Genus Monilinia on Pome and Stone Fruit Species

  • Jovana Hrustić
  • Milica Mihajlović
  • Mila Grahovac
  • Goran Delibašić
  • Aleksandra Bulajić
  • Branka Krstić
  • Brankica Tanović
Keywords: Control, Identification, Disease cycle, Symptoms,

Abstract


Different species of the genus Monilinia are common plant pathogens that endanger pome and stone fruit production worldwide. In Serbia, two species of this genus are widely distributed – M. laxa and M. fructigena, while M. fructicola, which is officially on the A2 EPPO List of quarantine pest organisms in Europe and on the 1A part I list of quarantine pest organisms in Serbia, has so far been detected only on stored apple and nectarine fruits. The most important control measures against these pathogens include chemical control in combination with adequate cultural practices, particularly under favourable conditions for  disease development. Concerning that species of this genus can cause significant economic losses, knowledge of the pathogen biology, disease epidemiology and pathogen-host interactions is a necessary prerequisite for stable and profitable production of pome and stone fruits.

References

Amiri, A., Scherm, H., Brannen, P. M., and Schnabel, G.: Laboratory evaluation of three rapid, agar-based assays to assess fungicide sensitivity in Monilinia fructicola. Plant Disease, 92: 415-420, 2008.

Anonymous: Monilinia fructicola. In: Quarantine Pests for Europe, 2nd edn (Eds. Smith IM, McNamara DG, Scott PR & Holderness M), CAB International, Wallingford, GB, 1997, pp. 530-535.

Anonymous: Brown rot of stone fruits. University of Nebrasca-Lincoln, Department of Plant Pathology, 1997a.

Anonymous: Monilinia fructigena (brown rot). Crop Protection Compendium. CAB International, Wallingford, UK, 2004.

Anonymous: Diagnostic Protocol for Monilinia fructigena (Apple Brown Rot), 2008.

Anonymous: Diagnostic protocols for regulated pests - Monilinia fructicola. Bulletin OEPP/EPPO Bulletin, 39: 337-343, 2009.

Anonymous: Pesticidi u prometu u Srbiji (2011). Biljni lekar, 39: 279-316, 2011.

Baker, R. et al.: European Food Safety Authority. Online publication. www.efsa.europa.eu/efsajournal. EFSA J. 9 (4): 2119, 2011.

Balaž, J.: Monilia spp. kao parazit voćaka. Biljni lekar, 2-3: 155-162, 2000.

Batra, L.R.: First authenticated North American record of Monilinia fructigena, with notes on related species. Mycotaxon, 8: 476-484, 1979.

Batra, L.R. and Harada, Y.: A Field Record of Apothecia of Monilinia fructigena in Japan and Its Significance. Mycologia, 78: 913-917, 1986.

Batra, L.R.: World species of Monilinia (Fungi): their ecology, biosystematics and control. Mycologia Memoir, No 16, 246 pp. 1991.

Biggs, A.R. and Northover, J.: Early and late-season susceptibility of peach fruits to Monilinia fructicola. Plant Disease, 72: 1070–1074, 1988.

Borve, J. and Stensvand, A.: Use of a plastic rain shield reduces fruit decay and need for fungicides in sweet cherry. Plant Disease 87: 523–528, 2003.

Byrde, R.J.W. and Willetts, H.J.: The Brown Rot Fungi of Fruit. Their Biology and Control. Pergamon Press, Oxford, UK, 1977.

Casals, C., Viñas, I., Torres, R., Griera, C. and Usall, J.: Effect of temperature and water activity on in vitro germination of Monilinia spp. Journal of Applied Microbiology, 108: 47–54, 2010.

Chand-Goyal, T. and Spotts, R.A.: Postharvest biological control of blue mold of apple and brown rot of cherry by natural saprophytic yeasts alone or in combination with low doses of fungicides. Biological Control, 6: 253-259, 1996.

Côté, M.J., Tardif, M.C. and Meldrum, A.J.: Identification of Monilinia fructigena, M. fructicola, M. laxa, and Monilia polystroma on inoculated and naturally infected fruit using multiplex PCR. Plant Disease, 88: 1219-1225, 2004.

De Cal, A., M-Sagasta, E. and Melgarejo, P.: Antifungal substances produced by Penicillium frequentans and their relationship to the biocontrol of Monilinia laxa. Phytopathology, 78: 888–893, 1988.

De Cal, A. and Melgarejo, P.: Effects of long-wave UV light on Monilinia growth and identification of species. Plant Disease, 83: 62-65, 1999.

