2.1 Mutual sensing of plant root and Trichoderma

Trichoderma root colonization is a prerequisite of the diverse interaction between plants and Trichoderma (Kredics et al., 2018). Several species of Trichoderma are known to colonize the root surface, inducing drastic changes in plant metabolism (Contreras et al., 2016). Chemical signals that facilitate the recognition process are released both by the plant and Trichoderma. For instance, tomato plants under pathogen attack secrete reactive oxygen species ROS and oxylipins, which have the ability to act as specific chemo-attractants to Trichoderma (Lombardi et al., 2018) (Figure 1A). Wheat plants were also reported to produce a variety of phenolics, including carbohydrates, lipids, terpenoids, and amino acids, in T. atroviride presence, which promotes the Trichoderma growth toward the plant (Lucini et al., 2019). Likewise, differences were observed in the types of carbohydrates released by the host plants under pre and post-colonization of roots by the Trichoderma. An increase in the release of carbohydrates was observed in plants before colonization, indicating that these chemicals may act as chemo-attractants, guiding the fungi toward the roots (Macías-Rodríguez et al. 2018).

Trichoderma also produces cysteine-rich hydrophobins that facilitate recognition and root colonization (Tyśkiewicz et al., 2022). Hydrophobins, along with CAZymes, play key roles in Trichoderma-roots interaction (Samolski et al., 2012). Hydrophobin gene qid74 from T. harzianum mediates the fungal root colonization in tomato plants (Samolski et al., 2012). On the contrary, when the TasHyd1 hydrophobin gene was deleted from T. asperellum, it caused an altering hyphae wettability and drastic disablement in root adherence (Viterbo and Chet, 2010). The interconnection between Trichoderma-intracellular signaling pathways and host-induced signals might be the G-protein located in the cell membrane of the host plant that results in an increase in the mycoparasitism-related processes and is crucial in recognition of Trichoderma by the plant (Omann and Zeilinger 2010; Zhong et al., 2019). Besides, Trichoderma secondary metabolite clusters, which are essential for communication with a plant for efficient root colonization, were also discovered. These plant recognition clusters mediate early chemical communication between plants and fungus and are required for colonization (Schalamun et al., 2023).

Previously it was believed that Trichoderma colonizes mainly the elongation zone and root hair, but current findings reveal their ability to colonize root cap border cells (RBCs) as well (Jaroszuk-Ściseł et al., 2019). The RBCs play a vital role during the interaction between the host plants and microflora in the rhizosphere (Hawes et al., 2016). These cells are delivered into the rhizosphere from the external boundary of the cap cells during the process of root elongation. It is believed that the cells and the affiliated root efflux are composed of a rich source of nutrients and metabolites for rhizosphere microflora (Jaroszuk-Ściseł et al., 2009). Furthermore, RBCs determine the structure and composition of the rhizosphere community, playing a role as attractants for microbes and assisting the interaction with the plants, thereby facilitating root colonization (Jaroszuk-Ściseł et al., 2009; Jaroszuk and Kurek, 2008). Penetration of roots is assisted by cellulose-binding expansins released by the microbes that disrupt the integrity of plant cell walls through channel formation, which facilitates the entry (Sood et al., 2020; Kumar and Khurana, 2021; Ramírez-Valdespino et al., 2019). Proteins, like swollenins and cerato-platanins, having enhanced affinity for cellulose, are also released by Trichoderma, which are vital for the efficient colonization of plant roots (Brotman et al., 2010; Sánchez-Cruz et al., 2021). Efficient root colonization with vigorous plant growth-enhancing impact was observed in pepper (Capsicum annuum L.) roots when T. atroviride showed enhanced expression of the Taswo1 swollenin gene (Sánchez-Cruz et al., 2021). Moreover, there is a strong correlation between Trichoderma root colonization and the release of proteolytic, cellulolytic, xylanolytic, and pectinolytic plant cell wall degrading enzymes (PCWDEs), facilitating the root colonization of epidermis and cortex areas (Sood et al., 2020; Contreras et al., 2016; Chen et al., 2020). During the process of colonization, Trichoderma may alter its transcriptional profile either to save the energy needed for the enhanced transcription of proteins required for root colonization or to avoid stimulation of plant defenses. This was observed during the interaction between T. viren and maize roots, where T. virens repressed the transcription of genes across a broad spectrum of activity upon recognition of plant roots. During root colonization, T. virens increases the expression of genes necessary to assist the entry of T. virens into the maize root and established there (Malinich et al., 2019).

