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Fulvia fulva [syn. Cladosporium fulvum, Passalora fulva] races in Argentina are evolving through genetic changes and carry polymorphic avr and ecp gene sequences

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Abstract

The aim of this work was to study further the population of Fulvia fulva [syn. Cladosporium fulvum, Passalora fulva] in Argentina particularly in terms of diversity at the genetic level by means of ISSR. Also, we studied polymorphisms within avr and ecp sequences, what incidentally might lead to the development of new races. Argentinian tomato cultivars only are affected by two races of F. fulva and the data we provide here indicates that the populations of these two races are under an evolutionary process. Representatives of them had several polymorphisms within the coding sequences of effectors, but they are not constrained to avr genes, probably because, based on field data, resistant cultivars are not available. Most polymorphisms observed in avr and ecp genes were deletions or insertions (INDELs) or single nucleotide polymorphisms (SNPs). Therefore, probably the environment and management practices are the most important factors driving evolution of these races in Argentina and this might explain why the pathogen population is not driven at the pathogenic or race level.

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References

  • Allen, R. L., Bittner-Eddy, P. D., Grenville-Briggs, L. J., Meitz, J. C., Rehmany, A. P., Rose, L. E., & Beynon, J. L. (2004). Host-parasite coevolutionary conflict between Arabidopsis and downy mildew. Science, 306(5703), 1957–1960. https://doi.org/10.1126/science.1104022.

    Article  CAS  PubMed  Google Scholar 

  • Blancard, D., & Iglesias, A. P. (1988). Enfermedades del tomate: observar, identificar, luchar (N°. 635.6429 B535E.). Mundi-Prensa.

  • Bolton, M. D., & Thomma, B. P. H. J. (2008). The complexity of nitrogen metabolism and nitrogen-regulated gene expression in plant pathogenic fungi. Physiological and Molecular Plant Pathology, 72(4–6), 104–110. https://doi.org/10.1016/j.pmpp.2008.07.001.

    Article  CAS  Google Scholar 

  • Bolton, M. D., Van Esse, H. P., Vossen, J. H., De Jonge, R., Stergiopoulos, I., Stulemeijer, I. J. E., et al. Bolton M.D., van Esse H.P., Vossen J.H., de Jonge R., Stergiopoulos I., Stulemeijer I.J.E., van den Berg J.C.M., Borrás-Hidalgo O., Dekker H.L., de Koster C.G., de Wit P.J.G.M., Joosten M.H.A.J., & Thomma B.P.H.J. (2008). The novel Cladosporium Fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Molecular Microbiology, 69(1), 119–136. https://doi.org/10.1111/j.1365-2958.2008.06270.x.

  • De Jonge R., van Esse, H.P., Kombrink, A., Shinya, T., Desaki, Y., Bours, R., van der Krol , S., Shibuya, N., Joosten M.H.A.J., & Thomma B.P.H.J. (2010). Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science, 329(5994), 953–955. https://doi.org/10.1126/science.1190859.

  • De Wit, P. J. G. M. (1977). A light and scanning-electron microscopic study of infection of tomato plants by virulent and avirulent races of Cladosporium Fulvum. Netherlands Journal of Plant Pathology, 83(3), 109–122. https://doi.org/10.1007/BF01981556.

    Article  Google Scholar 

  • De Wit, P. J. G. M. (1982). Partial characterization and specificity of glycoprotein elicitors present in filtrates of cultures and cell walls of Cladosporium fulvum. Active Defence Mechanisms in Plants, 364–365.

  • De Wit, P. J. G. M. (1992). Molecular characterization of gene-for-gene systems in plant-fungus interactions and the application of avirulence genes in control of plant pathogens. Annual Review of Phytopathology, 30(1), 391–418. https://doi.org/10.1146/annurev.py.30.090192.002135.

    Article  PubMed  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), 1–23. https://doi.org/10.1146/annurev-phyto-011516-040249.

    Article  CAS  PubMed  Google Scholar 

  • De Wit, P. J. G. M., Joosten, M. H. A. J., Thomma, B. H. P. J., & Stergiopoulos, I. (2009a). Gene for gene models and beyond: The Cladosporium fulvum – Tomato pathosystem. Plant Relationships, 135–156. https://doi.org/10.1007/978-3-540-87407-2_7.

  • De Wit, P. J. G. M., Mehrabi, R., Van Den Burg, H. A., & Stergiopoulos, I. (2009b). Fungal effector proteins: Past, present and future: Review. Molecular Plant Pathology, 10(6), 735–747. https://doi.org/10.1111/j.1364-3703.2009.00591.x.

