Co-inoculation with two non-infectious cDNA copies of potato spindle tuber viroid (PSTVd) leads to the appearance of novel fully infectious variants.
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Potato spindle tuber viroid (PSTVd) is one of the smallest (about 360 nt) infectious plant agents. It is composed of a single-stranded circular non-coding RNA molecule. In the course of previous passage experiments with two intermediate PSTVd variants I2 and I4, three non-infectious clones (I2-50, I4-37 and I4 VI-17) were found. When inoculated separately as cDNAs on tomato "Rutgers" test plants these variants did not induce any visible disease symptoms and did not produce progeny. The presence of such non-infectious variants raises several questions about their origin and biology and to answer them, mixed co-infections with cDNA copies of two non-infectious variants (I2-50, I4-37) were performed. PSTVd infection was observed in seven out of 30 inoculated plants. The progeny isolated from three separate plants contained novel variants, together with the parental I2 and I4 sequences. It is conceivable that the appearance of repaired PSTVd molecules, clearly capable of cell-to-cell movement leading to the systemic infection, results from recombination events. An analysis of the recombinant molecules and comparison with databases identified the specific sites responsible for the restricted infectivity of the I2-50 and I4-37 PSTVd variants. In parallel experiments in which (+) strand PSTVd infectious transcripts were used, no recombinants were observed, and the original I2-50 and I4-37 non-infectious sequences were not detected in the progeny.
- Allison R, Thompson G, Ahlquist P. (1990) Regeneration of a functional RNA virus genome by recombination between deletion mutants and requirement for cowpea chlorotic mottle virus 3a and coat genes for systemic infection. Proc Natl Acad Sci USA.; 87: 1820-4.
- Aziz R, Tepfer M. (1999) Recombination in RNA viruses and in virus-resistant transgenic plants. J Gen Virol.; 80: 1339-46.
- Baur M, Potrykus I, Paszkowski J. (1990) Intermolecular homologous recombination in plants. Mol Cell Biol.; 10: 492-500.
- Candresse T, Diener TO, Owens RA. (1990) The role of the viroid central conserved region in cDNA infectivity. Virology.; 175: 232-7.
- Carpenter CD, Simon AE. (1996) Changes in locations of crossover sites over time in de novo generated RNA recombinants. Virology.; 223: 165-73.
- De Groot MJA, Offringa R, Does MP, Hooykaas PJJ, Van den Elzen JM. (1992) Mechanisms of intermolecular homologous recombination in plants as studied with single- and double-stranded DNA molecules. Nucleic Acids Res.; 20: 2785-94.
- Diener TO. (1971) Potato spindle virus. A replicating, low molecular weight RNA. Virology.; 45: 411-28.
- Feng Q, Heinrich C, Loss P, Steger G, Po T, Riesner D. (1993) Multiple pathways of reversion in viroids for conservation of structural elements. EMBO J.; 12: 2129-39.
- Fernow KH. (1967) Tomato test plant for detecting mild strains of potato spindle tuber virus. Phytopathology.; 57: 1347-52.
- Gandia M, Duran-Vila N. (2004) Variability of the progeny of a sequence variant Citrus bent leaf viroid (CBLVd). Arch Virol.; 149: 407-16.
- Gozmanova M, Denti MA, Minkov IN, Tsagaris M, Tabler M. (2003) Characterization of RNA motif responsible for the specific interaction of potato spindle tuber viroid RNA (PSTVd) and tomato protein Virp1. Nucleic Acids Res.; 31: 5534-43.
- Gomez J, Martell M, Quer J, Cabot B, Esteban JI. (1999) Hepatitis C viral quasispecies. J Viral Hepat.; 6: 3-16.
- Góra A, Candressse T, Zagórski W. (1994) Analysis of the population structure of three phenotypically different PSTVd isolates. Arch Virol.; 138: 233-45.
- Góra-Sochacka A, Kierzek A, Candresse T, Zagórski W. (1997) The genetic stability of potato spindle tuber viroid (PSTVd) molecular variants. RNA.; 3: 68-74.
- Gross HJ, Lossow C, Jank P, Raba M, Alberty H, Sänger HL. (1978) Nucleotide sequence and secondary structure of potato spindle tuber viroid. Nature.; 273: 203-8.
