Advances in Methylation and Acetylation Modification of RNA in Plant Growth and Development

doi:10.13560/j.cnki.biotech.bull.1985.2024-0327

Abstract

Abstract:

RNA modification is an important type of epigenetic modification, which refers to the addition of chemical modifying groups to the bases or ribose of RNA molecules, and can occur in a variety of RNAs, such as messenger RNAs（mRNAs）, transfer RNAs（tRNAs）, ribosomal RNAs（rRNAs）, and cyclic RNAs（circRNAs）, etc. RNA methylation and acetylation are two of the key types of modifications that perform important biological functions by regulating the genetic information of organisms. Both modifications are dynamically and reversibly regulated by three types of regulators, namely writers, erasers and readers, which have a crucial impact on different RNA metabolic processes such as RNA splicing, translocation, translation, transport and degradation. In recent years, with the development of RNA modification detection technologies, numerous studies have identified new RNA modification sites in plants and confirmed that methylation and acetylation modifications of RNAs play key roles in plant growth and development as well as in response to biotic and abiotic stresses. This paper firstly outlines the types of RNA modifications and their biological properties, and on this basis focuses on reviewing the research progress on RNA methylation and acetylation regulators in recent years, and finally summarizes the functions of RNA methylation and acetylation in plant growth and development and in response to stresses, and looks forward to some new research directions for RNA modifications in plants, with a view to providing theoretical basis and new ideas for further research related to RNA methylation and acetylation modification in plants.

Key words: RNA modification, methylation, acetylation, biotic stress, abiotic stress

ZHANG Yan-yan, LU Du-xian, ZUO Xin-xiu, LI Yan-jun, LIN Jin-xing, CUI Ya-ning. Advances in Methylation and Acetylation Modification of RNA in Plant Growth and Development[J]. Biotechnology Bulletin, 2024, 40(10): 108-121.

Figures/Tables 5

References 99

[1]	Waddington CH. The epigenotype[J]. Endeavour, 1942, 1: 18-20.
[2]	Hotchkiss RD. The quantitative separation of purines, pyrimidines, and nucleosides by paper chromatography[J]. J Biol Chem, 1948, 175(1): 315-332. pmid: 18873306
[3]	Zhang L, Xu XN, Su XL. Modifications of noncoding RNAs in cancer and their therapeutic implications[J]. Cell Signal, 2023, 108: 110726.
[4]	Liu YB, Liu SZ, Yan L, et al. Contribution of m⁵C RNA modification-related genes to prognosis and immunotherapy prediction in patients with ovarian cancer[J]. Mediators Inflamm, 2023, 2023: 1400267.
[5]	Desrosiers R, Friderici K, Rottman F. Identification of methylated nucleosides in messenger RNA from Novikoff hepatoma cells[J]. Proc Natl Acad Sci USA, 1974, 71(10): 3971-3975. doi: 10.1073/pnas.71.10.3971 pmid: 4372599
[6]	Zhong SL, Li HY, Bodi Z, et al. MTA is an Arabidopsis messenger RNA adenosine methylase and interacts with a homolog of a sex-specific splicing factor[J]. Plant Cell, 2008, 20(5): 1278-1288.
[7]	Nichols JL, Welder L. A modified nucleotide in the poly(A)tract of maize RNA[J]. Biochim Biophys Acta, 1981, 652(1): 99-108. pmid: 6163465
[8]	Kennedy TD, Lane BG. Wheat embryo ribonucleates. XIII. Methyl-substituted nucleoside constituents and 5'-terminal dinucleotide sequences in bulk poly(AR)-rich RNA from imbibing wheat embryos[J]. Can J Biochem, 1979, 57(6): 927-931. pmid: 476526
[9]	Jiang XL, Liu BY, Nie Z, et al. The role of m⁶A modification in the biological functions and diseases[J]. Signal Transduct Target Ther, 2021, 6(1): 74.