    Article  PubMed  Google Scholar 

  • De Wit, P. J. G. M., Van Der Burgt, A., Ökmen, B., Stergiopoulos, I., Abd-Elsalam, K. A., Aerts, A. L., Bahkali A.H., Beenen H.G., Chettri P., Cox M.P., Datema E., de Vries R.P., Dhillon B., Ganley A.R., Griffiths S.A., Guo Y., Hamelin R.C., enrissat B., Shahjahan Kabir M, Karimi Jashni M., Kema G., Klaubauf S., Lapidus A., Levasseur A., Lindquist E., Mehrabi R., Ohm R.A., Owen T.J., Salamov A., Schwelm A., Schijlen E., Sun H., van den Burg H.A., van Ham R.C.H.J., Zhang S., Goodwin S.B., Grigoriev I.V., Collemare J., & Bradshaw R.E. (2012). The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry. PLoS Genetics, 8(11), 23209441. https://doi.org/10.1371/journal.pgen.1003088.

  • Dixon, M. S., Jones, D. A., Keddie, J. S., Thomas, C. M., Harrison, K., & Jones, J. D. G. (1996). The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell, 84(3), 451–459. https://doi.org/10.1016/S0092-8674(00)81290-8.

    Article  CAS  PubMed  Google Scholar 

  • Dixon, M. S., Hatzixanthis, K., Jones, D. A., Harrison, K., & Jones, J. D. G. (1998). The tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell, 10, 1915–1925. https://doi.org/10.1105/tpc.10.11.1915.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dodds, P. N., Lawrence, G. J., Catanzariti, A. M., Teh, T., Wang, C. I. A., Ayliffe, M. A., Kobe, B., & Ellis, J. G. (2006). Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proceedings of the National Academy of Sciences, 103(23), 8888–8893. https://doi.org/10.1073/pnas.0602577103.

    Article  CAS  Google Scholar 

  • Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5), 1792–1797. https://doi.org/10.1093/nar/gkh340.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Excoffier, L., & Lischer, H. E. L. (2010). Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and windows. Molecular Ecology Resources., 10, 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x.

    Article  PubMed  Google Scholar 

  • Franco, M. E. E., Troncozo, M. I., López, S. M. Y., Lucentini, C. G., Medina, R., Saparrat, M. C. N., Ronco B.L. & Balatti, P.A. (2017). A survey on tomato leaf grey spot in the two main production areas of Argentina led to the isolation of Stemphylium lycopersici representatives which were genetically diverse and differed in their virulence. European Journal of Plant Pathology, 149(4), 983–1000. https://doi.org/10.1007/s10658-017-1248-z.

  • Gabriëls, S. (2006). Functional analysis of tomato genes expressed during the Cf-4/Avr4- induced hypersensitive response. Thesis Wageningen University, The Netherlands. ISBN 90-8504-405-7, https://pdfs.semanticscholar.org/b16a/f07b3e41d361bdee9d1a9c0807a2aa0d0628.pdf#page=63.

  • Heath, M. C. (2000). Hypersensitive response-related death. Plant Molecular Biology, no., 44, 321–334.

    Article  CAS  Google Scholar 

  • Iakovidis, M., Soumpourou, E., Anderson, E., Etherington, G., Yourstone, S., & Thomas, C. (2020). Genes encoding recognition of the Cladosporium fulvum effector protein Ecp5 are encoded at several loci in the tomato genome. G3: Genes, Genomes. Genetics, 10(5), 1753–1763. https://doi.org/10.1534/g3.120.401119.

    Article  CAS  Google Scholar 

  • Iida, Y., Van ’T Hof, P., Beenen, H., Mesarich, C. H., Kubota, M., Stergiopoulos, I., Rahim Mehrabi R., Notsu A., Fujiwara K., Bahkali A., Abd-Elsalam K., Collemare J., & de Wit P.J.G.M(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), 1–18. https://doi.org/10.1371/journal.pone.0123271.

  • Jashni, M. K., Van Der Burgt, A., Battaglia, E., Mehrabi, R., Collemare, J., & De Wit, P. J. G. M. (2019). Transcriptome and proteome analyses of proteases in biotroph fungal pathogen Cladosporium fulvum. Journal of Plant Pathology, 102, 377–386. https://doi.org/10.1007/s42161-019-00433-0.