De Cal, A., Larena, I., Liñan, M., Torres, R., Lamarca, N., Usall, J., Domenichini, P., Bellini, A., Eribe, X. and Melgarejo, P.: Population dynamics of Epicoccum nigrum, a biocontrol agent against brown rot in stone fruit. Journal of Applied Microbiology, 106: 592–605, 2009.

Elad, Y.: Biological control of grape grey mould by Trichoderma harzianum. Crop Protection, 13: 35-38, 1994.

Elmer, P.A.G., Spiers, T.M. and Wood, P.N.: Effects of pre-harvest foliar calcium sprays on fruit calcium levels and brown rot of peaches. Crop Protection, 26: 11–18, 2007.

Emery, K.M., Michailides, T.J. and Scherm, H.: Incidence of latent infection of immature peach fruit by Monilinia fructicola and relationship to brown rot in Georgia. Plant Disease, 84: 853–857, 2000.

EU Pesticide Database: Active substances. Regulation (EC) No 1107/2009. http://ec.europa.eu/sanco_pesticides/public/, datum pristupa: 11. april 2012.

Filajdić, N., Vukša, P., Ivanović, M. i Rekanović, E.: Biološke mere zaštite bilja: problemi i perspektive. Pesticidi i fitomedicina, 18: 69-75, 2003.

Fulton, C.E., van Leeuwen, G.C.M. and Brown, A.E.: Genetic variation among and within Monilinia species causing brown rot of stone and pome fruits. European Journal of Plant Pathology, 105: 495–500, 1999.

Gell, I., De Cal, A., Torres, R., Usall, J. and Melgarejo, P.: Relationship between the incidence of latent infections caused by Monilinia spp. and the incidence of brown rot of peach fruit: factors affecting latent infection. European Journal of Plant Pathology, 121: 487–498, 2008.

Gell, I., De Cal, A., Torres, R., Usall, J. and Melgarejo, P.: Conidial density of Monilinia spp. on peach fruit surfaces in relation to the incidences of latent infections and brown rot. European Journal of Plant Pathology, 123: 415–424, 2009.

Grahovac, M., Inđić, D., Tanović, B., Lazić, S., Vuković, S., Hrustić, J. i Gvozdenac, S.: Integralna zaštita jabuka od prouzrokovača truleži u skladištima. Pesticidi i fitomedicina, 26: 289-299, 2011.

Grahovac, M., Hrustić, J., Tanović, B., Inđić, D., Vuković, S., Mihajlović, M. i Gvozdenac, S.: In vitro effects of essential oils on Colletotrichum spp. Role of research in sustainable development of agriculture and rural areas 2012, 23 – 26 May, Podgorica, Montenegro, 2012. Proceedings, in press.

Gullino, M.L., Gilardi, G., Tinivella, F. and Garibaldi, A.: Observations on the behaviour of different populations of Plasmopara viticola resistant to QoI fungicides in Italian vineyards. Phytopathology Mediterranea, 43: 341-350, 2004.

Harman, J.E. and Beever, D.J.: The use of post-harvest fungicides to control storage rots in nectarines. Orchardist of New Zealand, 60: 384, 1987.

Holb, I.J.: Effect of Fungicide Treatments and Sanitation Practices on Brown Rot Blossom Blight Incidence, Phytotoxity, and Yiel for Organic Sour Cherry Production. Plant Disease, 11: 1164-1170, 2005.

Holb, I.J.: Possibilities of brown rot management in organic stone fruit roduction in Hungary. International Journal of Horticultural Science, 12: 87–91, 2006.

Holb, I.J.: Brown rot blossom blight of pome and stone fruits: symptom, disease cycle, host resistance, and biological control. International Journal of Horticultural Science, 14: 15–21, 2008.

Holtz, B.A., Michailides, T.J. and Hong, C.X.: Development of apothecia from stone fruit infected and stromatized by Monilinia fructicola in California. Plant Disease, 82: 1375–1380, 1998.

Hong, C., Holtz, B.A., Morgan, D. P. and Michailides, T.J.: Significance of thinned fruit as a source of the secondary inoculum of Monilinia fructicola in California nectarine orchards. Plant Disease, 81: 519-524, 1997.

Hrustić, J., Tanović, B., Grahovac, M. i Delibašić, G.: Molekularna identifikacija Monilinia spp., prouzrokovača truleži ploda dunje. Zbornik rezimea radova X savetovanja o zaštiti bilja, Zlatibor, 2010, pp. 29-30.

Hrustić, J., Tanović, B., Grahovac, M., Mihajlović, M., Delibašić, G. i Vukša, P.: In vitro i in vivo efekat etarskog ulja timijana na Monilinia fructigena. Zbornik rezimea radova XI savetovanja o zaštiti bilja, Zlatibor, 2011, pp. 36-37.

