1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Plant Biology
  4. Volume 74, 2023
  5. Article

Annual Review of Plant Biology

Volume 74, 2023

The Diversity and Functions of Plant RNA Modifications: What We Know and Where We Go from Here

Abstract

Since the discovery of the first ribonucleic acid (RNA) modifications in transfer RNAs (tRNAs) and ribosomal RNAs (rRNAs), scientists have been on a quest to decipher the identities and functions of RNA modifications in biological systems. The last decade has seen monumental growth in the number of studies that have characterized and assessed the functionalities of RNA modifications in the field of plant biology. Owing to these studies, we now categorize RNA modifications based on their chemical nature and the RNA on which they are found, as well as the array of proteins that are involved in the processes that add, read, and remove them from an RNA molecule. Beyond their identity, another key piece of the puzzle is the functional significance of the various types of RNA modifications. Here, we shed light on recent studies that help establish our current understanding of the diversity of RNA modifications found in plant transcriptomes and the functions they play at both the molecular (e.g., RNA stability, translation, and transport) and organismal (e.g., stress response and development) levels. Finally, we consider the key research questions related to plant gene expression and biology in general and highlight developments in various technologies that are driving our insights forward in this research area.

Keyword(s): functional diversity of RNA modification, m5C, m6A, mRNA modifications, plant stress response, rRNA modifications, tRNA modifications
Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-071122-085813
2023-05-22
2024-05-02
Loading full text...

Full text loading...

/deliver/fulltext/arplant/74/1/annurev-arplant-071122-085813.html?itemId=/content/journals/10.1146/annurev-arplant-071122-085813&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Alvarado-Marchena L, Marquez-Molins J, Martinez-Perez M, Aparicio F, Pallás V. 2021. Mapping of functional subdomains in the atALKBH9B m6A-demethylase required for its binding to the viral RNA and to the coat protein of alfalfa mosaic virus. Front. Plant Sci. 12:701683
     [Google Scholar]
  2. 2.
    Anderson SJ, Kramer MC, Gosai SJ, Yu X, Vandivier LE et al. 2018. N6-Methyladenosine inhibits local ribonucleolytic cleavage to stabilize mRNAs in Arabidopsis. Cell Rep. 25:51146–57.e3
     [Google Scholar]
  3. 3.
    Arribas-Hernández L, Bressendorff S, Hansen MH, Poulsen C, Erdmann S, Brodersen P. 2018. An m6A-YTH module controls developmental timing and morphogenesis in Arabidopsis. Plant Cell 30:5952–67
     [Google Scholar]
  4. 4.
    Arribas-Hernández L, Rennie S, Schon M, Porcelli C, Enugutti B et al. 2021. The YTHDF proteins ECT2 and ECT3 bind largely overlapping target sets and influence target mRNA abundance, not alternative polyadenylation. eLife 10:e72377
     [Google Scholar]
  5. 5.
    Batista PJ, Molinie B, Wang J, Qu K, Zhang J et al. 2014. m6A RNA modification controls cell fate transition in mammalian embryonic stem cells. Cell Stem Cell 15:6707–19
     [Google Scholar]
  6. 6.
    Bhat SS, Bielewicz D, Gulanicz T, Bodi Z, Yu X et al. 2020. mRNA adenosine methylase (MTA) deposits m6A on pri-miRNAs to modulate miRNA biogenesis in Arabidopsis thaliana. PNAS 117:3521785–95
     [Google Scholar]
  7. 7.
    Boccaletto P, Stefaniak F, Ray A, Cappannini A, Mukherjee S et al. 2022. MODOMICS: a database of RNA modification pathways. 2021 update. Nucleic Acids Res. 50:D1D231–35
     [Google Scholar]
  8. 8.
    Bodi Z, Fray RG. 2017. Detection and quantification of N6-methyladenosine in messenger RNA by TLC. Methods Mol. Biol. 1562:79–87
     [Google Scholar]
  9. 9.
    Bodi Z, Zhong S, Mehra S, Song J, Graham N et al. 2012. Adenosine methylation in Arabidopsis mRNA is associated with the 3′ end and reduced levels cause developmental defects. Front. Plant Sci. 3:48
     [Google Scholar]
  10. 10.
    Burgess AL, David R, Searle IR 2015. Conservation of tRNA and rRNA 5-methylcytosine in the kingdom Plantae. BMC Plant Biol. 15:199
     [Google Scholar]
  11. 11.
    Camper SA, Albers RJ, Coward JK, Rottman FM. 1984. Effect of undermethylation on mRNA cytoplasmic appearance and half-life. Mol. Cell. Biol. 4:3538–43
     [Google Scholar]
  12. 12.
    Cantara WA, Crain PF, Rozenski J, McCloskey JA, Harris KA et al. 2011. The RNA modification database, RNAMDB: 2011 update. Nucleic Acids Res. 39:Database issueD195–201
     [Google Scholar]
  13. 13.
