A glimmer of hope – ash genotypes with increased resistance to ash dieback pathogen show cross‐resistance to emerald ash borer

• Published in: The New phytologist Vol. 240; no. 3; pp. 1219 - 1232
• Main Authors: Gossner, Martin M., Perret‐Gentil, Anouchka, Britt, Elisabeth, Queloz, Valentin, Glauser, Gaétan, Ladd, Tim, Roe, Amanda D., Cleary, Michelle, Liziniewicz, Mateusz, Nielsen, Lene R., Ghosh, Soumya K., Bonello, Pierluigi, Eisenring, Michael
• Format: Journal Article
• Language: English
• Published: England Wiley Subscription Services, Inc 01-11-2023
• Subjects: Agrilus planipennis; ash dieback; Biological invasions; Botanik; Botany; cross‐resistance; defense chemistry; Dieback; emerald ash borer; Fraxinus; Fraxinus excelsior; Genetics and Breeding; Genetik och förädling; Genotypes; Hardwoods; intraspecific variation; Invasive insects; invasive species; Keystone species; Metabolomics; Pathogens; Pest resistance; Pests; Phloem; Phylogeny; Plant species; Resistance mechanisms; metabolomics; intraspecific variation; cross-resistance; ash dieback; Fraxinus; emerald ash borer; invasive species; defense chemistry
• ISSN: 0028-646X; 1469-8137; 1469-8137
• DOI: 10.1111/nph.19068

Summary
Plants rely on cross‐resistance traits to defend against multiple, phylogenetically distinct enemies. These traits are often the result of long co‐evolutionary histories. Biological invasions can force naïve plants to cope with novel, coincident pests, and pathogens. For example, European ash (Fraxinus excelsior) is substantially threatened by the emerald ash borer (EAB), Agrilus planipennis, a wood‐boring beetle, and the ash dieback (ADB) pathogen, Hymenoscyphus fraxineus. Yet, plant cross‐resistance traits against novel enemies are poorly explored and it is unknown whether naïve ash trees can defend against novel enemy complexes via cross‐resistance mechanisms.
To gain mechanistic insights, we quantified EAB performance on grafted replicates of ash genotypes varying in ADB resistance and characterized ash phloem chemistry with targeted and untargeted metabolomics.
Emerald ash borer performed better on ADB‐susceptible than on ADB‐resistant genotypes. Moreover, changes in EAB performance aligned with differences in phloem chemical profiles between ADB‐susceptible and ADB‐resistant genotypes.
We show that intraspecific variation in phloem chemistry in European ash can confer increased cross‐resistance to invasive antagonists from different taxonomic kingdoms. Our study suggests that promotion of ADB‐resistant ash genotypes may simultaneously help to control the ADB disease and reduce EAB‐caused ash losses, which may be critical for the long‐term stability of this keystone tree species.
See also the Commentary on this article by Johnson & Whitehill, 240: 912–914.