Papavizas 1985

ANNUAL
REVIEWS Further
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Ann. Rev. Phytopathol. 1985. 23:23-54
TRICHODERMA AND
GLIOCLADIUM: BIOLOGY,
Annu. Rev. Phytopathol. 1985.23:23-54. Downloaded from www.annualreviews.org
ECOLOGY, AND POTENTIAL FOR

BIOCONTROL 1
by University of Sussex on 09/18/12. For personal use only.
G. C. Papavizas
Soilborne Diseases Laboratory, Plant Protection Institute, Agricultural Research Ser

vice, US Department of Agriculture, Beltsville, Maryland 20705
INTRODUCTION
The three decades that followed the pioneering work of Weindling (149, 150)
on Trichoderma and Gliocladium were marked by blurred efforts to promote
the idea that these two fungi have the potential to be effective agents for
biocontrol. The last few years, however, have witnessed a dramatic increase in
research efforts, and several recent review articles (123, 136) and books (26,
117) consider the use of specific microorganisms for the biocontrol of plant
diseases. Yet, no reviews deal specifically with Trichoderma or Gliocladium.
An exception is Rifai's taxonomic treatise of the genus Trichoderma (133),
which clarifies some of the taxonomic confusion about this genus .
The many recent advances described in this review have taken place in only
the last six or seven years and indicate that biocontrol of plant pathogens can be
successfully exploited. It is difficult to predict the full extent to which research
on Trichoderma and Gliocladium will develop over the next few years. Howev
er, the initial momentum is evident and some practical results are beginning to
appear. Because of space limitations, this review will focus on information that
may have an effect on practical biocontrol, with the understanding that many
important research articles have been left out.
lThe u.s. Government has the right to retain a non-exclusive, royalty-free license in and to any
copyright covering this paper.
23
24 PAPAVIZAS
BIOLOGY
Biosystematics and Morphology
The more extensive and complex the involvement of Trichoderma and Gliocla
dium in biocontrol, the more useful and necessary is their accurate classifica
tion . Unfortunately, the taxonomy of the genera has been in disarray for most of
the last half century. In 1969 Rifai (133) distinguished nine species aggregates
based on microscopic characters . Other stUldies on the biosystematics and
morphology of the genus and detailed studies on the relationship between the
anamorph (Trichoderma) and the teliomorph (Hypocrea) can be found else
where (26, 37, 38). The taxonomy and morphology of the genus Gliocladium
has also been discussed by others (38, 105) and there is no need to elaborate
further here.
Growth, Morphogenesis, and Sporulation in Culture

Studies on the growth, morphogenesis, and sporulation of Trichoderma and
Gliocladium in vitro can be useful if the information derived from such studies
can be used to develop the technology for the large-scale production of biomass
for use in biocontrol. This review refers to Trichoderma only, since no direct
information on the growth and sporulation of Gliocladium is available. Because
of early confusion about taxonomy , however, some research reportedly on the
growth and sporulation of Trichoderma might actually have been conducted on
Gliocladium.
GROWTH As expected with saprophytic soil fungi, species of Trichoderma

use a wide range of compounds as sole carbon and nitrogen sources . The carbon
and energy requirements of Trichoderma can be satisfied by monosaccharides
and disaccharides (30); complex polysaccharides, purines, pyrimidines , and
amino acids (146); condensed tannins and catechins (3); aldehydes and organic
acids, particularly long-chain fatty acids (E.. B . Nelson, G. E. Harman, un
published data); and even methanol, methylamine, and formate (146).
Although ammonium appears to be the most readily utilized source of
nitrogen by Trichoderma spp. in buffered media (30), other sources of ni
trogen, such as amino acids, urea, nitrate, and even nitrite, support abundant
vegetative growth (30). The role of salts , sulfur sources, and compounds such
as vitamins as growth-affecting ingredients has largely been ignored. A few
papers make it clear that inorganic salts may be very important for growth .
Several salts , those of magnesium, for instance, increased growth of T. viride
(137). In contrast, growth and pigment deve:lopment by seven species aggre
gates of Trichoderma was slower when 5% sodium chloride was added to a
culture medium (55).
There has also been considerable interest in the effects of CO2 on the in vitro
TRICHODERMA AND GLIOCLADIUM 25
growth of Trichoderma and the implications of such effects on the ecology of

the antagonist in soil. Most investigators agree that the response to CO2 varies
with the species aggregate tested (29 , 97) . The effects of CO2 on growth,
however, have been variable and appear to depend on CO2 concentration and
medium pH (29, 97) . Other investigators have found that Trichoderma is
relatively unaffected by CO2 levels up to 10% ( 1 9). The rapid growth of
Trichoderma at high CO2 concentrations in alkaline media may explain why
Trichoderma, a normally acidophilic soil inhabitant, abounds in very wet,
slightly basic habitats (127). Also, since the effect of CO2 on growth is most
pronounced at high pH values, it can be ascribed to the bicarbonate ion (HC03)

rather than to the CO2 directly. In fact, some investigators have presumed that
HC03 has a greater effect on growth than CO2 does (29, 97) .
MORPHOGENESIS Turian (145) recently defined morphogenesis as "the de

velopment of an organism to its specific form." For Trichoderma and Gliocla
dium, this concept implies the differentiation of their cells into types that vary in
their size, shape, structure, function, and chemical composition. Many aspects
of Trichoderma morphogenesis are covered in a recent review article (59) .
Sporulation Most species of Trichoderma are photosensitive, sporulating

readily on many natural and artificial substrates in a concentric pattern of
alternating rings in response to diurnal alternation of light and darkness, with
conidia being produced during the light period (58). Exposure of agar cultures
for 20 to 30 seconds to light of 85 to 90 lux intensity is usually sufficient to
induce some sporulation. The best photoinduction of phialoconidiogenesis has
been obtained with exposure to daylight for three minutes or to near ultraviolet
(UV) radiation (366 nm) for 1 0 to 30 seconds (15). Pronounced synthesis of
DNA, RNA, and protein also have been found after photoinduction. Some
researchers (58) observed maximum photoinduction activity at around 380 nm
and at 440 nm, with sporulation not occurring below 254 nm or above 1,1 00
nm. The photoinduced conidiation in Trichoderma can be inhibited by chemi
cals. Compounds such as azaguanine, 5-fluorouracil, actinomycin D, cyc
loheximide, phcncthyl alcohol, and ethidium bromide ( 1 5 , 59) inhibit photoin
duced sporulation partially or fully in surface-growing colonies and in sub
merged cultures of T. viride without inhibiting growth. Inhibitors of membrane
functions do not exhibit such an effect.
An important aspect of sporulation almost completely disregarded in the last
50 years is the ability of Trichoderma and Gliocladium to produce chlamydo
spores. Although chlamydospores are routinely mentioned in taxonomic papers
(38, 1 33), very little has been reported on the formation and ecological im
portance of these structures or their potential role in biocontrol. Recent research
(89, 90) has demonstrated the formation of chlamydospores by T. hamatum, T.
26 PAPAVIZAS
harzianum, T. viride, and G. virens in both liquid and solid fermentation

media, in sterile soil and soil extracts, and in natural plant debris and amended
natural soil.
Germination Although many reports have appeared on sporulation in

Trichoderma and on the role of light and various chemicals as inducers and
inhibitors respectively, the molecular and biochemical processes involved in
germination have largely been ignored. This is perhaps due to the ease with
which conidia of Trichoderma and Gliocladium germinate on many substrates,
perhaps to other reasons. The few papers available indicate that conidia of
Trichoderma require an external source of nutrients for germination in vitro
(31). Normally, washed conidia do not germinate in distilled water. Unwashed
conidia or unwashed agar contribute enough nutrients to initiate and support

germination. The response of conidia to nutrients is affected by the H-ion
concentration, with germination being greater under acid conditions than under
neutral conditions (31).
Even less is known about the germination of chlamydospores in vitro.
Although fresh chlamydospores germinate well (approximately 75%) on nutri
ent agar (89), only 13 to 31% of chlamydospores from air-dried preparations
germinate, despite their apparent viability as determined with tetrazolium
bromide. This suggests that the dried chlamydospores (expected to be found in
biocontrol preparations) may be dormant but become germinable under appro
priate conditions. Considerable research is still needed on several aspects of
chlamydospore biology, including their ecological importance and long-term
survival and the factors that enhance their formation. It is possible, but un
known, whether these propagules ensure the continued survival of the two
genera in soil under adverse conditions not conducive to the survival of the
smaller, ephemeral, single-walled conidia.
Metabolite Production
Our first knowledge of toxic metabolite production by species of Trichoderma
and Gliocladium is largely due to Weindling (149-151), who showed the
production of an antifungal metabolite by T. lignorum [later stated to be G.
jibriatum (151)]. Weindling & Emerson (152) isolated in crystalline form an
organic metabolite very toxic at high dilultion to Rhizoctonia solani. The
metabolite was later given the trivial name of gliotoxin (151). Brian & McGow
an (17) described a second highly fungistatic antibiotic, viridin, produced by T.
viride. Webster & Lomas eventually questioned (148) whether the gliotoxin
reported by Weindling & Emerson (152), and the viridin reported by Brian &
McGowan (17), were actually produced by Trichoderma. They (148) were
unable to show production of the two antibiotJics in culture filtrates of T. viride.
Reexamination of Weindling's gliotoxin-producing isolate and of the isolate
from which Brian & McGowan originally obtained (17) viridin showed that
these were not T. viride (Hypocrea rufa) but actually matched the type isolate of
G. virens (H. gelatinosa).
Almost 30 years after the discovery of gliotoxin and viridin, interest has been
renewed in toxic metabolites produced by species of Gliocladium and
Trichoderma and in the role they may play in biocontrol. Recently, Howell &
Stipanovic (72) reported on the isolation and structure of a new toxic metabolite
from G. virens, a diketopiperazine (139) given the trivial name of gliovirin, that
is active against Pythium spp.
The early attempts to obtain and characterize toxic metabolites from

