Abstract
Infection of Malus x domestica cv. Royal Gala fruit by Colletotrichum acutatum causing bitter rot was studied in the temperate climate of New Zealand. Temperatures above 15 °C were required for lesions to develop on detached apple wound-inoculated or inoculated without wounding with C. acutatum spores, regardless of maturity. A wetness period of 72 h was required for infection of mature detached apple fruit without wounding. On wound-inoculated detached apple fruits, sporulation was related to temperature and followed a similar pattern. In the field, a mean temperature above 15 °C for 72 h after wound-inoculation was required for lesions to develop. Buds were a more important source of inoculum than twigs, and it was shown that C. acutatum could be isolated more frequently from outer bud scales than from inner scales. Asymptomatic infection of vegetative and reproductive buds was detected. C. acutatum was detected on asymptomic surface-sterilised petals and fruit, more commonly during summer than spring. Symptomless sterilised leaves generally yielded C. acutatum throughout the season, but isolations were more frequent in summer. Recovery of inoculum using a splash meter to detect vertical dispersal showed that in summer inoculum was primarily splashed up from the ground. In spring, inoculum was recovered in similar quantities from all heights up to a metre, suggesting that splash dispersal occurs from the canopy as well as from the ground. A disease cycle for C. acutatum infecting apples and causing bitter rot in New Zealand is suggested.
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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, 458–458.
Anonymous. (2009). The Southeast Regional Climate Center. Retrieved 18 November, 2009, from The University of North Carolina.: http://www.sercc.com/cgi-bin/sercc/cliMAIN.pl?sc0165
Atkinson, J. D. (1971). Diseases of fruit trees in New Zealand. (Department of Scientific and Industrial Research: Auckland).
Bannon, F. J., & Cooke, B. M. (1998). Studies on dispersal of Septoria tritici pycnidiospores in wheat-clover intercrops. Plant Pathology, 47, 49–56.
Biggs, A. R. (1995). Detection of latent infections in apple fruit with paraquat. Plant Disease, 79, 1062–1067.
Biggs, A. R., & Miller, S. S. (2001). Relative susceptibility of selected apple cultivars to Colletotrichum acutatum. Plant Disease, 85, 657–660.
Boateng, K., & Lewis, K. J. (2015). Spore dispersal by Dothistroma septosporum in Northwest British Columbia. Phytopathology, 105, 69–79.
Børve, J., & Stensvand, A. (2006). Colletotrichum acutatum overwinters on sweet cherry buds. Plant Disease, 90, 1452–1456.
Børve, J. & Stensvand, A. (2007). Colletotrichum acutatum found on apple buds in Norway. Health Progress: https://doi.org/10.1094/PHP-2007-0522-01-RS.
Børve, J., & Stensvand, A. (2013a). Colletotrichum acutatum can establish on sweet and sour cherry trees throughout the growing season. European Journal of Horticultural Science, 78, 258–266.
Børve, J., & Stensvand, A. (2013b). Incidence of Colletotrichum acutatum on apple fruits and possible sources of inoculum. IOBC/WPRS Bulletin, 91, 385–388.
Børve, J., & Stensvand, A. (2015). Colletotrichum acutatum on apple in Norway. IOBC/WPRS Bulletin, 110, 151–157.
Børve, J., & Stensvand, A. (2017). Colletotrichum acutatum occurs asymptomatically on apple leaves. European Journal of Plant Pathology, 147, 943–948.
Børve, J., Roen, D., & Stensvand, A. (2013). Harvest time influences incidence of storage diseases and fruit quality in organically grown 'Aroma' apples. European Journal of Horticultural Science, 78, 232–238.
Boudreau, M. A., & Madden, L. V. (1995). Effect of strawberry density on dispersal of Colletotrichum acutatum by simulated rain. Phytopathology, 85, 934–941.
Boyd-Wilson, K. S. H., Butler, R. C., Alspach, P. A., Everett, K. R., Pushparajah, I. P. S., & Walter, M. (2014). Compounds alone and in combination with yeasts to control Colletotrichum acutatum in apples. Australasian Plant Pathology, 43, 703–714.
Braganca, C. A. D., Damm, U., Baroncelli, R., Massola, 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.
Brook, P. J. (1957). Ripe spot of apples in New Zealand. New Zealand Journal of Science and Technology, A38, 735–741.
Brook, P. J. (1959). Experiments on the control of ripe spot on Sturmer apples. New Zealand Journal of Agricultural Research, 2, 463–474.
