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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

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Abstract

Tomato gray leaf spot was first reported in Argentina in 1990. Since then, the disease has not only increased in endemic areas, but also disseminated in other tomato-growing areas. In a survey of plants with typical symptoms of Tomato grey leaf spot disease we isolated 27 Stemphylium representatives from the two main tomato-growing areas of Argentina. Cultural features such as sporulation, conidia morphometry among others revealed high variability between isolates, which was confirmed by Inter Simple Sequence Repeat (ISSR)-PCR technique. A molecular phylogenetic analysis comprising the Internal Transcribed Spacer (ITS) and the glyceraldehyde-3-phosphate dehydrogenase (gpd) gene partial sequences unambiguously identified all isolates as Stemphylium lycopersici. Based on disease severity on detached leaves, isolates were grouped in three categories (high, medium and low virulent). No correlation was found between phenotypic or genotypic characters and the geographical origin of the isolates.

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References

  • Akaike, H. (1974). A new look at the statistical model identification. IEEE Transactions on Automatic Control, 19(6), 716–723.

    Article  Google Scholar 

  • Al-Amri, K., Al-Sadi, A. M., Al-Shihi, A., Nasehi, A., Al-Mahmooli, I., & Deadman, M. L. (2016). Population structure of Stemphylium lycopersici associated with leaf spot of tomato in a single field. SpringerPlus, 5(1), 1642.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bentes, J. L., & Matsuoka, K. (2005). Histologia da interação Stemphylium solani e tomateiro. Fitopatologia Brasileira, 30, 224–231.

    Article  Google Scholar 

  • Blancard, D. (2012). A colour handbook. Tomato diseases. Identification, biology and control. 2nd ed. London: Manson Publishing Ltd.

  • Bornet, B., & Branchard, M. (2001). Nonanchored inter simple sequence repeat (ISSR) markers: reproducible and specific tools for genome fingerprinting. Plant Molecular Biology Reporter, 19(3), 209–215.

    Article  CAS  Google Scholar 

  • Câmara, M. P., O’Neill, N. R., & Van Berkum, P. (2002). Phylogeny of Stemphylium spp. based on ITS and glyceraldehyde-3-phosphate dehydrogenase gene sequences. Mycologia, 94(4), 660–672.

    Article  PubMed  Google Scholar 

  • Chaisrisook, C., Skinner, D. Z., & Stuteville, D. L. (1995). Molecular genetic relationships of five Stemphylium species pathogenic to alfalfa. Sydowia, 47(1), 1–9.

    Google Scholar 

  • Colombo, M. D. H., & Obregón, V. G. (2008). Primera cita de Stemphylium solani en plantines de pimiento en almácigo en la Provincia de Corrientes. In Congreso Argentino de Fitopatología. 1. 2008 05 28-30, 28-30 de mayo de 2008. Córdoba. AR.

  • Colombo, M. D. H., Lenscak, M. P., & Ishikawa, A. (2001). Mancha gris del tomate causada por Stemphylium floridanum. Primera cita en Argentina. Reunión de Comunicaciones Científicas y Técnicas. 12. 2001 08 01-03, 1 al 3 de Agosto 2001. Corrientes. AR.

  • Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9(8), 772–772.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Rienzo, J. A., Casanoves, F., Balzarini, M. G., Gonzalez, L., Tablada, M., & Robledo, C. W. (2015). InfoStat versión 2015l. Córdoba: Universidad Nacional de Córdoba.

  • Ellis, M. B. (1971). Dematiaceous hyphomycetes (608 p). Kew: Common wealth Mycological Institute.

    Google Scholar 

  • Ellis, M. B., & Gibson, I. A. S. (1975a). Stemphylium solani. CMI descriptions of pathogenic fungi and bacteria (472).

  • Ellis, M. B., & Gibson, I. A. S. (1975b). Stemphylium lycopersici. CMI descriptions of pathogenic fungi and bacteria (471).

