Skip to main content
SpringerLink
Log in

Study of infection process of five species of Colletotrichum comparing symptoms of glomerella leaf spot and bitter rot in two apple cultivars

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

Abstract

Bitter rot (BR) and glomerella leaf spot (GLS) occur in all the Brazilian South orchards with different species frequency per region. The main species found in Brazil belong to the Colletotrichum acutatum complex (Cac) and to the C. gloeosporioides complex (Cgc). The objectives of this study were to evaluate the favorable conditions for the germination and growth of five Colletotrichum species and, to compare pathogenicity and aggressiveness among species and between two apple cultivars in fruit, causing BR, and in leaves, causing GLS. The highest germination of conidia (above 90%) was achieved between 15 and 30 °C for Cgc species while for Cac species the highest germination (mean of 71%) was at 25 °C. The optimal temperature for mycelial growth did not differ between complexes and ranged from 23 to 27 °C. Althought, Cgc had a higher estimated maximum temperature then Cac. C. siamense cause BR symptoms regardless of cultivar or type of inoculation. C. nymphaeae and C. melonis caused symptoms in wounded and unwounded fruit but for C. paranaense and C. fructicola the symptoms were observed only in wounded fruit. Leaf symptoms of GLS was more severe in stressed leaves inoculated on the abaxial side compared to non-stressed leaves inoculated on the adaxial side. C. fructicola and C. nymphaeae were able to cause GLS symptoms in leaves with severity varying from 17.5 to 25% (cv. Gala). C. fructicola was the most severe causing GLS symptoms in cv. Gala (severity around 20.5%) and, in cv. Eva (severity around 11%). We discuss the roles that each species plays as a pathogen to better understand BR and GLS in different orchards conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alaniz, S., Hernandez, L., Damasco, D., & Mondino, P. (2012). First report of Colletotrichum acutatum and C. fragariae causing bitter rot of apple in Uruguay. Plant Disease, 96, 458.

    CAS  PubMed  Google Scholar 

  • Amorim, L., & Bergamin Filho, A. (2018). Epidemiologia: análises temporal e espacial. In Lilian Amorim, Jorge Alberto Marques Rezende, Armando Bergamin Filho. (Org.). Manual de Fitopatologia: Princípios e Conceitos. 5ed. Ouro Fino: Agronômica Ceres Ltda, v. 1, p. 520-530.

  • Araujo, L., Gonçalves, A. E., & Stadnik, M. J. (2014). Ulvan effect on conidial germination and appressoria formation of Colletotrichum gloeosporioides. Phytoparasitica, 42, 631–640.

    CAS  Google Scholar 

  • Baggio, J., Gonçalves, F. P., Lourenço, S. A., Tanaka, F. A. O., Pascholati, S. F., & Amorim, L. (2015). Direct penetration of Rhyzopus stolonifer into stone fruits causing Rhyzopus rot. Plant Pathology, 65, 633–642.

    Google Scholar 

  • Baroncelli, R., Sreenivasaprasad, S., Thon, M. R., & Sukno, S. A. (2014). First report of apple bitter rot caused by Colletotrichum godetiae in the United Kingdom. Plant Disease, 98, 1000.

    CAS  PubMed  Google Scholar 

  • Bassanezi, R. B., Amorim, L., Bergamin Filho, A., & Hau, B. (1998). Effects of bean line pattern mosaic virus on the monocyclic components of rust and angular leaf spot of Phaseolus bean at different temperatures. Plant Pathology, 47, 289–298.

    Google Scholar 

  • Becker, W. F., Katsurayama, Y., & Boneti, J. I. S. (2000). Mancha foliar da Gala: principal doença de verão da cultura da macieira. Agropecuária Catarinense, 13, 14–20.

    Google Scholar 

  • Bedendo, I. P., Amorim, L., & Mattos Junior, D. (2018). Ambiente e Doença. In: Lilian Amorim, Jorge Alberto Marques Rezende, Armando Bergamin Filho. (Org.). Manual de Fitopatologia: Princípios e Conceitos. 5ed. Ouro Fino: Agronômica Ceres Ltda, v. 1, p. 93-103.