Brook, P. J. (1972). The apple bitter rot epidemic in Auckland. Orchardist of New Zealand, 45(238), 241.
Brook, P. J. (1977). Glomerella cingulata and bitter rot of apple. New Zealand Journal of Agricultural Research, 20, 547–555.
Campbell, C. L., & Madden, L. V. (1990). Introduction to plant disease epidemiology. New York: Wiley.
Cannon, P. F., Damm, U., Johnston, P. R., & Weir, B. S. (2012). Colletotrichum - current status and future directions. Studies in Mycology, 73, 181–213.
Crusius, L. U., Forcelini, C. A., Sanhueza, R. M. V., & Fernandes, J. M. C. (2002). Epidemiology of apple leaf spot. Fitopatologia Brasileira, 27, 65–70.
Damm, U., Cannon, P. F., Woudenberg, J. H. C., & Crous, P. W. (2012). The Colletotrichum acutatum species complex. Studies in Mycology, 73, 37–113.
Dieguez-Uribeondo, J., Forster, H., Soto-Estrada, A., & Adaskaveg, J. E. (2005). Subcuticular-intracellular hemibiotrophic and intercellular necrotrophic development of Colletotrichum acutatum on almond. Phytopathology, 95, 751–758.
Dyko, B. J. & Mordue, J. E. M. (1979). Colletotrichum acutatum. CMI Descriptions of Pathogenic Fungi and Bacteria (2 pp.)
Eastburn, D. M., & Gubler, W. D. (1990). Strawberry anthracnose: Detection and survival of Colletotrichum acutatum in soil. Plant Disease, 74, 161–163.
Everett, K. R. (2003). The effect of low temperatures on Colletotrichum acutatum and Colletotrichum gloeosporioides, fungi causing body rots of avocado in New Zealand. Australasian Plant Pathology, 32, 441–448.
Everett, K. R. (2014). Anthracnose and stem-end rots of tropical and subtropical fruit- new names for old foes. In D. Prusky & M. L. Gullino (Eds.), Plant pathology in the 21st Century, ICPP 2013 Postharvest Pathology (Vol. 7, pp. 55–70). Switzerland: Springer International Publishing.
Everett, K. R., Timudo-Torrevilla, O. E., Pushparajah, I. P. S., Scheper, R. W. A., Shaw, P. W., Spiers, T. M., Ah Chee, A., Taylor, J. T., Wood, P., Wallis, D. R. & Manning, M. A. (2009). Criteria for infection of apples by Colletotrichum acutatum causing summer rots. The Orchardist, August, 24–27.
Everett, K. R., Timudo-Torrevilla, O. E., Pushparajah, I. P. S., Scheper, R. W. A., Shaw, P. W., Spiers, T. M., Ah Chee, A., Taylor, J. T., Wood, P., Wallis, D. R. & Manning, M. A. (2010). Inoculum sources for Colletotrichum acutatum causing summer rot of apple. The Orchardist, March, 18–22.
Everett, K. R., Pushparajah, I. P. S., Taylor, J. T., Timudo-Torrevilla, O. E., Spiers, T. M., Ah Chee, A., Shaw, P. W., & Wallis, D. R. (2015). Evaluation of fungicides for control of bitter and sprinkler rots on apple fruit. New Zealand Plant Protection, 68, 264–274.
Estrada, A. B., Dodd, J. C., & Jeffries, P. (2000). Effect of humidity and temperature on conidial germination and appressorium development of two Philippine isolates of the mango anthracnose pathogen Colletotrichum gloeosporioides. Plant Pathology, 49, 608–618.
Fernando, T. H. P. S., Jayasinghe, C. K., & Wijesundera, R. L. C. (2000). Factors affecting spore production, germination and viability of Colletotrichum acutatum isolates from Hevea brasiliensis. Mycological Research, 104, 681–685.
Fitzell, R. D., & Peak, C. M. (1984). The epidemiology of anthracnose disease of mango: Inoculum sources, spore production and dispersal. Annals of Applied Biology, 104, 53–59.
Forster, K., & Adaskaveg, J. E. (1999). Identification of subpopulations of Colletotrichum acutatum and epidemiology of almond anthracnose in California. Phytopathology, 89, 1056–1065.
Gonzalez-Dominguez, E., Rossi, V., Michereff, S. J., Garcia-Jimenez, J., & Armengol, J. (2014). Dispersal of conidia of Fusicladium eriobotryae and spatial patterns of scab in loquat orchards in Spain. European Journal of Plant Pathology, 139, 849–861. https://doi.org/10.1007/s10658-014-0439-0.
