Trichoderma spp.: A biocontrol agent for sustainable management of plant diseases

Abstract

Trichoderma spp. are mainly asexual fungi that are present in all types of agricultural soils and also in decaying wood. The antagonistic activity of Trichoderma species showed that it is parasitic on many soil-borne and foliage pathogens. The fungus is also a decomposer of cellulosic waste materials. Recent discoveries show that the fungi not only act as biocontrol agents, but also stimulate plant resistance, and plant growth and development resulting in an increase in crop production. The biocontrol activity involving mycoparasitism, antibiotics and competition for nutrients, also induces defence responses or systemic resistance responses in plants. These responses are an important part of Trichoderma in biocontrol program. Currently, Trichoderma spp., is being used to control plant diseases in sustainable diseases management systems. This paper reviews the published information on Trichoderma spp., and its biocontrol activity in sustainable disease management programs.

Full text

Pak. J. Bot., 46(4): 1489-1493, 2014.
TRICHODERMA SPP.: A BIOCONTROL AGENT FOR SUSTAINABLE
MANAGEMENT OF PLANT DISEASES
LAILA NAHER1,2*, UMI KALSOM YUSUF2, AHMAD ISMAIL2 AND KAUSAR HOSSAIN3
1Faculty of Agro Based Industry, Universiti Kelantan Malaysia,17600 Jeli, Kelantan
2Department of Biology, Faculty of Science, Universiti Putra Malaysia, 43400 Serdang, Malaysia
3Laboratory of Food Crops, Institute of Tropical Agriculture, Universiti Putra Malaysia, 43400 Serdang, Selangor, Malaysia
*Corresponding author e-mail: umikay@science.upm.edu.my; laila_islam@yahoo.com
Abstract
Trichoderma spp. are mainly asexual fungi that are present in all types of agricultural soils and also in decaying wood. The
antagonistic activity of Trichoderma species showed that it is parasitic on many soil-borne and foliage pathogens. The fungus is
also a decomposer of cellulosic waste materials. Recent discoveries show that the fungi not only act as biocontrol agents, but
also stimulate plant resistance, and plant growth and development resulting in an increase in crop production. The biocontrol
activity involving mycoparasitism, antibiotics and competition for nutrients, also induces defence responses or systemic
resistance responses in plants. These responses are an important part of Trichoderma in biocontrol program. Currently,
Trichoderma spp., is being used to control plant diseases in sustainable diseases management systems. This paper reviews the
published information on Trichoderma spp., and its biocontrol activity in sustainable disease management programs.
Introduction
Plant disease management as well as improvement of
yields using traditional methods such as chemical
pesticides, herbicides, or fertilizer are not an ecofriendly
approach, as they consist of various aromatic groups or
methylated and ethylated substances which to a large extent
have extreme effects on the environment. Long term using
of chemical pesticides contaminate water, cause
atmosphere pollution, and some-times leave harmful
residues which can lead to development of certain resistant
organisms. To overcome these problems researchers look
for alternative options such as the use of bicontrol agents
(BCA) for disease control either alone or in an integrated
approach with other chemicals for ecofriendly and
sustainable methods of disease control. Currently, several
biocontrol agents have been recognized and are available as
bacterial agents for example Pseudomas, Bacillus, and
Agrobacterinum, and as fungal agents such as Aspergillus,
Gliocladium, Trichoderma, Ampelomyces, Candida, and
Coniothyrium (Papavizas, 1985; Koumoutsi et al., 2004;
Mavrodi et al., 2002; Atehnkeng et al., 2008; Gilardi et al.,
2008). Among these biocontrol agents Trichoderma spp. is
one of the most versatile biocontrol agents which has long
been used for managing plant pathogenic fungi. A previous
study found that the disease of seed rot, damping off, root
rot of sunflower and mugbean caused by Sclerotium rolfsii
was prevented as well as the plant growth was enhanced
when plants were treated with the conidial suspensions of
Trichoderma spp. (Yaqub & shahzad, 2008). The
pathogenic fungal growth of Ganoderma was inhibited by
T. harzianum and T. virens (Naher et al., 2012).
Trichoderma spp., are typical anaerobic, facultative
and cosmopolitan fungi that can be found in large numbers
in agricultural soils and in other substrates such as decaying
wood (Samuels, 1996; Irina & Christian, 2004). They
belong to the subdivision Deuteromycetes, members of
which do not have or do not exhibit a determinate sexual
state as most strains are adapted to an asexual life cycle
(Harman, 2004a). The role of Trichoderma spp. is not only
to control growth of pathogenic microbes, but there are
various other uses for Trichoderma such as, i) stimulate
colonization of rhizosphores, (ii) stimulates plant growth,
root growth, and (iii) enhance plant defence responses
(Vinale et al., 2008; Harman, 2004a).
