Skip to main content
SpringerLink
Log in

Pathotypic diversity of Hyaloperonospora brassicae collected from Brassica oleracea

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

Abstract

Downy mildew caused by Hyaloperonospora brassicae is an economically destructive disease of brassica crops in many growing regions throughout the world. Specialised pathogenicity of downy mildews from different Brassica species and closely related ornamental or wild relatives has been described from host range studies. Pathotypic variation amongst Hyaloperonospora brassicae isolates from Brassica oleracea has also been described; however, a standard set of B. oleracea lines that could enable reproducible classification of H. brassicae pathotypes was poorly developed. For this purpose, we examined the use of eight genetically refined host lines derived from our previous collaborative work on downy mildew resistance as a differential set to characterise pathotypes in the European population of H. brassicae. Interaction phenotypes for each combination of isolate and host line were assessed following drop inoculation of cotyledons and a spectrum of seven phenotypes was observed based on the level of sporulation on cotyledons and visible host responses. Two host lines were resistant or moderately resistant to the entire collection of isolates, and another was universally susceptible. Five lines showed differential responses to the H. brassicae isolates. A minimum of six pathotypes and five major effect resistance genes are proposed to explain all of the observed interaction phenotypes. The B. oleracea lines from this study can be useful for monitoring pathotype frequencies in H. brassicae populations in the same or other vegetable growing regions, and to assess the potential durability of disease control from different combinations of the predicted downy mildew resistance genes.

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

Similar content being viewed by others

References

  • Agnola, B., Boury, S., Monot, C., Quillévéré, A., Hervé, Y., & Silué, D. (2003). Evidence that a leaf-disk test allows assessment of isolate-specific resistance in Brassica oleracea crops against downy mildew (Peronospora parasitica). European Journal of Plant Pathology, 109, 471–478.

    Article  CAS  Google Scholar 

  • Armstrong, M. R., Whisson, S. C., Pritchard, L., Bos, J. I. B., Venter, E., Avrova, A. O., Rehmany, A. P., Böhme, U., Brooks, K., Cherevach, I., Hamlin, N., White, B., Fraser, A., Lord, A., Quail, M. A., Churcher, C., Hall, N., Berriman, M., Huang, S., Kamoun, S., Beynon, J. L., & Birch, P. R. J. (2005). An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proceedings of the National Academy of Sciences USA, 102, 7766–7771.

    Article  CAS  Google Scholar 

  • Bahcevandziev, K. (2003). Caracterização da resistência ao míldio (Peronospora parasitica (Pers. Ex. Fr.) Fr.) no estado cotiledonar em Brassica oleracea. Dissertation, Instituto Superior de Agronomia, Technical University of Lisbon.

  • Channon, A. G. (1981). Downy mildew of brassicas. In D. M. Spencer (Ed.), The downy mildews (pp. 321–339). London: Academic.

    Google Scholar 

  • Coelho, P., Leckie, D., Bahcevandziev, K., Valério, L., Astley, D., Boukema, I., Crute, I. R., & Monteiro, A. (1998). The relationship between cotyledon and adult plant resistance to downy mildew (Peronospora parasitica) in Brassica oleracea. Acta Horticulturae, 459, 335–342.

    Google Scholar 

  • Correll, J. C., Feng, C., Irish, B. M., Koike, S. T., Morelock, T. E., Bentley, T. C., & Tomlinson, A. N. (2007). Spinach downy mildew: overview of races and the development of molecular markers linked to major resistance genes. In A. Lebeda & P. T. N. Spencer-Phillips (Eds.), Advances in downy mildew research (pp. 135–142). Olomouc: Organising Committee of the 2nd International Downy Mildews Symposium.

    Google Scholar 

  • Crute, I. R., & Johnson, A. G. (1976). The genetic relationship between races of Bremia lactucae and cultivares of Lactuca sativa. Annals of Applied Biology, 83, 125–137.

    Article  Google Scholar 

  • Delmotte, F., Giresse, X., Richard-Cervera, S., M’Baya, J., Vear, F., Tourvieille, J., Walser, P., & Labrouhe, D. T. (2008). Single nucleotide polymorphisms reveal multiple introductions into France of Plasmopara halstedii, the plant pathogen causing sunflower downy mildew. Infection, Genetics and Evolution, 8, 534–540.

    Article  PubMed  CAS  Google Scholar 

  • Dickinson, C. H., & Greenhalgh, J. R. (1977). Host range and taxonomy of Peronospora on crucifers. Transactions of the British Mycological Society, 69, 111–116.

    Article  Google Scholar 

  • Dickson, M. H., & Petzoldt, R. (1993). Plant age and isolate source affect expression of downy mildew resistance in broccoli. HortScience, 28, 730–731.