Gregory, P. H., Guthrie, E. J., & Bunce, M. E. (1959). Experiments on splash dispersal of fungus spores. Journal of General Microbiology, 20, 328–354.
Hampson, C. R., & Kemp, H. (2003). Characteristics of important commercial apple cultivars. In D. C. Ferree & I. J. Warrington (Eds.), Apples, Botany, production and uses (pp. 61–89). Wallingford: CABI Publishing.
Ivic, D., Voncina, D., Sever, Z., Simon, S., & Pejic, I. (2013). Identification of Colletotrichum species causing bitter rot of apple and pear in Croatia. Journal of Phytopathology, 161, 284–286.
Johnston, P. R., & Jones, D. (1997). Relationships among Colletotrichum isolates from fruit-rots assessed using rDNA sequences. Mycologia, 89, 420–430.
Johnston, P. R., Pennycook, S. R., & Manning, M. A. (2005). Taxonomy of fruit-rotting fungal pathogens: what's really out there? New Zealand Plant Protection, 58, 42–46.
Jones, A. L., Ehret, G. R., Meyer, M. P., & Shane, W. W. (1996). Occurrence of bitter rot on apple in Michigan. Plant Disease, 80, 1294–1297.
King, W. T., Madden, L. V., Ellis, M. A., & Wilson, L. L. (1997). Effects of temperature on sporulation and latent period of Colletotrichum spp. infecting strawberry fruit. Plant Disease, 81, 77–84.
Lamari, L. (2002). Assess Image Analysis Software for Plant Disease Quantification. St. Paul: The American Phytopathological Society.
Landsberg, J. J., Butler, D. R., & Thorpe, M. R. (1974). Apple bud and blossom temperatures. Journal of Horticultural Science, 49, 227–239.
Leandro, L. F. S., Gleason, M. L., Nutter, F. W., Wegulo, S. N., & Dixon, P. A. (2003). Influence of temperature and wetness duration on conidia and appressoria of Colletotrichum acutatum on symptomless strawberry leaves. Phytopathology, 93, 513–520.
Madden, L. V. (1993). Aggregation of Colletotrichum acutatum in response to simulated rain episodes. Journal of Phytopathology, 138, 145–156.
Madden, L. V., Wilson, L. L., Yang, X., & Ellis, M. A. (1992). Splash dispersal of Colletotrichum acutatum and Phytophthora cactorum by short-duration simulated rains. Plant Pathology, 41, 427–436.
Mari, M., Guidarelli, M., Martini, C., & Spadoni, A. (2012). First report of Colletotrichum acutatum causing bitter rot on apple in Italy. Plant Disease, 96, 144–144.
McCartney, H. A., & Fitt, B. D. L. (1985). Construction of dispersal models. In C. A. Gilligan (Ed.), Advances in Plant Pathology Volume 3 Mathematical modelling of crop disease (Vol. 3, pp. 107–143). London: Academic Press Inc..
McKay, S. F., Shtienberg, D., Sedgley, M., & Scott, E. S. (2014). Anthracnose on almond in Australia: Disease progress and inoculum sources of Colletotrichum acutatum. European Journal of Plant Pathology, 139, 773–783.
Milholland, R. D. (1995). Anthracnose fruit rot (ripe rot). In F. L. Caruso & D. C. Ramsdell (Eds.), Compendium of Blueberry and Cranberry Diseases (p. 17). St. Paul: American Phytopathological Society.
Miles, T. D., Gillett, J. M., Jarosz, A. M., & Schilder, A. M. C. (2013). The effect of environmental factors on infection of blueberry fruit by Colletotrichum acutatum. Plant Pathology, 62, 1238–1247.
Moral, J., Jurado-Bello, J., Isabel Sanchez, M., de Oliveira, R., & Trapero, A. (2012). Effect of temperature, wetness duration, and planting density on olive anthracnose caused by Colletotrichum spp. Phytopathology, 102, 974–981.
Moraes, S. R. G., Escanferla, M. E., & Massola Junior, N. S. (2015). Prepenetration and penetration of Colletotrichum gloeosporioides into guava fruit (Psidium guajava L.): Effects of temperature, wetness period and fruit age. Journal of Phytopathology, 163, 149–159.
