The CarO rhodopsin of the fungus Fusarium fujikuroi is a light-driven proton pump that retards spore germination

Abstract

Rhodopsins are membrane-embedded photoreceptors found in all major taxonomic kingdoms using retinal as their chromophore. They play well-known functions in different biological systems, but their roles in fungi remain unknown. The filamentous fungus Fusarium fujikuroi contains two putative rhodopsins, CarO and OpsA. The gene carO is light-regulated, and the predicted polypeptide contains all conserved residues required for proton pumping. We aimed to elucidate the expression and cellular location of the fungal rhodopsin CarO, its presumed proton-pumping activity and the possible effect of such function on F. fujikuroi growth. In electrophysiology experiments we confirmed that CarO is a green-light driven proton pump. Visualization of fluorescent CarO-YFP expressed in F. fujikuroi under control of its native promoter revealed higher accumulation in spores (conidia) produced by light-exposed mycelia. Germination analyses of conidia from carO− mutant and carO+ control strains showed a faster development of light-exposed carO− germlings. In conclusion, CarO is an active proton pump, abundant in light-formed conidia, whose activity slows down early hyphal development under light. Interestingly, CarO-related rhodopsins are typically found in plant-associated fungi, where green light dominates the phyllosphere. Our data provide the first reliable clue on a possible biological role of a fungal rhodopsin.

White collar 1‐induced photolyase expression contributes to UV ‐tolerance of Ustilago maydis

“…; Garzia‐Martinez et al. ); 3. We sampled only at one time point (60 min) after light on and thus could have missed transcripts expressed late or very transient as has been described for N. crassa (Chen et al.…”

“…We used a very stringent cutoff for the analysis of array data; 2. We checked the specific role of blue light thus excluding activation of rhodopsins and phytochrome, which operate in the green and red spectral range, respectively (Blumenstein et al 2005;Brandt et al 2008;Purschwitz et al 2008;Garzia-Martinez et al 2015); 3. We sampled only at one time point (60 min) after light on and thus could have missed transcripts expressed late or very transient as has been described for N. crassa (Chen et al 2009).…”

Carotenoid Cleavage Oxygenases from Microbes and Photosynthetic Organisms: Features and Functions

“…Very few fungal rhodopsins have been functionally investigated, among them NOP-1 in N. crassa [44], Ops in Leptosphaeria maculans [45,46], and CarO [47], and OpsA in F. fujikuroi [48]. The participation of retinal in the activity of these proteins has only been demonstrated for NOP-1 [49] and CarO [50]. …”

Seeing the world differently: variability in the photosensory mechanisms of two model fungi

“…CarO is distributed primarily at the plasma membrane, where it serves as a green light-activated proton pump (Garcia-Martinez J. et al ., 2015). Unlike NOP-1 of N. crassa , which does not affect light-dependent processes in that organism, loss of CarO function leads to enhanced conidial germination rates in light (Garcia-Martinez J. et al ., 2015). This suggests that CarO plays a role in repressing conidial germination, comparable to the role of the phytochrome in A. nidulans .…”