[10]	Ozanick S, Krecic A, Andersland J, et al. The bipartite structure of the tRNA m1A58 methyltransferase from S. cerevisiae is conserved in humans[J]. RNA, 2005, 11(8): 1281-1290. pmid: 16043508
[11]	Chujo T, Suzuki T. Trmt61B is a methyltransferase responsible for 1-methyladenosine at position 58 of human mitochondrial tRNAs[J]. RNA, 2012, 18(12): 2269-2276. doi: 10.1261/rna.035600.112 pmid: 23097428
[12]	Sprinzl M, Vassilenko KS. Compilation of tRNA sequences and sequences of tRNA genes[J]. Nucleic Acids Res, 2005, 33(Database issue): D139-D140.
[13]	Suzuki T, Yashiro Y, Kikuchi I, et al. Complete chemical structures of human mitochondrial tRNAs[J]. Nat Commun, 2020, 11(1): 4269. doi: 10.1038/s41467-020-18068-6 pmid: 32859890
[14]	Roovers M, Kaminska KH, Tkaczuk KL, et al. The YqfN protein of Bacillus subtilis is the tRNA: m1A22 methyltransferase(TrmK)[J]. Nucleic Acids Res, 2008, 36(10): 3252-3262.
[15]	Grosjean H, Auxilien S, Constantinesco F, et al. Enzymatic conversion of adenosine to inosine and to N1-methylinosine in transfer RNAs: a review[J]. Biochimie, 1996, 78(6): 488-501. pmid: 8915538
[16]	Sloan KE, Warda AS, Sharma S, et al. Tuning the ribosome: the influence of rRNA modification on eukaryotic ribosome biogenesis and function[J]. RNA Biol, 2017, 14(9): 1138-1152. doi: 10.1080/15476286.2016.1259781 pmid: 27911188
[17]	Dominissini D, Nachtergaele S, Moshitch-Moshkovitz S, et al. The dynamic N(1)-methyladenosine methylome in eukaryotic messenger RNA[J]. Nature, 2016, 530(7591): 441-446.
[18]	Li XY, Xiong XS, Wang K, et al. Transcriptome-wide mapping reveals reversible and dynamic N1-methyladenosine methylome[J]. Nat Chem Biol, 2016, 12: 311-316.
[19]	Squires JE, Preiss T. Function and detection of 5-methylcytosine in eukaryotic RNA[J]. Epigenomics, 2010, 2(5): 709-715. doi: 10.2217/epi.10.47 pmid: 22122054
[20]	Motorin Y, Helm M. tRNA stabilization by modified nucleotides[J]. Biochemistry, 2010, 49(24): 4934-4944. doi: 10.1021/bi100408z pmid: 20459084
[21]	Gigova A, Duggimpudi S, Pollex T, et al. A cluster of methylations in the domain IV of 25S rRNA is required for ribosome stability[J]. RNA, 2014, 20(10): 1632-1644. doi: 10.1261/rna.043398.113 pmid: 25125595
[22]	David R, Burgess A, Parker B, et al. Transcriptome-wide mapping of RNA 5-methylcytosine in Arabidopsis mRNAs and noncoding RNAs[J]. Plant Cell, 2017, 29(3): 445-460.
[23]	Cui XA, Liang Z, Shen LS, et al. 5-methylcytosine RNA methylation in Arabidopsis thaliana[J]. Mol Plant, 2017, 10(11): 1387-1399.
[24]	Cowling VH. Regulation of mRNA cap methylation[J]. Biochem J, 2009, 425(2): 295-302. doi: 10.1042/BJ20091352 pmid: 20025612
[25]	Chen C, Chao YH, Zhang CC, et al. TROP2 translation mediated by dual m⁶A/m⁷G RNA modifications promotes bladder cancer development[J]. Cancer Lett, 2023, 566: 216246.
