Skip to main content
Log in

Monitoring virulence of Bremia lactucae as a breeding tool against lettuce downy mildew from south and southwest Brazilian regions

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

Abstract

Lettuce downy mildew caused by Bremia lactucae is one of the main diseases in high humidity and low temperature conditions. The identification of virulence factors appearing in the pathogen population could help improve breeding programs against this disease. This study aimed to monitor and evaluate virulence dynamic changes in B. lactucae virulence among two Brazilian regions to recommend resistance genes for breeding programs. Isolates from São Paulo, Rio Grande do Sul, and Paraná states were assessed using the sextet code EU-C composed by 16 Lactuca spp. genotypes, between 2015 and 2016. To understand the population dynamics, the frequencies of virulence phenotypes and factors and the virulence complexity per isolate (Ci), phenotype (Cp), and Gleason (Ig), indexes were calculated. B. lactucae virulence from Paraná, Rio Grande do Sul and São Paulo were similar and shared nine out of the 15 evaluated virulence factors. In total, 90 isolates were analyzed, and 27 virulence phenotypes were found. The most frequent sextet codes were 31–00-00, 31–00-02, 31–01-00, and 31–01-02. The genes or resistance factors present in ‘Argelès’ (Dm38), ‘Balesta’, and ‘Bartoli’ could be used as sources of resistance by Brazilian lettuce breeders.

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

  • Andrivon, D. (1994). Race structure and dynamics in populations of Phytophthora infestans. Canadian Journal of Botany, 72, 1681–1687.

    Article  Google Scholar 

  • Braz, L. T., Dalpian, T., Camargo, M., & Pissardi, M. A. (2007). Identification of races of Bremia lactucae in São Paulo, Brazil. Acta Horticulturae, 760, 317–322.

    Article  Google Scholar 

  • Braz, L. T., Diniz, G. M. M., Castoldi, R., Nunes, R. C., Galatti, F. S., Camargo, M., Marin, M. V., Dalpian, T., Souza, J. O., Gomes, R. F., & Rabelo, H. O. (2016). Monitoring races of Bremia lactucae in the state of São Paulo from 2003 to 2012. Acta Horticulturae, 1127, 325–330.

    Article  Google Scholar 

  • Brown, S., Koike, S. T., Ochoa, O. E., Laemmlen, F., & Michelmore, R. W. (2004). Insensitivity to the fungicide Fosetyl-aluminum in California isolates of the lettuce downy mildew pathogen, Bremia lactucae. Plant Disease, 88, 502–508.

    Article  CAS  Google Scholar 

  • Castoldi, R., Charlo, H. C. O., Dalpian, T., Melo, D. M., Botelho, A. P., & Braz, L. T. (2012). Identification of new Bremia lactucae races in lettuce in São Paulo state. Horticultura Brasileira, 30, 209–213.

    Article  Google Scholar 

  • Ceresini, P. C. (2018). Estrutura Genética de Populações, Abordagens Analíticas e Estratégias de Manejo Durável de Doenças Baseadas no Potencial Evolutivo de Fitopatógenos. In L. J. DALLAGNOL (Ed.), Resistência genética: de plantas a patógenos (pp. 103–125). Ed. UFPel: Pelotas.

    Google Scholar 

  • Crute, I. R. (1987). The geographical distribution and frequency of virulence determinants in Bremia lactucae: Relationships between genetic control and host selection. In M. S. Wolfe & C. E. Caten (Eds.), Populations of plant pathogens: Their dynamics and genetics (pp. 193–212). Blackwell Scientific: Oxford, UK.

    Google Scholar 

  • Crute, I. R. (1992). The role of resistance breeding in the integrated control of downy mildew (Bremia lactucae) in protected lettuce. Euphytica, 63, 95–102.

    Article  Google Scholar 

  • Fall, M. L., Van der Heyden, H., Beaulieu, C., & Carisse, O. (2015). Bremia lactucae infection efficiency in lettuce is modulated by temperature and leaf wetness duration under Quebec field conditions. Plant Disease, 99, 1010–1019.

    Article  CAS  Google Scholar 

  • Franco, C.A. (2016) Monitoramento de raças de Bremia lactucae em alface no ano de 2014 e sua distribuição no Estado de São Paulo. 34 f. Dissertação (Mestrado em Agronomia) - Unesp, Jaboticabal.

  • Galatti, F. S., Castoldi, R., Braz, L. T., & Panizzi, R. C. (2013). Monitoramento de raças de Bremia lactucae em 2010 e 2011 no Estado de São Paulo. Summa Phytopathologica, 38, 271–279.

    Article  Google Scholar 

  • Hovius, M. H. Y., Carisse, O., Philion, V., & McDonald, M. R. (2007). Field evaluation of weather-based spray programs for the control of downy mildew of lettuce (Lactuca sativa), caused by Bremia lactucae, in Quebec and Ontario. Canadian Journal of Plant Patholology, 29, 9–17.

