Interfamilial recombination between viruses led to acquisition of a novel translation-enhancing RNA element that allows resistance breaking
Article first published online: 24 DEC 2013
© 2013 The Authors. New Phytologist © 2013 New Phytologist Trust
Volume 202, Issue 1, pages 233–246, April 2014
How to Cite
Miras, M., Sempere, R. N., Kraft, J. J., Miller, W. A., Aranda, M. A. and Truniger, V. (2014), Interfamilial recombination between viruses led to acquisition of a novel translation-enhancing RNA element that allows resistance breaking. New Phytologist, 202: 233–246. doi: 10.1111/nph.12650
- Issue published online: 25 FEB 2014
- Article first published online: 24 DEC 2013
- Manuscript Accepted: 19 NOV 2013
- Manuscript Received: 30 AUG 2013
- Ministerio de Ciencia e Innovación. Grant Numbers: AGL2009-07552/AGR, EUI2009-04009
- USDA National Research Initiative. Grant Number: 2011-67012-30715
- 2005. Poinsettia latent virus is not a cryptic virus, but a natural polerovirus–sobemovirus hybrid. Virology 336: 240–250. , , , , .
- 2013. Genetic recombination in plant-infecting messenger-sense RNA viruses: overview and research perspectives. Frontiers in Plant Science 4: 68. doi: 10.3389/fpls.2013.00068. .
- 1992. Mueller′s ratchet and the advantage of sex in the RNA virus f6. Evolution 46: 289–299. , .
- 1997. The advantage of sex in the RNA phage f6. Genetics 14: 953–959. , .
- 2006. A phylogenetic survey of recombination frequency in plant RNA viruses. Archives of Virology 151: 933–946. , .
- 2002. Inter- and intramolecular recombinations in the Cucumber Mosaic Virus genome related to adaptation to Alstroemeria. Journal of Virology 76: 4119–4124. , , .
- 2008. The promiscuous evolutionary history of the family Bromoviridae. Journal of General Virology 89: 1739–1747. , .
- 2005. SAFA: semi-automated footprinting analysis software for high-throughput quantification of nucleic acid footprinting experiments. RNA 11: 344–354. , , , , .
- 2003. Nucleotide sequence and infectious transcripts from a full-length cDNA clone of the carmovirus Melon necrotic spot virus. Archives of Virology 148: 599–607. , , , .
- 2002. Spanish Melon necrotic spot virus isolate overcomes the resistance conferred by the recessive nsv gene of melon. Plant Disease 86: 694. , , , .
- 2004. Molecular characterization of a Melon necrotic spot virus strain that overcomes the resistance in melon and nonhost plants. Molecular Plant-Microbe Interactions 17: 668–675. , , , , .
- 2005. Inheritance of resistance to Watermelon mosaic virus in Cucumis melo that impairs virus accumulation, symptom expression, and aphid transmission. Phytopathology 95: 840–846. , , , .
- 1998. Carmovirus isolation and RNA extraction. In: Foster G, Taylor S, eds. Plant virology protocols. Totawa, NJ, USA: Humana Press, 211–217. , , .
- 2006. Comparative and functional genomics of closteroviruses. Virus Research 117: 38–51. , , .
- 2002. Nucleotide sequence shows that Bean leafroll virus has a Luteovirus-like genome organization. Journal of General Virology 83: 1791–1798. , , , .
- 2010. Mechanisms of viral emergence. Veterinary Research 41: 38. .
- 2006. Translational control in positive strand RNA plant viruses. Virology 344: 185–197. , .
- 2011. The evolutionary genetics of emerging plant RNA viruses. Molecular Plant-Microbe Interactions 24: 287–293. , , , , , , , , , .
- 2007. Constraints to genetic exchange support gene coadaptation in a tripartite RNA virus. PLoS Pathogens 3: e8. , , .
- 1994. Increase in the relative fitness of a plant virus RNA associated with its recombinant nature. Virology 203: 373–377. , , , , , .
- 2012. A ribosome-binding, 3′ translational enhancer has a T-shaped structure and engages in a long-distance RNA–RNA interaction. Journal of Virology 86: 9828–9842. , , , , .
- 2003. An analysis of the durability of resistance to plant viruses. Phytopathology 93: 941–952. , .
- 2006. Functional analysis of the five Melon necrotic spot virus genome-encoded proteins. Journal of General Virology 87: 2371–2380. , , .
- 2009. Mixed infections of Pepino mosaic virus strains modulate the evolutionary dynamics of this emergent virus. Journal of Virology 83: 12 378–12 387. , , , .
- 2008. Distribution and pathway for phloem-dependent movement of Melon necrotic spot virus in melon plants. Molecular Plant Pathology 9: 447–461. , , , , .
- 2008. Evolutionary history and phylogeography of human viruses. Annual Review of Microbiology 62: 307–328. .
- 2009. The evolutionary genetics of emerging viruses. Annual Review of Ecology Evolution and Systematics 40: 353–372. .
- 2012. Poly(A)-binding protein facilitates translation of an uncapped/nonpolyadenylated viral RNA by binding to the 3′ untranslated region. Journal of Virology 86: 7836–7849. , , , , , , , .
- 2010. The combined effect of environmental and host factors on the emergence of viral RNA recombinants. PLoS Pathogens 6: e1001156. , .
- 2009. Recombination between polioviruses and co-circulating Coxsackie A viruses: role in the emergence of pathogenic vaccine-derived polioviruses. PLoS Pathogens 5: e1000412. , , , , , , , , .
- 2013. Relative incidence, spatial distribution and genetic diversity of cucurbit viruses in eastern Spain. Annals of Applied Biology 162: 362–370. , , , , , , , .