    Article  Google Scholar 

  • Jones, D. A., Thomas, C. M., Hammond-Kosack, K. E., Balint-Kurti, P. J., & Jones, J. D. G. (1994). Isolation of the tomato Cf- 9 gene for resistance to Cladosporium fulvum by transposon tagging. Science, 266, 789–793. https://doi.org/10.1126/science.7973631.

    Article  CAS  PubMed  Google Scholar 

  • Joosten, M. H., Cozijnsen, T. J., & De Wit, P. J. (1994). Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene. Nature, 367(6461), 384–386. https://doi.org/10.1038/367384a0.

    Article  CAS  PubMed  Google Scholar 

  • Joosten, M. H., Vogelsang, R., Cozijnsen, T. J., Verberne, M. C., & De Wit, P. J. G. M. (1997). The biotrophic fungus Cladosporium fulvum circumvents Cf-4-mediated resistance by producing unstable AVR4 elicitors. The Plant Cell, 9(3), 367–379. https://doi.org/10.1105/tpc.9.3.367.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kahlon, P. S., Seta, S. M., Zander, G., Scheikl, D., Hückelhoven, R., Joosten, M. H., & Stam, R. (2020). Population studies of the wild tomato species Solanum chilense reveal geographically structured major gene-mediated pathogen resistance. bioRxiv, 020.05.29.122960. https://doi.org/10.1101/2020.05.29.122960.

  • Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., & Drummond, A. (2012). Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28(12), 1647–1649. https://doi.org/10.1093/bioinformatics/bts199.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kruijt, M., Kip, D. J., Joosten, M. H., Brandwagt, B. F., & de Wit, P. J. (2005). The Cf-4 and Cf-9 resistance genes against Cladosporium fulvum are conserved in wild tomato species. Molecular Plant-Microbe Interactions, 18(9), 1011–1021. https://doi.org/10.1094/MPMI-18-1011.

    Article  CAS  PubMed  Google Scholar 

  • Laugé, R., Joosten, M. H. A. J., Van Den Ackerveken, G. F. J. M., Van Den Broek, H. W. J., & De Wit, P. J. G. M. (1997). The in planta-produced extracellular proteins ECP1 and ECP2 of Cladosporium fulvum are virulence factors. Molecular Plant-Microbe Interactions : MPMI, 10(6), 725–734. https://doi.org/10.1094/MPMI.1997.10.6.725.

    Article  Google Scholar 

  • Laugé, R., Joosten, M. H. A. J., Haanstra, J. P. W., Goodwin, P. H., Lindhout, P., & De Wit, P. J. G. M. (1998). Successful search for a resistance gene in tomato targeted against a virulence factor of a fungal pathogen. Proceedings of the National Academy of Sciences, 95(15), 9014–9018. https://doi.org/10.1073/pnas.95.15.9014.

    Article  Google Scholar 

  • Laugé, R., Goodwin, P. H., De Wit, P. J. G. M., & Joosten, M. H. A. J. (2000). Specific HR-associated recognition of secreted proteins from Cladosporium Fulvum occurs in both host and non-host plants. Plant Journal, 23(6), 735–745. https://doi.org/10.1046/j.1365-313X.2000.00843.x.

    Article  Google Scholar 

  • Lazarovits, G., & Higgins, V. J. (1976). Histological comparison of Cladosporium fulvum race 1 on immune, resistant, and susceptible tomato varieties. Canadian Journal of Botany, 54(3), 224–234. https://doi.org/10.1139/b76-022.

    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(3), 143–148. https://doi.org/10.1007/BF01999969.

    Article  Google Scholar 

  • Luderer, R. F. L., Takken, W., De Wit, P. J. G. M., & Joosten, M. H. A. J. (2002a). Cladosporium Fulvum overcomes Cf-2-mediated resistance by producing truncated AVR2 elicitor proteins. Molecular Microbiology, 45(3), 875–884. https://doi.org/10.1046/j.1365-2958.2002.03060.x.

    Article  CAS  PubMed  Google Scholar 

  • Luderer, R., De Kock, M. J. D., Dees, R. H. L., De Wit, P. J. G. M., & Joosten, M. H. A. J. (2002b). Functional analysis of cystein residues of Ecp elicitor proteins of the fungal tomato pathogen Cladosporium fulvum. Molecular Plant Pathology, 3, 91–95. https://doi.org/10.1046/j.1464-6722.2001.00095.x.

    Article  CAS  PubMed  Google Scholar 

  • Ma, W., & Guttman, D. S. (2008). Evolution of prokaryotic and eukaryotic virulence effectors. Current Opinion in Plant Biology, 11(4), 412–419. https://doi.org/10.1016/j.pbi.2008.05.001.

