Biological Control of Oomycetes and Fungal Pathogens
B
Eric B. Nelson
Cornell University, Ithaca, New York, U.S.A.
INTRODUCTION
Oomycetes and fungi are economically damaging plant
pathogens whose presence and activities invoke the use of
repeated fungicide applications to minimize losses in plant
yield, quality, or aesthetics. Increasing environmental and
human health concerns associated with widespread fungicide use has prompted scientists and plant producers to
explore biological methods of disease control.
Biological control strategies make use of microorganisms to mitigate disease losses. Such disease suppressive
microorganisms are commonly found in many different
habitats. Biological control strategies attempt to enhance
the activities of these disease-suppressive microorganisms
either by introducing high populations of specific microorganisms or by enhancing the conditions that enable
microorganisms in their natural habitats to suppress
diseases. Common strategies for manipulation of biological control microbes will be discussed along with the
commercialization potential of biological disease control
strategies in agriculture.
by indirectly altering the biochemistry of the leaf surface, spermosphere, or rhizosphere such that pathogenesis is disrupted. This can be accomplished by producing
antibiotic compounds active against the target pathogen,
by competing with the target pathogen for specific resources such as iron or carbon, or by parasitizing hyphae or reproductive structures of the target pathogen.
Both fungal and bacterial biocontrol microbes can also
induce the expression of resistance responses in the host
plant, making the host less susceptible to infection or
disease development.
Various formulations of Trichoderma harzianum have
been the most widely commercialized and efficacious
inoculants used for the control of oomycete and fungal
diseases. Of particular importance is strain T-22 of T.
harzianum sold under the trade names RootShieldTM,
PlantShieldTM, and TurfShieldTM (Table 1). This inoculant is sold in the U.S. to the greenhouse, row crop, and
turf industries. During 1999, retail sales of T-22 products
totaled around $3 million[2] and were expected to increase
in the next years.
MICROBIAL INOCULANTS
COMMERCIALIZATION HURDLES
Microbial inoculation strategies attempt to increase soil
or foliar populations of specific disease-suppressive microbes temporarily and dramatically. Microorganisms
commonly studied and deployed for control of oomycete
and fungal diseases include species of bacteria in the genera Bacillus, Pseudomonas, and Streptomyces and fungi
in the genera Coniothyrium, Gliocladium, and Trichoderma.[1] Several organisms have served as model systems
for generating many of our concepts of biological disease
control. These include specific strains of Bacillus cereus
and B. subtilus, Enterobacter cloacae, Pseudomonas
fluorescens, and Trichoderma harzianum. Often specific
strains of bacteria and fungi are deployed for biological
control. Many times such strains, operating under rather
narrow modes of action, have relatively narrow ranges of
pathogen species for which they are effective.
The processes and traits expressed by biocontrol microbes result in reduced disease development by either
directly disrupting stages of the pathogen’s life cycle or
Despite decades of research on the biological control of
oomycete and fungal plant diseases, there remain few
widely adopted and commercially successful microbial
inoculants. Fewer than 25 microbial species have been
commercialized worldwide (Table 1). There are a number
of reasons for the lack of development and grower
adoption. Among the more important are problems in
formulation and delivery, variability in performance, and
problems with poor efficacy under optimum conditions
for disease development. There are countless examples of
biological control organisms that perform effectively
under defined laboratory conditions but fail when introduced on different crops under varying field conditions.
Still others might perform effectively in the field, but
exhibit strong year-to-year or site-to-site variability.
Additionally, the economics and level of biological knowledge necessary for growers to implement biological control strategies is still not favorable for many cropping
systems, making adoption levels low.
Encyclopedia of Plant and Crop Science
DOI: 10.1081/E-EPCS 120019935
Copyright D 2004 by Marcel Dekker, Inc. All rights reserved.
137
U.S.A.
U.S.A.
U.S.A., Britain, Japan, South Africa,
New Zealand
U.S.A.
Armillaria, Botryosphaeria, and others
Turfgrass diseasesa
Soybean seed and root rotsb
Various foliar and root diseasesa
Seed, seedling, and root rotsb
Turfgrass diseases
Seed, seedling, and root rotsb
Postharvest fruit diseases
Wilts, seed, and root rotsd
Wilts, seed, and root rotsd
Various fungal diseases
Trichoderma viride
Bacteria
Bacillus licheniformis
Bacillus pumilus
Bacillus subtilis
Burkholderia cepacia
Pseudomonas aureofaciens
Pseudomonas chlororaphis
Pseudomonas syringae
Streptomyces griseoviridis
Streptomyces lydicus
Streptomyces hygrospinosis var. beijingensis
b
Diseases cause by species of Rhizoctonia, Fusarium, Alternaria, Aspergillus, and other fungi and Oomycetes powdery mildew, downy mildew, early leaf spot, early blight, and late blight diseases.