    Article  Google Scholar 

  • Hulbert, S. H., & Michelmore, R. W. (1988). DNA restriction fragment length polymorphism and somatic variation in the lettuce downy mildew fungus, Bremia lactucae. Molecular Plant Microbe Interacteraction, l, 1, 17–24.

    Article  Google Scholar 

  • ISF. (2020) The International Bremia Evaluation Board (IBEB). Available in: <https://www.worldseed.org/our-work/plant-health/other-initiatives/ibeb/>. 9/5000 Accessed in: 20 jan. 2020.

  • Lebeda, A. (1984). Race-specific factors of resistance to Bremia lactucae in the world assortment of lettuce. Scientia Horticulturae, 22, 23–32.

    Article  Google Scholar 

  • Lebeda A. (2002) Occurrence and Variation in Virulence of Bremia Lactucae in Natural Populations of Lactuca serriola. In: Spencer-Phillips P.T.N., Gisi U., Lebeda A. (eds) Advances in Downy Mildew Research. Springer, Dordrecht. https://doi.org/10.1007/0-306-47914-1_8

  • Lebeda, A., & Petrželová, I. (2004). Variation and distribution of virulence phenotypes of Bremia lactucae in natural populations of Lactuca serriola. Plant Pathology, 53, 316–324.

    Article  Google Scholar 

  • Lebeda, A., & Zinkernagel, V. (2003a). Characterization of new highly virulent German isolates of Bremia lactucae and efficiency of resistance in wild Lactuca spp. germplasm. Journal of Phytopathology, 151, 274–282.

    Article  Google Scholar 

  • Lebeda, A., & Zinkernagel, V. (2003b). Evolution and distribution of virulence in the German population of Bremia lactucae. Plant Pathology, 52, 41–51.

    Article  Google Scholar 

  • Lebeda, A., Pink, D. A. C., & Astley, D. (2002). Aspects of the interactions between wild Lactuca Spp. and related genera and lettuce downy mildew (Bremia lactucae). In P. T. N. Spencer- Phillips, U. Gisi, & A. Lebeda (Eds.), Advances in downy mildew research (pp. 85–117). Holanda: Kluwer Academic Publishers.

    Chapter  Google Scholar 

  • Marin, M. V., Franco, C. A., Smilde, D., Panizzi, R. C., & Braz, L. T. (2019). Distribution of races and virulence factors of Bremia lactucae in the main lettuce production area in Brazil. Journal of Plant Pathology, 102, 395–407.

    Article  Google Scholar 

  • McDonald, B. A. (2014). Using dynamic diversity to achieve durable disease resistance in agricultural ecosystems. Tropical Plant Pathology, 39(3), 191–196.

    Article  Google Scholar 

  • Michelmore, R. W., & Crute, I. R. (1982). A method for determining the virulence phenotype of Bremia lactucae isolates. Transactions of the British Mycological Society, 79, 542–546.

    Article  Google Scholar 

  • Michelmore, R., & Wong, J. (2008). Classical and molecular genetics of Bremia lactucae, cause of lettuce downy mildew. European Journal of Plant Pathology, 122, 19–30.

    Article  CAS  Google Scholar 

  • Michelmore, R. W., Christopoulou, M., & Caldwell, K. S. (2013). Impacts of resistance gene genetics, function and evolution on a durable future. Annual Review of Phytopathology, 51, 291–319.

    Article  CAS  Google Scholar 

  • Michelmore, R.W., Truco, M.J., Sanders, P., Xu, H., Kenefick, A., Gil, J., Simko, I., Mccreight, J., Subbarao, K., Gordon, T., Koike, S. (2018) Breeding Crisphead and leafy lettuce. Annual Report. Anais eletrônicos… Salina, CA, USA, 2018. Available in: <http://calgreens.org/wp-content/uploads/2018/08/Michelmore-Truco-crisp-leafy-report-2017-2018-06-23-18-final.pdf>. Accessed in January 20th, 2020.

  • Nordskog, B., Elameen, A., Gadoury, D. M., & Hermansen, A. (2014). Virulence characteristics of Bremia lactucae populations in Norway. European Journal of Plant Pathology, 139, 679–686.

    Article  Google Scholar 

  • Nunes, R. C., Castoldi, R., Gomes, R. F., Tobar-Tosse, D. E., & Braz, L. T. (2016). Levantamento de raças do agente causador do míldio da alface no Estado de São Paulo em 2012 e 2013. Summa Phytopathologica, 42, 53–58.

