Abstract
Mechanisms involved in the biological suppression of infection and inoculum potential ofBotrytis cinerea are numerous and variable and the involvement of two or more mechanisms has been demonstrated in several systems. Reported combinations include antibiosis with enzyme degradation ofB. cinerea cell walls; competition for nutrients followed by interference with pathogenicity enzymes of the pathogen or with induced resistance; and alteration of plant surface wettability combined with antibiosis. Since germinatingB. cinerea conidia are dependent on the presence of nutrients, competition for nutrients is regarded as important in systems where biocontrol is involved. Conidial viability and germination capacity are also potentially affected by the presence of antibiotics produced by biocontrol agents and present in the phyllosphere. Slower in action are mechanisms involving induced resistance in the host plant and production of hydrolytic enzymes that degradeB. cinerea cell walls. The latter has been demonstrated much more convincinglyin vitro than in the phyllosphere. Biocontrol in established lesions and reduction of sporulation on necrotic plant tissues is a means to minimize the pathogen inoculum.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- BCA:
-
bio-control agent
- Bc :
-
Botrytis cinerea
- PG:
-
polygalacturonase
- PL:
-
Pectin lyase
- PME:
-
Pectin methyl esterase
- PR:
-
pathogenesis related
- VPD:
-
vapour pressure deficit
References
Ale-Agha N, Dubos B, Grosclaude C and Ricard LL (1974) Antagonism between non-geminated spores ofTrichoderma viride andBotrytis cinerea, Monilla laxa, M. fructigena andPhomopsis viticola. Plant Dis Reptr 58: 915–917
Andrews JH (1985) Strategies for selecting antagonistic microorganisms from the phylloplan. In: Windels CE and Lindow SE (eds) Biological Control on the Phylloplane (pp. 31–34), American Phytopathological Society, St Paul, MN, USA
Andrews JH (1992) Biological control in the phyllosphere. Annu Rev Phytopathol 30: 603–635
Baigent NL and Ogawa JM (1960) Activity of the antibiotic produced byPullularia pullulans. Phytopathology 50: 82
Barak R, Elad Y and Chet I (1986) The properties of L-fucose binding agglutinin associated with the cell wall ofRhizoctonia solani. Arch Microbiol 144: 346–349
Barak R, Elad Y, Mirelman D and Chet I (1985) Lectins: A possible basis for specific recognition inTrichoderma-Sclerotium rolfsii interaction. Phytopathology 75: 458–462
Bélanger RR, Dufour N, Caron J and Benhamou N (1995) Chronological events associated with antagonistic properties ofTrichoderma harzianum againstBotrytis cinerea: Indirect evidence for sequential role of antibiosis and parasitism. Biocontrol Sci Technol 5: 41–53
Bélanger RR, Labbé C and Jarvis WR (1994) Commercial-scale control of rose powdery mildew with fungal antagonists. Plant Dis 78: 420–424
Bhatt DD and Vaughan EK (1962) Preliminary investigations on biological control of grey mould (Botrytis cinerea) of strawberries. Plant Dis Reptr 46: 342–345
Blakeman JP (1972) Effect of plant age on inhibition ofBotrytis cinerea spores by bacteria on beetroot leaves. Physiol Plant Pathol 2: 143–152
Blakeman JP (1975) Germination ofBotrytis cinerea conidiain vitro in relation to nutrient conditions on leaf surfaces. Trans Br mycol Soc 65: 239–247
Blakeman JP (1980) Behaviour of conidia on aerial plant surfaces. In: Coley-Smith JR, Verhoeff K and Jarvis WR (eds) The Biology of Botrytis (pp. 115–151), Academic Press, London, UK
Blakeman JP (1982) Phylloplane interactions. In: Mount MS and Lacey GH (eds) Phytopathogenic Procariots, Vol I (pp. 308–333), Academic Press, London, UK
