Abstract
The management of certain plant beneficial microorganisms [biological control agents (BCAs)] seems to be a promising and environmental friendly method to control plant pathogens. However, applications are still limited because of the lack of consistency of BCAs when they are applied in the field. In the present paper, the advantages and limitations of BCAs are seen through the example of Pythium oligandrum, an oomycete that has received much attention in the last decade. The biological control exerted by P. oligandrum is the result of a complex process, which includes direct effects through the control of pathogens and/or indirect effects mediated by P. oligandrum, i.e. induction of resistance and growth promotion. P. oligandrum antagonism is a multifaceted and target fungus-dependent process. Interestingly, it does not seem to disrupt microflora biodiversity on the roots. P. oligandrum has an atypical relationship with the plant because it rapidly penetrates into the root tissues but it cannot stay alive in planta. After root colonisation, because of the elicitation by P. oligandrum of the plant-defence system, plants are protected from a range of pathogens. The management of BCAs, here P. oligandrum, is discussed with regard to its interactions with the incredibly complex agrosystems.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.References
Abdelzaher HA, Elnaghy M, Fadl-Allah E (1997) Isolation of Pythium oligandrum from Egyptian soil and its mycoparasitic effect on Pythium ultimum var. ultimum the damping-off organism of wheat. Mycopathol 139(2):97–106
Al-Rawahi AK, Hancock JG (1998) Parasitism and biological control of Verticillium dahliae by Pythium oligandrum. Plant Dis 82(10):1100–1106
Alabouvette C, Rouxel F, Louvet J (1979) Characteristics of Fusarium wilt suppressive soils and prospects for their utilization in biological control. In: Schippers B, Gams W (eds) Soil-borne plant pathogens. Academic, London, pp 165–183
Alabouvette C, Couteaudier Y, Louvet J (1983) Soils suppressive to Fusarium wilt: mechanism and management of suppressiveness. In: Parker CA (ed) The ecology and management of soilborne plant pathogens. American Phytopathological Society, St Paul, pp 101–106
Alabouvette C, Lemanceau P (1999) Joint action of microbials for disease control. In: Hall F, Menn J (eds) Biopesticides: use and delivery. Methods in biotechnology. Humana, Totowa, pp 117–135
Alabouvette C, Olivain C, Migheli Q, Steinberg C (2009) Microbiological control of soil-borne phytopathogenic fungi with special emphasis on wilt-inducing Fusarium oxysporum. New Phytol 184(3):529–544
Alabouvette C, Olivain C, Steinberg C (2006) Biological control of plant diseases: the European situation. Eur J Plant Pathol 114(3):329–341
Al-hamdani AM, Cooke RC (1983) Effects of the mycoparasite Pythium oligandrum on cellulolysis and sclerotium production by Rhizoctonia solani. Trans Br Mycol Soc 81:619–621
Al-hamdani AM, Lutchmeah RS, Cooke RC (1983) Biological control of Pythium ultimum-induced damping-off by treating cress seed with the mycoparasite Pythium oligandrum. Plant Pathol 32(4):449–45
Ali-Shtayeh MS (1985) Pythium populations in Middle Eastern soils relative to different cropping practices. Trans Br Mycol Soc 84:695–700
Ali-Shtayeh MS, Saleh ASF (1999) Isolation of Pythium acanthicum, P. oligandrum, and P. periplocum from soil and evaluation of their mycoparasitic activity and biocontrol efficacy against selected phytopathogenic Pythium species. Mycopathologia 45:143–53
Baker R (1968) Mechanisms of biological control of soil-borne pathogens. Annu Rev Phytopathol 6(1):263–294
Benhamou N, Rey P, Cherif M, Hockenhull J, Tirilly Y (1997) Treatment with the mycoparasite Pythium oligandrum triggers induction of defense-related reactions in tomato roots when challenged with Fusarium oxysporum f. sp. radicis-lycopersici. Phytopathol 87(1):108–122