[26]	Deng K, Li JX, Yang R, et al. Identification and validation of a novel prognostic model for gastric cancer based on m7G-related genes[J]. Transl Cancer Res, 2023, 12(7): 1836-1851. doi: 10.21037/tcr-22-2614 pmid: 37588749
[27]	Shi M, Zhu SS, Sun LY, et al. Transcriptome-wide dynamics of m⁷G-related LncRNAs during the progression from HBV infection to hepatocellular carcinoma[J]. Front Biosci(Landmark Ed), 2023, 28(12): 339.
[28]	Létoquart J, Huvelle E, Wacheul L, et al. Structural and functional studies of Bud23-Trm112 reveal 18S rRNA N7-G1575 methylation occurs on late 40S precursor ribosomes[J]. Proc Natl Acad Sci USA, 2014, 111(51): E5518-E5526.
[29]	Zhang LS, Liu C, Ma HH, et al. Transcriptome-wide mapping of internal N⁷-methylguanosine methylome in mammalian mRNA[J]. Mol Cell, 2019, 74(6): 1304-1316.e8. doi: S1097-2765(19)30265-5 pmid: 31031084
[30]	Oliva R, Cavallo L, Tramontano A. Accurate energies of hydrogen bonded nucleic acid base pairs and triplets in tRNA tertiary interactions[J]. Nucleic Acids Res, 2006, 34(3): 865-879. pmid: 16461956
[31]	Kowalski S, Yamane T, Fresco JR. Nucleotide sequence of the “denaturable” leucine transfer RNA from yeast[J]. Science, 1971, 172(3981): 385-387. pmid: 4927676
[32]	Tardu M, Jones JD, Kennedy RT, et al. Identification and quantification of modified nucleosides in Saccharomyces cerevisiae mRNAs[J]. ACS Chem Biol, 2019, 14(7): 1403-1409.
[33]	Ito S, Akamatsu Y, Noma A, et al. A single acetylation of 18 S rRNA is essential for biogenesis of the small ribosomal subunit in Saccharomyces cerevisiae[J]. J Biol Chem, 2014, 289(38): 26201-26212.
[34]	Taniguchi T, Miyauchi K, Sakaguchi Y, et al. Acetate-dependent tRNA acetylation required for decoding fidelity in protein synthesis[J]. Nat Chem Biol, 2018, 14(11): 1010-1020. doi: 10.1038/s41589-018-0119-z pmid: 30150682
[35]	Orita I, Futatsuishi R, Adachi K, et al. Random mutagenesis of a hyperthermophilic archaeon identified tRNA modifications associated with cellular hyperthermotolerance[J]. Nucleic Acids Res, 2019, 47(4): 1964-1976. doi: 10.1093/nar/gky1313 pmid: 30605516
[36]	Arango D, Sturgill D, Alhusaini N, et al. Acetylation of cytidine in mRNA promotes translation efficiency[J]. Cell, 2018, 175(7): 1872-1886.e24. doi: S0092-8674(18)31383-7 pmid: 30449621
[37]	Parthasarathy R, Ginell SL, De NC, et al. Conformation of N4-acetylcytidine, a modified nucleoside of tRNA, and stereochemistry of codon-anticodon interaction[J]. Biochem Biophys Res Commun, 1978, 83(2): 657-663.
[38]	Knuckles P, Lence T, Haussmann IU, et al. Zc3h13/Flacc is required for adenosine methylation by bridging the mRNA-binding factor Rbm15/Spenito to the m⁶A machinery component Wtap/Fl(2)D[J]. Genes Dev, 2018, 32(5-6): 415-429.
[39]	Patil DP, Chen CK, Pickering BF, et al. M(6)a RNA methylation promotes XIST-mediated transcriptional repression[J]. Nature, 2016, 537(7620): 369-373.
