Professional Documents
Culture Documents
Re v ie w
1 Institute of Plant Genetics, Polish Academy of Sciences, Strzeszyńska 34, 60-479 Poznań, Poland
2 University of Life Sciences, Department of Vegetable Crops, Dąbrowskiego 159, 60-594 Poznań, Poland
Abstract: Fungi of the genus Trichoderma are a very large group of microorganisms that play a significant role in the environment.
They use a variety of mechanisms to colonise various ecological niches. Several Trichoderma spp. positively affect plants by stimulating
plant growth, and protecting plants from fungal and bacterial pathogens. They are used in biological plant protection as biofungi-
cides as well as in bioremediation. Members of the genus Trichoderma are also utilised in various industry branches – mainly in the
production of enzymes, antibiotics, and other metabolites, but also of biofuel. Moreover, the genus Trichoderma comprises edible and
medicinal mushrooms, but also the pathogens of humans. Currently, Trichoderma has entered the genomic era and parts of genome se-
quences are publicly available. This is why, Trichoderma fungi have the potential to be used for human needs to an even greater extent
than before. Nevertheless, further studies are needed to increase the efficiency and safety of the application of these fungi.
Key words: biological plant protection, cell wall degrading enzymes, green mould
*Corresponding address:
mjed@igr.poznan.pl
310 Journal of Plant Protection Research 54 (4), 2014
Fig. 1. The variation of colours and morphology of the fungal colonies of Trichoderma spp. are shown on Potato Dextrose Agar (PDA)
medium. Upper row, then lower row (from left) are: T. cremeum (strain AN 392), T. longipile (AN 414), T. viride (AN 253),
T. harzianum (AN 261), T. atroviride (AN 287), and T. citrinoviride (AN 262)
random amplified polymorphic DNA markers (RAPD) mechanisms facilitating colonisation of different eco-
and coding sequence variation phylogenetic markers logical niches are well-developed and highly diverse in
for molecular species identification, had a considerable Trichoderma spp. (Herrera-Estrella and Chet 2004; Har-
influence on the development of taxonomy at that time. man 2006; Vinale et al. 2008). Trichoderma interacts with
From the late 1990’s up to the year 2002, the number of other microorganisms, but mainly with pathogenic fungi.
Trichoderma species increased to 47 (Kullnig-Gradinger et These interactions include hyperparasitism, competition,
al. 2002). The verification of the taxonomy of the entire and antibiosis.
genus was started by Kindermann et al. (1998) who ana- Hyperparasitism is connected with the direct contact
lysed the internal transcribed region 1 (ITS1) sequence of an antagonist with a pathogen and is composed of such
of the rRNA coding region. Further development of mo- stages as: pathogen recognition, attack, gradual penetra-
lecular methods, including the presentation of the first tion of the pathogen cells and death (Vinale et al. 2008).
fungal oligonucleotide barcode for the identification of In this process a considerable role is played by CWDE
Hypocrea and Trichoderma species – TrichOKey version 1.0 (Cell Wall Degrading Enzymes) lytic enzymes, synthe-
(Druzhinina et al. 2005), has contributed to the doubling sised by Trichoderma species that facilitate hydrolytic
of the number of newly described species. At present, the degradation of pathogen cell walls, composed of chitin
International Subcommission on Trichoderma/Hypocrea and glucan polysaccharides. Trichoderma species are also
(http://www.isth.info/biodiversity//index.php) lists 104 capable of producing cell wall degrading enzymes such
species established on the basis of phylogenetic analyses. as cellulase, xylanase, pectinase, glucanase, lipase, amy-
According to Jaklitsch (2009), 75 species have been identi- lase, arabinase, and protease (Strakowska et al. 2014) as
fied in Central Europe. However, it should be stressed that well as many volatile metabolites, such as 6-n-pentyl-2H-
the number of the so-called morphological species has not -pyran-2-one (6-PAP) (Jeleń et al. 2013). Chitinases are the
increased dramatically and at present it amounts to 1/3 of most important lytic enzymes playing a key role in the
the species described on the basis of molecular analyses. degradation of cell walls of other plant pathogenic fungi.
