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
Forest Health & Biotic Interactions, Swiss Federal Institute for Forest, Snow and Landscape Research (WSL), 8903, Birmensdorf, Switzerland.
Institute of Terrestrial Ecosystems, ETH Zürich, 8092, Zurich, Switzerland.
New Phytol. 2023 Nov;240(3):1219-1232. doi: 10.1111/nph.19068. Epub 2023 Jun 21.
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.
植物依靠交叉抗性特征来抵御多种系统发育上不同的敌人。这些特征通常是长期共同进化历史的结果。生物入侵会迫使单纯的植物应对新出现的、同时存在的害虫和病原体。例如，欧洲白蜡树（Fraxinus excelsior）受到翡翠灰螟（EAB）、光肩星天牛（Agrilus planipennis，一种蛀木甲虫）和白蜡树枯梢病（ADB）病原体——白蜡 Hymenoscyphus fraxineus 的严重威胁。然而，针对新敌人的植物交叉抗性特征研究甚少，单纯的白蜡树是否能通过交叉抗性机制抵御新的敌人复合体尚不清楚。为了获得机理上的见解，我们量化了翡翠灰螟在对白蜡树枯梢病抗性不同的白蜡树基因型嫁接复制品上的表现，并通过靶向和非靶向代谢组学对白蜡树韧皮部化学特征进行了表征。翡翠灰螟在对白蜡树枯梢病敏感的基因型上的表现优于对白蜡树枯梢病抗性强的基因型。此外，翡翠灰螟表现的变化与对白蜡树枯梢病敏感和抗性强的基因型之间韧皮部化学特征的差异一致。我们表明，欧洲白蜡树韧皮部化学特征的种内变异可以增强对来自不同分类界的入侵拮抗剂的交叉抗性。我们的研究表明，推广对白蜡树枯梢病抗性强的白蜡树基因型可能同时有助于控制白蜡树枯梢病，并减少翡翠灰螟造成的白蜡树损失，这对于这种关键树种的长期稳定性可能至关重要。
