Impact of the White Collar Photoreceptor WcoA on the Fusarium fujikuroi Transcriptome

Abstract

The proteins of the White Collar 1 family (WC) constitute a major class of flavin photoreceptors, widely distributed in fungi, that work in cooperation with a WC 2 protein forming a regulatory complex. The WC complex was investigated in great detail in Neurospora crassa, a model fungus in photobiology studies, where it controls all its major photoresponses. The fungus Fusarium fujikuroi, a model system in the production of secondary metabolites, contains a single WC-1 gene called wcoA. The best-known light response in this fungus is the photoinduction of the synthesis of carotenoids, terpenoid pigments with antioxidant properties. Loss of WcoA in F. fujikuroi results in a drastic reduction in the mRNA levels of the carotenoid genes, and a diversity of morphological and metabolic changes, including alterations in the synthesis of several secondary metabolites, suggesting a complex regulatory role. To investigate the function of WcoA, the transcriptome of F. fujikuroi was analyzed in the dark and after 15-, 60- or 240-min illumination in a wild strain and in a formerly investigated wcoA insertional mutant. Using a threshold of four-fold change in transcript levels, 298 genes were activated and 160 were repressed in the wild strain under at least one of the light exposures. Different response patterns were observed among them, with genes exhibiting either fast, intermediate, and slow photoinduction, or intermediate or slow repression. All the fast and intermediate photoresponses, and most of the slow ones, were lost in the wcoA mutant. However, the wcoA mutation altered the expression of a much larger number of genes irrespective of illumination, reaching at least 16% of the annotated genes in this fungus. Such genes include many related to secondary metabolism, as well as others related to photobiology and other cellular functions, including the production of hydrophobins. As judged by the massive transcriptomic changes exhibited by the wcoA mutant in the dark, the results point to WcoA as a master regulatory protein in F. fujikuroi, in addition to a central function as the photoreceptor responsible for most of the transcriptional responses to light in this fungus.

Blue Light-Dependent Pre-mRNA Splicing Controls Pigment Biosynthesis in the Mushroom Terana caerulea

“…For ascomycetes, A. nidulans with its velvet complex VelB/VeA and LaeA, the global regulator of secondary metabolism, was pivotal in unraveling the triple interconnection of light with the development and regulation of natural product metabolism ( 43 ). A comparative transcriptomic study confirmed the role of light in the regulation of carotene and other natural product genes by comparing wild-type Fusarium fujikuroi to a wcoA mutant that lost the functional white collar 1 protein ( 44 ).…”

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

“…Furthermore, in the transcriptome we found a strong reduction in the number of transcripts responsive to blue light in the Δ blr -1 mutant, which shows that it is the main photoreceptor within the blue light perception system in T. atroviride . It was recently described in Fusarium fujikuroi that a drastic decrease occurs in the mRNA levels of carotenoid genes, as well as morphological and metabolic changes in a mutant of the wco A gene, encoding a White-Collar 1 orthologue ( Pardo-Medina et al, 2021 ). This result is quite interesting since this analysis was carried out early (15, 60, and 240 min) upon exposure to constant light of the WT and the wcoA strains and their results coincide with ours at 30 min, even though these two species of fungi are phylogenetically distant.…”

Fungal Secondary Metabolism

“…Another general regulator of special interest is LaeA [70], which is associated with light regulation and development control with Velvet proteins forming a complex [71,72]. It has recently been observed that the main regulator by light in F. fujikuroi, WcoA, positively or negatively controls different SM clusters in this fungus [73]. This double positive/negative role on different pathways is frequent in these global regulatory systems, even when responding to the same signal.…”