1887

Journal of General Virology

Volume 94, Issue 3

The genetic diversity of populations is mainly dependent on the infected host species Free

Abstract

As with viruses, viroids infect their hosts as polymorphic populations of variants. Identifying possible sources of genetic variability is significant in the case of the species (CDVd) which has been proposed as a dwarfing agent for high-density citrus plantings. Here, a natural CDVd isolate (CMC) was used as an inoculum source for long-term (25 years) and short-term (1 year) bioassays in different citrus host species. Characterization of progenies indicated that the genetic stability of CDVd populations was high in certain hosts (trifoliate orange, Troyer citrange, Etrog citron, Navelina sweet orange), which preserve viroid populations similar to the original CMC isolate even after 25 years. By contrast, CDVd variant populations in Interdonato lemon and Volkamer lemon were completely different to those in the inoculated sources, highlighting how influential the host is on the genetic variability of CDVd populations. Implications for risk assessment of CDVd as a dwarfing agent are discussed.

  • Received:
  • Accepted:
  • Published Online:
© 2013 SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.048025-0
2013-03-01
2020-01-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/3/687.html?itemId=/content/journal/jgv/10.1099/vir.0.048025-0&mimeType=html&fmt=ahah

References

  1. Albanese G. , La Rosa R. , Tessitori M. , Fuggetta E. , Catara A. . ( 1996; ). Long-term effect of CVd-III of plants on citrange, trifoliate and sour orange. . In Proc Conf Int Org Citrus Virol 13th IOCV, pp. 367––369. Edited by da Graça J. V. , Moreno P. , Yokomi R. K. . Riverside, CA:: IOCV;.
     [Google Scholar]
  2. Altschul S. F. , Gish W. , Miller W. , Myers E. W. , Lipman D. J. . ( 1990; ). Basic local alignment search tool. . J Mol Biol 215:, 403––410.[PubMed] [CrossRef]
    [Google Scholar]
  3. Amari K. , Gomez G. , Myrta A. , Di Terlizzi B. , Pallás V. . ( 2001; ). The molecular characterization of 16 new sequence variants of Hop stunt viroid reveals the existence of invariable regions and a conserved hammerhead-like structure on the viroid molecule. . J Gen Virol 82:, 953––962.[PubMed]
    [Google Scholar]
  4. Bernad L. , Duran-Vila N. , Elena S. F. . ( 2009; ). Effect of citrus hosts on the generation, maintenance and evolutionary fate of genetic variability of citrus exocortis viroid. . J Gen Virol 90:, 2040––2049. [CrossRef] [PubMed]
    [Google Scholar]
  5. Broadbent P. , Nicholl P. , Freeman B. . ( 1988; ). Effect of graft-transmissible dwarfing agents on lemons. . In Proc Conf Int Org Citrus Virol 10th IOCV, pp. 211––218. Edited by Timmer L. W. , Garnsey S. M. , Navarro L. . Riverside, CA:: IOCV;.
     [Google Scholar]
  6. Codoñer F. M. , Darós J. A. , Solé R. V. , Elena S. F. . ( 2006; ). The fittest versus the flattest: experimental confirmation of the quasispecies effect with subviral pathogens. . PLoS Pathog 2:, e136. [CrossRef] [PubMed]
    [Google Scholar]
  7. Ding B. . ( 2009; ). The biology of viroid–host interactions. . Annu Rev Phytopathol 47:, 105––131. [CrossRef] [PubMed]
    [Google Scholar]
  8. Domingo E. , Sabo D. , Taniguchi T. , Weissmann C. . ( 1978; ). Nucleotide sequence heterogeneity of an RNA phage population. . Cell 13:, 735––744. [CrossRef] [PubMed]
