N6‐Methyladenosine mRNA methylation is important for salt stress tolerance in Arabidopsis

Alarcón, C.R., Lee, H., Goodarzi, H., Halberg, N. & Tavazoie, S.F. (2015) N6‐methyladenosine marks primary microRNAs for processing. Nature, 519, 482–485. Anderson, S.J., Kramer, M.C., Gosai, S.J., Yu, X., Vandivier, L.E., Nelson, A.D.L. et al. (2018) N6‐methyladenosine inhibits local ribonucleolytic cleavage to stabilize mRNAs in Arabidopsis. Cell Reports, 25, 1146–1157. Arribas‐Hernández, L., Bressendorff, S., Hansen, M.H., Poulsen, C., Erdmann, S. & Brodersen, P. (2018) An m6A‐YTH module controls developmental timing and morphogenesis in Arabidopsis. The Plant Cell, 30, 952–967. Arribas‐Hernández, L. & Brodersen, P. (2020) Occurrence and functions of m6A and other covalent modifications in plant mRNA. Plant Physiology, 182, 79–96. Arribas‐Hernández, L., Simonini, S., Hansen, M.H., Paredes, E.B., Bressendorff, S., Dong, Y. et al. (2020) Recurrent requirement for the m6A‐ECT2/ECT3/ECT4 axis in the control of cell proliferation during plant organogenesis. Development, 147, dev189134. Baquero‐Perez, B., Antanaviciute, A., Yonchev, I.D., Carr, I.M., Wilson, S.A. & Whitehouse, A. (2019) The Tudor SND1 protein is an m6A RNA reader essential for replication of Kaposi’s sarcoma‐associated herpesvirus. eLife 8, e47261. Batista, P., Molinie, B., Wang, J., Qu, K., Zhang, J., Li, L. et al. (2014) m6A RNA modification controls cell fate transition in mammalian embryonic stem cells. Cell Stem Cell, 15, 707–719. Bhat, S.S., Bielewicz, D., Gulanicz, T., Bodi, Z., Yu, X., Anderson, S.J. et al. (2020) mRNA adenosine methylase (MTA) deposits m6A on pri‐miRNAs to modulate miRNA biogenesis in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 117, 21785–21795. Boccaletto, P., Machnicka, M.A., Purta, E., Piatkowski, P., Bagiński, B., Wirecki, T.K. et al. (2018) MODOMICS: a database of RNA modification pathways. 2017 update. Nucleic Acids Research, 46, D303–D307. Bodi, Z., Zhong, S., Mehra, S., Song, J., Graham, N., Li, H. et al. (2012) Adenosine methylation in Arabidopsis mRNA is associated with the 3ʹ end and reduced levels cause developmental defects. Frontiers in Plant Science, 3, 48. Bushkin, G.G., Pincus, D., Morgan, J.T., Richardson, K., Lewis, C., Chan, S.H. et al. (2019) m6A modification of a 3ʹUTR site reduces RME1 mRNA levels to promote meiosis. Nature Communications, 10, 3414. Chen, J.H., Jiang, H.W., Hsieh, E.J., Chen, H.Y., Chien, C.T., Hsieh, H.L. et al. (2012) Drought and salt stress tolerance of an Arabidopsis glutathione S‐transferase U17 knockout mutant are attributed to the combined effect of glutathione and abscisic acid. Plant Physiology, 158, 340–351. Chen, M., Urs, M.J., Sánchez‐González, I., Olayioye, M.A., Herde, M. & Witte, C.‐P. (2018) m6A RNA degradation products are catabolized by an evolutionarily conserved N6‐methyl‐AMP deaminase in plant and mammalian cells. The Plant Cell, 30, 1511–1522. Dai, D., Wang, H., Zhu, L., Jin, H. & Wang, X. (2018) N6‐methyladenosine links RNA metabolism to cancer progression. Cell Death & Disease, 9, 124. David, R., Burgess, A., Parker, B., Li, J., Pulsford, K., Sibbritt, T. et al. (2017) Transcriptome‐wide mapping of RNA 5‐methylcytosine in Arabidopsis mRNAs and non‐coding RNAs. The Plant Cell, 29, 445–460. Dinh, S.N., Park, S.J., Han, J.H. & Kang, H. (2019) A