Trichoderma Histone Deacetylase HDA-2 Modulates Multiple Responses in Arabidopsis

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 Δhda-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 Δhda-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, Δhda-2 VOCs were incapable of triggering plant defenses to counterattack foliar pathogens. The Δhda-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 Δhda-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.