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Review Article
Trichodermaplantpathogen interactions
Francesco Vinalea,, Krishnapillai Sivasithamparamb, Emilio L. Ghisalbertic,
Roberta Marraa, Sheridan L. Wooa, Matteo Loritoa
a
Dipartimento di Arboricoltura, Botanica e Patologia Vegetale, Universita` degli Studi di Napoli Federico II, Via Universita` 100, 80055 Portici, Naples,
Italy
b
School of Earth and Geographical Sciences, Faculty of Natural and Agricultural Sciences, The University of Western Australia, WA 6009, Australia
c
School of Biomedical, Biomolecular and Chemical Sciences, Faculty of Life and Physical Sciences, The University of Western Australia, WA 6009, Australia
Received 8 March 2007; received in revised form 3 July 2007; accepted 6 July 2007
Available online 9 August 2007
Abstract
Biological control involves the use of beneficial organisms, their genes, and/or products, such as metabolites, that reduce the negative
effects of plant pathogens and promote positive responses by the plant. Disease suppression, as mediated by biocontrol agents, is the
consequence of the interactions between the plant, pathogens, and the microbial community. Antagonists belonging to the genus
Trichoderma are among the most commonly isolated soil fungi. Due to their ability to protect plants and contain pathogen populations
under different soil conditions, these fungi have been widely studied and commercially marketed as biopesticides, biofertilizers and soil
amendments. Trichoderma spp. also produce numerous biologically active compounds, including cell wall degrading enzymes, and
secondary metabolites. Studies of the three-way relationship established with Trichoderma, the plant and the pathogen are aimed at
unravelling the mechanisms involved in partner recognition and the cross-talk used to maintain the beneficial association between the
fungal antagonist and the plant. Several strategies have been used to identify the molecular factors involved in this complex tripartite
interaction including genomics, proteomics and, more recently, metabolomics, in order to enhance our understanding. This review
presents recent advances and findings regarding the biocontrol-resulting events that take place during the Trichodermaplantpathogen
interaction. We focus our attention on the biological aspects of this topic, highlighting the novel findings concerning the role of
Trichoderma in disease suppression. A better understanding of these factors is expected to enhance not only the rapid identification of
effective strains and their applications but also indicate the potentials for improvement of natural strains of Trichoderma.
r 2007 Elsevier Ltd. All rights reserved.
Keywords: Trichoderma; Biocontrol; Elicitors; Three-way interaction; Induced systemic resistance; Secondary metabolites
1. Introduction
Traditional methods used to protect crops from diseases
have been largely based on the use of chemical pesticides.
Applications of fungicides and fumigants can have drastic
effects on the environment and consumer, and are often
applied in greater quantities than herbicides and insecticides
in agricultural production. Chemical methods, are not
economical in the long run because they pollute the
atmosphere, damage the environment, leave harmful residues, and can lead to the development of resistant strains
among the target organisms with repeated use (Naseby
Corresponding author. Tel.: +39 081 2539338; fax: +39 081 2539339.
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Fig. 1. The pre-contact events of the mycoparasitic interaction Trichodermahost fungus. Phase 1: the mycoparasite produces high molecular weight
compounds that reach the host. Phase 2: low molecular weight-degradation products that are released from the host cell walls reach the mycoparasite and
activate the mycoparasitic gene expression cascade.
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4
R
O
O
O
H
N
H
O
5
MeO
HO
OH
2R = -CH2COCH3
3R = -CH2CHOHCH3
4R = -CHCHCH3
O 1
MeO
OH
O
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CH3
O 7R =H
8R =OH
H
H3C
H
OH
O
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OH
OH
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10
CN
CO2H
12
11
HO
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OH
O HO
OH
S
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OCH3
N
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OH
CH2OH
15
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H
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17
Ac-Aib-Ala-Ala-Aib-Aib-Gln-Aib-Aib-Aib-Ser-Leu-Aib-Pro-Leu-Aib-Ile-Gln-Gln-Leuol
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Fig. 3. Chemical structures of secondary metabolites isolated from Trichoderma spp. 1: T22azaphilone; 2: T39butenolide; 3: harzianolide; 4: dehydro
harzianolide; 5: harzianopyridone; 6: 6-pentyl-a-pyrone; 7: 1-hydroxy-3-methyl-anthraquinone; 8: 1,8-dihydroxy-3-methyl-anthraquinone; 9: harziandione; 10: koninginin A; 11: heptelidic acid; 12: trichoviridin; 13: harzianic acid; 14: gliotoxin; 15: gliovirin; 16: viridin; 17: viridiol; 18: trichorzianines.
