Identification of factors required for m6 A mRNA methylation in Arabidopsis reveals a role for the conserved E3 ubiquitin ligase HAKAI
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
323052
European Research Council - International
BB/C513369/1
Biotechnology and Biological Sciences Research Council - United Kingdom
PubMed
28503769
PubMed Central
PMC5488176
DOI
10.1111/nph.14586
Knihovny.cz E-zdroje
- Klíčová slova
- Arabidopsis, HAKAI, N6-adenosine methylation (m6A), VIRILIZER, mRNA methylation, protoxylem,
- MeSH
- adenosin metabolismus MeSH
- Arabidopsis metabolismus MeSH
- geneticky modifikované rostliny metabolismus MeSH
- konzervovaná sekvence MeSH
- messenger RNA metabolismus MeSH
- methyltransferasy genetika metabolismus fyziologie MeSH
- metylace MeSH
- proteiny huseníčku genetika metabolismus fyziologie MeSH
- sekvenční seřazení MeSH
- ubikvitinligasy genetika metabolismus fyziologie MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- 6-methyladenine mRNA methyltransferase MeSH Prohlížeč
- adenosin MeSH
- messenger RNA MeSH
- methyltransferasy MeSH
- proteiny huseníčku MeSH
- ubikvitinligasy MeSH
N6-adenosine methylation (m6 A) of mRNA is an essential process in most eukaryotes, but its role and the status of factors accompanying this modification are still poorly understood. Using combined methods of genetics, proteomics and RNA biochemistry, we identified a core set of mRNA m6 A writer proteins in Arabidopsis thaliana. The components required for m6 A in Arabidopsis included MTA, MTB, FIP37, VIRILIZER and the E3 ubiquitin ligase HAKAI. Downregulation of these proteins led to reduced relative m6 A levels and shared pleiotropic phenotypes, which included aberrant vascular formation in the root, indicating that correct m6 A methylation plays a role in developmental decisions during pattern formation. The conservation of these proteins amongst eukaryotes and the demonstration of a role in writing m6 A for the E3 ubiquitin ligase HAKAI is likely to be of considerable relevance beyond the plant sciences.
Department of Plant Biotechnology and Bioinformatics Ghent University 9052 Gent Belgium
Department of Plant Systems Biology VIB 9052 Gent Belgium
Institute of Biotechnology University of Helsinki 00014 Helsinki Finland
Research Center in Biodiversity and Genetic Resources University of Porto 4485 661 Vairão Portugal
Sainsbury Laboratory University of Cambridge Cambridge CB2 1LR UK
Zobrazit více v PubMed
Agarwala SD, Blitzblau HG, Hochwagen A, Fink GR. 2012. RNA methylation by the MIS complex regulates a cell fate decision in yeast. PLoS Genetics 8: e1002732. PubMed PMC
Alarcón CR, Goodarzi H, Lee H, Liu X, Tavazoie S, Tavazoie SF. 2015a. HNRNPA2B1 is a mediator of m6A‐dependent nuclear RNA processing events. Cell 162: 1299–1308. PubMed PMC
Alarcón CR, Lee H, Goodarzi H, Halberg N, Tavazoie SF. 2015b. N6‐methyladenosine marks primary microRNAs for processing. Nature 519: 482–485. PubMed PMC
Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biology 11: R106. PubMed PMC
Aparicio LA, Valladares M, Blanco M, Alonso G, Figueroa A. 2012. Biological influence of Hakai in cancer: a 10‐year review. Cancer Metastasis Reviews 31: 375–386. PubMed PMC
Bishopp A, Help H, El‐Showk S, Weijers D, Scheres B, Friml J, Benková E, Mähönen AP, Helariutta Y. 2011. A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Current Biology 21: 917–926. PubMed