chloroplast‐targeted S1 RNA‐binding domain protein plays a role in Arabidopsis response to diverse abiotic stresses. Journal of Plant Biology, 62, 74–81. Dominissini, D., Moshitch‐Moshkovitz, S., Salmon‐Divon, M., Amariglio, N. & Rechavi, G. (2013) Transcriptome‐wide mapping of N6‐methyladenosine by m6A‐seq based on immunocapturing and massively parallel sequencing. Nature Protocols, 8, 176. Dominissini, D., Moshitch‐Moshkovitz, S., Schwartz, S., Salmon‐Divon, M., Ungar, L., Osenberg, S. et al. (2012) Topology of the human and mouse m6A RNA methylomes revealed by m6A‐seq. Nature, 485, 201–206. Du, H., Zhao, Y., He, J., Zhang, Y., Xi, H., Liu, M. et al. (2016) YTHDF2 destabilizes m6A‐containing RNA through direct recruitment of the CCR4–NOT deadenylase complex. Nature Communications, 7, 12626. Duan, H.‐C., Wei, L.‐H., Zhang, C., Wang, Y., Chen, L., Lu, Z. et al. (2017) ALKBH10B is an RNA N6‐methyladenosine demethylase affecting Arabidopsis floral transition. The Plant Cell, 29, 2995–3011. Elkon, R., Ugalde, A.P. & Agami, R. (2013) Alternative cleavage and polyadenylation: extent, regulation and function. Nature Reviews Genetics, 14, 496–506. Fu, Y., Dominissini, D., Rechavi, G. & He, C. (2014) Gene expression regulation mediated through reversible m6A RNA methylation. Nature Reviews Genetics, 15, 293–306. Fustin, J.‐M., Doi, M., Yamaguchi, Y., Hida, H., Nishimura, S., Yoshida, M. et al. (2013) RNA‐methylation‐dependent RNA processing controls the speed of the circadian clock. Cell, 155, 793–806. Gao, Y., Liu, X., Wu, B., Wang, H., Xi, F., Kohnen, M.V. 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 Biology, 22, 22. Grozhik, A.V., Linder, B., Olarerin‐George, A.O. & Jaffrey, S.R. (2017) Mapping m6A at individual‐nucleotide resolution using crosslinking and immunoprecipitation (miCLIP). Methods in Molecular Biology, 1562, 55–78. Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y.C., Laslo, P. et al. (2010) Simple combinations of lineage‐determining transcription factors prime cis‐regulatory elements required for macrophage and B cell identities. Molecular Cell, 38, 576–589. Hu, J., Manduzio, S. & Kang, H. (2019) Epitranscriptomic RNA methylation in plant development and abiotic stress responses. Frontiers in Plant Science, 10, 500. Huang, H., Weng, H., Sun, W., Qin, X., Shi, H., Wu, H. et al. (2018) Recognition of RNA N6‐methyladenosine by IGF2BP proteins enhances mRNA stability and translation. Nature Cell Biology, 20, 285–295. Kan, L., Grozhik, A.V., Vedanayagam, J., Patil, D.P., Pang, N., Lim, K.S. et al. (2017) The m6A pathway facilitates sex determination in Drosophila. Nature Communications, 8, 15737. Kang, B.‐C., Yun, J.‐Y., Kim, S.‐T., Shin, Y.J., Ryu, J., Choi, M. et al. (2018) Precision genome engineering through adenine base editing in plants. Nature Plants, 4, 427–431. Kang, H., Park, S.J. & Kwak, K.J. (2013) Plant RNA chaperones in stress response. Trends in Plant Science, 18, 100–106. Ke, S., Alemu, E.A., Mertens, C., Gantman, E.C., Fak, J.J., Mele, A. 