Widespread adenine N6-methylation of active genes in fungi
Abstract
N6-methyldeoxyadenine (6mA) is a noncanonical DNA base modification present at low levels in plant and animal genomes1,2,3,4, but its prevalence and association with genome function in other eukaryotic lineages remains poorly understood. Here we report that abundant 6mA is associated with transcriptionally active genes in early-diverging fungal lineages5. Using single-molecule long-read sequencing of 16 diverse fungal genomes, we observed that up to 2.8% of all adenines were methylated in early-diverging fungi, far exceeding levels observed in other eukaryotes and more derived fungi. 6mA occurred symmetrically at ApT dinucleotides and was concentrated in dense methylated adenine clusters surrounding the transcriptional start sites of expressed genes; its distribution was inversely correlated with that of 5-methylcytosine. Our results show a striking contrast in the genomic distributions of 6mA and 5-methylcytosine and reinforce a distinct role for 6mA as a gene-expression-associated epigenomic mark in eukaryotes.
- Authors:
-
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- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Roche Sequencing Solutions Inc., Pleasanton, CA (United States)
- Univ. of Georgia, Athens, GA (United States). Dept. of Genetics
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); The Jackson Lab. for Genomic Medicine, Farmington, CT (United States)
- L. F. Lambert Spawn Co., Coatesville, PA (United States)
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Univ. of Michigan, Ann Arbor, MI (United States). Dept. of Ecology and Evolutionary Biology
- Univ. of California, Santa Barbara, CA (United States). Dept. of Chemical Engineering
- Univ. of California, Riverside, CA (United States). Dept. of Plant Pathology and Microbiology
- Oregon State Univ., Corvallis, OR (United States). Dept. of Botany and Plant Pathology
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Merced, CA (United States). School of Natural Sciences
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of California, Santa Barbara, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division; National Science Foundation (NSF); Pew Charitable Trusts
- OSTI Identifier:
- 1469129
- Alternate Identifier(s):
- OSTI ID: 1485164
- Grant/Contract Number:
- AC02-05CH11231; DEB-1441715; DEB-1441604; DEB-1354625; SC0010352; W911NF-09- 0001
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Genetics
- Additional Journal Information:
- Journal Volume: 49; Journal Issue: 6; Related Information: © 2017 Nature America, Inc., part of Springer Nature. All rights reserved.; Journal ID: ISSN 1061-4036
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Mondo, Stephen J., Dannebaum, Richard O., Kuo, Rita C., Louie, Katherine B., Bewick, Adam J., LaButti, Kurt, Haridas, Sajeet, Kuo, Alan, Salamov, Asaf, Ahrendt, Steven R., Lau, Rebecca, Bowen, Benjamin P., Lipzen, Anna, Sullivan, William, Andreopoulos, Bill B., Clum, Alicia, Lindquist, Erika, Daum, Christopher, Northen, Trent R., Kunde-Ramamoorthy, Govindarajan, Schmitz, Robert J., Gryganskyi, Andrii, Culley, David, Magnuson, Jon, James, Timothy Y., O'Malley, Michelle A., Stajich, Jason E., Spatafora, Joseph W., Visel, Axel, and Grigoriev, Igor V. Widespread adenine N6-methylation of active genes in fungi. United States: N. p., 2017.
Web. doi:10.1038/ng.3859.
Mondo, Stephen J., Dannebaum, Richard O., Kuo, Rita C., Louie, Katherine B., Bewick, Adam J., LaButti, Kurt, Haridas, Sajeet, Kuo, Alan, Salamov, Asaf, Ahrendt, Steven R., Lau, Rebecca, Bowen, Benjamin P., Lipzen, Anna, Sullivan, William, Andreopoulos, Bill B., Clum, Alicia, Lindquist, Erika, Daum, Christopher, Northen, Trent R., Kunde-Ramamoorthy, Govindarajan, Schmitz, Robert J., Gryganskyi, Andrii, Culley, David, Magnuson, Jon, James, Timothy Y., O'Malley, Michelle A., Stajich, Jason E., Spatafora, Joseph W., Visel, Axel, & Grigoriev, Igor V. Widespread adenine N6-methylation of active genes in fungi. United States. https://doi.org/10.1038/ng.3859
Mondo, Stephen J., Dannebaum, Richard O., Kuo, Rita C., Louie, Katherine B., Bewick, Adam J., LaButti, Kurt, Haridas, Sajeet, Kuo, Alan, Salamov, Asaf, Ahrendt, Steven R., Lau, Rebecca, Bowen, Benjamin P., Lipzen, Anna, Sullivan, William, Andreopoulos, Bill B., Clum, Alicia, Lindquist, Erika, Daum, Christopher, Northen, Trent R., Kunde-Ramamoorthy, Govindarajan, Schmitz, Robert J., Gryganskyi, Andrii, Culley, David, Magnuson, Jon, James, Timothy Y., O'Malley, Michelle A., Stajich, Jason E., Spatafora, Joseph W., Visel, Axel, and Grigoriev, Igor V. Mon .
"Widespread adenine N6-methylation of active genes in fungi". United States. https://doi.org/10.1038/ng.3859. https://www.osti.gov/servlets/purl/1469129.