  • Bentes, J. L. S., & Matsuoka, K. (2002). Histology of Colletotrichum guaranicola and Paullinia cupana var. sorbilis on resistant and susceptible clones. Fitopatologia Brasileira, 27, 71–77.

    Google Scholar 

  • Bragança, C. A. D., Damm, U., Baroncelli, R., Massola Júnior, N. S., & Crous, P. W. (2016). Species of the Colletotrichum acutatum complex associated with anthracnose diseases of fruit in Brazil. Fungal Biology, 120, 547–561.

    PubMed  Google Scholar 

  • Bringe, K., Schumacher, C. F. A., Schmitz-Eiberger, M., Steiner, U., & Oerke, E.-C. (2006). Ontogenetic variation in chemical and physical characteristics of adaxial apple leaf surfaces. Phytochemistry, 67, 161–170.

    CAS  PubMed  Google Scholar 

  • Cannon, P. F., Damm, U., Johnston, P. R., & Weir, B. S. (2012). Colletotrichum current status and future directions. Studies in Mycology, 73, 181–213.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Damm, U., Cannon, P. F., Woudenberg, J. H. C., & Crous, P. W. (2012). The Colletotrichum acutatum species complex. Studies in Mycology, 73, 37–113.

    CAS  PubMed  PubMed Central  Google Scholar 

  • De Silva, D. D., Crous, P. W., Ades, P. K., Hyde, K. D., & Taylor, P. W. J. (2017). Life styles of Colletotrichum species and implications for plant biosecurity. Fungal Biology Reviews, 31, 155–168.

    Google Scholar 

  • Denardi, F., Berton, O., & Spengler, M. M. (2003). Resistencia genética a podridão amarga em maçã determinadas pela taxa de desenvolvimento da doença em frutos com e sem ferimentos. Revista Brasileira de Fruticultura, 25, 494–497.

    Google Scholar 

  • Diéguez-Uribeondo, J., Förster, H., Soto-Estrada, A., & Adaskaveg, J. E. (2005). Subcuticular-intracellular hemibiotrophic and intercellular necrotrophic development of Colletotrichum acutatum on almond. Phytopathology, 95, 751–758.

    PubMed  Google Scholar 

  • Doyle, V. P., Oudemans, P. V., Rehner, S. A., & Litt, A. (2013). Habitat and host indicate lineage identity in Colletotrichum gloeosporioides from wild and agricultural landscapes in North America. PLoS One, 8, 62–94.

    Google Scholar 

  • Freeman, S., Katan, T., & Shabi, E. (1998). Characterization of Colletotrichum species responsible for anthracnose diseases of various fruits. Plant Disease, 82, 596–605.

    PubMed  Google Scholar 

  • Furlan, C. R. C., Mesquita Dantas, A. C., Denardi, F., Becker, W. F., & Mantovani, A. (2010). Resistência genética dos acessos do banco de germoplasma de macieira da epagri à mancha foliar de glomerella (Colletotrichum gloeosporioides). Revista Brasileira de Fruticultura, 32, 507–514.

    Google Scholar 

  • Gomes, S., Prieto, P., Martins-Lopes, P., Carvalho, T., Martin, A., & Guedes-Pinto, H. (2009). Development of Colletotrichum acutatum on tolerant and susceptible Olea europaea L. cultivars: A microscopic analysis. Mycopathologia, 168, 203–211.

    PubMed  Google Scholar 

  • Gonzalez, E., & Sutton, T. B. (1999). First report of Glomerella leaf spot (Glomerella cingulata) of apple in the United States. Plant Disease, 83, 1074–1074.

    CAS  PubMed  Google Scholar 

  • Gonzalez, E., Sutton, T. B., & Correl, J. C. (2006). Clarification of the etiology of Glomerella leaf spot and bitter rot of apple caused by Colletotrichum spp. based on morphology and genetic, molecular and pathogenicity tests. Phytopathology, 96, 982–992.