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. Kim, J., Shim, S., Lee, H. & Seo, P.J. (2020) m6A mRNA modification as a new layer of gene regulation in plants. Journal of Plant Biology, 63, 97–106. Kim, W.Y., Ali, Z., Park, H.J., Park, S.J., Cha, J.Y., Perez‐Hormaeche, J. et al. (2013) Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in Arabidopsis. Nature Communications, 4, 1352. Kim, Y.O., Bae, H.J., Cho, E.J. & Kang, H.S. (2017) Exogenous glutathione enhances mercury tolerance by inhibiting mercury entry into plant cells. Frontiers in Plant Science, 8, 683. Langmead, B. & Salzberg, S.L. (2012) Fast gapped‐read alignment with Bowtie 2. Nature Methods, 9, 357–359. Lee, K. & Kang, H. (2016) Emerging roles of RNA‐binding proteins in plant growth, development, and stress responses. Molecules and Cells, 39, 179–185. Li, X., Xiong, X., Wang, K., Wang, L., Shu, X., Ma, S. et al. (2016) Transcriptome ‐wide mapping reveals reversible and dynamic N1‐methyladenosine methylome. Nature Chemical Biology, 12, 311–316. Lichtenthaler, H.K. (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology, 148, 350–382. Liu, J., Gao, M., Xu, S., Chen, Y., Wu, K., Liu, H. et al. (2020) YTHDF2/3 are required for somatic reprogramming through different RNA deadenylation pathways. Cell Reports, 32, 108–120. Liu, N. & Pan, T. (2016) N6‐methyladenosine–encoded epitranscriptomics. Nature Structural & Molecular Biology, 23, 98–102. Luo, G.Z., MacQueen, A., Zheng, G., Duan, H., Dore, L.C., Lu, Z. et al. (2014) Unique features of the m6A methylome in Arabidopsis thaliana. Nature Communications, 5, 5630. Luo, J.‐H., Wang, Y., Wang, M., Zhang, L.‐Y., Peng, H.‐R., Zhou, Y.‐Y. et al. (2020) Natural variation in RNA m6A methylation and its relationship with translational status. Plant Physiology, 182, 332–344. Martin, M. (2011) CUTADAPT removes adapter sequences from high‐throughput sequencing reads. EMBnet.journal, 17, 10. Martínez‐Pérez, M., Aparicio, F., López‐Gresa, M.P., Bellés, J.M., Sánchez‐Navarro, J.A. & Pallás, V. (2017) Arabidopsis m6A demethylase activity modulates viral infection of a plant virus and the m6A abundance in its genomic RNAs. Proceedings of the National Academy of Sciences of the United States of America, 114, 10755–10760. Meng, J., Lu, Z., Liu, H., Zhang, L., Zhang, S., Chen, Y. et al. (2014) A protocol for RNA methylation differential analysis with MeRIP‐Seq data and exomePeak R/Bioconductor package. Methods, 69, 274–281. Meyer, K.D. & Jaffrey, S.R. (2014) The dynamic epitranscriptome: N6 methyladenosine and gene expression control. Nature Reviews Molecular Cell Biology, 15, 313–326. Miao, Z., Zhang, T., Qi, Y., Song, J., Han, Z. & Ma, C. (2020) Evolution of the RNA N6‐methyladenosine methylome mediated by genomic duplication. Plant Physiology, 182, 345–360. Munns, R. & Gilliham, M. (2015) Salinity tolerance of crops ‐ what is the cost? New Phytologist, 208, 668–673. Munns, R. & Tester, M. (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology, 59, 651–681. Murik, O., Chandran, S.A., Nevo‐Dinur, K., Sultan, L.D., Best, C., Stein, Y. et al. (2020) Topologies of N6‐adenosine methylation (m6A) in land plant mitochondria and their putative effects on organellar gene expression. The Plant Journal, 101, 1269–1286. Pan, Y., Ma, P., Liu, Y., Li, W. & Shu, Y. (2018) Multiple functions of m6A RNA methylation in cancer. Journal of Hematology & Oncology, 11, 48. Parker, M.T., Knop, K., Sherwood, A.V., Schurch, N.J., Mackinnon, K., Gould, P.D. et al. (2020) Nanopore direct RNA sequencing maps the complexity of Arabidopsis mRNA processing and m6A modification. eLife, 9, e49658. Pertea, M., Pertea, G.M., Antonescu, C.M., Chang, T.