Bodi Z, Bottley A, Archer N, May ST, Fray RG. 2015. Yeast m6A methylated mRNAs are enriched on translating ribosomes during meiosis, and under rapamycin treatment. PLoS ONE 10: e0132090. PubMed PMC
Bodi Z, Zhong S, Mehra S, Song J, Graham N, Li H, May S, Fray RG. 2012. Adenosine methylation in Arabidopsis mRNA is associated with the 3′ end and reduced levels cause developmental defects. Frontiers in Plant Science 3: 48. PubMed PMC
Bokar JA, Rath‐Shambaugh ME, Ludwiczak R, Narayan P, Rottman F. 1994. Characterization and partial purification of mRNA N6‐adenosine methyltransferase from HeLa cell nuclei. Internal mRNA methylation requires a multisubunit complex. Journal of Biological Chemistry 269: 17 697–17 704. PubMed
Bokar JA, Shambaugh ME, Polayes D, Matera AG, Rottman FM. 1997. Purification and cDNA cloning of the AdoMet‐binding subunit of the human mRNA (N 6‐adenosine)‐methyltransferase. RNA (New York, N.Y.) 3: 1233–1247. PubMed PMC
Bujnicki JM, Feder M, Radlinska M, Blumenthal RM. 2002. Structure prediction and phylogenetic analysis of a functionally diverse family of proteins homologous to the MT‐A70 subunit of the human mRNA: m6A methyltransferase. Journal of Molecular Evolution 55: 431–444. PubMed
Caño‐Delgado A, Lee J‐Y, Demura T. 2010. Regulatory mechanisms for specification and patterning of plant vascular tissues. Annual Review of Cell and Developmental Biology 26: 605–637. PubMed
Clancy MJ, Shambaugh ME, Timpte CS, Bokar JA. 2002. Induction of sporulation in Saccharomyces cerevisiae leads to the formation of N6‐methyladenosine in mRNA: a potential mechanism for the activity of the IME4 gene. Nucleic Acids Research 30: 4509–4518. PubMed PMC
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. STAR: ultrafast universal RNA‐seq aligner. Bioinformatics 29: 15–21. PubMed PMC
Dominissini D, Moshitch‐Moshkovitz S, Schwartz S, Salmon‐Divon M, Ungar L, Osenberg S, Cesarkas K, Jacob‐Hirsch J, Amariglio N, Kupiec M et al 2012. Topology of the human and mouse m6A RNA methylomes revealed by m6A‐seq. Nature 485: 201–206. PubMed
Du Z, Zhou X, Ling Y, Zhang Z, Su Z. 2010. agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Research 38: W64–W70. PubMed PMC
Edgren H, Murumagi A, Kangaspeska S, Nicorici D, Hongisto V, Kleivi K, Rye IH, Nyberg S, Wolf M, Borresen‐Dale A‐L et al 2011. Identification of fusion genes in breast cancer by paired‐end RNA‐sequencing. Genome Biology 12: R6. PubMed PMC
Fang Y, Hearn S, Spector DL. 2004. Tissue‐specific expression and dynamic organization of SR splicing factors in Arabidopsis . Molecular Biology of the Cell 15: 2664–2673. PubMed PMC
Figueroa A, Kotani H, Toda Y, Mazan‐Mamczarz K, Mueller E‐C, Otto A, Disch L, Norman M, Ramdasi RM, Keshtgar M et al 2009. Novel roles of Hakai in cell proliferation and oncogenesis. Molecular Biology of the Cell 20: 3533–3542. PubMed PMC
Fray RG, Simpson GG. 2015. The Arabidopsis epitranscriptome. Current Opinion in Plant Biology 27: 17–21. PubMed
Friml J, Benková E, Blilou I, Wisniewska J, Hamann T, Ljung K, Woody S, Sandberg G, Scheres B, Jürgens G et al 2002. AtPIN4 mediates sink‐driven auxin gradients and root patterning in Arabidopsis . Cell 108: 661–673. PubMed
Fujita Y, Krause G, Scheffner M, Zechner D, Leddy HEM, Behrens J, Sommer T, Birchmeier W. 2002. Hakai, a c‐Cbl‐like protein, ubiquitinates and induces endocytosis of the E‐cadherin complex. Nature Cell Biology 4: 222–231. PubMed