    Article  CAS  PubMed  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., & 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(12), 1732–1737. https://doi.org/10.1094/PDIS-12-14-1270-RE.

    Article  PubMed  Google Scholar 

  • Mesarich, C. H., Griffiths, S. A., Van Der Burgt, A., Ӧkmen, B., Beenen, H. G., Etalo, D. W., Joosten M.H.A.J. & de Wit P.J.G. M. (2014). Transcriptome sequencing uncovers the Avr5 Avirulence gene of the tomato leaf mold pathogen Cladosporium Fulvum. MolPlant Microbe Interact., 27(8), 846–857. https://doi.org/10.1094/MPMI-02-14-0050-R.

  • Mesarich, C. H., Ӧkmen, B., Rovenich, H., Griffiths, S. A., Wang, C., Karimi Jashni, M., Mihajlovski, A., Collemare, J., Hunziker, L., Deng, C. H., van der Burgt, A., Beenen, H. G., Templeton, M. D., Bradshaw, R. E., & de Wit, P. J. G. M. (2018). Specific hypersensitive response–associated recognition of new apoplastic effectors from Cladosporium fulvum in wild tomato. Molecular Plant-Microbe Interactions, 31(1), 145–162. https://doi.org/10.1094/MPMI-05-17-0114-FI.

    Article  PubMed  Google Scholar 

  • Ökmen, B., Etalo, D. W., Joosten, M. H. A. J., Bouwmeester, H. J., De Vos, R. C. H., Collemare, J. & de Wit P.J.G.M. (2013). Detoxification of α-tomatine by Cladosporium fulvum is required for full virulence on tomato. New Phytologist, 198(4), 1203–1214. https://doi.org/10.1111/nph.12208.

  • Rivas, S., & Thomas, C. M. (2005). Molecular interactions between tomato and the leaf mold pathogen Cladosporium Fulvum. Annual Review of Phytopathology, 43(1), 395–436. https://doi.org/10.1146/annurev.phyto.43.040204.140224.

    Article  CAS  PubMed  Google Scholar 

  • Rollan, C., Protto, V., Medina, R., Lopez, S. M. Y., Bahima, J. V., Ronco, L., Saparrat M.C.N., & Balatti P.A. (2013). Identification of races 0 and 2 of Cladosporium fulvum (Syn. Passalora fulva) on tomato in the cinturón hortícola de La Plata, Argentina. Plant Disease, 97(7). https://doi.org/10.1094/PDIS-10-12-0987-PDN.

  • Sambrook, J., Fritsch, E. F., & Maniatis, T. (1989). Molecular cloning: a laboratory manual (no. Ed. 2). New York: Cold Spring Harbor Laboratory Press.

    Google Scholar 

  • Sánchez-Vallet, A., Saleem-Batcha, R., Kombrink, A., Hansen, G., Valkenburg, D. J., Thomma, B. P., & Mesters, J. R. (2013). Fungal effector Ecp6 outcompetes host immune receptor for chitin binding through intrachain LysM dimerization. elife, 2, e00790. https://doi.org/10.7554/eLife.00790.

    Article  PubMed  PubMed Central  Google Scholar 

  • Soanes, D. M., & Talbot, N. J. (2008). Moving targets: Rapid evolution of oomycete effectors. Trends in Microbiology, 16(11), 507–510. https://doi.org/10.1016/j.tim.2008.08.002.

    Article  CAS  PubMed  Google Scholar 

  • Stavrinides, J., McCann, H. C., & Guttman, D. S. (2008). Host-pathogen interplay and the evolution of bacterial effectors. Cellular Microbiology, 10(2), 285–292. https://doi.org/10.1111/j.1462-5822.2007.01078.x.

    Article  CAS  PubMed  Google Scholar 

  • Stergiopoulos, I., & De Wit, P. J. G. M. (2009). Fungal effector proteins. Annual Review of Phytopathology, 47, 233–263. https://doi.org/10.1146/annurev.phyto.112408.132637.

    Article  CAS  PubMed  Google Scholar 

  • Stergiopoulos, I., De Kock, M. J. D., Lindhout, P., & De Wit, P. J. G. M. (2007). Allelic variation in the effector genes of the tomato pathogen Cladosporium fulvum reveals different modes of adaptive evolution. Molecular Plant-Microbe Interactions : MPMI, 20(10), 1271–1283. https://doi.org/10.1094/MPMI-20-10-1271.