@article{osti_1469129,
title = {Widespread adenine N6-methylation of active genes in fungi},
author = {Mondo, Stephen J. and Dannebaum, Richard O. and Kuo, Rita C. and Louie, Katherine B. and Bewick, Adam J. and LaButti, Kurt and Haridas, Sajeet and Kuo, Alan and Salamov, Asaf and Ahrendt, Steven R. and Lau, Rebecca and Bowen, Benjamin P. and Lipzen, Anna and Sullivan, William and Andreopoulos, Bill B. and Clum, Alicia and Lindquist, Erika and Daum, Christopher and Northen, Trent R. and Kunde-Ramamoorthy, Govindarajan and Schmitz, Robert J. and Gryganskyi, Andrii and Culley, David and Magnuson, Jon and James, Timothy Y. and O'Malley, Michelle A. and Stajich, Jason E. and Spatafora, Joseph W. and Visel, Axel and Grigoriev, Igor V.},
abstractNote = {N6-methyldeoxyadenine (6mA) is a noncanonical DNA base modification present at low levels in plant and animal genomes1,2,3,4, but its prevalence and association with genome function in other eukaryotic lineages remains poorly understood. Here we report that abundant 6mA is associated with transcriptionally active genes in early-diverging fungal lineages5. Using single-molecule long-read sequencing of 16 diverse fungal genomes, we observed that up to 2.8% of all adenines were methylated in early-diverging fungi, far exceeding levels observed in other eukaryotes and more derived fungi. 6mA occurred symmetrically at ApT dinucleotides and was concentrated in dense methylated adenine clusters surrounding the transcriptional start sites of expressed genes; its distribution was inversely correlated with that of 5-methylcytosine. Our results show a striking contrast in the genomic distributions of 6mA and 5-methylcytosine and reinforce a distinct role for 6mA as a gene-expression-associated epigenomic mark in eukaryotes.},
doi = {10.1038/ng.3859},
journal = {Nature Genetics},
number = 6,
volume = 49,
place = {United States},
year = {Mon May 08 00:00:00 EDT 2017},
month = {Mon May 08 00:00:00 EDT 2017}
}
Web of Science
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Distribution and Diversity of Cytochrome P450 Monooxygenases in the Fungal Class Tremellomycetes
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Epigenetic Methylations on N6-Adenine and N6-Adenosine with the same Input but Different Output
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Draft genome sequence of Annulohypoxylon stygium, Aspergillus mulundensis, Berkeleyomyces basicola (syn. Thielaviopsis basicola), Ceratocystis smalleyi, two Cercospora beticola strains, Coleophoma cylindrospora, Fusarium fracticaudum, Phialophora cf. hyalina, and Morchella septimelata
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Repeat elements organise 3D genome structure and mediate transcription in the filamentous fungus Epichloë festucae
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Early Diverging Insect-Pathogenic Fungi of the Order Entomophthorales Possess Diverse and Unique Subtilisin-Like Serine Proteases
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Adenine DNA methylation, 3D genome organization, and gene expression in the parasite Trichomonas vaginalis
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Enzymes of early-diverging, zoosporic fungi
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Structural insight into human N6amt1–Trm112 complex functioning as a protein methyltransferase
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Author Correction: Recurrent acquisition of cytosine methyltransferases into eukaryotic retrotransposons
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Diversity of cytosine methylation across the fungal tree of life
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Study of the whole genome, methylome and transcriptome of Cordyceps militaris
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Methylation content sensitive enzyme ddRAD (MCSeEd): a reference-free, whole genome profiling system to address cytosine/adenine methylation changes
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N6-adenine DNA methylation is associated with the linker DNA of H2A.Z-containing well-positioned nucleosomes in Pol II-transcribed genes in Tetrahymena
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N6-Methyladenosine in RNA and DNA: An Epitranscriptomic and Epigenetic Player Implicated in Determination of Stem Cell Fate
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Sources of artifact in measurements of 6mA and 4mC abundance in eukaryotic genomic DNA
journal, June 2019
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DNA N6-Methyladenosine modification role in transmitted variations from genomic DNA to RNA in Herrania umbratica
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Transcriptome analysis of Aspergillus niger xlnR and xkiA mutants grown on corn Stover and soybean hulls reveals a highly complex regulatory network
journal, November 2019
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Phytophthora methylomes are modulated by 6mA methyltransferases and associated with adaptive genome regions
journal, October 2018
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Genome expansion by allopolyploidization in the fungal strain Coniochaeta 2T2.1 and its exceptional lignocellulolytic machinery
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Hiding in plain sight: New virus genomes discovered via a systematic analysis of fungal public transcriptomes
journal, July 2019
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Early Diverging Insect-Pathogenic Fungi of the Order Entomophthorales Possess Diverse and Unique Subtilisin-Like Serine Proteases
journal, August 2018
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- G3: Genes|Genomes|Genetics, Vol. 8, Issue 10
iDNA-MS: An Integrated Computational Tool for Detecting DNA Modification Sites in Multiple Genomes
preprint, March 2020
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MASQC: Next Generation Sequencing Assists Third Generation Sequencing for Quality Control in N6-Methyladenine DNA Identification
journal, March 2020
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SMRT Sequencing Revealed Mitogenome Characteristics and Mitogenome-Wide DNA Modification Pattern in Ophiocordyceps sinensis
journal, July 2017
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Application of Transcriptomics to Compare the Carbohydrate Active Enzymes That Are Expressed by Diverse Genera of Anaerobic Fungi to Degrade Plant Cell Wall Carbohydrates
journal, July 2018
- Gruninger, Robert J.; Nguyen, Thi T. M.; Reid, Ian D.
- Frontiers in Microbiology, Vol. 9
Distribution and Diversity of Cytochrome P450 Monooxygenases in the Fungal Class Tremellomycetes
journal, June 2019
- Akapo, Olufunmilayo Olukemi; Padayachee, Tiara; Chen, Wanping
- International Journal of Molecular Sciences, Vol. 20, Issue 12
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