Blakeman JP (1985) Ecological succession of leaf surface microorganisms in relation to biological control. In: Windels CE and Lindow SE (eds) Biological Control on the Phylloplane (pp. 6–7), American Phytopathological Society, St. Paul, MN, USA
Blakeman JP (1993) Pathogens in the foliar environment. Plant Pathol 42: 479–493
Blakeman JP and Brodie IDS (1976) Inhibition of pathogens by epiphytic bacteria on aerial plant surfaces. In: Dickson CH and Preece TF (eds) Microbiology of Aerial Plant Surfaces, Academic Press, London
Blakeman JP and Fokkema NJ (1982) Potential for biological control of plant diseases on the phylloplane. Annu Rev Phytopathol 20: 167–192
Blakeman JP and Sztejnberg A (1974) Germination ofBotrytis cinerea spores on beetroot leaves treated with antibiotics. Trans Br mycol Soc 62: 537–545
Brodie IDS and Blakeman JP (1975) Competition for carbon compounds by a leaf surface bacterium and conidia ofBotrytis cinerea. Physiol Plant Pathol 6: 125–136
Bunster L, Fokkema NJ and Schippers B (1986) Effect of surfaceactivePseudomonas spp. on leaf wettability. Appl Environ Microbiol 55: 1340–1345
Burrage SW (1971) The micro-climate at the leaf surface. In Preece TF and Dickinson CH (eds) Ecology of Leaf Surface Microorganism (pp. 91–101), Academic Press, London, UK
Calderon AA, Zapata JM, Munoz R, Fedreno MA and Barcelo AR (1993) Resveratrol production as a part of the hypersensitive-like response of grapevine cells to an elicitor fromTrichoderma viride. New Phytol 124: 455–463
Calderon AA, Zapata JM and Barcelo AR (1994) Peroxidasemediated formation of resveratrol oxidation products during the hypersensitive-like reaction of grapevine cells to an elicitor fromTrichoderma viride. Physiol Mol Plant Mol Biol 44: 289–299
Coley-Smith JR (1980) Sclerotia and other structures in survival. In: Coley-Smith JR, Verhoeff K and Jarvis WR (eds) The Biology of Botrytis (pp 85–114), Academic Press, London, UK
Coley-Smith JR and Cooke RC (1971) Survival and germination of fungal sclerotia. Ann Rev Phytopathol 9: 65–92
Collmer A and Keen NT (1986) The role of pectic enzymes in plant pathogenesis. Annu Rev Phytopathol 24: 383–409
Cook DWM and Long PG (1995) Screening of microbes that attach to Botrytis cinerea hyphae before tests for biocontrol activity. XIII Intern Plant Protec Cong, The Hague. Eur J Plant Pathol, Abstr No 503
Cooper DG (1986) Biosurfactants. Microbiol Sci 3: 145–149
Cutter EG (1978) Aspects of the structure and development of the aerial surfaces of higher plants, In: Dickinson CH and Preece TF (eds) Microbiology of Aerial Plant Surfaces (pp. 1–40) Academic Press, London, UK
Dik AJ, Fokkema NJ and Van Pelt JA (1991) Consumption of aphid honeydew, a wheat yield reduction factor, by phyllosphere yeasts under field conditions. Neth J Plant Pathol 97: 209–232
Dik AJ, Fokkema NJ and Van Pelt JA (1992) Influence of climatic and nutritional factors on yeast population dynamics in the phyllosphere of wheat. Microb Ecol 23: 41–52
Di Pietro A, Lorito M, Hayers CK, Broadway RM and Harman CE (1993) Endochitinase fromGliocladium virens: Isolation, characterization, and synergistic antifungal activity in combination with gliotoxin. Phytopathology 73: 308–313
Douglas W (1987) Adhesion to surfaces. In: Rose AH and Harrison JS (eds) The Yeast, vol II, Academic Press, New York, NY, USA
Droby S, Chalutz E and Wilson L (1991) Antagonistic microorganisms as biological control agents of postharvest diseases of fruits and vegetables. Postharvest News Inf 2: 169–173
Dubos B (1987) Fungal antagonism in aerial agrobiocenoses. In: Innovative Approaches to Plant Disease Control (pp. 107–135), J Wiley and Sons, New York, NY, USA