    Article  CAS  PubMed  Google Scholar 

  • Stergiopoulos, I., van den Burg, H. A., Okmen, B., Beenen, H. G., Van Liere, S., Kema, G. H. J., & De Wit, P. J. G. M. (2010). Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots. Proceedings of the National Academy of Sciences, 107(16), 7610–7615. https://doi.org/10.1073/pnas.1002910107.

    Article  Google Scholar 

  • Stergiopoulos, I., Kourmpetis, Y. A., Slot, J. C., Bakker, F. T., De Wit, P. J., & Rokas, A. (2012). In silico characterization and molecular evolutionary analysis of a novel superfamily of fungal effector proteins. Molecular Biology and Evolution, 29(11), 3371–3384. https://doi.org/10.1093/molbev/mss143.

    Article  CAS  PubMed  Google Scholar 

  • Stergiopoulos, I., Cordovez, V., Ökmen, B., Beenen, H. G., Kema, G. H. J., & De Wit, P. J. G. M. (2014). Positive selection and intragenic recombination contribute to high allelic diversity in effector genes of Mycosphaerella fijiensis, causal agent of the black leaf streak disease of banana. Molecular Plant Pathology, 15(5), 447–460. https://doi.org/10.1111/mpp.12104.

    Article  CAS  PubMed  Google Scholar 

  • Takken, F. L. W., Thomas, C. M., Joosten, M. H. A. J., Golstein, C., Westerink, N., Hille, J., Nijkamp, H. J. J., de Wit, P. J. G. M., & Jones, J. D. G. (1999). A second gene at the tomato Cf-4 locus confers resistance to Cladosporium fulvum through recognition of a novel avirulence determinant. The Plant Journal, 20, 279–288. https://doi.org/10.1046/j.1365-313X.1999.00601.x.

    Article  CAS  PubMed  Google Scholar 

  • Thomas, C. M., Jones, D. A., Parniske, M., Harrison, K., Balint-Kurti, P. J., Hatzixanthis, K., & Jones, J. D. (1997). Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell, 9, 2209–2224. https://doi.org/10.1105/tpc.9.12.2209.

    Article  CAS  PubMed  PubMed Central  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. https://doi.org/10.1007/BF00301063.

    Article  CAS  PubMed  Google Scholar 

  • Thomma, B. P., Nürnberger, T., & Joosten, M. H. (2011). Of PAMPs and effectors: The blurred PTI-ETI dichotomy. The Plant Cell, 23(1), 4–15. https://doi.org/10.1105/tpc.110.082602.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). ClustalW: Improving the sensitivity of progressive multiple sequence aligment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research Acids Res, 22(22), 4673–4680. https://doi.org/10.1093/nar/22.22.4673.

    Article  CAS  Google Scholar 

  • Van den Ackerveken, G. F. J. M., Van Kan, J. A. L., & De Wit, P. J. G. M. (1992). Molecular analysis of the avirulence gene Avr9 of the fungal tomato pathogen Cladosporium fulvum fully supports the gene-for-gene hypothesis. The Plant Journal, 2, 359–366. https://doi.org/10.1046/j.1365-313X.1992.t01-34-00999.x.

    Article  PubMed  Google Scholar 

  • Van den Ackerveken, G. F. J. M., Vossen, P., & De Wit, P. J. G. M. (1993). The AVR9 race-specific elicitor of Cladosporium fulvum is processed by endogenous and plant proteases. Plant Physiology, 103(1), 91–96. https://doi.org/10.1104/pp.103.1.91.

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Den Burg, H. A., Harrison, S. J., Joosten, M. H. A. J., Vervoort, J., & De Wit, P. J. G. M. (2006). Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Molecular Plant-Microbe Interactions, 19(12), 1420–1430. https://doi.org/10.1094/MPMI-19-1420.

    Article  CAS  PubMed  Google Scholar 

  • Van Den Hooven, H. W., Appelman, A. W. J., Zey, T., De Wit, P. J. G. M., & Vervoort, J. (1999). Folding and conformational analysis of AVR9 peptide elicitors of the fungal tomato pathogen Cladosporium fulvum. European Journal of Biochemistry, 264(1), 9–18. https://doi.org/10.1046/j.1432-1327.1999.00503.x.