    CAS  PubMed  Google Scholar 

  • Grahovac, M., Indic, D., Vukovic, S., Hrust, J., Gvozdenac, S., Mihajlovic, M., & Tanovi, B. (2012). Morphological and ecological features as differentiation criteria for Colletotrichum species. Zemdirbyste-Agriculture, 99, 189–195.

    Google Scholar 

  • Hamada, N. A., Moreira, R. R., Gomes Figueiredo, J. A., & May De Mio, L. L. (2020). Colletotrichum acutatum complex isolated from apple flowers can cause bitter rot and glomerella leaf spot. Bragantia, 79, 399–406.

    Google Scholar 

  • Jain, S., & Kumar, A. (2015). The pathogenesis related class 10 proteins in plant defense against biotic and abiotic stresses. Advanced Plants Agricultural Research, 2, 305–314.

    Google Scholar 

  • Jingjing, J., Hongyan, Z., Huannan, L., Zhenhua, W., Yongsen, C., Ni, H., Guoping, W., Gilbert, N., & Wenxing, X. (2014). Identification and characterization of Colletotrichum fructicola causing black spots on young fruits related to bitter rot of pear (Pyrus bretschneideri Rehd.) in China. Crop Protection, 58, 41–48.

    Google Scholar 

  • Karnovsky, M. J. (1965). A formaldehyde–glutaraldehyde fixative of high osmolality for use in electron microscopy. The Journal Cell Biology, 27, 137–138.

    Google Scholar 

  • Katsurayama, Y., & Boneti J. I. S. (2009). Manejo das doenças de verão da macieira no sul do Brasil. In: Stadnik, M. J. Manejo integrado de doenças da macieira. Florianópolis-SC: Federal University of Santa Catarina, p. 45–64.

  • Katsurayama, Y., & Boneti, J. I. S. (2010). Model for forecasting the leaf spot disease in apple trees based on temperature and leaf wetness duration. Agropecuária Catarinense, 23, 82–84.

    Google Scholar 

  • Kim, K. W. (2008). Vapor fixation of intractable fungal cells for simple and versatile scanning electron microscopy. Journal of Phytopathology, 156, 125–128.

    Google Scholar 

  • Kou, L., Verneta, G., Luo, Y., & Jurick, W. (2014). First report of Colletotrichum fioriniae causing postharvest decay on ‘Nittany’ apple fruit in the United States. Plant Disease, 98, 993.

    CAS  PubMed  Google Scholar 

  • Kowata, L. S., Strapasson, M., Challiol, M. A., & May De Mio, L. L. (2010). Glomerella leaf spot in apple: Validation of proposed diagrammatic scale and efficiency of fungicides. Ciência Rural, 40, 1502–1508.

    CAS  Google Scholar 

  • Lakshmi, B. K. M., Reddy, P. N., & Prasad, R. D. (2011). Cross-infection potential of Colletotrichum gloeosporioides Penz. isolates causing anthracnose in subtropical fruit crops. Tropical Agricultural Research, 22, 183–193.

    Google Scholar 

  • Leite, R. P., Tsuneta, M., & Kishino, A. Y. (1988). Ocorrência de mancha foliar de Glomerella em maicieira no estado do Paraná. Fundação Institito Agronômico do Paraná. Informe de Pesquisa, 81p.

  • Liao, C. Y., Chen, M. Y., Chen, Y. K., Wang, T. C., Sheu, Z. M., Kuo, K. C., Chang, P. F. L., Chung, K. R., & Lee, M. H. (2012). Characterization of three Colletotrichum acutatum isolates from Capsicum spp. European Journal of Plant Pathology, 133, 599–608.

    Google Scholar 

  • Liu, J. J., & Ekramoddoullah, A. K. M. (2006). The family 10 of plant pathogenesis-related proteins: Their structure, regulation, and function in response to biotic and abiotic stresses. Physiological and Molecular Plant Pathology, 68, 3–13.