    Carlile TM, Martinez NM, Schaening C, Su A, Bell TA et al. 2019. mRNA structure determines modification by pseudouridine synthase 1. Nat. Chem. Biol. 15:10966–74
     [Google Scholar]
  14. 14.
    Chen P, Jäger G, Zheng B. 2010. Transfer RNA modifications and genes for modifying enzymes in Arabidopsis thaliana. BMC Plant Biol. 10:201
     [Google Scholar]
  15. 15.
    Chen YG, Kowtoniuk WE, Agarwal I, Shen Y, Liu DR. 2009. LC/MS analysis of cellular RNA reveals NAD-linked RNA. Nat. Chem. Biol. 5:12879–81
     [Google Scholar]
  16. 16.
    Cheng P, Bao S, Li C, Tong J, Shen L, Yu H. 2022. RNA N6-methyladenosine modification promotes auxin biosynthesis required for male meiosis in rice. Dev. Cell 57:2246–59.e4
     [Google Scholar]
  17. 17.
    Cognat V, Pawlak G, Duchêne A-M, Daujat M, Gigant A et al. 2013. PlantRNA, a database for tRNAs of photosynthetic eukaryotes. Nucleic Acids Res. 41:Database issueD273–79
     [Google Scholar]
  18. 18.
    Cui X, Liang Z, Shen L, Zhang Q, Bao S et al. 2017. 5-Methylcytosine RNA methylation in Arabidopsis thaliana. Mol. Plant 10:111387–99
     [Google Scholar]
  19. 19.
    Dai X, Wang T, Gonzalez G, Wang Y. 2018. Identification of YTH domain-containing proteins as the readers for N1-methyladenosine in RNA. Anal. Chem. 90:116380–84
     [Google Scholar]
  20. 20.
    Dannfald A, Favory J-J, Deragon J-M. 2021. Variations in transfer and ribosomal RNA epitranscriptomic status can adapt eukaryote translation to changing physiological and environmental conditions. RNA Biol. 18:Suppl. 14–18
     [Google Scholar]
  21. 21.
    David R, Burgess A, Parker B, Li J, Pulsford K et al. 2017. Transcriptome-wide mapping of RNA 5-methylcytosine in Arabidopsis mRNAs and noncoding RNAs. Plant Cell 29:3445–60
     [Google Scholar]
  22. 22.
    Davis FF, Allen FW. 1957. Ribonucleic acids from yeast which contain a fifth nucleotide. J. Biol. Chem. 227:2907–15
     [Google Scholar]
  23. 23.
    Desrosiers R, Friderici K, Rottman F. 1974. Identification of methylated nucleosides in messenger RNA from Novikoff hepatoma cells. PNAS 71:103971–75
     [Google Scholar]
  24. 24.
    Dominissini D, Moshitch-Moshkovitz S, Schwartz S, Salmon-Divon M, Ungar L et al. 2012. Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 485:7397201–6
     [Google Scholar]
  25. 25.
    Dominissini D, Nachtergaele S, Moshitch-Moshkovitz S, Peer E, Kol N et al. 2016. The dynamic N1-methyladenosine methylome in eukaryotic messenger RNA. Nature 530:7591441–46
     [Google Scholar]
  26. 26.
    Du H, Zhao Y, He J, Zhang Y, Xi H et al. 2016. YTHDF2 destabilizes m6A-containing RNA through direct recruitment of the CCR4-NOT deadenylase complex. Nat. Commun. 7:12626
     [Google Scholar]
  27. 27.
    Duan H-C, Wei L-H, Zhang C, Wang Y, Chen L et al. 2017. ALKBH10B is an RNA N6-methyladenosine demethylase affecting Arabidopsis floral transition. Plant Cell 29:122995–3011
     [Google Scholar]
  28. 28.
    Eickbush TH, Eickbush DG. 2007. Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics 175:2477–85
     [Google Scholar]
  29. 29.
    Enroth C, Poulsen LD, Iversen S, Kirpekar F, Albrechtsen A, Vinther J. 2019. Detection of internal N7-methylguanosine m7G RNA modifications by mutational profiling sequencing. Nucleic Acids Res. 47:20e126
     [Google Scholar]
  30. 30.
    Frye M, Harada BT, Behm M, He C. 2018. RNA modifications modulate gene expression during development. Science 361:64091346–49
     [Google Scholar]
  31. 31.
    Furuichi Y. 2015. Discovery of m7G-cap in eukaryotic mRNAs. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 91:8394–409
     [Google Scholar]
  32. 32.
    Furuichi Y, Morgan M, Muthukrishnan S, Shatkin AJ. 1975. Reovirus messenger RNA contains a methylated, blocked 5′-terminal structure: m-7G(5′)ppp(5′)G-MpCp-. PNAS 72:1362–66
     [Google Scholar]
  33. 33.
