Genome-wide analyses of light-regulated genes in Aspergillus nidulans reveal a complex interplay between different photoreceptors and novel photoreceptor functions

Abstract

Fungi sense light of different wavelengths using blue-, green-, and red-light photoreceptors. Blue light sensing requires the “white-collar” proteins with flavin as chromophore, and red light is sensed through phytochrome. Here we analyzed genome-wide gene expression changes caused by short-term, low-light intensity illumination with blue-, red- or far-red light in Aspergillus nidulans and found that more than 1100 genes were differentially regulated. The largest number of up- and downregulated genes depended on the phytochrome FphA and the attached HOG pathway. FphA and the white-collar orthologue LreA fulfill activating but also repressing functions under all light conditions and both appear to have roles in the dark. Additionally, we found about 100 genes, which are red-light induced in the absence of phytochrome, suggesting alternative red-light sensing systems. We also found blue-light induced genes in the absence of the blue-light receptor LreA. We present evidence that cryptochrome may be part of this regulatory cue, but that phytochrome is essential for the response. In addition to in vivo data showing that FphA is involved in blue-light sensing, we performed spectroscopy of purified phytochrome and show that it responds indeed to blue light. Author summary Fungi are microorganisms with important roles in the environment, as symbionts, as pathogens, or as workhorses in biotechnology. They constantly need to adapt to changing environmental conditions, often far away from their optima. One important environmental factor, fungi respond to is ambient light. The presence of light tells them if they are exposed to a surface and thus potentially to heat, harmful irradiation, or desiccation or other stressful conditions, or whether they are growing inside soil or litter with more constant conditions. Interestingly, many fungi harbor photosensors for blue-, green- and red light. We show here that in the model fungus Aspergillus nidulans a large proportion of the genome is under light control, and many genes are regulated through phytochrome and thus by red light. However, phytochrome is also used for blue-light sensing. Many genes are controlled by blue- and by red light signaling systems, but many also respond only to specific wavelengths. The study provides important groundwork for future research to unravel how different genes are regulated at the molecular level and to decipher the biological meaning for the complex light-regulatory systems found in fungi.