Red- and Blue-Light Sensing in the Plant Pathogen Alternaria alternata Depends on Phytochrome and the White-Collar Protein LreA

The filamentous fungus is a common postharvest contaminant of food and feed, and some strains are plant pathogens. Many processes in are triggered by light. Interestingly, blue light inhibits sporulation, and red light reverses the effect, suggesting interactions between light-sensing systems. The genome encodes a phytochrome (FphA), a white collar 1 (WC-1) orthologue (LreA), an opsin (NopA), and a cryptochrome (CryA) as putative photoreceptors. Here, we investigated the role of FphA and LreA and the interplay with the high-osmolarity glycerol (HOG) mitogen-activated protein (MAP) kinase pathway. We created loss-of function mutations for , , and using CRISPR-Cas9 technology. Sporulation was reduced in all three mutant strains already in the dark, suggesting functions of the photoreceptors FphA and LreA independent of light perception. Germination of conidia was delayed in red, blue, green, and far-red light. We found that light induction of ( lock- ontrolled ene in and light-induced gene in ) and the catalase gene depended on FphA, LreA, and HogA. Light induction of (a putative ferrochelatase gene) and ( light regulated, unknown function) required LreA and HogA but not FphA. Blue- and green-light stimulation of alternariol formation depended on LreA. A lack of FphA or LreA led to enhanced resistance toward oxidative stress due to the upregulation of catalases and superoxide dismutases. Light activation of FphA resulted in increased phosphorylation and nuclear accumulation of HogA. Our results show that germination, sporulation, and secondary metabolism are light regulated in with distinct and overlapping roles of blue- and red-light photosensors. Light controls many processes in filamentous fungi. The study of light regulation in a number of model organisms revealed an unexpected complexity. Although the molecular components for light sensing appear to be widely conserved in fungal genomes, the regulatory circuits and the sensitivity of certain species toward specific wavelengths seem different. In , most light responses are triggered by blue light, whereas in , red light plays a dominant role. In , both blue and red light appear to be important. In , photoreceptors control morphogenetic pathways, the homeostasis of reactive oxygen species, and the production of secondary metabolites. On the other hand, high-osmolarity sensing required FphA and LreA, indicating a sophisticated cross talk between light and stress signaling.