2.2 Plant response to Trichoderma colonization

The pattern-recognition receptors (PRPs) are activated by damage or microbe-associated molecular pattern (DAMP or MAMP) before the colonization of plant roots by Trichoderma sp. (Jacoby et al., 2017; Sood et al., 2020; Mendoza et al., 2018; Ramírez-Valdespino et al., 2019; Alfiky and Weisskopf, 2021). The structural elements of the Trichoderma cell membrane and cell wall (sterols, chitin, and β-glucans) behave like MAMPs (Alfiky and Weisskopf, 2021). The host cell wall oligomers released as a result of the hydrolytic action of Trichoderma on plant surface or the derivatives due to biocontrol activity of other microbes (antagonism) might act as DAMPs, which on recognition by PRRs, trigger MAMP-stimulated immunity (MTI) and hence activating plant resistance (Woo et al., 2023). A number of biochemical and physical responses are stimulated, limiting the fungal invasion to only a few cortical cell layers of host roots. These physical or biochemical responses include strengthening and modification of the host cell wall, production of antimicrobial secondary metabolites (SMs), and reactive oxygen species. Deposition of callose, oxidative burst, ROS, and Ca²⁺ signaling are triggered quickly after the attack; as at that stage, the plant could not comprehend it as a friendly assault. Trichoderma arrival is also responded with SA level enhancement (a vital plant hormone controlling root colonization) to restrict Trichoderma in the apoplastic area of the cortex and epidermis (Carrero-Carrón et al., 2018; Alonso-Ramírez et a., 2014) (Figure 1B).

2.3 Management of plant immunity against root colonization

In order to maintain a long-term mutualistic alliance, Trichoderma has developed several mechanisms to suppress plant immunity. During the host root colonization, Trichoderma strains exploit their ability to compete in the rhizosphere, as they can effectively tolerate increased levels of ROS produced as an initial defense response by the host plant (Morán et al., 2010; Montero et al., 2011; Liu et al., 2016). Trichoderma gets host tolerance through the suppression of plant defense responses by the activity of different effectors (Alfiky and Weisskopf, 2021). Significant insight into global proteome and transcriptome changes mediated by Trichoderma has revealed sophisticated interactive mechanisms that help root colonization of host plants by Trichoderma (Martínez-Medina et al., 2019). Components of the Trichoderma secretome were reported to induce susceptibility in host plants by suppressing initial plant resistance, which helps the Trichoderma to penetrate the root surface (Lamdan et al., 2015). In maize plants, 36% less proteins in secretome was observed, including important families of peroxidases and glycosyl hydrolases that participate in plant defense against the invasion of microbes during the root colonization process by T. virens. In response, T. virens releases a plethora of SMs and proteins, facilitating root colonization synergistically in a synchronized way. This includes the release of cell wall degradation enzymes to ease entry into the host roots, antioxidant production to neutralize defense-stimulated oxidative burst (comprising of hydrogen peroxide, hydroxyl radical and superoxide, and several SMs as well as effector-like proteins) that intervene with plant hormones homeostasis that plays vital roles in plant defense (Lamdan et al., 2015). Similarly, drastic changes have been reported in the transcriptome of Arabidopsis thaliana affiliated with transient suppression of the plant immune reactions and repression of defense genes in the roots during root colonization by T. asperelloides (Brotman et al., 2013). Furthermore, high resistance has been observed in Trichoderma sp. against phytoalexins, phenols, aglycones, terpenoids, and flavonoids released by plants during infection caused by foreign micro-organisms. It facilitates the swift colonization of this fungi and its alteration of the root system of host plants (Błaszczyk et al., 2014; Tyśkiewicz et al., 2022). The compounds like maleic acid, citric acid, and oxalic acid released by Trichoderma may also assist root colonization (Zhang et al., 2014).

