Skip to main content

Brown spot of pear, an emerging disease in Argentina: identification and pathogenicity characterization of Argentinean Stemphylium vesicarium isolates

Abstract

Recently, a new plant disease was detected in the rural area of the High Valley of Río Negro, in Northern Patagonia, Argentina, called “Brown Spot of Pear” (BSP), caused by Stemphylium vesicarium (teleomorph: Pleospora herbarum, syn. Pantoea allii) in its sexual and asexual stages which produces lesions on leaves and fruits. BSP has been reported previously in pear growing areas of Europe and Japan where research studies have assessed the production of two host-specific toxins (HSTs) in culture filtrates of S. vesicarium (SV-I and SV-II toxin). The purpose of the present study was to characterize Stemphylium isolates from air and from brown spot lesions on pear leaves and fruits grown in this rural area, at a morphological, molecular and pathogenic level. The pathogen’s identity was determined as S. vesicarium and its aggressiveness and toxicity were demonstrated through conidia and culture filtrate bioassays showing different degrees of pathogenicity. D’Anjou and Abate Fetel were the most susceptible pear cultivars to S. vesicarium isolates.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  • Begerow, D., Nilsson, H., Unterseher, M., & Maier, W. (2010). Current state and perspectives of fungal DNA barcoding and rapid identification procedures. Applied Microbiology and Biotechnology, 87(1), 99–108.

    Article  CAS  PubMed  Google Scholar 

  • Belisario, A., Maccaroni, M., Corazza, L., Balmas, V., & Valier, A. (2002). Occurrence and etiology of brown apical necrosis on Persian (English) walnut fruit. Plant Disease, 86(6), 599–602.

    Article  CAS  PubMed  Google Scholar 

  • Carbone, I., & Kohn, L. M. (1999). A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia, 91(3), 553–556.

    Article  CAS  Google Scholar 

  • Cavanni, P., & Ponti, I. (1994). Maculatura bruna del pero: una micopatia sempre d’attualità. Riv Fruticultura, 12, 37–42.

    Google Scholar 

  • Coakley, S. M., Scherm, H., & Chakraborty, S. (1999). Climate change and plant disease management. Annual Review of Phytopathology, 37(1), 399–426.

    Article  CAS  PubMed  Google Scholar 

  • Di Masi, S. (2017). La mancha negra del peral afecta la region. Diario Río Negro. On line: http://www.rionegro.com.ar/la-mancha-negra-del-peral-afecta-la-region-YG2293441.

  • Dobra, A. C., Garcia, L. (2015). Presencia de mancha negra del peral, Stemphylium vesicarium, en el Valle Medio del Río Negro, Patagonia Argentina. - XXXVIII Congreso Argentino de Horticultura. Bahía Blanca. Buenos Aires. 05-08 de octubre - Página/s: 34(85):73.

  • Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5), 1792–1797.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elad, Y., & Pertot, I. (2014). Climate change impacts on plant pathogens and plant diseases. Journal of Crop Improvement, 28(1), 99–139.

    Article  CAS  Google Scholar 

  • Foster, J. M., Tayviah, C. S., Stricker, S. M., Gossen, B. D., & McDonald, M. R. (2019). Susceptibility to Stemphylium vesicarium of asparagus, onion, pear, and rye in Canada. Canadian Journal of Plant Pathology, 41(2), 228–241.

    Article  Google Scholar 

  • Graf, S., Bohlen-Janssen, H., Miessner, S., Wichura, A., & Stammler, G. (2016). Differentiation of Stemphylium vesicarium from Stemphylium botryosum as causal agent of the purple spot disease on asparagus in Germany. European Journal of Plant Pathology, 144(2), 411–418.

    Article  CAS  Google Scholar 

  • Greco, M., Kemppainen, M., Pose, G., & Pardo, A. (2015). Taxonomic characterization and secondary metabolite profiling of aspergillus section aspergillus contaminating feeds and feedstuffs. Toxins, 7(9), 3512–3537.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heijne, B., & Van Mourik, J. (2001). Zwartvruchtrot op peer neemt toe. Fruitteelt Den Haag, 91(8), 18–19.

    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, 102(32), 11390–11395.

    Article  CAS  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 

  • Köhl, J., Groenenboom-de Haas, B. H., Kastelein, P., Rossi, V., & Waalwijk, C. (2009). Quantitative detection of pear-pathogenic Stemphylium vesicarium in orchards. Phytopathology, 99(12), 1377–1386.

    Article  PubMed  Google Scholar 

  • Köppen, W. P. (1931). Grundis der Klimakunde. Walter de Gruyter & Co. p. 388

  • Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547–1549.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurose, D., Misawa, T., Suzui, T., Ichikawa, K., Kisaki, G., Hoang, L. H., & Sato, T. (2015). Taxonomic re-examination of several Japanese Stemphylium strains based on morphological and molecular phylogenetic analyses. Journal of General Plant Pathology, 81(5), 358–367.

    Article  Google Scholar 

  • Lenth, R., Singmann, H., Love, J., Buerkner, P., Herve, M. (2020). Emmeans: Estimated marginal means, aka least-squares means. R package version 1.5.0. On line: https://CRAN.R-project.org/package=emmeans.

