Abstract
AbstractThe emerald ash borer (Agrilus planipennis, EAB) invasion in North America threatens most North American Fraxinus species, including green ash (F. pennsylvanica), the mostly widely distributed species (1, 2). A small number of green ash (“lingering ash”, 0.1-1%) survive years of heavy EAB attack (3) and kill more EAB larvae when challenged in greenhouse studies than susceptible controls (4). We combined untargeted metabolomics with intensive phenotyping of segregating F1 progeny from susceptible or lingering ash parents to detect chemotypes associated with defensive responses to EAB. We examined three contrasting groups: low larval kill (0-25% of larvae killed), high larval kill (55-95% of larvae killed) and uninfested. Contrasting the chemotypes of these groups revealed evidence of an induced response to EAB. Infested trees deployed significantly higher levels of select secoiridoids than uninfested trees. Within the infested group, the low larval kill (LLK) individuals deployed significantly higher levels of select secoiridoids than the high larval kill (HLK) individuals. The HLK individuals deployed significantly higher concentrations of three metabolites annotated as aromatic alkaloids compared to the LLK and uninfested individuals. We propose a two-part model for the North American Fraxinus response to EAB wherein every individual has the capacity to detect and respond to EAB, but only certain trees mount an effective defense, killing enough EAB larvae to prevent or minimize lethal damage to the vascular system. Integration of intensive phenotyping of structured populations with metabolomics reveals the multi-faceted nature of the defenses deployed in naïve host populations against invasive species.SignificanceLong-lived forest trees employ evolutionarily conserved templates to synthesize an array of defensive metabolites. The regulation of these metabolites, honed against native pests and pathogens, may be ineffective against novel species, as illustrated by the high mortality (>99%) in green ash infested by the invasive emerald ash borer (EAB). However, high standing genetic variation may produce a few individuals capable of an effective defense, as seen in the rare surviving green ash. In an investigation of this plant-insect interaction, we annotated metabolites associated with generalized but ineffective responses to EAB, and others associated with successful defensive responses. Untargeted metabolomics combined with intensive phenotyping of structured populations provides a framework for understanding resistance to invasive species in naïve host populations.
Publisher
Cold Spring Harbor Laboratory
Reference57 articles.
1. Important Insect and Disease Threats to United States Tree Species and Geographic Patterns of Their Potential Impacts;Forests,2019
2. Challenges, tactics and integrated management of emerald ash borer in North America
3. K. S. Knight et al. (2012) Dynamics of surviving ash (Fraxinus spp.) populations in areas long infested by emerald ash borer (Agrilus planipennis). in Proceedings of the fourth international workshop on the genetics of host-parasite interactions in forestry: Disease and insect resistance in forest trees (Pacific Southwest Research Station, Forest Service, U.S. Department of Agriculture, Albany, CA), pp 143–152.
4. Intraspecific variation in Fraxinus pennsylvanica responses to emerald ash borer (Agrilus planipennis);New Forests,2015
5. C. F. Miniat et al., “Impacts of Invasive Species on Forest and Grassland Ecosystem Processes in the United States” in Invasive Species in Forests and Rangelands of the United States, T. M. Poland et al., Eds. (Springer International Publishing, Cham, 2021), pp. 41–55.