1887

Abstract

Viroids, small single-stranded circular RNAs endowed with autonomous replication, are unique systems to conduct evolutionary studies of complete RNA genomes. The primary structure of 36 progeny variants of peach latent mosaic viroid (PLMVd), evolved from inoculations of the peach indicator GF-305 with four individual PLMVd cDNAs differing in their pathogenicity, has been determined. Most progeny variants had unique sequences, revealing that the extremely heterogeneous character of PLMVd natural isolates most probably results from the intrinsic ability of this RNA to accumulate changes, rather than from repeated inoculations of the same individual trees under field conditions. The structure of the populations derived from single PLMVd sequences differed according to the observed phenotype. Variant gds6 induced a reproducible symptomatic infection and gave rise to a more uniform progeny that preserves some parental features, whereas variant gds15, which induced a variable phenotype, showed a more complex behaviour, generating two distinct progenies in symptomatic and asymptomatic individual plants. Progenies derived from variants esc10 and ls11, which incited latent infections, followed a similar evolutionary pattern, leading to a population structure consisting of two main groups of variants, one of which was formed by variants closely related to the parental sequence. The evolution rate exhibited by PLMVd, considerably higher than that reported for potato spindle tuber viroid, may contribute to the fluctuating symptomatology of the severe PLMVd natural isolates. However, the polymorphism observed in PLMVd progenies does preserve some structural and functional elements previously proposed for this viroid, supporting the fact that they act as constraints limiting the genetic divergence of PLMVd quasispecies generated .

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1999-08-01
2020-01-23
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References

  1. Ambrós, S. & Flores, R. ( 1998; ). In vitro and in vivo self-cleavage of a viroid RNA with a mutation in the hammerhead catalytic pocket. Nucleic Acids Research 26, 1877-1883.[CrossRef]
    [Google Scholar]
  2. Ambrós, S., Desvignes, J. C., Llácer, G. & Flores, R. ( 1995; ). Peach latent mosaic and pear blister canker viroids: detection by molecular hybridization and relationships with specific maladies affecting peach and pear trees. Acta Horticulturae 386, 515-521.
    [Google Scholar]
  3. Ambrós, S., Hernández, C., Desvignes, J. C. & Flores, R. ( 1998; ). Genomic structure of three phenotypically different isolates of peach latent mosaic viroid: implications of the existence of constraints limiting the heterogeneity of viroid quasispecies. Journal of Virology 72, 7397-7406.
    [Google Scholar]
  4. Aranda, M. A., Fraile, A. & García-Arenal, F. ( 1993; ). Genetic variability and evolution of the satellite RNA of cucumber mosaic virus during natural epidemics. Journal of Virology 67, 5896-5901.
    [Google Scholar]
  5. Bonfiglioli, R. G., McFadden, G. I. & Symons, R. H. ( 1994; ). In situ hybridization localizes avocado sunblotch viroid on chloroplast thylakoid membranes and coconut cadang-cadang viroid in the nucleus. Plant Journal 6, 99-103.[CrossRef]
    [Google Scholar]
  6. Bonfiglioli, R. G., Webb, D. R. & Symons, R. H. ( 1996; ). Tissue and intra-cellular distribution of coconut cadang-cadang viroid and citrus exocortis viroid determined by in situ hybridization and confocal laser scanning and transmission electron microscopy. Plant Journal 9, 457-465.[CrossRef]
    [Google Scholar]
  7. Bruening, G. ( 1989; ). Compilation of self-cleaving sequences from plant virus satellite RNAs and other sources. Methods in Enzymology 180, 546-558.
    [Google Scholar]
  8. Desvignes, J. C. ( 1976; ). The virus diseases detected in greenhouse and in field by the peach seedling GF 305 indicator. Acta Horticulturae 67, 315-323.
    [Google Scholar]
  9. Diener, T. O. ( 1991; ). Subviral pathogens of plants: viroids and viroidlike satellite RNAs. FASEB Journal 5, 2808-2813.
