Abstract

The generation of thousands of fungal genomes is leading to a better understanding of genes and genomic organization within the kingdom. However, the epigenome, which includes DNA and chromatin modifications, remains poorly investigated in fungi. Large comparative studies in animals and plants have deepened our understanding of epigenomic variation, particularly of the modified base 5-methylcytosine (5mC), but taxonomic sampling of disparate groups is needed to develop unifying explanations for 5mC variation. Here, we utilize the largest phylogenetic resolution of 5mC methyltransferases (5mC MTases) and genome evolution to better understand levels and patterns of 5mC across fungi. We show that extant 5mC MTase genotypes are descendent from ancestral maintenance and de novo genotypes, whereas the 5mC MTases DIM-2 and RID are more recently derived, and that 5mC levels are correlated with 5mC MTase genotype and transposon content. Our survey also revealed that fungi lack canonical gene-body methylation, which distinguishes fungal epigenomes from certain insect and plant species. However, some fungal species possess independently derived clusters of contiguous 5mC encompassing many genes. In some cases, DNA repair pathways and the N6-methyladenine DNA modification negatively coevolved with 5mC pathways, which additionally contributed to interspecific epigenomic variation across fungi.

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Data availability

Genome assemblies and gene annotations are available via the URL links listed in Supplementary Table 2. Gene Expression Omnibus and SRA accessions for RNA-Seq and WGBS data generated and used in this study are provided in the Methods.

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Acknowledgements

We thank E. Demers for DNA from Candida albicans, Clavispora lusitaniae and Candida auris, T. Giraud for DNA from M. lychnidis-dioicae A1, A. Idnurm for DNA from S. roseus, and N. Ponts for DNA from A. bisporus, B. cinerea, Fusarium fujikuroi, L. maculans ‘brassicae’ and P. anserina. We also thank M. Perlin for DNA from M. lychnidis-dioicae. We thank N. Rohr and T. Ethridge for WGBS library preparation for all species sequenced in this study except C. cinerea, H. irregulare and W. cocos. We thank D. Carter-House and J. Ortanez for DNA preparation of Zygomycetes Coemansia spiralis, Hesseltinella vesiculosa, Kirkomyces cordense, Lobosporangium transversale, Parasitella parasitica, P. blakesleeanus, R. spectabilis, S. fusiger and Syncephalis fuscata. We thank N. Morffy and Z. Lewis for useful feedback during manuscript preparation. We thank the following collaborators for the use of unpublished genic data: C. Aime, A. Andrianopoulos, D. Armaleo, G. Bills, G. Bonito, S. Branco, T. Bruns, K. Bushley, Y. Chang, I.-G. Choi, A. Churchill, L. Corrochano, C. Cuomo, A. Desirò, P. Dyer, J. Franciso, R. Gazis, J. Gladden, S. Goodwin, A. Gryganskyi, D. Hibbett, D. Johnson, A. Kohler, B. Lindahl, F. Lutzoni, J. Magnuson, J. Maria Barrasa, F. Martin, M. Milgroom, L. Nagy, W. Nierman, M. Nowrousian, D. Nuss, K. O’Donnell, R. Ohm, C. Pires, B. Schwessinger, S. Singer, B. Slippers, J. Spatafora, J. Taylor, A. Tsang, S. Unruh, K. Wolfe and L. Zettler. We also thank the Georgia Advanced Computing Resource Center and Georgia Genomics and Bioinformatics Core at the University of Georgia for sequencing and computational resources, respectively. This work was supported by the Office of the Vice President for Research at the University of Georgia (to R.J.S.) and US National Science Foundation grant DEB 1441715 (to J.E.S.). R.J.S. is a Pew Scholar in the Biomedical Sciences, supported by The Pew Charitable Trusts. Computational analysis on the University of California, Riverside High-Performance Computing Center cluster were supported by grants from the National Science Foundation (DBI-1429826) and National Institutes of Health (S10-OD016290). The work conducted by the US Department of Energy Joint Genome Institute—a DOE Office of Science User Facility—is supported by the Office of Science of the US Department of Energy under contract number DE-AC02-05CH11231.

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Affiliations

  1. Department of Genetics, University of Georgia, Athens, GA, USA

    • Adam J. Bewick
    •  & Robert J. Schmitz
  2. Institute of Bioinformatics, University of Georgia, Athens, GA, USA

    • Brigitte T. Hofmeister
  3. Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, USA

    • Rob A. Powers
    •  & Timothy Y. James
  4. US Department of Energy Joint Genome Institute, Walnut Creek, Berkeley, CA, USA

    • Stephen J. Mondo
    •  & Igor V. Grigoriev
  5. Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA, USA

    • Igor V. Grigoriev
  6. Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA, USA

    • Jason E. Stajich

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Contributions

A.J.B., R.J.S. and J.E.S. designed the study. WGBS data were generated by R.J.S. A.J.B. analysed the data under the supervision of R.J.S. and J.E.S. B.T.H. built JBrowse genome browsers for all of the species used in the study. T.Y.J. and R.P. contributed WGBS data. S.J.M. and I.V.G. contributed genomic data.

Competing interests

The authors declare no competing interests.

Corresponding authors

Correspondence to Adam J. Bewick or Robert J. Schmitz.

Supplementary information

  1. Supplementary Information

    Supplementary Figs. 1–16

  2. Reporting Summary

  3. Supplementary Table 1

    5mC DNA MTase and the tRNA methyltransferase DNMT2 annotations for 528 fungal species investigated in this study.

  4. Supplementary Table 2

    WGBS and mapping statistics for 40 fungal species investigated in this study.

  5. Supplementary Table 3

    Number of species per phylum for each observed 5mC MTase genotype.

  6. Supplementary Table 4

    5mC DNA MTase and the tRNA methyltransferase DNMT2 annotations for a subset of Animalia, Chlorophyta, Fungi, and Prokaryota. Protein models correspond to those used in Supplementary Fig. 2.

  7. Supplementary Table 5

    Number of CG-, CH-, and CN-enriched genes across fungal species investigated.

  8. Supplementary Table 6

    ALKBH annotations for Chordata, Fungi, and Nematoda investigated in this study. Protein models correspond to those used in Supplementary Fig. 15.

  9. Supplementary Table 7

    Results from Pagel’s test for correlated evolution.

  10. Supplementary Table 8

    Results from phylogenetic generalized least squares (PGLS).

  11. Supplementary Table 9

    Annotated proteins from fungal species containing the N-6 DNA Methylase domain (PF02384) as identified by Interproscan v5.23-62.0.

  12. Supplementary Table 10

    METTL annotations for fungal species investigated in this study. Protein models correspond to those used in Supplementary Fig. 16.

  13. Supplementary Table 11

    Annotated proteins for fungal species containing the domain the methyltransferase small domain (N6AMT1 proteins) as identified by Interproscan v5.23-62.0.

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https://doi.org/10.1038/s41559-019-0810-9