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The first report on the occurrence race 9 of the tomato leaf mold pathogen Cladosporium fulvum (syn. Passalora fulva) in Cuba

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Abstract

Leaf mold caused by the fungus Cladosporium fulvum (syn. Passalora fulva) has been a serious disease in greenhouse tomatoes in Cuba, but less damage is seen in outdoor grown plants. This study was conducted to identify races of the causal agent of tomato leaf mold. A total of 36 single conidial isolates obtained from different provinces in Cuba and the reference strain race 0 were inoculated on a differential set of tomato cultivars carrying different Cf resistance genes. Further, a polymerase chain reaction (PCR) was developed using Avr9 gene-specific primers. As result, all isolates could overcome the Cf-9 resistance gene only, but not resistance genes Cf-2, Cf-4 and Cf-5 and must therefore be coined race 9. Race identity was also confirmed by PCR analysis, which showed that the Avr9 gene was not amplified in any of 36 single conidial isolates studied proving that they all lack this gene. This is the first report of the occurrence of race 9 of C. fulvum in Cuba. Pyramiding other Cf genes in hybrid of tomato may provide a more durable level of resistance to C. fulvum.

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References

  • Altin, N. (2016). Identification of race 2.5 of leaf mold (Passalora fulva, syn. Cladosporium fulvum) on tomato. Journal of Plant Diseases and Protection, 123, 279–284.

    Article  Google Scholar 

  • Bernal, A., Martínez, B., & Infante, D. (2009). Method for the evaluation of the response of tomato genotypes inoculated with Passalora fulva (Cooke) U. Braun and Crous in a greenhouse. Revista de Protección Vegetal, 24(2), 102–105.

    Google Scholar 

  • Bernal, A., Infante, D., Martínez, B., Herrera, L., de Wit, P. J. G. M., Peteira, B., & Leiva, M. (2020). First report on the occurrence of Cladosporium fulvum strains in Cuba that can overcome the Cf-9 resistance gene. Revista de Protección Vegetal, 35(1), 1.

    Google Scholar 

  • Braun, U., Crous, P. W., Dugan, F., Groenewald, J. E., & De Hoog, G. S. (2003). Phylogeny and taxonomy of Cladosporium-like hyphomycetes, including Davidiella gen. Nov., the teleomorph of Cladosporium s. str. Mycological Progress, 2(1), 3–18.

    Article  Google Scholar 

  • de Wit, P. J. G. M. (2016). Cladosporium fulvum effectors: Weapons in the arms race with tomato. Annual Review of Phytopathology, 54, 1–23.

    Article  Google Scholar 

  • Enya, J., Ikeda, K., Takeuchi, T., Horikoshi, N., Higashi, T., Sakai, T., Lida, Y., Nishi, K., & Kubota, M. (2009). The first occurrence of leaf mold of tomato caused by races 4.9 and 4.9.11 of Passalora fulva (syn. Fulvia fulva) in Japan. Journal of General Plant Pathology, 75, 76–79.

    Article  Google Scholar 

  • Hubbeling, N. (1978). Breakdown of resistance of the Cf5 gene in tomato by another new race of Fulvia fulva. Medelelingen van de Facultiet voor Landbouwwetenschappen van de Rijksuniversitiet Gent, 43, 891–894.

    Google Scholar 

  • Iida, Y., Iwadate, Y., Kubota, M., & Terami, F. (2010). Occurrence of a new race 2.9 of leaf mold of tomato in Japan. Journal of General Plant Pathology, 76, 84–86.

    Article  Google Scholar 

  • Iida, Y., van’t Hof, P., Beenen, H., Mesarich, C., Kubota, M., Stergiopoulos, I., Mehrabi, R., Notsu, A., Fujiwara, K., Bahkali, A., Abd-Elsalam, K., Collemare, J., & de Wit, P. J. (2015). Novel mutations detected in avirulence genes overcoming tomato Cf resistance genes in isolates of a Japanese population of Cladosporium fulvum. PLoS One, 10(4), e0123271.

    Article  Google Scholar 

  • Kourelis, J., & van der Hoorn, R. A. (2018). Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function. Plant Cell, 30(2), 285–299.

    Article  CAS  Google Scholar 

  • Kubota, M., Morishima, M., & Iida, Y. (2015). First occurrence of tomato leaf mold caused by race 2.5.9 and 4.5.9 of the pathogen, Passalora fulva, in Japan. Journal of General Plant Pathology, 81, 320–323.