Trichoderma spp. employed very simple techniques. Improvements followed
the introduction of various new techniques in metabolite production that had
been used successfully in industrial microbiology. These improvements, cou
pled with clarification of the Trichoderma taxonomy (133), resulted in a

renewed interest in the abi lity of Trichoderma spp. to produce toxic metabo
lites. Dennis & Webster (36) showed that Trichoderma spp. produce antibiotics
different from gliotoxin and viridin. Although they were unable to show
production of gliotoxin and viridin by nine species aggregates of Trichoderma,
they showed production of other chloroform-soluble antibiotics such as
trichodermin (by T. viride and T. polysporum) and other peptide antibiotics by
T. hamatum. They did not exclude the possibility, however, that gliotoxin and
viridin are also produced in low concentrations by Trichoderma isolates.
Papavizas et al (122) found that several UV-induced mutants of T. harzianum
produce two unidentified metabolites, one heat-labile, the other heat-stable.
Trichodermin, the least structurally complicated sesquiterpenoid metabolite,
originally described by Godtfredsen & Vangedal (57) from Trichoderma,
should not be confused with trichodermin-4 reported in the literature (52). This
so-called antibiotic is a crude preparation produced by growing T. lignorum (T.
viride?) on concentrated solid protein-carbohydrate media or liquid molasses
media, drying the preparations, and grinding the biomass, including the solids
from the media.
Trichoderma and Gliocladium are not only good sources of various toxic
metabolites and antibiotics, but also of various enzymes such as exo- and
endoglucanases, cellobiase, and chitinase. This review will focus only on
recent information dealing with enzymes implicated in the mechanism of action
of biological control.
ECOLOGY
Understanding the ecological factors affecting the distribution of Trichoderma

and Gliocladium in their natural habitats may lead to an understanding of the
population dynamics of the two antagonists in soils and other habitats and of
28 PAPAVIZAS
their survival and proliferation in soil and the rhizosphere. For this reason, a
careful analysis of the behavior of these two fungi in the soil ecosystem may be
worthwhile.
Occurrence and Distribution

Trichoderma and Gliocladium are widely distributed all over the world (38) and
occur in nearly all soils and other natural habitats, especially in those containing
or consisting of organic matter. Individual species aggregates may be restricted
in their geographic distribution (28). Trichoderma seems to be a secondary
colonizer, as its frequent isolation from well-decomposed organic matter in

dicates (28). Trichoderma is also found on root surfaces of various plants (125);
on decaying bark, especially when it is damaged by other fungi (28); and on
sclerotia or other propagules of other fungi (32, 1 53) . Qualitative studies on the
distribution and occurrence of individual speciies aggregates were hampered by
taxonomic uncertainties prior to 1969 (133) and by the lack of precise tech
niques and culture media for their isolation and enumeration. Because of these
difficulties, most of the present discussion on OCCUrrence and distribution,
especially that referring to literature published before 1969, refers to the genus
level only.
The ecological preferences of Trichoderma are discussed in the com
prehensive reviews of Danielson & Davey (28, 29, 31). When dry conditions in
soil are maintained for long periods of time, populations of Trichoderma and
Gliocladium as a group decrease (33, 34). Danielson & Davey (28) also
concluded that certain strains of T. hamatum and T. pseudokoningii are adapted
to conditions of excessive soil moisture and that T. viride and T. polysporum are
restricted to areas where low temperatures prevail, whereas T. harzianum is
most commonly found in warm climatic regions and T. hamatum and T.
koningii are widely distributed in areas of diverse climatic conditions. Addi
tional suggested physical and chemical determinants are the heterogeneity of
species aggregates, soil pH, chemical properties, CO2, HC03, salt and organic
matter content, and the presence or absence of other microorganisms in soil.
The iron content of the soil may also be an important determinant of the
microsite preference of Trichoderma; a recent study (74) showed that soil
pseudomonads limited the efficacy and establishment of T. hamatum in soil and
rhizosphere containing little available iron.
Isolation and Enumeration

Although there have been numerous attempts to study the occurrence and
distribution of Trichoderma and Gliocladium in their natural habitats, few
workers have attempted quantitativ� studies of their population dynamics and
survival in soil and other habitats. Until recently, the scarcity of information on
the survival of the antagonists in soil was due in part to the lack of precise
techniques and the appropriate culture media for isolation and enumeration
(116). A selective medium containing allyl alcohol and the fungicide vindozo
lin (33), modified with the addition ofigepal CO 630 (E. B. Nelson, W. Chao,
G. E. Harman, unpublished data), is claimed to be satisfactory for isolation, but
the medium must be prepared immediately before use because of the volatility
of allyl alcohol. Rose bengal and pentachloronitrobenzene (PCNB) were used
together with captan as the basic antimicrobial agents for developing a semi
selective medium for the quantitative isolation of Trichoderma from soil (42).
A new semiselective medium with neither rose bengal nor PCNB has also been
described for the isolation and enumeration of Trichoderma spp. from soil and
plant rhizosphere (116). The new Trichoderma medium E (TME), with or
without benomyl, gave good results with soils that did not contain rapidly
spreading fungi such as Mucor and Rhizopus (1, 116). The TME was further
improved with the addition of alkylaryl polyether alcohol (124) and was used
effectively to recover Trichoderma and Gliocladium from soil, rhizosphere,
and other habitats with the dilution-plate method. The addition of benomyl
makes the medium selective for the isolation and enumeration of mutants
resistant to the fungicide.
Population Dynamics in Soil

SURVIVAL IN SOIL The abundance of Trichoderma, and to a lesser extent of
Gliocladium, in various soils, coupled with their ability to degrade various
organic substrates in soil, their metabolic versatility, and their resistance to
microbial inhibitors, suggests that they may possess the ability to survive in
many ecological niches depending on prevailing conditions and the species or
strain involved. This assumption may blur the distinction between passive
survival and active competitive saprophytic ability, including the dynamic
colonization of plant rhizosphere. Such considerations can be elucidated more
readily with introduced isolates than with static, natural populations of
Trichoderma or Gliocladium.
Very little is known about the fate of conidia and chlamydospores of
Trichoderma added to soil or to any other environment. Some of the conidia of
T. harzianum added to soil without nutrient-supplying amendments survived
between 110 and 130 days, but the length of survival depended on the isolate
used (116, 122). Most of the conidia were probably lysed without first
germinating, or they germinated in response to some nutrients released from
organic matter and subsequently lysed in the absence of food bases adequate
enough to sustain further growth and sporulation. In other studies, conidia
added to soil decreased initially, then stabilized for two years to about one-tenth
the original number added (33). Hyphae also survive in soil (119).
Although the ecological importance of chlamydospores has been disregarded
30 PAPAVIZAS
in the past, there is now evidence for their importance in the survival of the two
genera in soil. Caldwell (20) was among the first to observe that chlamydo
spores survive in soil better than conidia. Recently, Lewis & Papavizas (90)
demonstrated the potential of various Trichoderma species aggregates to form
chlamydospores readily and in great numbers in natural soil or in fragments of
organic matter after the introduction of the fungus to the soil as conidia. They
suggested that introduced isolates have the potential and aggressiveness to
colonize and establish themselves in organic matter in natural environments. If
chlamydospores can be demonstrated to survive in soil for extended periods ,
the ecological importance of these structures would be significant.
SOIL FUNGIGTASIS The fungistatic nature of soil (95) and our ability to annul
or enhance soil fungistasis (123) may have considerable impact on the survival
and popUlation dynamics in soil of natural and introduced species of
Trichoderma and Gliocladium. Trichoderma conidia have been found to be
either very sensitive to fungi stasis (95) or to be relatively insensitive (102).
Sensitivity to fungistasis was more pronounced in neutral or alkaline than in
acid soils (31). Various organic substrates added to soils partially or completely
reverse fungistasis, with the reversal being more pronounced in acid than in
alkaline soil (95). A relationship also seems to exist between the kind or size of
propagule of Trichoderma and its sensitivity to fungistasis; conidia are ex
pected to be more sensitive than the larger c:hlamydospores and hyphae less
sensitive than conidia (95). The sensitivity of chlamydospores is only a con
jecture, however , since we know very little about their behavior in soil.
Schippers et al (135) recently advanced an intriguing aspect of soil fungista
sis in relation to Trichoderma and Gliocladium conidia that involves volatile
substances. They presented evidence that ammonia is fungistatic to conidia of
the two genera in alkaline soils and that species aggregates differ in their
sensitivity to gases in soil atmosphere and to ammonia released from soil. Even
ammonia at I J.Lg/g of air is fungistatic to conidia of T. hamatum and T.
koningii, but not to those of T. harzianum or G. roseum. They postulated that
the success of T. hamatum as a biocontrol agent may be limited by con
centrations of ammonia in soil. However , ammonia affects certain species
aggregates of Trichoderma in alkaline soils only; this observation is interesting
but may be a special case unrelated to the main mechanisms of soil fungistasis
(95). Nothing is known about the effects of volatile substances on Trichoderma
or Gliociadium chlamydospores.
One of the most striking natural events associated with spore germination in
soil, or the lack of it, is the enhanced survival of antagonists because of the
dormancy imposed on their spores by fungistasis (95, 123). With most fungi,
including Trichoderma and Gliocladium, fungistasis is a natural mechanism of
preservation. Caldwell (20) noticed that conidia and chlamydospores added to
various fungistatic soils survived as long as 20 months. However, a progressive

