The Dark Side of Orchid Symbiosis: Can Tulasnella calospora Decompose Host Tissues?

Photosynthetic orchids associate with mycorrhizal fungi that can be mostly ascribed to the
"rhizoctonia" species complex. Rhizoctonias' phylogenetic diversity covers a variety of
ecological/nutritional strategies that include, beside the symbiosis establishment with host plants,
endophytic and pathogenic associations with non-orchid plants or saprotrophic soil colonization.
In addition, orchid mycorrhizal fungi (OMF) that establish a symbiotic relationship with an orchid
host can later proliferate in browning and rotting orchid tissues. Environmental triggers and
molecular mechanisms governing the switch leading to either a saprotrophic or a mycorrhizal
behavior in OMF remain unclear. As the sequenced OMF genomes feature a wide range of genes
putatively involved in the degradation of plant cell wall (PCW) components, we tested if these
transitions may be correlated with a change in the expression of some PCW degrading enzymes.
Regulation of several genes encoding PCW degrading enzymes was evaluated during saprotrophic
growth of the OMF Tulasnella calospora on different substrates and under successful and
unsuccessful mycorrhizal symbioses. Fungal gene expression in planta was investigated in two
orchid species, the terrestrial Mediterranean Serapias vomeracea and the epiphytic tropical Cattleya
purpurata. Although we only tested a subset of the CAZyme genes identified in the T. calospora
genome, and we cannot exclude therefore a role for different CAZyme families or members inside
a family, the results showed that the degradative potential of T. calospora is finely regulated during
saprotrophic growth and in symbiosis, often with a different regulation in the two orchid species.
These data pose novel questions about the role of fungal PCW degrading enzymes in the
development of unsuccessful and successful interactions.
Keywords: CAZymes; orchid mycorrhiza; gene expression; saprotrophic