Hrustić, J., Grahovac, M., Mihajlović, M., Delibašić, G., Ivanović, M., Nikolić, M. and Tanović, B.: Molecular detection of Monilinia fructigena as causal agent of brown rot on quince. Pesticides and Phytomedicine, 27: 15-24, 2012.

Hrustić, J., Tanović, B., Mihajlović, M., Grahovac, M., Delibašić, G. and Bulajić, A.: Monilinia spp. causal agents of apple fruit rot. Book of Abstracts I International Symposium and XVII Scientific Conference of Agronomists of Republica Srpska, Trebinje, Bosnia and Herzegovina, 2012a, pp. 192.

Hrustić, J., Tanović, B., Mihajlović, M., Delibašić, G., Stanković, I., Krstić, B. and Bulajić, A.: First Report of Brown Rot Caused by Monilinia fructicola on Nectarine in Serbia, Plant Disease, http://dx.doi.org/10.1094/PDIS-08-12-0718-PDN, 2012b.

Hughes, K.J.D., Fulton, C.E., McReynolds, D. and Lane, C.R.: Development of new PCR primers for identification of Monilinia species. Bulletin OEPP/EPPO Bulletin 30: 507-511, 2000.

Ivanović, M. i Ivanović, D.: Mikoze i pseudomikoze biljaka. P. P. De-eM-Ve, Beograd, 2001.

Jevremović, V.: Osetljivost sorti breskve na Moniliju (Monilia sp.) u uslovima Ruma-Irug. Jugoslovensko voćarstvo, 39/40: 639-643, 1976.

Jones, A.L and Aldwinckle, H.S.: Brown rot diseases. Compendium of Apple and Pear Diseases. American Phytopathology Society Press, pp. 100, 1990.

Jordović, M.: Osetljivost plodova nekih sorata bresaka prema parazitu Monilia sp. Arhiv za poljoprivredne nauke, 17: 96-99, 1954.

Karabulut, O.A. and Baykal, N.: Integrated control of postharvest diseases of peaches with a yeast antagonist, hot water and modified atmosphere packaging. Crop Protection, 23: 431-435, 2004.

Karabulut, O.A., Smilanick, J.L., Crisosto, C.H. and Palou, L.: Control of brown rot of stone fruits by brief heated water immersion treatments. Crop Protection 29: 903–906, 2010.

Kišpatić, J. i Maceljski, M.: Zaštita voćaka. Znanje, Zagreb, 1989.

Köller, W., Parker, D.M., Turechek, W.W. and Avila-Adame, C.: A two-phase resistance response of Venturia inaequalis populations to the QoI fungicides kresoxim-methyl and trifloxystrobin. Plant Disease, 88: 537-544, 2004.

Lane, C.R.: A synoptic key for differentiation of Monilinia fructicola, M. fructigena and M. laxa, based on examination of cultural characters. Bulletin OEPP/EPPO, Bulletin 32: 489-493, 2002.

Larena, I. and Melgarejo, P.: Biological control of Monilinia laxa and Fusarium oxysporum f. sp. lycopersici by a lytic enzyme-producing Penicillium purpurogenum. Biological Control, 6: 361–367, 1996.

Larena, I., Torres, R., De Cal, A., Liñán, M., Melgarejo, P., Domenichini, P., Bellini, A., Mandrin, J.F., Ochoa De Eribe, X. and Usall, J.: Biological control of postharvest brown rot (Monilinia spp.) of peaches by field applications of Epicoccum nigrum. Biological Control, 32: 305–310, 2005.

Leeuwen, van G.C.M., Stein, A., Holb, I. and Jeger, M.J.: Yield loss in apple caused by Monilinia fructigena (Aderh. & Ruhl.) Honey, and spatio-temporaldynamics of disease development. European Journal of Plant Pathology, 106: 519-528, 2000.

Leeuwen, van G.C.M., Holb I.J. and Jeger, M.J.: Factors affecting mummification and sporulation of pome fruit infected by Monilinia fructigena in Dutch orchards. Plant Pathology, 51: 787–793, 2002.

Lučić, K.: Sadržaj sredstava za zaštitu bilja 2009.g. Glasnik zaštite bilja, 1-2: 191-192, 2009.

Luo, Y. and Michailides, T.J.: Factors affecting latent infection of prune fruit by Monilinia fructicola. Phytopathology, 91: 864–872, 2001.

Luo, Y. and Michailides, T.J.: Risk analysis for latent infection of prune by Monilinia fructicola in California. Phytopathology, 91:1197-1208, 2001a.

