2007 Plant Management Network. Accepted for publication 5 February 2007. Published. Colletotrichum acutatum Found on Apple Buds in Norway Jorunn Børve, Norwegian Institute for Agricultural and Environmental Research, Ullensvang, 5781 Lofthus, Norway; and Arne Stensvand, Norwegian Institute for Agricultural and Environmental Research, Høgskoleveien 7, 1432 Ås, Norway Corresponding author: Jorunn Børve. jorunn.borve@bioforsk.no Børve, J., and Stensvand, A. 2007. Colletotrichum acutatum found on apple buds in Norway. Online. Plant Health Progress doi:10.1094/php-2007-0522-01-rs. Bitter rot causes important pre- or postharvest losses in apple (Malus domestica) worldwide. Preharvest loss is important for example in the southeastern USA (14), New Zealand (7), and Brazil (5), while postharvest loss has been reported from e.g., Sweden (10) and Norway (3). In Norway, only Colletotrichum acutatum Simmonds ex. Simmonds is found on apple (classified by PCR) (13), while in USA and Brazil both C. acutatum and C. gloeosporioides (Penz.) Penz. & Sacc. in Penz, and its teleomorph Glomerella cingulata (Stoneham.) Schrenk & Spaulding, cause bitter rot on apple fruits (5,8). In Norway, visible symptoms of bitter rot in apple orchards occur occasionally prior to or at harvest; however, the disease normally develops following cold storage. Symptoms in cold storage can be diverse (Fig. 1), and are not easily distinguished from bulls eye rot (caused by Pezicula malicorticis, anamorph Cryptosporiopsis curvispora) and lenticell rot (caused by Pezicula alba, anamorph Phlyctaena vagabunda). All three diseases cause brown, circular, sunken lesions that develop during storage. Conidia of C. acutatum are often formed in orange masses, as opposed to the whitish to creamy sporulation of the other two fungi. Possible inoculum sources for C. gloeosporioides and G. cingulata are cankers (G. cingulata only), mummified fruits, old fruit stems, and mycelium, perithecia, or acervuli on dead wood (2,12,14). Sources of inoculum for C. acutatum in apple have not been studied in detail (11). In Brazil, both C. acutatum and C. gloeosporioides were found on apple buds during the winter (1,5). C. acutatum was also found on apple buds in New Zealand, but at a lower level than on dormant twigs (7). In Sweden, P. vagabunda was found on apple buds during the winter and they were suggested as a possible inoculum source during the spring (10).
A B C Fig. 1. Apple lesions caused by Colletotrichum acutatum with (A) conidia sporulating in orange masses, (B) pink mycelium, and (C) black acervuli and no formation of conidia. Old fruit spurs (spurs that had borne fruit for one year or more) or young fruit spurs (developed during the previous season, which had not borne fruit before) with one to three generative buds were collected from five apple cultivars in 11 orchards (two experimental and nine commercial orchards located in Ullensvang and Kvam, in the Hardanger region, in southwestern Norway) (Table 1) prior to bud break. The buds were incubated in saturated air at 20 C for 2 to 3 weeks. Some vegetative shoots also were collected, cut in pieces (each containing one bud), and incubated as the generative buds. After incubation, the buds were assessed for sporulation of C. acutatum with a stereo magnifier. The fungus sporulated in orange horn-like structures on bud scales (Fig. 2) and in one case also on the wood below an infected bud (Fig. 3).
Table 1. Number of generative apple buds infected with Colletotrichum acutatum from different orchards in Ullensvang and Kvam (in the Hardanger region) in southwestern Norway. Year Cultivar Orchard x Material y C. acutatum Buds with Total no. of buds assessed 2002 Aroma Løeflaten old spurs 1 76 2005 Aroma Fykse 1 old spurs 2 45 Aroma Steinstø old spurs 1 41 Aroma Fykse 2 old spurs 0 33 Aroma Opedal old spurs 2 30 Elan Munkagard young spurs 1 30 Elstar Opedal young spurs 0 30 Daytona Munkagard young spurs 0 30 2006 Aroma, red mutant Munkagard old spurs 1 22 Aroma Munkagard old spurs 0 60 Aroma Øvrehus old spurs 0 40 Aroma Hauso old spurs 0 36 Aroma Bleie old spurs 0 57 Aroma Djønne old spurs 0 30 Aroma Reiseter old spurs 0 32 Elan Munkagard old spurs 1 21 Sunrise Munkagard old spurs 0 76 Total 9 689 x Løeflaten and Munkagard were experimental orchards at Ullensvang Research Centre, while the others were commercial orchards. y Old spurs had borne fruit in one or more years prior to sampling; young spurs were developed in the season prior to sampling and had not borne fruit. Fig. 2. Apple bud with sporulation of Colletotrichum acutatum on bud scales. Fig. 3. Apple bud with sporulation of Colletotrichum acutatum on bud scales, at bud basis, and down the fruit spur. Infections were found on buds from both experimental orchards (at Ullensvang) and in four of the commercial orchards. Two orchards in southeastern Norway were assessed in 2006, but the fungus was not found (data not shown). Sporulation were found on zero, one, and two generative buds in each sample (0 to 7%) on fruiting spurs (Table 1). In total 9 of 689 (1.3%) buds
