A trans-activator-like structure in RCNMV RNA1 evokes the origin of the trans-activator in RNA2


Autoři: Laura R. Newburn aff001;  K. Andrew White aff001
Působiště autorů: Department of Biology, York University, Toronto, Ontario, Canada aff001
Vyšlo v časopise: A trans-activator-like structure in RCNMV RNA1 evokes the origin of the trans-activator in RNA2. PLoS Pathog 16(1): e1008271. doi:10.1371/journal.ppat.1008271
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.ppat.1008271

Souhrn

The Red clover necrotic mosaic virus (RCNMV) genome consists of two plus-strand RNA genome segments, RNA1 and RNA2. RNA2 contains a multifunctional RNA structure known as the trans-activator (TA) that (i) promotes subgenomic mRNA transcription from RNA1, (ii) facilitates replication of RNA2, and (iii) mediates particle assembly and copackaging of genome segments. The TA has long been considered a unique RNA element in RCNMV. However, by examining results from RCNMV genome analyses in the ViRAD virus (re-)annotation database, a putative functional RNA element in the polymerase-coding region of RNA1 was identified. Structural and functional analyses revealed that the novel RNA element adopts a TA-like structure (TALS) and, similar to the requirement of the TA for RNA2 replication, the TALS is necessary for the replication of RNA1. Both the TA and TALS possess near-identical asymmetrical internal loops that are critical for efficient replication of their corresponding genome segments, and these structural motifs were found to be functionally interchangeable. Moreover, replacement of the TA in RNA2 with a stabilized form of the TALS directed both RNA2 replication and packaging of both genome segments. Based on their comparable properties and considering evolutionary factors, we propose that the TALS appeared de novo in RNA1 first and, subsequently, the TA arose de novo in RNA2 as a functional mimic of the TALS. This and other related information were used to formulate a plausible evolutionary pathway to describe the genesis of the bi-segmented RCNMV genome. The resulting scenario provides an evolutionary framework to further explore and test possible origins of this segmented RNA plant virus.

Klíčová slova:

Messenger RNA – Northern blot – RNA analysis – RNA structure – RNA synthesis – RNA viruses – Viral genomics – Viral replication


Zdroje

1. Sit TL, Lommel SA. “Tombusviridae”. In Encyclopedia of Life Sciences (ELS). Chichester: John Wiley & Sons, Ltd. 2010; doi: 10.1002/9780470015902.a0000756.pub2

2. Okuno T, Hiruki C. Molecular biology and epidemiology of dianthoviruses. Adv Virus Res. 2013; 87:37–74. doi: 10.1016/B978-0-12-407698-3.00002-8 23809920

3. Xiong Z, Lommel SA. The complete nucleotide sequence and genome organization of red clover necrotic mosaic virus RNA-1. Virology. 1989; 171(2):543–554. doi: 10.1016/0042-6822(89)90624-7 2763465

4. Kendall TL, Lommel SA. Nucleotide sequence of carnation ringspot dianthovirus RNA-2. J Gen Virol. 1992; 73(Pt 9):2479–2482.

5. Mizumoto H, Tatsuta M, Kaido M, Mise K, Okuno T. Cap-independent translational enhancement by the 3' untranslated region of red clover necrotic mosaic virus RNA1. J Virol. 2003; 77(22):12113–12121. doi: 10.1128/JVI.77.22.12113-12121.2003 14581548

6. Iwakawa HO, Tajima Y, Taniguchi T, Kaido M, Mise K, Tomari Y, Taniguchi H, Okuno T. Poly(A)-binding protein facilitates translation of an uncapped/nonpolyadenylated viral RNA by binding to the 3' untranslated region. J Virol. 2012; 86(15):7836–7849. doi: 10.1128/JVI.00538-12 22593149

7. Mizumoto H, Iwakawa HO, Kaido M, Mise K, Okuno T. Cap-independent translation mechanism of red clover necrotic mosaic virus RNA2 differs from that of RNA1 and is linked to RNA replication. J Virol. 2006; 80(8):3781–3791. doi: 10.1128/JVI.80.8.3781-3791.2006 16571795

