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Give an account of the web of interactions between plants and biotrophic species of the fungal...

Give an account of the web of interactions between plants and biotrophic species of the fungal genus trichoderma in the rhizosphere that supports natural biocontrol systems. In your answer, outline how species of trichoderma defend plants against plant pathogens.

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Trichoderma have been reported as effective antagonists against Ganoderma boninense in coconut [1] and oil palm [2, 3, 4]. In 1990, [5] evaluated the incorporation of Trichoderma spp. grown on dried palm oil mill effluent into planting holes as a prophylactic measure. Later, [6] reported delays in infection in the field following treatment with Trichoderma, but eventually, the disease incidence was similar to untreated controls. Thus, the possible explanation for this could be due to a low natural occurrence of Trichodermaspp. in the soil [7]. In Malaysia, certain Trichoderma strains such as Trichoderma virens and Trichoderma harzianum have shown good biocontrol ability against G. boninense in nurseries [8]. Besides that, in Indonesia, a biofungicide consisting of Trichoderma koningii was reported to reduce BSR in decomposing oil palm residues in the field [9].

Biological control of BSR disease in oil palm can be effectively achieved through the utilization of an effective strain of Trichoderma spp. The strain must not only have the potential mechanisms for biological control such as antibiosis and mycoparasitism but also a strong competitive ability to displace the causative fungus G. boninense so as to reduce the pathogen’s opportunity for root colonization. It must be able to favorably compete and adopt well within the environment in which it will operate and be able to rapidly colonize and proliferate on the existing and newly formed roots immediately after its application [10].

2. Mechanisms of Trichoderma species

Trichoderma spp. employ several antagonistic mechanisms against plant pathogens. These include antibiosis, mycoparasitism, competition for nutrients and space, promotion of plant growth, induced plant defense mechanisms, and modification of environmental conditions [11].

2.1. Mycoparasitism

The potential of Trichoderma spp. to parasitize, suppress, or even kill other plant pathogenic fungi has been recognized as an important mechanism for its success as a biological control [12]. Mycoparasitism is a direct mechanism for biological control that works by parasitizing, detecting, growing, and colonizing pathogen [11, 13]. The ability to mycoparasitize other fungi has been widely used for the biological control of agricultural pests (mainly against pathogenic fungi and parasitic nematodes). Some species of Trichoderma such as T. asperellum, T. atroviride, T. virens, and T. harzianum are widely used as biological control agents of plant pathogens [11]. It is able to directly kill pathogens and other plant-associated fungi, with a wider host range in diverse ecologies [14]. This is done via the use of many mycoparasitic strategies [15, 16]. These mycoparasitic abilities appear to be very complex, involving the detection of plant pathogen through chemotropism; lysis of the pathogen’s cell wall (the key to mycoparasitism) [17]; pathogen’s hyphal penetration by appresorial formation; production of cell wall-degrading enzymes (CWDEs) and peptaibols, mediated by heterotrimeric G-proteins and mitogen-activated protein (MAP) kinases [11]; and parasitizing pathogen’s cell wall contents [12]. Degradation of pathogen’s cell wall during mycoparasitism is mediated by a set of hydrolytic enzymes including β-(1,6)-glucanases, chitinases, and proteases. Several members from each of these classes have been shown to be involved in mycoparasitism and/or to be induced under mycoparasitism-related growth conditions [18]. Genome analysis enabled the assessment of cell wall-degrading enzymes encoded in the genomes of Trichoderma spp. and unraveled even more complex enzymatic degradation machinery for fungal cell walls than previously anticipated [19].

Considerable research work has been done to identify and understand the enzymes induced by Trichoderma to recognize host pathogen [20]. The degradation of a pathogen’s cell wall is an important aspect of mycoparasitism and biological control of plant diseases. Trichoderma also produces secondary metabolites (volatile and nonvolatile) [21]. With regard to the production of secondary metabolites, two Trichoderma species—T. virens and T. reesei—are the highest producers of secondary metabolites [22].

Three important Trichoderma species—T. virens, T. atroviride, and T. harzianum—have been identified with the highest production of chitinolytic enzymes compared to other fungi known to have similar biological control abilities [21]. Most of the secondary metabolites’ coding gene clusters are exclusively specific to certain Trichoderma spp., while some are found in all three species [21]. Studies on the responsible signal transduction pathways of T. atroviride during mycoparasitism have led to the isolation of key constituents of MAP and cAMP kinase signaling pathways, such as the α-subunits of G-proteins (G-α) that control antibiotic production, extracellular enzyme, and coiling around host hypha [23].