    CAS  Google Scholar 

  • Liu, G., Kennedy, R., Greenshields, D. L., Peng, G., Forseille, L., Selvaraj, G., & Wei, Y. (2007). Detached and attached arabidopsis leaf assays reveal distinctive defense responses against hemibiotrophic Colletotrichum spp. Molecular Plant-Microbe Interactions, 20, 1308–1319.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Mendgen, K., & Hahn, M. (2002). Plant infection and the establishment of fungal biotrophy: Review. Trends in Plant Science, 10, 1–5.

    Google Scholar 

  • Moreira, R. R., Peres, N. A., & May De Mio, L. L. (2019). Colletotrichum acutatum and C. gloeosporioides species complex associated with apple in Brazil. Plant Disease, 103, 268–275.

    CAS  PubMed  Google Scholar 

  • Moreira, R. R., Araldi, G. S., & May De Mio, L. L. (2020). Colletotrichum acutatum complex causing anthracnose on peach in Brazil. Australasian Plant Pathology, 49, 179–189.

    CAS  Google Scholar 

  • Munir, M., Amsden, B., Dixon, E., Vaillancourt, L., & Ward Gauthier, N. A. (2016). Characterization of Colletotrichum species causing bitter rot of apples in Kentucky orchards. Plant Disease, 100, 2194–2203.

    CAS  PubMed  Google Scholar 

  • O’Brien, T. P., & Mc Cully, M. E. (1981). The study of plant structure principles and select methods (45p). Melbourne: Termarcrphi Pty.

    Google Scholar 

  • Peres, N. A., Timmer, L. W., Adaskaveg, J. E., & Correll, J. C. (2005). Lifestyles of Colletotrichum acutatum. Plant Disease, 89, 784–796.

    CAS  PubMed  Google Scholar 

  • Petri, J. L., Leite, G. B., Couto, M., & Francescatto, P. (2011). Avanços na cultura da macieira no Brasil (pp. 48–56). Special Issue: Revista Brasileira de Fruticultura.

    Google Scholar 

  • Phoulivong, S., McKenzie, E. H. C., & Hyde, K. D. (2012). Cross infection of Colletotrichum species; a case study with tropical fruits. Current Research in Environmental & Applied Mycology, 2, 99–111.

    Google Scholar 

  • Prabhpreet, I., Dhillon, M., Singh, P. P., & Inder, P. (2000). Mesophyll characteristics of muskmelon leaf in relation to resistance/susceptibility to downy mildew. Plant Disease Research, 15, 18–23.

    Google Scholar 

  • Raetano, C. G., & Bauer, F. C. (2000). Effect of the air speed in air-assisted sprayer on bean crop pesticide. Bragantia, 62, 329–334.

    Google Scholar 

  • Rockenbach, M. F., Boneti, J. I., Cangahuala-Inocente, G. C., Gavioli-Nascimento, M. C. A., & Guerra, M. P. (2015). Histological and proteomics analysis of apple defense responses to the development of Colletotrichum gloeosporioides on leaves. Physiological and Molecular Plant Pathology, 89, 97–107.

    CAS  Google Scholar 

  • Santos, A. F., Matsuoka, K., Maffia, L. A., & Alfenas, A. C. (1999). Importância da estrutura da superfície foliar ima interação Phytophthora capsici - Hevea brasiliensis. Boletim de Pesquisa Florestal, 39, 67–80.

    Google Scholar 

  • Sutton, T. B., & Sanhueza, R. M. V. (1998). Necrotic leaf blotch of Golden delicious e Glomerella leaf spot: A resolution of common names. Plant Disease, 82, 267–268.

    PubMed  Google Scholar 

  • Sutton, T. B., & Shane, W. W. (1983). Epidemiology of the perfect stage of Glomerella cingulata on apples. Phytopathology, 73, 1179–1183.

    Google Scholar 

  • Sutton, B.C., Bailey, J.A., & Jeger, M.J. (1992). The genus Glomerella and its anamorph Colletotrichum. In: J.A. Bayley, M.J. Jeger (Eds.), Colletotrichum: Biology, pathology and control (pp. 1-26). Wallingford:CABI.