    Article  PubMed  Google Scholar 

  • Van Den Hooven, H. W., Van Den Burg, H. A., Vossen, P., Boeren, S., De Wit, P. J. G. M., & Vervoort, J. (2001). Disulfide bond structure of the AVR9 elicitor of the fungal tomato pathogen Cladosporium fulvum: Evidence for a cystine knot. Biochemistry, 40(12), 3458–3466. https://doi.org/10.1021/bi0023089.

    Article  CAS  PubMed  Google Scholar 

  • Van der Hoorn, R. A., Roth, R., & De Wit, P. J. (2001). Identification of distinct specificity determinants in resistance protein Cf-4 allows construction of a Cf-9 mutant that confers recognition of avirulence protein AVR4. The Plant Cell, 13(2), 273–285. https://doi.org/10.1105/tpc.13.2.273.

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Kan, J. A., Van Den Ackerveken, G. F. J. M., & De Wit, P. J. G. M. (1991). Cloning and characterization of cDNA of avirulence gene Avr9 of the fungal pathogen Cladosporium Fulvum, causal agent of tomato leaf mold. Molecular Plant-Microbe Interactions, 8, e53937. https://doi.org/10.1371/journal.pone.0053937.

    Article  CAS  Google Scholar 

  • Westerink, N., Joosten, M. H. A. J., & De Wit, P. J. G. M. (2004a). Fungal (a)virulence factors at the crossroads of disease susceptibility and resistance. In Z. K. Punja (Ed.), Fungal disease resistance in plants: Biochemistry, molecular biology, and genetic engineering (pp. 93–137). Binghamton: Food Products Press.

    Google Scholar 

  • Westerink, N., Brandwagt, B. F., De Wit, P. J. G. M., & Joosten, M. H. A. J. (2004b). Cladosporium Fulvum circumvents the second functional resistance gene homologue at the Cf-4 locus (Hcr9-4E) by secretion of a stable avr4E isoform. Molecular Microbiology, 54(2), 533–545. https://doi.org/10.1111/j.1365-2958.2004.04288.x.

    Article  CAS  PubMed  Google Scholar 

  • White, T. J., Bruns, S., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal rna genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications, citeulike-article-id:671166.

  • Wulff, B. B. H., Chakrabarti, A., & Jones, D. A. (2009). Recognitional specificity and evolution in the tomato– Cladosporium fulvum pathosystem. Molecular Plant-Microbe Interactions, 22(10), 1191–1202. https://doi.org/10.1094/MPMI-22-10-1191.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We wish to thank to Ph Pierre J.G.M. De Wit, from the Laboratory of Phytopathology, Wageningen University, Wageningen, Netherlands, for his valuable contribution.

Funding

This work was supported by the Universidad Nacional de La Plata y la Comision de Investigaciones Científicas de la Provincia de Buenos Aires (CICBA).

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Authors and Affiliations

  1. Centro de Investigación de Fitopatologías, Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata, La Plata, Buenos Aires, Argentina

    César G. Lucentini, Roció Medina & Pedro A. Balatti

  2. Comisión de Investigaciones Científicas de la provincia de Buenos Aires (CICBA), Buenos Aires, Argentina

    César G. Lucentini & Pedro A. Balatti

  3. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina

    Roció Medina, Mario C. N. Saparrat & Pedro A. Balatti

  4. Department of Agricultural and Biosystems Engineering, University of Arizona, Tucson, AZ, USA

    Mario E. E. Franco

  5. Cátedra de Microbiología Agrícola, Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata, La Plata, Buenos Aires, Argentina

    Mario C. N. Saparrat

  6. Instituto de Fisiología Vegetal, Facultad de Ciencias Naturales y Museo-Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata. CCT-La Plata-CONICET, La Plata, Buenos Aires, Argentina

    Mario C. N. Saparrat

  7. Instituto de Botánica Carlos Spegazzini, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, La Plata, Buenos Aires, Argentina

    Mario C. N. Saparrat

Authors
  1. César G. Lucentini
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  2. Roció Medina
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  3. Mario E. E. Franco
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  4. Mario C. N. Saparrat
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  5. Pedro A. Balatti
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Corresponding author

Correspondence to Pedro A. Balatti.

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Declaration of competing interest

The authors declare that they have no competing interests.

This work does not include research involving humand participants and/or animals-.

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Lucentini, C.G., Medina, R., Franco, M.E.E. et al. Fulvia fulva [syn. Cladosporium fulvum, Passalora fulva] races in Argentina are evolving through genetic changes and carry polymorphic avr and ecp gene sequences. Eur J Plant Pathol 159, 525–542 (2021). https://doi.org/10.1007/s10658-020-02181-9

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