Benhamou N, Rey P, Picard K, Tirilly Y (1999) Ultrastructural and cytochemical aspects of the interaction between the mycoparasite Pythium oligandrum and soilborne plant pathogens. Phytopathol 89(6):506–517
Benhamou N, Belanger RR, Rey P, Tirilly Y (2001) Oligandrin, the elicitin-like protein produced by the mycoparasite Pythium oligandrum, induces systemic resistance to Fusarium crown and root rot in tomato plants. Plant Physiol Biochem 39:681–696
Benhamou N, Garand C (2001) Cytological analysis of defense-related mechanisms induced in pea root tissues in response to colonization by nonpathogenic Fusarium oxysporum Fo47. Phytopathol 91(8):730–740
Benhamou N, Garand C, Goulet A (2002) Ability of nonpathogenic Fusarium oxysporum strain Fo47 to induce resistance against Pythium ultimum infection in cucumber. Appl Environ Microbiol-SGM 68(8):4044–4060
Benhamou N, le Floch G, Vallance J, Gerbore J, Grizard D, Rey P (2012) Pythium oligandrum: an example of opportunistic success. Microbiol 158:2679–2694
Benitez T, Rincon AM, Limon MC, Codon AC (2004) Biocontrol mechanisms of Trichoderma strains. Int Microbiol 7(4):249–260
Bloemberg GV, Lugtenberg BJJ (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol 4(4):343–350
Bradshaw-Smith RP, Whalley WM, Craig GD (1991) Interactions between Pythium oligandrum and the fungal footrot pathogens of peas. Mycol Res 95:861–865
Brozova J (2002) Exploitation of the mycoparasitic fungus Pythium oligandrum in plant protection. Plant Prot Sci 38(1):29–35
Bull AT (1970) Inhibition of polysaccharases by melanin: enzyme inhibition in relation to mycolysis. Arch Biochem Biophys 137(2):345–356
Butler EE (1957) Rhizoctonia solani as a parasite of fungi. Mycol 49(3):354–373
Conrath U (2009) Priming of induced plant defense responses. In: Loon LCV (ed) Advances in botanical research. Academic, New York, pp 361–395
Conrath U, Pieterse CMJ, Mauch-Mani B (2002) Priming in plant–pathogen interactions. Trends Plant Sci 7(5):210–216
Cooney T, Nonhebel H (1991) Biosynthesis of indole-3-acetic acid in tomato shoots: measurement, mass-spectral identification and incorporation of 2H from 2H2O into indole-3-acetic acid, D- and L-tryptophan, indole-3-pyruvate and tryptamine. Planta 184(3):368–376
Cother EJ, Gilbert RL (1993) Comparative pathogenicity of Pythium species associated with poor seedling establishment of rice in Southern Australia. Plant Pathol 42(2):151–157
Drechsler C (1930) A new species of Pythium. J Wash Acad Sci 20(16):398–418
Cwalina-Ambroziak B, Nowak M (2012) The effects of biological and chemical controls on fungal communities colonising tomato (Lycopersicon esculentum Mill.) plants and soil. Folia Hort 24:13–20
Edel-Hermann V, Brenot S, Gautheron N, Aime S, Alabouvette C, Steinberg C (2009) Ecological fitness of the biocontrol agent Fusarium oxysporum Fo47 in soil and its impact on the soil microbial communities. FEMS Microbiol Ecol 68(1):37–45
El-Katatny MH, Abdelzaher HMA, Shoulkamy MA (2006) Antagonistic actions of Pythium oligandrum and Trichoderma harzianum against phytopathogenic fungi (Fusarium oxysporum and Pythium ultimum var. ultimum). Arch Phytopathol Plant Prot 39(4):289–301
Fletcher JT, Smewin BJ, Obrien A (1990) Pythium oligandrum associated with a cropping disorder of Agaricus bisporus. Plant Pathol 39(4):603–605
Foley MF, Deacon JW (1986) Susceptibility of Pythium spp. and other fungi to antagonism by the mycoparasite Pythium oligandrum. Soil Biol Biochem 18(1):91–95
Frankenberger WT, Arshad M (1995) Phytohormones in soil: microbial production and function. Marcel Dekker, New York
Fravel DR (1988) Role of antibiosis in the biocontrol of plant-diseases. Annu Rev Phytopathol 26:75–91
Fravel D, Olivain C, Alabouvette C (2003) Fusarium oxysporum and its biocontrol. New Phytol 157(3):493–502