[40]	Pendleton KE, Chen BB, Liu KQ, et al. The U6 snRNA m⁶A methyltransferase METTL16 regulates SAM synthetase intron retention[J]. Cell, 2017, 169(5): 824-835.e14. doi: S0092-8674(17)30530-5 pmid: 28525753
[41]	Jia GF, Fu Y, Zhao X, et al. N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO[J]. Nat Chem Biol, 2011, 7(12): 885-887. doi: 10.1038/nchembio.687 pmid: 22002720
[42]	Zheng GQ, Dahl JA, Niu YM, et al. ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility[J]. Mol Cell, 2013, 49(1): 18-29. doi: 10.1016/j.molcel.2012.10.015 pmid: 23177736
[43]	Xu C, Wang X, Liu K, et al. Structural basis for selective binding of m⁶A RNA by the YTHDC1 YTH domain[J]. Nat Chem Biol, 2014, 10: 927-929. doi: 10.1038/nchembio.1654 pmid: 25242552
[44]	Liu N, Dai Q, Zheng GQ, et al. N(6)-methyladenosine-dependent RNA structural switches regulate RNA-protein interactions[J]. Nature, 2015, 518(7540): 560-564.
[45]	Liu N, Zhou KI, Parisien M, et al. N6-methyladenosine alters RNA structure to regulate binding of a low-complexity protein[J]. Nucleic Acids Res, 2017, 45(10): 6051-6063. doi: 10.1093/nar/gkx141 pmid: 28334903
[46]	Alarcón CR, Goodarzi H, Lee H, et al. HNRNPA2B1 is a mediator of m(6)A-dependent nuclear RNA processing events[J]. Cell, 2015, 162(6): 1299-1308. doi: 10.1016/j.cell.2015.08.011 pmid: 26321680
[47]	Huang HL, Weng HY, Sun WJ, et al. Recognition of RNA N⁶-methyladenosine by IGF2BP proteins enhances mRNA stability and translation[J]. Nat Cell Biol, 2018, 20(3): 285-295.
[48]	Edupuganti RR, Geiger S, Lindeboom RGH, et al. N⁶-methyladenosine(m⁶A)recruits and repels proteins to regulate mRNA homeostasis[J]. Nat Struct Mol Biol, 2017, 24(10): 870-878. doi: 10.1038/nsmb.3462 pmid: 28869609
[49]	Anderson J, Phan L, Hinnebusch AG. The Gcd10p/Gcd14p complex is the essential two-subunit tRNA(1-methyladenosine)methyltransferase of Saccharomyces cerevisiae[J]. Proc Natl Acad Sci USA, 2000, 97(10): 5173-5178. pmid: 10779558
[50]	Kadaba S, Krueger A, Trice T, et al. Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae[J]. Genes Dev, 2004, 18(11): 1227-1240.
[51]	Howell NW, Jora M, Jepson BF, et al. Distinct substrate specificities of the human tRNA methyltransferases TRMT10A and TRMT10B[J]. RNA, 2019, 25(10): 1366-1376. doi: 10.1261/rna.072090.119 pmid: 31292261
[52]	Xu BF, Liu DY, Wang ZR, et al. Multi-substrate selectivity based on key loops and non-homologous domains: new insight into ALKBH family[J]. Cell Mol Life Sci, 2021, 78(1): 129-141.
[53]	Motorin Y, Grosjean H. Multisite-specific tRNA: m⁵C-methyltransferase(Trm4)in yeast Saccharomyces cerevisiae: identification of the gene and substrate specificity of the enzyme[J]. RNA, 1999, 5(8): 1105-1118. pmid: 10445884
[54]	Gu WF, Hurto RL, Hopper AK, et al. Depletion of Saccharomyces cerevisiae tRNA(His)guanylyltransferase Thg1p leads to uncharged tRNAHis with additional m(5)C[J]. Mol Cell Biol, 2005, 25(18): 8191-8201.
[55]	Reid R, Greene PJ, Santi DV. Exposition of a family of RNA m⁵C methyltransferases from searching genomic and proteomic sequences[J]. Nucleic Acids Res, 1999, 27(15): 3138-3145. pmid: 10454610
[56]	Sharma S, Yang J, Watzinger P, et al. Yeast Nop2 and Rcm1 methylate C2870 and C2278 of the 25S rRNA, respectively[J]. Nucleic Acids Res, 2013, 41(19): 9062-9076. doi: 10.1093/nar/gkt679 pmid: 23913415
[57]	Schaefer M, Pollex T, Hanna K, et al. RNA methylation by Dnmt2 protects transfer RNAs against stress-induced cleavage[J]. Genes Dev, 2010, 24(15): 1590-1595.