    Furuichi Y, Morgan M, Shatkin AJ, Jelinek W, Salditt-Georgieff M, Darnell JE. 1975. Methylated, blocked 5 termini in HeLa cell mRNA. PNAS 72:51904–8
     [Google Scholar]
  34. 34.
    Gao Y, Liu X, Wu B, Wang H, Xi F et al. 2021. Quantitative profiling of N6-methyladenosine at single-base resolution in stem-differentiating xylem of Populus trichocarpa using Nanopore direct RNA sequencing. Genome Biol. 22:122
     [Google Scholar]
  35. 35.
    Garalde DR, Snell EA, Jachimowicz D, Sipos B, Lloyd JH et al. 2018. Highly parallel direct RNA sequencing on an array of nanopores. Nat. Methods 15:3201–6
     [Google Scholar]
  36. 36.
    Garcia-Campos MA, Edelheit S, Toth U, Safra M, Shachar R et al. 2019. Deciphering the “m6A Code” via antibody-independent quantitative profiling. Cell 178:3731–47.e16
     [Google Scholar]
  37. 37.
    Geula S, Moshitch-Moshkovitz S, Dominissini D, Mansour AA, Kol N et al. 2015. m6A mRNA methylation facilitates resolution of naïve pluripotency toward differentiation. Science 347:62251002–6
     [Google Scholar]
  38. 38.
    Govindan G, Sharma B, Li Y, Armstrong CD, Merum P et al. 2022. mRNA N6-methyladenosine is critical for cold tolerance in Arabidopsis. Plant J. 111:1052–68
     [Google Scholar]
  39. 39.
    Grosjean H. 2015. RNA modification: the Golden Period 1995–2015. RNA 21:4625–26
     [Google Scholar]
  40. 40.
    Grozhik AV, Olarerin-George AO, Sindelar M, Li X, Gross SS, Jaffrey SR. 2019. Antibody cross-reactivity accounts for widespread appearance of m1A in 5′ UTRs. Nat. Commun. 10:15126
     [Google Scholar]
  41. 41.
    Gu C, Begley TJ, Dedon PC. 2014. tRNA modifications regulate translation during cellular stress. FEBS Lett. 588:234287–96
     [Google Scholar]
  42. 42.
    Guo Q, Ng PQ, Shi S, Fan D, Li J et al. 2019. Arabidopsis TRM5 encodes a nuclear-localised bifunctional tRNA guanine and inosine-N1-methyltransferase that is important for growth. PLOS ONE 14:11e0225064
     [Google Scholar]
  43. 43.
    Guo T, Liu C, Meng F, Hu L, Fu X et al. 2022. The m6A reader MhYTP2 regulates MdMLO19 mRNA stability and antioxidant genes translation efficiency conferring powdery mildew resistance in apple. Plant Biotechnol. J. 20:511–25
     [Google Scholar]
  44. 44.
    Han C, Zhang F, Qiao X, Zhao Y, Qiao Q et al. 2022. Multi-omics analysis reveals the dynamic changes of RNA N6-methyladenosine in pear (Pyrus bretschneideri) defense responses to Erwinia amylovora pathogen infection. Front. Microbiol. 12:803512
     [Google Scholar]
  45. 45.
    He Y, Li L, Yao Y, Li Y, Zhang H, Fan M 2021. Transcriptome-wide N6-methyladenosine (m6A) methylation in watermelon under CGMMV infection. BMC Plant Biol. 21:516
     [Google Scholar]
  46. 46.
    Hou Y, Sun J, Wu B, Gao Y, Nie H et al. 2021. CPSF30-L-mediated recognition of mRNA m6A modification controls alternative polyadenylation of nitrate signaling-related gene transcripts in Arabidopsis. Mol. Plant 14:4688–99
     [Google Scholar]
  47. 47.
    Hu J, Cai J, Park SJ, Lee K, Li Y et al. 2021. N6-Methyladenosine mRNA methylation is important for salt stress tolerance in Arabidopsis. Plant J. 106:61759–75
     [Google Scholar]
  48. 48.
    Hu J, Cai J, Umme A, Chen Y, Xu T, Kang H. 2022. Unique features of mRNA m6A methylomes during expansion of tomato (Solanum lycopersicum) fruits. Plant Physiol. 188:2215–27
     [Google Scholar]
  49. 49.
    Imanishi M, Tsuji S, Suda A, Futaki S. 2017. Detection of N6-methyladenosine based on the methyl-sensitivity of MazF RNA endonuclease. Chem. Commun. 53:9612930–33
     [Google Scholar]
  50. 50.
    Janssen KA, Xie Y, Kramer MC, Gregory BD, Garcia BA. 2022. Data-independent acquisition for the detection of mononucleoside RNA modifications by mass spectrometry. J. Am. Soc. Mass. Spectrom. 33:5885–93
     [Google Scholar]
  51. 51.
