Fungal community and metabolomic investigations reveal ash metabolites shaping phloem fungal communities in ash trees (Fraxinus spp.) resistant and susceptible against highly invasive emerald ash borer (Agrilus planipennis)

Authors: KOSHI, TUULI-MARJAANA - Chinese Academy Of Sciences; ZHANG, BIN - Hebei University; MOGOUONG, JUDITH - Cornell University; WANG, HUALING - Hebei University; CHEN, ZHENZHU - Hebei University; LI, HUIPING - Hebei University; Bushley, Kathryn; SUN, JIANGHUA - Hebei University

Submitted to: Plant Cell and Environment
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/29/2024
Publication Date: 6/27/2024
Citation: Koshi, T., Zhang, B., Mogouong, J., Wang, H., Chen, Z., Li, H., Bushley, K.E., Sun, J. 2024. Fungal community and metabolomic investigations reveal ash metabolites shaping phloem fungal communities in ash trees (Fraxinus spp.) resistant and susceptible against highly invasive emerald ash borer (Agrilus planipennis). Plant Cell and Environment. 1-19. https://doi.org/10.1111/pce.14996.
DOI: https://doi.org/10.1111/pce.14996

Interpretive Summary: Emerald ash borer (EAB, Agrilus planipennis), a beetle native to Asia, has become an invasive killer of ash trees (Fraxinus spp.) in North America. It has already caused millions of dollars in damage and continues to spread to new areas in the U.S. as most management strategies have had limited efficacy. Very little is known about microbial associates of ash or emerald ash borer or resistance mechanisms of ash trees. In this research, we compared the microbial communities and metabolites between a resistant native Asian (Chinese) and a susceptible North American (Velvet) ash species both in healthy trees and in reponse to emerald ash borer infestation. We disccovered 7 compounds found in ash trees that were strongly influencing the microbial communities. One flavonol compounds strongly influenced the microbial communities and is potentially involved in natural resistance of Chinese ash to this invasive beetle. Two coumarin compounds previously implicated in defense (fraxetin and fraxin) were instead found to be associated with microbial communities in susceptible velvet ash and to decrease in abundance in response to beetle infestation, suggesting it is unlikely they play a role in resistance. Our findings identify both microbes and ash metabolites that may confer resistance to emerald ash borer and could be manipulated or applied to ash trees to manage this pest.

Technical Abstract: Emerald ash borer (EAB, Agrilus planipennis), a beetle native to Asia, has become an invasive killer of ash trees (Fraxinus spp.) in North America and parts of Europe. We preformed the first comparison of phloem mycobiota and metabolomics between a resistant ash species native to Asia and a susceptible ash species native to North America in the context of the larval mycobiota. Phloem alpha diversity in resistant trees appeared more stable and robust EAB-mediated changes compared to susceptible trees, whereas phloem fungal communities (beta diversity) in both tree species were unaffected by EAB infestation. Mycobiota in the larval gut was affected by the host tree species, and several indicator taxa detected in the larval gut shared high relative abundance with the phloem of resistant tree. Despite generally similar metabolomic responses to EAB infestation, resistant and susceptible trees differed in relative abundance patterns of several compounds due to EAB infestation. Among them, a flavonol (Chrysoeriol-7-O-glucoside) was found to be the major driver of the fungal community in resistant trees, including those taxa that were shared with the larval gut. As the relative abundance of Chrysoeriol-7-O-glucoside remained high in resistant trees regardless of infestation status, it may be involved in constitutive resistance. Two coumarins, fraxetin and fraxin, strongly affected the fungal communities in susceptible trees, and their relative abundance decreased in susceptible trees to similar level as in resistant trees in response to EAB infestation. We also identified a number of fungal taxa whose potential roles in ash defence against EAB and fungal pathogens warrant further investigation.