Abstract:
Norway spruce (Picea abies) is periodically attacked by the bark beetle Ips typographus and its fungal associate,
Endoconidiophora polonica, whose infection is thought to be required for successful beetle attack. Norway spruce
produces terpenoid resins and phenolics in response to fungal and bark beetle invasion. However, how the fungal
associate copes with these chemical defenses is still unclear. In this study, we investigated changes in the phenolic
content of Norway spruce bark upon E. polonica infection and the biochemical factors mediating these changes.
Although genes encoding the rate-limiting enzymes in Norway spruce stilbene and flavonoid biosynthesis were
actively transcribed during fungal infection, there was a significant time-dependent decline of the corresponding
metabolites in fungal lesions. In vitro feeding experiments with pure phenolics revealed that E. polonica transforms
both stilbenes and flavonoids to muconoid-type ring-cleavage products, which are likely the first steps in the
degradation of spruce defenses to substrates that can enter the tricarboxylic acid cycle. Four genes were identified in
E. polonica that encode catechol dioxygenases carrying out these reactions. These enzymes catalyze the cleavage of phenolic
rings with a vicinal dihydroxyl group to muconoid products accepting a wide range of Norway spruce-produced phenolics
as substrates. The expression of these genes and E. polonica utilization of the most abundant spruce phenolics as carbon
sources both correlated positively with fungal virulence in several strains. Thus, the pathways for the degradation of
phenolic compounds in E. polonica, initiated by catechol dioxygenase action, are important to the infection, growth, and
survival of this bark beetle-vectored fungus and may play a major role in the ability of I. typographus to colonize spruce
trees.