    [Google Scholar]
  10. Diener, T. O. ( 1996; ). Origin and evolution of viroids and viroid-like satellite RNAs. Virus Genes 11, 47-59.
    [Google Scholar]
  11. Di Serio, F., Darós, J. A., Ragozzino, A. & Flores, R. ( 1997; ). A 451-nucleotide circular RNA from cherry with hammerhead ribozymes in its strands of both polarities. Journal of Virology 71, 6603-6610.
    [Google Scholar]
  12. Domingo, E. & Holland, J. J. ( 1994; ). Mutation rates and rapid evolution of RNA viruses. In The Evolutionary Biology of Viruses, pp. 161-184. Edited by S. S. Morse. New York: Raven Press.
  13. Domingo, E., Martínez-Salas, E., Sobrino, F., de la Torre, J. C., Portela, A., Ortín, J., López-Galíndez, C., Pérez-Breña, P., Villanueva, N., Nájera, R., Vandepol, S., Steinhauer, D., Depolo, N. & Holland, J. J. ( 1985; ). The quasispecies (extremely heterogeneous) nature of viral RNA genome populations: biological relevance – a review. Gene 40, 1-8.
    [Google Scholar]
  14. Eigen, M. ( 1993; ). The origin of genetic information: virus as models. Gene 135, 37-47.[CrossRef]
    [Google Scholar]
  15. Elena, S. F., Dopazo, J., Flores, R., Diener, T. O. & Moya, A. ( 1991; ). Phylogeny of viroids, viroidlike satellite RNAs, and the viroidlike domain of hepatitis δ virus RNA. Proceedings of the National Academy of Sciences, USA 88, 5631-5634.[CrossRef]
    [Google Scholar]
  16. Flores, R., Hernández, C., Desvignes, J. C. & Llácer, G. ( 1990; ). Some properties of the viroid inducing peach latent mosaic disease. Research in Virology 141, 109-118.[CrossRef]
    [Google Scholar]
  17. Flores, R., Di Serio, F. & Hernández, C. ( 1997; ). Viroids: the non coding genomes. Seminars in Virology 8, 65-73.[CrossRef]
    [Google Scholar]
  18. Flores, R., Randles, J. W., Bar-Joseph, M. & Diener, T. O. ( 1998; ). A proposed scheme for viroid classification and nomenclature. Archives of Virology 143, 623-629.[CrossRef]
    [Google Scholar]
  19. Forster, A. C. & Symons, R. H. ( 1987; ). Self-cleavage of plus and minus RNAs of a virusoid and a structural model for the active sites. Cell 49, 211-220.[CrossRef]
    [Google Scholar]
  20. Góra, A., Candresse, T. & Zagórski, W. ( 1994; ). Analysis of the population structure of three phenotypically different PSTVd isolates. Archives of Virology 138, 223-245.
    [Google Scholar]
  21. 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.
    [Google Scholar]
  22. Hammond, R. W. & Owens, R. A. ( 1987; ). Mutational analysis of potato spindle tuber viroid reveals complex relationships between structure and infectivity. Proceedings of the National Academy of Sciences, USA 84, 3967-3971.[CrossRef]
    [Google Scholar]
  23. Harders, J., Lukacs, N., Robert-Nicoud, M., Jovin, J. M. & Riesner, D. ( 1989; ). Imaging of viroids in nuclei from tomato leaf tissue by in situ hybridization and confocal laser scanning microscopy. EMBO Journal 8, 3941-3949.
    [Google Scholar]
  24. Hernández, C. & Flores, R. ( 1992; ). Plus and minus RNAs of peach latent mosaic self-cleave in vitro via hammerhead structures. Proceedings of the National Academy of Sciences, USA 89, 3711-3715.[CrossRef]
    [Google Scholar]
  25. Hu, Y., Feldstein, P. A., Hammond, J., Hammond, R. W., Bottino, P. J. & Owens, R. A. ( 1997; ). Destabilization of potato spindle tuber viroid by mutations in the left terminal loop. Journal of General Virology 78, 1199-1206.