- Hammond RW. (1994) Agrobacterium-mediated inoculation of PSTVd cDNAs onto tomato reveals the biological effects of apparently lethal mutations. Virology.; 201: 36-45.
- Hecker R, Wang Z, Steger G, Riesner D. (1988) Analysis of RNA structures by temperature gradient gel electrophoresis: viroid replication and processing. Gene.; 72: 59-74.
- Keese P, Symons R. (1985) Domains in viroids evidence for intermolecular RNA rearrangements and their contribution to viroid evolution. Proc Natl Acad Sci USA.; 82: 4582-6.
- Kofalvi S, Marcos J, Canizares M, Pallas V, Candresse T. (1997) Hop stunt viroid (HSVd) sequence variants from Prunus species: evidence for recombination between HSVd isolates. J Gen Virol.; 78: 3177-86.
- Lai M. (1992) RNA Recombination in animal and plant viruses. Microbiol Rev.; 56: 61-79.
- Lyznik LA, McGee JD, Tung PY, Bennetzen JL, Hodges TK. (1991) Homologous recombination between plasmid DNA molecules in maize protoplasts. Mol Gen Genet.; 230: 209-18.
- Maniataki E, Martinez de Alba AE, Gesser RS, Tabler M, Tsagris M. (2003) Viroid RNA systemic spread may depend on the interaction of a 71-nucleotide bulged hairpin with the host protein VirP1. RNA.; 9: 346-54.
- Nagy P, Simon A. (1997) New insights into mechanisms of RNA recombination. Virology.; 235: 1-9.
- Naraghi-Arani P, Daubert S, Rowhani A. (2001) Quasispecies nature of the genome of grapewine fanleaf virus. J Gen Virol.; 82: 1791-5.
- Owens RA, Yang G, Gundersen-Rindal D, Hammond RW, Candresse T, Bar-Joseph M. (2000) Both point mutation and RNA recombination contribute to the sequence diversity of citrus viroid III. Virus Genes.; 20: 243-52.
- Pellerin M, Lopez-Aguirre Y, Penin F, Dhumeaux D, Pawlotsky JM. (2004) Hepatitis C virus quasispecies variability modulates nonstructural protein 5A transcriptional activation, pointing to cellular compartmentalization of virus-host interactions. J Virol.; 78: 4617-27.
- Puchta H, Hohn B. (1991) A transient assay in plant cells reveals a positive correlation between extrachromosomal recombination rates and length of homologous overlap. Nucleic Acids Res.; 19: 2693-700.
- Pugachev KV, Guirakhoo F, Ocran SW, Mitchell F, Parsons M, Penal C, Girakhoo S, Pougatcheva SO. Arroyo J, Trent DW, Monath TP. (2004) High fidelity of yellow fever virus RNA polymerase. J Virol.; 78: 1032-8.
- Rezaian M. (1990) Australian grapevine viroid - evidence for extensive recombination between viroids. Nucleic Acids Res.; 18: 1813 -8.
- Schneider WL, Roossinck MJ. (2001) Genetic diversity in RNA virus quasispecies is controlled by host-virus interactions. J Virol.; 75: 6566-71.
- Schnölzer M, Hass B, Ramm K, Hofmann H, Sanger HL. (1985) Correlation between structure and pathogenicity of potato spindle tuber viroid (PSTVd). EMBO J.; 4: 2181-90
- Wassenegger M, Heimes S, Sänger HL. (1994) An infectious viroid RNA replicon evolved from an in vitro generated non-infectious viroid deletion mutant via a complementary deletion in vivo. EMBO J.; 13: 6172-7.
- Wełnicki M, Hiruki C. (1993) Chemiluminescent assay for the detection of viral and viroid RNAs using digoxygenin-labeled probes. In Bioluminescence and Chemiluminescence - Status Report. Szalay AA, Stanley PE, Kricka LJ. eds, pp 415-19. John Wiley, Chichester.
- White K, Morris T. (1994) Recombination between defective tombusvirus RNAs generates functional hybrid genomes. Proc Natl Acad Sci USA.; 91: 3642-6.
- Worobey M, Holmes EC. (1999) Evolutionary aspects of recombination in RNA viruses. J Gen Virol.; 80: 2535-43.
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