‐C., Mendell, J.T. & Salzberg, S.L. (2015) StringTie enables improved reconstruction of a transcriptome from RNA‐seq reads. Nature Biotechnology, 33, 290–295. Pontier, D., Picart, C., El Baidouri, M., Roudier, F., Xu, T., Lahmy, S. et al. (2019) The m6A pathway protects the transcriptome integrity by restricting RNA chimera formation in plants. Life Science Alliance, 2, e201900393. Ramel, F., Sulmon, C., Bogard, M., Couee, I. & Gouesbet, G. (2009) Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose‐induced tolerance in Arabidopsis thaliana plantlets. BMC Plant Biology, 9, 28. Robinson, M.D., McCarthy, D.J. & Smyth, G.K. (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26, 139–140. Roundtree, I.A., Luo, G.‐Z., Zhang, Z., Wang, X., Zhou, T., Cui, Y. et al. (2017) YTHDC1 mediates nuclear export of N6‐methyladenosine methylated mRNAs. eLife, 6, https://doi.org/10.7554/eLife.31311s. Růžička, K., Zhang, M., Campilho, A., Bodi, Z., Kashif, M., Saleh, 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 Phytologist, 215, 157–172. Sanchez, D.H. & Paszkowski, J. (2014) Heat‐induced release of epigenetic silencing reveals the concealed role of an imprinted plant gene. PLoS Genetics, 10, e1004806. Schwab, R., Ossowski, S., Riester, M., Warthmann, N. & Weigel, D. (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. The Plant Cell, 18, 1121–1133. Scutenaire, J., Deragon, J.‐M., Jean, V., Benhamed, M., Raynaud, C., Favory, J.‐J. et al. (2018) The YTH domain protein ECT2 is an m6A reader required for normal trichome branching in Arabidopsis. The Plant Cell, 30, 986–1005. Shen, L., Liang, Z., Gu, X., Chen, Y., Teo, Z.W.N., Hou, X. et al. (2016) N6‐methyladenosine RNA modification regulates shoot stem cell fate in Arabidopsis. Developmental Cell, 38, 186–200. Shi, H., Wang, X., Lu, Z., Zhao, B.S., Ma, H., Hsu, P.J. et al. (2017) YTHDF3 facilitates translation and decay of N6‐methyladenosine modified RNA. Cell Research, 27, 315–328. Shi, H., Wei, J. & He, C. (2019) Where, when, and how: context‐dependent functions of RNA methylation writers, readers, and erasers. Molecular Cell, 74, 640–650. Shu, X., Cao, J., Cheng, M., Xiang, S., Gao, M., Li, T. et al. (2020) A metabolic labeling method detects m6A transcriptome‐wide at single base resolution. Nature Chemical Biology, 16, 887–895. Si, X., Zhang, H., Wang, Y., Chen, K. & Gao, C. (2020) Manipulating gene translation in plants by CRISPR–Cas9‐mediated genome editing of upstream open reading frames. Nature Protocols, 15, 338–363. Slobodin, B., Han, R., Calderone, V., Vrielink, J.A.O., Loayza‐Puch, F., Elkon, R. et al. (2017) Transcription impacts the efficiency of mRNA translation via co‐transcriptional N6‐adenosine methylation. Cell, 169, 326–337. Song, P., Yang, J., Wang, C., Lu, Q., Shi, L., Tayier, S. et al. (2021) Arabidopsis N6‐methyladenosine reader CPSF30‐L recognizes FUE signals to control polyadenylation site choice in liquid‐like nuclear bodies. Molecular Plant, 14, 1–17. Taji, T., Seki, M., Satou, M., Sakurai, T., Kobayashi, M., Ishiyama, K. et al. (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis‐related halophyte salt cress using Arabidopsis microarray. Plant Physiology, 135, 1697–1709. Tian, B. & Manley, J.L. (2017) Alternative polyadenylation of mRNA precursors. Nature Reviews Molecular Cell Biology, 18, 18–30. 