8. Kusumanegara K, Mine A, Hyodo K, Kaido M, Mise K, Okuno T. Identification of domains in p27 auxiliary replicase protein essential for its association with the endoplasmic reticulum membranes in Red clover necrotic mosaic virus. Virology. 2012; 433(1):131–141. doi: 10.1016/j.virol.2012.07.017 22898643

9. Hyodo K, Mine A, Iwakawa HO, Kaido M, Mise K, Okuno T. Identification of amino acids in auxiliary replicase protein p27 critical for its RNA-binding activity and the assembly of the replicase complex in Red clover necrotic mosaic virus. Virology. 2011; 413(2):300–309. doi: 10.1016/j.virol.2011.02.017 21440279

10. Mine A, Hyodo K, Takeda A, Kaido M, Mise K, Okuno T. Interactions between p27 and p88 replicase proteins of Red clover necrotic mosaic virus play an essential role in viral RNA replication and suppression of RNA silencing via the 480-kDa viral replicase complex assembly. Virology. 2010; 407(2):213–224. doi: 10.1016/j.virol.2010.07.038 20828775

11. Mine A, Takeda A, Taniguchi T, Taniguchi H, Kaido M, Mise K, Okuno T.Identification and characterization of the 480-kilodalton template-specific RNA-dependent RNA polymerase complex of red clover necrotic mosaic virus. J Virol. 2010; 84(12):6070–6081. doi: 10.1128/JVI.00054-10 20375154

12. Tajima Y, Iwakawa HO, Kaido M, Mise K, Okuno T. A long-distance RNA-RNA interaction plays an important role in programmed -1 ribosomal frameshifting in the translation of p88 replicase protein of Red clover necrotic mosaic virus. Virology. 2011; 417(1):169–178. doi: 10.1016/j.virol.2011.05.012 21703656

13. Sit TL, Vaewhongs AA, Lommel SA. RNA-mediated trans-activation of transcription from a viral RNA. Science. 1998; 281(5378):829–832. doi: 10.1126/science.281.5378.829 9694655

14. Xiong Z, Kim KH, Giesman-Cookmeyer D, Lommel SA. The roles of the red clover necrotic mosaic virus capsid and cell-to-cell movement proteins in systemic infection. Virology. 1993; 192(1):27–32. doi: 10.1006/viro.1993.1004 8517020

15. Guenther RH, Sit TL, Gracz HS, Dolan MA, Townsend HL, Liu G, Newman WH, Agris PF, Lommel SA. Structural characterization of an intermolecular RNA-RNA interaction involved in the transcription regulation element of a bipartite plant virus. Nucleic Acids Res. 2004; 32(9):2819–2828. doi: 10.1093/nar/gkh585 15155850

16. Basnayake VR, Sit TL, Lommel SA. The genomic RNA packaging scheme of Red clover necrotic mosaic virus. Virology. 2006; 345(2):532–539. doi: 10.1016/j.virol.2005.10.017 16297955

17. Basnayake VR, Sit TL, Lommel SA. The Red clover necrotic mosaic virus origin of assembly is delimited to the RNA-2 trans-activator. Virology. 2009; 384(1):169–178. doi: 10.1016/j.virol.2008.11.005 19062064

18. Park SH, Sit TL, Kim KH, Lommel SA. The red clover necrotic mosaic virus capsid protein N-terminal amino acids possess specific RNA binding activity and are required for stable virion assembly. Virus Res. 2013; 176(1–2):107–118. doi: 10.1016/j.virusres.2013.05.014 23747688

19. Tatsuta M, Mizumoto H, Kaido M, Mise K, Okuno T. The red clover necrotic mosaic virus RNA2 trans-activator is also a cis-acting RNA2 replication element. J Virol. 2005; 79(2):978–986. doi: 10.1128/JVI.79.2.978-986.2005 15613326

20. Firth AE. Mapping overlapping functional elements embedded within the protein-coding regions of RNA viruses. Nucleic Acids Res. 2014; 42(20):12425–12439. doi: 10.1093/nar/gku981 25326325

21. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003; 31(13):3406–3415. doi: 10.1093/nar/gkg595 12824337

22. Iwakawa HO, Mizumoto H, Nagano H, Imoto Y, Takigawa K, Sarawaneeyaruk S, Kaido M, Mise K, Okuno T. A viral noncoding RNA generated by cis-element-mediated protection against 5'->3' RNA decay represses both cap-independent and cap-dependent translation. J Virol. 2008; 82(20):10162–10174. doi: 10.1128/JVI.01027-08 18701589

