1887

Abstract

Viroids are highly structured, single-stranded, non-protein-coding circular RNA pathogens that replicate, spread and elicit severe to mild disease symptoms in sensitive host species. The functions of viroids are thought to be due to a molecular element (or elements) embedded within the small RNA molecule that recruits the host factors responsible for transcription, RNA transportation and regulation of gene expression. Coleus blumei viroid 1 (CbVd-1) is distributed worldwide and is known for its characteristic property of having an extremely high frequency of seed transmission. During our analysis of CbVd-1 seed transmission, two variants, CbVd-1/25A and CbVd-1/25UU, were shown to have distinct seed-transmission frequencies: 30 and 0 %, respectively. Seven infectious dimeric forms of CbVd-1 cDNA clones were created based on the sequences of CbVd-1/25A,CbVd-1/25UU and an additional five variants with unique loop structures in other portion(s) of the molecule, and in vitro transcripts were inoculated into viroid-free coleus seedlings. All seven CbVd-1 variants showed infectivity. Nucleotide sequence analysis of the progeny revealed that four of the five additional mutants changed to either CbVd-1/25A or CbVd-1/25UU, while, CbVd-1/25A, CbVd-1/25UU and one of the five additional mutants (CbVd-1/I2) replicated stably. As expected, CbVd-1/25A and CbVd-1/I2 were transmitted through seeds, but CbVd-1/25UU was not. CbVd-1/25A and CbVd-1/I2 shared the same nucleotide at position 25 in loop five but are different from CbVd-1/25UU at that position. Therefore, nucleotide 25 in loop five was identified as a determinant for seed transmission of CbVd-1.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001013
2018-01-23
2019-10-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/99/3/393.html?itemId=/content/journal/jgv/10.1099/jgv.0.001013&mimeType=html&fmt=ahah