    Article  Google Scholar 

  • Parra, L., Maisonneuve, B., Lebeda, A., Schut, J., Christopoulou, M., Jeuken, M., Mchale, L., Truco, M. J., Crute, I., & Michelmore, R. (2016). Rationalization of genes for resistance to Bremia lactucae in lettuce. Euphytica, 210, 309–326.

    Article  CAS  Google Scholar 

  • Petrželová, I., Lebeda, A., & Kosman, E. (2013). Distribution, disease level and virulence variation of Bremia lactucae on Lactuca sativa in the Czech Republic in the period 1999-2011. Journal of Phytopathology, 161, 503–514.

    Article  Google Scholar 

  • Sharaf, K., Lewinsohn, D., Nevo, E., & Beharav, A. (2007). Virulence patterns of Bremia lactucae in Israel. Phytoparasitica, 35, 100–108.

    Article  Google Scholar 

  • Souza, J. O., Dalpian, T., Braz, L. T., & Camargo, M. (2011). Novas raças de Bremia lactucae, agente causador do míldio da alface, identificadas no estado de São Paulo. Horticultura Brasileira, 29, 282–286.

    Article  Google Scholar 

  • Spring, O., Gomez-Zeledon, J., Hadziabdic, D., Trigiano, R. N., Thines, M., & Lebeda, A. (2018). Biological characteristics and assessment of virulence diversity in Pathosystems of economically important biotrophic Oomycetes. Critical Reviews in Plant Sciences, 37(6), 439–495. https://doi.org/10.1080/07352689.2018.1530848.

    Article  CAS  Google Scholar 

  • Tobar-Tosse, D. E., dos Santos Candido, W., Marin, M. V., de Cassia Panizi, R., Barbosa, J. C., & Braz, L. T. (2017). Resistência de linhagens de alface crespa às raças de Bremia lactucae identificadas no Estado de São Paulo. Summa Phytopathologica, 43(1), 55–57.

    Article  Google Scholar 

  • Töfoli, J. G., Domingues, R. J., & Ferrari, J. T. (2014). Míldio e mofo branco da alface: doenças típicas de inverno. Biológico, 76, 19–24.

    Google Scholar 

  • Trimboli, D. S. (2004). A new pathotype of Bremia lactucae on lettuce in Australia. Australasian Plant Pathology, 33, 605.

    Article  CAS  Google Scholar 

  • Trimboli, D. S., & Nieuwenhuis, J. (2011). New races of Bremia lactucae on lettuce in Australia. Australasian Plant Disease Notes, 6, 62–63.

    Article  Google Scholar 

  • van Ettekoven, K., van der Arend, A. (1999) Identification and denomination of “new” races of Bremia lactucae. In: Lebeda, A., Křístková, E. (Eds.): Eucarpia Leafy Vegetables ´99, Proceedings of Eucarpia Meeting on Leafy Vegetables Genetics and Breeding. Palacký University, Olomouc (Czech Republic), p. 171–175.

  • van Hese, N., Huang, C. J., Vleesschauwer, D., Delaere, I., Pauwelyn, E., Bleyaert, P., & Höfte, M. (2016). Evolution and distribution of virulence characteristics of Belgian Bremia lactucae populations between 2008 and 2013. European Journal of Plant Pathology, 144, 431–441.

    Article  Google Scholar 

  • Vargas, P. F., Túlio, F. A., & Andrade, M. A. P. (2012). Monitoramento de raças de Bremia Lactucae em alface no Estado de Minas Gerais em 2010. Ciência et Praxis, 5, 7–10.

    Google Scholar 

Download references

Acknowledgments

Thanks go to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) - Financing Code 001 for a research grant, to members of NEOM and Matheus Flávio for help during this study, to the farmers for allowing us to collect the samples, to Agristar do Brasil Ltda. for assisting in the collection of samples, and to Dr. Diederik Smilde for providing the seeds for the different cultivars.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to C. A. Franco, M. V. Marin or L. T. Braz.

Ethics declarations

All authors of this research paper have directly participated in the planning, execution, or analysis of this study;

All authors of this research have read and approved the final version submitted;

The contents of this manuscript have not been copyrighted or published previously;

The contents of this manuscript are not now under consideration for publication elsewhere;

The contents of this manuscript will not be copyrighted, submitted, or published elsewhere, while acceptance by the Journal is under consideration;

There are no directly related manuscripts or abstracts, published or unpublished, by any authors of this paper.

All the authors declare no conflict of interest.

Supplementary Information

ESM 1

(DOCX 22 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Franco, C.A., Marin, M.V., Silva, E.H.C. et al. Monitoring virulence of Bremia lactucae as a breeding tool against lettuce downy mildew from south and southwest Brazilian regions. Eur J Plant Pathol 159, 179–189 (2021). https://doi.org/10.1007/s10658-020-02154-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-020-02154-y

Keywords

Navigation