  • Excoffier, L., Laval, G., & Schneider, S. (2005). Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47.

    CAS  Google Scholar 

  • FAOSTAT (2016). FAO. http://faostat.fao.org/. Accessed 2016.

  • Farr D.F., & Rossman, A.Y. (2016) Fungal databases, systematic mycology and microbiology laboratory, ARS, USDA. From http://nt.ars-grin.gov/fungaldatabases/. Accessed 2016.

  • Farris, J. S., Källersjö, M., Kluge, A. G., & Bult, C. (1994). Testing significance of incongruence. Cladistics, 10(3), 315–319.

    Article  Google Scholar 

  • Franco, M. E., López, S., Medina, R., Saparrat, M. C., & Balatti, P. (2015). Draft genome sequence and gene annotation of Stemphylium lycopersici strain CIDEFI-216. Genome Announcements, 3(5), e01069–e01015.

    Article  PubMed  PubMed Central  Google Scholar 

  • Griffith, G. W., Easton, G. L., Detheridge, A., Roderick, K., Edwards, A., Worgan, H. J., Nicholson, J., & Perkins, W. T. (2007). Copper deficiency in potato dextrose agar causes reduced pigmentation in cultures of various fungi. FEMS Microbiology Letters, 276(2), 165–171.

    Article  CAS  PubMed  Google Scholar 

  • Guindon, S., & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52(5), 696–704.

    Article  PubMed  Google Scholar 

  • Hannon, C. I., & Weber, G. F. (1955). A leaf spot of tomato caused by Stemphylium floridanum sp. nov. Phytopathology, 45(1), 11–16.

    Google Scholar 

  • Hawker, L. E. (2016). The physiology of reproduction in fungi. London: Cambridge University Press.

  • Hong, S. K., Choi, H. W., Lee, Y. K., Shim, H. S., & Lee, S. Y. (2012). Leaf spot and stem rot on Wilford swallowwort caused by Stemphylium lycopersici in Korea. Mycobiology, 40(4), 268–271.

    Article  PubMed  PubMed Central  Google Scholar 

  • Inderbitzin, P., Harkness, J., Turgeon, B. G., & Berbee, M. L. (2005). Lateral transfer of mating system in Stemphylium. Proceedings of the National Academy of Sciences of the United States of America, 102(32), 11390–11395.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inderbitzin, P., Mehta, Y. R., & Berbee, M. L. (2009). Pleospora species with Stemphylium anamorphs: a four locus phylogeny resolves new lineages yet does not distinguish among species in the Pleospora herbarum clade. Mycologia, 101(3), 329–339.

    Article  CAS  PubMed  Google Scholar 

  • Joly, P. (1962). Recherches sur les genres Alternaria et Stemphylium. III. Action de la lumiere et des ultra-violets. Rev. mycol, 27, 1–16.

    Google Scholar 

  • Jones, J. B., Jones, J. P., Stall, R. E., & Zitter, T. A. (2014). Compendium of tomato diseases and pests. St. Paul: APS Press.

  • Kim, B. S., Yu, S. H., Cho, H. J., & Hwang, H. S. (2004). Gray leaf spot in peppers caused by Stemphylium solani and S. lycopersici. The Plant Pathology Journal, 20(2), 85–91.

    Article  Google Scholar 

  • Kurose, D., Hoang, L. H., Furuya, N., Takeshita, M., Sato, T., Tsushima, S., & Tsuchiya, K. (2014). Pathogenicity of Stemphylium lycopersici isolated from rotted tobacco seeds on seedlings and leaves. Journal of General Plant Pathology, 80(2), 147–152.

    Article  Google Scholar 

  • Kwon, J. H., Jeong, B. R., Yun, J. G., & Lee, S. W. (2007). Leaf spot of Kalanchoe (Kalanchoe blossfeldiana) caused by Stemphylium lycopersici. Research in Plant Disease, 13(2), 122–125.