breakdown of propagules, especially conidia, took place. In assessing the
potential of soil fungistasis for the biocontrol of soilborne pathogens with
Trichoderma or Gliocladium, therefore, it is fairly obvious that the prospects of
control by maintaining or elevating the levels of fungistasis to the antagonists
are less promising than the prospects of control by manipulating the soil
environment to reduce or annul fungistasis to the antagonists.
If we realize that fungi stasis hinders spore germination of Trichoderma or
Gliocladium in soil, and therefore hinders growth and sporulation (prolifera
tion) but does not prevent the slow attrition of propagules, a possible approach
to biocontrol may be to reduce fungistasis to Trichoderma and Gliocladium
spores following their addition to soil. This can be achieved by any of several
approaches. Energy sources and other organic materials may be added to soil
initially to reduce or completely annul fungistasis (95 , 123). Even a temporary

annulment, no matter how temporary it may be, coupled with a simultaneous
enrichment with a food base, would allow spores to germinate and the fungus
theoretically to proliferate in soil. On the other hand, the addition of a food base
along with the propagules may allow spores to germinate, but subsequent
growth may not occur. Recent unpublished studies (G. C. Papavizas, un
published data) have shown that organic amendments of various carbon!
nitrogen ratios, mono-, di-, and polysaccharides, nitrogen sources, and iron
chelates do not allow proliferation of the fungus when conidia of T. hamatum,
T. harzianum, and T. viride are added to soil together with the amendments. A
possible explanation for this is suggested by the results of Nelson et al (111),
who found that the proliferation of Trichoderma in soil is influenced by the
degree of decomposition of hardwood bark compost. Trichoderma populations
do not change in soil in response to green compost but increase greatly in
response to mature compost. In addition, organic substrates may be colonized
and exploited more rapidly by pathogenic or saprophytic fungi possessing high
competitive saprophytic ability than by the antagonists (123). Kelly (79) found
that excess nutrients (molasses) in granules containing T. harzianum can be
used rapidly by Phytophthora cinnamomi when growth of the antagonist is
suppressed by lack of oxygen. This results in a net increase of the pathogen
rather than of the antagonist.
ESTABLISHMENT AND PROLIFERATION IN SOIL Selective passive or active

possession and exploitation of substrates by soil microorganisms may be
determined by various factors (18), and in many instances these factors may not
be favorable for Trichoderma or Gliocladium. Several new approaches have
recently been proposed to overcome this difficulty. Lewis & Papavizas (93)
showed that Trichoderma, Gliocladium, and other potential biocontrol fungi
proliferate abundantly in various natural soils when added as young mycelia in
32 PAPAVIZAS
intimate contact with a food base (sterile moist bran inoculated with conidia and
allowed to incubate for one to three days before addition to soil), but not as
conidia with or without bran. Proliferation (up to 106-fold) and subsequent
establishment in soil (population levels remain constant from nine to 36 weeks
after the colonized food base is introduced) depend on inoculum age and how it
is added in relation to the food base. The thorough colonization [possession in
Bruehl's sense ( 1 8)] of the food base by the mycelia enables Trichoderma or
Gliocladium to grow relatively unimpeded through the soil.
Thorough primary colonization of a substrate by Trichoderma or Gliocla
dium before addition to soil may not be the only approach to overcoming
secondary colonization of the food base by soil microorganisms and of enhanc
ing the chances for antagonist establishment and proliferation. Alginate pellets
containing ground dry or wet fermentor biomass preparations of Trichoderma
or Gliocladium thoroughly established in a food base (bran) also stimulate a

great increase in populations (91). Pellets wilth conidia are less effective than
those prepared with ground biomass (mostly chlamydospores). In addition,
ground fermentor biomass of Trichoderma or Gliocladium added to soil as a dry
Pyrax® (anhydrous aluminum silicate) fommlation appeared to proliferate
greatly (119), increasing from an initial amount of 5 x 103 to a maximum of
6-7 x 106 conidialg of soil. In contrast, the numbers of conidia added to soil or
to a soilless mix without nutrients remained constant for 10 to 20 days and then
declined.
The unique ability of young hyphae but not of conidia of Trichoderma or
Gliocladium to proliferate from a thoroughly colonized substrate or from
alginate pellets may be due in part to their insensitivity to fungistasis. Hyphae
are known to be less sensitive to fungistasis than spores (95). Although there is
skepticism on the importance antibiotics or other toxic metabolites play in soil
ecology, there is now some evidence that such metabolites play a role in active
possession of substrates (18). If the young, vigorous hyphae produce toxic
metabolites when in active possession of a substrate, they may be able to
establish territorial rights using such substances to succeed in those rights (18).
Soil chemical treatment The microbiologieal balance of the soil, often re
ferred to as dynamic equilibrium, is subject to alterations mediated by various
environmental factors, including the application of pesticides or other chemical
substances. Heat or chemical treatments that eliminate groups of microorga
nisms undoubtedly create a partial biological vacuum in the soil (8), the
magnitude of which depends on the kind of Itreatment. If any alteration of the
microbiological balance, temporary though it may be, favors certain in
digenous or introduced strains of Trichoderma or Gliocladium antagonistic to
plant pathogens, diseases may be suppressed. The literature on the nontarget
effects of soil chemical treatments on Gliocladium, and especially on
Trichoderma, is so voluminous that a special review is required. Most of the

pertinent information can be found in several books or review articles (26, 86,
106, 107, 134) and key publications (51, 80, 92, 100, 101 , 114).
Indigenous or introduced Trichoderma is known to have greater tolerance for
broad-spectrum biocides than many other soil microorganisms and to colonize
the treated soil more rapidly than other soil competitors (106). Trichoderma
was the dominant recolonizer of substrates in a carbon disulfide-treated soil
(16) or in formaldehyde-treated soil (5 1). The antagonist not only predominated
in soil three weeks after fumigation with dilute formaldehyde or carbon di
sulfide but also persisted for at least six months after fumigation. The applica
tion of sodium azide to soil also resulted in the development of a large
population of native Trichoderma (80). The dominance of Trichoderma in soil
following the application of biocides is probably due to its inherent resistance to
most biocides and to its ability to rapidly colonize substrates in the absence of
significant competition from other microorganisms.
Dominance by Trichoderma of the ecological niches made available by
broad-spectrum biocides is not the only mechanism whereby the antagonist can
proliferate in soil and suppress disease. Biocides can stress, weaken , and render
pathogen propagules more susceptible to attack by the antagonists. As with
Armillaria mellea (114) , sublethal doses of soil fumigants may interfere with
the defense mechanisms of resting structures such as sclerotia so that they are
biologically degraded more rapidly in soil (101). Sclerotia of S. rolfsii
"weakened" by sublethal concentrations of metham-sodium became suscepti
ble to invasion and degradation by T. harzianum (68); T. harzianum alone did
not degrade fresh viable sclerotia.
Trichoderma, and presumably Gliocladium, do not always become domi
nant in soils treated with broad-spectrum biocides. This is particularly true in
compacted soil (51) or in soil augmented with Trichoderma after mild treat
ments (92). Lewis & Papavizas (92) recently showed that the number of
colony-forming units of T. harzianum and T. viride introduced four days
before, or at the time of fumigation with a sublethal rate of metham-sodium,
was significantly less than those in nonfumigated soil. The number of colony
forming units of isolates introduced four days after fumigation was similar to
that in nonfumigated soils. More interestingly, populations of introduced
isolates remained static in nonfumigated soils and those of indigenous
Trichoderma were unaffected by the levels of metham used. The addition of a
food base (bran) to the treated soil did not stimulate the introduced Trichoderma
to proliferate. Failure to proliferate was attributed (92) to a lack of appropriate
food bases in the soil, to the inherently poor colonizing ability of the isolates
used, and to the quantity and quality of the residual microflora in the metham
treated soils.
Very few positive effects of fungicide use on the proliferation of
34 PAPAVIZAS
Trichoderma in the soil can be found in the literature. A little over 20 years ago,
Richardson ( 1 32) showed that the fungicide thiram , used almost exclusively for
seed treatments, had a selective effect on Trichoderma and Penicillium; in
thiram-treated soil, Trichoderma consistently survived well and multiplied,
and it protected against Pythium on pea seedlings for a considerable time after
the fungicide reached levels not toxic to the pathogen. Similar beneficial effects
of thiram have been verified recently with T. harzianum (34). Interesting
nontarget effects on T. harzianum were also obtained with metalaxyl; the
infusion of pea seed with this fungicide before coating it with conidia of T.
harzianum improved the survival o f conidia and even increased the number
of colony-forming units in the rhizosphere compared with the number in the
rhizosphere from seed that received conidia only (11 6). Metalaxyl was not toxic
to T. harizanum in vitro, in contrast to the benzimidazole fungicides (e.g.