  • Llorente, I., & Montesinos, E. (2006). Brown spot of pear: An emerging disease of economic importance in Europe. Plant Disease, 90(11), 1368–1375.

    Article  PubMed  Google Scholar 

  • Llorente, I., Moragrega, C., Ruz, L., Santamaría, G., Vilardell, A., Vilardell, P., & Montesinos, E. (2010). Basis for new strategies in integratred control of brown spot of pear (Stemphylium vesicarium, telemorpoh Pleospora allii). IOBC/WPRS Bulletin, 54, 35–39.

    Google Scholar 

  • Llorente, I., Moragrega, C., Ruz, L., & Montesinos, E. (2012). An update on control of brown spot of pear. Trees, 26(1), 239–245.

    Article  CAS  PubMed  Google Scholar 

  • McNeill, J., Barrie, F. R., Buck, W. R., Demoulin, V., Greuter, W., Hawksworth, D. L., Herendeen, P. S., Knapp, S., Marhold, K., Prado, W. F., Prud’homme van Reine, W. F., Smith, G. F., Wiersema, J. H., & Turland, N. J. (2012). International Code of Nomenclature for algae, fungi, and plants (Melbourne Code) adopted by the Eighteenth International Botanical Congress Melbourne, Australia, July 2011. Regnum Vegetabile 154. Koenigstein: Koeltz Scientific Books.

  • Montesinos, E., Moragrega, C., Llorente, I., & Vilardell, P. (1995). Susceptibility of selected European pear cultivars to infection by Stemphylium vesicarium and influence of leaf and fruit age. Plant Disease, 79(5), 471–473.

    Article  Google Scholar 

  • Moragrega, C., Puig, M., Ruz, L., Montesinos, E., & Llorente, I. (2018). Epidemiological features and trends of brown spot of pear disease based on the diversity of pathogen populations and climate change effects. Phytopathology, 108(2), 223–233.

    Article  PubMed  Google Scholar 

  • Moslemi, A., Ades, P. K., Groom, T., Nicolas, M. E., & Taylor, P. W. (2017). Alternaria infectoria and Stemphylium herbarum, two new pathogens of pyrethrum (Tanacetum cinerariifolium) in Australia. Australasian Plant Pathology, 46(1), 91–101.

    Article  Google Scholar 

  • Nördenstrom, G. H. (2006). El Cambio Climático en el Alto Valle. On line: http://www.redagraria.com/meteorologia/Alto%20Valle%20Clima.html.

  • Otani, H., Kohnobe, A., Kodama, M., & Kohmoto, K. (1998). Production of a host-specific toxin by germinating spores of Alternaria brassicicola. Physiological and Molecular Plant Pathology, 52(5), 285–295.

    Article  CAS  Google Scholar 

  • Pattori, E., Rossi, V., Bugiani, R., & Giosuè, S. (2006). Virulence of Stemphylium vesicarium isolates from pear and other host species. IOBC WPRS Bulletin, 29(1), 195.

    Google Scholar 

  • Pinheiro, J., & Bates, D. (2000). Mixed-effects models in S and S-PLUS. Springer (Statistics And Computing series).

    Book  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team. (2021). _nlme: Linear and nonlinear mixed effects Models_. R package version 3.1-152, URL: https://CRAN.R-project.org/package=nlme

  • Pitt, J. I., & Hocking, A. D. (2009). Fungi and food spoilage (Vol. 519, p. 388). Springer.

    Book  Google Scholar 

  • Polfliet, M. (2002). Aantasting Stemphylium neemt met het jaar toe [infection of Stemphylium increases every year]. Fruitteelt, 92(20), 16–17.

    Google Scholar 

  • Pose, G. (2007). Caracterización de hongos fitopatógenos toxicogénicos en productos frutihortícolas. El modelo Alternaria causante de enmohecimiento negro en tomates cultivados en Argentina. Tesis Doctoral. Universidad Nacional de Quilmes.

  • Puig, M., Ruz, L., Montesinos, E., Moragrega, C., & Llorente, I. (2015). Combined morphological and molecular approach for identification of Stemphylium vesicarium inoculum in pear orchards. Fungal Biology, 119(2–3), 136–144.

    Article  CAS  PubMed  Google Scholar 

  • R Core Team. (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing https://www.R-project.org/

    Google Scholar 

  • Rodriguez, A. B. (2013a). Análisis agroclimático 2012-2013. F&D N°70. On line: http://inta.gob.ar/sites/default/files/script-tmp-inta_agroclimatico_2012-2013.pdf.

  • Rodriguez, A. B. (2013b). Análisis Agroclimatológico ciclo 2012-2013. Boletin 11. On line: http://inta.gob.ar/sites/default/files/script-tmp-inta_boletin_clima_2012.pdf.

  • Rodriguez, A. B. (2014a). Precipitaciones acumuladas en la región. Información meteorológica de los días 2 al 8 de abril de 2014 en Alto Valle. On line: http://inta.gob.ar/noticias/precipitaciones-acumuladas-en-la-region.

