Abstract
Postbloom fruit drop (PFD) is caused by both Colletotrichum acutatum and C. gloeosporioides and is a potentially serious disease in citrus that occurs when flowering coincides with rainfall. The fungus incites necrotic lesions in petals and stigmas leading to premature fruit drop and reduced yield. The mechanisms of infection and survival of the causal agents remain to be fully elucidated. In the present study, we investigated the histopathology of PFD caused by C. acutatum in the petals and stigmas of sweet oranges using electron and light microscopy. In the petals, pathogen penetration occurred intra and intercellularly and also through the stomata, with intercellular penetration occurring most frequently. The distinct tissues of the petals were colonised, including the vascular system, particularly the xylem. Acervuli were observed on both sides of the petals. Although the fungus did not penetrate through the epidermal cells of the stigma, C. acutatum caused necrosis and an increase of phenolics in this tissue. A protective layer rich in lipophilic and phenolic compounds was formed under the necrotic area and crystals of oxalate were associated with the sites where the pathogen was present.
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Adaskaveg, J. E., & Förster, H. (2000). Occurrence and management of anthracnose epidemics caused by Colletotrichum species on tree fruit crops in California. In D. Prusky, S. Freeman, & M. B. Dickman (Eds.), Colletotrichum: Host specificity, pathology, and host-pathogen interaction (pp. 317–336). St. Paul: The American Phytopathological Society.
Bailey, J. A., O’Connel, R. J., Pring, T. J., & Nash, C. (1992). Infection strategies in Colletotrichum species. In M. J. Jeger & J. A. Bailey (Eds.), Colletotrichum: Biology, pathology and control (pp. 88–120). Wallingford: CAB.
Brown, G. E. (1975). Factors affecting postharvest development of Colletotrichum gloeosporioides in citrus fruits. Phytopathology, 65, 404–409.
Centis, S., Guillas, I., Séjalon, N., Esquerré-Tugayé, M., & Dumas, B. (1997). Endopolygalacturonase genes from Colletotrichum lindemuthianum: cloning of CLPG2 and comparison of its expression to that of CLPG1 during saprophytic and parasitic growth of the fungus. Molecular Plant-Microbe Interactions, 10, 769–775.
Chamberlain, C. J. (1932). Methods in plant histology. Chicago: The University of Chicago Press.
Cortelazzo, A. L., & Vidal, B. C. (1991). Soybean seed proteins: detection in situ and mobilization during germination. Revista Brasileira de Botânica, 14, 27–33.
Curry, K. J., Abril, M., Avant, J. B., & Smith, B. J. (2002). Strawberry anthracnose: histopatology of Colletotrichum acutatum and C. fragarie. Phytopathology, 10, 1055–1063.
De Goes, A., & Kupper, K. C. (2002). Controle das doenças causadas por fungos e bactérias na cultura dos citros. In L. Zambolim (Ed.), Manejo Integrado: Fruteiras Tropicais—Doencas e Pragas (pp. 353–412). Vicosa: Universidade Federal de Viçosa.
Feichtenberger, E., Bassanezi, R. B., Sposito, M. B., & Belasque, Jr., J. (2005). Doenças dos Citros (Citrus spp.). In H. Kimati, L. Amorim, J. A. M. Rezende, A. Bergamin Filho, & L. E. A. Camargo (Eds.), Manual de Fitopatologia: Doenças das Plantas Cultivadas. 4 ed. v. 2 (pp. 239–269). São Paulo: Editora Agronômica Ceres Ltda.
Ferreira, R. B., Monteiro, S., Freitas, R., Santos, C. N., Chen, Z., Batista, L. M., et al. (2007). The role of plant defence proteins in fungal pathogenesis. Molecular Plant Pathology, 8, 677–700.
Hammerschmidt, R. (2006). Hemibiotrophic growth: combining two forms of fungal parasitism. Physiological and Molecular Plant Pathology, 69, 1–2.
Horridge, G. A., & Tamm, S. L. (1969). Critical point drying for scanning electron microscopy study of ciliar motion. Science, 13, 817–818.
Jensen, W. A. (1962). Botanical histochemistry. San Francisco: W. H. Freeman.
Johansen, D. A. (1940). Plant microtechnique. New York: McGraw-Hill Book Company.
Karnovsky, M. J. (1965). A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. The Journal of Cell Biology, 27, 137–138.