2.2. Promoting plant growth

Microbial organisms colonize a plant’s root system and at the same time play a beneficial role in biological control, protecting the plant from soil-borne pathogens as well stimulating plant growth [13]. These beneficial relationships between plants and microbes often occur in the rhizosphere, improving plant growth or helping the plant overcome biotic or abiotic stresses [24]. Trichoderma spp. proliferate in the rhizosphere, establishing a symbiotic association, thus improving plant nutrition and growth in a natural way [25]. It is able to colonize roots, improving plant nutrition, growth, and development as well as enhancing plant resistance to abiotic stresses. Increasing plant growth by using biological control agents is usually attributed to an indirect effect associated with control of plant pathogens. It was also reported that the application of T. harzianum to cucumber or tomato seedlings increased the concentration of trace and essential elements such as Fe, Zn, Cu, Mn, Mg, Ca, N, P, K, and Na both in the shoots and roots [26]. This is due to its ability to produce many phytohormones, siderophores, and phosphate-solubilizing enzymes [27]. Phytohormones stimulate root growth, thus increasing the absorptive surface of plant roots. These phytohormones include cytokinins, indole-3-acetic acid, and gibberellins [28]. Growth promotion of plant antimicrobial compounds of Trichoderma has been demonstrated [29]. Harzianopyridone, 6PP, trichocereus A-D, koninginins, cyclonerodiol, harzianolide, and harzianic acid (HA) are examples of isolated compounds that promote plant growth in a concentration-dependent manner [30]. A novel secondary metabolite—cerinolactone—has been isolated and characterized from Trichoderma cerinums and was able to positively alter the growth of tomato seedlings 3 days after treatment [30]. Similarly, HA and iso-harzianic acid found in T. harzianum metabolites were also found to promote plant growth, through the strong binding of iron [30]. It was also shown that T. virens and T. atroviride produce certain types of indole-3-acetic acid-related indoles (IAA-related indoles). The production of IAA-related indoles in Trichoderma liquid cultures was stimulated by the addition of l-tryptophan. This observation proposed that the production of IAA-related indoles could be one of the mechanisms employed by Trichoderma to promote plant growth and an increase in the number of secondary roots, leading to a higher biomass in Arabidopsis [31]. On the other hand, [32] proposed that degradation of IAA by Trichoderma leads to a reduction of detrimental effects of IAA on root elongation that could cause reduced ethylene (ET) production, by decreasing its precursor, 1-aminocyclopropane-1-carboxylic acid (ACC), and/or ACC deaminase activity present in Trichoderma. Recently, it was shown that T. asperellum has high 1-aminocyclopropane-1-carboxylic acid deaminase (ACCD) activity when grown with ACC as the sole nitrogen source. The ACCD-encoding gene Tas-acdS was upregulated when ACC was added to the artificial growth medium. Silencing of Tas-acdS showed decreased ability of silenced transformants to promote root elongation of canola plants [33]. These mechanisms could be responsible for the plant growth-promoting activity of Trichoderma [31, 33]. The application of Trichoderma spp. results in significant vegetative growth on a wide range of crop plants [31, 34]. Interaction between Trichoderma spp. and the plant triggers enhanced immunity against plant diseases, thus improving plant health [35]. The ability to promote plant growth may be an important characteristic; however, this is not found in every Trichoderma species [13, 36]. Plant growth enhancement is evidenced by the increase in productivity, nutrient uptake, biomass, resistance to stress, and improvement of plant health [37]. Trichoderma isolates from the rhizosphere of the mangrove Avicennia marina solubilize P from the insoluble Ca3(PO4)2 and correlate with an increase of the extracellular phytase activity—an acidic phosphatase and extracellular activity of phytase were induced only in the presence of Ca3(PO4)2 [38]. In addition, the application of Trichoderma spp. in consortium was reported to enhance the physical strength and durability of the plant’s cell wall toward cell wall-degrading plant pathogenic fungi [39, 40, 41, 42]. It is likely that improvement in root growth was the effect of one or more mechanisms, and this may include an increase in soil nutrient solubilization, increase in the rate of carbohydrate photosynthetic activities and carbohydrate metabolism, plant growth regulatory effect, and increased rooting depth, thus increasing resistance to drought conditions [43]. Trichoderma spp. are more effective in colonizing and enhancing plant growth, if there are enriched inorganic soil substrates such as bioorganic fertilizers [44].


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