Diversity of cytosine methylation across the fungal tree of life

Bewick, Adam J.; Hofmeister, Brigitte T.; Powers, Rob A.; Mondo, Stephen J.; Grigoriev, Igor V.; James, Timothy Y.; Stajich, Jason E.; Schmitz, Robert J.

doi:10.1038/s41559-019-0810-9

Diversity of cytosine methylation across the fungal tree of life

Journal Article · Sun Feb 17 23:00:00 EST 2019 · Nature Ecology and Evolution

DOI:https://doi.org/10.1038/s41559-019-0810-9· OSTI ID:1619115

^[1]; Hofmeister, Brigitte T. ^[1]; Powers, Rob A. ^[2]; Mondo, Stephen J. ^[3]; ^[4]; James, Timothy Y. ^[2]; ^[5]; ^[1]

Univ. of Georgia, Athens, GA (United States)
Univ. of Michigan, Ann Arbor, MI (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
Univ. of California, Riverside, CA (United States)

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. Finally, 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.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Science Foundation (NSF); National Institutes of Health (NIH)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1619115

Journal Information:: Nature Ecology and Evolution, Journal Name: Nature Ecology and Evolution Journal Issue: 3 Vol. 3; ISSN 2397-334X

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Draft Genome Sequences of Human Pathogenic Fungus Geomyces pannorum Sensu Lato and Bat White Nose Syndrome Pathogen Geomyces (Pseudogymnoascus) destructans Chibucos, M. C.; Crabtree, J.; Nagaraj, S. Genome Announcements, Vol. 1, Issue 6 https://doi.org/10.1128/genomeA.01045-13	journal	October 2013
Assembly of a phased diploid Candida albicans genome facilitates allele-specific measurements and provides a simple model for repeat and indel structure Muzzey, Dale; Schwartz, Katja; Weissman, Jonathan S. Genome Biology, Vol. 14, Issue 9 https://doi.org/10.1186/gb-2013-14-9-r97	journal	January 2013
Characterization and functional analysis of phytoene synthase gene family in tobacco Wang, Zhaojun; Zhang, Lin; Dong, Chen BMC Plant Biology, Vol. 21, Issue 1 https://doi.org/10.1186/s12870-020-02816-3	journal	January 2021
Widespread natural variation of DNA methylation within angiosperms Niederhuth, Chad E.; Bewick, Adam J.; Ji, Lexiang Genome Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s13059-016-1059-0	journal	September 2016
BEAST 2: A Software Platform for Bayesian Evolutionary Analysis Bouckaert, Remco; Heled, Joseph; Kühnert, Denise PLoS Computational Biology, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pcbi.1003537	journal	April 2014
Deciphering the Cryptic Genome: Genome-wide Analyses of the Rice Pathogen Fusarium fujikuroi Reveal Complex Regulation of Secondary Metabolism and Novel Metabolites Wiemann, Philipp; Sieber, Christian M. K.; von Bargen, Katharina W. PLoS Pathogens, Vol. 9, Issue 6 https://doi.org/10.1371/journal.ppat.1003475	journal	June 2013
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Additional file 10 of The stem rust fungus Puccinia graminis f. sp. tritici induces centromeric small RNAs during late infection that are associated with genome-wide DNA methylation Sperschneider, Jana; Jones, Ashley W.; Nasim, Jamila figshare https://doi.org/10.6084/m9.figshare.16625228	dataset	January 2021
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Additional file 1 of The stem rust fungus Puccinia graminis f. sp. tritici induces centromeric small RNAs during late infection that are associated with genome-wide DNA methylation Sperschneider, Jana; Jones, Ashley W.; Nasim, Jamila figshare https://doi.org/10.6084/m9.figshare.16625246.v1	image	January 2021
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Additional file 4 of The stem rust fungus Puccinia graminis f. sp. tritici induces centromeric small RNAs during late infection that are associated with genome-wide DNA methylation Sperschneider, Jana; Jones, Ashley W.; Nasim, Jamila figshare https://doi.org/10.6084/m9.figshare.16625255	image	January 2021
Additional file 5 of The stem rust fungus Puccinia graminis f. sp. tritici induces centromeric small RNAs during late infection that are associated with genome-wide DNA methylation Sperschneider, Jana; Jones, Ashley W.; Nasim, Jamila figshare https://doi.org/10.6084/m9.figshare.16625258	dataset	January 2021
Additional file 6 of The stem rust fungus Puccinia graminis f. sp. tritici induces centromeric small RNAs during late infection that are associated with genome-wide DNA methylation Sperschneider, Jana; Jones, Ashley W.; Nasim, Jamila figshare https://doi.org/10.6084/m9.figshare.16625261	dataset	January 2021
Additional file 7 of The stem rust fungus Puccinia graminis f. sp. tritici induces centromeric small RNAs during late infection that are associated with genome-wide DNA methylation Sperschneider, Jana; Jones, Ashley W.; Nasim, Jamila figshare https://doi.org/10.6084/m9.figshare.16625264.v1	dataset	January 2021
Additional file 8 of The stem rust fungus Puccinia graminis f. sp. tritici induces centromeric small RNAs during late infection that are associated with genome-wide DNA methylation Sperschneider, Jana; Jones, Ashley W.; Nasim, Jamila figshare https://doi.org/10.6084/m9.figshare.16625267	dataset	January 2021
Additional file 9 of The stem rust fungus Puccinia graminis f. sp. tritici induces centromeric small RNAs during late infection that are associated with genome-wide DNA methylation Sperschneider, Jana; Jones, Ashley W.; Nasim, Jamila figshare https://doi.org/10.6084/m9.figshare.16625270.v1	dataset	January 2021
Comparative analysis of genome-wide DNA methylation in Neurospora Hosseini, Sara; Meunier, Cécile; Nguyen, Diem Epigenetics, Vol. 15, Issue 9 https://doi.org/10.1080/15592294.2020.1741758	journal	March 2020
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Widespread conservation and lineage-specific diversification of genome-wide DNA methylation patterns across arthropods Lewis, Samuel H.; Ross, Laura; Bain, Stevie A. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.54874	text	January 2020