[58]	Yang X, Yang Y, Sun BF, et al. 5-methylcytosine promotes mRNA export—NSUN2 as the methyltransferase and ALYREF as an m⁵C reader[J]. Cell Res, 2017, 27(5): 606-625. doi: 10.1038/cr.2017.55 pmid: 28418038
[59]	Motorin Y, Lyko F, Helm M. 5-methylcytosine in RNA: detection, enzymatic formation and biological functions[J]. Nucleic Acids Res, 2010, 38(5): 1415-1430. doi: 10.1093/nar/gkp1117 pmid: 20007150
[60]	Frye M, Watt FM. The RNA methyltransferase Misu(NSun2)mediates Myc-induced proliferation and is upregulated in tumors[J]. Curr Biol, 2006, 16(10): 971-981.
[61]	Van Haute L, Dietmann S, Kremer L, et al. Deficient methylation and formylation of mt-tRNAMet wobble cytosine in a patient carrying mutations in NSUN3[J]. Nat Commun, 2016, 7: 12039.
[62]	Boriack-Sjodin PA, Ribich S, Copeland RA. RNA-modifying proteins as anticancer drug targets[J]. Nat Rev Drug Discov, 2018, 17(6): 435-453. doi: 10.1038/nrd.2018.71 pmid: 29773918
[63]	Schosserer M, Minois N, Angerer TB, et al. Methylation of ribosomal RNA by NSUN5 is a conserved mechanism modulating organismal lifespan[J]. Nat Commun, 2015, 6: 6158. doi: 10.1038/ncomms7158 pmid: 25635753
[64]	Harris T, Marquez B, Suarez S, et al. Sperm motility defects and infertility in male mice with a mutation in Nsun7, a member of the Sun domain-containing family of putative RNA methyltransferases[J]. Biol Reprod, 2007, 77(2): 376-382. pmid: 17442852
[65]	Zhou Z, Luo MJ, Straesser K, et al. The protein Aly links pre-messenger-RNA splicing to nuclear export in metazoans[J]. Nature, 2000, 407(6802): 401-405.
[66]	Alexandrov A, Martzen MR, Phizicky EM. Two proteins that form a complex are required for 7-methylguanosine modification of yeast tRNA[J]. RNA, 2002, 8(10): 1253-1266. pmid: 12403464
[67]	Leulliot N, Chaillet M, Durand D, et al. Structure of the yeast tRNA m⁷G methylation complex[J]. Structure, 2008, 16(1): 52-61. doi: 10.1016/j.str.2007.10.025 pmid: 18184583
[68]	Trotman JB, Giltmier AJ, Mukherjee C, et al. RNA guanine-7 methyltransferase catalyzes the methylation of cytoplasmically recapped RNAs[J]. Nucleic Acids Res, 2017, 45(18): 10726-10739. doi: 10.1093/nar/gkx801 pmid: 28981715
[69]	Grasso L, Suska O, Davidson L, et al. mRNA cap methylation in pluripotency and differentiation[J]. Cell Rep, 2016, 16(5): 1352-1365. doi: S2211-1247(16)30858-0 pmid: 27452456
[70]	Haag S, Kretschmer J, Bohnsack MT. WBSCR22/Merm1 is required for late nuclear pre-ribosomal RNA processing and mediates N7-methylation of G1639 in human 18S rRNA[J]. RNA, 2015, 21(2): 180-187. doi: 10.1261/rna.047910.114 pmid: 25525153
[71]	Shen Q, Zheng XZ, McNutt MA, et al. NAT10, a nucleolar protein, localizes to the midbody and regulates cytokinesis and acetylation of microtubules[J]. Exp Cell Res, 2009, 315(10): 1653-1667. doi: 10.1016/j.yexcr.2009.03.007 pmid: 19303003