    [Google Scholar]
  26. Hutchins, C. J., Rathjen, P. D., Forster, A. C. & Symons, R. H. ( 1986; ). Self-cleavage of plus and minus RNA transcripts of avocado sunblotch viroid. Nucleic Acids Research 14, 3627-3640.[CrossRef]
    [Google Scholar]
  27. Jukes, T. H. & Cantor, C. R. ( 1969; ). Evolution of protein molecules. In Mammalian Protein Metabolism, pp. 21-132. Edited by H. N. Munro. New York: Academic Press.
  28. Keese, P. & Symons, R. H. ( 1985; ). Domains in viroids: evidence of intermolecular RNA rearrangements and their contribution to viroid evolution. Proceedings of the National Academy of Sciences, USA 82, 4582-4586.[CrossRef]
    [Google Scholar]
  29. Keese, P., Visvader, J. E. & Symons, R. H. ( 1988; ). Sequence variability in plant viroid RNAs. In RNA Genetics, vol. III, Variability of RNA Genomes, pp. 71-98. Edited by E. Domingo, J. J. Holland & P. Ahlquist. Boca Raton, FL: CRC.
  30. Kofalvi, S. A., Marcos, J. F., Cañizares, M. C., Pallás, V. & Candresse, T. ( 1997; ). Hop stunt viroid (HSVd) sequence variants from Prunus species: evidence for recombination between HSVd isolates. Journal of General Virology 78, 3177-3186.
    [Google Scholar]
  31. Koltunow, A. M. & Rezaian, M. A. ( 1988; ). Grapevine yellow speckle viroid: structural features of a new viroid group. Nucleic Acids Research 16, 849-864.[CrossRef]
    [Google Scholar]
  32. Kore, A. R., Vaish, N. K., Kutzke, U. & Eckstein, F. ( 1998; ). Sequence specificity of the hammerhead ribozyme revisited; the NHH rule. Nucleic Acids Research 26, 4116-4120.[CrossRef]
    [Google Scholar]
  33. Kurath, G. & Palukaitis, P. ( 1989; ). RNA sequence heterogeneity in natural populations of three satellite RNAs of cucumber mosaic virus. Virology 173, 231-240.[CrossRef]
    [Google Scholar]
  34. Lakshman, D. K. & Tavantzis, S. M. ( 1992; ). RNA progeny of an infectious two-base deletion cDNA mutant of potato spindle tuber viroid (PSTV) acquire two nucleotides in planta. Virology 187, 565-572.[CrossRef]
    [Google Scholar]
  35. Lakshman, D. K. & Tavantzis, S. M. ( 1993; ). Primary and secondary structure of a 360-nucleotide isolate of potato spindle tuber viroid. Archives of Virology 128, 319-331.[CrossRef]
    [Google Scholar]
  36. Lima, M. I., Fonseca, M. E. N., Flores, R. & Kitajima, E. W. ( 1994; ). Detection of avocado sunblotch viroid in chloroplasts of avocado leaves by in situ hybridization. Archives of Virology 138, 285-390.
    [Google Scholar]
  37. Loss, P., Schimtz, M., Steger, G. & Riesner, D. ( 1991; ). Formation of a thermodynamically metastable structure containing hairpin II is critical for infectivity of potato spindle tuber viroid RNA. EMBO Journal 10, 719-727.
    [Google Scholar]
  38. Miller, W. A., Hercus, T., Waterhouse, P. M. & Gerlach, W. L. ( 1991; ). A satellite RNA of barley yellow dwarf virus contains a novel hammerhead structure in the self-cleavage domain. Virology 183, 711-720.[CrossRef]
    [Google Scholar]
  39. Navarro, B. & Flores, R. ( 1997; ). Chrysanthemum chlorotic mottle viroid: unusual structural properties of a subgroup of self-cleaving viroids with hammerhead ribozymes. Proceedings of the National Academy of Sciences, USA 94, 11262-11267.[CrossRef]
    [Google Scholar]
