Elsevier

Biological Control

Volume 174, November 2022, 105037
Biological Control

Review
The riddles of Trichoderma induced plant immunity

https://doi.org/10.1016/j.biocontrol.2022.105037Get rights and content

Highlights

  • Review is primarily focused on the role of Trichoderma in plant immunity.

  • We have described the role of Trichoderma in SAR and ISR.

  • Dual role of Trichoderma involving both JA / ET as well as SA has been described.

Abstract

Since the initial finding of Trichoderma as a biocontrol agent, efforts have been largely focused on understanding the role of glycosyl hydrolases and antibiotics in mycoparasitism, plant pathogen suppression and other plant growth promotion attributes. However, comparatively less attention has been given for reviewing the role of Trichoderma-derived molecules in plant immunity. Microbial derived molecular signatures are well known for the induction of systemic resistance in plants. In general, the molecules from non-pathogenic microorganisms, activate the plant's immune response via induced systemic response (ISR) that is driven through jasmonic acid (JA) / ethylene (ET) pathways whereas the signature molecules of pathogens origin, induce systemic acquired resistance (SAR) which is driven by salicylic acid (SA). The role of Trichoderma, in triggering the plant immunity has been studied in isolation both at local and systemic level. In this context, various signature molecules from Trichoderma and their roles in activating the plant immune responses have been identified. The elicitors such as Epl1 from Trichoderma through synergistic action, involving both JA / ET as well as SA primed systemic resistance. Furthermore, histone modification system from endophytic strain of Trichoderma through its epigenetic modification of histone proteins have been explored for modulating the expression of genes. The recent experimental studies have unraveled new players of Trichoderma induced systemic resistance with their probable role in SAR as well ISR mediated response. Here, we have described the complexity of biological repertoire and multifaceted aspects of Trichoderma in mediating the plant immune response.

Introduction

Hypocrea/Trichoderma is a cosmopolitan fungus and widely used in agricultural fields as a natural enemy against plant fungal pathogens (Reino et al., 2008). Its ability to produce lytic enzymes and antibiotics has been explored to counter environmental stresses, enhance the plant growth and hence agricultural productivity (Chet and Chernin, 2002, Benitez et al., 2004, Hermosa et al., 2013, Mukherjee et al., 2013, Mukherjee, Sharma et al., 2022) and even for industrial enzymes (Mukherjee et al., 2013). Efforts have been made over a period of time to identify, characterize and review the molecular mechanisms of Trichoderma as biocontrol agents (Djonovic et al., 2006, Sharma et al., 2013, Sharma et al., 2016a & Sharma et al., 2016b, Sharma et al., 2017, Sharma et al., 2018a & 2018b). Beside biocontrol attributes, Trichoderma species assist in activating the plant systemic resistance (Van Loon et al., 1998, Yedidia et al., 2003, Djonovic et al., 2007, Contreras-cornejo et al., 2011, Salas-Marina et al., 2011, Velazquez-Robledo et al., 2011, Vos et al., 2015, Vlot et al., 2021). The plant immune response is manifested through conserved microbe associated molecular patterns (MAMP) or pathogen-associated molecular patterns (PAMPs) that are recognized by pattern recognition receptors (PRRs) including receptor kinases and the receptor-like proteins present on the host plant cell surface (Boller and Felix, 2009, Dodds and Rathjen, 2010). The stimulation of PRRs by MAMP- or PAMP activates the basal layer of immunity refer as pattern-triggered immunity (PTI) or microbe triggered immunity (MTI) to restrict the pathogen. Once pathogen enters the host cytoplasm, the pathogen enhances its growth by suppressing PTI through the secretion of effectors. In resistance responses, the effectors revamp the resistance response of the host plant result in the localized death of the infected cell. Such immune responses are refer as effector triggered immunity (ETI) (Jones and Dangl, 2006, Bartels and Boller, 2015).

