Phytohormones and Biomolecules Produced by Trichoderma Strains as Eco-Friendly Alternative for Stimulation of Plant Growth

Abstract

The increase in agricultural food demand during the last years has caused the expansion of cultivated areas. As a result, more chemical fertilizers are used in agriculture to fulfill the demand of the increasing population worldwide. Pesticides and chemical fertilizers are not recommended because they lead to environmental pollution, the development of resistant pests, and cause serious health problems. Thus, the reduction in the use of synthetic products is highly recommended. In this regard, alternative strategies for sustainable agriculture should be implemented. One of these strategies is the use of biofertilizers, specifically biofertilizer fungi that are widely applied in agriculture. Trichoderma seems to be the best candidate for use in green technologies due to its wide biofertilization and biostimulatory potential. Most Trichoderma species increase nutrient availability and uptake in plants. They are considered as plant growth-promoting fungi (PGPF). This genus colonizes the root systems of plants and promotes their growth. It can increase nutrient availability and uptake in plants by fixing nitrogen and solubilizing phosphorus. Moreover, they help plants tolerate environmental stresses such as drought, salinity, and stimulate plant growth due to their capacity to produce phytohormones such as indole-3-acetic acid (IAA) and gibberellins (GAs). Phytohormones play an important role in agriculture; they enhance plant growth through several processes.

1. Introduction

Food security and intensive crop production have led to increased use of chemical fertilizers in agriculture [1, 2]. The use of chemical fertilizers has negative effects on the environment, soil microbiomes, terrestrial and aquatic ecosystems, as well as human and animal health [3]. Furthermore, the application of chemical pesticides in agriculture increases the resistance of microorganisms to pesticides and contaminates soil and groundwater [4, 5]. Thus, alternative measures should be taken instead of using synthetic chemicals. Plant growth-promoting microbes offer promising strategies to enhance plant growth [6, 7, 8]. Numerous researchers have studied the functions of plant growth-promoting fungi (PGPF). Many Trichoderma strains are capable of producing compounds as growth regulators that stimulate plant growth through several processes [9]. The effectiveness of Trichoderma species in agriculture is related to their metabolic activity and their type of interaction with plants and other microorganisms. They colonize the root systems of plants and promote their growth. Trichoderma species can increase nutrient availability and uptake in plants by fixing nitrogen, mineralizing organic matter, and producing several biomolecules and phytohormones [10, 11]. Phytohormones play an important role in agriculture [12]. They are synthesized by many rhizosphere microorganisms, including Trichoderma spp. They can enhance plant growth through several processes, such as modifying the physiological functions of plants to accelerate their growth by intensive cell division in callus tissue, promoting phloem development, enhancing lateral root development, stimulating plant growth, and preventing leaf aging by slowing down the breakdown of chlorophyll pigments in plants, as well as improving metabolism [13, 14, 15]. Other beneficial effects of Trichoderma are related to the stimulation of root development due to their ability to increase the solubilization of insoluble forms of phosphorus (P) in the soil, as well as acting as P-mobilizing microorganisms for plants [16]. Thus, the utilization of effective plant growth-promoting fungi to enhance crop production represents an eco-friendly alternative for sustainable crop production [17]. This review highlights the benefits of Trichoderma species for sustainable crop production providing a sustainable alternative to agrochemical products. Besides, this review provides environment friendly approach by exploring effective Trichoderma species with beneficial effects such as nutrient uptake, nitrogen fixation, siderophore and phytohormone production as well as phosphorus solubilizing. Therefore, these effective strains could be applied in crops production to increase their productivity.

2. Trichoderma as a biofertilizer

2.1 Characteristics of the Trichoderma spp.

Trichoderma genus is a group of filamentous fungi classified as anamorphic Hypocreales. Many strains are widespread around the world, typically colonizing rotting wood and other forms of organic plant matter [18]. They inhabit various ecological niches, including farmland, salt marshes, forests, and deserts in all climatic zones, encompassing temperate and tropical regions, Antarctica, and the tundra [3, 19]. Trichoderma genus is recognized as a cosmopolitan group of saprotrophic fungi, often existing as endophytes in woody plants [19]. Furthermore, Trichoderma strains produce diffusible pigments that can range from greenish-yellow to reddish tinges, and colorless strains may also be available. Conidia can exhibit different hues, ranging from dull to various shades of green or brown [20]. Microscopic identification criteria for Trichoderma are as follows: septate and translucent hyphae; conidiophores are short, translucent, and branched, often giving a pyramidal appearance, not verticillate; phialides are attached at right angles to the conidiophores. Spores produced are translucent and ovoid in shape, borne in small terminal clusters at the tips of phialides. Some species can produce globose chlamydospores, which are intercalary or terminal. These chlamydospores are usually unicellular [21] (Figure 1).