    Jiao X, Doamekpor SK, Bird JG, Nickels BE, Tong L et al. 2017. 5′ end nicotinamide adenine dinucleotide cap in human cells promotes RNA decay through DXO-mediated deNADding. Cell 168:61015–27.e10
     [Google Scholar]
  52. 52.
    Jin X, Lv Z, Gao J, Zhang R, Zheng T et al. 2019. AtTrm5a catalyses 1-methylguanosine and 1-methylinosine formation on tRNAs and is important for vegetative and reproductive growth in Arabidopsis thaliana. Nucleic Acids Res. 47:2883–98
     [Google Scholar]
  53. 53.
    Ke S, Alemu EA, Mertens C, Gantman EC, Fak JJ et al. 2015. A majority of m6A residues are in the last exons, allowing the potential for 3′ UTR regulation. Genes Dev. 29:192037–53
     [Google Scholar]
  54. 54.
    Kramer MC, Anderson SJ, Gregory BD. 2018. The nucleotides they are a-changin’: function of RNA binding proteins in post-transcriptional messenger RNA editing and modification in Arabidopsis. Curr. Opin. Plant Biol. 45:88–95
     [Google Scholar]
  55. 55.
    Kramer MC, Janssen KA, Palos K, Nelson ADL, Vandivier LE et al. 2020. N6-methyladenosine and RNA secondary structure affect transcript stability and protein abundance during systemic salt stress in Arabidopsis. Plant Direct 4:7e00239
     [Google Scholar]
  56. 56.
    Krogh N, Asmar F, Côme C, Munch-Petersen HF, Grønbæk K, Nielsen H. 2020. Profiling of ribose methylations in ribosomal RNA from diffuse large B-cell lymphoma patients for evaluation of ribosomes as drug targets. NAR Cancer 2:4zcaa035
     [Google Scholar]
  57. 57.
    Kullolli M, Knouf E, Arampatzidou M, Tewari M, Pitteri SJ. 2014. Intact microRNA analysis using high resolution mass spectrometry. J. Am. Soc. Mass Spectrom. 25:180–87
     [Google Scholar]
  58. 58.
    Lauman R, Garcia BA. 2020. Unraveling the RNA modification code with mass spectrometry. Mol. Omics 16:4305–15
     [Google Scholar]
  59. 59.
    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 Biol. 11:91180–88
     [Google Scholar]
  60. 60.
    Liang Z, Riaz A, Chachar S, Ding Y, Du H, Gu X. 2020. Epigenetic modifications of mRNA and DNA in plants. Mol. Plant 13:114–30
     [Google Scholar]
  61. 61.
    Linder B, Grozhik AV, Olarerin-George AO, Meydan C, Mason CE, Jaffrey SR. 2015. Single-nucleotide-resolution mapping of m6A and m6Am throughout the transcriptome. Nat. Methods 12:8767–72
     [Google Scholar]
  62. 62.
    Liu F, Clark W, Luo G, Wang X, Fu Y et al. 2016. ALKBH1-mediated tRNA demethylation regulates translation. Cell 167:3816–28.e16
     [Google Scholar]
  63. 63.
    Liu F, Marquardt S, Lister C, Swiezewski S, Dean C. 2010. Targeted 3′ processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327:596194–97
     [Google Scholar]
  64. 64.
    Liu H, Begik O, Lucas MC, Ramirez JM, Mason CE et al. 2019. Accurate detection of m6A RNA modifications in native RNA sequences. Nat. Commun. 10:14079
     [Google Scholar]
  65. 65.
    Liu N, Parisien M, Dai Q, Zheng G, He C, Pan T. 2013. Probing N6-methyladenosine RNA modification status at single nucleotide resolution in mRNA and long noncoding RNA. RNA 19:121848–56
     [Google Scholar]
  66. 66.
    Lu L, Zhang Y, He Q, Qi Z, Zhang G et al. 2020. MTA, an RNA m6A methyltransferase, enhances drought tolerance by regulating the development of trichomes and roots in poplar. Int. J. Mol. Sci. 21:72462
     [Google Scholar]
  67. 67.
    Luo J-H, Wang M, Jia G-F, He Y. 2021. Transcriptome-wide analysis of epitranscriptome and translational efficiency associated with heterosis in maize. J. Exp. Bot. 72:2933–46
     [Google Scholar]
  68. 68.
    Luo J-H, Wang Y, Wang M, Zhang L-Y, Peng H-R et al. 2020. Natural variation in RNA m6A methylation and its relationship with translational status. Plant Physiol. 182:1332–44
     [Google Scholar]
  69. 69.
    Malbec L, Zhang T, Chen Y-S, Zhang Y, Sun B-F et al. 2019. Dynamic methylome of internal mRNA N7-methylguanosine and its regulatory role in translation. Cell Res. 29:11927–41
     [Google Scholar]
  70. 70.