Munir, M., Amsden, B., Dixon, E., Vaillancourt, L., & Gauthier, N. A. W. (2016). Characterization of Colletotrichum species causing bitter rot of apple in Kentucky orchards. Plant Disease, 100, 2194–2203.
Nair, J., Newhook, F. J., & Corbin, J. B. (1983). Survival of Colletotrichum acutatum f.sp. pinea in soil and pine debris. Transactions of the British Mycological Society, 81, 53–63.
Noe, J. P., & Starkey, T. E. (1982). Relationship of apple fruit maturity and inoculum concentration to infection by Glomerella cingulata. Plant Disease, 66, 379–381.
Norman, D. J., & Strandberg, J. O. (1997). Survival of Colletotrichum acutatum in soil and plant debris of leatherleaf fern. Plant Disease, 81, 1177–1180.
Ntahimpera, N., Hacker, J. K., Wilson, L. L., Hall, F. R., & Madden, L. V. (1999). Characterization of splash droplets from different surfaces with a phase doppler particle analyzer. Agricultural and Forest Meteorology, 97, 9–19.
NZMS (1980). Summaries of climatological observations to 1980 New Zealand Meteorological Service Miscellaneous Publication, 177.
Pennycook, S. R. (1989). Plant diseases recorded in New Zealand. Auckland: Plant Diseases Division, DSIR.
Peres, N. A. R., Kim, S., Beck, H. W., Souza, N. L., & Timmer, L. W. (2002). A fungicide application decision (FAD) support system for postbloom fruit drop of citrus (PFD). Plant Health Progress. https://doi.org/10.1094/PHP-2002-0731-01-RV.
Peres, N. A. R., Souza, N. L., Furtado, E. L., & Timmer, L. W. (2004). Evaluation of systems for timing of fungicide sprays for control of postbloom fruit drop of citrus in Brazil. Plant Disease, 88, 731–735.
Peres, N. A., Timmer, L. W., Adaskaveg, J. E., & Correll, J. C. (2005). Lifestyles of Colletotrichum acutatum. Plant Disease, 89, 784–796.
Petrini, O. (1986). Taxonomy of endophytic fungi in aerial plant tissues. In N. J. Fokkema & J. van den Heuvel (Eds.), Microbiology of the phyllosphere (pp. 175–187). Cambridge: Cambridge University Press.
Reid, M. S., Padfield, C. A. S., Watkins, C. B., & Harman, J. E. (1982). Starch iodine pattern as a maturity index for Granny Smith apples. New Zealand Journal of Agricultural Research, 25, 229–237.
Roger, C., & Tivoli, B. (1996). Spatio-temporal development of pycnidia and perithecia and dissemination of spores of Mycosphaerella pinodes on pea (Pisum sativum). Plant Pathology, 45, 518–528.
Shane, W. W., & Sutton, T. B. (1981). Germination, appressorium formation, and infection of immature and mature apple fruit by Glomerella cingulata. Phytopathology, 71, 454–457.
Shaw, M. W. (1987). Assessment of upward movement of rain splash using a fluorescent tracer method and its application to the epidemiology of cereal pathogens. Plant Pathology, 36, 201–213.
Shi, Y., Correll, J. C., Guerber, J. C., & Rom, C. R. (1996). Frequency of Colletotrichum species causing bitter rot of apple in the southeastern United States. Plant Disease, 80, 692–696.
Stensvand, A., & Børve, J. (2010). Sources of inoculum for Colletotrichum acutatum in cherry and apple. IOBC/WPRS Bulletin, 54, 65–67.
Stensvand, A., Talgø, V., Strømeng, G. M., Aamot, H. U., Børve, J., Sletten, A., & Klemsdal, S. (2006). Colletotrichum acutatum in Norwegian strawberry production and sources of potential inoculum in and around strawberry fields. Bulletin OILB/SROP, 29, 87–91.
Stensvand, A., Børve, J., & Talgo, V. (2017). Overwintering diseased plant parts and newly infected flowers and fruit as sources of inoculum for Colletotrichum acutatum in sour cherry. Plant Disease, 101, 1207–1213.
Sugar, D. (2014). Side rot. In T. B. Sutton, H. S. Aldwinckle, A. M. Agnello, & J. F. Walgenbach (Eds.), Compendium of apple and pear diseases and pests (Second Edition, pp. 81–82). St. Paul: The American Phytopathological Society.