Guetsky R, Shtienberg D, Elad Y, Dinoor A (2001) Combining biocontrol agents to reduce the variability of biological control. Phytopathol 91(7):621–627
Guetsky R, Shtienberg D, Elad Y, Fischer E, Dinoor A (2002) Improving biological control by combining biocontrol agents each with several mechanisms of disease suppression. Phytopathol 92(9):976–985
Haas D, Defago G (2005) Biological control of soil-borne pathogens by Fluorescent pseudomonads. Nat Rev Microbiol 4:307–19
Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2(1):43–56
Hase S, Shimizu A, Nakaho K, Takenaka S, Takahashi H (2006) Induction of transient ethylene and reduction in severity of tomato bacterial wilt by Pythium oligandrum. Plant Pathol 55(4):537–543
Hase S, Takahashi S, Takenaka S, Nakaho K, Arie T, Seo S, Ohashi Y, Takahashi H (2008) Involvement of jasmonic acid signalling in bacterial wilt disease resistance induced by biocontrol agent Pythium oligandrum in tomato. Plant Pathol 57(5):870–876
He SS, Zhang BX, Ge QX (1992) On the antagonism by hyperparasite Pythium oligandrum. Acta Phytopathol Sini 22:77–82
Helman Y, Burdman S, Okon Y (2011) Plant growth promotion by rhizosphere bacteria through direct effects. In: Rosenberg E, Gophna U (eds) Beneficial microorganisms in multicellular life forms. Springer, Berlin, pp 89–103
Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiol 158:17–25
Horner NR, Grenville-Briggs LJ, Van West P (2012) The oomycete Pythium oligandrum expresses putative effectors during mycoparasitism of Phytophthora infestans and is amenable to transformation. Fungal Biol 116(1):24–41
Howell CR (2003) Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87(1):4–10
Hyakumachi M, Kubota M (2003) Fungi as plant growth promoter and disease suppressor. In: Arora DK, Bridge PD, et al. (eds) Fungal biotechnology in agricultural, food, and environmental applications. Mycology. CRC, Boca Raton
Ikeda S, Shimizu A, Shimizu M, Takahashi H, Takenaka S (2012) Biocontrol of black scurf on potato by seed tuber treatment with Pythium oligandrum. Biol Control 60(3):297–304
Jeger MJ, Jeffries P, Elad Y, Xu XM (2009) A generic theoretical model for biological control of foliar plant diseases. J Theor Biol 256(2):201–214
Jones EE, Deacon JW (1995) Mycoparasite-like behaviour of the plant pathogen Pythium aphanidermatum in vitro. Plant Pathol 44(2):396–405
Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity. Sci 324(5923):89–91
Kawamura Y, Takenaka S, Hase S, Kubota M, Ichinose et al (2009) Enhanced defense responses in Arabidopsis induced by the cell wall protein fractions from Pythium oligandrum require SGT1, RAR1, NPR1 and JAR1. Plant Cell Physiol 50(5):924–934
Kilpatrick RA (1968) Seedling reaction of barley, oats and wheat to Pythium species. Plant Dis 52:209–212
Klemmer HW, Nakano RY (1964) Distribution and pathogenicity of Phytophthora and Pythium in pineapple soils of Hawaii. Plant Dis Rep 48:848–852
Kobayasi Y, Matsushima T, Takada M, Hagiwara H (1977) Reports of Japanese mycological expedition to Mts Ruwenzori, Central-Africa. Trans Mycol Soc Jpn 18(1):64–94
Kloepper JW, Zablotowicz RM, Tipping EM, Lifshitz R (1991) Plant growth promotion mediated by bacterial rhizosphere colonizers. In: Keister DL, Cregan PB (eds) The rhizosphere and plant growth. Kluwer Academic, Dordrecht, pp 315–326
Kratka J, Bergmanova E, Kudelova A (1994) Effect of Pythium oligandrum and Pythium ultimum on biochemical-changes in cucumber (Cucumis-Sativus L). J Plant Dis Prot 101(4):406–413
Le Floch G, Rey P, Déniel F, Benhamou N, Picard K, Tirilly Y (2003a) Enhancement of development and induction of resistance in tomato plants by the antagonist, Pythium oligandrum. Agron 23(5–6):455–460
Le Floch G, Rey P, Benizri E, Benhamou N, Tirilly Y (2003b) Impact of auxin-compounds produced by the antagonistic fungus Pythium oligandrum or the minor pathogen Pythium group F on plant growth. Plant Soil 257(2):459–470
