101 Dothideomycetes genomes: a test case for predicting lifestyles and emergence of pathogens

Authors: HARIDAS, SAJEET - Joint Genome Institute; ALBERT, RYAN - Joint Genome Institute; BINDER, MANDRED - Fungal Biodiversity; BLOEM, JANNEKE - Fungal Biodiversity; LABUTTI, KURT - Joint Genome Institute; SALAMOV, ASAF - Joint Genome Institute; ANDREOPOULOS, BILL - Joint Genome Institute; BAKER, SCOTT - Pacific Northwest National Laboratory; BARRY, KERRIE - Joint Genome Institute; BILLS, GERALD - University Of Texas; BLUHM, BURT - University Of Arkansas; CANNON, CHARLES - Texas Tech University; CASTANERA, RAUL - Joint Genome Institute; CULLEY, DAVID - Pacific Northwest National Laboratory; DAUM, CHRIS - Joint Genome Institute; EZRA, DAVID - Volcani Center (ARO); GONZALEZ, JONATHAN - Cornell University; HENRISSAT, BERNARD - Inland Northwest Research Alliance, Inra; INDERBITZIN, PATRIK - University Of California; KUO, ALAN - Joint Genome Institute; LIANG, CHEN - Qingdao Agricultural University; LIPZEN, ANNA - Joint Genome Institute; LUTZONI, FRANCOIS - Duke University; MAGNUSON, JON - Pacific Northwest National Laboratory; MONDO, STEPHEN - Joint Genome Institute; NOLAN, MATT - Joint Genome Institute; OHM, ROBIN - Joint Genome Institute; PANGILINAN, JASMYM - Joint Genome Institute; PARK, HEE-JIN - Cornell University; SANCHEZ, MANUEL ALFARO - Public University Of Navarra; RAMIREZ, LUCIA - Public University Of Navarra; SUN, HUI - Joint Genome Institute; TRITT, ANDREW - Joint Genome Institute; YOSHINAGA, YUKO - Joint Genome Institute; ZWIERS, LUTE-HARM - Fungal Biodiversity; TURGEON, B. GILLIAN - Cornell University; Goodwin, Stephen; SPATAFORA, JOSEPH - Oregon State University; CROUS, PEDRO - Fungal Biodiversity; GRIGORIEV, IGOR - Joint Genome Institute

Submitted to: Studies in Mycology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/22/2020
Publication Date: 3/17/2020
Publication URL: https://handle.nal.usda.gov/10113/6829815
Citation: Haridas, S., Albert, R., Binder, M., Bloem, J., Labutti, K., Salamov, A., Andreopoulos, B., Baker, S.E., Barry, K., Bills, G., Bluhm, B.H., Cannon, C., Castanera, R., Culley, D.E., Daum, C., Ezra, D., Gonzalez, J.B., Henrissat, B., Inderbitzin, P., Kuo, A., Liang, C., Lipzen, A., Lutzoni, F., Magnuson, J., Mondo, S., Nolan, M., Ohm, R., Pangilinan, J., Park, H., Sanchez, M., Ramirez, L., Sun, H., Tritt, A., Yoshinaga, Y., Zwiers, L., Turgeon, B., Goodwin, S.B., Spatafora, J.W., Crous, P., Grigoriev, I.V. 2020. 101 Dothideomycetes genomes: a test case for predicting lifestyles and emergence of pathogens. Studies in Mycology. 96:141-153. https://doi.org/10.1016/j.simyco.2020.01.003.
DOI: https://doi.org/10.1016/j.simyco.2020.01.003

Interpretive Summary: The Dothideomycetes contains more species with the largest variability of lifestyles than any other fungal class. Many species in this class are plant pathogens that cause diseases on virtually every major crop, whether for food, feed, fiber or feedstocks for bioenergy production. However, how and when the pathogens evolved and what makes one become a pathogen are unknown. To search for pathogen-specific gene clusters and to better predict lifestyle, 56 new genome sequences of Dothideomycetes were generated and added to 55 others for analysis of evolutionary relationships and ability to predict lifestyle. The results allowed genes associated with pathogenicity to be identified and provided an excellent means to predict the lifestyle of a fungus from the gene content of its genome sequence. These results will be of interest to fungal biologists studying fungal evolution, to plant pathologists trying to control plant diseases and to evolutionary biologists trying to understand how fungi adapt to new environments. Ability to predict lifestyle adaptation could be very useful for assessing the risk of disease development and for understanding the ability of fungi to adapt to new hosts, cause diseases and affect crop productivity in response to future climate change.

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.