Furuta KM, Yadav SR, Lehesranta S, Belevich I, Miyashima S, Heo J, Vatén A, Lindgren O, De Rybel B, Van Isterdael G et al 2014. Plant development. Arabidopsis NAC45/86 direct sieve element morphogenesis culminating in enucleation. Science (New York, N.Y.) 345: 933–937. PubMed
Fustin J‐M, Doi M, Yamaguchi Y, Hida H, Nishimura S, Yoshida M, Isagawa T, Morioka MS, Kakeya H, Manabe I et al 2013. RNA‐methylation‐dependent RNA processing controls the speed of the circadian clock. Cell 155: 793–806. PubMed
Geldner N, Dénervaud‐Tendon V, Hyman DL, Mayer U, Stierhof Y‐D, Chory J. 2009. Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant Journal 59: 169–178. PubMed PMC
Geula S, Moshitch‐Moshkovitz S, Dominissini D, Mansour AA, Kol N, Salmon‐Divon M, Hershkovitz V, Peer E, Mor N, Manor YS et al 2015. m6A mRNA methylation facilitates resolution of naïve pluripotency toward differentiation. Science 347: 1002–1006. PubMed
Gleave AP. 1992. A versatile binary vector system with a T‐DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Molecular Biology 20: 1203–1207. PubMed
Grabov A, Ashley MK, Rigas S, Hatzopoulos P, Dolan L, Vicente‐Agullo F. 2005. Morphometric analysis of root shape. New Phytologist 165: 641–651. PubMed
Haussmann IU, Bodi Z, Sanchez‐Moran E, Mongan NP, Archer N, Fray RG, Soller M. 2016. m6A potentiates Sxl alternative pre‐mRNA splicing for robust Drosophila sex determination. Nature 540: 301–304. PubMed
Hilfiker A, Amrein H, Dübendorfer A, Schneiter R, Nöthiger R. 1995. The gene virilizer is required for female‐specific splicing controlled by Sxl, the master gene for sexual development in Drosophila . Development (Cambridge, England) 121: 4017–4026. PubMed
Hongay CF, Orr‐Weaver TL. 2011. Drosophila Inducer of MEiosis 4 (IME4) is required for Notch signaling during oogenesis. Proceedings of the National Academy of Sciences, USA 108: 14 855–14 860. PubMed PMC
Horiuchi K, Kawamura T, Iwanari H, Ohashi R, Naito M, Kodama T, Hamakubo T. 2013. Identification of Wilms’ tumor 1‐associating protein complex and its role in alternative splicing and the cell cycle. Journal of Biological Chemistry 288: 33 292–33 302. PubMed PMC
Horowitz S, Horowitz A, Nilsen TW, Munns TW, Rottman FM. 1984. Mapping of N 6‐methyladenosine residues in bovine prolactin mRNA. Proceedings of the National Academy of Sciences, USA 81: 5667–5671. PubMed PMC
Ito T, Chiba T, Ozawa R, Yoshida M, Hattori M, Sakaki Y. 2001. A comprehensive two‐hybrid analysis to explore the yeast protein interactome. Proceedings of the National Academy of Sciences, USA 98: 4569–4574. PubMed PMC
Jia G, Fu Y, Zhao X, Dai Q, Zheng G, Yang Y, Yi C, Lindahl T, Pan T, Yang Y‐G et al 2011. N6‐Methyladenosine in nuclear RNA is a major substrate of the obesity‐associated FTO. Nature Chemical Biology 7: 885–887. PubMed PMC
Kaido M, Wada H, Shindo M, Hayashi S. 2009. Essential requirement for RING finger E3 ubiquitin ligase Hakai in early embryonic development of Drosophila. Genes to Cells 14: 1067–1077. PubMed
Kania U, Fendrych M, Friml J. 2014. Polar delivery in plants; commonalities and differences to animal epithelial cells. Open Biology 4: 140017. PubMed PMC
Karimi M, Depicker A, Hilson P. 2007. Recombinational cloning with plant gateway vectors. Plant Physiology 145: 1144–1154. PubMed PMC
Ke S, Alemu EA, Mertens C, Gantman EC, Fak JJ, Mele A, Haripal B, Zucker‐Scharff I, Moore MJ, Park CY et al 2015. A majority of m6A residues are in the last exons, allowing the potential for 3′ UTR regulation. Genes & Development 29: 2037–2053. PubMed PMC