Figure 1.

Macroscopic and microscopic appearance of colonies representing phenotypic groups of Trichoderma isolated from rhizosphere of olive trees: (A): T. koninji, (B): T. aureoviride [22].

2.2 Plant growth-promoting properties of Trichoderma

Trichoderma species are often associated with the rhizosphere of host plants. They are typically known as symbiotic and saprotrophic fungi that invade the roots and stimulate plant growth through several mechanisms [23]. They exhibit beneficial effects on plants, such as promoting their growth, elongating lateral root growth, enhancing seed germination, as well as increasing photosynthesis efficiency, flowering, and yield quality [24]. The synthesis of phytohormones and phytoregulators is the most important stimulating factor at almost all stages of plant growth and development [12, 25].

2.3 Competition and plant root colonization

Rapid growth of Trichoderma strains makes them competitive candidates for space and nutrients because the growth of antagonistic microorganisms will be restricted, especially when nutrients become a limiting factor [26]. Importantly, Trichoderma can also colonize space by producing chelators such as siderophores, which increase the absorption and concentration of certain nutrients (copper, iron, phosphorus, manganese, and sodium). As a result, iron becomes less available for pathogens. Therefore, competition in the soil between microorganisms is considered an indirect mechanism for stimulating plant growth [27]. Trichoderma plays a role in stimulating plant growth by reducing oxidative stress. Additionally, studies conducted by [28] showed the role of siderophores produced by Trichoderma asperellum T34 in controlling Fusarium oxysporum, resulting in a reduction in tomato infestation and stimulation of root plant growth. Moreover, Trichoderma species can colonize the root surfaces of olive trees, leading to changes in metabolism. It has been previously reported that these fungi can invade olive roots [22]. Furthermore, the interaction between plants and Trichoderma offers a valuable source of nutrients released into root exudates for the benefit of Trichoderma [29, 30].

2.4 Phytohormones as inducers of systemic resistance

The recognition between the plant and Trichoderma leads to the synthesis of phytoalexins (fungitoxic molecules) [31, 32]. Phytohormones contribute to the regulation of complex and interrelated plant immune signaling pathways, providing a rapid defense response and adaptation to various environmental conditions [33]. Trichoderma species are capable of eliciting plant defense mechanisms through the synthesis of the enzyme ACC deaminase (1-aminocyclopropane-1-carboxylate) and indole-3-acetic acid. The biosynthesis of ethylene increases in response to ACC deaminase. In fact, plant development and defense systems are interconnected through a network of hormonal signaling pathways [34, 35].

2.5 The synthesis of phytohormones and metabolites influencing the phytohormonal balance

Phytohormones produced by fungi play crucial roles in agriculture, with a growing interest in their industrial production [36]. Many Trichoderma species are able to produce phytoregulators and phytohormones such as auxin and gibberellin, including the enzyme 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase, which regulates the ethylene biosynthetic pathway [33, 37]. The enhancement of rhizosphere and root colonization by Trichoderma occurs through the synthesis of indole-3-acetic acid [38]. Moreover, Trichoderma species isolated from the rhizosphere soil of olive trees were able to produce a complex of growth hormones, IAA and gibberellin [39].

2.5.1 Production of auxin phytohormone indole-3-acetic acid

Several strains of Trichoderma are capable of producing auxin phytohormones, including IAA, which can enhance plant growth through various processes [40]. IAA regulates plant development; this phytohormone is responsible for the division, extension, and differentiation of plant cells and tissues. IAA stimulates seed and tuber germination, increases the rate of xylem and root formation, and controls processes of vegetative growth, tropism, fluorescence, and fructification of plants. It affects photosynthesis, pigment formation, resistance to stress factors, and the biosynthesis of various metabolites [41, 42]. The production of IAA usually depends on the presence of its precursor, L-tryptophan. This production is influenced by abiotic factors such as temperature and pH [12, 43]. IAA at low concentrations stimulates root elongation, while high concentrations are responsible for the proper formation of lateral and adventitious roots [12]. Moreover, several in planta studies have reported that Trichoderma species affect and increase plant growth in various crops such as olive [39], tomato [44], sorghum [45], bean [46], and wheat [47], due to the action of IAA produced by Trichoderma.