    Article  Google Scholar 

  • Lamari, L. (2002). Assess 2.0: image analysis software for plant disease quantification. St Paul: APS Press.

    Google Scholar 

  • Leach, C. M., & Aragaki, M. (1970). Effects of temperature on conidium characteristics of Ulocladium chartarum and Stemphylium floridanum. Mycologia, 62(5), 1071–1076.

    Article  Google Scholar 

  • Malca, I., & Ullstrup, A. J. (1962). Effects of carbon and nitrogen nutrition on growth and sporulation of two species of Helminthosporium. Bulletin of the Torrey Botanical Club, 240–249.

  • McDonald, B. A., & Linde, C. (2002). Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology, 40(1), 349–379.

    Article  CAS  PubMed  Google Scholar 

  • Mehta, Y. R. (2001). Genetic diversity among isolates of Stemphylium solani from cotton. Fitopatologia Brasileira, 26(4), 703–709.

    Article  CAS  Google Scholar 

  • Mehta, Y. R., Mehta, A., & Rosato, Y. B. (2002). ERIC and REP-PCR banding patterns and sequence analysis of the internal transcribed spacer of rDNA of Stemphylium solani isolates from cotton. Current Microbiology, 44(5), 323–328.

    Article  CAS  PubMed  Google Scholar 

  • Nasehi, A., Kadir, J. B., Nasr-Esfahani, M., Abed-Ashtiani, F., Wong, M. Y., Rambe, S. K., & Golkhandan, E. (2014). Analysis of genetic and virulence variability of Stemphylium lycopersici associated with leaf spot of vegetable crops. European Journal of Plant Pathology, 140(2), 261–273.

    Article  CAS  Google Scholar 

  • Nasehi, A., Kadir, J., Nasr-Esfahani, M., Abed-Ashtiani, F., Golkhandan, E., & Ashkani, S. (2015). Identification of the new pathogen (Stemphylium lycopersici) causing leaf spot on Pepino (Solanum muricatum). Journal of Phytopathology. doi:10.1111/jph.12431.

  • Neergaard, P. (1945). Danish species of Alternaria and Stemphylium. Copenhagen: Einar Munksgaard.

    Google Scholar 

  • Nishi, N., Muta, T., Ito, Y., Nakamura, M., & Tsukiboshi, T. (2009). Ray speck of chrysanthemum caused by Stemphylium lycopersici in Japan. Journal of General Plant Pathology, 75(1), 80–82.

    Article  Google Scholar 

  • Ramallo, A. C., Hongn, S. I., Baino, O., Quipildor, L., & Ramallo, J. C. (2005). Stemphylium solani en tomate de invernadero en Tucumán, Argentina. Fitopatologia, 40(1), 17–22.

    Google Scholar 

  • Snyder, W. C., & Hansen, H. N. (1941). The effect of light on taxonomic characters in Fusarium. Mycologia, 33(6), 580–591.

    Article  Google Scholar 

  • Swofford, D. L. (2002). PAUP* version 4.0 b10, Phylogenetic analysis using parsimony (* and other methods). Sunderland: Sinauer.

    Google Scholar 

  • Sy-Ndir, M., Assigbetse, K. B., Nicole, M., Diop, T. A., & Ba, A. T. (2015). Differentiation of Stemphylium solani isolates using random amplified polymorphic DNA markers. African Journal of Microbiology Research, 9(13), 915–921.

    Article  CAS  Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10), 2731–2739.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tomato Genome Consortium. (2012). The tomato genome sequence provides insights into fleshy fruit evolution. Nature, 485(7400), 635–641.

    Article  Google Scholar 

  • Tomioka, K., & Sato, T. (2011). Fruit rot of sweet pepper caused by Stemphylium lycopersici in Japan. Journal of General Plant Pathology, 77(6), 342–344.