Luo, Y., Morgan, D.P. and Michailides, T.J.: Risk analysis of brown rot blossom blight of prune caused by Monilinia fructicola. Phytopathology, 91: 759–768, 2001.

Luo, Y. and Michailides, T.J.: Threshold conditions that lead latent infection to prune fruit rot caused by Monilinia fructicola. Phytopathology, 93: 102-111, 2003.

Luo, Y., Michailides, T.J., Morgan, P.D., Krueger, W.H. and Buchner, R.P.: Inoculum dynamics, fruit infection, and development of brown rot in prune orchards in California. Phytopathology, 95: 1132-1136, 2005.

Ma, Z., Yoshimura, M.A. and Michailides, T.J.: Identification and characterization of benzimidazole resistance in Monilinia fructicola from stone fruit orchards in California. Applied and environmental microbiology, 69: 7145–7152, 2003.

Madrigal, C. and Melgarejo, P.: Mechanisms of action of the antibiotic flavipin on Monilinia laxa and Saccharomyces cerevisiae. Mycological Research, 98: 874–878, 1994.

Mari, M., Torres, R., Casalini, N., Lamarca, N., Mandrin, J.F., Lichou, I., Larena, I., De Cal, A., Melgarejo, P. and Usall, J.: Control of postharvest brown rot on nectarine by Epicoccum nigrum and physicochemical treatments. Journal of the Science of Food and Agriculture, 87: 1271–1277, 2007.

Meier, U.: Entwicklungsstadien mono- und dikotyler Pflanzen, BBCH-Monograph, Blackwell Wissenschafte-Verlag, Berlin, 1997.

Melgarejo, P., Carrillo, R. and M-Sagasta, E.: Mycoflora of peach twigs and flowers and its possible significance in biological control of Monilinia laxa. Transaction for the British Mycological Society, 85: 313–317, 1985.

Michailides, T.J., Ogawa, J.M. and Opgenorth, D.C.: Shift of Monilinia spp. and distribution of isolates sensitive and resistant to benomyl in California prune and apricot orchards. Plant Disease, 71: 893–896, 1987.

Michailides, T.J. and Morgan, D.P.: Influence of fruit-to-fruit contact on the susceptibility of French prune to infection by Monilinia fructicola. Plant Disease, 81: 1416–1424, 1997.

Michailides, T., Luo, Y., Ma, Z. and Morgan, D.P.: Brown rot of dried plum in California: new insights on an old disease. APSnet Feature Story, March 2007. Available from: http://www.apsnet.org/publications/apsnetfeatures/Pages/BrownRot.aspx.

Miletić, N., Rekanović, E., Stević, M., Latinović, N. i Miladinović, Z.: Preliminarna ispitivanja biofungicida Polyversum (Pythium oligandrum Drechsler). Zbornik rezimea Šestog savetovanja o zaštiti bilja, Zlatibor, 2003, pp. 63.

Muñoz, Z., Moret, A. and Bech, J.: Morphological and molecular characterization of Monilinia sp. isolates and pathogenicity on apple. Agrociencia, 42: 119-128, 2008.

Ogawa, J.M., Manji, B.T. and Schreader, W.R.: Monilinia life cycle on sweet cherries and its control by overhead sprinkler fungicide applications. Plant Disease Reporter, 59: 876–880, 1975.

Ogawa, J.M. and English, H.: Diseases of temperate zone tree fruit and nut crops. University of California, Division of Agriculture and Natural Resources Pub. 3345, 1991.

Ogawa, J.M., Zehr, E.I., Bird, G.W., Ritchie, D.F., Uriu, K. and Uyemoto, J.K.: Brown Rot. Compendium of stone fruit diseases. American Phytopathological Society Press, St. Paul, MN, 7–10.g, 1995.

Pusey, P.L. and Wilson, C.L.: Postharvest biological control of stone fruit brown rot by Bacillus subtilis. Plant Disease, 68: 753-756, 1984.

Ritchie, D.F. and Pollard, D.W.: Evaluation of preharvest fungicide sprays for control of brown rot of peach fruit, 2001. Fungic. Nematicide Tests 57: STF16, 2002.

Rüegg, J., Lauber, H.P., Siegfried, W., Viret, O., and Hilber, U.: Experiences with anilinopyrimidines in Switzerland. Pesticide Outlook, 8: 28–33, 1997.

Schnabel, G., Bryson, P.K., Bridges, W.C. and Brannen, P.M.: Reduced sensitivity in Monilinia fructicola to propiconazole in Georgia and implications for disease management. Plant Disease, 88: 1000-1004, 2004.

