Methyltransferase-like (METTL) homologues participate in Nicotiana benthamiana antiviral responses

References

• Wiener D, Schwartz S. The epitranscriptome beyond m6A. Nat Rev Genet. 2021;22(2):119–10. doi:10.1038/s41576-020-00295-8.
   PubMed Web of Science ®Google Scholar
• Martin JL, McMillan FM. SAM (dependent) I AM: the S-Adenosylmethionine-dependent methyltransferase fold. Curr Opin Struct Biol. 2002;12(6):783–793. doi:10.1016/s0959-440x(02)00391-3.
   PubMed Web of Science ®Google Scholar
• Schubert HL, Blumenthal RM, Cheng X. Many paths to methyltransfer: a chronicle of convergence. Trends Biochem Sci. 2003;28:329–335.
   PubMed Web of Science ®Google Scholar
• Huang J, Yin P. Structural insights into N6-methyladenosine (m6A) modification in the transcriptome. Genom Proteom Bioinformat. 2018;16(2):85–98. doi:10.1016/j.gpb.2018.03.001.
   PubMed Web of Science ®Google Scholar
• Sun Q, Huang M, Wei Y. Diversity of the reaction mechanisms of SAM-dependent enzymes. Acta Pharm Sin B. 2021;11(3):632–650. doi:10.1016/j.apsb.2020.08.011.
   PubMed Web of Science ®Google Scholar
• Fischer TR, Meidner L, Schwickert M, Weber M, Zimmermann RA, Kersten C, Schirmeister T, Helm M. Chemical biology and medicinal chemistry of RNA methyltransferases. Nucleic Acids Res. 2022;50(8):4216–4245. doi:10.1093/nar/gkac224.
   PubMed Web of Science ®Google Scholar
• Zaccara S, Ries RJ, Jaffrey SR. Reading, writing and erasing MRNA methylation. Nat Rev Mol Cell Biol. 2019;20(10):608–624. doi:10.1038/s41580-019-0168-5.
   PubMed Web of Science ®Google Scholar
• Dang W, Xie Y, Cao P, Xin S, Wang J, Li S, Li Y, Lu J. N6-methyladenosine and viral infection. Front Microbiol. 2019;10:417. doi:10.3389/fmicb.2019.00417.
   PubMed Web of Science ®Google Scholar
• Miao Z, Zhang T, Xie B, Qi Y, Ma C, Echave J. Evolutionary implications of the RNA N6-methyladenosine methylome in plants. Mol Biol Evol. 2022;39(1):msab299. doi:10.1093/molbev/msab299.
   PubMed Web of Science ®Google Scholar
• Yue J, Wei Y, Zhao M. The reversible methylation of m6A is involved in plant virus infection. Biology. 2022;11(2):271. doi:10.3390/biology11020271.
   PubMedGoogle Scholar
• Li N, Rana TM. Regulation of antiviral innate immunity by chemical modification of viral RNA. Wiley Interdiscip Rev RNA. 2022;13(6):e1720. doi:10.1002/wrna.1720.
   PubMed Web of Science ®Google Scholar
• Liang Z, Riaz A, Chachar S, Ding Y, Du H, Gu X. Epigenetic modifications of mRNA and DNA in plants. Mol Plant. 2020;13(1):14–30. doi:10.1016/j.molp.2019.12.007.
   PubMed Web of Science ®Google Scholar
• Duan H, Wang Y, Jia G. Dynamic and reversible RNA N6‐methyladenosine methylation. WIREs RNA. 2019;10(1):1. doi:10.1002/wrna.1507.
   Google Scholar
• Wong JM, Eirin-Lopez JM, Larracuente A. Evolution of methyltransferase-like (METTL) proteins in Metazoa: a complex gene family involved in epitranscriptomic regulation and other epigenetic processes. Mol Biol Evol. 2021;38(12):5309–5327. doi:10.1093/molbev/msab267.
   PubMed Web of Science ®Google Scholar
• Geula S, Moshitch-Moshkovitz S, Dominissini D, Mansour AA, Kol N, Salmon-Divon M, Hershkovitz V, Peer E, Mor N, Manor YS, et al. m6A mRNA methylation facilitates resolution of naïve pluripotency toward differentiation. Sci. 2015;347(6225):1002–1006. doi:10.1126/science.1261417.
   PubMed Web of Science ®Google Scholar
• Zhong S, Li H, Bodi Z, Button J, Vespa L, Herzog M, Fray RG. MTA is an Arabidopsis messenger RNA adenosine methylase and interacts with a homolog of a sex-specific splicing factor. Plant Cell. 2008;20(5):1278–1288. doi:10.1105/tpc.108.058883.