Chitinolytic enzymes identified in Trichoderma species
(T. harzianum, T. atroviride P. Karst. and T. asperel-
Interaction of Trichoderma with other lum Samuels, Lieckf. & Nirenberg) include β-N-
microorganisms and plants acetylglucosamidase, endochitinase, and chitobiosidase
Fungi from the genus Trichoderma, due to their coloni- (Haran et al. 1996). Other enzymes determining the ca-
sation of different environments, are forced to compete pacity of Trichoderma fungi for hyperparasitism, mainly
for nutrients and space with many other organisms. The in relation to fungus-like organisms, i.e. Phytophthora sp.
Trichoderma spp. – application and prospects for use in organic farming and industry 311
and Pythium sp. are β-1,3- and β-1,6-glucanases (Lorito T. viride; trichorzianins A and B, trichorzins HA and MA
et al. 1994; Thrane et al. 1997). An important role is also found in the cultures of T. harzianum; tricholongins BI
attributed to proteolytic enzymes (endo- an exoprote- and BII, and longibrachins produced by T. longibrachia-
ases), which in Trichoderma are responsible for the con- tum; trichokonins originating in cultures of T. koningii, as
trol of exocellular enzyme secretion. The proteolytic en- well as atroviridins A-C and neoatroviridins A-D isolated
zymes influence the activity and stability of exocellular from cultures of T. atroviride. Other compounds with an-
enzymes and participate in post-secretion modifications tibacterial and fungicidal properties (R. solani, F. oxyspo-
of cellulases (Viterbo et al. 2004). Proteolytic enzymes rum, Botrytis alli, Penicilium expansum, Aspergillus niger,
also affect enzymatic activity of pathogenic fungi such Escherichia coli, Bacillus subtilis, Pseudomonas aeruginosa,
as Botrytis cinerea, Rhizoctonia solani, Fusarium culmorum, Bacterioides fragilis) include koningins, viridin, dermadin,
and nematode Meloidogyne javanica (Sharon et al. 2001). trichoviridin, lignoren, and koningic acid, produced by T.
Cellulases form yet another group of enzymes produced koningii, T. harzianum, T. aureoviride, T. viride, T. virens (J.H.
by the Trichoderma species. These enzymes are capable of Mill., Giddens & A.A. Foster) Arx, T. hamatum, and T. lig-
hydrolysing lignocellulose biomass and comprise three norum (Tode) Harz (Reino et al. 2008). When discussing
types of enzymes which act synergistically. The three secondary metabolites produced by fungi from the ge-
types are exo-β-1,4-glucanases, endo-β-1,4-glucanases, nus Trichoderma, it should be noted that literature sourc-
and β-glucosidases (Enari and Niku-Paavola 1987). es have reported examples of isolates that were able to
As often reported in scientific research articles, spe- synthesise compounds considered toxic to humans and
cies from the genus Trichoderma compete with pathogens animals. Gliotoxin was the first toxin detected in those
for nutrients, ecological niches or infection sites on plant species. Production of this mycotoxin was observed in
roots. Certain Trichoderma strains are capable of produc- certain isolates belonging to such species as T. lignorum,
ing siderophores, which are iron chelating compounds. T. virens (G. virens), T. viride, and T. hamatum (Reino et al.
By trapping iron, ions from the environment certain 2008). Corley et al. (1994) identified strains of T. harzianum
Trichoderma strains inhibit the growth of other fungi, e.g. capable of synthesising harzianum A toxin, then 10 years
B. cinerea, which is strongly affected by a nutrient deficit. later Gallo et al. (2004) isolated from the same species
Trichoderma fungi may also acidify the environment, pro- a gene (tri5) homologous to the gene encoding trichodi-
ducing adverse conditions for the development of other ene sythetase in Fusarium spp.
fungi (Benitez et al. 2004). Furthermore, Trichoderma fun- In Trichoderma fungi, the activity of antibiotics is fre-
gi are capable of intensive colonisation of the plant root quently combined with the activity of lytic enzymes.
zone. Benitez et al. (2004) claimed that the mechanisms in- Their joint action provides a higher level of antagonism
volved in this process are similar to those in mycorrhizal compared to the activity of either enzymes or antibiot-
fungi. In the T. harzianum strain, an enhanced activity of ics alone (Monte 2001). According to Howell (2003), pre-
the so-called hydrophobins was shown during plant root liminary degradation of the cell walls in B. cinerea and F.
colonisation, causing attachment of mycelial filaments to oxysporum by lytic enzymes facilitated easier penetration
hydrophobic root surfaces. In addition, Trichoderma strains of antibiotics to pathogen cells.
