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RNA Modification and Its Implication in Plant Pathogenic Fungi

  • Jeon, Junhyun (Department of Biotechnology, College of Life and Applied Sciences, Yeungnam University) ;
  • Lee, Song Hee (Plant Immunity Center, Seoul National University)
  • Received : 2021.07.14
  • Accepted : 2021.09.17
  • Published : 2021.12.01

Abstract

Interaction of a pathogen with its host plant requires both flexibility and rapid shift in gene expression programs in response to environmental cues associated with host cells. Recently, a growing volume of data on the diversity and ubiquity of internal RNA modifications has led to the realization that such modifications are highly dynamic and yet evolutionarily conserved system. This hints at these RNA modifications being an additional regulatory layer for genetic information, culminating in epitranscriptome concept. In plant pathogenic fungi, however, the presence and the biological roles of RNA modifications are largely unknown. Here we delineate types of RNA modifications, and provide examples demonstrating roles of such modifications in biology of filamentous fungi including fungal pathogens. We also discuss the possibility that RNA modification systems in fungal pathogens could be a prospective target for new agrochemicals.

Keywords

Acknowledgement

This work was supported by 2019 Yeungnam University Research Grant.

References

  1. Adler, M., Weissmann, B. and Gutman, A. B. 1958. Occurrence of methylated purine bases in yeast ribonucleic acid. J. Biol. Chem. 230:717-723. https://doi.org/10.1016/S0021-9258(18)70494-8
  2. Alexandrov, A., Chernyakov, I., Gu, W., Hiley, S. L., Hughes, T. R., Grayhack, E. J. and Phizicky, E. M. 2006. Rapid tRNA decay can result from lack of nonessential modifications. Mol. Cell 21:87-96. https://doi.org/10.1016/j.molcel.2005.10.036
  3. Anderson, S. J., Kramer, M. C., Gosai, S. J., Yu, X., Vandivier, L. E., Nelson, A. D. L., Anderson, Z. D., Beilstein, M. A., Fray, R. G., Lyons, E. and Gregory, B. D. 2018. N6-methyladenosine inhibits local ribonucleolytic cleavage to stabilize mRNAs in Arabidopsis. Cell. Rep. 25:1146-1157. https://doi.org/10.1016/j.celrep.2018.10.020
  4. Barrett, M. P., Burchmore, R. J. S., Stich, A., Lazzari, J. O., Frasch, A. C., Cazzulo, J. J. and Krishna, S. 2003. The trypanosomiases. Lancet 362:1469-1480. https://doi.org/10.1016/S0140-6736(03)14694-6
  5. Benne, R., Van den Burg, J., Brakenhoff, J. P., Sloof, P., Van Boom, J. H. and Tromp, M. C. 1986. Major transcript of the frameshifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell 46:819-826. https://doi.org/10.1016/0092-8674(86)90063-2
  6. Boccaletto, P., Machnicka, M. A., Purta, E., Piatkowski, P., Baginski, B., Wirecki, T. K., de Crecy-Lagard, V., Ross, R., Limbach, P. A., Kotter, A., Helm, M. and Bujnicki, J. M. 2018. MODOMICS: a database of RNA modification pathways. 2017 update. Nucleic Acids Res. 46:D303-D307. https://doi.org/10.1093/nar/gkx1030
  7. Boo, S. H. and Kim, Y. K. 2020. The emerging role of RNA modifications in the regulation of mRNA stability. Exp. Mol. Med. 52:400-408. https://doi.org/10.1038/s12276-020-0407-z
  8. Chan, C. T. Y., Dyavaiah, M., DeMott, M. S., Taghizadeh, K., Dedon, P. C. and Begley, T. J. 2010. A quantitative systems approach reveals dynamic control of tRNA modifications during cellular stress. PLoS Genet. 6:e1001247. https://doi.org/10.1371/journal.pgen.1001247