Kleinboelting N, Huep G, Kloetgen A, Viehoever P, Weisshaar B. 2012. GABI‐Kat SimpleSearch: new features of the Arabidopsis thaliana T‐DNA mutant database. Nucleic Acids Research 40: D1211–D1215. PubMed PMC
Koegl M, Uetz P. 2007. Improving yeast two‐hybrid screening systems. Briefings in Functional Genomics & Proteomics 6: 302–312. PubMed
Lahav R, Gammie A, Tavazoie S, Rose MD. 2007. Role of transcription factor Kar4 in regulating downstream events in the Saccharomyces cerevisiae pheromone response pathway. Molecular and Cellular Biology 27: 818–829. PubMed PMC
Lence T, Akhtar J, Bayer M, Schmid K, Spindler L, Ho CH, Kreim N, Andrade‐Navarro MA, Poeck B, Helm M et al 2016. m6A modulates neuronal functions and sex determination in Drosophila . Nature 540: 242–247. PubMed
Letunic I, Doerks T, Bork P. 2012. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Research 40: D302–D305. PubMed PMC
Li Y, Wang X, Li C, Hu S, Yu J, Song S. 2014. Transcriptome‐wide N6‐methyladenosine profiling of rice callus and leaf reveals the presence of tissue‐specific competitors involved in selective mRNA modification. RNA Biology 11: 1180–1188. PubMed PMC
Liu N, Dai Q, Zheng G, He C, Parisien M, Pan T. 2015. N6‐methyladenosine‐dependent RNA structural switches regulate RNA‐protein interactions. Nature 518: 560–564. PubMed PMC
Liu J, Yue Y, Han D, Wang X, Fu Y, Zhang L, Jia G, Yu M, Lu Z, Deng X et al 2014. A METTL3‐METTL14 complex mediates mammalian nuclear RNA N 6‐adenosine methylation. Nature Chemical Biology 10: 93–95. PubMed PMC
Lorković ZJ, Hilscher J, Barta A. 2008. Co‐localisation studies of Arabidopsis SR splicing factors reveal different types of speckles in plant cell nuclei. Experimental Cell Research 314: 3175–3186. PubMed
Luo G‐Z, MacQueen A, Zheng G, Duan H, Dore LC, Lu Z, Liu J, Chen K, Jia G, Bergelson J et al 2014. Unique features of the m6A methylome in Arabidopsis thaliana . Nature Communications 5: 5630. PubMed PMC
Machnicka MA, Milanowska K, Osman Oglou O, Purta E, Kurkowska M, Olchowik A, Januszewski W, Kalinowski S, Dunin‐Horkawicz S, Rother KM et al 2013. MODOMICS: a database of RNA modification pathways – 2013 update. Nucleic Acids Research 41: D262–D267. PubMed PMC
Mähönen AP, Bishopp A, Higuchi M, Nieminen KM, Kinoshita K, Törmäkangas K, Ikeda Y, Oka A, Kakimoto T, Helariutta Y. 2006. Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science (New York, N.Y.) 311: 94–98. PubMed
Mähönen AP, ten Tusscher K, Siligato R, Smetana O, Díaz‐Triviño S, Salojärvi J, Wachsman G, Prasad K, Heidstra R, Scheres B. 2014. PLETHORA gradient formation mechanism separates auxin responses. Nature 515: 125–129. PubMed PMC
Meyer KD, Jaffrey SR. 2014. The dynamic epitranscriptome: N6‐methyladenosine and gene expression control. Nature Reviews. Molecular Cell Biology 15: 313–326. PubMed PMC
Meyer KD, Saletore Y, Zumbo P, Elemento O, Mason CE, Jaffrey SR. 2012. Comprehensive analysis of mRNA methylation reveals enrichment in 3′ UTRs and near stop codons. Cell 149: 1635–1646. PubMed PMC
Narayan P, Rottman FM. 1988. An in vitro system for accurate methylation of internal adenosine residues in messenger RNA. Science 242: 1159–1162. PubMed
Nekrasov V, Staskawicz B, Weigel D, Jones JDG, Kamoun S. 2013. Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA‐guided endonuclease. Nature Biotechnology 31: 691–693. PubMed
Niessen M, Schneiter R, Nothiger R. 2001. Molecular identification of virilizer, a gene required for the expression of the sex‐determining gene Sex‐lethal in Drosophila melanogaster . Genetics 157: 679–688. PubMed PMC