3.1 Trichoderma modulates phytohormones signaling pathways for plant growth

Phytoregulators and phytohormones produced by microbes are among the direct mechanisms that kick in the quick and durable soil colonization with microbes promoting the growth and development of host plant (Tamayo and Osorio et al., 2017; Zhou et al., 2018). The mechanism of plant growth stimulation by Trichoderma invasion is through the release of compounds having a direct impact on several plant hormone-mediated signaling pathways (Garnica-Vergara et al., 2016) (Figure 2A). A number of Trichoderma spp. have been characterized with the potential to release phytohormones (auxin, gibberellin, and ethylene) and phytoregulators that are vital for plant growth by controlling the biosynthesis pathway of phytohormones in host plants (Jaroszuk-Ściseł et al., 2019; Alfiky and Weisskopf, 2021; Ozimek et al., 2018). Indole-3-Acetic Acid (IAA), an auxin phytohormone, is vital for the majority of the procedures required for the appropriate development and growth of plants (Fu et al., 2015; Nieto-Jacobo et al., 2017). At reduced concentrations, IAA promotes root length, whereas high IAA concentration is vital for the proper production of adventitious and lateral roots (Jaroszuk-Ściseł et al., 2019). Inoculation of Trichoderma spp. capable of releasing IAA (T. virens and T. atroviride) increased the total biomass and number of lateral roots of A. thaliana seedlings. In a study investigating the roles of the phytohormone IAA released by Trichoderma on Arabidopsis growth and development, Contreras et al. (2009) concluded that Arabidopsis plants mutated in genes regulating auxins transport or important in signaling pathways (AXR1, EIR1, BIG, and AUX1) were non-responsive to the favorable impacts of T. virens in contexts of fungi- or IAA-triggered root branching and shoot growth. The understanding of IAA and related auxin-like compounds by changes induced in the root tips in auxin-sensitive marker DR5:GUS has been related to increases in lateral root production and cell proliferation. Moreover, the exogenic employment of IAA itself or/and its precursor (indole-3-acetaldehyde) to Arabidopsis plants has resulted in enhancing a concentration-dependent accumulation of foliar biomass and promoting plant growth. A number of other crops, including tomato (Bader et al., 2020), sorghum (Saber et al., 2017), bean (Hoyos et al., 2009), wheat (Illescas et al., 2021), and pepper (Sánchez-Montesinos et al., 2020) revealed growth improvement in plants as a result of IAA action procured from the Trichoderma species. Environmental factors, including nutrient status and pH, are believed to be responsible for regulating the IAA production in Trichoderma strains (Nieto-Jacobo et al., 2017).

Another phytohormone, ethylene (ET), is important in controlling several different physiological activities in plants, partially through complicated and sophisticated interactions with different phytohormones (Dubois et al., 2018). It has been proclaimed that T. atroviride enhances growth in plants via ET emission in a reaction that encompasses a unique molecular mechanism conglomerating a network of signals governed by ETHYLENE INSENSITIVE 2 (EIN2), a modulator of ET response. Release of fungal ET is involved in this mechanism, which stimulates the production of root hairs and impacts the formation of lateral roots through modulation of the ET receptors ETR1 and EIN2 via MITOGEN-ACTIVATED PROTEIN KINASE 6 (MPK6) regulation. It is interesting to note that T. atroviride and its IAA metabolite have been found to promote MPK6 efficiency, which in turn regulates both ET and auxin signaling pathways through an information exchange mechanism (Contreras et al., 2015). Although phytohormones play a crucial role in regulating plant growth, their excess can harm plants and Trichoderma assists the plants in maintaining the phytohormones' levels. For example, an increased amount of ET can restrict root elongation, eventually resulting in the death of plants (Glick, 2014; Nascimento et al., 2014). Trichoderma spp. have the capacity to release the ACC-deaminase enzyme (ACCD), an enzyme that cutdown the ethylene precursor (ACC) into ammonia and α-ketobutyrate, which assists in adjusting the level of plant ET; hence promoting plant development and growth (Todorovic and Glick, 2008). Several species of Trichoderma are known to have the potential to release ACCD, which enhances plant growth (Jaroszuk-Ściseł et al., 2019; Saravanakumar et al., 2018a; Zhang et al., 2020). Rauf et al. (2021) have reported increased growth in wheat due to the beneficial influence of ACCD released by T. asperellum. Furthermore, ACCD produced by T. harzianum beneficially impacted maize seedling growth and germination in a greenhouse environment (Zhang et al., 2020). The ACCD enzyme encoding gene (Tas-acdS) was characterized in Trichoderma genomes. Gene silencing in T. asperellum resulted in a reduced capacity to promote root growth in canola crop (Viterbo et al., 2010). By changing the plant hormonal homeostasis, Trichoderma modifies the physiology and enhances the fitness of the host plant (Martínez et al., 2014).