Dubos B (1992) Biological control ofBotrytis: State-of-the-art. In: Verhoeff K, Malathrakis NE and Williamson B (eds) Recent Advances in Botrytis Research (pp. 169–178), Pudoc Scientific Publishers, Wageningen, The Netherlands
Dubos B and Bulit J (1981) Filamentous fungi as biocontrol agents on aerial plant surfaces. In: Blakeman JP (ed) Microbial Ecology of the Phylloplane (pp. 353–356), In: Academic Press, London, UK
Dubos B, Jailloux F and Bulit J (1982) Protection du vignoble contre la pourriture gris: les proprietes antagonistes duTrichoderma a l'egard duBotrytis cinerea. Les Colloques de l'lNRA 11: 205–219
Edwards SG and Seddon B (1992)Bacillus brevis as biocontrol agent againstBotrytis cinerea on protected chinese cabbage. In: Verhoeff K, Malathrakis NE and Williamson B (eds) Recent Advances in Botrytis Research (pp. 267–271), Pudoc Scientific Publishers, Wageningen, The Netherlands
Elad Y (1988) Latent infection ofBotrytis cinerea in rose flowers and combined chemical physiological control of the disease Crop Prot 7: 361–366
Elad Y (1989) Effect of abiotic conditions on development of grey mould of rose and scanning electron microscopy. Phytopathol Medit 28: 122–130
Elad Y (1990) Reasons for the delay in development of biological control of foliar pathogens: Phytoparasitica 18: 99–105
Elad Y (1995a) Mycoparasitism. In: Kohmoto K, Singh US and Singh RP (ed) Pathogenesis and Host Specificity in Plant Diseases: Histopathological, Biochemical, Genetic and Molecular Basis. Volume II: Eukaryotes (pp. 289–307), Pergamon, Elsevier Science Ltd, Oxford, UK
Elad Y (1995b) Physiological factors involved in susceptibility of plants to pathogens and possibilities for disease control — TheBotrytis cinerea example. In: Lyr H, Russel PE and Sisler HD (eds) Modern Fungicides and Antifungal Compounds (pp. 217–233), British Crop Protection Council, Intercept, UK
Elad Y and Chet I (1995) Practical approaches for biocontrol implementation. In: Reuveni R (ed) Novel Approaches to Integrated Pest Management (pp. 323–338), Lewis Publishers Inc, Chelsea, Michigan
Elad Y and Evensen K (1995) Physiological aspects of resistance toBotrytis cinerea. Phytopathology 85: 637–643
Elad Y and Kirshner B (1992) Establishment of an activeTrichoderma population in the phylloplane and its effect on grey mould (Botrytis cinerea). Phytoparasitica 20(Suppl): 137S-141S
Elad Y and Kirshner B (1993) Survival in the phylloplane of an introduced biocontrol agent (Trichoderma harzianum) and populations of the plant pathogenBotrytis cinerea as modified by abiotic conditions. Phytoparasitica 21: 303–313
Elad Y, Kirshner B, Gokkes M and Peer R (1992) Disease symptoms caused byBotrytis cinerea in ruscus (Ruscus hypoylossum L.) plants and their control. Phytoparasitica 21: 53–61
Elad Y, Malathrakis NE and Dik A (1996) Biological control of Botrytis incited diseases and powdery mildews in greenhouse crops. Crop Prot 15: 224–240
Elad Y, Köhl J and Fokkema NJ (1994a) Control of infection and sporulation ofBotrytis cinerea on bean and tomato by saprophitic yeasts. Phytopathology 84: 1193–1200
Elad Y, Köhl, J and Fokkema NJ (1994b) Control of infection and sporulation ofBotrytis cinerea on bean and tomato by saprophitic bacteria and fungi. Europ J Plant Pathol 100: 315–336
Elad Y and Shtienberg D (1995)Botrytis cinerea in greenhouse vegetables; chemical, cultural, physiological and biological controls and their integration. Integ Pest Manag Rev 1: 15–29
Elad Y, Shtienberg D and Niv A (1994c)Trichoderma harzianum T39 integrated with fungicides: Improved biocontrol of grey mould. Brighton Crop Prot Conf Pests Diseases: 109–1113
Elad Y, Yunis H and Mahrer Y (1989) Effect of Climatic conditions in polyethylene-covered structures on grey mould disease of winter cucumber. Appl agric Res 3: 243–247