Lima, W. G., Spósito, M. B., Amorim, L., Gonçalves, F. P., & De-Filho, P. A. M. (2011). Colletotrichum gloeosporioides, a new causal agent of citrus post-bloom fruit drop. European Journal of Plant Pathology, 131, 57–165.
McGovern, R. J., Seijo, T. E., Hendricks, K., & Roberts, P. D. (2012). New report of Colletotrichum gloeosporioides causing postbloom fruit drop on citrus in Bermuda. Canadian Journal of Plant Pathology. doi:10.1080/07060661.2012.670137.
Mendgen, K., & Hahn, M. (2002). Plant infection and the establishment of fungal biotrophy. Trends in Plant Science, 7, 352–356.
Mercer, P. C., Wood, R. K. S., & Greenwood, A. D. (1975). Ultrastructure of the parasitism of Phaseolus vulgaris by Colletotrichum lindemuthianum. Physiology Plant Pathology, 5, 203–314.
Milholland, R. D. (1982). Histopathology of strawberry infected with Colletotrichum fragariae. Phytopathology, 72, 1434–1439.
Nair, J., & Corbin, J. P. (1981). Histopathology of Pinus radiata seedlings infected by Colletotrichum acutatum f. sp. pinea. Phytopathology, 71, 777–783.
O’Connell, R. J., Bailey, J. A., & Richmond, D. V. (1985). Cytology and physiology of infection of Phaseolus vulgaris by Colletotrichum lindemuthianum. Physiology and Molecular Plant Pathology, 27, 75–98.
Pearse, A. G. E. (1968). Histochemistry, theoretical and applied, 3a ed. v. 1. London: Churchill.
Peres, N. A., Timmer, L. W., Adaskaveg, J. E., & Correll, J. C. (2005). Lifestyles of Colletotrichum acutatum. Plant Disease, 89, 784–796.
Perfect, S. E., Hughes, H. B., O’Connell, R. J., & Gren, J. R. (1999). Colletotrichum: a model genus for studies on pathology and fungal-plant interactions. Fungal Genetics and Biology, 27, 186–198.
Read, N. D., Kellock, L. J., Knight, H., & Trewavas, A. J. (1992). Contact sensing during infection by fungal pathogens. In J. A. Gallow & J. R. Green (Eds.), Perspective in plant cell recognition. Cambridge: Cambridge University Press.
Reynolds, E. S. (1963). The use of lead citrate at high pH as an electron-opaque stain for electron microscopy. The Journal of Cell Biology, 17, 208–212.
Sakai, W. S. (1973). Simple method for differential staining of paraffin embedded plant material using toluidine blue O. Stain Technology, 48, 247–249.
Staples, R. C., Hoch, H. C., Epstein, L., Laccetti, L., & Hassouna, S. (1985). Recognition of host morphology by rust: responses and mechanisms. Canadian Journal of Plant Pathology, 7, 314–322.
Timmer, L. W. (1993). Postbloom fruit drop of citrus - symptoms, disease cycle, and control. Proceedings of Florida State Horticultural Society, 106, 102–105.
Wharton, P., & Diéguez-Uribeondo, J. (2004). The biology of Colletotrichum acutatum. Annales del Jardín Botánico de Madrid, 61, 3–22.
Yakoby, N., Freeman, S., Dinoor, A., Keen, N. T., & Prusky, C. D. (2000). Expression of pectate lyase from Colletotrichum gloeosporioides in C. magna promotes pathogenicity. Molecular Plant-Microbe Interactions, 13, 887–891.
Zulfiqar, M., Brlansky, R. H., & Timmer, L. W. (1996). Infection of flower and vegetative tissues by Colletotrichum acutatum and C. gloeosporioides. Mycologia, 88, 121–128.
Acknowledgments
The would like to thank FAPESP for financial support (projects n° 2008/ 541764; 2009/00425-6), FUNDECITRUS for the use of laboratories, and the Electron Microscopy Centre of the UNESP Biosciences Institute (Botucatu) for microscopy support. The authors would also like to thank Denis Marin for technical assistance.
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Marques, J.P.R., Amorim, L., Spósito, M.B. et al. Histopathology of postbloom fruit drop caused by Colletotrichum acutatum in citrus flowers. Eur J Plant Pathol 135, 783–790 (2013). https://doi.org/10.1007/s10658-012-0120-4
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DOI: https://doi.org/10.1007/s10658-012-0120-4