Le Floch G, Benhamou N, Mamaca E, Salerno MI, Tirilly Y, Rey P (2005) Characterisation of the early events in atypical tomato root colonisation by a biocontrol agent, Pythium oligandrum. Plant Physiol Biochem 43(1):1–11
Le Floch G, Tambong J, Vallance J, Tirilly Y, Levesque A, Rey P (2007) Rhizosphere persistence of three Pythium oligandrum strains in tomato soilless culture assessed by DNA macroarray and real-time PCR. FEMS Microbiol Ecol 61(2):317–326
Le Floch G, Vallance J, Benhamou N, Rey P (2009) Combining the oomycete Pythium oligandrum with two other antagonistic fungi: root relationships and tomato grey mold biocontrol. Biol Control 50(3):288–298
Lherminier J, Benhamou N, Larrue J, Milat ML, Boudon-Padieu E, Nicole M, Blein JP (2003) Cytological characterization of elicitin-induced protection in tobacco plants infected by Phytophthora parasitica or phytoplasma. Phytopathol 93(10):1308–1319
Lifshitz R, Kloepper JW, Kozlowski M, Simonson C, Carlson J, Tipping EM, Zaleska I (1987) Growth promotion of canola (Rapseed) seedlings by a strain of Pseudomonas putida under gnotobiotic conditions. Can J Microbiol 33(5):390–395
Liu SD, Baker R (1980) Mechanism of biological control in soil suppressive to Rhizoctonia solani. Phytopathol 70(5):404–412
Lou BG, Wang AY, Lin C, Xu T, Zheng XD (2011) Enhancement of defense responses by oligandrin against Botrytis cinerea in tomatoes. Afr J Biotechnol 10(55):442–449
Louvet J, Rouxel F, Alabouvette C (1976) Recherches sur la résistance des sols aux maladies, mise en evidence de la nature microbiologique de la résistance d′un sol au developpement de la fusanose vasculaire du melon. Ann Phytopathol 8:425–436, French
Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–566
Madsen AM, de Neergaard E (1999) Interactions between the mycoparasite Pythium oligandrum and sclerotia of the plant pathogen Sclerotinia sclerotiorum. Eur J Plant Pathol 105(8):761–768
Mallik MAB, Williams RD (2008) Plant growth promoting rhizobacteria and mycorrhizal fungi in sustainable agriculture and forestry. Sanashui, China
Martin FN, Hancock JG (1986) Association of chemical and biological factors in soils suppressive to Pythium ultimum. Phytopathol 76(11):1221–1231
Martin FN, Hancock JG (1987) The Use of Pythium oligandrum for biological control of pre-emergence damping-off caused by Pythium ultimum. Phytopathol 77(7):1013–1020
Masunaka A, Nakaho K, Sakai M, Takahashi H, Takenaka S (2009) Visualization of Ralstonia solanacearum cells during biocontrol of bacterial wilt disease in tomato with Pythium oligandrum. J Gen Plant Pathol 75(4):281–287
Masunaka A, Sekiguchi H, Takahashi H, Takenaka S (2010) Distribution and expression of elicitin-like protein genes of the biocontrol agent Pythium oligandrum. J Phytopathol 158(6):417–426
McQuilken MP, Whipps JM, Cooke RC (1990) Control of damping-off in cress and sugar beet by commercial seed-coating with Pythium oligandrum. Plant Pathol 39(3):452–462
McQuilken MP, Whipps JM, Cooke RC (1992) Use of oospore formulations of Pythium oligandrum for biological control of Pythium damping-off in cress. J Phytopathol 135(2):125–134
McQuilken MP, Powell HG, Budge SP, Whipps JM (1998) Effect of storage on the survival and biocontrol activity of Pythium oligandrum in pelleted sugar beet seed. Biocontrol Sci Technol 8(2):237–241
Meszka B, Bielenin A (2010) Polyversum WP a new biological product against strawberry grey mould. Phytopathol 58:13–19
Mohamed N, Lherminier J, Farmer MJ, Fromentin J, Beno N, Houot V, Milat ML, Blein JP (2007) Defense responses in grapevine leaves against Botrytis cinerea induced by application of a Pythium oligandrum strain or its elicitin, oligandrin, to roots. Phytopathol 97(5):611–620
Mulligan DFC, Deacon JW (1992) Detection of presumptive mycoparasites in soil placed on host-colonized agar plates. Mycol Res 96:605–608