    Mao X, Hou N, Liu Z, He J. 2022. Profiling of N6-methyladenosine (m6A) modification landscape in response to drought stress in apple (Malus prunifolia (Willd.) Borkh). Plants 11:103
     [Google Scholar]
  71. 71.
    Martínez-Pérez M, Aparicio F, López-Gresa MP, Bellés JM, Sánchez-Navarro JA, Pallás V. 2017. Arabidopsis m6A demethylase activity modulates viral infection of a plant virus and the m6A abundance in its genomic RNAs. PNAS 114:4010755–60
     [Google Scholar]
  72. 72.
    Martínez-Pérez M, Gómez-Mena C, Alvarado-Marchena L, Nadi R, Micol JL et al. 2021. The m6A RNA demethylase ALKBH9B plays a critical role for vascular movement of alfalfa mosaic virus in Arabidopsis. Front. Microbiol. 12:745576
     [Google Scholar]
  73. 73.
    Meyer KD, Patil DP, Zhou J, Zinoviev A, Skabkin MA et al. 2015. 5′ UTR m6A promotes cap-independent translation. Cell 163:4999–1010
     [Google Scholar]
  74. 74.
    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 149:71635–46
     [Google Scholar]
  75. 75.
    Miao Z, Zhang T, Xie B, Qi Y, Ma C. 2022. Evolutionary implications of the RNA N6-methyladenosine methylome in plants. Mol. Biol. Evol. 39:msab299
     [Google Scholar]
  76. 76.
    Monaco PL, Marcel V, Diaz J-J, Catez F. 2018. 2′-O-Methylation of ribosomal RNA: towards an epitranscriptomic control of translation?. Biomolecules 8:4106
     [Google Scholar]
  77. 77.
    Motorin Y, Helm M. 2010. tRNA stabilization by modified nucleotides. Biochemistry 49:244934–44
     [Google Scholar]
  78. 78.
    Ngoc LNT, Park SJ, Cai J, Huong TT, Lee K, Kang H. 2021. RsmD, a chloroplast rRNA m2G methyltransferase, plays a role in cold stress tolerance by possibly affecting chloroplast translation in Arabidopsis. Plant Cell Physiol. 62:6948–58
     [Google Scholar]
  79. 79.
    Niu Y, Zheng Y, Zhu H, Zhao H, Nie K et al. 2022. The Arabidopsis mitochondrial pseudouridine synthase homolog FCS1 plays critical roles in plant development. Plant Cell Physiol. 63:955–66
     [Google Scholar]
  80. 80.
    Park OH, Ha H, Lee Y, Boo SH, Kwon DH et al. 2019. Endoribonucleolytic cleavage of m6A-containing RNAs by RNase P/MRP complex. Mol. Cell 74:3494–507.e8
     [Google Scholar]
  81. 81.
    Parker MT, Knop K, Sherwood AV, Schurch NJ, Mackinnon K et al. 2020. Nanopore direct RNA sequencing maps the complexity of Arabidopsis mRNA processing and m6A modification. eLife 9:e49658
     [Google Scholar]
  82. 82.
    Patil DP, Chen C-K, Pickering BF, Chow A, Jackson C et al. 2016. m6A RNA methylation promotes XIST-mediated transcriptional repression. Nature 537:7620369–73
     [Google Scholar]
  83. 83.
    Pereira M, Francisco S, Varanda AS, Santos M, Santos MAS, Soares AR. 2018. Impact of tRNA modifications and tRNA-modifying enzymes on proteostasis and human disease. Int. J. Mol. Sci. 19:123738
     [Google Scholar]
  84. 84.
    Qin H, Ou L, Gao J, Chen L, Wang J-W et al. 2022. DENA: training an authentic neural network model using Nanopore sequencing data of Arabidopsis transcripts for detection and quantification of N6-methyladenosine on RNA. Genome Biol. 23:25
     [Google Scholar]
  85. 85.
    Rahman R, Xu W, Jin H, Rosbash M 2018. Identification of RNA-binding protein targets with HyperTRIBE. Nat. Protoc. 13:81829–49
     [Google Scholar]
  86. 86.
    Reichel M, Köster T, Staiger D. 2019. Marking RNA: m6A writers, readers, and functions in Arabidopsis. J. Mol. Cell Biol. 11:10899–910
     [Google Scholar]
  87. 87.
    Roundtree IA, Evans ME, Pan T, He C. 2017. Dynamic RNA modifications in gene expression regulation. Cell 169:71187–200
     [Google Scholar]
  88. 88.
    Růžička K, Zhang M, Campilho A, Bodi Z, Kashif M et al. 2017. Identification of factors required for m6A mRNA methylation in Arabidopsis reveals a role for the conserved E3 ubiquitin ligase HAKAI. New Phytol. 215:1157–72
     [Google Scholar]
  89. 89.
