Short ORF-Dependent Ribosome Shunting Operates in an RNA Picorna-Like Virus and a DNA Pararetrovirus that Cause Rice Tungro Disease

English version České info

Rice tungro disease is caused by synergistic interaction of an RNA picorna-like virus Rice tungro spherical virus (RTSV) and a DNA pararetrovirus Rice tungro bacilliform virus (RTBV). It is spread by insects owing to an RTSV-encoded transmission factor. RTBV has evolved a ribosome shunt mechanism to initiate translation of its pregenomic RNA having a long and highly structured leader. We found that a long leader of RTSV genomic RNA remarkably resembles the RTBV leader: both contain several short ORFs (sORFs) and potentially fold into a large stem-loop structure with the first sORF terminating in front of the stem basal helix. Using translation assays in rice protoplasts and wheat germ extracts, we show that, like in RTBV, both initiation and proper termination of the first sORF translation in front of the stem are required for shunt-mediated translation of a reporter ORF placed downstream of the RTSV leader. The base pairing that forms the basal helix is required for shunting, but its sequence can be varied. Shunt efficiency in RTSV is lower than in RTBV. But in addition to shunting the RTSV leader sequence allows relatively efficient linear ribosome migration, which also contributes to translation initiation downstream of the leader. We conclude that RTSV and RTBV have developed a similar, sORF-dependent shunt mechanism possibly to adapt to the host translation system and/or coordinate their life cycles. Given that sORF-dependent shunting also operates in a pararetrovirus Cauliflower mosaic virus and likely in other pararetroviruses that possess a conserved shunt configuration in their leaders it is tempting to propose that RTSV may have acquired shunt cis-elements from RTBV during their co-existence.

Vyšlo v časopise: Short ORF-Dependent Ribosome Shunting Operates in an RNA Picorna-Like Virus and a DNA Pararetrovirus that Cause Rice Tungro Disease. PLoS Pathog 8(3): e32767. doi:10.1371/journal.ppat.1002568
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002568

Souhrn

Zdroje

1. HullR 1996 Molecular biology of rice tungro viruses. Annu Rev Phytopathol 34 275 297

2. SanfaçonHWellinkJLe GallOKarasevAvan der VlugtR 2009 Secoviridae: a proposed family of plant viruses within the order Picornavirales that combines the families Sequiviridae and Comoviridae, the unassigned genera Cheravirus and Sadwavirus, and the proposed genus Torradovirus. Arch Virol 154 899 907

3. ShenPKaniewskaMSmithCBeachyRN 1993 Nucleotide sequence and genomic organization of rice tungro spherical virus. Virology 193 621 30

4. Thiébeauld de la CrouéeOPoogginMMRyabovaLA 2007 Alternative translation strategies in plant viruses. Plant Viruses 1 20 The Global Science Books

5. BelshamGJ 2009 Divergent picornavirus IRES elements. Virus Res 139 183 92

6. KnellerELRakotondrafaraAMMillerWA 2006 Cap-independent translation of plant viral RNAs. Virus Res 119 63 75

7. FüttererJKiss-LaszloZHohnT 1993 Nonlinear ribosome migration on cauliflower mosaic virus 35S RNA. Cell 73 789 802

8. FüttererJPotrykusIBaoYLiLBurnsTM 1996 Position-dependent ATT initiation during plant pararetrovirus rice tungro bacilliform virus translation. J Virol 70 2999 3010

9. PoogginMMFüttererJSkryabinKGHohnT 1999 A short open reading frame terminating in front of a stable hairpin is the conserved feature in pregenomic RNA leaders of plant pararetroviruses. J Gen Virol 80 2217 2228

10. RyabovaLAPoogginMMHohnT 2002 Viral strategies of translation initiation: ribosomal shunt and reinitiation. Prog Nucleic Acid Res Mol Biol 72 1 39

11. HullR 2007 Caulimoviridae (Plant Pararetroviruses). eLS John Wiley & Sons Ltd, Chichester http://www.els.net [doi: 10.1002/9780470015902.a0000746.pub2]

12. FüttererJRothnieHMHohnTPotrykusI 1997 Rice tungro bacilliform virus open reading frames II and III are translated from polycistronic pregenomic RNA by leaky scanning. J Virol 71 7984 9

13. PoogginMMRyabovaLAHohnT 2002 Translation strategies in members of the family Caulimoviridae. KhanJADijkstraJ Plant viruses as molecular pathogens New York Haworth Press Inc 317 338

14. FüttererJPotrykusIValles BrauMPDasguptaIHullR 1994 Splicing in a plant pararetrovirus. Virology 198 663 670

15. PoogginMMRyabovaLAHeXFuttererJHohnT 2006 Mechanism of ribosome shunting in Rice tungro bacilliform pararetrovirus. RNA 12 841 850

16. PoogginMMFüttererJHohnT 2008 Cross-species functionality of pararetroviral elements driving ribosome shunting. PLoS One 3 e1650

17. SchepetilnikovMSchottGKatsarouKThiébeauldOKellerM 2009 Molecular dissection of the prototype foamy virus (PFV) RNA 5′-UTR identifies essential elements of a ribosomal shunt. Nucleic Acids Res 37 5838 5847

18. SherrillKWLloydRE 2008 Translation of cIAP2 mRNA is mediated exclusively by a stress-modulated ribosome shunt. Mol Cell Biol 28 2011 22

19. DominguezDIRyabovaLAPoogginMMSchmidt-PuchtaWFüttererJ 1998 Ribosome shunting in cauliflower mosaic virus. Identification of an essential and sufficient structural element. J Biol Chem 273 3669 78

20. PoogginMMHohnTFüttererJ 2000 Role of a short open reading frame in ribosome shunt on the cauliflower mosaic virus RNA leader. J Biol Chem 275 17288 17296

21. PoogginMMFüttererJSkryabinKGHohnT 2001 Ribosome shunt is essential for infectivity of cauliflower mosaic virus. Proc Natl Acad Sci U S A 98 886 891

22. Hemmings-MieszczakMHohnT 1999 A stable hairpin preceded by a short open reading frame promotes nonlinear ribosome migration on a synthetic mRNA leader. RNA 5 1149 57

23. RyabovaLAHohnT 2000 Ribosome shunting in the cauliflower mosaic virus 35S RNA leader is a special case of reinitiation of translation functioning in plant and animal systems. Genes Dev 14 817 29

24. RyabovaLAPoogginMDominguezDHohnT 2000 Continuous and Discontinuous Ribosome Scanning on the Cauliflower Mosaic Virus 35 S RNA Leader Is Controlled by Short Open Reading Frames J Biol Chem 275 37278 37284

25. KozakM 1986 Influences of mRNA secondary structure on initiation by eukaryotic ribosomes. Proc Natl Acad Sci U S A 83 2850 4

26. Guerra-PerazaOde TapiaMHohnTHemmings-MieszczakM 2000 Interaction of the cauliflower mosaic virus coat protein with the pregenomic RNA leader. J Virol 74 2067 2072

27. BlevinsTRajeswaranRAreggerMBorahBKSchepetilnikovM 2011 Massive production of small RNAs from a non-coding region of Cauliflower mosaic virus in plant defense and viral counter-defense. Nucleic Acids Res 39 5003 5014

28. SeffensWDigbyD 1999 mRNAs have greater negative folding free energies than shuffled or codon choice randomized sequences. Nucleic Acids Res 27 1578 84

29. Hemmings-MieszczakMStegerGHohnT 1997 Alternative structures of the cauliflower mosaic virus 35 S RNA leader: implications for viral expression and replication. J Mol Biol 267 1075 88