The microorganism assisted systemic resistance are subcategorized into pathogen-induced systemic acquired resistance (SAR) and non-pathogenic rhizobacteria induced systemic resistance (ISR) (Contreras-cornejo et al., 2011, Alkooranee et al., 2017). The efforts have been made to investigate the role of plant hormones and molecular signaling events during Trichoderma mediated systemic resistance (Limpens and Bisseling, 2003, Harrison, 2005). For example, the root-colonization by T. harzianum TH12 induces ISR while application of its cell free filtrate (CF) induced SAR to Sclerotinia sclerotiorum (Alkooranee et al., 2017). The local and systemic elicitation of immune responses are manifested through SA/jasmonic acid (JA) and /ethylene (ET) (Glazebrook, 2005). For example, the induction of ISR signaling pathway of T. virens in Cucumis sativus and Zea mays (maize) contains JA and ET (Yedidia et al., 2003, Djonovic et al., 2007) while SA and JA have been depicted in cucumber plants in T. asperellum T34 induced resistance (Segarra et al., 2007). Another study, using pPr1a:uidA and pLox2:uidA markers showed that T. virens or T. atroviride mediated defense signaling pathway involves SA and/or JA depending on inoculum of spore suspension used (Contreras-cornejo et al., 2011). In cucumber, the treatment of T. longibrachiatum H9 in plant roots inhibited B. cinerea through the activation of JA, ET and SA (Yuan et al., 2019). In maize plants, the inoculation with T. gamsii (IMO5 and B21) resulted in systemic resistance against Fusarium verticillioides (Galletti et al., 2020). Further, the increase in systemic resistance was observed to be strain-specific. The strain IMO5, enhanced the expression of marker genes ZmLOX10, ZmAOS, and ZmHPL which are related to ISR and are responsible for the production of jasmonate and other volatile compounds in the leaves. On the other hand, B21 strain enhanced the expression of ZmPR1 and ZmPR5 genes linked to SAR (Galletti et al., 2020). Trichoderma guizhouense NJAU 4742 Tgui increased plant growth through the auxin biosynthesis in maize. Moreover, the extracellular proteins of NJAU 4742 elicited the ISR of maize plants against F. verticillioides through reactive oxygen species (ROS) production and deposition of callose tissues (Xu et al., 2020). Trichoderma T-78 - Meloidogyne incognita interaction in roots, activated PR1a and PR-P6, through SA production (Martínez-Medina et al., 2017b, Medeiros et al., 2017). During resistance response, elicitors induce ROS production as well as accumulation of phytoalexins, upregulation of pathogenesis-related (PR) proteins (Van Loon and Van Strien, 1999, Mittler et al., 2004). Additionally, the epigenetic changes through DNA methylation and posttranslational modifications (PTMs) of the histones proteins in the nucleosome complex also help in the activation or deactivation of the genes of plants, fungi and other organisms (Li et al., 2011, Seto and Yoshida, 2014, Schmoll et al., 2016, Willbanks et al., 2016, van der Woude et al., 2019).

Since the initial discovery of Trichoderma as a biocontrol agent, efforts to describe Trichoderma induced systemic resistance have resulted several new insights (Yedidia et al., 2003, Djonovic et al., 2007, Shoresh et al., 2010, Vos et al., 2015, Pieterse et al., 2014, Morán-Diez et al., 2021). However, the recent experimental studies have unraveled new players of Trichoderma induced systemic resistance with their probable role in SAR as well ISR mediated response. Here, we have described the role of Trichoderma derived systemic resistance in plants involving both systemic acquired resistance (SAR) as well as induced systemic resistance (ISR). We have also covered new candidates of Trichoderma origin responsible for boosting plant immunity.

Section snippets

Overview of SAR and ISR and role of plant hormones

The plant immune response involves PAMPs that trigger the initial broad host range immune responses known as pathogen triggered immunity (PTI) which is followed by second more specific response mediated through effector known as effector triggered immunity (ETI) to induce resistance against pathogens. The details of PTI and ETI has been reviewed by Jones and Dangl (2006). During ETI, the effector molecules mimic the potential pathogens instead of PAMPs in PTI triggered immunity. The downstream

Overview of Trichoderma induced plant immunity

For literature search databases such as Pubmed, Scopus and Web of Science were used. Literature to role of Trichodema in plant immunity till Feb 2022 was collected using a combination of keywords such as Trichoderma, Plant immunity, SAR. ISR, elicitors. The ISR-like responses induced by T. virens are exhibited through JA / ET and other diffusible signals (Djonović et al., 2007). In maize plants, T. gamsii treatment resulted in systemic resistance (Ferrigo et al., 2014, Galletti et al., 2020)

Biological repertoire of Trichoderma involved during elicitation of the plant immune response

The symbiotic association of Trichoderma (Guzmán-Guzmán et al., 2019) and its ecological role in rhizospheric interaction have been reviewed (Contreras-cornejo et al., 2016). Systemic studies on various plant beneficial attributes of Trichoderma (Harman et al., 2004, Harman, 2006, Sharma et al., 2022), distribution of cysteine-rich secreted proteins (Mukherjee et al., 2013), production of peptaibols (Daniel and Filho, 2007), effector-like molecules (Ramírez-Valdespino et al., 2019), secondary

Conclusion

The continuous efforts to unravel the molecular arsenal of Trichoderma led to exploration of its various aspects such as production of lytic enzymes (chitinases, glucanases and proteases), secondary metabolites, competition for space and nutrients acquisition which initially responsible for the pathogen suppression. With continuous investigations its other aspects such as plant growth promotion and systemic resistance were elucidated. In recent studies, Trichoderma triggered systemic resistance

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgment

Authors acknowledge Science for Equity, Empowerment and Development (SEED) Division SEED Division, Department of Science and Technology, GOI for providing financial benefits (SP/YO/125/ 2017) and (SEED-TIASN-023–2018).

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