    Article  Google Scholar 

  • Tomioka, K., Sato, T., Sasaya, T., & Koganezawa, H. (1997). Leaf spot of kalanchoe caused by Stemphylium lycopersici. Annals of the Phytopathological Society of Japan, 63, 337–340.

    Article  Google Scholar 

  • Virtual Colour Systems LTD (2013) Virtual colour atlas. http://www.vcsconsulting.co.uk/VirtualAtlasSilverlight4.htm. Accessed 2016.

  • Weber, G. F. (1930). Gray leaf spot of tomato caused by Stemphylium solani, sp. nov. Phytopathology, 20(6), 513–518.

    Google Scholar 

  • White, T. J., Bruns, T., Lee, S. J. W. T., & Taylor, J. W. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Pcr Protocols: A Guide to Methods and Applications, 18(1), 315–322.

    Google Scholar 

  • Williams, C. N. (1959). Spore size in relation to culture conditions. Transactions of the British Mycological Society, 42(2), 213–222.

    Article  Google Scholar 

  • Zhu, Y., Pan, J., Qiu, J., & Guan, X. (2008). Optimization of nutritional requirements for mycelial growth and sporulation of entomogenous fungus Aschersonia aleyrodis webber. Brazilian Journal of Microbiology, 39(4), 770–775.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was partially supported by the Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT) of the Ministro de Ciencia, Tecnología e Innovación Productiva through the projects PICT 2012-2760 (Pedro Alberto Balatti) and PICT 2015-1620 (Mario Carlos Nazareno Saparrat).

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Authors and Affiliations

  1. Centro de Investigaciones de Fitopatología, Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata, (1900), La Plata, Buenos Aires, Argentina

    Mario Emilio Ernesto Franco, Silvina Marianela Yanil López, Gustavo Lucentini, Rocio Medina, Lía Blanca Ronco & Pedro Alberto Balatti

  2. Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina

    Mario Emilio Ernesto Franco, Silvina Marianela Yanil López, Rocio Medina & Mario Carlos Nazareno Saparrat

  3. Cátedra de Microbiología Agrícola, Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata, CC 327, (1900), La Plata, Buenos Aires, Argentina

    Maria Inés Troncozo, Mario Carlos Nazareno Saparrat, Lía Blanca Ronco & Pedro Alberto Balatti

  4. Comisión de Investigaciones Científicas de la Provincia de Buenos Aires, La Plata, Buenos Aires, Argentina

    Gustavo Lucentini & Pedro Alberto Balatti

  5. 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, (1900), La Plata, Buenos Aires, Argentina

    Mario Carlos Nazareno Saparrat

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  1. Mario Emilio Ernesto Franco
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  2. Maria Inés Troncozo
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Correspondence to Pedro Alberto Balatti.

Electronic supplementary material

ESM 1

Cultural characteristics of Stemphylium isolates. Pictures were taken from 7-day old cultures grown on homemade or commercial PDA at 25 °C in continuous darkness. (EPS 15464 kb)

ESM 2

Conidia of Stemphylium isolates CIDEFI-216, CIDEFI-217, CIDEFI-218 and CIDEFI-219. Pictures were taken from 7-day old cultures grown on homemade PDA at 25 °C in continuous darkness. Scale bar = 30 μm. (EPS 2033 kb)

ESM 3

One single most parsimonious tree of Stemphylium/Pleospora inferred from the concatenated ITS-gpd data set. Sequences of seven representatives of five genera of the order Pleosporales (Alternaria, Bipolaris, Cochliobolus, Pyrenophora and Setosphaeria) were chosen as outgroups. Sequences generated in this study are in bold type letter. Numbers at the nodes represents bootstrap support values as a percentage of 1000 replicates. The scale bar represents the number of nucleotide changes (steps). (EPS 103 kb)

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Franco, M.E.E., Troncozo, M.I., López, S.M.Y. et al. 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. Eur J Plant Pathol 149, 983–1000 (2017). https://doi.org/10.1007/s10658-017-1248-z

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