Structural differences within the loop E motif imply alternative mechanisms of viroid processing

RNA

Volumn 13, Issue 6, 2007, Pages 824-834

  Owens, Robert A ^a   Baumstark, Tilman ^b  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b UNIVERSITY OF THE SCIENCES   (United States)

Author keywords

Citrus viroid III; Cleavage ligation; Loop E; RNA motifs; Viroid replication; Viroids

Indexed keywords

RNA;

ARTICLE; BASE PAIRING; CONTROLLED STUDY; GEL ELECTROPHORESIS; GENE REARRANGEMENT; GENETIC VARIABILITY; INVERTED REPEAT; NONHUMAN; PRIORITY JOURNAL; RNA PROCESSING; RNA STABILITY; RNA STRUCTURE; VIROID; VIRUS REPLICATION;

BASE SEQUENCE; CROSS-LINKING REAGENTS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PLANTS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, VIRAL; TEMPERATURE; ULTRAVIOLET RAYS; VIROIDS; VIRUS REPLICATION;

CITRUS VIROID III; POTATO SPINDLE TUBER VIROID; VIROIDS;

EID: 34249002274     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.452307     Document Type: Article

References (43)

1. Allison, L.A., Romaniuk, P.J., and Bakken, A.H. 1991. RNA-protein interactions of stored 5S RNA with TFIIIA and ribosomal protein L5 during Xenopus oogenesis. Dev. Biol. 144: 129-144.
2. Baumstark, T. and Ahlquist, P. 2001. The brome mosaic virus RNA3 intergenic replication enhancer folds to mimic a tRNA TψC-stem-loop and is modified in vivo. RNA 7: 1652-1670.
3. Baumstark, T. and Riesner, D. 1995. Only one of four possible secondary structures of the central conserved region of Potato spindle tuber viroid is a substrate for processing in a potato nuclear extract. Nucleic Acids Res. 2: 4246-4254.
4. Baumstark, T., Schröder, A.R.W., and Riesner, D. 1997. Viroid processing: switch from cleavage to ligation is driven by a change from a tetraloop to a loop E conformation. EMBO J. 16: 599-610.
5. Branch, A.D. and Robertson, H.D. 1984. A replication cycle for viroids and other small infectious RNAs. Science 223: 450-455.
6. Branch, A.D., Benenfeld, B.J., and Robertson, H.D. 1985. Ultraviolet light-induced cross-linking reveals a unique region of local tertiary structure in Potato spindle tuber viroid and HeLa 5S RNA. Proc. Natl. Acad. Sci. 82: 6590-6594.
7. Butcher, S.E. and Burke, J.M. 1994. A photo-cross-linkable tertiary structure motif found in functionally distinct RNA molecules is essential for catalytic function of the hairpin ribozyme. Biochemistry 33: 992-999.
8. Butcher, S.E., Allain, F.H.-T., and Feigon, J. 1999. Solution structure of the loop B domain from the hairpin ribozyme. Nat. Struct. Biol. 6: 212-216.
9. Correll, C.C., Freeborn, B., Moore, P.B., and Steitz, T.A. 1997. Metals, motif, and recognition in the crystal structure of a 5S rRNA domain. Cell 91: 705-712.
10. Côté, F., De la Peña, M., Flores, R., and Perreault, J.P. 2003. Ribozyme reactions of viroids. In Viroids (eds. A. Hadidi et al.), pp. 350-356. CSIRO Publishing, Collingwood, Australia.
11. Dallas, A. and Moore, P.B. 1997. The loop E-Loop D region of Escherichia coli 5S rRNA: The solution structure reveals an unusual loop that may be important for binding ribosomal proteins. Curr. Biol. 5: 1639-1653.
12. Ehresman, C., Baudin, F., Mougel, M., Romby, P., Ebel, J.-P., and Ehresman, B. 1987. Probing the structure of RNAs in solution. Nucleic Acids Res. 15: 9109-9128.
13. Endo, Y., Gluck, A., and Wool, I.G. 1993. Ribosomal RNA identity elements for recognition by ricin and by α-sarcin: Mutation in the putative CG pair that closes a GAGA tetraloop. Nucleic Acids Symp. Ser. 29: 165-166.
14. Flores, R., Hernández, C., Martinez de Alba, A.E., Daròs, J.-A., and DiSerio, F. 2005a. Viroids and viroid-host interactions. Annu. Rev. Phytopathol. 43: 4.1-4.23.
15. Flores, R., Randles, J.W., Owens, R.A., Bar-Joseph, M., and Diener, T.O. 2005b. Viroids. In Virus taxonomy - Eighth Report of the International Committee on Taxonomy of Viruses (eds. C.M. Fauquet et al.), pp. 1145-1159. Elsevier/Academic Press, San Diego, London.
16. Fox, G.E. and Woese, C.R. 1973. 5S rRNA secondary structure. Nature 256: 505-507.
17. Hampel, K.J. and Burke, J.M. 2001. A conformational change in the "loop E-like" motif of the hairpin ribozyme is coincidental with domain docking and is essential for catalysis. Biochemistry 40: 3723-3729.
18. Hecker, R., Wang, Z., Steger, G., and Riesner, D. 1986. Analysis of RNA structures by temperature-gradient gel electrophoresis: Viroid replication and processing. Gene 72: 59-74.