   PubMed Web of Science ®Google Scholar
• Růžička K, Zhang M, Campilho A, Bodi Z, Kashif M, Saleh M, Eeckhout D, El‐showk S, Li H, Zhong S, De Jaeger G, Mongan NP, Hejátko J, Helariutta Y, Fray RG. Identification of factors required for m6A mRNA methylation in Arabidopsis reveals a role for the conserved E3 ubiquitin ligase HAKAI. New Phytol. 2017;215(1):157–172. doi:10.1111/nph.14586.
   PubMed Web of Science ®Google Scholar
• Mushegian A. Methyltransferases of Riboviria. Biomolecul. 2022;12(9):1247. doi:10.3390/biom12091247.
   PubMed Web of Science ®Google Scholar
• Lichinchi G, Gao S, Saletore Y, Gonzalez GM, Bansal V, Wang Y, Mason CE, Rana TM. Dynamics of the human and viral m6A RNA methylomes during HIV-1 infection of T cells. Nat Microbiol. 2016;1(4):16011. doi:10.1038/nmicrobiol.2016.11.
   PubMed Web of Science ®Google Scholar
• Lichinchi G, Zhao BS, Wu Y, Lu Z, Qin Y, He C, Rana TM. Dynamics of human and viral RNA methylation during Zika virus infection. Cell Host & Microbe. 2016;20(5):666–673. doi:10.1016/j.chom.2016.10.002.
   PubMed Web of Science ®Google Scholar
• Sacco MT, Bland KM, Horner SM, Heise MT. WTAP targets the METTL3 m6A-methyltransferase complex to cytoplasmic hepatitis C virus RNA to regulate infection. J Virol. 2022;96(22): e00997-22. doi:10.1128/jvi.00997-22.
   PubMed Web of Science ®Google Scholar
• Gokhale NS, McIntyre ABR, McFadden MJ, Roder AE, Kennedy EM, Gandara JA, Hopcraft SE, Quicke KM, Vazquez C, Willer J, Ilkayeva OR, Law BA, Holley CL, Garcia-Blanco MA, Evans MJ, Suthar MS, Bradrick SS, Mason CE, Horner SM. N6-methyladenosine in Flaviviridae viral RNA genomes regulates infection. Cell Host & Microbe. 2016;20(5):654–665. doi:10.1016/j.chom.2016.09.015.
   PubMed Web of Science ®Google Scholar
• Liu J, Xu YP, Li K, Ye Q, Zhou HY, Sun H, Li X, Yu L, Deng YQ, Li RT, Cheng ML, He B, Zhou J, Li XF, Wu A, Yi C, Qin CF. The m6A methylome of SARS-CoV-2 in host cells. Cell Res. 2021;31(4):404–414. doi:10.1038/s41422-020-00465-7.
   PubMed Web of Science ®Google Scholar
• Zhou L, Gao G, Tang R, Wang W, Wang Y, Tian S, Qin G. m6A‐mediated regulation of crop development and stress responses. Plant Biotechnol J. 2022:13792. doi:10.1111/pbi.13792.
   Web of Science ®Google Scholar
• Martínez-Pérez M, Aparicio F, López-Gresa MP, Bellés JM, Sánchez-Navarro JA, Pallás V. Arabidopsis m6A demethylase activity modulates viral infection of a plant virus and the m6A abundance in its genomic RNAs. Proc Natl Acad Sci U S A. 2017;114(40):10755–10760. doi:10.1073/pnas.1703139114.
   PubMed Web of Science ®Google Scholar
• Martínez-Pérez M, Gómez-Mena C, Alvarado-Marchena L, Nadi R, Micol JL, Pallás V, Aparicio F. The m6A RNA demethylase ALKBH9B plays a critical role for vascular movement of alfalfa mosaic virus in Arabidopsis. Front Microbiol. 2021;12:745576. doi:10.3389/fmicb.2021.745576.
   PubMed Web of Science ®Google Scholar
• Pasin F, Daròs JA, Tzanetakis IE. Proteome expansion in the Potyviridae evolutionary radiation. FEMS Microbiol Rev. 2022;46(4):fuac011. doi:10.1093/femsre/fuac011.
