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ARS Home » Midwest Area » West Lafayette, Indiana » Crop Production and Pest Control Research » Research » Publications at this Location » Publication #365725

Research Project: Molecular Mechanisms of Host-Fungal Pathogen Interactions in Cereal Crops

Location: Crop Production and Pest Control Research

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

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

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.