Transcriptome analyses of the Chinese white pine beetle-fungal symbiont Leptographium qinlingensis under terpene stress or growth on host pine sawdust

Microbial consortia cohabitate within bark beetles, constituting an entity known as the bark beetle holobiont, which has been reported to play an important role in the nutrition of beetle host trees, in addition to the detoxification of tree chemical defences. The ascomycete Leptographium qinlingensis is one of the major externally living fungal associates of the Chinese white pine beetle (Dendroctonus armandi), which can kill host trees when it invades Chinese white pine (Pinus armandii) despite the accumulation of defence chemicals. Here, we observed the effect of monoterpenes and diterpenes on L. qinlingensis growth and reproduction and examined pine sawdust utilization by the fungus, including its enzyme activity related to cellulose and lignin degradation. The transcriptome of L. qinlingensis during growth on host pine sawdust and malt extract agar under monoterpene/diterpene treatment was analysed to reveal the main genes and enzymes involved in terpene tolerance and nutrition utilization. This symbiotic fungus showed tolerance to monoterpenes and diterpenes and was able to retrieve carbon sources in host pine sawdust. Many unigenes that encode diverse enzymes, including ABC transporters, monooxygenases, dioxygenases and dehydrogenases, were identified in the transcriptome analysis, as were enzymes involved in amino acid and carbohydrate metabolism. These candidate genes will be important for further studies examining the role of terpenoid tolerance in the pathogenicity of L. qinlingensis and for characterizing the molecular interactions between beetle-symbiotic fungi and their host trees.

Automated summary

This study reveals the tolerance of Leptographium qinlingensis to monoterpenes and diterpenes and its ability to utilize carbon sources in host pine sawdust. The transcriptome analysis identified key genes and enzymes involved in terpene tolerance and nutrition utilization. These findings are important for further understanding the pathogenicity of L. qinlingensis and the molecular interactions between beetle-symbiotic fungi and their host trees.