   PubMed Web of Science ®Google Scholar
• Inoue-Nagata AK, Jordan R, Kreuze J, Li F, López-Moya JJ, Mäkinen K, Ohshima K, Wylie SJ. ICTV report consortium. ICTV virus taxonomy profile: Potyviridae 2022. J Gen Virol. 2022;103(5):5. doi:10.1099/jgv.0.001738.
   Web of Science ®Google Scholar
• Yue J, Wei Y, Sun Z, Chen Y, Wei X, Wang H, Pasin F, Zhao M. AlkB RNA demethylase homologues and N6-methyladenosine are involved in Potyvirus infection. Mol Plant Pathol. 2022;23(10):1555–1564. doi:10.1111/mpp.13239.
   PubMed Web of Science ®Google Scholar
• Zhang T, Wang Z, Hu H, Chen Z, Liu P, Gao S, Zhang F, He L, Jin P, Xu M, et al. Transcriptome-wide N6-methyladenosine (m6A) profiling of susceptible and resistant wheat varieties reveals the involvement of variety-specific m6A modification involved in virus-host interaction pathways. Front Microbiol. 2021;12:656302. doi:10.3389/fmicb.2021.656302.
   PubMed Web of Science ®Google Scholar
• Zhang T, Shi C, Hu H, Zhang Z, Wang Z, Chen Z, Feng H, Liu P, Guo J, Lu Q, Zhong K, Chen Z, Liu J, Yu J, Chen J, Chen F, Yang J. N6-methyladenosine RNA modification promotes viral genomic RNA stability and infection. Nat Commun. 2022;13(1):6576. doi:10.1038/s41467-022-34362-x.
   PubMed Web of Science ®Google Scholar
• Kourelis J, Kaschani F, Grosse-Holz FM, Homma F, Kaiser M, van der Hoorn RAL. A homology-guided, genome-based proteome for improved proteomics in the alloploid Nicotiana Benthamiana. BMC Genomics. 2019;20(1):722. doi:10.1186/s12864-019-6058-6.
   PubMed Web of Science ®Google Scholar
• Pasin F, Shan H, García B, Müller M, San León D, Ludman M, Fresno DH, Fátyol K, Munné-Bosch S, Rodrigo G, García JA. Abscisic acid connects phytohormone signaling with RNA metabolic pathways and promotes an antiviral response that is evaded by a self-controlled RNA virus. Plant Commun. 2020;1(5):100099. doi:10.1016/j.xplc.2020.100099.
   PubMedGoogle Scholar
• Warda AS, Kretschmer J, Hackert P, Lenz C, Urlaub H, Höbartner C, Sloan KE, Bohnsack MT. Human METTL16 is a N6-methyladenosine (m6A) methyltransferase that targets pre-mRNAs and various non-coding RNAs. EMBO Rep. 2017;18(11):2004–2014. doi:10.15252/embr.201744940.
   PubMed Web of Science ®Google Scholar
• Satterwhite ER, Mansfield KD. RNA methyltransferase METTL16: targets and function. Wiley Interdiscip Rev RNA. 2022;13(2):e1681. doi:10.1002/wrna.1681.
   PubMed Web of Science ®Google Scholar
• Parker MT, Soanes BK, Kusakina J, Larrieu A, Knop K, Joy N, Breidenbach F, Sherwood AV, Barton GJ, Fica SM, et al. m6A modification of U6 snRNA modulates usage of two major classes of pre-mRNA 5’ splice site. Elife. 2022;11:e78808. doi:10.7554/eLife.78808.
   PubMed Web of Science ®Google Scholar
• Xu T, Wu X, Wong CE, Fan S, Zhang Y, Zhang S, Liang Z, Yu H, Shen L. FIONA1-mediated m6A modification regulates the floral transition in Arabidopsis. Adv Sci. 2022;9(6):e2103628. doi:10.1002/advs.202103628.
   Web of Science ®Google Scholar
• Wu R, Ding F, Wang R, Shen R, Zhang X, Luo S, Su C, Wu Z, Xie Q, Berger B, et al. High-resolution de novo structure prediction from primary sequence. Preprint. 2022. doi:10.1101/2022.07.21.500999.
   Google Scholar
• Varadi M, Anyango S, Deshpande M, Nair S, Natassia C, Yordanova G, Yuan D, Stroe O, Wood G, Laydon A, Žídek A, Green T, Tunyasuvunakool K, Petersen S, Jumper J, Clancy E, Green R, Vora A, Lutfi M, Figurnov M, Cowie A, Hobbs N, Kohli P, Kleywegt G, Birney E, Hassabis D, Velankar S. AlphaFold protein structure database: massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Res. 2022;50(D1):D439–444. doi:10.1093/nar/gkab1061.