    Ryvkin P, Leung YY, Silverman IM, Childress M, Valladares O et al. 2013. HAMR: high-throughput annotation of modified ribonucleotides. RNA 19:121684–92
     [Google Scholar]
  90. 90.
    Scutenaire J, Deragon J-M, Jean V, Benhamed M, Raynaud C et al. 2018. The YTH domain protein ECT2 Is an m6A reader required for normal trichome branching in Arabidopsis. Plant Cell 30:5986–1005
     [Google Scholar]
  91. 91.
    Seo KW, Kleiner RE. 2020. YTHDF2 recognition of N1-methyladenosine (m1A)-modified RNA is associated with transcript destabilization. ACS Chem. Biol. 15:1132–39
     [Google Scholar]
  92. 92.
    Shen L, Liang Z, Gu X, Chen Y, Teo ZWN et al. 2016. N6-Methyladenosine RNA modification regulates shoot stem cell fate in Arabidopsis. Dev. Cell. 38:2186–200
     [Google Scholar]
  93. 93.
    Shim S, Lee HG, Lee H, Seo PJ. 2020. H3K36me2 is highly correlated with m6A modifications in plants. J. Integr. Plant Biol. 62:101455–60
     [Google Scholar]
  94. 94.
    Slobodin B, Han R, Calderone V, Vrielink JAFO, Loayza-Puch F et al. 2017. Transcription impacts the efficiency of mRNA translation via co-transcriptional N6-adenosine methylation. Cell 169:2326–37.e12
     [Google Scholar]
  95. 95.
    Smith CM, Steitz JA. 1997. Sno storm in the nucleolus: new roles for myriad small RNPs. Cell 89:5669–72
     [Google Scholar]
  96. 96.
    Song J, Zhai J, Bian E, Song Y, Yu J, Ma C 2018. Transcriptome-wide annotation of m5C RNA modifications using machine learning. Front. Plant Sci. 9:519
     [Google Scholar]
  97. 97.
    Song P, Yang J, Wang C, Lu Q, Shi L et al. 2021. Arabidopsis N6-methyladenosine reader CPSF30-L recognizes FUE signals to control polyadenylation site choice in liquid-like nuclear bodies. Mol. Plant 14:4571–87
     [Google Scholar]
  98. 98.
    Su T, Fu L, Kuang L, Chen D, Zhang G et al. 2022. Transcriptome-wide m6A methylation profile reveals regulatory networks in roots of barley under cadmium stress. J. Haz. Mater. 423:127140
     [Google Scholar]
  99. 99.
    Sun L, Xu Y, Bai S, Bai X, Zhu H et al. 2019. Transcriptome-wide analysis of pseudouridylation of mRNA and non-coding RNAs in Arabidopsis. J. Exp. Bot. 70:195089–600
     [Google Scholar]
  100. 100.
    Tang J, Jia P, Xin P, Chu J, Shi D-Q, Yang W-C. 2020. The Arabidopsis TRM61/TRM6 complex is a bona fide tRNA N1-methyladenosine methyltransferase. J. Exp. Bot. 71:103024–36
     [Google Scholar]
  101. 101.
    Tang X-M, Ye T-T, You X-J, Yin X-M, Ding J-H et al. 2023. Mass spectrometry profiling analysis enables the identification of new modifications in ribosomal RNA. Chinese Chem. Lett. 34:107531
     [Google Scholar]
  102. 102.
    Tang Y, Gao C-C, Gao Y, Yang Y, Shi B et al. 2020. OsNSUN2-mediated 5-methylcytosine mRNA modification enhances rice adaptation to high temperature. Dev. Cell 53:3272–86.e7
     [Google Scholar]
  103. 103.
    Thomas NK, Poodari VC, Jain M, Olsen HE, Akeson M, Abu-Shumays RL. 2021. Direct nanopore sequencing of individual full length tRNA strands. ACS Nano 15:1016642–53
     [Google Scholar]
  104. 104.
    Tieu Ngoc LN, Jung Park S, Thi Huong T, Lee KH, Kang H 2021. N4-methylcytidine ribosomal RNA methylation in chloroplasts is crucial for chloroplast function, development, and abscisic acid response in Arabidopsis. J. Integr. Plant Biol. 63:3570–82
     [Google Scholar]
  105. 105.
    Vandivier LE, Campos R, Kuksa PP, Silverman IM, Wang L-S, Gregory BD. 2015. Chemical modifications mark alternatively spliced and uncapped messenger RNAs in Arabidopsis. Plant Cell 27:113024–37
     [Google Scholar]
  106. 106.
    Walters RW, Matheny T, Mizoue LS, Rao BS, Muhlrad D, Parker R. 2017. Identification of NAD+ capped mRNAs in Saccharomyces cerevisiae. PNAS 114:3480–85
     [Google Scholar]
  107. 107.
