The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Functional Implication of the tRNA Genes Encoded in the Chlorella Virus PBCV-l Genome

  • Published : 2005.12.01
Download PDF
⟨ Previous Next ⟩

Abstract

The prototype Chlorella virus PBCV-l encodes 11 tRNA genes and over 350 protein-encoding genes in its 330 kbp genome. Initial attempts to overexpress the recombinant A189/192R protein, a putative virus attachment protein, in E. coli strain BL21(DE3) SI were unsuccessful, and multiple protein bands were detected on Western blots. However, the full-length A189/192R recombinant protein or fragments derived from it were detected when they were expressed in E. coli BL21 CodonPlus (DE3) RIL, which contains extra tRNAs. Codon usage analysis of the a189/192r gene showed highly biased usage of the AGA and AVA codons compared to genes encoded by E. coli and Chlorella. In addition, there were biases of XXA/U($56\%$) and XXG/ C($44\%$) in the codons recognized by the viral tRNAs, which correspond to the codon usage bias in the PBCV-1 genome of XXA/U ($63\%$) over those ending in XXC/G ($37\%$). Analysis of the codon usage in the major capsid protein and DNA polymerase showed preferential usage of codons that can be recognized by the viral tRNAs. The Asn (AAC) and Lys (AAG) codons whose corresponding tRNA genes are duplicated in the tRNA gene cluster were the most abundant (i.e., preferred) codons in these two proteins. The tRNA genes encoded in the PBCV-l genome seem to play a very important role during the synthesis of viral proteins through supplementing the tRNAs that are frequently used in viral proteins, but are rare in the host cells. In addition, these tRNAs would help the virus to adapt to a wide range of hosts by providing tRNAs that are rare in the host cells.