Olivain C, Alabouvette C (1997) Colonization of tomato root by a non-pathogenic strain of Fusarium oxysporum. New Phytol 137(3):481–494
Olivain C, Alabouvette C (1999) Process of tomato root colonization by a pathogenic strain of Fusarium oxysporum f. sp. Lycopersici in comparison with a non-pathogenic strain. New Phytol 141(3):497–510
Olivain C, Humbert C, Nahalkova J, Fatehi J, L’Haridon F, Alabouvette C (2006) Colonization of tomato root by pathogenic and nonpathogenic Fusarium oxysporum strains inoculated together and separately into the soil. Appl Environ Microbiol 72(2):1523–1531
Picard K, Tirilly Y, Benhamou N (2000a) Cytological effects of cellulases in the parasitism of Phytophthora parasitica by Pythium oligandrum. Appl Environ Microbiol 66(10):4305–4314
Picard K, Ponchet M, Blein JP, Rey P, Tirilly Y, Benhamou N (2000b) Oligandrin. A proteinaceous molecule produced by the mycoparasite Pythium oligandrum induces resistance to Phytophthora parasitica infection in tomato plants. Plant Physiol 124(1):379–395
Plaats-Niterink AJVd (1981) Monograph of the genus Pythium. Baarn, Netherlands
Ponchet M, Panabieres F, Milat ML, Mikes V, Montillet JL, Suty L, Triantaphylides C, Tirilly Y, Blein JP (1999) Are elicitins cryptograms in plant–oomycete communications? Cell Mol Life Sci 56(11–12):1020–1047
Rekanovic E, Milijasevic S, Todorovic B, Potocnik I (2007) Possibilities of biological and chemical control of Verticillium wilt in pepper. Phytoparasit 35(5):436–441
Rey P, Benhamou N, Tirilly Y (1996) Ultrastructural and cytochemical studies of cucumber roots infected by two Pythium species with different modes of pathogenicity. Physiol Mol Plant Pathol 49(4):213–231
Rey P, Benhamou N, Wulff E, Tirilly Y (1998a) Interactions between tomato (Lycopersicon esculentum) root tissues and the mycoparasite Pythium oligandrum. Physiol Mol Plant Pathol 53(2):105–122
Rey P, Benhamou N, Tirilly Y (1998b) Ultrastructural and cytochemical investigation of asymptomatic infection by Pythium spp. Phytopathol 88(3):234–244
Rey P, Picard K, Déniel F, Benhamou N, Tirilly Y (1999) Development of an IPM system in soilless culture by using slow filtration and a biocontrol fungus, Pythium oligandrum. In: Van Lenteren JC (ed) Integrated control in glasshouses, IOBC WPRS Bulletin, pp 205–208
Rey P, Le Floch G, Benhamou N, Salerno MI, Thuillier E, Tirilly Y (2005) Interactions between the mycoparasite Pythium oligandrum and two types of sclerotia of plant-pathogenic fungi. Mycol Res 109:779–788
Rey P, Gl F, Benhamou N, Tirilly Y (2008) Pythium oligandrum biocontrol: its relationships with fungi and plants. In: Ait Barka E, Clément C (eds) Plant–microbe interactions. Research Signpost, Kerala, pp 43–67
Ribeiro WRC, Butler EE (1992) Isolation of mycoparasitic species of Pythium with spiny oogonia from soil in California. Mycol Res 96:857–862
Rouxel F, Alabouvette C, Louvet J (1979) Recherches sur la résistance des sols aux maladies IV-Mise en évidence du role des Fusanum autochtones dans la résistance d′un sol à la Fusariose vasculaire du Melon. Ann Phytopathol 11:199–207, French
Rybicka H (1981) Tryptophan in root exudate of mock orange and tomato. Acta Physiol Plant 3:95–98
Savazzini F, Longa CMO, Pertot I (2009) Impact of the biocontrol agent Trichoderma atroviride SC1 on soil microbial communities of a vineyard in northern Italy. Soil Biol Biochem 41(7):1457–1465
Schmitthenner AF (1962) Isolation of Pythium from soil particles. Phytopathol 52:1133–1138
Sharma RR, Singh D, Singh R (2009) Biological control of postharvest diseases of fruits and vegetables by microbial antagonists: a review. Biol Control 50(3):205–221
Taiz L, Zeiger E (1998) Auxins. In: Taiz L, Zeiger E (eds) Plant physiology. Sinauer Associates, Sunderland, pp 543–589
Takenaka S, Nishio Z, Nakamura Y (2003) Induction of defense reactions in sugar beet and wheat by treatment with cell wall protein fractions from the mycoparasite Pythium oligandrum. Phytopathology 93(10):1228–1232
