Conifer constitutive defense chemistry is resistant to short-term drought, but tree susceptibility to bark beetles may still increase via concurrent shifts in primary chemistry

Background/Question/Methods

Large-scale insect outbreaks are frequently correlated with drought, but the drought-induced physiological and metabolic mechanisms driving tree susceptibility to destructive herbivores remain unresolved. Specialized metabolites, including terpenes and phenolics, are effective defenses against insects yet may vary in concert with primary metabolites that provide carbon substrate for defense metabolism, and/or that have nutritive value for herbivores. For example, metabolic shifts that help trees cope with drought stress (e.g., increasing soluble sugars) may increase host suitability, but this effect could be masked by concurrent increases in defense metabolites. Both nutritive and defensive compounds vary in response to drought intensity and duration, but their potential net effect on bark beetles remains unknown. To address this research gap, we quantified starch, sugars, terpenes, and phenolics during three growing seasons from the secondary phloem of mature piñon pines (Pinus edulis) that experienced ambient conditions or have undergone either short- or long-term drought. Short-term drought treatments include removal of 45 or 90% of ambient precipitation over two years, while trees in the long-term drought treatment experienced 45% removal of ambient precipitation over eleven years. In tandem with targeted metabolomics, we measured pre-dawn water potential and net assimilation to link primary physiology to phloem metabolism.

Results/Conclusions

Targeted metabolites responded uniquely to short- and long-term drought, and were relatively resistant to drought overall. Notably, we observed that ambient trees had greater terpene concentrations relative to trees exposed to long-term drought, and greater starch concentrations compared to all drought treatments (short- and long-term). Contrary to expectations, we found no correlation among metabolite concentrations. Water potential and gas exchange also did not explain the variation in metabolite concentrations, though this was unsurprising since shifts in water potential and gas-exchange likely occur over much shorter timescales than phloem chemistry. To account for the effect of long-term drought physiology on phloem chemistry, we used monthly water potential measurements and the approximate zero-assimilation point to estimate the ‘cumulative drought stress’ experienced by trees. Employing this approach revealed decreased starch concentrations in response to cumulative drought stress. Together, these results show that the phloem chemistry of piñon pine is generally resistant to short-term drought, but cumulative drought stress may decrease starch availability with consequences for defensive metabolite synthesis. It is likely that tree susceptibility to bark beetles may be independent of constitutive defenses, and instead depend on starch availability to induce a defense response when challenged by bark beetle attacks.