Photostimulation of Hypocrea atroviridis growth occurs due to a cross-talk of carbon metabolism, blue light receptors and response to oxidative stress

Abstract

Light is a fundamental abiotic factor which stimulates growth and development of the majority of living organisms. In soil saprotrophic fungi, light is primarily known to influence morphogenesis, particularly sexual and asexual spore formation. Here we present a new function of light, the enhancement of mycelial growth. The photostimulated mycelial growth of the soil fungus Hypocrea atroviridis was detected on 17 (out of 95 tested carbon sources) carbohydrates and polyols, which are metabolically related to cellulose and hemicelluloses, and which are mainly available in the upper soil litter layer. This stimulation depends differently on the function of the two blue light receptor proteins BLR-1 and BLR-2, respectively, BLR-1 being responsible for carbon source selectivity and response to permanent light. Evocation of oxidative stress response in darkness imitates the photostimulation on nine of these carbon sources, and this effect was fully dependent on the function of BLR-1. We conclude that light in combination with the availability of litter-specific carbon sources serves as a signal for the fungus to be above ground, thereby stimulating fast growth in order to produce a maximum of propagules in the shortest time. We further deduce that this process involves oxidative stress response and the two blue light receptor proteins BLR-1 and BLR-2, the former playing the major role. INTRODUCTIONLight is a fundamental abiotic factor that influences the majority of living organisms. In fungi, light is primarily known to stimulate morphogenetic functions such as phototropism, hyphal branching, spore discharge, reproductive morphogenesis and conidiation (Tan, 1978;Cerdá-Olmedo & Corrochano, 2001; Berrocal-Tito et al., 1999;Nagahashi & Douds, 2004). It also enhances the formation of pigments in order to protect the organisms against the deleterious effects of UV light (Li & Schmidhauser, 1995;Arrach et al., 2001). In Neurospora crassa, all light-induced phenotypes are dependent on at least one of the two regulators white-collar-1 (WC-1; Linden, 2002) and whitecollar-2 (WC-2; Linden et al., 1997). These two proteins contain a zinc finger domain and a PAS domain through which they interact physically to form the heteromultimeric 'white-collar complex', which can then recruit further protein components (Corrochano, 2007). The WC-1 protein also functions as a blue light receptor via its LOV domain and by its binding of an FAD chromophore (Liu et al., 2003). Idnurm & Heitman (2005) recently demonstrated that the WC-1/WC-2 proteins of N. crassa are present in all asco-and basidiomycetous taxa, and represent an evolutionarily ancient and conserved system to control light-dependent processes.Apart from the aforementioned studies, knowledge on other physiological properties of fungi that are influenced by light is scarce. Some authors have described effects of light on hyphal growth or branching, thereby mostly referring to inhibitory effects (Lauter et al., 1998;Chen & Dickman, 2002;Ambra et al., 2004; Casas-Flores et al., 2004...

Global nutrient profiling by Phenotype MicroArrays: a tool complementing genomic and proteomic studies in conidial fungi

“…3 (biochemical and physiological groups of carbon sources are given in Fig. 1A), PM analyses of different species displayed significant intraspecies diversities (H. jecorina) or were conserved (H. atroviridis) (Seidl et al, 2006;Friedl et al, 2008b). It was interesting to see that for H. jecorina the level of this variability was in the same range as that obtained by DNA-mediated transformation .…”

“…Furthermore, Friedl et al (2008b) showed that enhancement of mycelia growth on various carbon sources is highly light-dependent. Carbon source utilization by PMs showed that Hypocrea atroviridis growth is light-stimulated on 17 of 95 carbon sources, which are mainly metabolically related to cellulose and hemicelluloses and can be found in the upper soil litter layer (Friedl et al, 2008b).…”

“…Utilization of carbon sources in darkness was nearly the same in both knock-out mutants (Δblr-1 and Δblr-2), and it was similar to that of the parent strain. But comparing carbon utilization profiles to those exposed to rhythmic and constant illumination, Friedl et al (2008b) concluded that the mutant strains are not photostimulated, but in contrast are inhibited by light, especially in Δblr-2. Evocation of oxidative stress response in darkness imitates the photostimulation on 9 of the mentioned 17 carbon sources, and this effect is fully dependent on the function of BLR-1.…”

“…Carbon source utilization by PMs showed that Hypocrea atroviridis growth is light-stimulated on 17 of 95 carbon sources, which are mainly metabolically related to cellulose and hemicelluloses and can be found in the upper soil litter layer (Friedl et al, 2008b). The light stimulation depends on the function of two blue light receptor proteins BLR-1 and BLR-2.…”

“…The resistance of both blr mutants to conditions of oxidative stress is therefore carbon source-dependent and is notably weaker compared to the wild-type strain. Friedl et al (2008b) concluded that light in combination with the availability of litter-specific carbon sources serves as a signal for the fungus to be above ground, thereby stimulating fast growth in order to produce a maximum of propagules in the shortest time. Furthermore, they deduced that this process involves oxidative stress response and the two blue light receptor proteins BLR-1 and BLR-2, the former playing the major role.…”