TRICHODERMA SPECIES — OPPORTUNISTIC, AVIRULENT PLANT SYMBIONTS
Gary E. Harman*, Charles R. Howell‡, Ada Viterbo§, Ilan Chet§ and Matteo Lorito||
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 establishrobust 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 areprotected 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.
An axenic system comprises a single type ofmicroorganism.
*Departments of Horticultural Sciences and Plant Pathology, Cornell University, Geneva, New York 14456, USA. ‡ USDA/ARS, SPARC, College Station, Texas 77845, USA. § Weizmann Institute, Rehovot 76100, Israel. || Dipartimento di Arboricoltura, Botanica e Patologia Vegetale, Universita degli Studi di Napoli Federico II, and Istituto CNR-IPP, 100-80055 Portici, Italy. Correspondence to G.E.H.e-mail: email@example.com
Trichoderma spp. (BOX 1) are free-living fungi that are highly interactive in root, soil and foliar environments. It has been known for many years that they produce a wide range of antibiotic substances1 and that they parasitize other fungi (BOX 2). They can also compete with other microorganisms; for example, they compete for key exudates fromseeds that stimulate the germination of propagules of plant-pathogenic fungi in soil2 and, more generally, compete with soil microorganisms for nutrients and/or space3. Furthermore, they inhibit or degrade pectinases and other enzymes that are essential for plant-pathogenic fungi, such as Botrytis cinerea, to penetrate leaf surfaces4. These direct effects on other fungi are complex and remarkableand, until recently, were considered to be the bases for how Trichoderma spp. exert beneficial effects on plant growth and development. Research on these topics has generated a large body of knowledge, including the isolation and cloning of a range of genes that encode proteins of which some have antimicrobial activity. There are several recent reviews of these materials
and their mechanisms ofaction5–8, so they will not be covered here in any detail. This research has also produced several useful findings, including that genes that encode fungitoxic cell-wall-degrading enzymes can be used to produce transgenic plants that are resistant to disease9–11, and the discovery of enzymes that are useful in the bioprocessing of chitin12. However, it is becoming increasingly clear that ourunderstanding of the mechanisms of biocontrol has been incomplete. In addition to the ability of Trichoderma spp. to attack or inhibit the growth of plant pathogens directly, recent discoveries indicate that they can also induce systemic and localized resistance to a variety of plant pathogens (TABLE 1). Moreover, certain strains also have substantial influence on plant growth and development. Theirenhancement of plant growth has been known for many years and can occur in both AXENIC systems13,14 and natural field soils15,16. These new findings are dramatically changing our knowledge of the mechanisms of action and uses of these fungi. We now consider that the direct effects of
VOLUME 2 | JANUARY 2004 | 4 3
NATURE REVIEWS | MICROBIOLOGY
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