In the early 1930s Trichoderma was introduced as
possessing biocontrol ability (Weindling, 1934).
Trichoderma is an opportunistic, avirulent plant symbiont
fungus which acts as an antagonistic and parasitic fungus
against many plant pathogenic fungi and offers protection
from phytopathogenic plant diseases. It has been proven in
numerous studies that Trichoderma spp. are effective
biocontrol agents for managing plant disease, and currently
commercial products of Trichoderma are available as
biopesticides or soil amendments or as enhancers for plant
growth (Papavizas, 1985; Chet 1987; Harman, 2004a;
Vinale et al., 2008). Weindling (1932) demonstrated the
biocontrol activity of Trichoderma lingnorum (viride) on
soil-borne fungal pathogen of Rhizoctonia solani. Later the
mycoparsitic action of the same species of Trichoderma on
Phytophthora, Pythium, Rhizopus and Sclerotium rolfsii
was observed (Well, 1988). Today fungal biocontrol
observation and foundation are based on Trichoderma spp.
and thus, this fungus has drawn much attention as a
biocontrol model (Chet, 1993).
This review paper highlights information on the
mechanisms of Trichoderma biocontrol activity and its role
as a plant health enhancer, its commercial production and
applications.
Biocontrol mechanisms of Trichoderma spp.:
Trichoderma spp. are biocontrol agents effective against
fungal phytopathogens. They can act indirectly, by
competing for nutrients and space, modifying
environmental conditions, or promoting plant growth and
plant defensive mechanisms and antibiosis, or directly, by
mechanisms such as mycoparasitism (Papavizas, 1985;
Howell, 2003; Vinale et al., 2008). The mechanisms can
be described as:
i. Biocontrol by competition for nutrients and living
space: Trichoderma spp., are rapidly growing fungi that
have persistent conidia and a broad spectrum of substrate
utilization. They are very efficient competitors for nutrition
and living space (Hjeljord et al., 2000). In addition,
Trichoderma spp., are naturally resistant to many toxic
compounds, including herbicides, fungicides, and phenolic
compounds. Therefore, they can grow rapidly and impact
pathogens by producing metabolic compounds that impede

LAILA NAHER ET AL.,
1490
spore germination (fungistasis), kill the cells (antibiosis), or
modify the rhizosphere, (e.g. by acidifying the soil so that
the pathogens cannot grow) (Benitez et al., 2004).
Starvation is the most common cause of death for
microorganisms, so competition for limited nutrients is
especially important in the biocontrol of phytopathogens.
Iron uptake is essential for filamentous fungi and under
iron starvation; fungi excrete low-molecular weight ferric-
iron-specific chelators, termed siderophores. Trichoderma
spp. produce highly efficient siderophores that chelate iron
and stop the growth of other fungi (Benitez et al., 2004).
Therefore, soil characteristics influence Trichoderma as a
biocontrol agent.
ii. Biocontrol by mycoparasitism: The direct interaction
between Trichoderma and pathogen is called
mycoparasitism. As mentioned earlier, Weindling (1932)
was the first to recognize that Trichoderma spp., is a
biocontrol agent and at the same time he also noticed
mycoparasitism of T. lignorum (viride) hypae coiling and
killing R. solani (Wells, 1988). Mycoparasitism is a
complex mechanism that generally involves the production
of a cell wall lytic enzyme. Chet et al., (1998) described
that the mycoparasitism process involves four sequential
steps: chemotropism and recognition; attachment and
coiling; cell wall penetration; and digestion of host cell.
Trichoderma strains detect other fungi, grow straight
towards them, and sequentially produce hydrolytic cell-
wall degrading enzymes. Trichoderma attach to the host,
and coil hyphae around the host, form appressoria on the
host surface, penetrate the host cell, and collapse the host
hyphae (Steyaert et al., 2003).