benomyl, thiabendazole, thiophanate methyl), which are deleterious to both
antagonists (122). Benomyl was strongly inhibitory to Trichoderma in culture,
even at concentrations as low as 0.5 mg per liter. Captan, chlorothalonil,
chloroneb, PCNB, and some new fungicides (iprodione, procymidone, vinclo
zolin) were not inhibitory to Trichoderma (1). Indirect evidence on the non
target effects of benomyl in soil was provided by Backman & Rodriguez
Kabana (6 , 7) , who showed that benomyl applied to control foliar diseases of
peanuts resulted in a lower yield because of more severe Southern stem blight
(S. rolfsii). Benomyl had no effect on the pathogen but was very toxic to
Trichoderma.
The dominance of Trichoderma following applications of sublethal rates of
pesticides is of special interest in biological control because of the ability of the
genus to proliferate in the treated environment as well as its demonstrated
ability to produce antibiotics, compete for nutJients , and act as a mycoparasite.
Despite our abundant knowledge about the ability of Trichoderma to dominate
treated environments, we have very little fundamental information on how
biocides affect the survival and population dynamics of Trichoderma and
especially of the long-neglected Gliocladium, on substrate preferences of these
fungi following biocide applications, on their resistance or tolerance to
biocides, on the mechanisms of "weakening" of pathogen structures by sub
lethal amounts of biocides, on fumigant-antagonist-pathogen-plant in
teractions , and on how to develop Trichoderma and Gliocladium strains resis
tant or tolerant to old and modem pesticides.
Soil treatments Treatment of soil with steam (9) , solaJization (78), and other
methods can also upset the ecosystem to the extent that it may allow the
proliferation of Trichoderma or Gliocladium. Sublethal heating of soil infested
with Armillaria mellea, for instance, stimulated the more heat-resistant resident
Trichoderma, which then proliferated and parasitized the weakenedA. mellea
( 107). Marois & Locke (99) recently suggested rapid recolonization of and
proliferation in steamed soil mixes of introduced T. viride as the reason for the
suppression of fusarium wilt of chrysanthemum (94) . Heat was the selective
treatment (6) that allowed T. viride to proliferate in soil or soil mixes and
successfully compete with Fusarium oxysporum f. sp. chrysanthemi.
ESTABLISHMENT IN THE RHIZOSPHERE Although Trichoderma and Gliocla

dium have been isolated from plant roots and there have been numerous
attempts to use them for the biocontrol of certain root diseases (26, 1 20), few
workers have tried quantitative studies on the survival, establishment, or

proliferation of the two antagonists in the plant rhizosphere. The effectiveness
of Trichoderma and Gliocladium as seed treatments is probably determined not
only by their biocontrol qualities but also by their abilities to multiply in the
rhizosphere when applied to seed. Trichoderma or Gliocladium introduced on

seed must multiply in the rhizosphere if they are to inhibit pathogens that infect
roots some distance away from the cotyledon attachment. If the Trichoderma
inoculum mUltiplies around the site of application, but not along the root
surfaces away from the cotyledon attachment, it may suppress pathogens
causing seed rot and seedling diseases, but not those that cause root diseases .
Recent studies ( 1 1 6) have shown that T. harzianum did not establish in the
rhizosphere of bean and pea seedlings grown from seed treated with conidia.
Even when the rhizosphere samples included the roots and decaying seed coats
and cotyledons, the number of colony-forming units recovered per gram of
rhizosphere soil was always considerably less than the number of conidia added
per individual seed, indicating failure to survive and/or sporulate in the rhizo
sphere. In addition, when conidia were added to the soil before planting but not
to the seed, the rhizosphere populations never exceeded those recovered from
nonrhizosphere soil, indicating no rhizosphere effect ( 1 1 6). Very few or no
colonies of T. harzianum were recovered from the rhizosphere soil from roots
removed 10 em away from the treated seed. In contrast, large numbers of
colonies were recovered when the rotting pea cotyledons and seed coats were
included in the rhizosphere samples. Lack of establishment or movement of
Trichoderma in plant rhizosphere was also observed (W.-L. Chao, G. E.
Harman, E. B. Nelson, unpublished data).
There are several possible explanations for the decline of added Trichoderma
inocula or the inability of the fungus to proliferate in the plant rhizosphere,
including lack of proper nutrients, the presence of toxic substances in the root
exudation, or the presence of antagonistic or competing microorganisms
(W.-L. Chao, G. E. Harman, E. B. Nelson, unpublished data) at the rhizo
sphere or rhizoplane level. Pseudomonas spp. may compete with the biocontrol
agent for iron in the rhizosphere (74) or produce metabolites toxic to
Trichoderma.
36 PAPAVIZAS
PRODUCTION AND DELIVERY SYSTEMS
One of the most critical obstacles to biocontrol by direct massive soil augmenta
tion or seed treatment with biocontrol fungi such as Trichoderma and Gliocla
dium has been the lack of knowledge of methods for mass culturing and
delivering the fungi. If the previously discussed studies on growth and sporula
tion are to produce results applicable to biocontrol , and if widespread control is
to be achieved with Trichoderma and Gliocladium, fermentation technology , in
the form of biopreparations containing spores , mycelia, or mixtures of the two,
must be developed to mass-produce the two antagonists rapidly. The past 30 to

40 years have seen considerable progress in fungal technology for the large
scale production of metabolites and industrial products (81 , 87). Consequently ,
it is possible that this technology can be adapted or transferred to Trichoderma
and Gliocladium.
Solid media for the experimental production of Trichoderma or Gliocladium
have frequently been used in laboratory and greenhouse studies. Such media
also have been tested in the field (35, 46, 50), and several were tabulated in a
recent review ( 1 20). In addition to those tabulated, additional substrates include
bark pellets (140), wheat-bran plus peat (138), barley grain (2), composted
hardwood bark (69, 1 10, I ll), and pellet formulations containing T. har
zianum and T. polysporum ( 1 30). Formulated products have also been de
veloped (but not yet registered) for applying T. harzianum to protect Acer
rubrum from hymenomycetes that enter through wounds ( 1 26). A Trichoderma
sp. was formulated in chainsaw oil (motor oil) and successfully inoculated on
pine stumps during tree cutting (75). Other examples of delivery include the
addition of Trichoderma or Gliocladium spores to soil with a liquid fertilizer if
the isolates used can tolerate high osmotic shock (J. M. Kraft, G. C. Papavizas,
unpublished data), or with seeding gels used for fluid drilling of small seeds
(53). A hitherto untested delivery system is the incorporation of Trichoderma or
Gliocladium spores with diluted liquid pesticides (e.g. metham) applied
through sprinkler irrigation. Spores of several isolates of T. hamatum, T.
harzianum, and T. viride can tolerate exposure t o metham i n solution u p t o 350
fl-g active ingredient/ml (92).
Deep-tank fermentation for the mass production of biomass of biocontrol
microorganisms is the technological approach most likely to be useful in the
United States. Growth media for liquid fermentation should include such
available inexpensive agricultural products as glucose, starch, hydrolyzed com
and soy products, whey, and molasses (81). Papavizas et al (119) have recently
shown that it is possible to use inexpensive liquid media such as molasses and
brewers yeast to produce viable inocula of the two antagonists with a deep-tank
fermentation system simulating large-scale industrial production; the two
organisms developed large amounts of biomass containing mycelia, chla-
TRICHODERMA AND OUOCLADIUM 37
mydospores, and some conidia after five to six days of incubation. A dry
formulation was prepared by air-drying the mats, grinding them, and diluting
the powder with the commercially available Pyrax® as a carrier. Although no
wettable powder formulations of Trichoderma or Gliocladium have ever been
reported, it should not be difficult to develop such formulations by using dry,
fine fermentation biomass and the proper wetting and suspending agents.
A recent development that may improve delivery technology for
Trichoderma and Gliocladium involves the encapsulation of propagules.
Encapsulation is based on the ability of aqueous solutions of sodium alginate to
react with certain metal cations (e.g. Ca++) to form gels. This process currently
is used to formulate chemical herbicides (147). The ease with which various
biocontrol fungi can be incorporated in sodium alginate gels in an aqueous
system was exploited by Walker & Connick (147) to prepare pelletized for
mulations of mycoherbicidal fungi and by Fravel et al (54) to prepare a

formulation of fungi antagonistic to plant pathogenic fungi. A further refine
ment of this technique is the incorporation of nutrient carriers (e.g. bran)
together with the alginate to provide a food base in intimate contact with the
antagonist (91).
PRODUCTION OF NEW STRAINS
Purposeful induction of tolerance or resistance to pesticides in Trichoderma or

Gliocladium and the selection of stable biotypes for use in combination with
pesticides is one of several options available for establishing an effective
control scheme that will encompass biological and chemical approaches to
single or multiple pest control. New biotypes of T. harzianum tolerant to
fungicides such as chlorothalonil, procymidone, iprodione, and vinc1oz01in
have been developed by exposing conidia to increasing concentrations of the
fungicides in culture media and then selecting surviving colonies for exposure
to even higher concentrations (1). Some biotypes with enhanced resistance to
fungicides survived longer in soil than the wild strains, but others were less
persistent in soil. A few selected biotypes showed enhanced ability to suppress
selected soilborne plant pathogens. However, several fungicide-tolerant
biotypes lost their ability to tolerate the fungicides after repeated transfers to
fungicide-free culture media. None of the isolates of T. harzianum used
developed tolerance to benomyl through prolonged exposure to increasing
concentration of the fungicide.
If the resistance to pesticides of Trichoderma and Gliocladium biotypes
results from nongenetic adaptation or training and is unstable, the development
of pesticide-resistant biotypes by genome modification may be a more promis
ing approach to biocontrol. Mutagenesis induced to increase enzyme produc
tion has been successful with strains of Trichoderma used in industrial micro-
38 PAPAVIZAS
biological processes (98, 103). Induced mutagenesis has also been used suc
cessfully with wild strains of T. harzianum and T. viride to develop new
biotypes (121, 122). These induced biotypes can tolerate between 50 and 500
f-tg benomyllml of medium. New biotypes differ from their respective wild
strains in growth characteristics and ability to sporulate, survive in soil, and
suppress the saprophytic activity of R. solani in soil. Several ultraviolet
induced biotypes were consistently more effective than the wild strains in
suppressing damping-off (Pythium ultimum) of peas, damping-off (R. solani)
of cotton and radish, damping-off and blight (Sclerotium rolfsii) of bean, and
white rot (Sclerotium cepivorum) of onion. One of the new benomyl-resistant

biotypes, T. viride (T-I-R9), deposited as NRRL 15165, was also effective
against fusarium wilt of chrysanthemum (94) and rhizoctonia scurf of potato
(13). Howell (71) has also produced mutants of G. virens that differ from wild
strains in their ability to produce the antibiotic gliovirin.