  9. Christofi, T. and Zaravinos, A. 2019. RNA editing in the forefront of epitranscriptomics and human health. J. Transl. Med. 17:319. https://doi.org/10.1186/s12967-019-2071-4
  10. Cohn, W. E. 1960. Pseudouridine, a carbon-carbon linked ribonucleoside in ribonucleic acids: isolation, structure, and chemical characteristics. J. Biol. Chem. 235:1488-1498. https://doi.org/10.1016/S0021-9258(18)69432-3
  11. Corley, M., Burns, M. C. and Yeo, G. W. 2020. How RNA-binding proteins interact with RNA: molecules and mechanisms. Mol. Cell 78:9-29. https://doi.org/10.1016/j.molcel.2020.03.011
  12. Dammann, R., Lucchini, R., Koller, T. and Sogo, J. M. 1993. Chromatin structures and transcription of rDNA in yeast Saccharomyces cerevisiae. Nucleic Acids Res. 21:2331-2338. https://doi.org/10.1093/nar/21.10.2331
  13. Decatur, W. A. and Fournier, M. J. 2002. rRNA modifications and ribosome function. Trends Biochem. Sci. 27:344-351. https://doi.org/10.1016/S0968-0004(02)02109-6
  14. Dominissini, D., Moshitch-Moshkovitz, S., Schwartz, S., Salmon-Divon, M., Ungar, L., Osenberg, S., Cesarkas, K., JacobHirsch, J., Amariglio, N., Kupiec, M., Sorek, R. and Rechavi, G. 2012. Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 485:201-206. https://doi.org/10.1038/nature11112
  15. Dominissini, D., Nachtergaele, S., Moshitch-Moshkovitz, S., Peer, E., Kol, N., Ben-Haim, M. S., Dai, Q., Di Segni, A., Salmon-Divon, M., Clark, W. C., Zheng, G., Pan, T., Solomon, O., Eyal, E., Hershkovitz, V., Han, D., Dore, L. C., Amariglio, N., Rechavi, G. and He, C. 2016. The dynamic N1-methyladenosine methylome in eukaryotic messenger RNA. Nature 530:441-446. https://doi.org/10.1038/nature16998
  16. Du, H., Zhao, Y., He, J., Zhang, Y., Xi, H., Liu, M., Ma, J. and Wu, L. 2016. YTHDF2 destabilizes m6 A-containing RNA through direct recruitment of the CCR4-NOT deadenylase complex. Nat. Commun. 7:12626. https://doi.org/10.1038/ncomms12626
  17. Engelke, D. R. and Hopper, A. K. 2006. Modified view of tRNA: stability amid sequence diversity. Mol. Cell 21:144-145. https://doi.org/10.1016/j.molcel.2006.01.002
  18. Fernandez, I. S., Ng, C. L., Kelley, A. C., Wu, G., Yu, Y.-T. and Ramakrishnan, V. 2013. Unusual base pairing during the decoding of a stop codon by the ribosome. Nature 500:107-110. https://doi.org/10.1038/nature12302
  19. Frye, M., Harada, B. T., Behm, M. and He, C. 2018. RNA modifications modulate gene expression during development. Science 361:1346-1349. https://doi.org/10.1126/science.aau1646
  20. Gagliardi, D. and Dziembowski, A. 2018. 5' and 3' modifications controlling RNA degradation: from safeguards to executioners. Philos. Trans. R. Soc. Lond. B Biol. Sci. 373:20180160. https://doi.org/10.1098/rstb.2018.0160
  21. Ghildiyal, M. and Zamore, P. D. 2009. Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 10:94-108. https://doi.org/10.1038/nrg2504
  22. Helm, M. and Motorin, Y. 2017. Detecting RNA modifications in the epitranscriptome: predict and validate. Nat. Rev. Genet. 18:275-291. https://doi.org/10.1038/nrg.2016.169
  23. Hussain, S., Sajini, A. A., Blanco, S., Dietmann, S., Lombard, P., Sugimoto, Y., Paramor, M., Gleeson, J. G., Odom, D. T., Ule, J. and Frye, M. 2013. NSun2-mediated cytosine-5 methylation of vault noncoding RNA determines its processing into regulatory small RNAs. Cell Rep. 4:255-261. https://doi.org/10.1016/j.celrep.2013.06.029