[72]	Liu XF, Tan YQ, Zhang CF, et al. NAT10 regulates p53 activation through acetylating p53 at K120 and ubiquitinating Mdm2[J]. EMBO Rep, 2016, 17(3): 349-366. doi: 10.15252/embr.201540505 pmid: 26882543
[73]	张雪, 汤华. 乙酰转移酶10通过介导盘状蛋白结构域受体1mRNA的ac4C乙酰化修饰促进宫颈癌细胞的恶性行为[J]. 中国生物化学与分子生物学报, 2022, 38(5): 603-613. doi: 10.13865/j.cnki.cjbmb.2022.04.0044
	Zhang X, Tang H. NAT10 promotes cervical cancer cell malignant behavior via N4-acetylcytidine modification of DDR1 mRNA[J]. Chin J Biochem Mol Biol, 2022, 38(5): 603-613. doi: 10.13865/j.cnki.cjbmb.2022.04.0044
[74]	Hao HJ, Liu WC, Miao YJ, et al. N4-acetylcytidine regulates the replication and pathogenicity of enterovirus 71[J]. Nucleic Acids Res, 2022, 50(16): 9339-9354. doi: 10.1093/nar/gkac675 pmid: 35971620
[75]	Wang K, Zhou LY, Liu F, et al. PIWI-interacting RNA HAAPIR regulates cardiomyocyte death after myocardial infarction by promoting NAT10-mediated ac⁴ C acetylation of tfec mRNA[J]. Adv Sci, 2022, 9(8): e2106058.
[76]	Sheikh AH, Tabassum N, Rawat A, et al. m⁶A RNA methylation counteracts dark-induced leaf senescence in Arabidopsis[J]. Plant Physiol, 2024, 194(4): 2663-2678.
[77]	Zhang Y, Wang JH, Ma WJ, et al. Transcriptome-wide m⁶A methylation in natural yellow leaf of Catalpa fargesii[J]. Front Plant Sci, 2023, 14: 1167789.
[78]	Amara U, Hu JZ, Cai J, et al. FLK is an mRNA m⁶A reader that regulates floral transition by modulating the stability and splicing of FLC in Arabidopsis[J]. Mol Plant, 2023, 16(5): 919-929.
[79]	Luo GZ, MacQueen A, Zheng GQ, et al. Unique features of the m⁶A methylome in Arabidopsis thaliana[J]. Nat Commun, 2014, 5: 5630.
[80]	Zhou LL, Tang RK, Li XJ, et al. N⁶-methyladenosine RNA modification regulates strawberry fruit ripening in an ABA-dependent manner[J]. Genome Biol, 2021, 22(1): 168.
[81]	Yang JX, Li L, Li X, et al. The blue light receptor CRY1 interacts with FIP37 to promote N⁶-methyladenosine RNA modification and photomorphogenesis in Arabidopsis[J]. New Phytol, 2023, 237(3): 840-854.
[82]	Arribas-Hernández L, Simonini S, Hansen MH, et al. Recurrent requirement for the m⁶A-ECT2/ECT3/ECT4 axis in the control of cell proliferation during plant organogenesis[J]. Development, 2020, 147(14): dev189134.
[83]	Yu Q, Liu S, Yu L, et al. RNA demethylation increases the yield and biomass of rice and potato plants in field trials[J]. Nat Biotechnol, 2021, 39(12): 1581-1588. doi: 10.1038/s41587-021-00982-9 pmid: 34294912
[84]	Duan HC, Wei LH, Zhang C, et al. ALKBH10B is an RNA N⁶-methyladenosine demethylase affecting Arabidopsis floral transition[J]. Plant Cell, 2017, 29(12): 2995-3011.
[85]	Zhou LL, Tian SP, Qin GZ. RNA methylomes reveal the m⁶A-mediated regulation of DNA demethylase gene SlDML2 in tomato fruit ripening[J]. Genome Biol, 2019, 20(1): 156.