Gibberellins (GAs) are major phytohormones whose deficiency has a negative impact on proper seed germination, shoot and root growth in plants, expansion of leaf, and development of flowers (Ozimek et al., 2018). Several research findings reported the potential of several species of Trichoderma to produce GAs (Jaroszuk-Ściseł et al., 2019; You et al., 2016; Kamaloy et al., 2018). It has been reported that inoculation of T. koningiopsis isolates in tomato resulted in significant growth improvement due to the release and activity of GA (You et al., 2016). Furthermore, T. asperellum releasing GA enhanced the amount of these hormones in cucumber seedling leaves (Zhao et al., 2015). The deposition of GA synthesized by T. harzianum along with IAA was reported to improve plant growth (Kamalov et al., 2018). Moreover, the release of GA by the strains of Trichoderma was favorably linked with the production of IAA phytohormone and ACCD in wheat seedlings (Jaroszuk-Ściseł et al., 2019). Few Trichoderma spp. are known to produce a mixture of growth hormones (gibberellin, ABA, IAA) that stimulate the growth of seedlings and roots (Zhao et al., 2015; Jaroszuk-Ściseł et al., 2019). Other secretions from different Trichoderma spp., like histone deacetylase (HAD), were also reported to improve plant growth (Estrada et al., 2019).

3.2 Improved uptake and accumulation of nutrients in plants

Trichoderma-plant interactions revealed that one of the aspects of triggering plant growth is the result of improved uptake of biogenic elements. Association of Trichoderma in rhizospheres are reported with an effective absorption of nutrients, like metallic Zn, MnO₂, and rock phosphate, especially Ca₃(PO₄)₂, after their early solubilization (Li et al., 2015; Singh et al., 2018a, b). The T. harzianum inoculated tomato plants have been reported to enhance Mg²⁺, Ca²⁺, P, and K⁺ concentrations. The enhanced concentrations of these nutrients are beneficial for various shoot parameters, including diameter, height, dry and fresh weights (Azarmi et al., 2011). Li et al. (2018) reported that pre-inoculated tomato plants with T. asperellum resulted in improved nutrient (K, P, Zn, K, and Mg) absorption. In another study, K⁺/Na⁺ ratio was improved in cowpea by applying T. longibrachiatum (Liu et al., 2023). Moreover, in tobacco plants, an increase in the production of NO, levels of total nitrogen, and piling up of cytosolic Ca²⁺ have been found in response to the addition of T. asperellum. Trichoderma improves the ability of nutrient absorption and its transport by modulating their translocation genes in the host plant. T. asperellum activates various genes in tobacco plants that translate nitrate transporters (NRTs), like NRT 2.1 and NRT 2.2. All these alterations were reported to be linked with Trichoderma-mediated growth enhancements, thus revealing that T. asperellum improves the utilization efficiency of nitrogen in tobacco plants (Singh et al., 2018a). Furthermore, the growth of roots and shoots in reaction to Trichoderma inoculation led to improved uptake of Na, Cu, Zn, and other micronutrients (Li et al., 2015).

3.3 Mechanism of increasing bioavailability of nutrients to plants

Trichoderma has a vital role in increasing the growth in plants through improved solubility of nutrients present in the rhizosphere (Cu²⁺, Fe³⁺, ZnO, Mn⁴⁺, phosphate); hence augmenting their absorption by plants (mainly phosphorus, potassium, nitrogen, and other microelements) and boosting plant growth and yield (Contreras et al., 2016; Jaroszuk-Ściseł et al., 2019; Sood et al., 2020) (Figure 2B). Among the different nutrients required by plants, phosphorus (P) is present in the soil in a form having the least bioavailability to the host plants (Menezes et al., 2018). It was demonstrated that the experimental application of Trichoderma in soil improved the solubilization of inorganic phosphate as a result of exogenous phytase activity (Saravanakumar et al., 2013; Yin et al., 2021) and soil acidification due to citric, butyric, acetic, and fumaric acids synthesis (Scervino et al., 2010). Improved growth in different plants (Borges et al., 2015; Paul and Rakshit, 2021) has been correlated with the phosphate solubilization potential of Trichoderma. Some strains of Trichoderma strains have the ability to synthesize gluconic acid and coumaric acid and can increase the acidity of the environment to improve solubilization of micronutrients, for example, Mn⁴⁺, Fe³⁺, and Mg²⁺, making them available for utilization by the plant (Shoresh et al., 2010; Li et al., 2018) (Figure 2B).