  24. Jia, G., Fu, Y. and He, C. 2013. Reversible RNA adenosine methylation in biological regulation. Trends Genet. 29:108-115. https://doi.org/10.1016/j.tig.2012.11.003
  25. Krutyholowa, R., Zakrzewski, K. and Glatt, S. 2019. Charging the code - tRNA modification complexes. Curr. Opin. Struct. Biol. 55:138-146. https://doi.org/10.1016/j.sbi.2019.03.014
  26. Li, X., Xiong, X., Wang, K., Wang, L., Shu, X., Ma, S. and Yi, C. 2016. Transcriptome-wide mapping reveals reversible and dynamic N1-methyladenosine methylome. Nat. Chem. Biol. 12:311-316. https://doi.org/10.1038/nchembio.2040
  27. Liu, H., Li, Y., Chen, D., Qi, Z., Wang, Q., Wang, J., Jiang, C. and Xu, J.-R. 2017. A-to-I RNA editing is developmentally regulated and generally adaptive for sexual reproduction in Neurospora crassa. Proc. Natl. Acad. Sci. U. S. A. 114:E7756-E7765.
  28. Liu, H., Wang, Q., He, Y., Chen, L., Hao, C., Jiang, C., Li, Y., Dai, Y., Kang, Z. and Xu, J.-R. 2016. Genome-wide A-to-I RNA editing in fungi independent of ADAR enzymes. Genome Res. 26:499-509. https://doi.org/10.1101/gr.199877.115
  29. Lyons, S. M., Fay, M. M. and Ivanov, P. 2018. The role of RNA modifications in the regulation of tRNA cleavage. FEBS Lett. 592:2828-2844. https://doi.org/10.1002/1873-3468.13205
  30. Motorin, Y. and Marchand, V. 2021. Analysis of RNA modifications by second- and third-generation deep sequencing: 2020 update. Genes 12:278. https://doi.org/10.3390/genes12020278
  31. O'Brien, J., Hayder, H., Zayed, Y. and Peng, C. 2018. Overview of microRNA biogenesis, mechanisms of actions, and circulation. Front. Endocrinol. 9:402. https://doi.org/10.3389/fendo.2018.00402
  32. Ovcharenko, A. and Rentmeister, A. 2018. Emerging approaches for detection of methylation sites in RNA. Open Biol. 8:180121. https://doi.org/10.1098/rsob.180121
  33. Proudfoot, N. J., Furger, A. and Dye, M. J. 2002. Integrating mRNA processing with transcription. Cell 108:501-512. https://doi.org/10.1016/S0092-8674(02)00617-7
  34. Razin, A. and Kantor, B. 2005. DNA methylation in epigenetic control of gene expression. Prog. Mol. Subcell. Biol. 38:151-167. https://doi.org/10.1007/3-540-27310-7_6
  35. Rintala-Dempsey, A. C. and Kothe, U. 2017. Eukaryotic standalone pseudouridine synthases - RNA modifying enzymes and emerging regulators of gene expression? RNA Biol. 14:1185-1196. https://doi.org/10.1080/15476286.2016.1276150
  36. Roundtree, I. A., Evans, M. E., Pan, T. and He, C. 2017. Dynamic RNA modifications in gene expression regulation. Cell 169:1187-1200. https://doi.org/10.1016/j.cell.2017.05.045
  37. Samuel, C. E. 2003. RNA editing minireview series. J. Biol. Chem. 278:1389-1390. https://doi.org/10.1074/jbc.R200032200
  38. Schibler, U., Kelley, D. E. and Perry, R. P. 1977. Comparison of methylated sequences in messenger RNA and heterogeneous nuclear RNA from mouse L cells. J. Mol. Biol. 115:695-714. https://doi.org/10.1016/0022-2836(77)90110-3
  39. Shelton, S. B., Reinsborough, C. and Xhemalce, B. 2016. Who watches the watchmen: roles of RNA modifications in the RNA interference pathway. PLoS Genet. 12:e1006139. https://doi.org/10.1371/journal.pgen.1006139