  40. Nei, M. (1987). Molecular Evolutionary Genetics. New York: Columbia University Press.
  41. Owens, R. A., Thomsom, S. M. & Steger, G. ( 1991; ). Effects of random mutagenesis upon potato spindle tuber viroid replication and symptom expression. Virology 185, 18-31.[CrossRef]
    [Google Scholar]
  42. Pallás, V., García-Luque, I., Domingo, E. & Flores, R. ( 1988; ). Sequence variability in avocado sunblotch viroid (ASBV). Nucleic Acids Research 16, 9864.[CrossRef]
    [Google Scholar]
  43. Qu, F., Heinrich, C., Loss, P., Steger, G., Tien, P. & Riesner, D. ( 1993; ). Multiple pathways of reversion in viroid conservation of structural domains. EMBO Journal 12, 2129-2139.
    [Google Scholar]
  44. Rakowski, A. G. & Symons, R. H. ( 1989; ). Comparative sequence studies of variants of avocado sunblotch viroid. Virology 173, 352-356.[CrossRef]
    [Google Scholar]
  45. Rozas, J. & Rozas, R. ( 1995; ). DnaSP, DNA sequence polymorphism: an interactive program for estimating population genetic parameters from DNA sequence data. Computer Applications in the Biosciences 11, 621-625.
    [Google Scholar]
  46. Ruffner, D. E., Stormo, G. D. & Uhlenbeck, O. C. ( 1990; ). Sequence requirements of the hammerhead RNA self-cleavage reaction. Biochemistry 29, 10695-10702.[CrossRef]
    [Google Scholar]
  47. Saitou, N. & Nei, M. ( 1987; ). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406-425.
    [Google Scholar]
  48. Sanger, F., Nicklen, S. & Coulson, A. R. ( 1977; ). DNA sequencing with chain terminating inhibitors. Proceedings of the National Academy of Sciences, USA 74, 5463-5467.[CrossRef]
    [Google Scholar]
  49. Semancik, J. S. & Szychowski, J. A. ( 1994; ). Avocado sunblotch disease: a persistent viroid infection in which variants are associated with differential symptoms. Journal of General Virology 75, 1543-1549.[CrossRef]
    [Google Scholar]
  50. Sheldon, C. C. & Symons, R. H. ( 1989; ). Mutagenesis analysis of a self-cleaving RNA. Nucleic Acids Research 17, 5679-5685.[CrossRef]
    [Google Scholar]
  51. Sheldon, C. C. & Symons, R. H. ( 1993; ). Is hammerhead self-cleavage involved in the replication of a virusoid in vivo? Virology 194, 463-474.[CrossRef]
    [Google Scholar]
  52. Sudhir, K., Tamura, K. & Nei, M. (1993). MEGA: molecular evolutionary genetics analysis, version 1.01. The Pennsylvania State University, University Park, PA, USA.
  53. Symons, R. H. ( 1997; ). Plant pathogenic RNAs and RNA catalysis. Nucleic Acids Research 20, 2683-2689.
    [Google Scholar]
  54. Thomson, J. D., Higgins, D. G. & Gibson, T. J. ( 1994; ). CLUSTAL W. Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673-4680.[CrossRef]
    [Google Scholar]
  55. Visvader, J. E. & Symons, R. H. ( 1985; ). Eleven new sequence variants of citrus exocortis viroid and the correlation of sequence with the pathogenicity. Nucleic Acids Research 13, 2907-2920.[CrossRef]
    [Google Scholar]
  56. Wassenegger, M., Heimes, S. & Sänger, H. L. ( 1994; ). An infectious viroid RNA replicon evolved from an in vitro-generated non-infectious viroid deletion mutant via a complementary deletion in vivo. EMBO Journal 13, 6172-6177.
    [Google Scholar]
  57. Zuker, M. ( 1989; ). On finding all suboptimal foldings of an RNA molecule. Science 244, 48-52.[CrossRef]
    [Google Scholar]
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