Integration of chemosensing and carbon catabolite repression impacts fungal enzyme regulation and plant associations

Abstract

Fungal metabolism and enzyme production are regulated by nutrient availability and by interactions with the living environment. We investigated the mechanisms underpinning adaptation of the biotechnological fungus Trichoderma reesei to decaying plant biomass versus living plants. We found that concentration-gated response to glucose, the main molecule sensed from dead plant biomass, is mediated by a conserved signaling pathway downstream of G protein-coupled receptors (GPCRs), while the carbon catabolite repressor CRE1 is critical for glucose concentration gating. The GPCRs CSG1 and CSG2 are further required for root colonization and formation of appressorium like structures on plant surfaces. Acceleration of sexual development in the presence of plant roots and their interactions with fruiting bodies indicates preferential association with plants. Our results reveal a complex sensing network governing resource distribution, enzyme production and fungal development that explains previously observed phenomena in fermentations and opens new perspectives for industrial strain improvement and agriculture.

Network Analysis Reveals Different Cellulose Degradation Strategies Across Trichoderma harzianum Strains Associated With XYR1 and CRE1

“…Heterotrimeric G proteins have been well studied in several Trichoderma species. In saprophytic species, such proteins are involved in the nutrient signaling pathway in connection with a light response, triggering the posttranscriptional regulation of cellulase expression ( Hinterdobler et al, 2021 ); in mycoparasitic species, G protein-coupled receptors are involved in the regulation of processes related to mycoparasitism ( Zeilinger and Atanasova 2020 ).…”

MAPkinases regulate secondary metabolism, sexual development and light dependent cellulase regulation in Trichoderma reesei

“…Investigation of G-protein coupled receptors (GPCRs) implicated two class XIII (DUF300 domain) GPCRs, CSG1 and CSG2 in glucose sensing due to their impact on cellulase regulation on cellulose and lactose 78 . This function was supported by the requirement of CSG1 and CSG2 for chemotropic responses to specific concentrations of glucose 84 . Since a role in chemotropic reaction to glucose was shown for FMK1, the Fusarium oxysporum homologue of filamentation pathway MAPkinase 22 , we were interested in the role of T. reesei MAPkinases in chemotropic reactions to glucose.…”

“…Since also the GPCRs CSG1 and CSG2 are required for chemotropic reactions to glucose 84 , the signaling pathway triggering this reaction in T. reesei might not be exclusively channeled through the G-protein pathway but may be subject to biased signaling 85 .…”

“…The GPCR CSG1, which is essential for the chemotropic response of T. reesei to glucose 84 , was shown to be required for posttranscriptional regulation of cellulase gene expression 78 . Importantly, this GPCR is not related to other known glucose sensing GPCRs like GPR-1 in N. crassa or Gpa2 of S. cerevisiae 78 .…”

Trichoderma – genomes and genomics as treasure troves for research towards biology, biotechnology and agriculture

“…show an exceptional versatility in their preferred habitats and substrates with lifestyles ranging from mycoparasitism to plant saprotrophy and accordingly life in habitats characterized by feeding on fungi or decaying plant material, in soil or even as endophytes in living plant tissue, which changed during evolution several times (Chaverri and Samuels, 2013) Starting from the genome sequence of T. reesei, which was published in 2008 (Martinez et al, 2008), the genomes of numerous Trichoderma model strains for enzyme production and biocontrol followed (Figure 1). The availability of the genome sequences of major model fungi of Trichoderma considerably contributed to detailed investigation of mechanisms of action and regulation of pathways (Sood et al, 2020), which is focused on systemic resistance of plants (Shoresh et al, 2010), colonization (Hinterdobler et al, 2021b;Taylor et al, 2021;Hafiz et al, 2022;Taylor et al, 2022), effector molecules (Ramirez-Valdespino et al, 2019) and plantfungus-pathogen interactions (Mendoza-Mendoza et al, 2018;Macias-Rodriguez et al, 2020;Alfiky and Weisskopf, 2021) among others.…”