  • Rodriguez, A. B. (2014b). Boletín Agrometeorológico N° 24 Análisis agrometeorológico Temporada 2013-2014. On line: http://inta.gob.ar/sites/default/files/script inta_boletin_agrometeorologico_n24_2013-2014.pdf

  • Rossi, V., Bugiani, R., Giosué, S., & Natali, P. (2005). Patterns of airborne conidia of Stemphylium vesicarium, the causal agent of brown spot disease of pears, in relation to weather conditions. Aerobiologia, 21(3–4), 203–216.

    Article  Google Scholar 

  • Samson, R., Hoekstra, E., Frisvad, J., & Filtenborg, O. (2000). Introduction to food- and airborne fungi (6th ed.). American Society for Microbiology.

    Google Scholar 

  • Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH image to ImageJ: 25 years of image analysis. Nature Methods, 9(7), 671–675.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schoch, C. L., Seifert, K. A., Huhndorf, S., Robert, V., Spouge, J. L., Levesque, C. A., & Fungal Barcoding Consortium. (2012). Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences, 109(16), 6241–6246.

    Article  CAS  Google Scholar 

  • Simmons, E. G. (1967). Typification of Alternaria, Stemphylium, and Ulocladium. Mycologia, 59(1), 67–92.

    Article  CAS  PubMed  Google Scholar 

  • Simmons, E. G. (1969). Perfect states of Stemphylium. Mycologia, 61(1), 1–26.

    Article  Google Scholar 

  • Simmons, E. G. (1985). Perfect states of Stemphylium II. Sydowia, 38, 284–293.

    Google Scholar 

  • Singh, P., Bugiani, R., Cavanni, P., Nakajima, H., Kodama, M., Otani, H., & Kohmoto, K. (1999). Purification and biological characterization of host-specific SV-toxins from Stemphylium vesicarium causing brown spot of European pear. Phytopathology, 89(10), 947–953.

    Article  CAS  PubMed  Google Scholar 

  • Singh, P., Park, P., Bugiani, R., Cavanni, P., Nakajima, H., Kodama, M., Otani, H., & Kohmoto, K. (2000). Effects of host-selective SV-toxin from Stemphylium vesicarium, the cause of Brown spot of European pear plants, on ultrastructure of leaf cells. Journal of Phytopathology, 148(2), 87–93.

    Article  CAS  Google Scholar 

  • Tanahashi, M., Minoguchi, C., Yokoyama, K., & Otani, H. (2008). The first report of brown spot of European pear caused by Stemphylium sp. in Niigata prefecture Japan. Japanese Journal of Phytopathology, 74, 183 (in Japanese).

    Google Scholar 

  • Tanahashi, M., Okuda, S., Miyazaki, E., Parada, R. Y., Ishihara, A., Otani, H., & Osaki-Oka, K. (2017). Production of host-selective SV-toxins by Stemphylium sp. causing brown spot of European pear in Japan. Journal of Phytopathology, 165(3), 189–194.

    Article  CAS  Google Scholar 

  • Temperini, C. V., Franchi, M. L., Rozo, M. E. B., Greco, M., Pardo, A. G., & Pose, G. N. (2019). Diversity and abundance of airborne fungal spores in a rural cold dry desert environment in Argentinean Patagonia. Science of the Total Environment, 665, 513–520.

    Article  CAS  PubMed  Google Scholar 

  • White, T. J., Bruns, T., Lee, S. J. W. T., & Taylor, J. (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 

  • Wickham, H. (2016). ggplot2: Elegant graphics for data analysis. Springer-Verlag New York. https://ggplot2-book.org/

  • Woudenberg, J. H. C., Hanse, B., Van Leeuwen, G. C. M., Groenewald, J. Z., & Crous, P. W. (2017). Stemphylium revisited. Studies in Mycology, 87, 77–103.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by the Universidad Nacional de Río Negro, Argentina and Universidad Nacional de Quilmes, Argentina. The authors also wish to thank researchers Kumiko Osaki-Oka y Roxana Parada Jaco from Tottori University (Japan) for their collaboration during this research.

Funding

This work was supported by Universidad Nacional de Río Negro [grant numbers PI 40-A-627]; Instituto Nacional de Tecnología Agropecuaria (INTA) and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Carolina Virginia Temperini.

Ethics declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Ethical statement

All authors are fully aware of this submission and have declared that they have no competing interests. The results presented in this manuscript did not involve any protected and/or endangered species, field studies, human participants, specimens or tissue samples or vertebrate animals, embryos or tissues.

Supplementary information

ESM 1

(DOCX 18 kb)

ESM 2

(DOCX 28 kb)

ESM 3

(DOCX 31 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Temperini, C.V., Tudela, M.A.A., Gimenez, G.N. et al. Brown spot of pear, an emerging disease in Argentina: identification and pathogenicity characterization of Argentinean Stemphylium vesicarium isolates. Eur J Plant Pathol 163, 529–544 (2022). https://doi.org/10.1007/s10658-022-02493-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-022-02493-y

Keywords

  • Brown spot of pear
  • Stemphylium vesicarium
  • SV-toxins
  • Emerging disease
  • Climate change