Elad Y and Zimand G (1991) Experience in integrated chemicalbiological control of grey mould (Botrytis cinerea). WPRS Bull 14: 195–199
Elad Y, Zimand G, Zaqs Y, Zuriel S and Chet I (1993) Use ofTrichoderma harzianum in combination or alternation with fungicides to control cucumber grey mould (Botrytis cinerea) under commercial greenhouse conditions. Plant Pathol 42: 324–332
Fokkema NJ (1971) The effect of pollen in the phyllosphere of rye on colonization by saprophytic fungi and on infection byHelminthosporium sativum and other leaf pathogens. Neth J Plant Pathol 77 Supplement no 1: 60 pp
Fokkema NJ (1973) The role of saprophytic fungi in antagonism againstDrechslera sorokiniana (Helminthosporium sativum) on agar plates and on rye leaves with pollen. Physiol Plant Pathol 3: 195–205
Fokkema NJ (1993) Opportunities and problems of control of foliar pathogens with microorganisms. Pestic Sci 37: 411–416
Fokkema NJ, Gerlagh M and Köhl J (1991) Biological control ofSclerotinia sclerotiorum andBotrytis spp. In: Tjamos ES, Papavizas G and Cook RJ (eds) Biological Control of Plant Diseases (pp. 267–271), Plenum Presss, New York, NY, USA
Fokkema NJ, Den Houter, JG, Kosterman, YJC and Nelis, AL (1979) Manipulation of yeasts on field-grown wheat leaves and their antagonistic effect onCochliobolus sativus andSeptoria nodorum. Trans Br mycol Soc 72: 19–29
Ghaffer A (1988) Biological control of sclerotial diseases (p. 155,Botrytis spp.). In: Mukerji KG and Garg KL (eds) Biocontrol of Plant Diseases (pp. 153–175), CRC Press, Boca Raton, FL, USA
Ghisalberti EL and Sivasithamparam K (1991) Antifungal antibiotics produced byTrichoderma spp. Soil Biol Biochem 23: 1011–1020
Gullino LM (t 992) Control of Botrytis rot of grapes and vegetables withTrichoderma spp. In: Tjamos EC, Papavizas GC and Cook RJ (eds) Biological Control of Plant Diseases: Progress and Challenges for the Future (pp. 125–132), Plenum Press, New York, NY, USA
Hallan ND and Juniper BE (1971) The anatomy of leaf surface. In: Preece TF and Dickinson CH (eds) Ecology of Leaf Surface Micro-organisms (pp. 3–37), Academic Press, London, UK
Jackson, AJ, Walters DR and Marshal G (1994) Evaluation ofPenicillium chrysogenum and its antifungal extracts as potential biological control agents againstBotrytis fabae on faba beans. Mycol Res 98: 1117–1126
Janisiewicz WJ (1988) Biocontrol of postharvest diseases of apples with antagonist mixtures. Phytopathology 78: 194–198
Janisiewicz WJ, Peterson DL and Bors R (1994) Control of apple storage decay withSporobolomyces roseus. Plant Dis 78: 466–470
Janisiewicz WJ and Roitman J (1988) Biological control of blue mold and grey mould of apple and pear withPseudomonas cepacia. Phytopathology 78: 1697–1700
Jarvis WR (1962) The dispersal of spores ofBotrytis cinerea Fr. in a raspberry plantation. Trans Br mycol Soc 45: 459–559
Jarvis WR (1980) Epidemiology. In: Coley-Smith JR, Verhoeff K and Jarvis WR (eds) The Biology of Botrytis (pp. 219–250), Academic Press, London, UK
Jarvis WR (1989) Managing diseases in greenhouse crops. Plant Dis 73: 190–194
Johnston DJ and Williamson B (1992) Purification and characterization of four polygalacturonases fromBotrytis cinerea. Mycol Res 96: 343–349
Jordan VWL and Pappas AC (1977) Inoculum suppression and control of strawberryBotrytis. Proc Brit Crop Prot Conf — Pests and Dis: 341–348
Kerssies A (1993) Postharvest biological control ofBotrytis cinerea on gerbera. WPRS Bull 16: 131–135
Köhl J and Fokkema NJ (1993) Fungal interactions on living and necrotic leaves. In: Blakeman JP and Williamson B (eds) Ecology of Plant Pathogen (pp. 321–334) CABI.