Iron deficiency, because of its insoluble form for plant uptake, is also a major constraint for proper plant growth. T. asperelloides application increased iron availability by up to 30% in the rhizosphere via siderophore production. Siderophores are high-affinity iron-chelating compounds secreted by microbes to solubilize Fe³⁺. T. asperellum treated roots of cucumber not only enhanced siderophore contents and Fe²⁺ in soil but also improved the activity of Fe³⁺ chelate reductase that helps in Fe³⁺ oxidation (Harman et al., 2004). Moreover, Colla et al. (2015) have shown the production of two types of siderophores (catechol and hydroxamate) by the T. atroviride that cause Fe³⁺ reduction. These findings reveal that the application of Trichoderma in soil facilitates Fe uptake of host plants by reducing Fe³⁺ to Fe²⁺, which ultimately enhances its solubilization and absorption. Besides siderophores, Trichoderma also secretes other metabolites that help nutrient availability and improve their uptake from the soil by plants. A polyketide, tricholignan-A, secreted by T. harzianum, acts as a redox-active ortho-hydroquinone having the ability to reduce Fe³⁺ (Vinale et al., 2014). Similarly, the synthesis of tricholignan A assists the growth of plants under Fe deficiency conditions (Chen et al., 2019). Trichoderma was also found to enhance the expression of nutrient uptake marker genes, assisting the plants in coping with low nutrient uptake. For example, VOCs synthesized by T. harzianum and T. asperellum induce plants' iron absorption by stimulating the expression of iron transport and regulation genes IRT1 and FRO2. They also express MYB72, encoding for a factor important for the transcription of genes having the double role of regulating iron uptake and controlling defense responses (Martínez-Medina et al., 2017b).

4.1 The basic plant immunity triggered by Trichoderma and phytopathogens

Pattern-recognition receptors (PRRs; present on plant cell walls) identify the structural components of the pathogen, at the time of infection, as pathogen-associated molecular patterns (PAMPs). This identification activates the host immunity, which is called pathogen-triggered immunity (PTI). The PTI is amplified and transmitted to an array of mitogen-activated protein kinases that change the exogenous signal into endogenous reactions, reprogramming the transcription that results in fortification of the plant cell wall, enhances concentrations of endogenous calcium, synthesis of reactive oxygen species, production of anti-microbial SMs and PRPs, and increase of phytohormones related to defense (such as ET, JA, and SA). Pathogens deploy relevant effector proteins in the cell cytoplasm of the host to overcome and repress PTI. The nucleotide-binding site leusine-rich repeat protein (NLR) of the cytoplasmic receptors then identifies cytoplasmic effector placed by pathogens. This perception activates effector-triggered immunity (ETI), which is quicker and stronger than PTI. It is characterized by cell death and early oxidative burst due to hypersensitive reactions restricting the attack of pathogens (Figure 3).