Ortega A, Niksic M, Bachi A, Wilm M, Sánchez L, Hastie N, Valcárcel J. 2003. Biochemical function of Female‐lethal (2)D/Wilms’ tumor suppressor‐1‐associated proteins in alternative pre‐mRNA splicing. Journal of Biological Chemistry 278: 3040–3047. PubMed
Pekárová B, Klumpler T, Třísková O, Horák J, Jansen S, Dopitová R, Borkovcová P, Papoušková V, Nejedlá E, Sklenář V et al 2011. Structure and binding specificity of the receiver domain of sensor histidine kinase CKI1 from Arabidopsis thaliana . Plant Journal 67: 827–839. PubMed
Ping X‐L, Sun B‐F, Wang L, Xiao W, Yang X, Wang W‐J, Adhikari S, Shi Y, Lv Y, Chen Y‐S et al 2014. Mammalian WTAP is a regulatory subunit of the RNA N 6 ‐methyladenosine methyltransferase. Cell Research 24: 177–189. PubMed PMC
Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J et al 2012. The Pfam protein families database. Nucleic Acids Research 40: D290–D301. PubMed PMC
Reddy ASN, Day IS, Göhring J, Barta A. 2012. Localization and dynamics of nuclear speckles in plants. Plant Physiology 158: 67–77. PubMed PMC
Ruzicka K, Strader LC, Bailly A, Yang H, Blakeslee J, Langowski L, Nejedlá E, Fujita H, Itoh H, Syono K et al 2010. Arabidopsis PIS1 encodes the ABCG37 transporter of auxinic compounds including the auxin precursor indole‐3‐butyric acid. Proceedings of the National Academy of Sciences, USA 107: 10749–10 753. PubMed PMC
Schneeberger K, Ossowski S, Lanz C, Juul T, Petersen AH, Nielsen KL, Jørgensen J‐E, Weigel D, Andersen SU. 2009. SHOREmap: simultaneous mapping and mutation identification by deep sequencing. Nature Methods 6: 550–551. PubMed
Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9: 671–675. PubMed PMC
Schwartz S, Mumbach MR, Jovanovic M, Wang T, Maciag K, Bushkin GG, Mertins P, Ter‐Ovanesyan D, Habib N, Cacchiarelli D et al 2014. Perturbation of m6A writers reveals two distinct classes of mRNA methylation at internal and 5′ sites. Cell Reports 8: 284–296. PubMed PMC
Shen L, Liang Z, Gu X, Chen Y, Teo ZWN, Hou X, Cai WM, Dedon PC, Liu L, Yu H. 2016. N 6‐methyladenosine RNA modification regulates shoot stem cell fate in Arabidopsis . Developmental Cell 38: 186–200. PubMed PMC
Shen S, Park JW, Lu Z, Lin L, Henry MD, Wu YN, Zhou Q, Xing Y. 2014. rMATS: robust and flexible detection of differential alternative splicing from replicate RNA‐Seq data. Proceedings of the National Academy of Sciences, USA 111: E5593–E5601. PubMed PMC
Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J et al 2011. Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology 7: 539 PubMed PMC
Siligato R, Wang X, Yadav SR, Lehesranta S, Ma G, Ursache R, Sevilem I, Zhang J, Gorte M, Prasad K et al 2016. MultiSite Gateway‐compatible cell type‐specific gene‐inducible system for plants. Plant Physiology 170: 627–641. PubMed PMC
Spector DL, Lamond AI. 2011. Nuclear Speckles. Cold Spring Harbor Perspectives in Biology 3: a000646. PubMed PMC
Tillemans V, Leponce I, Rausin G, Dispa L, Motte P. 2006. Insights into nuclear organization in plants as revealed by the dynamic distribution of Arabidopsis SR splicing factors. Plant Cell 18: 3218–3234. PubMed PMC
Tzafrir I, Dickerman A, Brazhnik O, Nguyen Q, McElver J, Frye C, Patton D, Meinke D. 2003. The Arabidopsis SeedGenes Project. Nucleic Acids Research 31: 90–93. PubMed PMC