Köhl J, Molhoek WML and Fokkema NJ (1991) Biological control of onion neck rot (Botrytis aclada): Protection of wounds made by leaf topping. Biol Sci Tech 1: 261–269
Köhl J, Molhoek WML, Van Der Plas CH and Fokkema NJ (1995a) Suppression of sporulation ofBotrytis spp. as a valid biocontrol strategy. Europ J Plant Pathol 101: 251–259
Köhl J, Molhoek WML, Van Der Plas CH and Fokkema NJ (1995b) Effect ofUlocladium atrum and other antagonists on sporulation ofBotrytis cinerea on dead lily leaves exposed to field conditions. Phytopathology 85: 393–401
Köhl J, Molhoek WML, Van Der Plas CH, Kessel GJT and Fokkema NJ (1992) Biological control ofBotrytis leaf blight of onions: Significance of sporulation suppression. In: Verhoeff K, Malathrakis NE and Williamson B (eds) Recent Advances in Botrytis Research (pp. 192–196), Podoc Scientific Publishers, Wageningen, The Netherlands
Köhl J and Schlösser F (1989) Decay of sclerotia ofBotrytis cinerea byTrichoderma spp. at low temperatures. J Phytopathol 125: 320–326
Köhl J, Van Der Plas CH, Molhoek WML, Van Der Plas CH Fokkema NJ (1995c) Effect of interrupted leaf wetness periods on suppression of sporulation of Botrytis allii and B. cinerea by antagonists on dead onion leaves. Europ J Plant in press
Kranz J (1981) Hyperparasitism of biotrophic fungi. In: Blakeman JP (ed) Microbiology of the Phylloplane (pp. 327–352), Academic Press, London, UK
Kuc J (1987) Plant immunization and its applicability for disease control. In: Chet I (ed) Innovative Approaches to Plant Disease Control (pp. 255–274), J Wiley and Sons, New York, NY, USA
Labudova I and Gogorova L (1988) Biological control of phytopathogenic fungi through Iytic action ofTrichoderma species. FEMS Microbiol Lett 52: 193–198
Lamy Krafft P and Roquebert MF (1981) Analyse des interactions entre deux champignons antagonists:Trichoderma viride Pers. etBotrytis cinerea Pers. ex Fr. Etudes preliminaires. Cryptog Mycol 2: 137–152
Leben C and Daft GC (1965) Influence of an epiphytic bacterium on cucumber anthracnose, early blight of tomato and northern leaf blight of corn. Phytopathology 55: 760–762
Leifert C, Li H, Chidburee S, Hampson S, Workman S, Sigee D, Epton HAS and Harbour A (1995) Antibiotic production and biocontrol activity byBacillus subtilis CL27 andBacillus pumilus CL45. J Appl Bac 78: 97–108
Leone G (1992) Significance of polygalacturonase production byBotrytis cinerea in pathogenesis. In: Verhoeff K, Malathrakis NE and Williamson B (eds) Recent Advances in Botrytis Research (pp. 63–68), Pudoc Scientific Publishers, Wageningen, The Netherlands
Li H and Leiffert C (1994) Development of resistance inBotryotinia fuckeliana (de Bary) Whetzel against the biological control agentBacilus subtilis. J Plant Dis Prot 101: 414–418
Lorito M, Harman GE, Hayers CK, Broadway RM, Tronsmo A, Woo SL and Di Pietro A (1993a) Chitinolytic enzymes produced byTrichoderma harzianum: Antifungal activity of purified endochitinase and chitobiosidase. Phytopathology 83: 302–307
Lorito M, Di Pietro A, Hayers CK, Woo SL and Harman GE (1993b) Antifungal, synergistic interaction between chitinolytic enzymes fromTrichoderma harzianum andEnterobacter cloacae. Phytopathology 83: 721–728
Magen N (1995) Ecophysiology ofGliocladium roseum for improved tolerance of low water availability in the phyllosphere. Proc. 6th International Symposium on Microbiology of Aerial Plant Surfaces. Bendol, France, P 56.