    Google Scholar 

  • Göker, M., Voglmayr, H., Blázquez, G. G., & Oberwinkler, F. (2009). Species delimitation in downy mildews: the case of Hyaloperonospora in the light of nuclear ribosomal ITS and LSU sequences. Mycological Research, 113, 308–325.

    Article  PubMed  Google Scholar 

  • Greenhalgh, J. R., & Dickinson, C. H. (1975). Differential reactions of three crucifers to infection by Peronospora parasitica (Pers. ex Fr.) Fr. Phytopathologische Zeitschrift—Journal of Phytopathology, 84, 131–141.

    Article  Google Scholar 

  • Holub, E. B. (2008). Natural history of Arabidopsis thaliana and oomycete symbioses. European Journal of Plant Pathology, 122, 91–109.

    Article  CAS  Google Scholar 

  • Hott, T. W., Durgan, M. E., & Michelmore, R. W. (1987). Genetics of virulence in Californian populations of Bremia lactucae (lettuce downy mildew). Phytopathology, 77, 1381–1386.

    Article  Google Scholar 

  • Hott, T. W., Hulbert, S. H., & Michelmore, R. W. (1989). Genetic analysis of the gene-for-gene interaction between lettuce (Lactuca sativa) and Bremia lactucae. Phytopathology, 79, 888–897.

    Article  Google Scholar 

  • Hulbert, S. H., & Michelmore, R. W. (1985). Linkage analysis of genes for resistance to downy mildew (Bremia lactucae) in lettuce (Lactuca sativa). Theoretical and Applied Genetics, 70, 520–528.

    Article  Google Scholar 

  • Irish, B. M., Correll, J. C., Koike, S. T., Schafer, J., & Morelock, T. E. (2003). Identification and cultivar reaction to three new races of the spinach downy mildew pathogen from the United States and Europe. Plant Disease, 87, 567–572.

    Article  Google Scholar 

  • Jensen, B. D., Hockenhull, J., & Munk, L. (1999). Seedling and adult plant resistance to downy mildew (Peronospora parasitica) in cauliflower (Brassica oleracea convar. botrytis var. botrytis). Plant Pathology, 48, 604–612.

    Article  Google Scholar 

  • Leckie, D., Astley, D., Crute, I. R., Ellis, P. R., Pink, D. A. C., Boukema, I., Monteiro, A. A., & Dias, S. (1996). The location and exploitation of genes for pest and disease resistance in European gene bank collections of horticultural brassicas. Acta Horticulturae, 407, 95–101.

    Google Scholar 

  • Leckie, D., Cogan, N., Astley, D., Crute, I. R., Boukema, I., Santos, M., Bahcevandziev, K., Silva-Dias, J., & Monteiro, A. A. (1998). Differential resistance to Peronospora parasitica and Albugo candida in Brassica oleracea. Acta Horticulturae, 459, 357–361.

    Google Scholar 

  • Lucas, J. A., Crute, I. R., Sherriff, C., & Gordon, P. L. (1988). The identification of a gene for race-specific resistance to Peronospora parasitica (downy mildew) in Brassica napus var. oleifera (oilseed rape). Plant Pathology, 37, 538–545.

    Article  Google Scholar 

  • MacGregor, T., Bhattacharyya, M., Tyler, B., Bhat, R., Schmitthenner, A. F., & Gijzen, M. (2002). Genetic and physical mapping of Avr1a in Phytophthora sojae. Genetics, 160, 949–959.

    PubMed  CAS  Google Scholar 

  • Monot, C., & Silué, D. (2009). Comparison of the resistance and susceptibility to downy mildew [Hyaloperonospora parasitica, constant. (Pers. Ex Fr)] of nine Brassica oleracea accessions in laboratory, seedbed, and field screens. Euphytica, 169, 413–419.

    Article  Google Scholar 

  • Monteiro, A. A., Coelho, P. S., Bahcevandziev, K., & Valério, L. (2005). Inheritance of downy mildew resistance at cotyledon and adult-plant stages in ‘Couve Algarvia’ (Brassica oleracea var. tronchuda). Euphytica, 141, 85–92.

    Article  Google Scholar 

  • Moss, N. A., Lucas, J. A., & Crute, I. R. (1991a). Evidence for differential response to isolates of Peronospora parasitica (downy mildew) in Brassica rapa. Annals of Applied Biology, 118, 96–97.

    Google Scholar 

  • Moss, N. A., Lucas, J. A., Crute, I. R., & Gordon, P. L. (1991b). Sources of seedling resistance to Peronospora parasitica (Downy mildew) in Brassica oleracea. Annals of Applied Biology, 118, 94–95.