19. Hendrix, D.K., Brenner, S.E., and Holbrook, S.R. 2005. RNA structural motifs: Building blocks of a modular biomolecule. Q. Rev. Biophys. 38: 221-243.
20. Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K., and Pease, L.R. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 59-74.
21. Leontis, N.B. and Westhof, E. 1998a. The 5S rRNA loop E: Chemical probing and phylogenetic data versus crystal structure. RNA 4: 1134-1153.
22. Leontis, N.B. and Westhof, E. 1998b. A common motif organizes the structure of multi-helix loops in 16S and 23S ribosomal RNAs. J. Mol. Biol. 283: 571-583.
23. Leontis, N.B. and Westhof, E. 2003. Analysis of RNA motifs. Curr. Opin. Struct. Biol. 13: 300-308.
24. Leontis, N.B., Stombaugh, J., and Westhof, E. 2002. The non-Watson-Crick base pairs and their associated isostericity matrices. Nucleic Acids Res. 30: 3497-3531.
25. Mathews, D.H., Sabina, J., Zuker, M., and Turner, D.H. 1999. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol. 288: 911-940.
26. Moazed, D., Stern, S., and Noller, H.F. 1986. Rapid chemical probing of conformation in 16S ribosomal RNA and 30S ribosomal subunits using primer extension. J. Mol. Biol. 187: 399-416.
27. Owens, R.A., Steger, G., Hu, Y., Fels, A., Hammond, R.W., and Riesner, D. 1996. RNA structural features responsible for Potato spindle tuber viroid pathogenicity. Virology 222: 144-158.
28. Owens, R.A., Yang, G., Gundersen-Rindal, D., Hammond, R.W., Candresse, T., and Bar-Joseph, M. 2000. Both point mutation and RNA recombination contribute to the sequence diversity of Citrus viroid III. Virus Genes 20: 243-252.
29. Owens, R.A., Thompson, S.M., Sieburth, P.J., and Hilf, M.E. 2006. Mutational analysis of Citrus viroid III symptom expression. In Proceedings 16th Conference IOCV, 2004 (eds. M. Hilf et al.), pp. 280-290. IOCV, Riverside, CA.
30. Qi, Y. and Ding, B. 2002. Replication of Potato spindle tuber viroid in cultured cells of tobacco and Nicotiana benthamiana: The role of specific nucleotides in determining replication levels for host adaptation. Virology 302: 445-456.
31. Qi, Y. and 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.
32. Qi, Y., Pelissier, T., Itaya, A., Hunt, E., Wasseneger, M., and Ding, B. 2004. Direct role of a viroid RNA motif in mediating direction RNA trafficking across a specific cellular boundary. Plant Cell 16: 1741-1752.
33. Rakowski, A.G., Szychowski, J.A., Avena, Z.S., and Semancik, J.S. 1994. Nucleotide sequence and structural features of the group III citrus viroids. J. Gen. Virol. 75: 3581-3584.
34. Riesner, D., Steger, G., Zimmat, R., Owens, R.A., Wagenhöfer, M., Hillen, W., Vollbach, S., and Henco, K. 1989. Temperature-gradient gel electrophoresis of nucleic acids: Analysis of conformational transitions, sequence variations, and protein-nucleic acid interactions. Electrophoresis 10: 377-389.
35. Rupert, P.B. and Ferré-D'-Amaré, A.R. 2001. Crystal structure of a hairpin ribozyme-inhibitor complex with implications for catalysis. Nature 410: 780-786.
36. Sambrook, J. and Russell, D.W. 2001. Molecular cloning: A laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. Schrader, O., Baumstark, T., and Riesner, D. 2003. A mini-RNA containing the tetraloop, wobble-pair and loop E motifs of the central conserved region of Potato spindle tuber viroid is processed into a minicircle. Nucleic Acids Res. 31: 988-998.
38. Schuster, P. 2001. Evolution in silico and in vitro: The RNA model. Biol. Chem. 382: 1301-1314.
39. Steger, G., Tabler, M., Brüggemann, W., Colpan, M., Klotz, G., Sänger, H.L., and Riesner, D. 1986. Structure of viroid replicative intermediates: physico-chemical studies on SP6 transcripts of cloned oligomeric Potato spindle tuber viroid. Nucleic Acids Res. 14: 9613-9630.
40. Wang, Y., Zhong, X., Itaya, A., and Ding, B. 2007. Evidence for the in vivo existence of loop E motif of Potato spindle tube viroid. J. Virol. 81: 2074-2077.
41. Wassenegger, M., Spieker, R.L., Thalmeir, S., Riedel, L., and Sänger, H.L. 1996. A single nucleotide substitution converts Potato spindle tuber viroid (PSTVd) from a noninfectious to an infectious RNA for Nicotiana tabacum. Virology 226: 191-197.
42. Zhong, X., Leontis, N., Qian, S., Itaya, A., Qi, Y., Boris-Lawrie, K., and Ding, B. 2006. Tertiary structural and functional analyses of a viroid RNA motif by isostericity matrix and mutagenesis reveal its essential role in replication. J. Virol. 80: 8566-8581.
43. Zuker, M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31: 3406-3415.