Manocha MS (1990) Cell-cell interaction in fungi. Zeitsch Pflanzenkrank Pflanzen 97: 655–669
Marois JJ, Redmond JC and MacDonald JD (1988) Quantification of the impact of environment on the susceptibility ofRosa hybrida flowers toBotrytis cinerea. J Am Soc hort Sci 113: 842–845
McLaughlin RJ, Wilson CL, Drobi S, Ben-Arie R and Chalutz E (1992) Biological control of post-harvest diseases of grape peach and apple with the yeastKloeckera apiculata andCandida guilliermondii. Plant Dis 76: 470–473
McLaughlin RJ, Wisniewski ME, Wilson CL and Chalutz E (1990) Effect of inoculum concentration and salt solutions on biological control of postharvest diseases of apple withCandida sp. Phytopathology 80: 456–461
McLeod LC and Poole PR (1994) Changes in enzymatic activities after harvest and in early stages ofBotrytis cinerea infection of kiwifruit. J Sci Food Agric 64: 95–100
Mercier J and Wilson CL (1994) Colonization of apple wounds by naturally occurring microflora and introducedCandida oleophila and their effect on infection byBotrytis cinerea during storage. Biol Cont 4: 138–144
Morris RAC and Lane SD (1990) Further observations on the interactions betweenTrichoderma viride andBotrytis species. The Mycolog 4: 195–197
Nair NG and Nadtotchei A (1987) Sclerotia ofBotrytis as a source of primary inoculum for bunch rot of grapes in New South Wales, Australia. Aust J Phytopathol 119: 42–51
Nelson ME and Powelson ML (1988) Biological control of gray mold of snap beans byTrichoderma hamatum. Plant Dis 72: 727–729
Newhook FJ (1951) Microbiological control ofBotrytis cinerea Pers. II Antagonism by fungi and actinomycetes. Ann appl Biol 35: 185–202
Newhook FJ (1957) The relationship of saprophytic antagonism to control ofBotrytis cinerea Pers. on tomatoes. NZ J Sci Tech 38: 474–481
O'Neill TM, Niv A, Elad Y and Shtienberg D (1996) Biological control ofBotrytis cinerea on tomato stem wounds withTrichoderma harzianum. Europ J Plant Pathol 102: 635–643.
Peng G and Sutton JC (1990) Biological methods to control grey mould of strawberry. In: Brighton Crop Protection Conference-Pests and Diseases 3C (pp. 233–240)
Roberts RG (1990) Postharvest biological control of grey mould of apple byCryptococcus laurentii. Phytopathology 80: 526–530
Roby D, Broglie K, Cressman R, Biddle P, Chet I and Broglie R (1990) Activation of bean chitinase promoter in transgenic tobacco plants by phytopathogenic fungi. The Plant Cell 2: 999–1007
Salinas J, Glandorf DCM, Picavet ED and Verhoeff K (1989) Effect of temperature, relative humidity and age of conidia on the incidence of spotting on gerbera flowers caused byBotrytis cinerea. Neth J Plant Path 95: 51–64
Salinas J, Schots A and Verhoeff K (1992) Prevention of gerbera flowers infection byBotrytis cinerea using monoclonal antibodies against cutinas. In: Function of Cutinolytic Enzymes in the Infection of Gerbera Flowers byBotrytis cinerea (pp. 75–84), PhD. thesis, Utrecht Univ, Utrecht, The Netherlands
Scherff RH (1973) Control of bacterial blight of soybean byBdellovibrio bacteriovorous. Phytopathology 63: 400–402
Sequeira L (1983) Mechanisms of induced resistance in plants. Annu Rev Microbiol 37: 51–79
Shaul O, Elad Y, Gallili S, Volpin H, Itzhaki H, Kapulnik Y and Chet I (1995) Peroxidase and pathogenicity related proteins in plant tissues infected byBotrytis cinerea. In: Walters DR, Scholes JD, Bryson RJ, Paul ND and McRoberts N (eds) Physiological Responses of Plants to Pathogens (pp. 285–291). Aspects of Applied Biology 42, Association of Applied Biologists
Schirmböck M, Lorito M, Wang Y, Hayers CK, Arisan-Atac I, Scala F, Harman GE and Kubicek C (1994) Parallel formation and synergism of hydrolytic enzymes and peptaibol antibiotics, molecular mechanisms involved in the antagonistic action ofTrichoderma harzianum against phytopathogenic fungi. Appl Environ Microbiol 60: 4364–4370
Sol HH (1967) Influence of different N-sources on (1) the sugars and amino acids leached from leaves and (2) the susceptibility ofVicia fabae to attack byBotrytis fabae. Meded Facult Landbouww Rijks Universiiteit Gent 32: 768–775