Takenaka S, Nakamura Y, Kono T, Sekiguchi H, Masunaka A, Takahashi H (2006) Novel elicitin-like proteins isolated from the cell wall of the biocontrol agent Pythium oligandrum induce defence-related genes in sugar beet. Mol Plant Pathol 7(5):325–339
Takenaka S, Sekiguchi H, Nakaho K, Tojo M, Masunaka A, Takahashi H (2008) Colonization of Pythium oligandrum in the tomato rhizosphere for biological control of bacterial wilt disease analyzed by real-time PCR and confocal laser-scanning microscopy. Phytopathol 98(2):187–195
Takenaka S, Tamagake H (2009) Foliar spray of a cell wall protein fraction from the biocontrol agent Pythium oligandrum induces defence-related genes and increases resistance against Cercospora leaf spot in sugar beet. J Gen Plant Pathol 75(5):340–348
Takenaka S, Ishikawa S (2013) Biocontrol of sugar beet seedling and taproot diseases caused by Aphanomyces cochlioides by Pythium oligandrum treatments before transplanting. Jpn Agric Res Quarter 47(1):75–83
Vaartaja O, Bumbieris M (1964) Abundance of Pythium species in nursery soils in South Australia. Aust J Biol Sci 17:436–445
Vallance J, Le Floch G, Deniel F, Barbier G, Levesque CA, Rey P (2009) Influence of Pythium oligandrum biocontrol on fungal and oomycete population dynamics in the rhizosphere. Appl Environ Microbiol 75(14):4790–4800
Vallance J, Deniel F, Barbier G, Guerin-Dubrana L, Benhamou N, Rey P (2012) Influence of Pythium oligandrum on the bacterial communities that colonize the nutrient solutions and the rhizosphere of tomato plants. Can J Microbiol 58(9):1124–1134
Veloso J, Diaz J (2012) Fusarium oxysporum Fo47 confers protection to pepper plants against Verticillium dahliae and Phytophthora capsici, and induces the expression of defence genes. Plant Pathol 61(2):281–288
Weaver M, Vedenyapina E, Kenerley CM (2005) Fitness, persistence, and responsiveness of a genetically engineered strain of Trichoderma virens in soil mesocosms. Appl Soil Ecol 29(2):125–134
Whipps JM, McQuilken MP (2001) Biocontrol activity of Pythium oligandrum and Coniothyrium minitans in pelleted and film-coated seed. Seed treatment: challenges & opportunities. BCPC Symposium Proceedings No. 76, pp 127–134
Wright JM (1956) The production of antibiotics in soil. Ann Appl Biol 44(3):461–466
Wulff EG, Pham ATH, Cherif M, Rey P, Tirilly Y, Hockenhull J (1998) Inoculation of cucumber roots with zoospores of mycoparasitic and plant pathogenic Pythium species: differential zoospore accumulation, colonization ability and plant growth response. Eur J Plant Pathol 104(1):69–76
Xu XM, Salama N, Jeffries P, Jeger MJ (2010) Numerical studies of biocontrol efficacies of foliar plant pathogens in relation to the characteristics of a biocontrol agent. Phytopathol 100(8):814–821
Xu XM, Jeffries P, Pautasso M, Jeger MJ (2011a) A numerical study of combined use of two biocontrol agents with different biocontrol mechanisms in controlling foliar pathogens. Phytopathol 101(9):1032–1044
Xu XM, Jeffries P, Pautasso M, Jeger MJ (2011b) Combined use of biocontrol agents to manage plant diseases in theory and practice. Phytopathol 101(9):1024–1031
Yedidia I, Benhamou N, Chet I (1999) Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl Environ Microbiol 65(3):1061–1070
Acknowledgments
This research was supported by Biovitis SA, Saint-Etienne de Chomeil, France and the French “Association Nationale de la Recherche et de la Technologie”.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
Cite this article
Gerbore, J., Benhamou, N., Vallance, J. et al. Biological control of plant pathogens: advantages and limitations seen through the case study of Pythium oligandrum . Environ Sci Pollut Res 21, 4847–4860 (2014). https://doi.org/10.1007/s11356-013-1807-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-013-1807-6