Widespread adenine N6-methylation of active genes in fungi

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.

doi:10.1038/ng.3859

Title: Widespread adenine N6-methylation of active genes in fungi

Journal Article · 08 May 2017 · Nature Genetics

DOI: https://doi.org/10.1038/ng.3859 · OSTI ID:1469129

Mondo, Stephen J. ^[1]; Dannebaum, Richard O. ^[2]; Kuo, Rita C. ^[1]; Louie, Katherine B. ^[1]; Bewick, Adam J. ^[3]; LaButti, Kurt ^[1]; Haridas, Sajeet ^[1]; Kuo, Alan ^[1]; Salamov, Asaf ^[1]; Ahrendt, Steven R. ^[4]; Lau, Rebecca ^[1]; Bowen, Benjamin P. ^[1]; Lipzen, Anna ^[1]; Sullivan, William ^[1]; Andreopoulos, Bill B. ^[1]; Clum, Alicia ^[1]; Lindquist, Erika ^[1]; Daum, Christopher ^[1]; Northen, Trent R. ^[1]; Kunde-Ramamoorthy, Govindarajan ^[5] more »

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

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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of California, Santa Barbara, CA (United States)

Sponsoring Organization:: 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

Grant/Contract Number:: AC02-05CH11231; DEB-1441715; DEB-1441604; DEB-1354625; SC0010352; W911NF-09- 0001

OSTI ID:: 1469129

Alternate ID(s):: OSTI ID: 1485164

Journal Information:: Nature Genetics, Vol. 49, Issue 6; Related Information: © 2017 Nature America, Inc., part of Springer Nature. All rights reserved.; ISSN 1061-4036