2.5.2 The production of gibberellin phytohormones

Gibberellins (GAs) are phytohormones that can enhance plant growth through seed germination, flowering, stem extension, aging, and stimulation of hydrolytic enzyme formation in germinating cereal grains [48, 49]. These properties are responsible for the extensive application of GAs in agriculture to improve the quality of agricultural and horticultural crops [50]. Several scientific reports have revealed the ability of numerous Trichoderma species to synthesize GAs [12, 51, 52]. After the inoculation of T. koningiopsis isolates, tomato growth was significantly improved, suggesting that GAs affect tomato growth [51]. Moreover, the production of GA by Trichoderma strains isolated from the rhizosphere of olive trees was confirmed previously [39]. Furthermore, the accumulation of GA3 produced by T. harzianum in combination with IAA was found to increase the plant growth-promoting effect [52].

2.5.3 The production of the ACC-deaminase enzyme

Trichoderma species are able to produce the enzyme 1-aminocyclopropane-1-carboxylate-deaminase (ACC deaminase), which is involved in promoting plant growth. This enzyme reduces the levels of ethylene (ET) in plants by cleaving the ET precursor ACC into ketobutyrate and ammonia [53]. The ACC deaminase enzyme affects the levels of ethylene (ET) when Trichoderma interacts with the plant roots [54]. This phytohormone (ET) affects the regulation of various physiological processes, in part through complex interactions with other phytohormones [55]. However, high levels of ET can inhibit root elongation and cause plant death [56, 57]. Several species of Trichoderma fungi have a considerable ability to produce ACC deaminase [12, 58, 59]. T. asperellum T203 produces ACC deaminase that regulates the endogenous ACC level and stimulates root elongation [34], enhancing plant tolerance to abiotic stress. Besides, ACC deaminase is able to modify the plant physiological functions and growth, enhancing plant tolerance to salinity stress [60].

2.6 Enhancement bioavailability and nutrient solubilization

Trichoderma plays an important role in enhancing plant growth by providing nutrient availability (phosphates, Fe3+, Cu2+, Mn4+, ZnO) and offering the necessary elements to the plant, mainly nitrogen, potassium, phosphorus, and microelements [61, 62, 63]. Phosphorus is an important element present in the soil with limited bioavailability to plants. It can be found in two forms: organic phosphorus and inorganic phosphorus, which is usually combined with calcium, aluminum, or manganese [64, 65]. Phosphorus solubilization in the soil is influenced by several factors such as microbial activity, pH, soil type, and organic matter availability [66]. The application of Trichoderma strains in the soil has been experimentally demonstrated to increase inorganic phosphate solubilization due to extracellular phytase activity [67] and the acidification of the soil environment through the production of acetic, butyric, citric, and fumaric acids [68]. Trichoderma spp. competes for the limited available phosphorus through various processes, such as solubilization, precipitation, absorption, and desorption. Inorganic phosphate and organic phosphorus can be mineralized through enzymatic action [66]. In previous studies, [69] reported that Trichoderma atroviride LBM 112 and T. stilbohypoxyli LBM 120 revealed positive results for phosphate solubilization with the formation of a halo-zone on the solid medium containing an insoluble inorganic phosphorus source. In addition, Trichoderma harzianum T11 (OL587563) isolated from the rhizosphere soil of olive trees has several plant growth-promoting traits, such as phosphate-solubilizing ability and the production of siderophores [39]. Furthermore, the T. asperellum CHF 78 strain showed increased nutrient uptake (P, K, Mg, and Zn) by tomato plants after pre-inoculation [70].