Considerable progress has been made in a very short time in developing new,
effective strains of Trichoderma and Gliocladium by adaptation and mutagene
sis. These attempts used very simple techniques that have been successful with
other industrial species of Trichoderma and other fungi. The application of
techniques for protoplast isolation and fusion and gene cloning will result in the
further development of new technologies for genetic manipulation of the two
fungi. This new area in biological control will undoubtedly receive increased
attention in the years ahead.
POTENTIAL FOR BIOCONTROL
In the Soil
ROLE OF THE INDIGENOUS POPULATION Before 1970, much of the work on

biocontrol involved the indirect enhancement of indigenous Trichoderma or
Gliocladium by manipulating the environm�mt. Yet the precise role of these
indigenous populations in the biocontrol of diseases is only a matter of specula
tion. Indigenous Trichoderma has long been known to partially or completely
fill the biological vacuum created by harsh soil treatments or stresses on the soil
microbiota, but the implication of this phenomenon in biological control is still
in question. Bliss (16) attributed the control of Armillaria mellea in citrus
following carbon disulfide fumigation to the action of indigenous Trichoderma
that rapidly colonized and reproduced in the fumigated soil, but he did not
provide direct evidence that the colonizer controlled the pathogen. Ohr et al
(114) provided the most convincing direct evidence of the involvement of
indigenous Trichoderma in the biocontrol of A. mellea in methyl bromide
fumigated soil. Trichoderma was more resistant to methyl bromide than was A .
mellea, and A. mellea weakened b y methyl bromide produced less o f the
antibiotic that otherwise protected it against the antagonist in nonfumigated soil

( 1 1 3) .
Additional conjectural evidence o f the role o f indigenous populations of
antagonists in biocontrol includes the observation that adding sulfur to soil to
maintain the pH below 3.9 controls root rot and heart rot of pineapple in
Australia. This control was attributed to a decrease in zoosporangium formation
of the casual agent (Phytophthora) and to an increase of the acidophilic native
T. viride (26). The ability of Trichoderma and Gliocladium to act as mycopara
sites of hyphae and resting structures of plant pathogens has been demonstrated
not only in vitro (4, 26) but also in natural soil (74). The proven ability of
Trichoderma and Gliocladium to produce diffusible substances toxic to other
fungi in vitro and even in organic substrates in soil ( 1 55) also strengthens the
hypothesis suggesting the importance of native Trichoderma and Gliocladium

in biocontrol.
It would be redundant to attempt a review of all the indirect evidence on the
importance of these two native antagonists in the biocontrol of plant diseases.
However, soil suppressiveness is an important piece of this evidence and must
be mentioned here. Trichoderma hamatum is abundant in Colombian organic
nursery soil suppressive to Rhizoctonia solani (23, 24) , and T. harzianum has
been abundantly isolated from Mexican soils suppressive to several soilborne
diseases (96). The reestablishment of suppressive properties to container media
that previously was rendered nonsuppressive to R. solani by heat or gamma
radiation, by introducing T. harzianum to the media ( 1 10, 1 1 1) , is further
indirect evidence of the role Trichoderma may play in biological control .
Trichoderma hamatum and T. harzianum were among the fungi most effective
in inducing suppressiveness isolated from composted hardwood bark and
capable of restoring suppressiveness to heat-treated media amended with com
posted hardwood bark ( 1 1 1 ) .
The suppressiveness o f soil to soilborne plant pathogens, especially to
Rhizoctonia solani and Pythium spp., that has been attributed to native or
introduced Trichoderma, has become the subject of intense studies during the
last few years. Several review articles ( 10 , 1 1 , 70) and books (9 , 26) have dealt
with the ability of Trichoderma to bring about suppressiveness to soilborne
plant pathogens.
AUGMENTATION OF SOIL WITH TRICHODERMA AND GLIOCIADIUM Recent

ly, there has been considerable interest in the biocontrol of plant pathogens ,
especially soilborne pathogens , by the purposeful introduction o f Trichoderma
and Gliocladium preparations, an interest reflected in the large number of
publications on the subject. This review will focus on advances made during the
last three to five years in the field. Coverage of greenhouse trials will be limited
to specialized crops.
40 PAPAVIZAS
Biocontrol by adding large amounts of T. harzianum with its food base to soil
is exemplified by the work of Wells et al ( 153) . These researchers were among
the first to report the large-scale use of Trichoderma preparations on solid
media (ground annual ryegrass seed) for field control of Sclerotium rolfsii on
tomato transplants. Their system, however, re:quired large amounts of organic
matter (4,200 kg per hectare) for disease control. Backman & Rodriguez
Kabana (5) grew T. harzianum on a commercial, insoluble diatomaceous earth
granule impregnated with molasses and applied the granules by hand over rows
of peanuts at 1 12 or 140 kg per hectare 70 and 1 00 days after planting. At 140 kg
per hectare , T. harzianum significantly limited damage caused by S. rolfsii and

increased yield over a three-year period. Control by this method was equivalent
to that obtained with PCNB .
Trichoderma species, especially T. harzianum, grown on solid substrates

have been tested with varying degrees of success against the following diseases:
white rot of onion (Sclerotium cepivorum) in Egypt ( 1 , 2) and in the United
States (122), cucumber diseases and cotton wilt (Verticillium dahliae) in the
USSR (52) , rhizoctonia damping-off and blight (S. rolfsii) of several crops in
Israel (25 , 44, 46-48) , and rhizoctonia fruit rot of cucumber (88) . Gliocladium
species , especially G. roseum and G. virens, grown on solid substrates have
also been tested successfully against black root rot of cucumber (Phomopsis
sclerotioides) (56) and damping-off of cotton caused by Pythium ultimum and
R . solani (7 1 ) . The efficiency of biocontrol with solid inoculants depended on
temperature, type of inoculum used, time of introduction of the antagonist to
soil in relation to the time of sowing (46) , the rate of application (inoculum
density) of the antagonist (48, 63) , and the inoculum density of the pathogen
( 1 56).
A more di fficult problem in the use of a readily available substrate with
Trichoderma or Gliocladium is a possible stimulation of a pathogen and hence
an increase in disease. Kelley (79) reported that T. harzianum-impregnated clay
granules similar to those used earlier (5) faikd to provide control of damping
off (Phytophthora cinnamomi) of pine seedlings. He attributed this to the ability
of the pathogen to use residual nutrients , especially in wet soils, resulting in
increased disease. A fresh nutrient source introduced into the soil with T.
harzianum also stimulated rapid colonization by Pythium of the organic sub
strate provided by pellets , resulting in more disease on greenhouse cucumbers
( 1 04) . No damping-off occurred when the antagonist was added on pellets 15 to
30 days before cucumber seedlings were transplanted.
Soil augmentation with conidia Because of poor conidiation, or lack of it, in

deep-tank fermentation systems , it is unlikely that commercial preparations
containing only conidia of Trichoderma or Gliocladium will ever become
available for biocontrol in the United States. . Despite this, soil augmentation
tests with naked conidia have been performed, sometimes with encouraging
results. Jordan & Tarr (77) dipped the roots of strawberry runners into sus
pensions of individual fungi and bacteria and planted them in soil infested with
Verticillium dahliae. Trichoderma viride and three other fungi limited the
incidence of wilt and increased plant growth.
Bare conidia can also be added following a selective compound (e.g. fumiga
tion) or a selective treatment such as soil pasteurization. Excellent control of
fusarium wilt of chrysanthemum was obtained recently (94) by the addition to
soil mix of aqueous conidial suspensions of a benomyl-resistant biotype of T.
viride . The biotype, used at 104 conidialcm2 after the soil mix was pasteurized
with steam (at 82°C for two hours) , rapidly colonized the soil mix , prevented
reinvasion by the pathogen, and provided control equal to a commercial
integrated procedure. The benomyl-resistant biotype was not inhibitory to the

pathogen in dual cultures. Resistance to benomyl also allowed compatible use
of the fungicide in soil or as a spray for the control of foliar diseases.
Soil augmentation with Jermentor biomass Recent research ( 1 3 , 1 1 9) has

indicated that fermentor biomass (FB) preparations formulated as a powder,
slurry, or alginate pellets and added to soil not only proliferate dramatically, but
also suppress diseases more effectively than bare conidia or chlamydospores.
Pellets of fermentor biomass of T. hamatum, T. harzianum, T. viride, and G.
virens reduced the survival and growth o f Rhizoctonia solani i n soil and
rhizoctonia fruit rot on tomato (9 1 ) . The manner in which fermentor-biomass
preparations are made will undoubtedly have a great effect on their shelf life,
their survival and proliferation in soil , and their potential for biocontrol .
Although it appears that fermentor-biomass preparations will be the biotech
nological approach of the future for disease control using fungal antagonists, it
is too early to predict the full extent of expansion and the significance of such
technology.
Seed Treatment
Most of the pertinent research published before 1 980 on seed and wound
applications of Trichoderma and other antagonists for the biocontrol of plant
diseases has been reviewed by Kommedahl & Windels (82). Only some recent
observations will be discussed here.
Although many strains of Trichoderma and Gliocladium have been used
experimentally for biocontrol, none has been registered for commercial use in
the United States ( 1 20). Several reasons may be responsible for this, one being
the large amount of biological material required to treat large areas of soil
(64-66). Applications of Trichoderma or Gliocladium to seed were suggested
(66) as an alternative approach to introducing them into soil. This method
42 PAPAVIZAS
requires smaller amounts of biological matel1al than in-furrow or broadcast