References

  1. Gabrial SA, Bozarth RF, Buck KW, Martelli GP, Milne RG et al. Family Partitiviridae. In van Regenmortel MHV. (editor) Virus Taxonomy. Classification and nomenclature of viruses Seventh Report San Diego, California: Academic Press; 2000
    [Google Scholar]
  2. Card SD, Pearson MN, Clover GRG. Plant pathogens transmitted by pollen. Australas Plant Pathol 2007; 36: 455– 461 [CrossRef]
    [Google Scholar]
  3. Hull R. Transmission 2: mechanical, seed, pollen and epidemiology. In Matthews’ Plant Virology The Netherlands: Elsevier Academic Press; 2004; pp. 533– 582
    [Google Scholar]
  4. Johansen E, Edwards MC, Hampton RO. Seed transmission of viruses: current perspectives. Annu Rev Phytopathol 1994; 32: 363– 386 [CrossRef]
    [Google Scholar]
  5. Mink GI. Pollen and seed-transmitted viruses and viroids. Annu Rev Phytopathol 1993; 31: 375– 402 [CrossRef] [PubMed]
    [Google Scholar]
  6. Tsuda S, Sano T. Threats to Japanese agriculture from newly emerged plant viruses and viroids. J Gen Pl Pathol 2014; 80: 2– 14 [CrossRef]
    [Google Scholar]
  7. Sastry KS. Seed-borne plant virus diseases India: Springer; 2013; [Crossref]
    [Google Scholar]
  8. Mandahar CL. Virus transmission through seed and pollen. In Maramorosch K, Harris KF. (editors) Plant Diseases and Vectors. Ecology and Epidemiology New York: Academic Press; 1981; pp. 241– 292
    [Google Scholar]
  9. Doolittle SP, Gilbert WW. Seed transmission of cucurbit mosaic by the wild cucumber. Phytopathology 1919; 9: 326– 327
    [Google Scholar]
  10. Reddick D, Stewart VB. Transmission of the virus of bean mosaic in seed and observations on thermal death point of seed and virus. Phytopathology 1919; 9: 445– 450
    [Google Scholar]
  11. Hanada K, Harrison BD. Effects of virus genotype and temperature on seed transmission of nepoviruses. Ann Appl Biol 1977; 85: 79– 92 [CrossRef]
    [Google Scholar]
  12. Diener TO. Viroids and Viroid Diseases New York, USA: John Wily and Sons; 1979
    [Google Scholar]
  13. Wallace JM, Drake RJ. A high rate of seed transmission of avocado sun-blotch virus from symptomless trees and the origin of such trees. Phytopathology 1962; 52: 237– 241
    [Google Scholar]
  14. Chung BN, Pak HS. Seed transmission of Chrysanthemum stunt viroid in Chrysanthemum. Plant Pathol J 2008; 24: 31– 35 [CrossRef]
    [Google Scholar]
  15. Antignus Y, Lachman O, Pearlsman M. Spread of Tomato apical stunt viroid (TASVd) in greenhouse tomato crops is associated with seed transmission and bumble bee activity. Plant Disease 2007; 91: 47– 50 [CrossRef]
    [Google Scholar]
  16. Singh RP, Boucher A, Wang RG. Detection, distribution and long-term persistence of potato spindle tuber viroid in true potato seed from heilongjiang, China. Am Potato J 1991; 68: 65– 74 [CrossRef]
    [Google Scholar]
  17. Singh RP. Detection of potato spindle tuber viroid in the pollen and various parts of potato plant pollinated with viroid-infected pollen. Plant Disease 1992; 76: 951– 953 [CrossRef]
    [Google Scholar]
  18. Matsushita Y, Usugi T, Tsuda S. Distribution of tomato chlorotic dwarf viroid in floral organs of tomato. Eur J Plant Pathol 2011; 130: 441– 447 [CrossRef]
    [Google Scholar]
  19. Fonseca MEN, Boiteux LS, Singh RP, Kitajima EW. A small viroid in Coleus species from Brazil. Fitopatologia Brasileira 1989; 14: 94– 96
    [Google Scholar]
  20. Chung B-N, Choi G-S. Incidence of Coleus blumei viroid 1 in seeds of commercial coleus in Korea. Plant Pathol J 2008; 24: 305– 308 [CrossRef]
    [Google Scholar]
  21. Ishiguro A, Sano T, Harada Y. Nucleotide sequence and host range of coleus viroid isolated from coleus (Coleus blumei Benth.) in Japan. Ann Phytopathol Soc Jpn 1996; 62: 84– 86 [CrossRef]
    [Google Scholar]
  22. Jiang D, Wu Z, Xie L, Sano T, Li S. Sap-direct RT-PCR for the rapid detection of coleus blumei viroids of the genus Coleviroid from natural host plants. J Virol Methods 2011; 174: 123– 127 [CrossRef] [PubMed]
    [Google Scholar]
  23. Sf L, Su Q, Guo R, Tsuji M, Sano T. First report of Coleus blumei viroid from coleus in China. Plant Pathol 2006; 55: 565
    [Google Scholar]
  24. Singh RP. High incidence of transmission and occurrence of a viroid in commercial seeds of Coleus in Canada. Plant Disease 1991; 75: 184– 187 [CrossRef]
    [Google Scholar]
  25. Spieker RL, Haas B, Charng YC, Freimüller K, Sänger HL. Primary and secondary structure of a new viroid 'species' (CbVd 1) present in the Coleus blumei cultivar 'Bienvenue'. Nucleic Acids Res 1990; 18: 3998 [CrossRef] [PubMed]