   PubMed Web of Science ®Google Scholar
• Ji L, Chen X. Regulation of small RNA stability: methylation and beyond. Cell Res. 2012;22(4):624–636. doi:10.1038/cr.2012.36.
   PubMed Web of Science ®Google Scholar
• van den Born E, Omelchenko MV, Bekkelund A, Leihne V, Koonin EV, Dolja VV, Falnes PØ. Viral AlkB proteins repair RNA damage by oxidative demethylation. Nucleic Acids Res. 2008;36(17):5451–5461. doi:10.1093/nar/gkn519.
   PubMed Web of Science ®Google Scholar
• Alvarado-Marchena L, Martínez-Pérez M, Úbeda JR, Pallas V, Aparicio F. Impact of the potential m6A modification sites at the 3’UTR of alfalfa mosaic virus RNA3 in the viral infection. Viruses. 2022;14(8):1718. doi:10.3390/v14081718.
   PubMed Web of Science ®Google Scholar
• Zhang K, Zhuang X, Dong Z, Xu K, Chen X, Liu F, He Z. The dynamics of N6-methyladenine RNA modification in interactions between rice and plant viruses. Genome Biol. 2021;22(1):189. doi:10.1186/s13059-021-02410-2.
   PubMed Web of Science ®Google Scholar
• Li Z, Shi J, Yu L, Zhao X, Ran L, Hu D, Song B. N6-methyl-adenosine level in Nicotiana tabacum is associated with tobacco mosaic virus. Virol J. 2018;15(1):87. doi:10.1186/s12985-018-0997-4.
   PubMedGoogle Scholar
• He Y, Li L, Yao Y, Li Y, Zhang H, Fan M. Transcriptome-wide N6-methyladenosine (m6A) methylation in watermelon under CGMMV infection. BMC Plant Biol. 2021;21(1):516. doi:10.1186/s12870-021-03289-8.
   PubMed Web of Science ®Google Scholar
• Niu J, Tang M, Wu W, Huo S, Wang X, Liang X, Huang X, Wang G, Jing C, Feng X. N6-methyladenosine regulatory genes in common bean (Phaseolus vulgaris): genome-wide investigation, evolution, structure, characterization, and expression patterns during viral infection. Preprint. 2022. doi:10.21203/rs.3.rs-2243840/v1.
   Google Scholar
• Tian S, Wu N, Zhang L, Wang X. RNA N6-methyladenosine modification suppresses replication of rice black streaked dwarf virus and is associated with virus persistence in its insect vector. Mol Plant Pathol. 2021;22(9):1070–1081. doi:10.1111/mpp.13097.
   PubMed Web of Science ®Google Scholar
• Bratlie MS, Drabløs F. Bioinformatic mapping of AlkB homology domains in viruses. BMC Genomics. 2005;6(1):1. doi:10.1186/1471-2164-6-1.
   PubMedGoogle Scholar
• Susaimuthu J, Tzanetakis IE, Gergerich RC, Martin RR. A member of a new genus in the Potyviridae infects Rubus. Virus Res. 2008;131(2):145–151. doi:10.1016/j.virusres.2007.09.001.
   PubMed Web of Science ®Google Scholar
• Garcia-Ruiz H. Host factors against plant viruses. Mol Plant Pathol. 2019;20(11):1588–1601. doi:10.1111/mpp.12851.
   PubMed Web of Science ®Google Scholar
• Pasin F, Bedoya LC, Bernabé-Orts JM, Gallo A, Simón-Mateo C, Orzaez D, García JA. Multiple T-DNA delivery to plants using novel mini binary vectors with compatible replication origins. ACS Synth Biol. 2017;6(10):1962–1968. doi:10.1021/acssynbio.6b00354.
   PubMed Web of Science ®Google Scholar
• Pasin F. Assembly of plant virus agroinfectious clones using biological material or DNA synthesis. STAR Protoc. 2022;3(4):101716. doi:10.1016/j.xpro.2022.101716.
   PubMedGoogle Scholar
• Chen S, Zhou Y, Chen Y, Gu J. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34(17):i884–890. doi:10.1093/bioinformatics/bty560.
   PubMed Web of Science ®Google Scholar
• Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods. 2017;14(4):417–419. doi:10.1038/nmeth.4197.
   PubMed Web of Science ®Google Scholar
• Bombarely A, Rosli HG, Vrebalov J, Moffett P, Mueller LA, Martin GB. A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Mol Plant Microbe Interact. 2012;25(12):1523–1530. doi:10.1094/MPMI-06-12-0148-TA.
