Trichoderma Histone Deacetylase HDA-2 Modulates Multiple Responses in Arabidopsis

Abstract

Trichoderma spp. are a rich source of secondary metabolites and volatile organic compounds (VOCs), which may induce plant defenses and modulate plant growth. In filamentous fungi, chromatin modifications regulate secondary metabolism. In this study we investigated how the absence of histone deacetylase HDA-2 in the Trichoderma atroviride strain Dhda-2 impacts its effect on a host, Arabidopsis (Arabidopsis thaliana). The production of VOCs and their impact on plant growth and development were assessed as well. The Dhda-2 strain was impaired in its ability to colonize Arabidopsis roots, thus affecting the promotion of plant growth and modulation of plant defenses against foliar pathogens Botrytis cinerea and Pseudomonas syringae, which normally result from interaction with T. atroviride. Furthermore, Dhda-2 VOCs were incapable of triggering plant defenses to counterattack foliar pathogens. The Dhda-2 overproduced the VOC 6-pentyl-2H-pyran-2-one (6-PP), which resulted in enhanced root branching and differentially regulated phytohormone-related genes. Analysis of ten VOCs (including 6-PP) revealed that three of them positively regulated plant growth, whereas six had the opposite effect. Assessment of secondary metabolites, detoxification, and communication with plant-related genes showed a dual role for HDA-2 in T. atroviride gene expression regulation during its interaction with plants. Chromatin immunoprecipitation of acetylated histone H3 on the promoters of plant-responsive genes in Dhda-2 showed, in the presence of Arabidopsis, low levels of epl-1 and abc-2 compared with that in the wild type; whereas ctf-1 presented high constitutive levels, supporting a dual role of HDA-2 in gene regulation. This work highlights the importance of HDA-2 as a global regulator in Trichoderma to modulate multiple responses in Arabidopsis. Phytohormones are small, signaling molecules, which occur at low concentrations and play pivotal roles in plants, including influencing plant growth and development. Classical phytohormones comprise auxins, abscisic acid, cytokinins, ethylene (ET), and gibberellic acid. However, brassinosteroids, jasmonates (JAs), and salicylic acid (SA) are considered phytohormones as well. These signaling molecules not only integrate, but also transmit environmental signals and modulate responses to abiotic and biotic stresses (Pieterse et al., 2009; De Bruyne et al., 2014). In their natural environments, plants interact with a plethora of microorganisms, establishing pathogenic or beneficial relationships. The plant response against these microbes lies primarily in an array of structural barriers or inducible defenses. The plant immune system has the ability to perceive nonself by recognizing pathogen-or microbe-associated molecular patterns (PAMPs or MAMPs, respectively), and translate this perception into an appropriate adaptive response (Pieterse et al., 2009). Plants have developed the ability to enhance their basal resistance after PAMPs or MAMPs are detected, by triggering the systemic acquired resistanc...

The Trichoderma atroviride Strains P1 and IMI 206040 Differ in Their Light-Response and VOC Production

“…oxysporum-T. atroviride co-cultivation further resulted in the production of 2-octanone, a volatile that was not emitted by any of the interaction partners upon axenic growth. Interestingly, a recent study revealed that deletion of the histone deacetylase-encoding gene hda-2 in T. atroviride IMI 206040 leads to the biosynthesis of 2-octanone as a new volatile in this strain [43]. This report together with our results points out that 2-octanone biosynthesis genes could be shut-down by a repressive chromatin structure and could be activated epigenetically as a consequence of environmental stimuli, in this case the interaction with F. oxysporum.…”

Trichoderma as a Model to Study Effector-Like Molecules

“…Successful establishment of the Trichoderma –plant interaction during early stages of root colonization implies the activation of cell detoxification and protection mechanisms in the fungi (Ruocco et al, 2009; Estrada-Rivera et al, 2019). Therefore, these fungi possess effective systems that efficiently scavenge harmful compounds from the cell.…”

“…The expression of these genes is transient and decreased to levels of the control plants. Trichoderma resembles mycorrhizal fungi in the establishment of symbiotic associations rather than fungal pathogens (Masunaka et al, 2011; Estrada-Rivera et al, 2019). Production of sRNAs by filamentous fungi, including Trichoderma species, has been documented.…”

Sniffing fungi – phenotyping of volatile chemical diversity inTrichodermaspecies

“…are able to establish in the rhizosphere of host plants, leading to beneficial effects (Guzmán‐Guzmán et al , 2018). The growth‐promoting effects are based on mobilization of nutrients (Harman, 2011), induction of plant systemic resistance (Shoresh et al , 2010; Estrada‐Rivera et al , 2019), and a mycotrophic lifestyle towards plant pathogens (Druzhinina et al , 2011; Kubicek et al , 2011). Recent studies show very species‐specific volatile profiles for Trichoderma (Siddiquee et al , 2012; Lee et al , 2016; Guo et al , 2019), whose patterns can drastically change in interaction with other organisms (Guo et al , 2019), suggesting important ecological functions for fVOCs of Trichoderma .…”