levels of an extracellular exochitinase. Diffusion of this enzyme
catalyzes release of cell wall fragments from target fungi and this,
in turn, induces expression of fungitoxic cell wall degrading enzymes
(8) that also diffuse and begin the attack on the target fungi
before contact is actually made (42,48). These cell wall fragments
are highly potent inducers of enzymes and induce a cascade of
physiological changes within the fungus, including an enhancement
in Trichoderma growth. This system will be described more
fully in this session by Lorito. Thus, there are numerous ways by
which Trichoderma spp. attack or otherwise directly inhibit other
fungi.
However, the direct effects of Trichoderma spp. on plants are
remarkable and at least as significant as their direct effects on
other fungi and have only recently been described. First, the fungi
are highly efficient inducers of systemic and localized resistance
in plants, a fact perhaps first conclusively demonstrated by
Bigirimana et al. (5) although it was suggested by numerous other
workers earlier. A recent review lists 11 separate reports demonstrating
control by Trichoderma spp. of a wide range of plant
pathogens, including fungi, oomycetes, bacteria, and one virus, by
elicitation of induced systemic or localized resistance (21). The
fungi, especially rhizosphere competent ones, colonize root surfaces
and penetrate the epidermis and into the cortex (46). Along
the way, the fungi may coil about root hairs in a manner reminiscent
of mycoparasitism (46). Once Trichoderma hyphae penetrate
the roots, a series of bioactive metabolites from the fungus is
produced that induces walling off and biochemical mechanisms
that limit growth of the Trichoderma to a small area. This reaction
may not always occur; for example, there now are known endophytic
Trichoderma strains that colonize vascular systems of certain
plants, as will be discussed elsewhere in this session
(Samuels). This may be similar to responses of other root colonizing
biocontrol fungi including binucleate Rhizoctonia species (29)
and nonpathogenic Fusaria (3). The bioactive molecules may include
several different proteins (19), avr-like proteins and cell
wall fragments released by action of extracellular enzymes, as has
been demonstrated in the mycoparasitic reaction (21).
This interaction results in both localized and systemic resistance
(21). Among other surprising findings are the demonstration
that, contrary to long-held opinion, the ability of T. virens to control
seedling disease in cotton caused by Rhizoctonia solani is not
due to antibiotics or mycoparasitism but is mediated by the abilities
of the biocontrol strains to induce terpenoid phytoalexins
(28), as will be discussed in this session. T. virens on cotton results
in localized resistance, but with most other plant–Trichoderma
systems, the resistance induced is systemic (21).
The systems for induced resistance appear to be in at least some
ways similar to those induced by rhizobacteria. Yedidia et al. (47)
demonstrated that mRNA for pathogenesis-related (PR) proteins
was only expressed transitorily in the absence of pathogens. However,
if leaves of beans whose roots were colonized by Trichoderma
were inoculated with the bacterial pathogen Pseudomonas
syringae pv. lachrymans, there was strong expression of mRNA
for several different PR proteins. If either the pathogen alone was
inoculated onto foliage or T. asperellum was not present on roots,
then the induction of the PR transcriptomes did not occur, or
occurred at a lower rate (21,47). Thus, in common with the effects
of plant growth promoting rhizobacteria, there appears to be a
priming effect of the root symbiont that is expressed when the
plant is challenged by a pathogen.
The resistance induced may be temporally and spatially distant
from the site of application or existence of the Trichoderma.
For example, T. harzianum strain T22 (41) was added at transplanting
to tomato roots. After 90 to 120 days, symptoms of
late blight appeared on the leaves, but in trials over 2 years, there
was up to 80% reduction in disease in the presence compared
with the absence of T22 even though T22 was present only on
roots (21).