    Google Scholar 

  • Moss, N. A., Crute, I. R., & Lucas, J. A. (1994). Laboratory production of oospores of Peronospora parasitica (crucifer downy mildew) and the recovery and characterization of sexual progeny from crosses between isolates with different host specificity. Plant Pathology, 43, 713–725.

    Article  Google Scholar 

  • Nashaat, N. I., & Awasthi, R. P. (1995). Evidence for differential resistance to Peronospora parasitica (downy mildew) in accessions of Brassica juncea (mustard) at the cotyledon stage. Journal of Phytopathology, 143, 157–159.

    Article  Google Scholar 

  • Nashaat, N. I., & Rawlinson, C. J. (1994). The response of oilseed rape (Brassica napus ssp. oleifera) accessions with different glucosinolate and erucic acid contents to four isolates of Peronospora parasitica (downy mildew) and the identification of new sources of resistance. Plant Pathology, 43, 278–285.

    Article  CAS  Google Scholar 

  • Natti, J. J., Dickson, M. H., & Atkin, J. D. (1967). Resistance of Brassica oleracea varieties to downy mildew. Phytopathology, 57, 144–147.

    Google Scholar 

  • Norwood, J. M., & Crute, I. R. (1984). The genetic control and expression of specificity in Bremia lactucae (lettuce downy mildew). Plant Pathology, 33, 385–400.

    Article  Google Scholar 

  • Shan, W., Cao, M., Leung, D., & Tyler, B. M. (2004). The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b. Molecular Plant-Microbe Interactions, 17, 394–403.

    Article  PubMed  CAS  Google Scholar 

  • Sherriff, C., & Lucas, J. A. (1990). The host range of isolates of downy mildew, Peronospora parasitica, from Brassica crop species. Plant Pathology, 39, 77–91.

    Article  Google Scholar 

  • Silué, D., Nashaat, N. I., & Tirilly, Y. (1996). Differential responses of Brassica oleracea and B. rapa accessions to seven isolates of Peronospora parasitica at the cotyledon stage. Plant Disease, 80, 142–144.

    Article  Google Scholar 

  • Tapsoba, H., & Wilson, J. P. (1996). Pathogenic variation in Puccinia substriata var. indica in the Southeastern United States and screening for resistance in pearl millet germ plasm. Plant Disease, 80, 395–397.

    Article  Google Scholar 

  • Thomas, C. E., & Jourdain, E. L. (1992). Resistance to race 2 of Peronospora parasitica in U.S. plant introductions of Brassica oleracea var. capitata. HortScience, 27, 1120–1122.

    Google Scholar 

  • Vicente, J. G., Gunn, N. D., Bailey, L., Pink, D. A. C., & Holub, E. B. (2012). Genetics of resistance to downy mildew in Brassica oleracea and breeding towards durable disease control for UK vegetable production. Plant Pathology, 61, 600–609.

    Article  Google Scholar 

  • Wang, M., Farnham, M. W., & Thomas, C. E. (2000). Phenotypic variation for downy mildew resistance among inbred broccoli. HortScience, 35, 925–929.

    Google Scholar 

Download references

Acknowledgments

The authors wish to thank Ms. Luísa Valério (ISA, Technical University of Lisbon) for the valuable technical assistance in experimental laboratory essays in Portugal. We also thank Dr. Graham J. King for supplying the ‘DH-GK97362’ rapid-cycling Brassica line used as susceptible control. The work conducted in Portugal was funded by the Portuguese Ministry of Education FCT project ‘Cloning Pp523, a downy mildew resistance gene of Brassica oleracea L.’ (PTDC/AGR-GPL/70135/2006). The work conducted in the UK was funded by the UK Department for the Environment, Food and Rural Affairs (Defra) as part of the project ‘Crop Improvement of field vegetables’ (HH37232SX).

Author information

Authors and Affiliations

  1. National Institute of Biological Resources (INRB/INIA), Av. República, 2784-505, Oeiras, Portugal

    Paula S. Coelho

  2. School of Life Sciences, Wellesbourne campus (formerly Warwick-HRI), University of Warwick, Warwick, CV35 9EF, UK

    Joana G. Vicente & Eric B. Holub

  3. Instituto Superior de Agronomia, Technical University of Lisbon, 1349-017, Lisbon, Portugal

    António A. Monteiro

Authors
  1. Paula S. Coelho
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joana G. Vicente
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. António A. Monteiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eric B. Holub
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Paula S. Coelho or Joana G. Vicente.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Coelho, P.S., Vicente, J.G., Monteiro, A.A. et al. Pathotypic diversity of Hyaloperonospora brassicae collected from Brassica oleracea . Eur J Plant Pathol 134, 763–771 (2012). https://doi.org/10.1007/s10658-012-0052-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-012-0052-z

Keywords

Search

Navigation