M. P. (1969). Host-parasite relations in spot anthracnose of Desmodium. Mycologia, 61, 1124–1141.

    Article  Google Scholar 

  • Murria, S., Kaur, N., Arora, N., & Mahal, A. K. (2018). Field reaction and metabolic alterations in grape (Vitis vinifera L.) varieties infested with anthracnose. Scientia Horticulturae, 235, 286–293.

    Article  CAS  Google Scholar 

  • Pascholati, S. F., & Dalio, R. J. D. (2018). Fisiologia do parasitismo: como os patógenos atacam as plantas. In L. Amorim, J. A. M. Rezende, & A. Bergamin Filho (Eds.), Manual de Fitopatologia: Princípios e Conceitos (pp. 389–421). São Paulo: Editora Agronômica Ceres.

    Google Scholar 

  • Pascholati, S. F., Deising, H., Leite, B., Anderson, D., & Nicholson, R. L. (1993). Cutinase and non-specific esterase activities in the conidial mucilage of Colletotrichum graminicola. Physiological Molecular Plant Pathology, 42, 37–51.

    Article  CAS  Google Scholar 

  • Paudyal, D. P., & Hyun, J. W. (2015). Physical changes in Satsuma mandarin leaf after infection of Elsinoë fawcettii causing citrus scab disease. The Plant Pathology Journal, 31, 421–427.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paudyal, D. P., Hyun, J. W., & Hwang, R. Y. (2017). Infection and symptom development by citrus scab pathogen Elsinoë fawcettii on leaves of Satsuma mandarin. European Journal of Plant Pathology, 148, 807–816.

  • Reynolds, E. S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. The Journal of Cell Biology, 17, 208–212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakai, W. S. (1973). Simple method for differential staining of paraffin embedded plant material using toluidine blue O. Stain Technology, 48, 247–249.

    Article  CAS  PubMed  Google Scholar 

  • Santos, R. F., Spósito, M. B., Ayres, M. R., & Sosnowski, M. R. (2018a). Phylogeny, morphology and pathogenicity of Elsinoë ampelina, the causal agent of grapevine anthracnose in Brazil and Australia. Journal of Phytopathology, 166, 187–198.

    Article  CAS  Google Scholar 

  • Santos, R. F., Ciampi-Guillardi, M., Amorim, L., Massola, N. S., & Spósito, M. B. (2018b). Aetiology of anthracnose on grapevine shoots in Brazil. Plant Pathology, 67, 692–706.

    Article  CAS  Google Scholar 

  • Santos, R. F., Spósito, M. B., Ayres, M. R., & Sosnowski, M. R. (2018c). In vitro production of conidia of Elsinoë ampelina, the causal fungus of grapevine anthracnose. European Journal of Plant Pathology, doi.org/10.1007/s10658-018-1502-z.

  • Shear, C. L. (1929). The life-history of Sphaceloma ampelinmn de Bary. Phytopathology, 19, 673–679.

    Google Scholar 

  • Thind, T. S. (2015). Anthracnose. In W. Wilcox, W. Gubler, & J. Uyemoto (Eds.), Compendium of grape diseases, disorders, and pests (pp. 17–19). St Paul: APS Press.

    Google Scholar 

  • Thind, T. S., Arora, J. K., Mohan, C., & Raj, P. (2004). Epidemiology of powdery mildew, downy mildew and anthracnose diseases of grapevine. In S. A. M. H. Naqvi (Ed.), Diseases of fruits and vegetables (pp. 621–638). Dordrecht: Springer.

    Chapter  Google Scholar 

  • Williamson, B., & McNicol, R. J. (1989). The histology of lesion development in raspberry canes infected by Elsinoe veneta. Annals of Applied Biology, 114, 35–44.

    Article  Google Scholar 

Download references

Acknowledgements

We would like to FAPESP for financial support (project n° 2013/24003-9), NAP-MEPA, ESALQ/USP for electron microscope facilities. This study was also financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001.

Author information

Authors and Affiliations

  1. Departamento de Ciências Biológicas, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, Piracicaba, SP, 13418-900, Brazil

    Zélia Valente Braga & Beatriz Appezzato-da-Glória

  2. Departamento de Fitopatologia e Nematologia, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, Piracicaba, SP, 13418-900, Brazil

    Ricardo Feliciano dos Santos & Lilian Amorim

Authors
  1. Zélia Valente Braga
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ricardo Feliciano dos Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lilian Amorim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Beatriz Appezzato-da-Glória
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Lilian Amorim or Beatriz Appezzato-da-Glória.

Ethics declarations

This manuscript is original and complies to the ethical rules applicable for this journal.

Conflict of interest

The authors do not present any actual or potential conflict of interests.

Electronic supplementary material

ESM 1

(DOCX 929 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Braga, Z.V., dos Santos, R.F., Amorim, L. et al. Histopathology of infection and colonisation of Elsinoë ampelina on grapevine leaves. Eur J Plant Pathol 154, 1009–1019 (2019). https://doi.org/10.1007/s10658-019-01721-2

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-019-01721-2

Keywords

Search

Navigation