Distinctive carbon repression effects in the carbohydrate-selective wood decay fungus Rhodonia placenta

Brown rot fungi dominate the carbon degradation of northern terrestrial conifers. These fungi adapted unique genetic inventories to degrade lignocellulose and to rapidly release a large quantity of carbohydrates for fungal catabolism. We know that brown rot involves “two-step” gene regulation to delay most hydrolytic enzyme expression until after harsh oxidative pretreatments. This implies the crucial role of concise gene regulation to brown rot efficacy, but the underlying regulatory mechanisms remain uncharacterized. Here, using the combined transcriptomic and enzyme analyses we investigated the roles of carbon catabolites in controlling gene expression in model brown rot fungus Rhodonia placenta. We identified co-regulated gene regulons as shared transcriptional responses to no-carbon controls, glucose, cellobiose, or aspen wood (Populus sp.). We found that cellobiose, a common inducing catabolite for fungi, induced expression of main chain-cleaving cellulases in GH5 and GH12 families (cellobiose vs. no-carbon > 4-fold, P_adj < 0.05), whereas complex aspen was a universal inducer for Carbohydrate Active Enzymes (CAZymes) expression. Importantly, we observed the attenuated glucose-mediated repression effects on cellulases expression, but not on hemicellulases and lignin oxidoreductases, suggesting fungi might have adapted diverged regulatory routes to boost cellulase production for the fast carbohydrate release. Using carbon regulons, we further predicted the cis- and trans-regulatory elements and assembled a network model of the distinctive regulatory machinery of brown rot. These results offer mechanistic insights into the energy efficiency traits of a common group of decomposer fungi with enormous influence on the carbon cycle.