A Global Analysis of Photoreceptor-Mediated Transcriptional Changes Reveals the Intricate Relationship Between Central Metabolism and DNA Repair in the Filamentous Fungus Trichoderma atroviride

Abstract

Light provides critical information for the behavior and development of basically all organisms. Filamentous fungi sense blue light, mainly, through a unique transcription factor complex that activates its targets in a light-dependent manner. In Trichoderma atroviride, the BLR-1 and BLR-2 proteins constitute this complex, which triggers the light-dependent formation of asexual reproduction structures (conidia). We generated an ENVOY photoreceptor mutant and performed RNA-seq analyses in the mutants of this gene and in those of the BLR-1, CRY-1 and CRY-DASH photoreceptors in response to a pulse of low intensity blue light. Like in other filamentous fungi BLR-1 appears to play a central role in the regulation of blue-light responses. Phenotypic characterization of the Δenv-1 mutant showed that ENVOY functions as a growth and conidiation checkpoint, preventing exacerbated light responses. Similarly, we observed that CRY-1 and CRY-DASH contribute to the typical light-induced conidiation response. In the Δenv-1 mutant, we observed, at the transcriptomic level, a general induction of DNA metabolic processes and strong repression of central metabolism. An analysis of the expression level of DNA repair genes showed that they increase their expression in the absence of env-1. Consistently, photoreactivation experiments showed that Δenv-1 had increased DNA repair capacity. Our results indicate that light perception in T. atroviride is far more complex than originally thought.

Fusarium Photoreceptors

“…Surprisingly, the lack of the WC complex altered the adaptation to constant illumination, as the number of genes differentially expressed in light increased to about 9% in the mutants of the wc-1 and wc-2 orthologs brl1 and brl2 . A new RNA-seq study of the effect of a 30 min light pulse in T. atroviride , using a different bioinformatic analysis for differential expression, found 97 and 38 genes upregulated and downregulated in the wild type, of which only 3 from each class maintained photoregulation in the blr-1 mutant, indicating that this WC protein mediates most of the photoresponses in this species [ 170 ]. This study of T. atroviride was extended to mutants for the ENVOY, CRY-1, and CRY-DASH photoreceptors, but their roles in photoregulation were subsidiary to Blr1, since the transcription of their genes was activated by light through this photoreceptor.…”

The bZIP transcription factor ATF1 regulates blue light and oxidative stress responses in Trichoderma guizhouense

“…The blue light receptor BLR1, the ortholog of Neurospora crassa white collar‐1 protein, tightly controls the photoconidiation process 26–29 . Recent genome‐wide transcriptome analyses have revealed that BLR1 is the main component of the blue light signaling network in Trichoderma 28,29 …”

“…Photobiology studies in Trichoderma have shown that blue light can efficiently promote conidia production and increase the resistance of conidia to several environmental stresses. The blue light receptor BLR1, the ortholog of Neurospora crassa white collar‐1 protein, tightly controls the photoconidiation process 26 , 27 , 28 , 29 . Recent genome‐wide transcriptome analyses have revealed that BLR1 is the main component of the blue light signaling network in Trichoderma .…”

Metarhizium pingshaense photolyase expression and virulence to Rhipicephalus microplus after UV‐B exposure

“…It can be defined as a direct enzymatic in situ reversal of dimerized pyrimidines in a DNA strand mediated by photolyase [23,24]. Several entomopathogenic fungal studies about photolyase have been reported [20,[25][26][27][28], but the expression curve of this enzyme in blastospores and the virulence of this fungal propagule to ticks after UV exposure are yet to be examined.…”