  40. Shi, Y., Wang, H., Wang, J., Liu, X., Lin, F. and Lu, J. 2019. N6-methyladenosine RNA methylation is involved in virulence of the rice blast fungus Pyricularia oryzae (syn. Magnaporthe oryzae). FEMS Microbiol. Lett. 366:fny286.
  41. Sledz, P. and Jinek, M. 2016. Structural insights into the molecular mechanism of the m6 A writer complex. elife 5:e18434. https://doi.org/10.7554/elife.18434
  42. Sloan, K. E., Warda, A. S., Sharma, S., Entian, K.-D., Lafontaine, D. L. J. and Bohnsack, M. T. 2017. Tuning the ribosome: the influence of rRNA modification on eukaryotic ribosome biogenesis and function. RNA Biol. 14:1138-1152. https://doi.org/10.1080/15476286.2016.1259781
  43. Tartaglia, G. G. 2016. The grand challenge of characterizing ribonucleoprotein networks. Front. Mol. Biosci. 3:24. https://doi.org/10.3389/fmolb.2016.00024
  44. Teichert, I., Dahlmann, T. A., Kuck, U. and Nowrousian, M. 2017. RNA editing during sexual development occurs in distantly related filamentous ascomycetes. Genome Biol. Evol. 9:855-868. https://doi.org/10.1093/gbe/evx052
  45. Thompson, D. M. and Parker, R. 2009. Stressing out over tRNA cleavage. Cell 138:215-219. https://doi.org/10.1016/j.cell.2009.07.001
  46. Torres, A. G., Pineyro, D., Filonava, L., Stracker, T. H., Batlle, E. and Ribas de Pouplana, L. 2014. A-to-I editing on tRNAs: biochemical, biological and evolutionary implications FEBS Lett. 588:4279-4286. https://doi.org/10.1016/j.febslet.2014.09.025
  47. Wilkinson, M. E., Charenton, C. and Nagai, K. 2020. RNA splicing by the spliceosome. Annu. Rev. Biochem. 89:359-388. https://doi.org/10.1146/annurev-biochem-091719-064225
  48. Wu, B., Gaskell, J., Held, B. W., Toapanta, C., Vuong, T. V., Ahrendt, S., Lipzen, A., Zhang, J., Schilling, J. S., Master, E., Grigoriev, I. V., Blanchette, R. A., Cullen, D. and Hibbett, D. S. 2021. Retracted and republished from: "substrate-specific differential gene expression and RNA editing in the brown rot fungus Fomitopsis pinicola". Appl. Environ. Microbiol. 87:e0032921. https://doi.org/10.1128/AEM.00329-21
  49. Wu, B., Gaskell, J., Zhang, J., Toapanta, C., Ahrendt, S., Grigoriev, I. V., Blanchette, R. A., Schilling, J. S., Master, E., Cullen, D. and Hibbett, D. S. 2019. Evolution of substratespecific gene expression and RNA editing in brown rot wooddecaying fungi. ISME J. 13:1391-1403. https://doi.org/10.1038/s41396-019-0359-2
  50. Yang, X., Yang, Y., Sun, B.-F., Chen, Y.-S., Xu, J.-W., Lai, W.-Y., Li, A., Wang, X., Bhattarai, D. P., Xiao, W., Sun, H.-Y., Zhu, Q., Ma, H.-L., Adhikari, S., Sun, M., Hao, Y.-J., Zhang, B., Huang, C.-M., Huang, N., Jiang, G.-B., Zhao, Y.-L., Wang, H.-L., Sun, Y.-P. and Yang, Y.-G. 2017. 5-methylcytosine promotes mRNA export - NSUN2 as the methyltransferase and ALYREF as an m5C reader. Cell Res. 27:606-625. https://doi.org/10.1038/cr.2017.55
  51. Yu, B. and Chen, X. 2010. Analysis of miRNA modifications. Methods Mol. Biol. 592:137-148. https://doi.org/10.1007/978-1-60327-005-2_10
  52. Zheng, G., Dahl, J. A., Niu, Y., Fedorcsak, P., Huang, C.-M., Li, C. J., Vagbo, C. B., Shi, Y., Wang, W.-L., Song, S.-H., Lu, Z., Bosmans, R. P. G., Dai, Q., Hao, Y.-J., Yang, X., Zhao, W.-M., Tong, W.-M., Wang, X.-J., Bogdan, F., Furu, K., Fu, Y., Jia, G., Zhao, X., Liu, J., Krokan, H. E., Klungland, A., Yang, Y.-G. and He, C. 2013. ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility. Mol. Cell 49:18-29. https://doi.org/10.1016/j.molcel.2012.10.015