The plant immune response induced by Trichoderma is much quicker and more intense compared to ETI and PTI. Trichoderma-triggered immunity (TTI) is initiated when the plant's PRRs recognize Trichoderma-originated DAMPs and MAMPs, which stimulate MAMP-triggered immunity (MTI), a type of immunity that is stronger than PTI or ETI, hence providing resistance to the host plant (Woo et al., 2023). Trichoderma also releases a cascade of effectors and metabolites like LysM protein Tal6 (Romero-Contreras et al., 2019), xylanase EIX (Ramírez-Valdespino et al., 2019), the peptaibol alamethicin, cerato-platanin EPL1, and the terpenes trichodiene (Malmierca et al., 2015) and harzianum A (Ramírez-Valdespino et al., 2019) in the apoplastic area of the cortex and epidermis. Those effectors are identified by host plant NLR receptors, which ultimately triggers Trichoderma effector-triggered immunity (TETI) (Carrero-Carrón et al., 2018; Alonso-Ramírez et al., 2014). Nonetheless, it is not yet known how the NLR receptors of plants correlate with the Trichoderma-generated effectors. NLR receptors in tomato plants are over-expressed in the leaves proteomes where roots of the host plants are invaded with Rhizoctonia solani and T. atroviride (Marra et al., 2006), and NLR receptors were also expressed by harzianic acid produced by T. harzianum (Manganiello et al., 2018). NLR receptors are overexpressed in the maize leaf proteome when host roots are inoculated with T. afroharzianum. Trichoderma effectors are not thought to act as ligands for NLR, the subsequent processes and signal transduction triggered by Trichoderma interaction, as well as their effects on host plants, are subjects of active and in-depth research (Morán-Diez et al., 2021; Ramírez-Valdespino et al., 2019).

The host plant induces a “transcriptional memory” when the Trichoderma-triggered signals progressively disappear. In this case, the cells previously stimulated with certain stimuli exhibit an intensified expression of the genes when re-stimulated subsequently (Liu and Avramova, 2016). The ability of defense induction is heritable, prompting subsequent memory levels named ‘heritable priming’, which can be transferred to the offspring. The level of expression of defense response is much stronger in the next-generation plants compared to the seedlings of non-induced plants. The beneficent impacts of Trichoderma on host plants are regulated by molecular networks, which shape the initial as well as long-term systemic reactions, crafting the metabolic exchanges between defense response and plant (Morán-Diez et al., 2021). During the nematode-tomato-Trichoderma interrelationship, the host resistance to root-knot nematodes and growth enhancement is inherited by the tomato seedlings without jeopardizing the defense status in the offspring of tomato plant while responding to the invasion of nematode (Medeiros et al., 2017).

The resistance developed in response to localized attacks systematically extends to the organs that are not damaged. The vasculature serves as a main route for diffusible signals that help in communication between roots and shoots, thereby assisting immunity in distant plant parts (Van Bel and Gaupels, 2004). For example, the xylem path was reported to transport signals from roots to shoots for triggering systemic resistance (Constantino et al., 2013). The mobile signaling molecules α-ketol of octadecadienoic acid (KODA) and 12-oxo-phytodienoic acid (12-OPDA) are implicated in Trichoderma-triggered ISR against maize anthracnose disease (Wang et al., 2019).

4.2 Trichoderma-triggered Induced Systemic Resistance and Systemic Acquired Resistance

Recent evidence from several research findings reveals that Trichoderma-induced defenses (TETI and MTI) against different pathogens are regulated by ET, SA, and JA (Woo et al., 2023). The increased concentrations and accumulation of Trichoderma-induced elicitors are affiliated with the induction of the immune response in the host plant, which comprises induced systemic resistance (ISR) and systemic acquired resistance (SAR) (Tyśkiewicz et al., 2022; Kumar and Ashraf, 2017). ISR is a vital mechanism in which Trichoderma residing in the rhizosphere stimulates the defense response in host plants against hemibiotrophic and biotrophic pathogens (Tyśkiewicz et al., 2022; Kumar and Ashraf, 2017; Nawrocka and Małolepsza, 2013). It is characterized by the release of ET and JA, which may cause rapid aging, chlorosis, and ultimately death of invaded tissue (Wang et al., 2021; Ding and Ding, 2020; Yang et al., 2015; Kumar and Khurana, 2021; Monfil and Casas, 2014). It has been reported that roots of cucumber plants inhabited with T. asperellum had significantly higher amounts of ET and JA within 24 h (Shoresh et al., 2005), quite in agreement with the idea that Trichoderma triggers ISR response (Pieterse et al., 2014). The ISR signals, JA, and ET are also important for generating several defense molecules like peroxidases, polyphenol oxidase, β1-3glucanase, catalase, β1-4-glucanase, chitinases and N-acetylglucosaminidases (Peng et al., 2021; Vargas et al., 2009). Trichoderma may also directly enhance the production of these defense molecules (Zhan et al., 2023). The first MAMP signal (xylanase) detected from Trichoderma was also reported for ET-modulation activity, triggering defense reactions in tobacco and tomato (Rotblat et al., 2002).