are resistant to toxic compounds produced by plants in When considering the interactions of Trichoderma fun-
response to infection, e.g. phytoalexins, flavonoids, terpe- gi with plants, it was found that these fungi have an ad-
noids, and phenols, which prevent root colonisation. vantageous effect on plants. Stimulation of plant growth
Antibiosis is a specific mechanism of antagonistic and yield takes place thanks to this interaction and the
interactions between Trichoderma fungi and other patho- advantageous effects are seen in the production of vita-
genic fungi. Antibiosis is based on the generation of sec- mins, the increased availability of biogenic elements (ni-
ondary metabolites, which exhibit an inhibitory or lethal trogen, phosphorus), the mobilisation of nutrients from
effect on a parasitic fungus. In fungal species from the the soil and from organic matter, and the enhanced inten-
genus Trichoderma, over 180 secondary metabolites have sity of mineral uptake and transport.
been characterised up to date, representing different Furthermore, Trichoderma fungi are capable of produc-
classes of chemical compounds (Gams and Bisset 1998; ing zeaxanthin and gibberellin, i.e. compounds accelerat-
Reino et al. 2008). These compounds may be divided into ing seed germination. Many Trichoderma strains produce
volatile antibiotics, water soluble compounds and peptai- acids, e.g. gluconic, citric, and coumaric acids, causing
bols. T. viride, T. harzianum, and T. koningii are able to pro- the release of phosphorus ions and microelements, which
duce 6PAP (6-pentyl-α-pyrone) that belongs to the group subsequently become available to plants (Harman et al.
of volatile antibiotics playing a role in biocontrol of such 2004). Yedidia et al. (2001), after applying T. harzianum
species as B. cinerea, R. solani, and Fusarium oxysporum. to growing cucumber, reported an increase in root mass
Peptaibols are polypeptide antibiotics of 500–2200 Da, and aboveground mass of plants as well as higher micro-
rich in non-proteinogenic amino acids, in particular alfa- element contents. Whereas, in the study by Porras and
aminoisobutyric acid, and their characteristic attributes colleagues (2007), fungi from the genus Trichoderma had
include the presence of N-acetylated ends and C-end a positive effect on strawberry yields.
amino alcohols (Degenkolb et al. 2003). Peptaibols exhibit Numerous authors (Howell 2003; Khan et al. 2004;
potent activity against a number of fungi and Gram-posi- Brunner et al. 2005; Woo and Lorito 2007) have reported
tive bacteria as well as against some viruses. Compounds that Trichoderma fungi stimulate systemic resistance in
belonging to this class include trichotoxins A and B, trich- plants. When colonising the rhizosphere of plants, Tricho-
odecenins, trichorovins, and trichocellins synthesised by derma acts against fungal, bacterial, and viral diseases af-
312 Journal of Plant Protection Research 54 (4), 2014
fecting the aboveground parts (Benitez et al. 2004). Based In many countries biocontrol products are based on
on numerous studies, a conclusion can be drawn that fungi from the genus Trichoderma. These products reduce
various groups of metabolites may play the role of elici- the development of diseases, stimulate plant growth,
tors or so-called resistance inducers in the interactions enhance their stress resistance, and accelerate compost-
of Trichoderma with plants (Harmann et al. 2004). These ing (Harman 2000). Bettiol and Morandi (2008) reported
metabolites include proteins exhibiting enzymatic activ- that cultivation costs are considerably reduced when us-
ity (e.g. xylanases, chitinases), gene products resembling ing Trichoderma. Howell (2003) claimed that most effec-
proteins encoded by avirulent genes, and low molecular tive strains of active microorganisms need to be collected
compounds released from cell walls of fungi or plants by from the regions in which they will be applied. Further-
fungal hydrolytic enzymes. In plants, an increase is ob- more, as it was observed by Monte (2001), the application
served in the concentration of enzymes and metabolites of Trichoderma with reduced fungicide doses in integrated
responsible for the induction of resistance, e.g. phenyl- farming, results in enhanced plant health − comparable
alamine ammonia lyase (PAL), phytoalexins, chitinases, with the level of protection provided by the application
and glucanases (Shoresh et al. 2005). Yedidia et al. (1999) of full fungicide doses. This fact makes it possible to re-
stated that inoculation of cucumber roots with spores of duce cultivation costs and has a positive effect on the
T. harzianum induced resistance reactions in the whole environment (Dubey et al. 2007). The literature describes
plants, which was connected with the increased activity numerous success stories of the use of biopreparations
of peroxidase and chitinase. As it was shown above, Trich- based on Trichoderma. Sometimes the comparisons of re-
oderma species are mostly opportunistic plant symbionts, sults obtained in different countries are not possible, due
with recognisable traits of hyperparasitism and antibiosis to the use of different strains, the ways of their growth
towards many pathogenic fungi. Trichoderma species are and preparation, various ways of formulation and com-
capable of producing enzymes and numerous secondary mercial names and doses.
