The role of phenylpropanoids and the plant microbiome in defenses of ash trees against invasive emerald ash borer

Authors: ZHANG, BIN - Hubei University; KOSKI, TUULI - Hubei University; WANG, HUALING - Hebei Academy Of Agriculture & Forestry; CHEN, ZHENZHU - Hebei Academy Of Agriculture & Forestry; LI, HUIPING - Hebei Academy Of Agriculture & Forestry; MOGOUONG, JUDITH - Cornell University; Bushley, Kathryn; XING, LONSHEN - Hubei University; SUN, JINAGHUA - Hubei University

Submitted to: Plant Cell and Environment
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/25/2025
Publication Date: 4/15/2025
Citation: Zhang, B., Koski, T., Wang, H., Chen, Z., Li, H., Mogouong, J., Bushley, K.E., Xing, L., Sun, J. 2025. The role of phenylpropanoids and the plant microbiome in defenses of ash trees against invasive emerald ash borer. Plant Cell and Environment. https://doi.org/10.1111/pce.15534.
DOI: https://doi.org/10.1111/pce.15534

Interpretive Summary: Native to Asia, the emerald ash borer is an invasive insect in North America and Russia that now threatens Europe. Most ash trees in North America and Europe are more susceptible to infestation with emerald ash borer, while those in its native range in Asia are more resistant. The reason for differences in resistance is not fully understand but may be a result of both defenses compounds that are either always expressed (constitutive) and/or those that are only expressed in response to infestation with the insect. This study examined differences in the microbial community and the plant defense chemistry (metabolome) between a native Asian resistant ash (Manchurian ash) and a susceptible North American susceptible ash (Velvet ash) both uninfested and infested with emerald ash borer. Results showed that the phenylpropanoid biosynthetic pathway may be important to defense in both ash trees species but is more highly expressed in the native ash. Analysis of the microbiome also found differences between the native Asian and non-native North American ash tree species that may contribute to resistance.

Technical Abstract: • Plants have co-evolved with herbivorous insects for millions of years, resulting in variation in resistance both within and between species. However, the mechanism shaping this variance remains elusive. • Using a manipulative experiment combined with untargeted metabolomics, metagenomics and, transcriptomics approaches, we investigated the roles of plant metabolites and the microbiome in defense mechanisms in native resistant Manchurian ash (Fraxinus mandshurica) trees and non-native susceptible Velvet ash (Fraxinus velutina) trees against the highly invasive emerald ash borer (EAB, Agrilus planipennis) • Comparative transcriptomics and metabolomics analyses showed that the phenylpropanoid pathway may serve as a potential regulator of resistance, being expressed to a higher extent in native resistant trees compared to non-native susceptible trees. • Analysis of ash microbial communities suggested that some bacteria and fungi may contribute to differences in resistance between the two ash species. • This study significantly enhances our understanding of the variation in resistance between ash species and its contribution to the invasion success of EAB, providing valuable insights for the development of pest management strategies.