examined were infected. No sporulation was observed on the 230 vegetative buds assessed (data not shown). C. acutatum was found on buds from two (cvs. Aroma and Elan) of the five cultivars examined. Aroma is the main late ripening cultivar grown in Norway, and it is known to be highly susceptible to storage decay. The number of infected buds was much lower in apple than was found in sweet cherry in Norway, when investigated at a similar developmental stage (4). Apple buds have previously been reported as hosts for C. acutatum only in the southern hemisphere (1,5,7). Apple buds were examined for presence of C. gloeosporioides in Brazil by placing bud parts on agar plates, and 12 to 33% of the buds contained the fungus (1). The fungus was detected on both the outer bud scales and on the inner scales and floral parts, and the frequency of infections did not differ between outer and inner parts of the buds. In a more recent investigation in Brazil, apple buds contained Colletotrichum spp. (no clear distinction between C. acutatum and C. gloeosporioides) during the dormant period (5). The lower frequency of infected buds found in Norway vs. Brazil may be explained by differences in methods of detection. We incubated the buds in moist air and did not attempt to isolate the fungus on an artificial growth medium. Even if the number of infected buds seemed low in these investigations, they may be a potential inoculum source in spring as was found for blueberry (6,15) and sweet cherry (4). Further investigations are needed in order to determine when fruit infections occur and whether or not C. acutatum is present asymptomatically on flowers and leaves during the growing season such as in strawberry and citrus (9,16). Literature Cited 1. Bernardi, J., Feliciano, A., and De Assis, M. 1983. Ocorrência de Glomerella cingulata (Colletotrichum gloeosporioides) nas gemas florais e flores de macieira [Occurrence of Glomerella cingulata (Colletotrichum gloeosporioides) in dormant floral buds and flowers of apple] Pesg. agropec. bras, Brasilia 18:609-611. 2. Burrill, T. J. 1907. Bitter rot of apples. Botanical Investigations. Bull. Univ. Illinois Agric. Exp. Stn. 118:555-608. 3. Børve, J. 2005. Bitterròte i eple. [Bitter rot of apple] Pages 113-117 in: Plantemøtet Vestlandet 2005. Vangdal, E. ed. Grønn kunnskap 9 (4). 4. Børve, J., and Stensvand, A. 2006. Colletotrichum acutatum overwinters on sweet cherry buds. Plant Dis. 90:1452-1456. 5. Crusius, L. U., Forcelini, C. A., Sanhueza, R. M. V., and Fernandes, J. M. C. 2002. Epidemiology of apple leaf spot. Fitopatol. bras. 27:65-70. 6. De Marsay, A. 2005. Anthracnose fruit rot of highbush blueberry: Biology and epidemiology. Ph.D. thesis, Rutgers, The State Univ. of New Jersey, New Brunswick, NJ. 7. Everett, K. R., Timudo-Torrevilla, O. E., Shaw, P., Wallis, R., Mundy, D., Scheper, R., Wood, P., and Butcher, M. 2006. Sustainable solutions for Colletotrichum apple fruit rot. Waikato Fruitgrowers Newsl. August: pages 13-15. 8. Gonzales, E., Sutton, T. B., and Correll, 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. 9. Leandro, L. F. S., Gleason, M. L., Nutter, F. W., Wegulo, S. N., and Dixon, P. M. 2001. Germination and sporulation of Colletotrichum acutatum on symptomless strawberry leaves. Phytopathology 91:659-664. 10. Olsson, K. 1965. A study of the biology of Gloeosporium album and G. perennans on apple. Statens Växtskyddsanstalt Med. 13:189-259. 11. Peres, N. A., Timmer, L. W., Adaskaveg, J. E., and Correll, J. C. 2005. Lifestyles of Colletotrichum acutatum. Plant Dis. 89:784-796. 12. Roberts, J. W. 1918. The sources of apple bitter-rot infections. U.S. Department of Agriculture. Bull. 684, Washington, DC. 13. Stensvand, A., Talgø, V., Strømeng, G. M., Børve, J., Sletten, A., and Klemsdal, S. S. 2006. Colletotrichum acutatum in Norwegian strawberry production and sources of potential inoculum in and around strawberry fields. Pages 87-91 in: Fifth IOBC meet. of Work. Group, Integrated Plant Prot. in Fruit Crops (Sub Group, Soft Fruits). Intn'l Organis. for Biolog. and Integrated Control 29(9).
14. Sutton, T. B. 1990. Bitter rot. Pages 15-16: Compendium of Apple and Pear Diseases. A. L. Jones and H. S. Aldwinckle, eds. American Phytopathological Society, St. Paul, MN. 15. Verma, N., MacDonald, L., and Punja, Z. K. 2006. Inoculum prevalence, host infection and biological control of Colletotrichum acutatum: causal agent of blueberry anthracnose in British Colombia. Plant Pathol. 55:442-450. 16. Zulfiqar, M., Brlansky, R. H., and Timmer, L. W. 1996. Infection of flower and vegetative tissue of citrus by Colletotrichum acutatum and C. gloeosporioides. Mycologia 88:121-128.