Sosa-Alvarez M, Madden L and Ellis MA (1995) Effects of temperature and wetness duration on sporulation ofBotrytis cinerea on strawberry leaf resiues. Plant Dis 79: 609–615
Sugar D, Roberts RG, Hilton RJ, Righetti TL and Sanchez EE (1994) Integration of cultural methods with yeast treatments for control of postharvest fruit decay in pear. Plant Dis 78: 791–795
Sutton JC (1990) Epidemiology and management of Botrytis leaf blight of onion and gray mold of strawberry: a comparative analysis. Can J Plant Pathol 12: 100–110
Sutton JC and Peng G (1993) Biocontrol of Botrytis cinerea in strawberry leaves. Phytopathology 83: 615–621
Tronsmo A (1992) Leaf and blossom epiphytes and endophytes as biological control agents. In: Tjamos ES, Papavizas G and Cook RJ (eds) Biological Control of Plant Diseases: Progress and Challenges for the Future (pp. 43–54), Plenum Press, New York, NY, USA
Tronsmo A and Dennis C (1977) The use ofTrichoderma species to control strawberry fruit rots. Neth J Plant Path 83 (Suppl 1): 449–455
Tronsmo A and Raa J (1977) Antagonistic action ofTrichoderma pseudokoningii against the apple pathogenBotrytis cinerea. Phytopathol Z 89: 216–220
Tukey HB Jr (1970) The leaching of substances from plants. Annu Rev Plant Physiol 21: 305–324
Urbanek H and Zalewska-Sobczak J (1984) Multiplicity of cell wall degrading glycosidic hydrolases produced by apple infectingBotrytis cinerea. J Phytopathol 110: 261–271
Verhoeff K (1970) Spotting of tomato fruits caused byBotrytis cinerea. Neth J Plant Path 76: 219–26
Verhoeff K (1980) The infection process and host-pathogen interactions. In: Coley-Smith JR, Verhoeff K and Jarvis WR (eds) The Biology of Botrytis (pp. 153–180), Academic Press, New York, NY, USA
Verhoeff K and Warren JM (1972)In vitro andin vivo production of cell wall degrading enzymes byBotrytis cinerea from tomato. Neth J Plant Pathol 78: 179–185
Weissman GS (1964) Effect of ammonium and nitrate solution on protein level and exudate composition. Plant Physiol 39: 947–951
Wilson CL (1989) Managing the microflora of harvested fruits and vegetables to enhance resistance. Phytopathology 79: 1387–1390
Windels CE and Lindow SE (Eds) (1985) Biological Control on the Phylloplane. The American Phytopathological Society, St Paul, MN
Wisniewski M, Biles C, Droby S, MacLaughlin RJ, Wilson C and Chalutz E (1991) Mode of action of postharvest biocontrol yeast,Pichia guilliermondii. I. Characterization of attachment toBotrytis cinerea. Physiol Mol Plant Pathol 39: 245–258
Wisniewski M, Droby S, Chalutz E and Eilam Y (1995) Effect of Ca2+ and Mg2+ onBotrytis cinerea andPenicillium expansum in vitro and on biocontrol activity ofCandida oleophila. Plant Pathol 44: 1016–1024
Wood RKS (1951) The control of diseases of lettuce by use of antagonistic microorganisms I The control ofBotrytis cinerea Pers. Ann appl Biol 38: 203–216
Yunis H and Elad Y (1993) Effect of microclimate and nutrients on development of cucumber gray mold (Botrytis cinerea). Phytoparasitica 21: 257–268
Yunis H, Elad Y and Mahrer Y (1990) Effects of air temperature, relative humidity and canopy wetness on grey mould of cucumbers in unheated greenhouses. Phytoparasitica 18: 203–215
Zhang PG, Sutton JC and Hopkins AA (1994) Evaluation of microorganisms for biocontrol ofBotrytis cinerea in container-grown black spruce seedlings. Can J For Res 24: 1312–1316
Zimand G, Elad Y and Chet I (1991) Biological control ofBotrytis cinerea byTrichoderma spp. Phytoparasitica 19: 252–253
Zimand G, Elad Y, Gagulashvily N and Chet I (1995) Effect of the biocontrol agentTrichoderma harzianum T-39 on the pathogenicity ofBotrytis cinerea. Phytoparasitica 23: 241–242
Zimand G, Elad Y, Kritzman G and Chet I (1994) Control ofBotrytis cinerea byTrichoderma harzianum (T39): Does the biocontrol agent produce inhibitory substances? Phytoparasitica 22: 150–151
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Elad, Y. Mechanisms involved in the biological control ofBotrytis cinerea incited diseases. Eur J Plant Pathol 102, 719–732 (1996). https://doi.org/10.1007/BF01877146
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01877146