[86]	Yang WY, Meng J, Liu JX, et al. The N¹-methyladenosine methylome of Petunia mRNA[J]. Plant Physiol, 2020, 183(4): 1710-1724.
[87]	Zhang DL, Guo WJ, Wang T, et al. RNA 5-methylcytosine modification regulates vegetative development associated with H3K27 trimethylation in Arabidopsis[J]. Adv Sci, 2022, 10(1): e2204885.
[88]	Wang YM, Pang CQ, Li XK, et al. Identification of tRNA nucleoside modification genes critical for stress response and development in rice and Arabidopsis[J]. BMC Plant Biol, 2017, 17(1): 261.
[89]	覃晓春. 矮牵牛RNA m⁵C修饰相关蛋白功能初步探索[D]. 广州: 华南农业大学, 2020.
	Qin XC. A preliminary exploration of the RNA m⁵C modification-related proteins functions in Petunia hybrida[D]. Guangzhou: South China Agricultural University, 2020.
[90]	Li B, Li DH, Cai LJ, et al. Transcriptome-wide profiling of RNA N⁴-cytidine acetylation in Arabidopsis thaliana and Oryza sativa[J]. Mol Plant, 2023, 16(6): 1082-1098.
[91]	Wang WL, Liu HJ, Wang FF, et al. N4-acetylation of cytidine in mRNA plays essential roles in plants[J]. Plant Cell, 2023, 35(10): 3739-3756.
[92]	Ma LL, Zheng YY, Zhou ZJ, et al. Dissection of mRNA ac⁴C acetylation modifications in AC and Nr fruits: insights into the regulation of fruit ripening by ethylene[J]. Mol Hortic, 2024, 4(1): 5.
[93]	Hou N, Li CS, He JQ, et al. MdMTA-mediated m⁶ A modification enhances drought tolerance by promoting mRNA stability and translation efficiency of genes involved in lignin deposition and oxidative stress[J]. New Phytol, 2022, 234(4): 1294-1314.
[94]	Zhang GY, Lv ZR, Diao SF, et al. Unique features of the m⁶A methylome and its response to drought stress in sea buckthorn(Hippophae rhamnoides Linn.)[J]. RNA Biol, 2021, 18(sup2): 794-803.
[95]	Wang S, Wang HY, Xu ZH, et al. m⁶A mRNA modification promotes chilling tolerance and modulates gene translation efficiency in Arabidopsis[J]. Plant Physiol, 2023, 192(2): 1466-1482.
[96]	Zhang M, Zeng YP, Peng R, et al. N⁶-methyladenosine RNA modification regulates photosynthesis during photodamage in plants[J]. Nat Commun, 2022, 13(1): 7441. doi: 10.1038/s41467-022-35146-z pmid: 36460653
[97]	Zhang K, Zhuang XJ, Dong ZZ, et al. The dynamics of N⁶-methyladenine RNA modification in interactions between rice and plant viruses[J]. Genome Biol, 2021, 22(1): 189. doi: 10.1186/s13059-021-02410-2 pmid: 34167554
[98]	He H, Ge LH, Chen YL, et al. m⁶A modification of plant virus enables host recognition by NMD factors in plants[J]. Sci China Life Sci, 2024, 67(1): 161-174.
[99]	Prall W, Sheikh AH, Bazin J, et al. Pathogen-induced m⁶A dynamics affect plant immunity[J]. Plant Cell, 2023, 35(11): 4155-4172.