    [Google Scholar]
  9. Duran-Vila N. , Semancik J. S. . ( 2003; ). Citrus viroid. . In Viroids, pp. 178––194. Edited by Hadidi A. , Flores R. , Randles J. W. , Semancik J. S. . . Collingwood, Australia:: CSIRO Publishing;.
     [Google Scholar]
  10. Eigen M. . ( 1993; ). Viral quasispecies. . Sci Am 269:, 42––49. [CrossRef] [PubMed]
    [Google Scholar]
  11. Flores R. , Llàcer G. . ( 1988; ). Isolation of a viroid-like RNA associated with peach latent mosaic disease. . Acta Hort. 235:, 325––332.
     [Google Scholar]
  12. Flores R. , Hernández C. , Martínez de Alba A. E. , Daròs J. A. , Di Serio F. . ( 2005; ). Viroids and viroid–host interactions. . Annu Rev Phytopathol 43:, 117––139. [CrossRef] [PubMed]
    [Google Scholar]
  13. Flores R. , Di Serio F. , Navarro B. , Duran-Vila N. , Owens R. A. . ( 2011; ). Viroids and viroid diseases of plants. . In Studies in Viral Ecology, Microbial and Botanical Host Systems, vol. 1, pp. 311––346. Edited by Hurst. C. J. . Chichester:: John Wiley & Sons;. [CrossRef]
    [Google Scholar]
  14. Flores R. , Serra P. , Minoia S. , Di Serio F. , Navarro B. . ( 2012; ). Viroids: from genotype to phenotype just relying on RNA sequence and structural motifs. . Front Microbiol 3:, 217.[PubMed]
    [Google Scholar]
  15. Gago S. , Elena S. F. , Flores R. , Sanjuán R. . ( 2009; ). Extremely high mutation rate of a hammerhead viroid. . Science 323:, 1308. [CrossRef] [PubMed]
    [Google Scholar]
  16. Gandía M. , Bernad L. , Rubio L. , Duran-Vila N. . ( 2007; ). Host effect on the molecular and biological properties of a Citrus exocortis viroid isolate from Vicia faba . . Phytopathology 97:, 1004––1010. [CrossRef] [PubMed]
    [Google Scholar]
  17. Góra A. , Candresse T. , Zagórski W. . ( 1994; ). Analysis of the population structure of three phenotypically different PSTVd isolates. . Arch Virol 138:, 233––245. [CrossRef] [PubMed]
    [Google Scholar]
  18. Góra-Sochaka 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]
  19. Hadidi A. , Flores R. , Randles J. W. , Semancik J. S. . ( 2003; ). Viroids. Collingwood, Australia:: CSIRO Publishing;.
     [Google Scholar]
  20. Hajeri S. , Ramadugu C. , Manjunath K. , Ng J. , Lee R. , Vidalakis G. . ( 2011; ). In vivo generated Citrus exocortis viroid progeny variants display a range of phenotypes with altered levels of replication, systemic accumulation and pathogenicity. . Virology 417:, 400––409. [CrossRef] [PubMed]
    [Google Scholar]
  21. Hardy S. , Sanderson G. , Barkley P. , Donovan N. . ( 2004; ). Dwarfing Citrus Trees Using Viroids. Agnote DPI-480. Edited by Smith W. E. . . New South Wales, Australia:: NWS Agriculture;.
     [Google Scholar]
  22. Hutton R. J. , Broadbent P. , Bevington K. B. . ( 2000; ). Viroid dwarfing for high density citrus plantings. . Horticult Rev 24:, 277––317.
    [Google Scholar]
  23. Ito T. , Ieki H. , Ozaki K. , Iwanami T. , Nakahara K. , Hataya T. , Ito T. , Isaka M. , Kano T. . ( 2002; ). Multiple citrus viroids in citrus from Japan and their ability to produce exocortis-like symptoms in citron. . Phytopathology 92:, 542––547. [CrossRef] [PubMed]
    [Google Scholar]
  24. Keese P. , Symons R. H. . ( 1985; ). Domains in viroids: evidence of intermolecular RNA rearrangements and their contribution to viroid evolution. . Proc Natl Acad Sci U S A 82:, 4582––4586. [CrossRef] [PubMed]
    [Google Scholar]