23. Gunawardene CD, Jaluba K, White KA. Conserved motifs in a tombusvirus polymerase modulate genome replication, subgenomic transcription, and amplification of defective interfering RNAs. J Virol. 2015; 89(6):3236–3246. doi: 10.1128/JVI.03378-14 25568204

24. Nicholson BL, Lee PK, White KA. Internal RNA replication elements are prevalent in Tombusviridae. Front Microbiol. 2012; 3:279. doi: 10.3389/fmicb.2012.00279 22888327

25. Monkewich S, Lin HX, Fabian MR, Xu W, Na H, Ray D, Chernysheva OA, Nagy PD, White KA. The p92 polymerase coding region contains an internal RNA element required at an early step in Tombusvirus genome replication. J Virol. 2005; 79(8):4848–4858. doi: 10.1128/JVI.79.8.4848-4858.2005 15795270

26. Pogany J, White KA, Nagy PD. Specific binding of tombusvirus replication protein p33 to an internal replication element in the viral RNA is essential for replication. J Virol. 2005; 79(8):4859–4869. doi: 10.1128/JVI.79.8.4859-4869.2005 15795271

27. Wu B, Pogany J, Na H, Nicholson BL, Nagy PD, White KA. A discontinuous RNA platform mediates RNA virus replication: building an integrated model for RNA-based regulation of viral processes. PLoS Pathog. 2009; 5(3):e1000323. doi: 10.1371/journal.ppat.1000323 19266082

28. Iwakawa HO, Mine A, Hyodo K, An M, Kaido M, Mise K, Okuno T. Template recognition mechanisms by replicase proteins differ between bipartite positive-strand genomic RNAs of a plant virus. J Virol. 2011; 85(1):497–509. doi: 10.1128/JVI.01754-10 20980498

29. Hyodo K, Okuno T. Pathogenesis mediated by proviral host factors involved in translation and replication of plant positive-strand RNA viruses. Curr Opin Virol. 2016; 17:11–18. doi: 10.1016/j.coviro.2015.11.004 26651023

30. Taliansky ME, Robinson DJ. Molecular biology of umbraviruses: phantom warriors. J Gen Virol. 2003; 84(Pt 8):1951–1960. doi: 10.1099/vir.0.19219-0 12867625

31. Falk BW, Tian T, Yeh HH. Luteovirus-associated viruses and subviral RNAs. Curr Top Microbiol Immunol. 1999; 239:159–175. doi: 10.1007/978-3-662-09796-0_9 9893374

32. White KA, Morris TJ. Nonhomologous RNA recombination in tombus- viruses: generation and evolution of defective interfering RNAs by stepwise deletions. J Virol. 1994; 68:14–24. 8254723

33. Mathews DH, Sabina J, Zuker M, Turner DH. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol. 1999; 288(5):911–940. doi: 10.1006/jmbi.1999.2700 10329189

34. Newburn LR, White KA. Atypical RNA Elements Modulate Translational Readthrough in Tobacco Necrosis Virus D. J Virol. 2017; 91(8):e02443–16. doi: 10.1128/JVI.02443-16 28148800

35. Vasa SM, Guex N, Wilkinson KA, Weeks KM, Giddings MC. ShapeFinder: a software system for high-throughput quantitative analysis of nucleic acid reactivity information resolved by capillary electrophoresis. RNA. 2008; 14(10):1979–1990. doi: 10.1261/rna.1166808 18772246

36. Choi IR, Ostrovsky M, Zhang G, White KA. Regulatory activity of distal and core RNA elements in Tombusvirus subgenomic mRNA2 transcription. J Biol Chem. 2001; 276(45):41761–41768. doi: 10.1074/jbc.M106727200 11546813

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2020 Číslo 1

Najčítanejšie v tomto čísle

Tejto téme sa ďalej venujú…


Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Význam nutraceutik u kardiovaskulárních onemocnění
nový kurz
Autori:

Faktory ovlivňující léčbu levotyroxinem

Kurz originály vs. generika

Autori: MUDr. Petr Výborný, CSc., FEBO

Autori: MUDr. Jiří Horažďovský, Ph.D

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Nemáte účet?  Registrujte sa

Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa