Trichoderma and the Plant Heritable Priming Responses

Abstract

There is no doubt that Trichoderma is an inhabitant of the rhizosphere that plays an important role in how plants interact with the environment. Beyond the production of cell wall degrading enzymes and metabolites, Trichoderma spp. can protect plants by inducing faster and stronger immune responses, a mechanism known as priming, which involves enhanced accumulation of dormant cellular proteins that function in intracellular signal amplification. One example of these proteins is the mitogen-activated protein kinases (MAPK) that are triggered by the rise of cytosolic calcium levels and cellular redox changes following a stressful challenge. Transcription factors such as WRKYs, MYBs, and MYCs, play important roles in priming as they act as regulatory nodes in the transcriptional network of systemic defence after stress recognition. In terms of long-lasting priming, Trichoderma spp. may be involved in plants epigenetic regulation through histone modifications and replacements, DNA (hypo)methylation, and RNA-directed DNA methylation (RdDM). Inheritance of these epigenetic marks for enhanced resistance and growth promotion, without compromising the level of resistance of the plant's offspring to abiotic or biotic stresses, seems to be an interesting path to be fully explored.

Keywords: biocontrol; epigenetics; immune response; inheritance; methylation; systemic defence; transcription factor.

Figure 1

Schematic outline of plant’s early response to the interaction with Trichoderma. Plant´s cell surface pattern recognition receptors (PRR) are the first line of defence against Trichoderma effectors during the early response (this first stage of the colonization being considered by the plant as an attack). As a result of this first encounter between the plant and Trichoderma, a series of events will be triggered in the plant including the rapid release of reactive oxygen species (ROS), the deposition of callose, calcium influx, and accumulation of salicylic acid (SA) at the primary inoculation site as well as for systemic defence. Another one of the early events triggered by PRR stimulation is the activation of the mitogen-activated protein kinases (MAPK) cascade mediated by the G-protein complex, which will lead to several intermediate and late defence responses. Trichoderma spp. will find their way to balance this early plant response into one of mutual benefit by regulating homeostasis and reducing the synthesis of plant lipid barrier polymers, as well as by decreasing the production of SA.

Figure 2

Schematic outline of plant immune local and systemic responses to Trichoderma priming stimulus. These responses involve a transcriptional reprogramming process where the action of enhancers (Mediator complex-subunit MED25) and transcription factors (TF) have a key role in the regulation of phytohormone synthesis pathways. Regulation of these processes is mediated by small RNAs (sRNA) through a transcriptional gene silencing (TGS) mechanism—mainly through the RNA-directed DNA methylation (RdDM) pathway—or through post-transcriptional gene silencing (PTGS), which has been proven to impact whole-genome DNA methylation patterns. The inheritance of these epigenetic marks on the offspring leads to the plant immune response against abiotic or biotic stresses without the need for an external stimulus triggered by Trichoderma. Abbreviations: SA, salicylic acid; JAs, jasmonates; ET, ethylene; ABA, abscisic acid; IAA, indole-3-acetic acid; GAs, gibberellins. Created in Biorender.com.