  25. 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. . J Gen Virol 78:, 3177––3186.[PubMed]
    [Google Scholar]
  26. Matoušek J. , Patzak J. , Orctová L. , Schubert J. , Vrba L. , Steger G. , Riesner D. . ( 2001; ). The variability of hop latent viroid as induced upon heat treatment. . Virology 287:, 349––358. [CrossRef] [PubMed]
    [Google Scholar]
  27. Murcia N. , Bernad L. , Serra P. , Bani Hashemian S. M. , Duran-Vila N. . ( 2009; ). Molecular and biological characterization of natural variants of Citrus dwarfing viroid . . Arch Virol 154:, 1329––1334. [CrossRef] [PubMed]
    [Google Scholar]
  28. Owens R. A. , Steger G. , Hu Y. , Fels A. , Hammond R. W. , Riesner D. . ( 1996; ). RNA structural features responsible for potato spindle tuber viroid pathogenicity. . Virology 222:, 144––158. [CrossRef] [PubMed]
    [Google Scholar]
  29. Owens R. A. , Thompson S. M. , Feldstein P. A. , Garnsey S. M. . ( 1999; ). Effects of natural sequence variation on symptom induction by citrus viroid III. . Ann Appl Biol 134:, 73––80. [CrossRef]
    [Google Scholar]
  30. Owens R. A. , Yang G. , Gundersen-Rindal D. , Hammond R. W. , 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––252. [CrossRef] [PubMed]
    [Google Scholar]
  31. Owens R. A. , Flores R. , Di Serio F. , Li S.-F. , Pallás V. , Randles J. W. , Sano T. , Vidalakis G. . ( 2012; ). Viroids. . In Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses, pp. 1221––1234. Edited by King A. M. Q. , Adams M. J. , Carstens E. B. , Lefkowitz E. J. . . London, UK:: Elsevier Academic Press;.
     [Google Scholar]
  32. Qi Y. , Ding B. . ( 2003; ). Inhibition of cell growth and shoot development by a specific nucleotide sequence in a noncoding viroid RNA. . Plant Cell 15:, 1360––1374. [CrossRef] [PubMed]
    [Google Scholar]
  33. Rakowski A. G. , Szychowski J. A. , Avena Z. S. , Semancik J. S. . ( 1994; ). Nucleotide sequence and structural features of the group III citrus viroids. . J Gen Virol 75:, 3581––3584. [CrossRef] [PubMed]
    [Google Scholar]
  34. Rivera-Bustamante R. F. , Gin R. , Semancik J. S. . ( 1986; ). Enhanced resolution of circular and linear molecular forms of viroid and viroid-like RNA by electrophoresis in a discontinuous-pH system. . Anal Biochem 156:, 91––95. [CrossRef] [PubMed]
    [Google Scholar]
  35. Rizza, S., , Nobile, G., , Tessitori, M., , Albanese, G., , La Rosa, R. , Catara, A. . ( 2010; ). Management of a high-density clementine orchard inoculated with pathogenic and non-pathogenic viroids. . In Proc Conf Int Org Citrus Virol 17th IOCV, pp. 218––220. Edited by Hilf M. E. , Timmer L. W. , Milne R. G. , da Graça J. V. . Riverside, CA:: IOCV;.
     [Google Scholar]
  36. Sano T. , Candresse T. , Hammond R. W. , Diener T. O. , Owens R. A. . ( 1992; ). Identification of multiple structural domains regulating viroid pathogenicity. . Proc Natl Acad Sci U S A 89:, 10104––10108. [CrossRef] [PubMed]
    [Google Scholar]
  37. Schneider T. D. , Stephens R. M. . ( 1990; ). Sequence logos: a new way to display consensus sequences. . Nucleic Acids Res 18:, 6097––6100. [CrossRef] [PubMed]
    [Google Scholar]
  38. Schnölzer M. , Haas B. , Raam K. , Hofmann H. , Sänger H. L. . ( 1985; ). Correlation between structure and pathogenicity of potato spindle tuber viroid (PSTV). . EMBO J 4:, 2181––2190.[PubMed]
    [Google Scholar]
