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http://dx.doi.org/10.5423/PPJ.RW.07.2021.0111

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)
Publication Information
The Plant Pathology Journal / v.37, no.6, 2021 , pp. 505-511 More about this Journal
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
epitranscriptome; plant pathogenic fungi; RNA modification;
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1 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.   DOI
2 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.   DOI
3 Christofi, T. and Zaravinos, A. 2019. RNA editing in the forefront of epitranscriptomics and human health. J. Transl. Med. 17:319.   DOI
4 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.   DOI
5 Helm, M. and Motorin, Y. 2017. Detecting RNA modifications in the epitranscriptome: predict and validate. Nat. Rev. Genet. 18:275-291.   DOI
6 Krutyholowa, R., Zakrzewski, K. and Glatt, S. 2019. Charging the code - tRNA modification complexes. Curr. Opin. Struct. Biol. 55:138-146.   DOI
7 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.   DOI
8 O'Brien, J., Hayder, H., Zayed, Y. and Peng, C. 2018. Overview of microRNA biogenesis, mechanisms of actions, and circulation. Front. Endocrinol. 9:402.   DOI
9 Sledz, P. and Jinek, M. 2016. Structural insights into the molecular mechanism of the m6 A writer complex. elife 5:e18434.   DOI
10 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.   DOI
11 Tartaglia, G. G. 2016. The grand challenge of characterizing ribonucleoprotein networks. Front. Mol. Biosci. 3:24.   DOI
12 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.   DOI
13 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.   DOI
14 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.   DOI
15 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.   DOI
16 Thompson, D. M. and Parker, R. 2009. Stressing out over tRNA cleavage. Cell 138:215-219.   DOI
17 Wilkinson, M. E., Charenton, C. and Nagai, K. 2020. RNA splicing by the spliceosome. Annu. Rev. Biochem. 89:359-388.   DOI
18 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.   DOI
19 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.   DOI
20 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.   DOI
21 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.
22 Ovcharenko, A. and Rentmeister, A. 2018. Emerging approaches for detection of methylation sites in RNA. Open Biol. 8:180121.   DOI
23 Proudfoot, N. J., Furger, A. and Dye, M. J. 2002. Integrating mRNA processing with transcription. Cell 108:501-512.   DOI
24 Razin, A. and Kantor, B. 2005. DNA methylation in epigenetic control of gene expression. Prog. Mol. Subcell. Biol. 38:151-167.   DOI
25 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.   DOI
26 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.   DOI
27 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.   DOI
28 Roundtree, I. A., Evans, M. E., Pan, T. and He, C. 2017. Dynamic RNA modifications in gene expression regulation. Cell 169:1187-1200.   DOI
29 Samuel, C. E. 2003. RNA editing minireview series. J. Biol. Chem. 278:1389-1390.   DOI
30 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.   DOI
31 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.   DOI
32 Motorin, Y. and Marchand, V. 2021. Analysis of RNA modifications by second- and third-generation deep sequencing: 2020 update. Genes 12:278.   DOI
33 Frye, M., Harada, B. T., Behm, M. and He, C. 2018. RNA modifications modulate gene expression during development. Science 361:1346-1349.   DOI
34 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.   DOI
35 Decatur, W. A. and Fournier, M. J. 2002. rRNA modifications and ribosome function. Trends Biochem. Sci. 27:344-351.   DOI
36 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.   DOI
37 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.   DOI
38 Engelke, D. R. and Hopper, A. K. 2006. Modified view of tRNA: stability amid sequence diversity. Mol. Cell 21:144-145.   DOI
39 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.   DOI
40 Adler, M., Weissmann, B. and Gutman, A. B. 1958. Occurrence of methylated purine bases in yeast ribonucleic acid. J. Biol. Chem. 230:717-723.   DOI
41 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.   DOI
42 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.   DOI
43 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.   DOI
44 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.   DOI
45 Yu, B. and Chen, X. 2010. Analysis of miRNA modifications. Methods Mol. Biol. 592:137-148.   DOI
46 Cohn, W. E. 1960. Pseudouridine, a carbon-carbon linked ribonucleoside in ribonucleic acids: isolation, structure, and chemical characteristics. J. Biol. Chem. 235:1488-1498.   DOI
47 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.   DOI
48 Jia, G., Fu, Y. and He, C. 2013. Reversible RNA adenosine methylation in biological regulation. Trends Genet. 29:108-115.   DOI
49 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.   DOI
50 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.
51 Ghildiyal, M. and Zamore, P. D. 2009. Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 10:94-108.   DOI
52 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.   DOI