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

S Haridas; R Albert; M Binder; J Bloem; K LaButti; A Salamov; B Andreopoulos; S E Baker; K Barry; G Bills; B H Bluhm; C Cannon; R Castanera; D E Culley; C Daum; D Ezra; J B González; B Henrissat; A Kuo; C Liang; A Lipzen; F Lutzoni; J Magnuson; S J Mondo; M Nolan; R A Ohm; J Pangilinan; H-J Park; L Ramírez; M Alfaro; H Sun; A Tritt; Y Yoshinaga; L-H Zwiers; B G Turgeon; S B Goodwin; J W Spatafora; P W Crous; I V Grigoriev

doi:10.1016/j.simyco.2020.01.003

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

Stud Mycol. 2020 Feb 1:96:141-153. doi: 10.1016/j.simyco.2020.01.003. eCollection 2020 Jun.

Authors

S Haridas¹, R Albert^{1

2}, M Binder³, J Bloem³, K LaButti¹, A Salamov¹, B Andreopoulos¹, S E Baker⁴, K Barry¹, G Bills⁵, B H Bluhm⁶, C Cannon⁷, R Castanera^{1

8}, D E Culley⁴, C Daum¹, D Ezra⁹, J B González¹⁰, B Henrissat^{11

12

13}, A Kuo¹, C Liang¹⁴, A Lipzen¹, F Lutzoni¹⁵, J Magnuson⁴, S J Mondo^{1

16}, M Nolan¹, R A Ohm^{1

17}, J Pangilinan¹, H-J Park¹⁰, L Ramírez⁸, M Alfaro⁸, H Sun¹, A Tritt¹, Y Yoshinaga¹, L-H Zwiers³, B G Turgeon¹⁰, S B Goodwin¹⁸, J W Spatafora¹⁹, P W Crous^{3

17}, I V Grigoriev^{1

2}

Affiliations

¹ US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
² Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA, USA.
³ Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands.
⁴ Functional and Systems Biology Group, Environmental Molecular Sciences Division, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington, USA.
⁵ University of Texas Health Science Center, Houston, TX, USA.
⁶ University of Arkansas, Fayelletville, AR, USA.
⁷ Texas Tech University, Lubbock, TX, USA.
⁸ Institute for Multidisciplinary Research in Applied Biology (IMAB-UPNA), Universidad Pública de Navarra, Pamplona, Navarra, Spain.
⁹ Agricultural Research Organization, Volcani Center, Rishon LeTsiyon, Israel.
¹⁰ Section of Plant Pathology and Plant-Microbe Biology, School of Integrative Plant Science, Cornell University, Ithaca, NY, USA.
¹¹ CNRS, Aix-Marseille Université, Marseille, France.
¹² INRA, Marseille, France.
¹³ Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia.
¹⁴ College of Agronomy and Plant Protection, Qingdao Agricultural University, China.
¹⁵ Department of Biology, Duke University, Durham, NC, USA.
¹⁶ Bioagricultural Science and Pest Management Department, Colorado State University, Fort Collins, CO, USA.
¹⁷ Microbiology, Department of Biology, Faculty of Science, Utrecht University, Utrecht, The Netherlands.
¹⁸ U.S. Department of Agriculture-Agricultural Research Service, 915 W. State Street, West Lafayette, IN, USA.
¹⁹ Department of Botany & Plant Pathology, Oregon State University, Oregon State University, Corvallis, OR, USA.

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 of 101 Dothideomycetes introducing 55 newly sequenced species. The availability of whole-genome data produced a high-confidence phylogeny leading to reclassification of 25 organisms, provided a clearer picture of the relationships among the various families, and indicated that 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 classified fungi into lifestyle classes with >95 % accuracy and identified a small number of gene families that positively correlated with these distinctions. This can become a valuable tool for genome-based prediction of species lifestyle, especially for rarely seen and poorly studied species.

Keywords: Aulographales Crous, Spatafora, Haridas & Grigoriev; Coniosporiaceae Crous, Spatafora, Haridas & Grigoriev; Coniosporiales Crous, Spatafora, Haridas & Grigoriev; Eremomycetales Crous, Spatafora, Haridas & Grigoriev; Fungal evolution; Genome-based prediction; Lineolataceae Crous, Spatafora, Haridas & Grigoriev; Lineolatales Crous, Spatafora, Haridas & Grigoriev; Machine-learning; New taxa; Rhizodiscinaceae Crous, Spatafora, Haridas & Grigoriev.