metabolites, mainly antibiotics, which make them impor-
tant microorganisms from the point of view of ecology,
agriculture, and industry.
Other applications of Trichoderma
The multi-sided activity of fungi from the genus Tricho-
derma provides a potential for their extensive applications
Application of Trichoderma in in different branches of economy. Several species are fre-
biological plant protection quently used in the degradation of organic pollutants.
Trichoderma fungi are microorganisms that are most fre- Bioremediation is often provided e.g. by T. harzianum,
quently tested and applied in biological plant protection. which detoxifies phenols, cyanides, and nitrates (Lynch
The use of Trichoderma fungi may cause a considerable and Moffat 2005). The capacity of Trichoderma fungi to
limitation in the use of chemical fungicides in agriculture produce lytic enzymes is used in animal feed, and wine
(Akhtar and Siddiqui 2008). It is estimated that 90% of all making and brewery industries. Cellulases, hemicellu-
antagonistic fungi used in plant protection belong to the lases, and pectinases produced by Trichoderma fungi are
genus Trichoderma (Benitez et al. 2004). Many scientific re- used in the partial hydrolysis of plant cell walls in feeds,
ports focus on the positive effect of these fungi on plants enhancing the digestibility of the feed and increasing the
(Hermosa et al. 2012). These reports focus on the efficacy nutritive value of the feed. This leads to increased body
of these fungi when it comes to disease control in the cul- weight gains in animals and higher milk yields (Galante
tivation of numerous agricultural and horticultural crops, et al. 1998b). Enzymes obtained from Trichoderma may
ornamental plants, and in fruit farming (Harman 2000; also be used as food additives, e.g. to increase raw mate-
Howell 2003; Benitez et al. 2004; Smolinska et al. 2007). rial maceration in the production of fruit and vegetable
For example, recent studies showed the potential of Trich- juices. The enzymes are also used to improve wine fla-
oderma spp. to control stem canker of brassicas, caused vour and enhance fermentation, filtration, and quality of
by Leptosphaeria maculans and L. biglobosa (Kaczmarek and beer (Blumenthal 2004).
Jedryczka 2011), with disease severity greatly depending Cellulases produced by Trichoderma are applied in the
on avirulence genes in fungi vs. resistance genes in plants textile industry to soften and condition the textiles as well
(Kaczmarek et al. 2014). The species of Trichoderma signifi- as to produce high quality washing powders. Enzymes
cantly differed in their hyperparasitic effects towards Lep- obtained from Trichoderma are also used in the pulp and
tosphaeria spp. The highest decrease in fungal growth rate paper industry to modify fibre properties and to reduce
was caused by T. atroviride (Dawidziuk et al. 2013). lignin contents (Galante et al. 1998a). In turn, mutanase
Disease control treatments using Trichoderma spp. are obtained from T. harzianum may be added in the produc-
also used in storage practice, e.g. for strawberry fruits tion of toothpaste to help prevent the formation of plaque
(Hjeljord et al. 2000) and apples (Batta 2004). The effec- (Wiater et al. 2005).
tiveness of Trichoderma fungi has been confirmed in the Cellulases and hemicellulases produced by T. re-
control of many fungal pests of plants (Lewis and Lums- esei Simmons are used in the production of bioethanol
den 2001; Dolatabadi et al. 2011). Trichoderma spp. are from farm waste. These enzymes catalyse degradation
also used in the control of bacterial and virus pests of of substrates to simple sugars, which are next sub-
crops (Hanson and Howell 2002). Moreover, studies have jected to fermentation by the yeasts Saccharomyces cere-
shown the usefulness of the species in weed control (He- viseae (Arthe et al. 2008). In the food industry, applica-
raux et al. 2005). tions have been found not only for enzymes, but also
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