  39. Semancik J. S. . ( 2003; ). Consideration for the introduction of viroids for economic advantage. . In Viroid, pp. 357––362. Edited by Hadidi A. , Flores R. , Randles J. W. , Semancik. J. S. . Collingwood, AUS:: CSIRO Publishing;.
     [Google Scholar]
  40. Semancik J. S. , Szychowski J. A. , Rakowski A. G. , Symons R. H. . ( 1993; ). Isolates of citrus exocortis viroid recovered by host and tissue selection. . J Gen Virol 74:, 2427––2436. [CrossRef] [PubMed]
    [Google Scholar]
  41. Semancik J. S. , Rakowski A. G. , Bash J. A. , Gumpf D. J. . ( 1997; ). Application of selected viroids for dwarfing and enhancement of production of Valencia orange. . J Hortic Sci & Biotechnol 72:, 563––570.
     [Google Scholar]
  42. Serra P. , Gago S. , Duran-Vila N. . ( 2008; ). A single nucleotide change in Hop stunt viroid modulates citrus cachexia symptoms. . Virus Res 138:, 130––134. [CrossRef] [PubMed]
    [Google Scholar]
  43. Sneath P. H. A. , Sokal R. R. . ( 1973; ). Numerical Taxonomy. The Principles and Practice of Numerical Classification. San Francisco, CA:: W.H. Freeman and Company;.
     [Google Scholar]
  44. Szychowski J. A. , Vidalakis G. , Semancik J. S. . ( 2005; ). Host-directed processing of Citrus exocortis viroid . . J Gen Virol 86:, 473––477. [CrossRef] [PubMed]
    [Google Scholar]
  45. Tamura K. , Peterson D. , Peterson N. , Stecher G. , Nei M. , Kumar S. . ( 2011; ). mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. . Mol Biol Evol 28:, 2731––2739. [CrossRef] [PubMed]
    [Google Scholar]
  46. Tessitori M. , La Rosa R. , Di Serio F. , Albanese G. , Catara A. . ( 2002; ). Molecular characterization of a Citrus viroid III (CVd-III) associated with citrus dwarfing in Italy. . In Proc Conf Int Org Citrus Virol 15th IOCV, pp. 387––389. Edited by Duran-Vila, N. , Milne R. G. , da Graça J. V. . Riverside, CA:: IOCV;.
     [Google Scholar]
  47. Tessitori M. , Maria G. , Capasso C. , Catara G. , Rizza S. , De Luca V. , Catara A. , Capasso A. , Carginale V. . ( 2007; ). Differential display analysis of gene expression in Etrog citron leaves infected by Citrus viroid III . . Biochim Biophys Acta 1769:, 228––235. [CrossRef] [PubMed]
    [Google Scholar]
  48. Tsagris E. M. , Martínez de Alba A. E. , Gozmanova M. , Kalantidis K. . ( 2008; ). Viroids. . Cell Microbiol 10:, 2168––2179. [CrossRef] [PubMed]
    [Google Scholar]
  49. Vernière C. , Perrier X. , Dubois C. , Dubois A. , Botella L. , Chabrier C. , Bové J. M. , Duran-Vila N. . ( 2004; ). Citrus viroids: symptom expression and effect vegetative growth and yield on clementine trees grafted on trifoliate orange. . Plant Dis 88:, 1189––1197. [CrossRef]
    [Google Scholar]
  50. Vidalakis G. , Pagliaccia D. , Bash J. A. , Afunian M. , Semancik J. S. . ( 2011; ). Citrus dwarfing viroid: effects on tree size and scion performance specific to Poncirus trifoliata rootstock for high-density planting. . Ann Appl Biol 158:, 204––217. [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.048025-0
Loading
The genetic diversity of Citrus dwarfing viroid populations is mainly dependent on the infected host species
J. Gen. Virol. 94, 687 (2013); https://doi.org/10.1099/vir.0.048025-0
/content/journal/jgv/10.1099/vir.0.048025-0
/content/journal/jgv/10.1099/vir.0.048025-0
Loading

Data & Media loading...

Supplements

Supplementary Material 

PDF

Most cited articles

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error