Sonoda, R.M., Ogawa, J.M., Manji, B.T., Shabi, E. and Rough, D.: Factors affecting control of blossom blight in a peach orchard with low level benomyl-resistant Monilinia fructicola. Plant Disease 67: 681–684, 1983.

Spiegel, J. and Stammler, G.: Baseline sensitivity of Monilinia laxa and M. fructigena to pyraclostrobin and boscalid. Journal of Plant Diseases and Protection, 113: 199–206, 2006.

Stojanović, D. i Kostić, B.: Monilia fructigena (Ader. et. Ruhl.) Honey na grožđu. Zaštita bilja, 46: 65-67, 1958.

Takamura, N. and Ochiai, M.: Control of brown rot of peaches by bitertanol. Annual Report of the Society of Plant Protection of North Japan, 40: 77–80, 1989.

Tanović, B., Rekanović, E., Potočnik, I. and Todorović, I.: Effectiveness of fungicides and biofungicides in the control of grey mould of raspberry in Serbia. Book of abstracts 9th International Rubus and Ribes Symposium, Santiago, Chile, 2005, pp. 31.

Tanović, B., Delibašić, G. and Hrustić, J.: In vitro effect of essential oils from some aromatic and medicinal plants on apple fruit pathogens. Book of Abstracts VI Congress of Plant Protection with Symposium about Biological Control of Invasive Species, Zlatibor, I, 2009, pp. 37.

Tanović, B., Hrustić, J. and Delibasic, G.: Toxicity of volatile phase of essential oils from aromatic and medicinal plants to apple fruit pathogens in vitro. Book of Abstracts of 28th International Horticultural Congress, Lisboa, Portugal, 2010.

Tanović, B., Hrustić, J., Ivanović, M. and Delibašić, G.: Effectiveness of biofungicides in the control of grey mould in raspberry in Serbia. Proceedings 28th International Horticultural Congress, Lisboa, Portugal, 2010a, pp. 17-18.

Tanović, B., Hrustić, J., Mihajlović, M., Grahovac, M., Delibašić, G. i Vukša, P.: Suzbijanje Botrytis cinerea i problem rezistentnosti na fungicide. Pesticidi i fitomedicina, 26: 99-110, 2011.

Tomlin, C.: The Pesticide Manual. British Crop Protection Council, Farnham, 2009.

Trkulja, V.: Vrste roda Monilia-Paraziti breskve i mogućnosti njihovog suzbijanja. Biljni lekar 3: 531-539, 1996.

van Leeuwen, G.C.M. and van Kesteren, H.A.: Delineation of the three brown rot fungi of fruit crops (Monilinia spp.) on the basis of quantitative characteristics. Canadian Journal of Botany, 76: 2042-2050, 1998.

Vasić, M., Duduk, N., Ivanović, M.M., Obradović, A. and Ivanović, M.S.: First Report of Brown Rot Caused by Monilinia fructicola on Stored Apple in Serbia. Plant Disease, 96: 456, 2012.

Vico, I. i Jurick, W.M.: Postžetvena patologija biljaka i biljnih proizvoda. Poljoprivredni fakultet Univerziteta u Beogradu, 2012.

Villarino, M., Melgarejom P., Usall, J., Segarra, J. and De Cal, A.: Primary inoculum sources of Monilinia spp. in Spanish peach orchards and their relative importance in brown rot. Plant Disease, 94: 1048–1054, 2010.

Wilson, E.E. and Ogawa, J.M.: Fungal, bacterial and certain non-parasitic diseases of fruit and nut crops in California. Californian Agricultural Science Publications, Berkeley, California, USA, 1979.

Wittig, H.P.P., Johnson, K.B. and Psheidt, J.W.: Effect of epifytic fungi on brown rot blossom blight and latent infections in sweet cherry. Plant Disease, 81: 383-378, 1997.

Wong, F.P. and Wilcox, W.F.: Sensitivity to azoxystrobin among isolates of Uncinula necator: Baseline distribution and relationship to myclobutanil sensitivity. Plant Disease, 86: 394- 404, 2002.

Yoshimura, M.A., Luo, Y., Ma, Z. and Michailides, T.J.: Sensitivity of Monilinia fructicola from stone fruit to thiophanate-methyl, iprodione, and tebuconazole. Plant Disease, 88: 373-378, 2004.

Zehr, E.I., Luszcz, L.A., Olien, W.C., Newall, W.C. and Toler, J.E.: Reduced sensitivity in Monilinia fructicola to propiconazole following prolonged exposure in peach orchards. Plant Disease, 83: 913-916, 1999.

Published
2013/02/12
Section
Review Paper