2.7 Nitrification and nitrogen fixation

Trichoderma species are among the beneficial rhizosphere microorganisms that are sustainably used for plant growth [71, 72]. The nitrogen fixation processes have significant ecological importance in various ecosystems, including those of agricultural interest. Trichoderma sp. is one of the important fungi that can colonize and solubilize various nutrients such as N, Zn, Fe, Cu, and Mn in soils [73]. Nitrogen fixation by microorganisms plays a key role in promoting plant growth. It has been suggested that the promotion effect on plant growth might be mediated by providing nitrogen through biological nitrogen fixation [74, 75]. The production of ammonia and nitrogen-fixing ability by Trichoderma strains is reported in previous findings. It has reported that ammonia is useful for plants. Ammonia production by the Trichoderma isolates may influence plant growth indirectly. ACC synthesized in plant tissues by ACC synthase is released from plant roots and taken up by neighboring microorganisms. Then, Trichoderma may hydrolyze 1-aminocyclopropane-1-carboxylic acid to ammonia [76]. Trichoderma harzianum T22 revealed nitrogen utilization efficiency in maize. Besides, it has been reported that Trichoderma species isolated from rhizosphere soil of olive were able to produce ammonia [39]. Furthermore, a previous study showed that among 20 Trichoderma spp. isolated from chili rhizosphere, 13 isolates were able to produce ammonia [77]. Due to the wide range of effects on plant growth and yields, Trichoderma applications have been widely extended over chemical fertilizers in the agriculture sector [78] (Figure 2 and Table 1).

Figure 2.

Schematic description of the main mechanisms used by plant growth-promoting fungi to enhance crop production [39].

Compound	Strain	Crops	Application mode	Beneficial outcome	References
Biofertilizer	T. asperellum T42	Tomato	Seed treatment	Improves nutrient uptake (enhance nitrogen utilization efficiency, increase Phosphorus uptake	[79]
	T. harzianum	Most crops	Compost	Improves the rate of Residue decomposition resulting in greater availability of soil nutrients	[80]
	T. asperellum strain GDFS1009	Maize	On soil as granules	Increased yields	[81]
	Trichoderma azevedoi	Lettuce	Simple exposure	Increases carotenoids and chlorophyll with reduction in the white mold attack to about 78.83%	[82]
	Trichoderma afroharzianum	Tomato	Seed inoculation or treatment	Helps in the secretion of Phytohormones like homeostasis, antioxidant activity, phenylpropanoid biosynthesis and glutathione metabolism	[83]
	Trichoderma harzianum, Trichoderma asperellum, Trichoderma hamatum, Trichoderma atroviride	Chinese cabbage	Irrigation	Increases soil enzyme activity, yield by 37%,; and increases the concentration of inorganic nitrogen and; phosphorus content of the soil	[84]
	Trichoderma brevicompactum, Trichoderma gamsii, T. harzianum	Tomato	Seedling drenching	Improved growth and yield due to the production of indole-3 acetic acid	[44]
	T. harzianum, T. asperellum	Tomato	Seed treatment	Improves phosphorus uptake	[85]
	T. brevicompactm, T. gamsii, T. harzianum	Tomato	Seed drenching	Improves phosphorus solubilization	[44]

Table 1.

Trichoderma sp. as bio-fertilizers for sustainable crop production.

3. Conclusion

This review elucidates the ability of Trichoderma to be used as an efficient biofertilizer in agriculture. It has shown various mechanisms of providing the crop with biomolecules that can enhance plant growth by increasing nutrient availability, producing plant growth hormones such as indole-3-acetic acid and gibberellin, as well as enzymes including phosphatases and 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase. Hence, it has various mechanisms to enhance plant growth, giving it an advantage compared to other fungi. Thus, the increased use of Trichoderma spp. as commercial biofertilizer offers promising prospects for sustainable and environmentally friendly agriculture. These eco-friendly alternatives can substitute the excessive use of chemical products that can cause long-term problems. These strains have sufficient potential to warrant assessing their practical applications in the real field. However, more studies need to be conducted to elucidate the development of sustainable biotechnological applications of Trichoderma species in the soil-plant system. Future research should be conducted on developing new strains that are more effective at promoting plant growth and elucidating the molecular mechanisms through which these effective strains interact with plants. In addition, the use of genetic engineering could provide cultivars more resistant to abiotic and biotic stresses, such as drought and salinity. This could contribute to establishing more sustainable crop varieties that can support changing environmental conditions. Besides, synergetic interactions and the influence of abiotic factors such as extreme pH, soil salinity, drought, and temperature fluctuations should be studied to determine the optimal growth values.

Conflict of interest

The authors declare no competing interests.