Sundelin, T., Stromeng, G. M., Gjaerum, H. B., Amby, D. B., Orstad, K., Jensen, B., Lund, O. S., & Stensvand, A. (2015). A revision of the history of the Colletotrichum acutatum species complex in the Nordic countries based on herbarium specimens. FEMS Microbiology Letters, 362, 1–7.
Sutton, T. B. (1990). Bitter rot. In A. L. Jones & H. S. Aldwinckle (Eds.), Compendium of Apple and Pear Diseases. St. Paul: American Phytopathological Society.
Sutton, T. B. (2014). Bitter rot. In T. B. Sutton, H. S. Aldwinckle, A. M. Agnello, & J. F. Walgenbach (Eds.), Compendium of apple and pear diseases and pests (Second Edition, pp. 20–21). St. Paul: The American Phytopathological Society.
Taylor, J. (1971). Epidemiology and symptomology of apple bitter rot. Phytopathology, 61, 1028–1029.
Tisserat, N., & Kuntz, J. E. (1983). Dispersal gradients of conidia of the butternut canker fungus in a forest during rain. Canadian Journal of Forest Research, 13, 1139–1144.
Urena-Padilla, A. R., MacKenzie, S. J., Bowen, B. W., & Legard, D. E. (2002). Etiology and population genetics of Colletotrichum spp. causing crown and fruit rot of strawberry. Phytopathology, 92, 1245–1252.
Verma, N., MacDonald, L., & Punja, Z. K. (2006). Inoculum prevalence, host infection and biological control of Colletotrichum acutatum: Causal agent of blueberry anthracnose in British Columbia. Plant Pathology, 55, 442–450.
Verma, N., MacDonald, L., & Punja, Z. K. (2007). Environmental and host requirements for field infection of blueberry fruits by Colletotrichum acutatum in British Columbia. Plant Pathology, 56, 107–113.
Vichova, J., Stankova, B., & Pokorny, R. (2012). First report of Colletotrichum acutatum on tomato and apple fruits in the Czech Republic. Plant Disease, 96, 769–770.
Wilson, L. L., Madden, L. V., & Ellis, M. A. (1990). Influence of temperature and wetness duration on infection of immature and mature strawberry fruit by Colletotrichum acutatum. Phytopathology, 80, 111–116.
Wilson, L. L., Madden, L. V., & Ellis, M. A. (1992). Overwinter survival of Colletotrichum acutatum in infected strawberry fruit in Ohio. Plant Disease, 76, 948–950.
Yang, X., Madden, L. V., Wilson, L. L., & Ellis, M. A. (1990). Effects of surface topography and rain intensity on splash dispersal of Colletotrichum acutatum. Phytopathology, 80, 1115–1120.
Yang, X. S., Madden, L. V., Reichard, D. L., Wilson, L. L., & Ellis, M. A. (1992). Splash dispersal of Colletotrichum acutatum and Phytophthora cactorum from strawberry fruit by single drop impactions. Phytopathology, 82, 332–340.
Yoshida, S., Tsukiboshi, T., Shinohara, H., Koitabashi, M., & Tsushima, S. (2007). Occurrence and development of Colletotrichum acutatum on symptomless blueberry bushes. Plant Pathology, 56, 871–877.
Zaitlin, B., Zehr, E. I., & Dean, R. A. (2000). Latent infection of peach caused by Colletotrichum gloeosporioides and Colletotrichum acutatum. Canadian Journal of Plant Pathology, 22, 224–228.
Zulfiqar, M., Brlansky, R. H., & Timmer, L. W. (1996). Infection of flower and vegetative tissues of citrus by Colletotrichum acutatum and C. gloeosporioides. Mycologia, 88, 121–128.
Acknowledgements
This work was supported by the MAF Sustainable Farming Fund, Nelson Group 8, the Waikato Fruitgrowers’ Association, Sunfruit Orchards, Pipfruit New Zealand and the Foundation for Research Science and Technology Contract No. C06X0810. Many thanks to Dr. Mike Butcher, Technical Manager of Pipfruit New Zealand during this study, for his support, and to Dr. Robert Beresford for alerting us to the work of Dr. Michael Shaw on splash dispersal, and for helpful comments.
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Everett, K.R., Pushparajah, I.P.S., Timudo, O.E. et al. Infection criteria, inoculum sources and splash dispersal pattern of Colletotrichum acutatum causing bitter rot of apple in New Zealand. Eur J Plant Pathol 152, 367–383 (2018). https://doi.org/10.1007/s10658-018-1481-0
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DOI: https://doi.org/10.1007/s10658-018-1481-0