Tzafrir I, Pena‐Muralla R, Dickerman A, Berg M, Rogers R, Hutchens S, Sweeney TC, McElver J, Aux G, Patton D et al 2004. Identification of genes required for embryo development in Arabidopsis . Plant Physiology 135: 1206–1220. PubMed PMC
Van Leene J, Eeckhout D, Persiau G, Van De Slijke E, Geerinck J, Van Isterdael G, Witters E, De Jaeger G. 2011. Isolation of transcription factor complexes from Arabidopsis cell suspension cultures by tandem affinity purification. Methods in Molecular Biology (Clifton, N.J.) 754: 195–218. PubMed
Van Leene J, Hollunder J, Eeckhout D, Persiau G, Van De Slijke E, Stals H, Van Isterdael G, Verkest A, Neirynck S, Buffel Y et al 2010. Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana . Molecular Systems Biology 6: 397. PubMed PMC
Van Leene J, Stals H, Eeckhout D, Persiau G, Van De Slijke E, Van Isterdael G, De Clercq A, Bonnet E, Laukens K, Remmerie N et al 2007. A tandem affinity purification‐based technology platform to study the cell cycle interactome in Arabidopsis thaliana . Molecular & Cellular Proteomics 6: 1226–1238. PubMed
Van Leene J, Witters E, Inzé D, De Jaeger G. 2008. Boosting tandem affinity purification of plant protein complexes. Trends in Plant Science 13: 517–520. PubMed
Vespa L, Vachon G, Berger F, Perazza D, Faure J‐D, Herzog M. 2004. The immunophilin‐interacting protein AtFIP37 from Arabidopsis is essential for plant development and is involved in trichome endoreduplication. Plant Physiology 134: 1283–1292. PubMed PMC
Wan Y, Tang K, Zhang D, Xie S, Zhu X, Wang Z, Lang Z. 2015. Transcriptome‐wide high‐throughput deep m6A‐seq reveals unique differential m6A methylation patterns between three organs in Arabidopsis thaliana . Genome Biology 16: 272. PubMed PMC
Wang X, Lu Z, Gomez A, Hon GC, Yue Y, Han D, Fu Y, Parisien M, Dai Q, Jia G et al 2014a. N 6‐methyladenosine‐dependent regulation of messenger RNA stability. Nature 505: 117–120. PubMed PMC
Wang X, Zhao BS, Roundtree IA, Lu Z, Han D, Ma H, Weng X, Chen K, Shi H, He C. 2015. N 6‐methyladenosine modulates messenger RNA translation efficiency. Cell 161: 1388–1399. PubMed PMC
Wang Y, Li Y, Toth JI, Petroski MD, Zhang Z, Zhao JC. 2014b. N 6‐methyladenosine modification destabilizes developmental regulators in embryonic stem cells. Nature Cell Biology 16: 191–198. PubMed PMC
Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ. 2009. Jalview Version 2 – a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189–1191. PubMed PMC
Xiao W, Adhikari S, Dahal U, Chen Y‐S, Hao Y‐J, Sun B‐F, Sun H‐Y, Li A, Ping X‐L, Lai W‐Y et al 2016. Nuclear m6A reader YTHDC1 regulates mRNA splicing. Molecular Cell 61: 507–519. PubMed
Yue Y, Liu J, He C. 2015. RNA N 6‐methyladenosine methylation in post‐transcriptional gene expression regulation. Genes & Development 29: 1343–1355. PubMed PMC
Zheng G, Dahl JA, Niu Y, Fedorcsak P, Huang C‐M, Li CJ, Vågbø CB, Shi Y, Wang W‐L, Song S‐H et al 2013. ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility. Molecular Cell 49: 18–29. PubMed PMC
Zhong S, Li H, Bodi Z, Button J, Vespa L, Herzog M, Fray RG. 2008. MTA is an Arabidopsis messenger RNA adenosine methylase and interacts with a homolog of a sex‐specific splicing factor. Plant Cell 20: 1278–1288. PubMed PMC
Zhou J, Wan J, Gao X, Zhang X, Jaffrey SR, Qian S‐B. 2015. Dynamic m6A mRNA methylation directs translational control of heat shock response. Nature 526: 591–594. PubMed PMC
N6-methyladenosine RNA modification regulates photosynthesis during photodamage in plants
RNA methylation in nuclear pre-mRNA processing