    Article  Google Scholar 

  • Laterrot, H. (1986). Race 2.5.9 a new race of Cladosporium fulvum (Fulvia fulva) and sources of resistance in tomato. Netherlands Journal of Plant Pathology, 92, 305–307.

    Article  Google Scholar 

  • Li, S., Zhao, T., Li, H., Xu, X., & Li, J. (2015). First report of races 2.5 and 2.4.5 of Cladosporium fulvum (syn. Passalora fulva), causal fungus of tomato leaf mold disease in China. Journal of General Plant Pathology, 81, 162–165.

    Article  Google Scholar 

  • Lindhout, P., Korta, W., Cislik, M., Vos, I., & Gerlagh, T. (1989). Further identification of races of Cladosporium fulvum (Fulvia fulva) on tomato originating from the Netherlands, France and Poland. Netherlands Journal of Plant Pathology, 95, 143–148.

    Article  Google Scholar 

  • Medina, R., López, S. M. Y., Franco, M. E. E., Rollan, C., Ronco, B. L., Saparrat, M. C. N., de Wit, P. J. G. M. G. M., & Balatti, P. A. (2015). A survey on occurrence of Cladosporium fulvum identifies race 0 and race 2 in tomato-growing areas of Argentina. Plant Disease, 99, 1732–1737.

    Article  Google Scholar 

  • Mesarich, C. H., Ӧkmen, B., Rovenich, H., Griffiths, S. A., Wang, C., Karimi Jashni, M., & Van Der Burgt, A. (2017). Specific hypersensitive response–associated recognition of new apoplastic effectors from Cladosporium fulvum in wild tomato. Molecular Plant-Microbe Interactions, 31(1), 145–162.

    Article  Google Scholar 

  • Satou, M., Shinozaki, T., Nishi, K., & Kubota, M. (2005). Leaf mold of tomato caused by races 4 and 4.11 of Passalora fulva in Japan. Journal of General Plant Pathology, 71, 436–437.

    Article  Google Scholar 

  • Stergiopoulos, I., De Kock, M. J., Lindhout, P., & de Wit, P. J. (2007). Allelic variation in the effector genes of the tomato pathogen Cladosporium fulvum reveals different modes of adaptive evolution. Molecular Plant-Microbe Interactions, 20(10), 1271–1283.

    Article  CAS  Google Scholar 

  • Thomma, B. P. H. J., van Esse, H. P., Crous, P. W., & de Wit, P. J. G. M. (2005). Cladosporium fulvum (syn. Passalora fulva), a highly specialized plant pathogen as a model for functional studies on plant pathogenic Mycosphaerellaceae. Molecular Plant Pathology, 6(4), 379–393.

    Article  CAS  Google Scholar 

  • Van den Ackerveken, G. F. J. M., Vossen, P., & de Wit, J. G. M. P. (1993). The Avr9 race-specific elicitor of Cladosporium fulvum is processed by endogenous and plant proteases. Plant Physiology, 103, 91–96.

    Article  Google Scholar 

  • Westerink, N., Brandwagt, B. F., de Wit, P. J. G. M., & Joosten, M. H. A. J. (2004). Cladosporium fulvum circumvents the second functional resistance gene homologue at the Cf-4 locus (Hcr9–4E) by secretion of a stable avr4E isoform. Molelucar Microbiology, 54, 533–545.

    Article  CAS  Google Scholar 

  • Yoshida, K., Asano, S., Sushida, H., & Lida, Y. (2021). Occurrence of tomato leaf mold caused by novel race 2.4.9 of Cladosporium fulvum in Japan. Journal of General Plant Pathology, 87, 35–38.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Prof. PhD. Monica Höfte (Ghent University) for providing seeds of cultivar Moneymaker NILs and Prof. PhD. Bart Thomma (Wageningen University), Luis Rojas and PhD. María I. Oloriz (Instituto de Biotecnología de las Plantas) for supplying laboratory facilities. This research was performed in the frame of the Institutional University Cooperation Programme with Universidad Central “Marta Abreu” de Las Villas, supported by the Flemish Interuniversity Council (IUC UCLV/VLIR).

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Correspondence to Alexander Bernal-Cabrera.

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Bernal-Cabrera, A., Martínez-Coca, B., Herrera-Isla, L. et al. The first report on the occurrence race 9 of the tomato leaf mold pathogen Cladosporium fulvum (syn. Passalora fulva) in Cuba. Eur J Plant Pathol 160, 731–736 (2021). https://doi.org/10.1007/s10658-021-02261-4

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