applications.
The advances in seed treatments with Trichoderma described below, which
have taken place during the last five years, provide a clear picture of the
promises and difficulties inherent in this approach. Good biocontrol of damp
ing-off caused by Rhizoctonia solani and Pythium spp. was achieved by treating
seeds of peas and radishes with conidia of T. hamatum isolated (24) from a
Rhizoctonia-suppressive Colombian soil (65 , 66). Control was also achieved
with conidia of several ultraviolet-induced biotypes of T. harzianum (122) and
T. viride (121). Improved stands and yields were also obtained in a Rhizocto
nia-infested field by planting soybean seed treated with T. pseudokoningii
(156) and seed of corn and soybean treated with T. harzianum (83). The use of
T. harzianum as a seed treatment to control R. solani on cotton also seemed
promising in the field in Israel (49) , but disease severity in the control was too
low to demonstrate convincing differences.
It is difficult at this time to predict the full extent to which seed treatment will
develop and expand as viable biocontrol technology over the next few years.
Development and expansion will depend on understanding and solving several
problems, none of which is as important as the economic feasibility and
acceptability of such technology by industry and agriculture. From a basic
standpoint, other considerations are also important. Success will depend on the
isolates used (64, 121, 122), the age of the seed inoculant (83), the soil
temperature and soil reaction (65, 66), the kind of soil and its microbiota (64) ,
the nutritional status of the inoculant (66) , the inoculant density on the seed (64,
122), the inoculum potential of the pathogen in the soil (156) , and even the
timing of planting (83).
For success beyond the suppression of seed rots and the damping-off of
young seedlings, Trichoderma or Gliocladium applied to seed must be able to
multiply in the soil or rhizosphere to inhibit a given pathogen by competition,
mycoparasitism, or antibiosis. The ideal seed inoculants should be effective
antagonists and aggressive sperrnosphere and rhizosphere colonizers. They
should also be insensitive to siderophore-producing bacteria (64, 66) and to
other soil microorganisms. Through searching, selection, genetic engineering,
and breeding, such ideal biotypes perhaps can be developed. Before this can
happen, however, research is needed to understand the peculiarities that enable
a fungus to establish and proliferate in the plant rhizosphere.
Aerial Application
As with seed treatments, research published before 1980 on the use of
Trichoderma to control above-ground plant diseases has already been reviewed
(82). Unfortunately, research pioneered by US Forest Service scientists and
others in the 1970s on forest tree diseases in the northeastern States of the US
TRICHODERMA AND OLiOCLADIUM 43
appears to have come to an end. Summer inoculation of red maple wounds with
T. harzianum prevented invasion by hymenomycetes after 2 1 months, but after
3 1 months 14% of the treated wounds yielded hymenomycetes ( 1 26) . The
antagonist was even less effective when applied in winter. Since Trichoderma
is a poor colonizer of fresh wood, the ameliorating effect was due to massive
amounts of inoculum applied to the wounds, enabling it to establish a temporary
position of dominance that was lost with time.
A more successful example of Trichoderma application to aerial plant parts is
the biocontrol of wounds on shrubs and trees applied at pruning , in advance of
decay fungi . Grosc1aude (6 1 ) demonstrated the effectiveness of T. viride

against Stereum (Chondrostereum) purpureum, the cause of silver leaf disease
on plum, and Grosclaude et al (62) developed an ingenious method to apply
conidia of the antagonist to wounds during cutting by means of special pruning

shears . The antagonist applied by this method 48 hours in advance of inocula
tion with the pathogen protected two-year-old plum trees thoroughly, but not
when the antagonist was applied simultaneously with the pathogen.
Not only a preventive but also a curative treatment has been reported (39) for
the control of silver leaf disease with Trichoderma. Live T. viride-impregnated
wood dowels (0 . 8 x l Ocm) are introduced into holes Glade at l O-cm intervals in
the trunk and major limbs of silvered plum, peach, or nectarine trees (27). In the
late 1 970s, 50% of more than 1 600 plum trees treated in this way with T. viride
exhibited fewer symptoms of silver leaf and most of the symptoms disappeared
on many trees (27) . Seventeen percent of the trees showed no change. The
strain of T. viride used in these experiments does not produce antibiotics or
enzymes and it is not allergenic (129). Ricard ( 1 28) coined the term immunizing
commensals for biocontrol agents with the ability to bring about biotherapeutic
effects and protect or cure plants from disease without themselves being
pathogenic. Products containing two psychrophilic species aggregates , T.
viride and T. polysporum, for the control of silver leaf disease on trees and
verticillium wilt on mushrooms have been registered for commercial use in
France and the United Kingdom. By 1981, more than 20,000 fruit trees had
been treated in commercial orchards ( 1 30) . Trichoderma pellets are also being
evaluated for the curative suppression of Dutch elm disease (Ceratocystis ulmi)
(131).
Attempts to suppress above-ground plant diseases with Trichoderma have
not been limited to wound applications. Tronsmo & Dennis ( 1 4 1 ) were able to
protect strawberry fruit against storage rot (Botrytis cinerea and Mucor muce
do) by spraying strawberry plants in the field, beginning at early flowering,
with aqueous suspensions of conidia of T. viride and T. polysporum . Although
biocontrol was as effective as sprays with the fungicide dichlofluanid , the level
of both biological and chemical control was not adequate from a commercial
standpoint. Tronsmo & Raa ( 142) were also able to protect apples against
44 PAPAVIZAS
eyespot (B . cinerea) by spraying conidia ofT. pseudokoningii after the artificial

inoculation of flowers with the pathogen, but not when infections occurred
from natural inoculum. The lack of control of natural infection was attributed to
low temperatures prevailing at flowering. Trichoderma pseudokoningii was
unable to grow below 9°C, whereas B. cinerea could infect the plants at lower
temperatures . In subsequent studies (143), apple flowers sprayed with conidia
of an isolate of T. harzianum capable of growing at low temperatures had
considerably lower incidence of dry eyespot in the field; dichlofluanid was
ineffective. The researchers claimed ( 1 43) that this was "the first report of
biological control of natural infection of fruilt rot under field conditions. " In
additional above-ground tests (40), the efficacy of T. harzianum against B .
cinerea of grapes depended o n temperature and the inoculum concentration of
conidia.
ROLE OF BIOCONTROL IN INTEGRATED PEST

MANAGEMENT
The integration of several control technologies may be required to increase

yield and quality and minimize environmental hazards. The potential of
Trichoderma and Gliocladium for biocontrol has been studied largely as an end
in itself rather than as a synergistic or additive component in integrated pest
management systems. Such approaches can be successful only if Trichoderma
or Gliocladium are compatible with pesticides or other control practices,
however. Integration of the two antagonists with pesticides will be 'a tech
nological challenge for the future. Trichoderma and Gliocladium can be man
ipulated genetically to tolerate some of the most important pesticides used in
production systems. A beginning has been made with considerable success (l ,
94 , 1 2 1 , 1 22) .
Research and technology have been limited not only with respect to the
development of new resistant biotypes, but also to their use in pest-management
systems. Integration of Trichoderma or Gliocladium with other control systems
would improve the prospects for single or multiple disease control. The two
biocontrol agents , especially Trichoderma, have been used in experimental
combinations with various management practices . For example, satisfactory
control of cucumber fruit rot (Rhizoctonia solani) in the field was achieved by a
combination of plowing and the addition of T. harzianum (88). The use of the
antagonist in association with plowing resulted in less disease than when either
component was used individually . Other examples of combining Trichoderma
with cultural practices include the displacement of Phellinus (Poria) weirii by
Trichoderma in root wood of alder by applying urea to forest soils ( 112) and the
increased control of diseases caused by R . solani and Sclerotium rolfsii by T.
harzianum combined with soil solarization (25 , 50, 78).
Control of Armillaria mellea with a combination of methyl bromide and
Trichoderma ( 1 1 4) has been cited in almost every review article during the last
ten years as a classical example of integrated pest management involving the
use of a pesticide with a biocontrol agent. Other examples of a pesticide and a
biocontrol agent include the use of combined T. harzianum and peNB against
rhizoctonia damping-off of several vegetables (50, 67) and bulbborne
pathogens of iris (25), and methyl bromide and T. harzianum combined for the
control of R. solani on strawberry (44) and R. solani and S. rolfsii on tomatoes
and peanuts (47) . Recently, Kraft & Papavizas (84) have shown that the highest
seed yields in the field with a pea cultivar (Dark Skin Perfection) susceptible to
Pythium ultimum are obtained with a seed treatment combining metalaxyl and
T. harzianum.
The use of tolerant strains of Trichoderma or Gliocladium together with
selective pesticides may offer a distinct possibility of control in cases where no
single component is effective. In addition to the systems discussed above , the

two antagonists may also be applied in tank mixtures or "chemigation" systems
together with a fungicide, herbicide , or liquid fertilizer, or coated onto seeds
together with infused seed treatment fungicides ( 1 1 6) . More research is needed
on the integration of Trichoderma, and especially Gliocladium, with chemical
approaches to improve the prospects for disease control .
MECHANISMS OF BIOCONTROL
In a recent review, Hornby (70) states that "a major problem that besets the
subject of microbial antagonisms in soil is that many of the mechanisms
discussed are presumptive and . . . proof is difficult to come by. " The
mechanisms proposed during the last ten years or so to explain the biocontrol of
plant pathogens by Trichoderma or Gliocladium are also presumptive. Sug
gested mechanisms for biocontrol by the two genera are antibiosis, lysis,
competition, and mycoparasitism (4, 26, 1 23).
Most attempts to correlate in vitro antibiosis by Trichoderma or Gliocladium
against fungal pathogens with what actually happens in natural systems have
failed. Thus, interest in studying antibiosis in vitro as a tool for making inroads
into the secrets of biocontrol has greatly diminished, although research papers
still appear on the subject ( 14). Several toxic metabolites are produced in vitro
by the two antagonists, and there is some evidence that such metabolites are
produced in bits of organic matter in soil ( 1 55). However, there is no direct
evidence to unequivocally implicate such metabolites as a mechanism for
biocontrol in soil, and there is no direct evidence that antibiotic substances are
produced in natural soil in effective quantities to bring about tangible results for
biological control ( 1 23). Although T. viride (Gliocladium?) produced gliotoxin
on seed coats in soil ( 1 55) and noninoculated pea seed planted in natural soil
containing the antagonist had gliotoxin in the seed coats ( 1 54), these observa
tions do not prove that gliotoxin is unequivocally involved in the mechanism of
46 PAPAVIZAS
action. Webster & Lomas ( 148) did not obtain gliotoxin or viridin from T.
viride although this species aggregate is implicated in biocontrol. T. viride
,
could have acted as a mycoparasite in Wright's tests, or gliotoxin could have

acted synergistically with mycoparasitism. Most experiments on antibiosis
have been designed in such a way that it is not possible to distinguish the direct
effects of antibiotics from other forms of antagonism . For instance, the ad
pressed growth habit of T. harzianum around hyphae of Rhizoctonia solani (88)
could involve antibiotic production and direct parasitism as well as lysis. It is
evident that the intricacies of soil and plant rhizosphere make it a difficult task
to discover the precise mechanism.