修饰类型Type of modification	生长发育Growth and development	蛋白/基因Protein/Gene	物种Species	参考文献Reference
m⁶A	影响种子发育	MTA	拟南芥	[6]
	对抗叶片衰老	MTA	拟南芥	[76]
	调节光合作用	At5g01920	拟南芥	[79]
	促进果实成熟	MTA, MTB, ALKBH2	草莓，番茄	[80,85]
	影响光形态建成	CRY1, FIP37	拟南芥	[81]
	刺激器官发生	ECT2, ECT3, ECT4	拟南芥	[82]
	增强根系生长分蘖芽形成	FTO	水稻，马铃薯	[83]
	调控花期	ALKBH10B	拟南芥	[84]
m¹A	调节叶片发育	PhTRMT61A	矮牵牛	[86]
m⁵C	调节光合作用叶绿体和质体发育	TRM4B	拟南芥	[87]
	影响根系发育	AtTRM4a, AtTRM4b	拟南芥	[23,88]
	调节叶片发育	PhNop2, ALYREF	矮牵牛	[89]
ac⁴C	调节种子发育影响叶生长	OsNAT10, AtNAT10a, AtNAT10b	拟南芥，水稻	[90-91]
	促进果实成熟	Solyc02g036350.3, Solyc06g053710.3等	番茄	[92]

修饰类型Type of modification	生长发育Growth and development	蛋白/基因Protein/Gene	物种Species	参考文献Reference
m⁶A	影响种子发育	MTA	拟南芥	[6]
	对抗叶片衰老	MTA	拟南芥	[76]
	调节光合作用	At5g01920	拟南芥	[79]
	促进果实成熟	MTA, MTB, ALKBH2	草莓，番茄	[80,85]
	影响光形态建成	CRY1, FIP37	拟南芥	[81]
	刺激器官发生	ECT2, ECT3, ECT4	拟南芥	[82]
	增强根系生长分蘖芽形成	FTO	水稻，马铃薯	[83]
	调控花期	ALKBH10B	拟南芥	[84]
m¹A	调节叶片发育	PhTRMT61A	矮牵牛	[86]
m⁵C	调节光合作用叶绿体和质体发育	TRM4B	拟南芥	[87]
	影响根系发育	AtTRM4a, AtTRM4b	拟南芥	[23,88]
	调节叶片发育	PhNop2, ALYREF	矮牵牛	[89]
ac⁴C	调节种子发育影响叶生长	OsNAT10, AtNAT10a, AtNAT10b	拟南芥，水稻	[90-91]
	促进果实成熟	Solyc02g036350.3, Solyc06g053710.3等	番茄	[92]

修饰类型 Type of modification	胁迫类型 Type of stress	蛋白/基因 Protein/ Gene	物种 Species	参考文献 Reference
m⁶A	干旱胁迫	MdMTA	苹果	[93]
		HrALKBH10B, HrALKBH10C, HrALKBH10D	沙棘	[94]
	低温胁迫	MTA	拟南芥	[95]
	强光胁迫	VIR	拟南芥	[96]
	生物胁迫	OsAGO18, OsSLRL1, MTA, HAKAI, NbECT 2A/B/C, ALKBH10B	水稻、本氏烟草、番茄、拟南芥	[97⇓-99]
m¹A	低温胁迫	At2g45730, At5g14600	拟南芥	[88]
	盐胁迫	LOC_Os04g02150等	水稻
m⁷G	低温胁迫盐胁迫	At5g24840, At1g03110, LOC_Os06g12990等	拟南芥水稻	[88]
m⁵C	氧化胁迫	TRM4B	拟南芥	[22]

修饰类型 Type of modification	胁迫类型 Type of stress	蛋白/基因 Protein/ Gene	物种 Species	参考文献 Reference
m⁶A	干旱胁迫	MdMTA	苹果	[93]
		HrALKBH10B, HrALKBH10C, HrALKBH10D	沙棘	[94]
	低温胁迫	MTA	拟南芥	[95]
	强光胁迫	VIR	拟南芥	[96]
	生物胁迫	OsAGO18, OsSLRL1, MTA, HAKAI, NbECT 2A/B/C, ALKBH10B	水稻、本氏烟草、番茄、拟南芥	[97⇓-99]
m¹A	低温胁迫	At2g45730, At5g14600	拟南芥	[88]
	盐胁迫	LOC_Os04g02150等	水稻
m⁷G	低温胁迫盐胁迫	At5g24840, At1g03110, LOC_Os06g12990等	拟南芥水稻	[88]
m⁵C	氧化胁迫	TRM4B	拟南芥	[22]