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. Wang, X., Lu, Z., Gomez, A., Hon, G.C., Yue, Y., Han, D. et al. (2014) N6‐methyladenosine‐dependent regulation of messenger RNA stability. Nature, 505, 117–120. Wang, X., Zhao, B.S., Roundtree, I.A., Lu, Z., Han, D., Ma, H. et al. (2015) N6‐methyladenosine modulates messenger RNA translation efficiency. Cell, 161, 1388–1399. Wei, L.H., Song, P., Wang, Y., Lu, Z., Tang, Q., Yu, Q. et al. (2018) The m6A reader ECT2 controls trichome morphology by affecting mRNA stability in Arabidopsis. The Plant Cell, 30, 968–985. Wu, Y., Deng, Z., Lai, J., Zhang, Y., Yang, C., Yin, B. et al. (2009) Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses. Cell Research, 19, 1279–1290. Xiao, W., Adhikari, S., Dahal, U., Chen, Y.S., Hao, Y.J., Sun, B.F. et al. (2016) Nuclear m6A reader YTHDC1 regulates mRNA splicing. Molecular Cell, 61, 507–519. Xuan, J.J., Wen, J.S., Peng, H.L., Zhou, K.R., Liu, S., Zheng, L.L. et al. (2018) RMBase v2.0: deciphering the map of RNA modifications from epitranscriptome sequencing data. Nucleic Acids Research, 46, D327–D334. Yadav, P.K. & Rajasekharan, R. (2017) The m6A methyltransferase Ime4 epitranscriptionally regulates triacylglycerol metabolism and vacuolar morphology in haploid yeast cells. Journal of Biological Chemistry, 292, 13727–13744. Yang, Y. & Guo, Y. (2018) Elucidating the molecular mechanisms mediating plant salt‐stress responses. New Phytologist, 217, 523–539. Yu, G., Wang, L.‐G. & He, Q.‐Y. (2015) ChIPseeker: an R/Bioconductor package for ChIP peak annotation, comparison and visualization. Bioinformatics, 31, 2382–2383. Yue, H., Nie, X., Yan, Z. & Weining, S. (2019) N6‐methyladenosine regulatory machinery in plants: composition, function and evolution. Plant Biotechnology Journal, 17, 1194–1208. Yue, Y., Liu, J., Cui, X., Cao, J., Luo, G., Zhang, Z. et al. (2018) VIRMA mediates preferential m6A mRNA methylation in 3ʹUTR and near stop codon and associates with alternative polyadenylation. Cell Discovery, 4, 10. Zhang, F., Zhang, Y.‐C., Liao, J.‐Y., Yu, Y., Zhou, Y.‐F., Feng, Y.‐Z. et al. (2019) The subunit of RNA N6‐methyladenosine methyltransferase OsFIP regulates early degeneration of microspores in rice. PLoS Genetics, 15, e1008120. Zhao, C., Zhang, H., Song, C., Zhu, J.‐K. & Shabala, S. (2020) Mechanisms of plant responses and adaptation to soil salinity. The Innovation, 1, 100017. Zheng, H., Sun, X., Li, J., Song, Y., Song, J., Wang, F. et al. (2021) Analysis of N6‐methyladenosine reveals a new important mechanism regulating the salt tolerance of sweet sorghum. Plant Science, 304, 110801. Zheng, H., Sun, X., Zhang, X. & Sui, N. (2020) m6A editing: new tool to improve crop quality? Trends in Plant Science, 25, 859–867. Zhong, S., Li, H., Bodi, Z., Button, J., Vespa, L., Herzog, M. et al. (2008) MTA is an Arabidopsis messenger RNA adenosine methylase and interacts with a homolog of a sex‐specific splicing factor. The Plant Cell, 20, 1278–1288. Zhou, L., Tian, S. & Qin, G. (2019) RNA methylomes reveal the m6A‐mediated regulation of DNA demethylase gene SlDML2 in tomato fruit ripening. Genome Biology, 20, 156. Zhu, J., Fu, X., Koo, Y.D., Zhu, J.K., Jenney, F.E., Adams, M.W. et al. (2007) An enhancer mutant of Arabidopsis salt overly sensitive 3 mediates both ion homeostasis and the oxidative stress response. Molecular and Cellular Biology, 27, 5214–5224.