Recent research has presented less conjectural evidence on the importance of
antibiosis on G. virens (7 1 , 72) . Howell (7 1 ) showed that cottonseed treatment
with G . virens protected seedlings from damping-off caused by Rhizoctonia
solani or Pythium ultimum. The antagonist parasitized hyphae of R . solani in

vitro and reduced the number of viable sclerotia after three weeks in natural
soil, but did not exhibit mycoparasitism of P. ultimum hyphae and did not affect
oospores of P . ultimum in soi l . G . virens produced an antibiotic di
ketopiperazine (gliovirin) that was highly inhibitory to P. ultimum but not to R .
solani (72). An ultraviolet light-induced mutant of G . virens deficient for
gliovirin production did not protect cotton seedlings from P. ultimum damping
off. In contrast, a mutant with enhanced gliovirin production provided good
biocontrol, even though it did not grow as well as the wild strain . The loss of
biocontrol effectiveness and the loss of antibiotic production by mutation,
coupled with the inability of the antagonist to exhibit mycoparasitism, provides
the best evidence we have today for the importance of antibiosis in biocontrol.
Following the discovery that T. lignorum (G . virens) has great potential for
biocontrol ( 149) , many researchers dealing with Trichoderma and Gliocladium
noticed that hyphae of the antagonists parasiti.zed hyphae of other fungi in vitro
and brought about several morphological changes (coiling, haustoria, disorga
nization of host cell contents, penetration of the host). Several recent review
articles (4, 26) and many research publications have covered the literature on
mycoparasitism (almost exclusively in vitro) by the two antagonists. Additional
discussion on these phenomena is redundanlt. Whether researchers used light
microscopy to observe parasitism, or more sophisticated approaches (scanning
electron microscopy , transmission electron microscopy, fluorescence micro
scopy) to study ultrastructural phenomena, the point raised by Ayers & Adams
(4) in reference to mycoparasitism in soil must be considered. They pointed out
that the "mere occurrence of one fungus on another in nature, or the observed
invasion of one fungus by another in vitro, is insufficient evidence that
mycoparasitism proceeds in a natural ecosystem. Before embarking on exten
sive biological control tests with presumed mycoparasites, it seems highly
desirable that one establish that the organism in question does, in fact,
parasitize the plant pathogen under natural conditions."
Recent advances made through the use of electron microscopy to study
mycoparasitism in vitro were not unexpected. In 1968, Durrell (4 1 ) , using
phase contrast and electron microscopy, produced interesting photographs
showing haustoria and hyphae of T. viride within hyphae of Phycomycetes
followed by digestion of their contents. Recent studies on parasitism of Sclero
tium rolfsii and Rhizoctonia solani by T. hamatum and T. harzianum corrobo
rated Durrell's findings and demonstrated additional phenomena at the molecu
lar level (e.g. extracellular fibrillar material deposited between the interacting
hyphae , the accumulation of parasite organelles in the parasitizing cells, the
production of a sheath matrix that encapsulates the penetrating hyphae) (43). In
vitro, the phenomena of physical contact followed by the disorganization of the

host cells and concomitant changes in the cells of the parasite have been
unequivocally established for Gliocladium (7 1 , 73, 1 44) and Trichoderma (43 ,
45) . However, despite all this progress on i n vitro mycoparasitism, the ecolog
ical significance of it or whether it occurs in nature is not well understood.
Griffin (60) expressed the opinion that it is unlikely that further field evidence
will reveal mycoparasitism to be a factor of great ecological importance.
Although the discovery and use of Sporidesmium sclerotivorum (4) dispels this
conclusion, we do not yet have similar ecological evidence with Trichoderma
or Gliocladium.
Research on mycoparasitism as a mechanism of biocontrol raises two addi
tional questions: is physical contact necessary for host destruction and how
important are enzymes and other extracellular compounds in mycoparasitism.
Pachenari & Dix ( 1 15) concluded that G. roseum need not make intimate
contact with Botrytis allii to cause severe internal disorganization of host cells,
coagulation of cytoplasm, vacuolation, and loss of contents from organelles. In
their tests, preparations of glucanases from the antagonist degraded the glucans
of the host. Cultures ofB . allii parasitized by G. roseum contained considerable
13-( 1 -3)-glucanase and chitinase, and coagulation of cytoplasm occurred with
out physical contact.
The capacity to produce cell wall-degrading enzyme is common among
saprophytic fungi. More than 1 0% of 160 fungi examined (22) produced
13-( 1 -3)-glucanase. In mycoparasitism, the host may first be softened si
multaneously by toxic metabolic products, including enzymes, before dis
organization and death occur. Barnett & Binder ( 1 2) were the first to implicate
toxic metabolites in necrotrophic mycoparasitism. However, the evidence of
toxic metabolites in mycoparasitism is circumstantial. Additional research with
new, sophisticated methods and equipment is needed to determine the im
portance of metabolites in mycoparasitism.
48 PAPAVIZAS
From a basic standpoint, the relationship between mycolytic enzymes pro

duced by Trichoderma and their significance in host cell degradation have been
established (26). Chet & Baker (23, 24) showed that Trichoderma produces
cellulase, j3-(l -3)-glucanase, and ch itinase
and degrades the glu cans in the
walls of Pythium spp. and the chitin and glucans in the walls of Rhizoctonia
solani. There was no evidence that T. hamatum (24) or T. harzianum (63)
produces any antibiotics. The importance of �1-(1-3)-glucanase and chitinase as
key enzymes responsible for fungal cell and sclerotial wall lysis and degrada
tion has also been stressed by others (43, 45 , 76).
FUTURE RESEARCH PRIORITIES

In the past five or six years , research on Trichoderma and Gliocladium has
entered a new phase with the introduction of new culture media for isolation and
enumeration, the development of new techniques for studying survival and
proliferation in soil and plant rhizosphere, the induction of new biotypes
resistant to fungicides , increased emphasis on the production of metabolites and
their probable involvement in the mechanism of biocontrol action, and new
biotechnological approaches to promote growth and develop delivery systems.
In spite of this progress , including registration and the projected role and
availability of Trichoderma inoculants in northern Europe, the use of these two
A major deterrent, among others, to their
biocontrol agents is still very limited.
commercial use is their specificity, the ability of any one strain to control only
one plant disease most of the time.
Before several Trichoderma and Gliocladium strains become available com
mercially for biocontrol , major research priorities must include the following
broad areas: (a) genetic manipulation to enhance the ability of the two an
tagonists to control several diseases, adapt to various environmental con
ditions, and tolerate pesticides; (b) development of fermentation technology
and delivery systems, two processes that will require a long-term commitment
by researchers and industry together before any practical applications can be
achieved; (c) development of computerized models to understand the effect of
the microenvironment on the survival and proliferation of the two antagonists in
soil and plant rhizosphere; (d) understanding the mechanisms of biocontrol at
the molecular and biochemical level and using the information to predict
biocontrol capabilities; (e) interaction of Trichoderma and Gliocladium with
other control components to develop integrated management systems for multi
ple disease control; and (f) understanding economic factors such as cost/benefit
ratios , development and distribution investment, time and investment need for
registration, economic competition from pesticides, to xicologic al aspects, and
acceptability by growers .
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7 1 : 1 2 1-25 Pathol. 1 3 :60-62
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1 19. Papavizas, G. c . , Dunn, M. T . , Lewis, 1 3 3 . Rifai, M. A. 1 969. A revision of the
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fermentation technology for ex Inst. Mycol. Pap . 1 1 6 . 56 pp.
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viride resistant to MBC fungicides. Selected topics in biological control .
Phytopathology 73:407- 1 1 Ann. Rev. Microbiol. 35:453-76
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biotypes of Trichoderma harzianum for Friesia 9:299-30 1
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biocontrol capabilities . Phytopathology Biological control effects of a new isolate
72: 1 26-32 of Trichoderma hurzianum on Pythium
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Biological control of soilborne fungal 498-50 1
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1 8:389-4 1 3 The structure of gliovirin, a new antibiot
1 24 . Papavizas, G . C . , Lumsden, R. D . 1 982. ic from Gliocladium virens. J. Antibiot.
Improved medium for isolation of 35 : 1 326-30
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66: 1 0 1 9-20 ical control of Phomopsis sclerotioides in
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R. 1 963. Studies on fungi in the root 439-42
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young roots. Plant Soil 1 9:322-49 of Trichoderma species to control straw
1 26. Pottle, H. W . , Shigo, A. L. , Blanchard, berry fruit rots. Neth. J. Plant Pathol.
R. O. 1 977. Biological control of wound 83:449-55
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pathogenic fungi. Neth . 1. Plant Patho!. cal control of Botrytis cinerea on apple.
75:287-95 Plant Dis. 64: 1 009
54 PAPAVIZAS
144. Tu, J. C. 1980. Glioe/adium virens, a Trichoderma and Glioe/adium . Phyto

destructive mycoparasite of Sclerotinia pathology 27: 1 1 75-77
sclerotiorum. Phytopathology 70:670- lSI. Weindling, R. 1 94 1 . Experimental con
74 sideration of the mold toxins of Gliocla
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ferentiation. In Fungal Differentiation, 3 1 :99 1 - 1 003
ed. J. E. Smith, pp. 1 - 1 8 . New York: 152. Weindling, R . , Emerson , O. H . 1936.
Dekker. 624 pp. The isolation of a toxic substance from
146. Tye, R. J . , Willets , A. J. 1973 . Fungal the culture filtrate of Trichoderma.
growth on methanol. 1. Gen. Microbiol. Phytopathology 26:1 068-70
77:i-ii 153. Wells, H. D Bell. D. K Jaworski. C.
. • . •
1 47 . Walker, H. L . , Connick, W. J. Jr. 1983 . A . 1972 . Efficacy of Trichoderma har