An alteration in the gene expressions, controlled by JA and ET, has been reported in many plant species invaded with Trichoderma. For instance, lipoxygenases (LOX) oxidize the polyunsaturated fatty acids, and the oxidation product is then transformed into JA precursor, i.e., 12-oxo-phytodienoic acid (12-OPDA), which is then transformed to JA (Feussner and Wasternack, 2002; Andreou et al., 2009; Borrego and Kolomiets, 2016). The lox mutants are unable to synthesize JA, which weakens maize immunity (Christensen et al., 2013; Gao et al., 2008). It is reported that T. asperellum regulates the expression of LOX and ETHYLENE RESPONSE 1 (ETR1) in cucumber (Shoresh et al., 2005). Trichoderma also assists the plants by countering pathogen-suppressed host defense response through JA regulation. For example, T. harizanum uplifted the JA-regulated defenses involving the expression of MULTICYSTATIN and PROTEINASE INHIBITOR II (PI-II) and hence resisted the downregulation of the JA-induced defense response activated by the nematodes, thereby inversely affecting the fecundity and galling by M. incognita (Martínez-Medina et al. 2017a). Analogous research findings have been shared by Leonetti et al. (2017), reporting T. harzianum-induced ET and SA synthesis in M. incognita-infected tomato plants.

The synthesis of SA and pathogenesis-related proteins (PR) is associated with the SAR response and restricts the establishment of pathogens within the plant by stimulating programmed cell death (Kumar and Khurana, 2021; Monfil and Casas-Flores, 2014; Yang et al., 2015; Ding and Ding, 2020; Wang et al., 2021). SA is synthesized in plants using the isochorismate synthase (ICS) route, beginning with chorismate (Lefevere et al., 2020). ICS genes (ICS1, ICS2) affiliated with pathogenesis-associated proteins, like PR-1-7, are among the important genes involved in the SA pathway in many plant species interacting with Trichoderma when attacked by different pathogens (Ali et al. 2018). SA activates a number of PR genes, the proteins of which have antimicrobial properties (Boamah et al., 2023). The NONEXPRESSOR OF PR GENES1 (NPR1) protein is involved in the regulation of defense genes by SA, such as PR-1. (Uquillas et al., 2004). T. hamatum stimulates the expression of PR-1 and PR-7 in tomato plants infected with TMV (Abdelkhalek et al., 2022). Martínez-Medina et al. (2017a) demonstrated T. harzianum-regulated ISR immunity in tomato plants against Meloidogyne incognita, which is achieved through SA-induced defense mechanisms employing the expression of PR-P6 and PR-1a to restrict the infection of host plant roots by M. incognita. In tomato plant roots where the root-knot nematode completes its life cycle, Trichoderma helps to reprogram immune response through JA and SA-induced defense mechanisms, depending on the infective stage of nematode (Medeiros et al., 2017; Martínez-Medina et al., 2017a).

The defense enzyme PHENYLALANINE AMMONIA-LYASE (PAL) is necessary for the biosynthesis of phenylpropane unit, which is a component of lignin and thus contributes to cell wall lignifications and resistance to pathogen invasion (Chen et al., 2020). Upon biotic stress, the plants increase lignification and use it as an adaptive mechanism to limit pathogen entry (Sarma et al., 2015; Chen et al., 2020). Trichodermainduced plant immunity by enhancing PAL activities in plants is evident from several studies. A substantial increase in the level of PAL activities is correlated with improved disease resistance in rice and tomato (Singh et al., 2016; Wang et al., 2021). Through transcriptional analyses, Wang et al. (2023) found that T. asperellum improved C. canephora resistance to anthracnose by up-regulating the expression of phenylpropane biosynthesis pathway genes (including PAL). Moreover, Zhang et al. (2022b) reported that T. asperellum is involved in the regulation of the watermelon phenylpropane synthesis pathway against Fusarium oxysporum. The defense mechanism of T. longibrachiatum in cucumber plants against Botrytis cinerea was reported to be due to the phenylalanine pathway synthesis of SA because of the enhanced PAL expression both at the gene and protein level (Yuan et al., 2019).

4.3 Role of different Trichoderma elicitors as regulators of plant immunity