    Wang C, Yang J, Song P, Zhang W, Lu Q et al. 2022. FIONA1 is an RNA N6-methyladenosine methyltransferase affecting Arabidopsis photomorphogenesis and flowering. Genome Biol. 23:140
     [Google Scholar]
  108. 108.
    Wang T, Li X, Zhang X, Wang Q, Liu W et al. 2021. RNA motifs and modification involve in RNA long-distance transport in plants. Front. Cell Dev. Biol. 9:651278
     [Google Scholar]
  109. 109.
    Wang X, Lu Z, Gomez A, Hon GC, Yue Y et al. 2014. N6-methyladenosine-dependent regulation of messenger RNA stability. Nature 505:7481117–20
     [Google Scholar]
  110. 110.
    Wang X, Zhao BS, Roundtree IA, Lu Z, Han D et al. 2015. N6-Methyladenosine modulates messenger RNA translation efficiency. Cell 161:61388–99
     [Google Scholar]
  111. 111.
    Wang Y, Du F, Li Y, Wang J, Zhao X et al. 2022. Global N6-methyladenosine profiling revealed the tissue-specific epitranscriptomic regulation of rice responses to salt stress. Int. J. Mol. Sci. 23:2091
     [Google Scholar]
  112. 112.
    Wang Y, Li D, Gao J, Li X, Zhang R et al. 2017. The 2′-O-methyladenosine nucleoside modification gene OsTRM13 positively regulates salt stress tolerance in rice. J. Exp. Bot. 68:71479–91
     [Google Scholar]
  113. 113.
    Wang Y, Li S, Zhao Y, You C, Le B et al. 2019. NAD+-capped RNAs are widespread in the Arabidopsis transcriptome and can probably be translated. PNAS 116:2412094–102
     [Google Scholar]
  114. 114.
    Wang Y, Pang C, Li X, Hu Z, Lv Z et al. 2017. Identification of tRNA nucleoside modification genes critical for stress response and development in rice and Arabidopsis. BMC Plant Biol. 17:1261
     [Google Scholar]
  115. 115.
    Wang Y, Wang H, Xi F, Wang H, Han X et al. 2020. Profiling of circular RNA N6-methyladenosine in moso bamboo (Phyllostachys edulis) using nanopore-based direct RNA sequencing. J. Integr. Plant Biol. 62:121823–38
     [Google Scholar]
  116. 116.
    Warda AS, Kretschmer J, Hackert P, Lenz C, Urlaub H et al. 2017. Human METTL16 is a N6-methyladenosine (m6A) methyltransferase that targets pre-mRNAs and various non-coding RNAs. EMBO Rep. 18:112004–14
     [Google Scholar]
  117. 117.
    Wei L-H, Song P, Wang Y, Lu Z, Tang Q et al. 2018. The m6A reader ECT2 controls trichome morphology by affecting mRNA stability in Arabidopsis. Plant Cell 30:5968–85
     [Google Scholar]
  118. 118.
    Wein S, Andrews B, Sachsenberg T, Santos-Rosa H, Kohlbacher O et al. 2020. A computational platform for high-throughput analysis of RNA sequences and modifications by mass spectrometry. Nat. Commun. 11:1926
     [Google Scholar]
  119. 119.
    Wu S, Wang Y, Wang J, Li X, Li J, Ye K. 2021. Profiling of RNA ribose methylation in Arabidopsis thaliana. Nucleic Acids Res. 49:74104–19
     [Google Scholar]
  120. 120.
    Xie Y, Gu Y, Shi G, He J, Hu W, Zhang Z. 2022. Genome-wide identification and expression analysis of pseudouridine synthase family in Arabidopsis and maize. Int. J. Mol. Sci. 23:52680
     [Google Scholar]
  121. 121.
    Xu C, Wu Z, Duan H-C, Fang X, Jia G, Dean C. 2021. R-loop resolution promotes co-transcriptional chromatin silencing. Nat. Commun. 12:11790
     [Google Scholar]
  122. 122.
    Xu T, Wu X, Wong CE, Fan S, Zhang Y et al. 2022. FIONA1-mediated m6A modification regulates the floral transition in Arabidopsis. Adv. Sci. 9:2103628
     [Google Scholar]
  123. 123.
    Xuan J-J, Sun W-J, Lin P-H, Zhou K-R, Liu S et al. 2018. RMBase v2.0: deciphering the map of RNA modifications from epitranscriptome sequencing data. Nucleic Acids Res. 46:D1D327–34
     [Google Scholar]
  124. 124.
    Yang D, Xu H, Liu Y, Li M, Ali M et al. 2021. RNA N6-methyladenosine responds to low-temperature stress in tomato anthers. Front. Plant Sci. 12:687826
     [Google Scholar]
  125. 125.