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References
Alfano, G., Lewis Ivey, M.L., Cakir, C., Bos, J.I.B., Miller, S.A., Madden, L.V.,
Kamoun, S., Hoitink, H.A.J., 2007. Systemic modulation of gene
expression in tomato by Trichoderma hamatum 382. Phytopathology 97,
429437.
Bae, Y.S., Knudsen, G.R., 2005. Soil microbial biomass influence on
growth and biocontrol efficacy of Trichoderma harzianum. Biological
Control 32, 236242.
Baek, J.M., Howell, C.R., Kenerley, C.M., 1999. The role of an
extracellular chitinase from Trichoderma virens Gv29-8 in the
biocontrol of Rhizoctonia solani. Current genetics 35, 4150.
Ben tez, T., Rincon, A.M., Limon, M.C., Codon, A.C., 2004. Biocontrol
mechanisms of Trichoderma strains. International Microbiology 7,
249260.
Brenner, M.L., 1981. Modern methods for plant growth substance
analysis. Annual Review of Plant Physiology 32, 511538.
Brunner, K., Zeilinger, S., Ciliento, R., Woo, S.L., Lorito, M., Kubicek, C.P.,
Mach, R.L., 2005. Genetic improvement of a fungal biocontrol agent to
enhance both antagonism and induction of plant systemic disease
resistance. Applied Environmental Microbiology 71, 39593965.
Carsolio, C., Benhamou, N., Haran, S., Cortes, C., Gutierrez, A., Chet, I.,
Herrera-Estrella, A., 1999. Role of the Trichoderma harzianum
endochitinase gene, ech42, in mycoparasitism. Applied Environmental
Microbiology 65, 929935.
Chet, I., Inbar, J., 1994. Biological control of fungal pathogens. Applied
Biochemistry and Biotechnology 48, 3743.
Chet, I., Inbar, J., Hadar, I., 1997. Fungal antagonists and mycoparasites.
In: Wicklow, D.T., Soderstrom, B. (Eds.), The Mycota IV: Environmental and Microbial Relationships. Springer, Berlin, pp. 165184.
Ciliento, R., Lanzuise, S., Gigante, S., Rocco, M., Anacleria, M., Woo, S.L.,
Marra, R., Vinale, F., Ferraioli, S., Ambrosino, P., Soriente, I., Turra`, D.,
Scala, F., Lorito, M., 2006. The tabc2 abc transporter gene is involved in
Trichoderma atroviride mycoparasitic and nutritional processes. In:
Proceedings of the Ninth International Workshop on Trichoderma and
Gliocladium, Vienna, Austria, April 68, 2006, T16.
Claydon, N., Allan, M., Hanson, J.R., Avent, A.G., 1987. Antifungal
alkyl pyrones of Trichoderma harzianum. Transactions of the British
Mycological Society 88, 503513.
Cleland, R., 1972. The dosageresponse curve for auxin-induced cell
elongation: a re-evaluation. Planta 104, 19.
Cutler, H.G., Cox, R.H., Crumley, F.G., Cole, P.D., 1986. 6-Pentyl-apyrone from Trichoderma harzianum: its plant growth inhibitory and
antimicrobial properties. Agricultural and Biological Chemistry 50,
29432945.
Cutler, H.G., Himmetsbach, D.S., Arrendale, R.F., Cole, P.D., Cox, R.H.,
1989. Koninginin A: a novel plant regulator from Trichoderma koningii.
Agricultural and Biological Chemistry 53, 26052611.
de Boer, W., Verheggen, P., Klein Gunnewiek, P.J., Kowalchuk, G.A.,
van Veen, J.A., 2003. Microbial community composition affects soil
fungistasis. Applied Environmental Microbiology 69, 835844.
De Meyer, G., Bigirimana, J., Elad, Y., Hofte, M., 1998. Induced systemic
resistance in Trichoderma harzianum T39 biocontrol of Botrytis
cinerea. European Journal of Plant Pathology 104, 279286.
Demain, A.L., Fang, A., 2000. The natural functions of secondary
metabolites. Advances in Biochemical Engineering/Biotechnology 69,
139.
Djonovic, S., Pozo, M.J., Dangott, L.J., Howell, C.R., Kenerley, C.M.,
2006. Sm1, a proteinaceous elicitor secreted by the biocontrol fungus
Trichoderma virens induces plant defense responses and systemic
resistance. Molecular PlantMicrobe Interaction 19, 838853.
Fogliano, V., Ballio, A., Gallo, M., Woo, S.L., Scala, F., Lorito, M., 2002.