Diseases caused by species of Rhizoctonia, Fusarium, and Pythium.
c
Diseases caused by species of Botrytis and Penicillium.
d
Diseases caused by species of Fusarium, Alternaria, Rhizoctonia, Phomopsis, Pythium, Phytophthora, and Botrytis.
e
Diseases caused by species of Pythium, Rhizoctonia, Verticillium, Sclerotium, Botrytis, and others.
(Largely from the EPA Biopesticides website http://www.epa.gov/pesticides/biopesticides/; the PAN Pesticides Database http://www.pesticideinfo.org/index.html; and ATTRA Microbial Pesticides,
Manufacturers & Suppliers Resource List http://attra.ncat.org/attra-pub/microbials.htm.)
a
EcoGuardTM
GB34TM
KodiakTM, EpicTM, ConcentrateTM, KodiakTM,
HBTM, Quantum 4000, HBTM, System 3TM,
TaegroTM, BotkillerTM, SerenadeTM, SubtilexTM
AvogreenTM, DenyTM,
Blue CircleTM, InterceptTM
SpotLessTM
AtEzeTM, CedomonTM
Bio-Save 10, 11, 100, 110, 1000TM
MycostopTM
ActinovateTM
AB 120TM
TrichopelTM, TrichojetTM,
TrichodowelsTM, TrichosealTM
Sporodex LTM
PolygandronTM
Milsana bioprotectant
RootShieldTM, PlantShieldTM, TurfShieldTM,
BioTrek 22GTM, SupresivitTM, T-22GTM,
T-22HBTM, TrichodexTM, EcoTTM, Harzan 1TM
BinabTM
YieldPlusTM
Biofox CTM, FusacleanTM
PrimastopTM
Soil GuardTM, GliomixTM
RotstopTM, PG Suspension
Contans WGTM, Intercept WGTM
AQ-10TM
AspireTM
Ketomium (R)TM
Product names
138
U.S.A.
U.S.A., Sweden
U.S.A.
U.S.A., Canada, Finland, Netherlands
U.S.A.
China
U.S.A., Britain, Sweden,
Denmark, Chile, Germany
New Zealand
Tree-wound pathogens
Pseudozyma flocculosa
Pythium oligandrum
Reynoutria sachalinensis
Trichoderma harzianum
Trichoderma polysporum
U.S.A., South Africa
U.S.A., Israel
China, Philippines, Russia,
Thailand, and Vietnam
U.S.A., Austria, France, Italy,
Luxembourg, Germany, Mexico, Poland
South Africa
Italy, France
U.S.A.
U.S.A., Finland
Britain, Sweden, Norway,
Switzerland, and Finland
U.S.A., Canada
Slovak Republic
U.S.A.
U.S.A., Canada, Europe, Israel,
Australia, South Africa
Countries registered
Postharvest fruit diseases
Fusarium wilt diseases
Fungal diseases of greenhouse crops
Seed, seedling, and root rotsb
Heterobasidion annosum on
pine and spruce trees
Powdery mildew diseases
Damping-off of sugar beets
Powdery mildew, gray mold
Seed and root rotting diseasese
Powdery mildews
Post-harvest diseasesc
Diseases caused by Phytophthora and
other root rot fungi
Diseases caused by Sclerotinia
Target disease(s)
Cryptococcus albidus
Fusarium oxysporum
Gliocladium catenulatum
Gliocladium virens
Phlebiopsis gigantea
Coniothyrium minitans
Fungi and oomycetes
Ampelomyces quisqualis
Candida oleophila
Chaetomium cupreum/C. globosum
Microbial inoculant
Table 1 Commercial microbial inoculants used worldwide for control of oomycete and fungal plant diseases
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Biological Control of Oomycetes and Fungal Pathogens
139
Table 2 Examples of soils suppressive to oomycete and fungal plant diseases
Pathogen
Disease
Aphanomyces euteiches
Armillaria mellea
Cephalosporium graminearum
Didymella lycopercisi
Fusarium oxysporum
Root rot of pea
Root rot of conifers
Stripe of wheat
Stem rot of tomato
Wilts of various crops
Fusarium solani
Fusarium culmorum
Gaeumannomyces graminis
Phytophthora capsici
Phytophthora cinnamomi
Phytophthora sojae
Poria weirii
Pseudocercosporella herpotrichoides
Pythium aphanidermatum
Pythium splendens
Pythium ultimum
Rhizoctonia solani
Sclerotium rolfsii
Thielaviopsis basicola
Verticillium albo-atrum
Root rot of bean
Foot rot of barley
Take-all of cereals
Damping-off of tomato
Root rots of various crops
Root rot of soybean
Root rot of conifers
Root rot of cereals
Root rot of many crops
Damping-off of cucumber
Damping-off of cotton
Root rot of many crops
Rot of tomato
Root rot of tobacco
Wilt of potato
Microorganisms responsible
Unknown
Unknown
Unknown
Unknown
Nonpathogenic Fusarium spp.;
Pseudomonas spp.
Unknown
Unknown
Pseudomonas spp.
Unknown
Various bacteria
Unknown
Unknown
Unknown
Unknown
Unknown
Seed-colonizing bacteria
Unknown
Unknown
Unknown
Unknown
(From Ref. 8.)