    [Google Scholar]
  26. Jiang D, Gao R, Qin L, Wu Z, Xie L et al. Infectious cDNA clones of four viroids in Coleus blumei and molecular characterization of their progeny. Virus Res 2014; 180: 97– 101 [CrossRef] [PubMed]
    [Google Scholar]
  27. Zhong X, Archual AJ, Amin AA, Ding B. A genomic map of viroid RNA motifs critical for replication and systemic trafficking. Plant Cell 2008; 20: 35– 47 [CrossRef] [PubMed]
    [Google Scholar]
  28. Gago S, Elena SF, Flores R, Sanjuán R. Extremely high mutation rate of a hammerhead viroid. Science 2009; 323: 1308 [CrossRef] [PubMed]
    [Google Scholar]
  29. Qi Y, Ding B. Inhibition of cell growth and shoot development by a specific nucleotide sequence in a noncoding viroid RNA. Plant Cell 2003; 15: 1360– 1374 [CrossRef] [PubMed]
    [Google Scholar]
  30. Wassenegger M, Spieker RL, Thalmeir S, Gast FU, Riedel L et al. A single nucleotide substitution converts potato spindle tuber viroid (PSTVd) from a noninfectious to an infectious RNA for Nicotiana tabacum. Virology 1996; 226: 191– 197 [CrossRef] [PubMed]
    [Google Scholar]
  31. Ding B. The biology of viroid-host interactions. Annu Rev Phytopathol 2009; 47: 105– 131 [CrossRef] [PubMed]
    [Google Scholar]
  32. Ding B, Itaya A. Control of directional macromolecular trafficking across specific cellular boundaries: a key to integrative plant biology. J Integr Plant Biol 2007; 49: 1227– 1234 [CrossRef]
    [Google Scholar]
  33. Ding B, Kwon MO, Hammond R, Owens R. Cell-to-cell movement of potato spindle tuber viroid. Plant J 1997; 12: 931– 936 [CrossRef] [PubMed]
    [Google Scholar]
  34. Ding B, Itaya A, Zhong X. Viroid trafficking: a small RNA makes a big move. Curr Opin Plant Biol 2005; 8: 606– 612 [CrossRef] [PubMed]
    [Google Scholar]
  35. Qi Y, Pélissier T, Itaya A, Hunt E, Wassenegger M et al. Direct role of a viroid RNA motif in mediating directional RNA trafficking across a specific cellular boundary. Plant Cell 2004; 16: 1741– 1752 [CrossRef] [PubMed]
    [Google Scholar]
  36. Zhong X, Tao X, Stombaugh J, Leontis N, Ding B. Tertiary structure and function of an RNA motif required for plant vascular entry to initiate systemic trafficking. Embo J 2007; 26: 3836– 3846 [CrossRef] [PubMed]
    [Google Scholar]
  37. Carroll TW. Inheritance of resistance to seed transmission of barley stripe mosaic virus in barley. Phytopathology 1979; 69: 431– 433 [CrossRef]
    [Google Scholar]
  38. Carroll TW. Seedborne viruses. Virus-host interactions. In Mararnorosch K, Harris KF. (editors) Plant Diseases and Vectors. Ecology and Epidemiology New York: Academic Press; 1981; pp. 293– 317
    [Google Scholar]
  39. Wang D, Woods RD, Cockbain AJ, Maule AJ, Biddle AJ. The susceptibility of pea cultivars to pea seed-borne mosaic virus infection and virus seed transmission in the UK. Plant Pathol 1993; 42: 42– 47 [CrossRef]
    [Google Scholar]
  40. Wang D, Maule AJ. A model for seed transmission of a plant virus: genetic and structural analyses of pea embryo invasion by pea seed-borne mosaic virus. Plant Cell 1994; 6: 777– 787 [CrossRef] [PubMed]
    [Google Scholar]
  41. Edwards MC. Mapping of the seed transmission determinants of barley stripe mosaic virus, MPMI. 1995;8 906– 915
  42. Johansen IE, Dougherty WG, Keller KE, Wang D, Hampton RO. Multiple viral determinants affect seed transmission of pea seedborne mosaic virus in Pisum sativum. J Gen Virol 1996; 77: 3149– 3154 [CrossRef] [PubMed]
    [Google Scholar]
  43. Wang D, MacFarlane SA, Maule AJ. Viral determinants of pea early browning virus seed transmission in pea. Virology 1997; 234: 112– 117 [CrossRef] [PubMed]
    [Google Scholar]
  44. Martín-Hernández AM, Baulcombe DC. Tobacco rattle virus 16-kilodalton protein encodes a suppressor of RNA silencing that allows transient viral entry in encodes a suppressor of RNA silencing that allows transient viral entry in meristems. J Virol 2008; 82: 4064– 4071 [Crossref]
    [Google Scholar]
  45. Adkar-Purushothama CR, Zhang Z, Li S, Sano T. Analysis and application of viroid-specific small RNAs generated by viroid-inducing RNA silencing. Methods Mol Biol 2015; 1236: 135– 170 [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001013
Loading
/content/journal/jgv/10.1099/jgv.0.001013
Loading

Data & Media loading...

Most Cited This Month

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