The molecular level induction of mycoparasitism
was first reported in 1994 (Carsolio et al., 1999), based
on the study of regulation of an endochitinase-encoding
gene (ech42). Ech42 was expressed during the
mycoparasitic interaction between T. harzianum and
Rhizoctonia solani. Another study showed that in the
P1 mutant strain of T. atroviride, the expression of
exochitinase nagI or endochitinase ech42 gene was
needed to induce mycoparasitism in treatments
containing purified colloidal chitin from the fungal cell
walls (Vinale et al., 2008). Production and regulation
of lytic enzymes such as chitinases, glucanases, and
proteases by Trichoderma spp. also play key roles in
the mycoparasitism/biocontrol process (Mukherjee et
al., 2008).
Plant growth enhancement by Trichoderma spp.:
Trichoderma spp. are not only control pathogens, they also
enhance plant growth and root development (biofertilizer)
and stimulate plant defence mechanisms (Harman, 2004a).
Some Trichoderma strains have been shown to penetrate
the epidermis and establish robust and long-lasting
colonization of root surfaces (Harman, 2004a).
Trichoderma spp. have been shown to improve growth of
lettuce, tomato and pepper plants (Vinale et al., 2006). In a
study of maize plants, several months after treatment with
Trichoderma harzianum strain T-22, the plant roots were
about twice as long when compared to untreated plants
(Harman, 2004a). Cutler (1986, 1989) showed that the
secondary metabolites produced by Trichoderma koningii
(koniningin A) and Trichoderma harzianum (6-pentyl-
alpha pryone) act as plant growth regulators. Trichoderma
spp. also produced gluconic and citric acids, decreased the
soil pH, and enhanced the solubilization of phosphates,
micronutrients, and mineral components such as iron,
magnesium, and manganese (Benitez et al., 2004; Harman
et al., 2004b; Vinale et al., 2008).
Induction of plant defence by Trichoderma spp.: It is
well documented that Trichoderma spp. induce gene
expression of proteins in plants such as chitinase,
glucanase, and peroxidase against antagonistic microbes
(Yedidia et al., 2003; Hanson et al., 2004; Harman, 2004b).
It has also been shown that pre-treatment of plants with
Trichoderma spp. increased plant resistance to pathogen
attack (Harman, 2004a). Trichoderma spp. are
opportunistic invaders, fast growers and large spore
producers. They contain cell wall degrading enzymes (e.g.,
celluloses, chitinases, and glucanases) and produce
antibiotics (Vinale et al., 2008). Moreover, the presence of
Trichoderma spp. stimulates the induction of the
hypersensitive response, systemic acquired resistance
(SAR), and induced systemic resistance (ISR) in plants
(Benitez et al., 2004; Vinale et al., 2008). For example,
tomato plants colonized by T. hamatum actively induced
systemic changes in plant physiology and disease resistance
(Alfano et al., 2007). In a study of cucumber plants, T.
asperellum induced a systemic response of two defence
genes encoding phenylalanine and hydroperoxidase lyase
and systemic accumulation of phytoalexins against
Pseudomonas syringae pv. lachrymans (Yedidia et al.,
2003). In oil palm plants the defence gene of chitinase
expression was increased in T. harzianum and Ganoderma
boninense treated plants compared to G. boninense alone
treated plants (Naher et al., 2011). Several studies also
showed that Trichoderma spp. may indirectly contribute to
systemic resistance (Ahmed et al., 2000; Lo et al., 2000).
Harman et al., (2004a) reported that the induction of
localized or systemic resistance is an important component
for plant disease control by Trichoderma spp. Thus, disease
control by root-colonizing Trichoderma spp. involves a
complex interaction between the host plant, the pathogen,
the biocontrol agent and several environmental factors
(Harman, 2004a; Hoitink, et al., 2006; Alfano et al., 2007).
Plant root colonization by Trichoderma spp.: Studies
of the early invading fungi Trichoderma spp. showed
that root colonization stimulated plant defence responses
such as induction of peroxidases, chitinases, β-1, 3
glucanase, phenylalanine, and hydroperoxidase lyase;
activated signaling of biosynthetic pathways; and caused
accumulation of low-molecular weight phytoalexins
(Howell et al., 2000; Yedidia et al., 2003; Harman et al.,
2004a;). Yedidia et al., (1999) observed the physical
interaction between T. harzianum T-203 and a cucumber
plant under the electron microscope and found that the
fungus penetrated the root and grew in the epidermis and
outer cortex, which stimulated increases of peroxidase
and chitinase. Therefore, the interaction appears to be a
symbiotic relationship in which Trichoderma lives in the
nutritional niche provided by the plant, and the plant
was protected from disease.