SUPPRESSIVE SOILS
Disease and pathogen suppressive soils have been known
for over a century and identified from many parts of the
world (Table 2).[3] They occur naturally or may be induced either through continuous monoculture or through
the addition of organic amendments. Among the bestknown are those suppressive to diseases caused by
oomycetes and fungi such as Pythium, Phytophthora,
Fusarium, Rhizoctonia, and Gaeumannomyces. The level
of disease control is related predominantly and directly to
unique microbiological properties associated with the
soils themselves or, more importantly, with the spermosphere or rhizosphere of plants grown in these soils.[4]
Although the specific microorganisms providing the
disease control are generally not known, suppressive soils
provide some of the best examples of effective biological
control where they can serve as models for understanding
how microorganisms in their natural habitats might be
manipulated to reduce plant disease losses.
Among the best examples of naturally suppressive soils
are those suppressive to Fusarium wilt diseases of various
crops.[5] These soils are characterized by elevated populations of nonpathogenic Fusarium and fluorescent Pseudomonas species. These organisms compete with pathogenic species of Fusarium for carbon and iron, resulting in
reduced plant infection.
Suppressiveness can be induced in soils either through
the introduction of organic amendments or, in some cases,
from crop monoculture. Organic soil amendments, particularly composts, have been studied extensively for their
ability to induce suppressiveness to many oomycete and
fungal diseases.[6] These studies confirm the involvement
of compost-associated and soil-enhanced microbial communities in the suppressive properties of amended soils.
The identities of the specific microorganisms contributing
to this suppressiveness remain elusive.
The most widely studied example of induced disease
suppressiveness in soils is the take-all decline phenomenon following cereal monoculture. Continuous cereal
monoculture has been observed worldwide to result in the
gradual decline in the severity of take-all disease caused
by Gaeumannomyces graminis var. tritici (Ggt). The
natural selection provided by monoculture results in the
buildup of specific antibiotic producing Pseudomonas
species on and in Ggt lesions on cereal roots that suppress
root infection by Ggt.[7] If this cropping strategy is
interrupted, disease suppression is lost.
CONCLUSION
The unpredictable nature of biological control systems has
plagued research in this field for over 80 years and to date,
B
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140
no clear means of overcoming this variability has been
discovered. Insights into how individual or communities
of biological control organisms succeed and how they fail
can come only from a detailed understanding of how these
organisms function during their interaction with the
pathogen, the plant, and the environment in which they
are placed.
Knowledge of specific microbial traits essential for
biological control activity and the important regulatory
role played by the plant, whether it be in eliciting preinfection developmental responses of pathogens, or
in regulating the pathogen-suppressive behavior of introduced biological control microorganisms, is crucial
to the ultimate success of biological control strategies.
By understanding how the host, pathogen, and associated
microbes contribute to biological control processes, we
will be able to predict better and manipulate microbial behavior with the goal of enhancing biological disease control.
ARTICLES OF FURTHER INTEREST
Biological Control in the Phyllosphere, p. 130
Fungal and Oomycete Plant Pathogens: Cell Biology,
p. 480
Management of Fungal and Oomycete Diseases: Fruit
Crops, p. 678
Management of Fungal and Oomycete Diseases: Vegetable Crops, p. 681
Mechanisms of Infection: Oomycetes, p. 697
Biological Control of Oomycetes and Fungal Pathogens
Oomycete-Plant Interactions: Current Issues in, p. 843
Population Genetics of Plant Pathogenic Fungi, p. 1046
Rhizosphere Management: Microbial Manipulation for
Biocontrol, p. 1098
REFERENCES
1.
Cook, R.J.; Baker, K.F. The Nature and Practice of
Biological Control; The American Phytopathological Society: St Paul, 1983.
2. Harman, G.E. Myths and dogmas of biocontrol—Changes in
perceptions derived from research on Trichoderma harzianum T-22. Plant Dis. 2000, 84 (4), 377 – 393.
3. Hornby, D. Suppressive soils. Annu. Rev. Phytopathol.
1983, 21, 65 – 85.
4. Whipps, J.M. Microbial interactions and biocontrol in the
rhizosphere. J. Exp. Bot. 2001, 52, 487 – 511.
5. Alabouvette, C. Fusarium wilt suppressive soils: An
example of disease-suppressive soils. Aust. Plant Pathol.
1999, 28 (1), 57 – 64.
6. Hoitink, H.A.J.; Boehm, M.J. Biocontrol within the context of soil microbial communities: A substrate-dependent phenomenon. Annu. Rev. Phytopathol. 1999, 37, 427 –
446.
7. Weller, D.M.; Raaijmakers, J.M.; Gardener, B.B.M.;
Thomashow, L.S. Microbial populations responsible for
specific soil suppressiveness to plant pathogens. Annu. Rev.
Phytopathol. 2002, 40, 309 – 348.
8. Schneider, R.W. Suppressive Soils and Plant Disease; The
American Phytopathological Society: St. Paul, 1982.
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