Sodium alginate for production and zianum as a biocontrol for Sclerotium
formulation of mycoherbicides. Weed rolfsii. Phytopathology 62:442-47

Sci. 3 1 :333-38 154. Wright, J. M . 1956. Biological control of
1 48. Webs ter , J . , Lomas N. 1 964. Does
, a soil-borne Pythium infection by seed
Trichoderma viride produce gliotoxin inoculation. Plant Soil 8: 1 32-40
and viridin? Trans. Br. Mycol. Soc. 1 55 . Wright, J. M . 1956. The production of
47:535-40 antibiotics in soil. III. Production of

149. Weindling, R. 1934. Studies on a lethal gliotoxin in wheatstraw buried in soil.
princip le effective in the parasitic action Ann. Appl. Biol. 44:46 1-66
of Trichoderma lignorum on Rhizoctonia 1 56. Wu, W.-S. 1982. Seed treatment by
solani and other soil fungi. Phytopathol applying Trichoderma spp. to increase
ogy 24: 1 1 53-79 the emergence of soybeans. Seed Sci.
ISO. Weindling, R . 1 937. Isolation of toxic Techno!' 1 0 :557-63
substances from the culture filtrates of
ANNUAL
REVIEWS /
Further
Quick links to online content
Annual Review of Phytopathology

Volume 23. 1985
CONTENTS
PREFATORY CHAPTER
Plant Pathology at the Crossroads, Arthur Kelman

HISTORICAL PERSPECTIVES
William Brown: Pioneer Leader in Plant Pathology, S. D.

Garrett 13
Ernst Giiumann, 1893-1963: Pioneer Leader in Plant Pathology,

H. Kern 19
ApPRAISAL OF PLANT DISEASE
The Spatial Analysis of Soilborne Pathogens and Root Diseases,

C. Lee Campbell and James P. Noe 129
Limiting the Effect of Disease Resistance on Yield, V.
Smedegaard-Petersen and K. Tolstrup 475
PATHOGENS/PUNGI
The Biology, Ecology, and Control of Sclerotium rolfsii. Z. K.

h* �
Parasite: Host: Environment Specificity in the Cereal Rusts, L. E.
Browder 201
PATHOGENS/BACTERIA
The Molecular Genetics of Plant Pathogenic Bacteria and Their

Plasmids, Nickolas J. Panopoulos and Richard C. Peet 381
PATHOGENS/NEMATODES
The Ecology of Nematodes in Agroecosystems, Diana W.

Freckman and Edward P. Caswell 275
PATHOGENS/VIRUSES
Advances in Geminivirus Research, B. D. Harrison 55
PHYSIOLOGY OF HOST-PATHOGEN INTERACTION
Transposon Mutagenesis and Its Potential for StUdying Virulence

Genes in Plant Pathogens, Dallice Mills 297
(Continued) vii
viii CONTENTS (Continued)
Enzymatic Penetration of the Plant Cuticle by Fungal Pathogens,

P. E. Kolattukudy 223
BREEDING FOR RESISTANCE
Strategies in Unconventional Breeding for Disease Resistance,

Gerhard Wenzel 149
The Current Status and Prospects of Multiline Cultivars and
Variety Mixtures for Disease Resistance, M. S. Wolfe 251
EPIDEMIOLOGY AND INFLUENCE OF ENVIRONMENT
The Epidemiology of Forest Nursery Diseases, W. J. Bloomberg 83

A Comparison of Simulation Approaches to Epidemic Modeling,
P. S. Teng 351
ACTION OF TOXICANTS AND CHEMICAL CONTROL
The Bioregulatory Action of Flavor Compounds on Fungal

Spores and Other Propagules, Richard C. French 173
The Chemical Control of Post-Harvest Diseases: Subtropical and
Tropical Fruits, Joseph W. Eckert and Joseph M. Ogawa 421
BIOLOGICAL AND CULTURAL CONTROL
Trichoderma and Gliocladium: Biology, Ecology, and Potential

for Biocontrol, G. C. Papavizas 23
SPECIAL TOPICS
Monoclonal Antibodies in Plant Disease Research, Edward L.

Halk and Solke H. De Boer 321
On the Conceptual Basis of Crop Loss Assessment: The
Threshold Theory, J. C. Zadoks 455
Plant Pathology in the Small Farm Context, Raul A. Moreno 491

Papavizas 1985

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ANNUAL

Ann. Rev. Phytopathol. 1985. 23:23-54

ECOLOGY, AND POTENTIAL FOR

Soilborne Diseases Laboratory, Plant Protection Institute, Agricultural Research Ser­

Growth, Morphogenesis, and Sporulation in Culture

GROWTH As expected with saprophytic soil fungi, species of Trichoderma

growth of Trichoderma and the implications of such effects on the ecology of

pronounced at high pH values, it can be ascribed to the bicarbonate ion (HC03)

MORPHOGENESIS Turian (145) recently defined morphogenesis as "the de­

Sporulation Most species of Trichoderma are photosensitive, sporulating

harzianum, T. viride, and G. virens in both liquid and solid fermentation

Germination Although many reports have appeared on sporulation in

conidia or unwashed agar contribute enough nutrients to initiate and support

The early attempts to obtain and characterize toxic metabolites from

pled with clarification of the Trichoderma taxonomy (133), resulted in a

Understanding the ecological factors affecting the distribution of Trichoderma

Occurrence and Distribution

colonizer, as its frequent isolation from well-decomposed organic matter in­

Isolation and Enumeration

Population Dynamics in Soil

the ecological importance of these structures would be significant.

various fungistatic soils survived as long as 20 months. However, a progressive

initially to reduce or completely annul fungistasis (95 , 123). Even a temporary

ESTABLISHMENT AND PROLIFERATION IN SOIL Selective passive or active

or Gliocladium thoroughly established in a food base (bran) also stimulate a

Trichoderma, is so voluminous that a special review is required. Most of the

to T. harizanum in vitro, in contrast to the benzimidazole fungicides (e.g.

ESTABLISHMENT IN THE RHIZOSPHERE Although Trichoderma and Gliocla­

workers have tried quantitative studies on the survival, establishment, or

rhizosphere when applied to seed. Trichoderma or Gliocladium introduced on

PRODUCTION AND DELIVERY SYSTEMS

must be developed to mass-produce the two antagonists rapidly. The past 30 to

mulations of mycoherbicidal fungi and by Fravel et al (54) to prepare a

PRODUCTION OF NEW STRAINS

Purposeful induction of tolerance or resistance to pesticides in Trichoderma or

white rot (Sclerotium cepivorum) of onion. One of the new benomyl-resistant

strains in their ability to produce the antibiotic gliovirin.

POTENTIAL FOR BIOCONTROL

ROLE OF THE INDIGENOUS POPULATION Before 1970, much of the work on

antibiotic that otherwise protected it against the antagonist in nonfumigated soil

hypothesis suggesting the importance of native Trichoderma and Gliocladium

AUGMENTATION OF SOIL WITH TRICHODERMA AND GLIOCIADIUM Recent­

per hectare , T. harzianum significantly limited damage caused by S. rolfsii and

Trichoderma species, especially T. harzianum, grown on solid substrates

Soil augmentation with conidia Because of poor conidiation, or lack of it, in

integrated procedure. The benomyl-resistant biotype was not inhibitory to the

Soil augmentation with Jermentor biomass Recent research ( 1 3 , 1 1 9) has

requires smaller amounts of biological matel1al than in-furrow or broadcast

decay fungi . Grosc1aude (6 1 ) demonstrated the effectiveness of T. viride

conidia of the antagonist to wounds during cutting by means of special pruning

eyespot (B . cinerea) by spraying conidia ofT. pseudokoningii after the artificial

ROLE OF BIOCONTROL IN INTEGRATED PEST

The integration of several control technologies may be required to increase

single component is effective. In addition to the systems discussed above , the

could have acted as a mycoparasite in Wright's tests, or gliotoxin could have

to discover the precise mechanism.

solani or Pythium ultimum. The antagonist parasitized hyphae of R . solani in

vitro, the phenomena of physical contact followed by the disorganization of the

From a basic standpoint, the relationship between mycolytic enzymes pro­

FUTURE RESEARCH PRIORITIES

3. Arrieta-Escobar, A. , Belin, J. M. 1982.

4. Ayers, W. A. , Adams, P. B. 1 98 1 . 1 8 . Bruehl, G. W. 1975. Systems and mech­

growth of Trichoderma in culture. Soil 198 3 . Parasitism of Trichoderma spp. on

Soilborne Diseases Laboratory, Plant Protection Institute, Agricultural Research Ser

MORPHOGENESIS Turian (145) recently defined morphogenesis as "the de

colonizer, as its frequent isolation from well-decomposed organic matter in

ESTABLISHMENT IN THE RHIZOSPHERE Although Trichoderma and Gliocla

AUGMENTATION OF SOIL WITH TRICHODERMA AND GLIOCIADIUM Recent

From a basic standpoint, the relationship between mycolytic enzymes pro

4. Ayers, W. A. , Adams, P. B. 1 98 1 . 1 8 . Bruehl, G. W. 1975. Systems and mech

Mohr, 16:603-39. Berlin: Springer J. BOl. 56:2243-46

144. Tu, J. C. 1980. Glioe/adium virens, a Trichoderma and Glioe/adium . Phyto

1 47 . Walker, H. L . , Connick, W. J. Jr. 1983 . A . 1972 . Efficacy of Trichoderma har