Transcriptional responses of Eucalyptus to infection by an aggressive leaf blight pathogen reveal the role of host secondary metabolites during pathogen germination

Teratosphaeria leaf blight disease caused by Teratosphaeria destructans poses a serious threat to Eucalyptus plantations worldwide. The pathogen infects leaves via stomatal penetration from 24 to 72 h after inoculation. Symptoms are visible after two weeks and pathogen sporulation commonly occurs four weeks after inoculation of a susceptible host. We studied the responses of a susceptible Eucalyptus clone during the entire disease cycle to identify susceptibility factors. RNA from healthy and infected leaves was isolated at 3, 14 and 28 days post inoculation. Differential expression and gene enrichment analysis showed that members of the transcription factor family TGA and MYB, involved in the salicylic acid and abscisic acid pathways, and genes involved in these hormone signaling pathways, were up-regulated. Overall, plant defense response pathways were enriched only at the late stage of infection (28 dpi). In contrast, both gene expression and chemical analysis revealed that the synthesis of the major flavonoids in Eucalyptus leaves was enhanced during pathogen infection, while the synthesis of terpenoids and flavan-3-ols declined. The flavonols, rutin and quercetin enhanced spore germination in-vitro while, the terpenoid eucalyptol and the flavan-3-ol catechin inhibited germination. This study provides insights into the molecular and chemical responses at different stages of infection of a susceptible host by T. destructans, thereby improving the current understanding of the pathosystem.