Forest health in the Anthropocene: the emergence of a novel tree disease is associated with poplar cultivation

Authors: FEAU, NICOLAS - UNIVERSITY OF BRITISH COLUMBIA; DHILLON, BRAHAM - UNIVERSITY OF BRITISH COLUMBIA; SAKALIDIS, MONIQUE - UNIVERSITY OF BRITISH COLUMBIA; DALE, ANGELA - UNIVERSITY OF BRITISH COLUMBIA; SØNDRELI, KELSEY - OREGON STATE UNIVERSITY; Goodwin, Stephen - Steve; LEBOLDUS, JARED - OREGON STATE UNIVERSITY; HAMELIN, RICHARD - UNIVERSITY OF BRITISH COLUMBIA

Submitted to: Royal Society Open Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/11/2022
Publication Date: 2/6/2023
Citation: Feau, N., Dhillon, B.D., Sakalidis, M., Dale, A.L., Søndreli, K.L., Goodwin, S.B., LeBoldus, J.M., Hamelin, R.C. 2023. Forest health in the Anthropocene: The emergence of a novel tree disease is associated with poplar cultivation. Philosophical Transactions of the Royal Society B. 378: 20220008. https://doi.org/10.1098/rstb.2022.0008.
DOI: https://doi.org/10.6084/m9.figshare.c.6370565

Interpretive Summary: The acquisition of genes from other species is an important evolutionary mechanism that can drive host shifts in plant pathogens, resulting in the emergence of new diseases. To test whether a new canker disease resulted from a host shift, samples of the causal fungal pathogens were collected from balsam poplars in Alberta, Canada, and from eastern cottonwoods in the eastern US. Analysis of multiple genome sequences from each location revealed that the new disease on balsam poplar resulted from a hybridization event between two isolates that occurred fewer than 100,000 years ago. Occasional recurring hybridization resulted in transfer and loss of genes involved in pathogenicity, facilitating adaptation and a shift to the new host. The specialization of this emerging hybrid lineage to its new host coupled with clonal propagation represent a serious threat to poplar production that could impact both natural and planted forests. This information will be useful to evolutionary biologists analyzing the origins of new diseases, and to plant pathologists and foresters as they try to limit losses caused by this recently emerged pathogen.

Technical Abstract: Dothideomycetes is the largest class of kingdom Fungi and comprises an incredible diversity of lifestyles, many of which have evolved multiple times. Plant pathogens represent a major ecological niche of the class Dothideomycetes and they are known to infect most major food crops and feedstocks for biomass and biofuel production. Studying the ecology and evolution of Dothideomycetes has significant implications for our fundamental understanding of fungal evolution, their adaptation to stress and host specificity, and practical implications with regard to the effects of climate change and on the food, feed, and livestock elements of the agro-economy. In this study, we present the first large-scale, whole-genome comparison that introduces 56 newly sequenced Dothideomycetes genomes. The availability of whole-genome data produces a high-confidence phylogeny leading to reclassification of 27 organisms, provided a clearer picture of the relationships among the various families and indicated that plant pathogenicity evolved multiple times within this class. We also identified gene family expansions and contractions across the Dothideomycetes phylogeny linked to ecological niches providing insights into genome evolution and adaptation across this group. Using machine-learning methods we accurately classify fungi into lifestyle classes and identify a small number of gene families that positively correlate with these distinctions. This can become a valuable tool for genome-based prediction of species lifestyle, especially for rarely seen and poorly studied species.