- 2007. Cucurbit aphid-borne yellows virus is prevalent in field-grown cucurbit crops of southeastern Spain. Plant Disease 91: 232–238. , , , , .
- 2006. Cap-independent translation of plant viral RNAs. Virus Research 119: 63–75. , , .
- 2013. Cation-dependent folding of 3′ cap-independent translation elements facilitates interaction of a 17-nucleotide conserved sequence with eIF4G. Nucleic Acids Research 41: 3398–3413. , , , .
- 2006. Resistance to Melon necrotic spot virus in Cucumis melo L. ‘Doublon’ artificially inoculated by the fungus vector Olpidium bornovanus. Crop Protection 25: 426–431. , , , , .
- 2010. RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26: 2462–2463. , , , , , .
- 1991. The 5′-terminal sequence of Potato leafroll virus RNA: evidence of recombination between virus and host RNA. Journal of General Virology 72: 2591–2595. , .
- 2002. Barley yellow dwarf virus: Luteoviridae or Tombusviridae? Molecular Plant Pathology 3: 177–183. , , .
- 2007. The amazing diversity of cap-independent translation elements in the 3′-untranslated regions of plant viral RNAs. Biochemical Society Transactions 35: 1629–1633. , , .
- 2006. Long-distance RNA–RNA interactions in plant virus gene expression and replication. Annual Review of Phytopathology 44: 447–467. , .
- 2000. Sugarcane yellow leaf virus: an emerging virus that has evolved by recombination between luteoviral and poleroviral ancestors. Virology 269: 156–171. , , .
- 2008. Time-resolved RNA SHAPE chemistry. Journal of the American Chemical Society 130: 16 178–16 180. , .
- 2006. Genetic diversity of plant virus populations: towards hypothesis testing in molecular epidemiology. In: Karl Maramorosch AJS, Thresh JM, eds. Advances in virus research. New York, USA: Academic Press, 49–87. , , , .
- 2011. 3′ Cap-independent translation enhancers of positive-strand RNA plant viruses. Current Opinion in Virology 1: 373–380. , .
- 2010. Tombusvirus recruitment of host translational machinery via the 3′ UTR. RNA 16: 1402–1419. , , , .
- 2013. Tombusvirus Y-shaped translational enhancer forms a complex with eIF4F and can be functionally replaced by heterologous translational enhancers. Journal of Virology 87: 1872–1883. , , , , .
- 2006. An eIF4E allele confers resistance to an uncapped and non-polyadenylated RNA virus in melon. Plant Journal 48: 452–462. , , , , , , , , , et al.
- 2011. Nicotiana benthamiana resistance to non-adapted Melon necrotic spot virus results from an incompatible interaction between virus RNA and translation initiation factor 4E. Plant Journal 66: 492–501. , , , , .
- 2007. Patterns of recombination in Turnip mosaic virus genomic sequences indicate hotspots of recombination. Journal of General Virology 88: 298–315. , , , , , , .
- 2010. Long-term evolution of the Luteoviridae: time scale and mode of virus speciation. Journal of Virology 84: 6177–6187. , .
- 2008. The MC-Fold and MC-Sym pipeline infers RNA structure from sequence data. Nature 452: 51–55. , .
- 2000. Virus taxonomy: seventh report of the international committee on taxonomy of viruses. San Diego, CA, USA: Academic Press. , , , , , , , , , et al.
- 2012. Melon RNA interference (RNAi) lines silenced for Cm-eIF4E show broad virus resistance. Molecular Plant Pathology 13: 755–763. , , , , , .
- 2001. Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press. , .
- 2004. The 3′ untranslated region of Tobacco necrosis virus RNA contains a Barley yellow dwarf virus-like cap-independent translation element. Journal of Virology 78: 4655–4664. , .
- 2013. 3′ cap-independent translation enhancers of plant viruses. Annual Review of Microbiology 67: 21–42. , .
- 2008. The 3′ proximal translational enhancer of Turnip crinkle virus binds to 60S ribosomal subunits. RNA 14: 2379–2393. , , , , , , .
- 2011. Ribosome binding to a 5′ translational enhancer is altered in the presence of the 3′ untranslated region in cap-independent translation of Turnip crinkle virus. Journal of Virology 85: 4638–4653. , , , , .
- 2011. RNA-RNA recombination in plant virus replication and evolution. Annual Review of Phytopathology 49: 415–443. , , , .
- 2008. The 3′ cap-independent translation element of Barley yellow dwarf virus binds eIF4F via the eIF4G subunit to initiate translation. RNA 14: 134–147. , , , , , .
- 2008. Mechanism of plant eIF4E-mediated resistance against a Carmovirus (Tombusviridae): cap-independent translation of a viral RNA controlled in cis by an (a)virulence determinant. Plant Journal 56: 716–727. , , , .
- 2010. Structural plasticity of Barley yellow dwarf virus-like cap-independent translation elements in four genera of plant viral RNAs. Virology 402: 177–186. , , , .
- 2011. The cap-binding translation initiation factor, eIF4E, binds a pseudoknot in a viral cap-independent translation element. Structure 19: 868–880. , , , .
- 2006. Selective 2′-hydroxyl acylation analyzed by primer extension (SHAPE): quantitative RNA structure analysis at single nucleotide resolution. Nature Protocols 1: 1610–1616. , , .
- 2009. A discontinuous RNA platform mediates RNA virus replication: building an integrated model for RNA–based regulation of viral processes. PLoS Pathogens 5: e1000323. , , , , , .
- 2003. A multifunctional Turnip crinkle virus replication enhancer revealed by in vivo functional SELEX. Journal of Molecular Biology 326: 35–48. , .