A BIOCONTROL AGENT FOR SUSTAINABLE MANAGEMENT OF PLANT DISEASES 1491
Production of antibiotics and secondary compounds by
Trichoderma spp.: Secondary compounds and antibiotics
produced by Trichoderma spp. play a vital role in
antagonistic biocontrol activity (Vinale et al., 2008; Ajitha &
Lakshmidevi, 2010). Sivasithamparam and Ghisalberti
(1998) reported that Trichoderma spp. produced several
secondary compounds, including antibacterial and antifungal
antibiotics such as polyketides, pyrones, and terpenes.
Secondary metabolites, including antibiotics, that are not
directly involved in natural growth, development, or
reproduction and are chemically different from natural
compounds may play important roles in the defence
response, symbiosis, metal transport, differentiation, and
stimulating or inhibiting spore formation and germination
(Demain & Fang, 2000; Vinale et al., 2008). Antibiotics are
often associated with biocontrol activity. For example, the
production of a pyrone-like antibiotic from T. harzianum
exhibited biocontrol activity against Ganumannomyces
graminis (Ghisalberti et al., 1990). The peptide antibiotic
paracelsin was the first secondary metabolite characterized in
Trichoderma spp. (Bruckner & Graf, 1983; Bruckner et al.,
1984). Sivasithamparam & Ghisalberti (1991) suggested that
secondary metabolites produced by Trichoderma spp., can
be grouped into three categories: (i) volatile compounds
(e.g., 6-pentyl-alpha-pyrone), (ii) water-soluble compounds
(e.g., heptelidic acid), and (iii) peptaibol compounds, which
are linear oligopeptides composed of 12-22 amino acids that
are rich in alpha-aminoisobutyrate, N-acetylated at the N-
terminus and have an amino alcohol group at the C-terminus.
Other uses of Trichoderma spp.: The discovery of
cellulase production by Trichoderma reesei, which was
isolated by Reese (1976), led to it becoming a very
important cellulase or enzyme producer. The cellulase
produced by Trichoderma spp. is used mainly for malting,
baking, and grain alcohol production (Galante et al.,
1998b). The filamentous cellulolytic Trichoderma spp.,
produce a broad range of cellulases and hemicellulases.
The main application of lignocellulosic biomass is the
production of biofuels such as ethanol (Lin & Tanaka,
2006; Gimbert et al., 2008), although it is also used in the
pulp, paper and textile industries (Galante et al., 1998a).
Trichoderma spp. are also used for safe industrial enzyme
production (Nevalaines et al., 1994). Macerating enzymes
are used to improve the brewing process for fruit juice
production and as a feed additive for livestock and pet food
(Schaster & Schmoll, 2010). Trichoderma also used for
seed germination for example, a study showed that
sunflower seeds germination significantly increased in T.
viride or T. resei treated plants compared to control plants
(Anis et al., 2012). The commercial use of several
Trichoderma species for the protection and growth
enhancement of a number of crops is ongoing (Lumsden et
al., 1993; Samuels, 1996). Currently, the commercially
available formulations are RootShieldTM, BioTrek 22TM, T-
22GTM, and T-22HBTM (Bio-works, USA); SuprevisitTM
(Borregaard BioPlant, Denmark); BinabTM (Bio-Innovation
Sweden); TrichopelTM, TrichojetTM, TrichodowelsTM, and
TrichosealTM (Agimm, New Zealand); TriecoTM (Ecosense
Labs, India), and Tricho-green (Mycology Lab, Malaysia).
Not all of these products are registered as biocontrol agent,
but they are marketed as plant growth promoters, plant
strengtheners, or soil conditioners.
Conclusion
In 1930, Weindling first discovered the genus
Trichoderm spp. as a biocontrol agent and since then
numerous studies have demonstrated that Trichoderma
is an effective bicontrol agent for phytopathogenic
microorganisms (Harman, 1996). A biocontrol program
is only established when the bicontrol agent can
successfully manage the interaction between the host
plant and pathogen. The ability of Trichoderma to
successfully manage this interaction has been well
established. The fungi have also been demonstrated to
enhance the defence responses in plants. Thus, as an
effective biocontrol agent the use of Trichoderma will
certainly ensure sustainable disease management.
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(Received for publication 30 January 2013)