Pseudomonas lipodepsipeptides and fungal cell wall-degrading enzymes
ARTICLE IN PRESS
F. Vinale et al. / Soil Biology & Biochemistry 40 (2008) 110
act synergistically in biological control. Molecular PlantMicrobe
Interaction 15, 323333.
Ghisalberti, E.L., Sivasithamparam, K., 1991. Antifungal antibiotics
produced by Trichoderma spp. Soil Biology & Biochemistry 23,
10111020.
Ghisalberti, E.L., Narbey, M.J., Dewan, M.M., Sivasithamparam, K.,
1990. Variability among strains of Trichoderma harzianum in their
ability to reduce take-all and to produce pyrones. Plant and Soil 121,
287291.
Gullino, M.L., 1992. Control of Botrytis rot of grapes and vegetables with
Trichoderma spp. In: Tjamos, E.C., Papavizas, G.C., Cook, R.J.
(Eds.), Biological Control of Plant Diseases, Progress and Challenges
for the Future. Plenum Press, New York, pp. 125132.
Hanson, L.E., Howell, C.R., 2004. Elicitors of plant defense responses
from biocontrol strains of Trichoderma virens. Phytopathology 94,
171176.
Harman, G.E., 2000. Myths and dogmas of biocontrol: changes in
perceptions derived from research on Trichoderma harzianum T-22.
Plant Disease 84, 377393.
Harman, G.E., 2006. Overview of mechanisms and uses of Trichoderma
spp. Phytopathology 96, 190194.
Harman, G.E., Kubicek, C.P., 1998. Trichoderma and Gliocladium.
Taylor & Francis, London, 278pages.
Harman, G.E., Howell, C.R., Viterbo, A., Chet, I., Lorito, M., 2004.
Trichoderma species-opportunistic, avirulent plant symbionts. Nature
Review Microbiology 2, 4356.
Hoitink, H.A.J., Boehm, M.J., 1999. Biocontrol within the context of soil
microbial communities: a substrate-dependent phenomenon. Annual
Review of Phytopathology 37, 427446.
Hoitink, H.A.J., Madden, L.V., Dorrance, A.E., 2006. Systemic resistance
induced by Trichoderma spp.: interactions between the host, the
pathogen, the biocontrol agent, and soil organic matter quality.
Phytopathology 96, 186189.
Howell, C.R., 1998. The role of antibiosis in biocontrol. In: Harman, G.E.,
Kubicek, C.P. (Eds.), Trichoderma and Gliocladium. Enzymes, Biological
Control and Commercial Application, vol. 2. Taylor and Francis Ltd.,
London, pp. 173183.
Howell, C.R., 2002. Cotton seedling preemergence damping-off incited by
Rhizopus oryzae and Pythium spp and its biological control with
Trichoderma spp. Phytopathology 92, 177180.
Howell, C.R., 2003. Mechanisms employed by Trichoderma species in the
biological control of plant diseases: the history and evolution of
current concepts. Plant Disease 87, 410.
Howell, C.R., 2006. Understanding the mechanisms employed by
Trichoderma virens to effect biological control of cotton diseases.
Phytopathology 96, 178180.
Howell, C.R., Puckhaber, L.S., 2005. A study of the characteristics of P
and Q strains of Trichoderma virens to account for differences in
biological control efficacy against cotton seedling diseases. Biological
Control 33, 217222.
Howell, C.R., Stipanovic, R.D., 1983. Gliovirin, a new antibiotic
from Gliocladium virens, and its role in the biological control
of Pythium ultimum. Canadian Journal of Microbiology 29,
321324.
Howell, C.R., Stipanovic, R.D., Lumsden, R.D., 1993. Antibiotic
production by strains of Gliocladium virens and its relation to the
biocontrol of cotton seedling diseases. Biocontrol Science and
Technology 3, 435441.
Howell, C.R., Hanson, E.L., Stipanovic, R.D., Puckhaber, L.S., 2000.
Induction of terpenoid synthesis in cotton roots and control of
Rhizoctonia solani by seed treatment with Trichoderma virens.
Phytopathology 90, 248252.
Khan, J., Ooka, J.J., Miller, S.A., Madden, L.V., Hoitink, H.A.J., 2004.
Systemic resistance induced by Trichoderma hamatum 382 in cucumber
against Phytophthora crown rot and leaf blight. Plant Disease 88,
280286.
Krause, M.S., Madden, L.V., Hoitink, H.A.J., 2001. Effect of potting mix
microbial carrying capacity on biological control of Rhizoctonia
ARTICLE IN PRESS
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