   PubMed Web of Science ®Google Scholar
• Robinson MD, McCarthy DJ, Smyth GK. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformat. 2010;26(1):139–140. doi:10.1093/bioinformatics/btp616.
   Google Scholar
• Suzuki R, Shimodaira H. Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformat. 2006;22(12):1540–1542. doi:10.1093/bioinformatics/btl117.
   Google Scholar
• Woodcroft BJ, Boyd JA, Tyson GW. OrfM: a fast open reading frame predictor for metagenomic data. Bioinformat. 2016;32(17):2702–2703. doi:10.1093/bioinformatics/btw241.
   Google Scholar
• Blum M, Chang HY, Chuguransky S, Grego T, Kandasaamy S, Mitchell A, Nuka G, Paysan-Lafosse T, Qureshi M, Raj S, Richardson L, Salazar GA, Williams L, Bork P, Bridge A, Gough J, Haft DH, Letunic I, Marchler-Bauer A, Mi H, Natale DA, Necci M, Orengo CA, Pandurangan AP, Rivoire C, Sigrist CJA, Sillitoe I, Thanki N, Thomas PD, Tosatto SCE, Wu CH, Bateman A, Finn RD. The InterPro protein families and domains database: 20 years on. Nucleic Acids Res. 2021;49(D1):D344–354. doi:10.1093/nar/gkaa977.
   PubMed Web of Science ®Google Scholar
• Wilson D, Pethica R, Zhou Y, Talbot C, Vogel C, Madera M, Chothia C, Gough J. SUPERFAMILY—sophisticated comparative genomics, data mining, visualization and phylogeny. Nucleic Acids Res. 2009;37(Database issue):D380–386. doi:10.1093/nar/gkn762.
   PubMedGoogle Scholar
• Sainsbury F, Thuenemann EC, Lomonossoff GP. pEAQ: versatile expression vectors for easy and quick transient expression of heterologous proteins in plants. Plant Biotechnol J. 2009;7(7):682–693. doi:10.1111/j.1467-7652.2009.00434.x.
   PubMed Web of Science ®Google Scholar
• Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33(7):1870–1874. doi:10.1093/molbev/msw054.
   PubMed Web of Science ®Google Scholar
• Wang P, Doxtader KA, Nam Y. Structural basis for cooperative function of Mettl3 and Mettl14 methyltransferases. Mol Cell. 2016;63(2):306–317. doi:10.1016/j.molcel.2016.05.041.
   PubMed Web of Science ®Google Scholar
• Mendel M, Chen KM, Homolka D, Gos P, Pandey RR, McCarthy AA, Pillai RS. Methylation of structured RNA by the m6A writer METTL16 is essential for mouse embryonic development. Mol Cell. 2018;71(6):986–1000.e11. doi:10.1016/j.molcel.2018.08.004.
   PubMed Web of Science ®Google Scholar
• Pettersen EF, Goddard TD, Huang CC, Meng EC, Couch GS, Croll TI, Morris JH, Ferrin TE. UCSF ChimeraX: structure visualization for researchers, educators, and developers. Protein Sci. 2021;30(1):70–82. doi:10.1002/pro.3943.
   PubMed Web of Science ®Google Scholar
• Pei J, Kim BH, Grishin NV. PROMALS3D: a tool for multiple protein sequence and structure alignments. Nucleic Acids Res. 2008;36(7):2295–2300. doi:10.1093/nar/gkn072.
   PubMed Web of Science ®Google Scholar
• Holm L, Laakso LM. Dali server update. Nucleic Acids Res. 2016;44(W1):W351–355. doi:10.1093/nar/gkw357.
   PubMed Web of Science ®Google Scholar
• Zhang C, Shine M, Pyle AM, Zhang Y. US-align: universal structure alignments of proteins, nucleic acids, and macromolecular complexes. Nat Methods. 2022;19(9):1109–1115. doi:10.1038/s41592-022-01585-1.
   PubMed Web of Science ®Google Scholar
• Degasperi A, Birtwistle MR, Volinsky N, Rauch J, Kolch W, Kholodenko BN. Evaluating strategies to normalise biological replicates of Western blot data. PLos One. 2014;9(1):e87293. doi:10.1371/journal.pone.0087293.
   PubMed Web of Science ®Google Scholar
• Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc: Ser B (Methodol). 1995;57(1):289–300. doi:10.1111/j.2517-6161.1995.tb02031.x.
   Google Scholar