Association between resistance to an introduced invasive pathogen and phenolic compounds that may serve as biomarkers in native oaks

• We inoculated coast live oaks with Phytophthora ramorum, cause of sudden oak death.
• Tree responses to inoculation were consistent with quantitative resistance.
• Canker size after 9 months predicted both resistance and survival 7 years later.
• Soluble phloem phenolic compounds concentrations were associated with resistance.
• Biomarkers may identify resistant trees in advance of exposure to the pathogen.

California coast live oaks (Quercus agrifolia Nee) have suffered large losses from sudden oak death, caused by the introduced oomycete Phytophthora ramorum. Infected mature coast live oaks exhibit cankers on the main stem that produce a viscous sap-derived exudate, referred to as bleeding. Subsequent attacks by ambrosia and bark beetles, followed by the activity of fungi introduced by these insects, have led to mortality levels greater than 50% since the mid-1990s. Despite an infection rate of 5% year−1, asymptomatic trees still persist in many heavily infected stands after more than 15 years of exposure to the pathogen. We hypothesized that varying responses to P. ramorum, including apparent recovery from infections, reflected phenotypic differences in susceptibility. In this study we evaluated the relationship between the early development of symptoms in mature trees that were experimentally inoculated with P. ramorum and long-term survival. A logit model showed that external canker lengths measured 9 months following inoculation predicted survival 7 years later. We defined resistance to P. ramorum in the surviving trees as absence or cessation of bleeding after the 7 years of the study and absence of beetle attacks on bleeding trees. Probability of resistance was also predicted by external canker length measured 9 months after inoculation. Canker length distribution was consistent with quantitative resistance to P. ramorum. The role of plant chemistry in resistance was examined by quantifying soluble phenolics in phloem methanol extracts prepared from the surviving trees. A logistic regression model found that expression of resistance was associated with four phenolic compounds; ellagic acid and a partially characterized ellagic acid derivative, and two chromatographic peaks that represent two uncharacterized phenolic compounds. Ellagic acid and a crude methanol extract from coast live oak phloem (total phenolics) were fungistatic when assayed in vitro at physiologically relevant levels and total phenolics were fungicidal at the highest concentration tested. The association of certain phenolics with resistance may facilitate the use of biomarkers in minimally invasive assays to predict the response of trees to P. ramorum, thereby increasing the options for managing threatened forests.