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 205 works

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Genome-scale data resolve ancestral rock-inhabiting lifestyle in Dothideomycetes (Ascomycota) Ametrano, Claudio G.; Grewe, Felix; Crous, Pedro W. IMA Fungus, Vol. 10, Issue 1 https://doi.org/10.1186/s43008-019-0018-2	journal	October 2019
Hiding in plain sight: New virus genomes discovered via a systematic analysis of fungal public transcriptomes Gilbert, Kerrigan B.; Holcomb, Emily E.; Allscheid, Robyn L. PLOS ONE, Vol. 14, Issue 7 https://doi.org/10.1371/journal.pone.0219207	journal	July 2019
iDNA6mA-Rice: A Computational Tool for Detecting N6-Methyladenine Sites in Rice Lv, Hao; Dao, Fu-Ying; Guan, Zheng-Xing Frontiers in Genetics, Vol. 10 https://doi.org/10.3389/fgene.2019.00793	journal	September 2019
SMRT Sequencing Revealed Mitogenome Characteristics and Mitogenome-Wide DNA Modification Pattern in Ophiocordyceps sinensis Kang, Xincong; Hu, Liqin; Shen, Pengyuan Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01422	journal	July 2017
PCR and Omics Based Techniques to Study the Diversity, Ecology and Biology of Anaerobic Fungi: Insights, Challenges and Opportunities Edwards, Joan E.; Forster, Robert J.; Callaghan, Tony M. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01657	journal	September 2017
Application of Transcriptomics to Compare the Carbohydrate Active Enzymes That Are Expressed by Diverse Genera of Anaerobic Fungi to Degrade Plant Cell Wall Carbohydrates Gruninger, Robert J.; Nguyen, Thi T. M.; Reid, Ian D. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01581	journal	July 2018
Distribution and Diversity of Cytochrome P450 Monooxygenases in the Fungal Class Tremellomycetes Akapo, Olufunmilayo Olukemi; Padayachee, Tiara; Chen, Wanping International Journal of Molecular Sciences, Vol. 20, Issue 12 https://doi.org/10.3390/ijms20122889	journal	June 2019
Epigenetic Methylations on N6-Adenine and N6-Adenosine with the same Input but Different Output Li, Zhiqing; Zhao, Ping; Xia, Qingyou International Journal of Molecular Sciences, Vol. 20, Issue 12 https://doi.org/10.3390/ijms20122931	journal	June 2019
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 Wingfield, Brenda D.; Bills, Gerald F.; Dong, Yang IMA Fungus, Vol. 9, Issue 1 https://doi.org/10.5598/imafungus.2018.09.01.13	journal	June 2018
Repeat elements organise 3D genome structure and mediate transcription in the filamentous fungus Epichloë festucae Winter, David J.; Ganley, Austen R. D.; Young, Carolyn A. PLOS Genetics, Vol. 14, Issue 10 https://doi.org/10.1371/journal.pgen.1007467	journal	October 2018
Early Diverging Insect-Pathogenic Fungi of the Order Entomophthorales Possess Diverse and Unique Subtilisin-Like Serine Proteases Arnesen, Jonathan A.; Małagocka, Joanna; Gryganskyi, Andrii G3: Genes\|Genomes\|Genetics, Vol. 8, Issue 10 https://doi.org/10.1534/g3.118.200656	journal	August 2018
Characteristics and homogeneity of N6-methylation in human genomes. Pacini, Clare E.; Bradshaw, Charles; Garrett, Nigel Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.37741	text	January 2019
Adenine DNA methylation, 3D genome organization, and gene expression in the parasite Trichomonas vaginalis Lizarraga, Ayelen; O’Brown, Zach Klapholz; Boulias, Konstantinos Proceedings of the National Academy of Sciences, Vol. 117, Issue 23 https://doi.org/10.1073/pnas.1917286117	journal	May 2020
Enzymes of early-diverging, zoosporic fungi Lange, Lene; Barrett, Kristian; Pilgaard, Bo Applied Microbiology and Biotechnology, Vol. 103, Issue 17 https://doi.org/10.1007/s00253-019-09983-w	journal	July 2019
Structural insight into human N6amt1–Trm112 complex functioning as a protein methyltransferase Li, Wenjing; Shi, Yu; Zhang, Tianlong Cell Discovery, Vol. 5, Issue 1 https://doi.org/10.1038/s41421-019-0121-y	journal	September 2019
Author Correction: Recurrent acquisition of cytosine methyltransferases into eukaryotic retrotransposons de Mendoza, Alex; Bonnet, Amandine; Vargas-Landin, Dulce B. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-04260-2	journal	May 2018
Diversity of cytosine methylation across the fungal tree of life Bewick, Adam J.; Hofmeister, Brigitte T.; Powers, Rob A. Nature Ecology & Evolution, Vol. 3, Issue 3 https://doi.org/10.1038/s41559-019-0810-9	journal	February 2019
Study of the whole genome, methylome and transcriptome of Cordyceps militaris Chen, Yujiao; Wu, Yuqian; Liu, Li Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-018-38021-4	journal	January 2019
Methylation content sensitive enzyme ddRAD (MCSeEd): a reference-free, whole genome profiling system to address cytosine/adenine methylation changes Marconi, Gianpiero; Capomaccio, Stefano; Comino, Cinzia Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-51423-2	journal	October 2019
N6-adenine DNA methylation is associated with the linker DNA of H2A.Z-containing well-positioned nucleosomes in Pol II-transcribed genes in Tetrahymena Wang, Yuanyuan; Chen, Xiao; Sheng, Yalan Nucleic Acids Research, Vol. 45, Issue 20 https://doi.org/10.1093/nar/gkx883	journal	October 2017
N6-Methyladenosine in RNA and DNA: An Epitranscriptomic and Epigenetic Player Implicated in Determination of Stem Cell Fate Ji, Pengfei; Wang, Xia; Xie, Nina Stem Cells International, Vol. 2018 https://doi.org/10.1155/2018/3256524	journal	October 2018
Sources of artifact in measurements of 6mA and 4mC abundance in eukaryotic genomic DNA O’Brown, Zach K.; Boulias, Konstantinos; Wang, Jie BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-5754-6	journal	June 2019
DNA N6-Methyladenosine modification role in transmitted variations from genomic DNA to RNA in Herrania umbratica Luan, Mei-Wei; Chen, Wei; Xing, Jian-Feng BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-5776-0	journal	June 2019
Transcriptome analysis of Aspergillus niger xlnR and xkiA mutants grown on corn Stover and soybean hulls reveals a highly complex regulatory network Khosravi, Claire; Kowalczyk, Joanna E.; Chroumpi, Tania BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-6235-7	journal	November 2019
Phytophthora methylomes are modulated by 6mA methyltransferases and associated with adaptive genome regions Chen, Han; Shu, Haidong; Wang, Liyuan Genome Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s13059-018-1564-4	journal	October 2018
Genome expansion by allopolyploidization in the fungal strain Coniochaeta 2T2.1 and its exceptional lignocellulolytic machinery Mondo, Stephen J.; Jiménez, Diego Javier; Hector, Ronald E. Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1569-6	journal	September 2019
Hiding in plain sight: New virus genomes discovered via a systematic analysis of fungal public transcriptomes Gilbert, Kerrigan B.; Holcomb, Emily E.; Allscheid, Robyn L. PLOS ONE, Vol. 14, Issue 7 https://doi.org/10.1371/journal.pone.0219207	journal	July 2019
Early Diverging Insect-Pathogenic Fungi of the Order Entomophthorales Possess Diverse and Unique Subtilisin-Like Serine Proteases Arnesen, Jonathan A.; Małagocka, Joanna; Gryganskyi, Andrii G3: Genes\|Genomes\|Genetics, Vol. 8, Issue 10 https://doi.org/10.1534/g3.118.200656	journal	August 2018
iDNA-MS: An Integrated Computational Tool for Detecting DNA Modification Sites in Multiple Genomes Lv, Hao; Dao, Fu-Ying; Zhang, Dan https://doi.org/10.2139/ssrn.3543840	preprint	March 2020
MASQC: Next Generation Sequencing Assists Third Generation Sequencing for Quality Control in N6-Methyladenine DNA Identification Yang, Siqian; Wang, Yaoxin; Chen, Ying Frontiers in Genetics, Vol. 11 https://doi.org/10.3389/fgene.2020.00269	journal	March 2020
SMRT Sequencing Revealed Mitogenome Characteristics and Mitogenome-Wide DNA Modification Pattern in Ophiocordyceps sinensis Kang, Xincong; Hu, Liqin; Shen, Pengyuan Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01422	journal	July 2017
Application of Transcriptomics to Compare the Carbohydrate Active Enzymes That Are Expressed by Diverse Genera of Anaerobic Fungi to Degrade Plant Cell Wall Carbohydrates Gruninger, Robert J.; Nguyen, Thi T. M.; Reid, Ian D. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01581	journal	July 2018
Distribution and Diversity of Cytochrome P450 Monooxygenases in the Fungal Class Tremellomycetes Akapo, Olufunmilayo Olukemi; Padayachee, Tiara; Chen, Wanping International Journal of Molecular Sciences, Vol. 20, Issue 12 https://doi.org/10.3390/ijms20122889	journal	June 2019