    Yang L, Perrera V, Saplaoura E, Apelt F, Bahin M et al. 2019. m5C Methylation guides systemic transport of messenger RNA over graft junctions in plants. Curr. Biol. 29:152465–76.e5
     [Google Scholar]
  126. 126.
    Yang W, Meng J, Liu J, Ding B, Tan T et al. 2020. The N1-methyladenosine methylome of petunia mRNA. Plant Physiol. 183:41710–24
     [Google Scholar]
  127. 127.
    Yin S, Ao Q, Tan C, Yang Y. 2021. Genome-wide identification and characterization of YTH domain-containing genes, encoding the m6A readers, and their expression in tomato. Plant Cell Rep. 40:71229–45
     [Google Scholar]
  128. 128.
    Yu B, Bi L, Zhai J, Agarwal M, Li S et al. 2010. siRNAs compete with miRNAs for methylation by HEN1 in Arabidopsis. Nucleic Acids Res. 38:175844–50
     [Google Scholar]
  129. 129.
    Yu F, Liu X, Alsheikh M, Park S, Rodermel S. 2008. Mutations in SUPPRESSOR OF VARIEGATION1, a factor required for normal chloroplast translation, suppress var2-mediated leaf variegation in Arabidopsis. Plant Cell 20:71786–804
     [Google Scholar]
  130. 130.
    Yu X, Sharma B, Gregory BD. 2021. The impact of epitranscriptomic marks on post-transcriptional regulation in plants. Brief Funct. Genom. 20:2113–24
     [Google Scholar]
  131. 131.
    Yu X, Willmann MR, Vandivier LE, Trefely S, Kramer MC et al. 2021. Messenger RNA 5′ NAD+ capping is a dynamic regulatory epitranscriptome mark that is required for proper response to abscisic acid in Arabidopsis. Dev. Cell 56:1125–40.e6
     [Google Scholar]
  132. 132.
    Zhang G, Lv Z, Diao S, Liu H, Duan A et al. 2021. Unique features of the m6A methylome and its response to drought stress in sea buckthorn (Hippophae rhamnoides Linn.). RNA Biol. 18:sup2794–803
     [Google Scholar]
  133. 133.
    Zhang H, Zhong H, Zhang S, Shao X, Ni M et al. 2019. NAD tagSeq reveals that NAD+-capped RNAs are mostly produced from a large number of protein-coding genes in Arabidopsis. PNAS 116:2412072–77
     [Google Scholar]
  134. 134.
    Zhang L-S, Liu C, Ma H, Dai Q, Sun H-L et al. 2019. Transcriptome-wide mapping of internal N7-methylguanosine methylome in mammalian mRNA. Mol. Cell 74:61304–16.e8
     [Google Scholar]
  135. 135.
    Zhang M, Bodi Z, Mackinnon K, Zhong S, Archer N et al. 2022. Two zinc finger proteins with functions in m6A writing interact with HAKAI. Nat. Commun. 13:1127
     [Google Scholar]
  136. 136.
    Zhang T-Y, Wang Z-Q, Hu H-C, Chen Z-Q, Liu P et al. 2021. 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. 12:656302
     [Google Scholar]
  137. 137.
    Zhang Z, Chen L-Q, Zhao Y-L, Yang C-G, Roundtree IA et al. 2019. Single-base mapping of m6A by an antibody-independent method. Sci. Adv. 5:7eaax0250
     [Google Scholar]
  138. 138.
    Zheng H, Sun X, Li J, Song Y, Wang F 2021. Analysis of N6-methyladenosine reveals a new important mechanism regulating the salt tolerance of sweet sorghum. Plant Sci. 304:110801
     [Google Scholar]
  139. 139.
    Zhong S, Li H, Bodi Z, Button J, Vespa L et al. 2008. MTA is an Arabidopsis messenger RNA adenosine methylase and interacts with a homolog of a sex-specific splicing factor. Plant Cell 20:51278–88
     [Google Scholar]
  140. 140.
    Zhou L, Tang R, Li X, Tian S, Li B, Qin G. 2021. N6-methyladenosine RNA modification regulates strawberry fruit ripening in an ABA-dependent manner. Genome Biol. 22:168
     [Google Scholar]
  141. 141.
    Zhou L, Tian S, Qin G. 2019. RNA methylomes reveal the m6A-mediated regulation of DNA demethylase gene SlDML2 in tomato fruit ripening. Genome Biol. 20:1156
     [Google Scholar]
/content/journals/10.1146/annurev-arplant-071122-085813
Loading
The Diversity and Functions of Plant RNA Modifications: What We Know and Where We Go from Here
Annual Review of Plant Biology 74, 53 (2023); https://doi.org/10.1146/annurev-arplant-071122-085813
/content/journals/10.1146/annurev-arplant-071122-085813
/content/journals/10.1146/annurev-arplant-071122-085813
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error