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Trichoderma species — opportunistic, avirulent plant symbionts

Key Points

  • Trichoderma spp. are free-living fungi that are common in soil and root ecosystems. These fungi are well known for their ability to produce a wide range of antibiotic substances and for their ability to parasitize other fungi.

  • Until recently, these direct effects on other fungi were thought to be the basis for the beneficial effects of Trichoderma spp. on plant growth and development. However, recent evidence indicates that many Trichoderma spp., including Trichoderma virens, Trichoderma atroviride and Trichoderma harzianum, can induce both localized and systemic resistance in a range of plants to a variety of plant pathogens, and certain strains can also have substantial influence on plant growth and development.

  • When propagative Trichoderma structures, such as spores, are added to soil, they come into contact with plant roots and can germinate and grow on root surfaces, and some Trichoderma strains can infect the outer few root cells. Trichoderma spp. produce at least three classes of compound that elicit plant defence responses: peptides, proteins and low-molecular-weight compounds.

  • Induced resistance by Trichoderma spp. increases the expression of defence-related genes throughout the plant, at least in the short term, and is therefore similar to systemic acquired resistance (SAR). For one interaction — that between T. asperellum and cucumber — a longer-term response has elements in common with rhizobacteria-induced systemic resistance (RISR).

  • Root colonization by Trichoderma spp. also frequently enhances root growth and development, and can therefore improve crop productivity. The greatest long-term effects on productivity are probably associated with rhizosphere-competent strains. These responses are often the result of direct effects on plants, decreased activity of deleterious root microflora, and inactivated toxic compounds in the root zone. Trichoderma spp. also increase nutrient uptake and the efficiency of nitrogen use, and can solubilize nutrients in the soil. At present, the genetic and molecular bases of these effects are unknown.

Abstract

Trichoderma spp. are free-living fungi that are common in soil and root ecosystems. Recent discoveries show that they are opportunistic, avirulent plant symbionts, as well as being parasites of other fungi. At least some strains establish robust and long-lasting colonizations of root surfaces and penetrate into the epidermis and a few cells below this level. They produce or release a variety of compounds that induce localized or systemic resistance responses, and this explains their lack of pathogenicity to plants. These root–microorganism associations cause substantial changes to the plant proteome and metabolism. Plants are protected from numerous classes of plant pathogen by responses that are similar to systemic acquired resistance and rhizobacteria-induced systemic resistance. Root colonization by Trichoderma spp. also frequently enhances root growth and development, crop productivity, resistance to abiotic stresses and the uptake and use of nutrients.

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Figure 1: Features of induced resistance caused by Trichoderma species.
Figure 2: Effects of root colonization by Trichoderma T-22 on induced systemic resistance and plant growth.
Figure 3: Interactions of Trichoderma asperellum T-203 with cucumber roots, and effects of these interactions.

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Acknowledgements

We are grateful to K. Ondik and T. Björkman for suggestions and corrections, to R. Bostock for use of the illustration in Box 3, to J. Bissett for contributions to the text in Box 1, to G. Samuels for helpful discussions and to T. Xu for unpublished information on his research on rice. This work was supported in part by the US–Israel Binational Agricultural Research and Development Fund (G.E.H. and I.C.), the Cornell Center for Advanced Technology and Advanced Biological Marketing and BioWorks, Inc. Research by M.L. was supported by the following projects: FIRB-MIUR 2002; PON-MIUR 2002; EU TRICHOEST; Project EU FAIR 98PL-4140; MIUR-MIPAF 2002; and MIUR PRIN 2002.

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Correspondence to Gary E. Harman.

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Competing interests

G. E. Harman is co-founder, co-principal investigator and a shareholder in BioWorks, Inc., which manufactures and sells Trichoderma harzianum strain T-22, and is a co-principal inventor, consultant and shareholder in Advanced Biological Marketing, which sells T-22 to the field-crop market.

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DATABASES

Entrez

Avr4

Avr9

NPR1S

Glossary

AXENIC

An axenic system comprises a single type of microorganism.

TELEOMORPH

The sexual form of a fungus.

HETEROKARYOTIC

A fungus or other organism that contains multiple types of nucleus.

RHIZOBACTERIA

Bacteria that are commonly associated with, and colonize, roots.

MYCORRHIZAL FUNGI

Mycorrhizae are associations (usually mutualistic) between a fungus and the root of a plant, and are found in most plants. The fungi associate with the primary cortex of the root.

MYCOPARASITISM

Parasitism of one fungus by another fungus.

ANTIBIOSIS

Strains acting through antibiosis produce antifungal metabolites.

DICOTYLEDONOUS PLANTS

Flowering plants, the seedlings of which have two seed leaves (cotyledons).

MONOCOTYLEDONS

Flowering plants that have only one seed leaf (cotyledon).

APPRESSORIA

Specialized pressing organs from which a minute infection peg can grow and infect a cell.

PHYTOALEXINS

Low-molecular-weight compounds that have antimicrobial activity and are produced by plants in response to attack by pathogens.

XENOBIOTIC

A chemical that is present in a natural environment that does not normally occur in nature.

PETIOLE

A slender stem that supports a leaf.

ENDOPHYTE

A non-pathogenic organism living within a plant.

PHYLLOSPHERE

The area immediately adjacent to a root surface.

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Harman, G., Howell, C., Viterbo, A. et al. Trichoderma species — opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2, 43–56 (2004). https://doi.org/10.1038/nrmicro797

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