Summary: Conidia of Trichoderma guizhouense (Hypocreales, Ascomycota) are frequently applied to the production of biofertilizers and biocontrol agents. Conidiation of some Trichoderma species depends on blue light and the action of different blue light receptors. However, the interplay between different blue‐light receptors in light signalling remained elusive. Here, we studied the functions of the blue light receptors BLR1 and ENV1, and the MAP kinase HOG1 in blue light signalling in T . guizhouense . We found that the BLR1 dominates light responses and ENV1 is responsible for photoadaptation. Genome‐wide gene expression analyses revealed that 1615 genes, accounting for ~13.4% of the genes annotated in the genome, are blue‐light regulated in T . guizhouense , and remarkably, these differentially expressed genes (DEGs) including 61 transcription factors. BLR1 and HOG1 are the core components of the light signalling network, which control 79.9% and 73.9% of the DEGs respectively. In addition, the strict regulation of hydrophobin production by the blue light signalling network is impressive. Our study unravels the regulatory network based on the blue light receptors and the MAPK HOG pathway for conidiation, hydrophobin production and other processes in T . guizhouense .

In several filamentous fungi, incident light and environmental stress signaling share the mitogen‐activated protein kinase (MAPK) HOG (SAK) pathway. It has been revealed that short‐term illumination with blue light triggers the activation of the HOG pathway in Trichoderma spp. In this study, we demonstrate the crucial role of the basic leucine zipper transcription factor ATF1 in blue light responses and signaling downstream of the MAPK HOG1 in Trichoderma guizhouense. The lack of ATF1 severely impaired photoconidiation and delayed vegetative growth and conidial germination. Upon blue light or H₂O₂ stimuli, HOG1 interacted with ATF1 in the nucleus. Genome‐wide transcriptome analyses revealed that 61.8% (509 out of 824) and 85.2% (702 out of 824) of blue light‐regulated genes depended on ATF1 and HOG1, respectively, of which 58.4% (481 out of 824) were regulated by both of them. Our results also show that blue light promoted conidial germination and HOG1 and ATF1 played opposite roles in controlling conidial germination in the dark. Additionally, the lack of ATF1 led to reduced oxidative stress resistance, probably because of the downregulation of catalase‐encoding genes. Overall, our results demonstrate that ATF1 is the downstream component of HOG1 and is responsible for blue light responses, conidial germination, vegetative growth, and oxidative stress resistance in T. guizhouense.

Light is perceived by photoreceptors in fungi and further integrated into the stress-activated MAPK HOG pathway, and thereby potentially activates the expression of genes for stress responses. This indicates that the precise control of light conditions can likely improve the conidial yield and stress resistance to guarantee the low cost and long shelf life of Trichoderma-based biocontrol agents and biofertilizers. In this study, effects of wavelengths and intensities of light on conidial yield and stress tolerance to osmotic, oxidative and pH stresses in Trichoderma guizhouense were investigated. We found that 2 μmol photons/(m² × s) of blue light increased the conidial yield more than 1000 folds as compared to dark condition and simultaneously enhanced conidial stress resistance. The enhanced conidial stress resistance is probably due to the upregulated stress-related genes in blue light, which is under the control of the blue light receptor BLR1 and the MAP kinase HOG1.

Light as a source of information regulates morphological and physiological processes of fungi, including development, primary and secondary metabolism, or the circadian rhythm. Light signaling in fungi depends on photoreceptors and downstream components that amplify the signal to govern the expression of an array of genes. Here, we investigated the effects of red and far-red light in the mycoparasite Trichoderma guizhouense on its mycoparasitic potential. We show that the invasion strategy of T. guizhouense depends on the attacked species and that red and far-red light increased aerial hyphal growth and led to faster overgrowth or invasion of the colonies. Molecular experiments and transcriptome analyses revealed that red and far-red light are sensed by phytochrome FPH1 and further transmitted by the downstream MAPK HOG pathway and the bZIP transcription factor ATF1. Overexpression of the red- and far-red light-induced fluffy gene fluG in the dark resulted in abundant aerial hyphae formation and thereby improvement of its antagonistic ability against phytopathogenic fungi. Hence, light-induced fluG expression is important for the mycoparasitic interaction. The increased aggressiveness of fluG-overexpressing strains was phenocopied by four random mutants obtained after UV mutagenesis. Therefore, aerial hyphae formation appears to be a trait for the antagonistic potential of T. guizhouense.

Glyphosate-based herbicides (GBHs) are used worldwide for weed management. However, GBHs pose a threat to soil fungal community, although fungi can degrade and use glyphosate as a nutrient source. How fungi respond to GBHs remains enigmatic. Here, we found that, not as in plants, the commercial GBH Roundup does not target the 5-enolpyruvyl-shikimate-3-phosphate synthase in the soil-derived fungus Trichoderma guizhouense , whereas it impairs fungal growth. We demonstrate that the herbicide adjuvant Triton CG-110 is more toxic to fungal cells than pure glyphosate. It limits nitrogen uptake, which induces the expression of proteinase YPS1 to catalyze the shedding of the MSB2 extracellular domain from the plasma membrane, leading to the activation of the MAPK TMK1 pheromone pathway. The downstream B2H2-type transcription factor STE12 directly regulates ergosterol biosynthesis, affecting membrane fluidity and stability. To our knowledge, this is the first evidence that the pheromone pathway is implicated in ergosterol biosynthesis and plasma membrane integrity.