  • Taylor, J. (1971). A necrotic leaf blotch and fruit rot of apple caused by a strain of Glomerella cingulata. Phytopathology, 61, 221–224.

    Google Scholar 

  • Timmer, L. W., & Agostini, J. P. (1994). Population dynamics and survival of strains of Colletotrichum gloeosporioides on citrus in Florida. Phytopathology, 84, 420–425.

    Google Scholar 

  • Velho, A. C., Alaniz, S., Casanova, L., Mondino, P., & Stadnik, M. J. (2015). New insights into the characterization of Colletotrichum species associated with apple diseases in southern Brazil and Uruguay. Fungal Biology, 119, 229–244.

    PubMed  Google Scholar 

  • Velho, A. C., Mondino, P., & Stadnik, M. J. (2018). Extracellular enzymes of Colletotrichum fructicola isolates associated to apple bitter rot and Glomerella leaf spot. Mycology, 9, 145–154.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weir, B. S., Johnston, P. R., & Damm, U. (2012). The Colletotrichum gloeosporioides species complex. Studies in Mycology, 73, 115–180.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wharton, P. S., & Dieguez-Uribeondo, J. (2004). The biology of Colletotrichum acutatum. Anales del Jardin Botánico de Madrid, 61, 3–22.

    Google Scholar 

  • Wharton, P. S., Julian, A. M., & O’Connell, R. J. (2001). Ultrastructure of the infection of Sorghum bicolor by Colletotrichum sublineolum. Phytopathology, 91, 149–158.

    CAS  PubMed  Google Scholar 

  • Zanão Junior, L. A. (2007). Resistência do arroz à mancha-parda mediada por Silício e Manganês. Viçosa:Federal University of Viçosa, Master thesis.

  • Ziadi, S., Poupard, P., Brisset, M. N., Paulin, J. P., & Simoneau, P. (2001). Characterization in apple leaves of two subclasses of PR-10 transcripts inducible by acibenzolar-S-methyl, a functional analogue of salicylic acid. Physiological and Molecular Plant Pathology, 59, 33–43.

    CAS  Google Scholar 

Download references

Acknowledgments

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001, Fundação Araucária (FA), by Conselho Nacional de desenvolvimento Científico e tecnológico (CNPq), and by Casadinho/Procad - Chamada Pública MCT/CNPq/MEC/CAPES - Ação Transversal n°06/2011. Grant numbers: 483566/2013-6, 552334/2011-1, and 552334/2011-1. The authors would also like to thank Professor Dr. Nelson Sidnei Massola Junior, coordinator of the Phytopathogenic Fungi Laboratory of the Escola Superior de Agricultura Luiz de Queiros (ESALQ/USP), for providing the isolates used in this study.

Author information

Authors and Affiliations

  1. Department of Plant Protection/SCA-UFPR, Curitiba, Paraná, CEP 81531-980, Brazil

    Rafaele Regina Moreira, Erica Camila Zielinski, Camilla Castellar & Louise Larissa May De Mio

  2. Department of Plant Pathology/ESALQ-USP, Piracicaba, São Paulo, CEP 13418-900, Brazil

    Armando Bergamin Filho

Authors
  1. Rafaele Regina Moreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Erica Camila Zielinski
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Camilla Castellar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Armando Bergamin Filho
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Louise Larissa May De Mio
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rafaele Regina Moreira.

Ethics declarations

We declare that our manuscript complies to the all ethical rules applicable for this journal and that there are no potential conflicts of interest or even research involving human participants and/or animals.

Electronic supplementary material

ESM 1

(DOCX 13 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moreira, R.R., Zielinski, E.C., Castellar, C. et al. Study of infection process of five species of Colletotrichum comparing symptoms of glomerella leaf spot and bitter rot in two apple cultivars. Eur J Plant Pathol 159, 37–53 (2021). https://doi.org/10.1007/s10658-020-02138-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-020-02138-y

Keywords

Search

Navigation