Keywords

References

  1. Amberg, S. M. and Meints, R. H. 1991. Nucleotide sequence of the genes for ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit and ribosomal protein S14 from a Chlorella-like green alga. J. Phycol. 27:753-758 https://doi.org/10.1111/j.0022-3646.1991.00753.x
  2. Bowden, R. J., Simas, J. P., Davis, A. J. and Efstathiou, S. 1997. Murine gammaherpesvirus 68 encodes tRNA-like sequences which are expressed during latency. J. Gen. Virol. 78:1675-1687 https://doi.org/10.1099/0022-1317-78-7-1675
  3. Carstens, C.-P., Bonnardel, J., Allen, R. and Anna Waesche, A. 2002. BL21-CodonPlus cells correct expression problems caused by codon bias. Strategies 14:50-51
  4. Chen, G. T. and Inouye, M. 1994. Role of the AGA/AGG codons, the rarest codons in global gene expression in Escherichia coli. Genes Dev. 8:2641-52 https://doi.org/10.1101/gad.8.21.2641
  5. Cowe, E. and Sharp, P. M. 1991. Molecular evolution of bacteriophages: discrete patterns of codon usage in T4 genes are related to the time of gene expression. J. Mol. Evol. 33:13-22 https://doi.org/10.1007/BF02100191
  6. Calendar, R. 1988. The bacteriophages. In: The Viruses, ed. by H. Fraenkel-Conrat and R. R. Wagner, Plenum Press, New York. 56pp
  7. Cho, H. H., Park, H. H., Kim, J. O. and Choi, T. J. 2002. Isolation and characterization of chlorella viruses from freshwater sources in Korea. Mol. Cells. 14:168-176
  8. Deana, A., Ehrlich, R. and Reiss, C. 1998. Silent mutations in the Escherichia coli ompA leader peptide region strongly affect transcription and translation in vivo. Nucl. Acids Res. 26:4778-82 https://doi.org/10.1093/nar/26.20.4778
  9. Desai, S. M., Vaughan, J. and Weiss, S. B. 1986. Identification and location of nine T5 bacteriophage tRNA genes by DNA sequence analysis. Nucl. Acids Res. 14:4197-4205 https://doi.org/10.1093/nar/14.10.4197
  10. Ford, M. E., Sarkis, G. J., Belanger, A. E., Hendrix, R. W. and Hatfull, G. F. 1998. Genome structure of mycobacteriophage D29: implication for phage evolution. J. Mol. Biol. 279:143-164 https://doi.org/10.1006/jmbi.1997.1610
  11. Fraser, C. M., Gocayne, J. D., White, O., Adams, M. D., Clayton, R. A., Fleischmann, R. D., Bult, C. J., Kerlavage, A. R., Sutton, G., Kelly, J. M., Fritchman, J. L., Weidman, J. F., Small, K. V., Sandusky, M., Fuhrmann, J., Nguyen, D., Utterback, J. F., Saudek, D. M., Phillips, C. A., Merrick, J. M., Tomb, J. F., Dougherty, B. A., Bott, K. F., Bu, P. C., Lucier, T. S., Peterson, S. N., Smith, H. O., Hutchison, C. A., III. and Venter, J. C. 1995. The minimal gene complement of Mycoplasma genitalium. Science 270:397-403 https://doi.org/10.1126/science.270.5235.397
  12. Hershko, A and Ciechanover, A. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425-479 https://doi.org/10.1146/annurev.biochem.67.1.425
  13. Hushpulian, D. M., Savitski, P. A., Rojkova, A. M., Chubar, T. A., Fechina, V. A., Sakharov, I. Y., Lagrimini, L. M., Tishkov, V. I. and Gazaryan, I. G. 2003. Expression and refolding of tobacco anionic peroxidase from E. coli inclusion bodies. Biochemistry(Mosc) 68:1189-1194 https://doi.org/10.1023/B:BIRY.0000009132.45842.93
  14. Goldberg, A. L. 1992. The mechanism and functions of ATP-dependent proteases in bacterial and animal cells. Eur. J. Biochem. 203:9-23 https://doi.org/10.1111/j.1432-1033.1992.tb19822.x
  15. Graves, M. V., Burbank, D. E., Roth, R., Heuser, J., DeAngelis, P. L. and Van Etten, J. L. 1999. Hyaluronan synthesis in virus PBCV-1 infected chlorella-like green algea. Virology 257:15-23 https://doi.org/10.1006/viro.1999.9628
  16. Jiang, X., Nakano, H., Kigawa, T., Yabuki, T., Yokoyama, S., Clark, D. S. and Yamane, T. 2001. Dosage effect of minor arginyl- and isoleucyl-tRNAs on protein synthesis in an Escherichia coli in vitro coupled transcription / translation system. J. Biosci. Bioeng. 91:53-57 https://doi.org/10.1263/jbb.91.53
  17. Kanjo, N. and Inokushi, H. 1999. Genes for tRNA-Arg located in the upstream region of the Shiga toxin II operon in enteromorrhagic Escherichia coli O157:H7. DNA Res. 6:71-73 https://doi.org/10.1093/dnares/6.1.71
  18. Kleber-Janke, T. and Becker, W. M. 2000. Use of modified BL21(DE3) Escherichia coli cells for high-level expression of recombinant peanut allergens affected by poor codon usage. Prot. Exp. Purification 19:419-424 https://doi.org/10.1006/prep.2000.1265
  19. Kumar, S., Birah, A., Chaudhary, B., Burma, P. K., Gupta, G. P. and Pental, D. 2005. Plant codon optimized cry genes of Bacillus thuringiensis can be expressed as soluble proteins in Escherichia coli BL21 Codon Plus strain as NusA-Cry protein fusions. J. Invertebr. Pathol. 88:83-86 https://doi.org/10.1016/j.jip.2004.09.002
  20. Kunisawa, T. 2000. Functional role of mycobacteriophage transfer RNAs. J. Theor. Biol. 205:167-170 https://doi.org/10.1006/jtbi.2000.2057
  21. Kunisawa, T. 2002. Functional role of bacteriophage transfer RNAs: codon usage analysis of genomic sequences stored in the GENBANK/EMBL/DDBJ tadabases. Data Science J. 1:216-228 https://doi.org/10.2481/dsj.1.216
  22. Kutish, G., Li, Y., Lu, Z., Furuta, M., Rock, D. L. and Van Etten, J. L. 1996. Analysis of 76kb of the Chlorella virus PBCV-1 330kb genome: Map position 182 to 258. Virology 223:303-317 https://doi.org/10.1006/viro.1996.0482
  23. Lavrukhin, O. V., Fortune, F. M., Wood, T. G., Burbank, D. E., Van Etten, J. L., Osheroff, N. and Lloyd, R. S. 2000. Topoisomerase II from chlorella virus PBCV-1. Characterization of the smallest known type II topoisomerase. J. Biol. Chem. 275:6915-6921 https://doi.org/10.1074/jbc.275.10.6915
  24. Li, Y., Lu, Z., Burbank, D. E., Kutish, G. F. and Van Etten, J. L. 1995. Analysis of 43kb of the Chlorella virus PBCV-1 330kb genome: Map position 45 to 88. Virology 212:134-150 https://doi.org/10.1006/viro.1995.1462
  25. Li, Y., Lu, Z., Sun, L., Ropp, S., Kutish, G. F., Rock, D. L. and Van Etten, J. L. 1997. Analysis of 74 kb of DNA located at the right end of the 330-kb Chlorella virus PBCV-1 genome. Virology 237:360-377 https://doi.org/10.1006/viro.1997.8805
  26. Lu, Z., Li, Y., Zhang, Y., Kutish, G. F., Rock, D. L. and Van Etten, J. L. 1995. Analysis of 45kb of DNA located at the left end of the chlorella virus PBCV-1 genome. Virology 206:339-352 https://doi.org/10.1016/S0042-6822(95)80049-2
  27. Lu, Z., Li, Y., Que, Q., Kutish, G. F., Rock, D. L. and Van Etten, J. L. 1996. Analysis of 94 kb of the Chlorella virus PBCV-1 330 kb genome: Map position 88 to 182. Virology 216:102-123 https://doi.org/10.1006/viro.1996.0038
  28. Nishida, K., Suzuki, S., Kimura, Y., Nomura, N., Fujie, M. and Yamada, T. 1998. Group I introns found in chlorella viruses: Biological implications. Virology 242:319-326 https://doi.org/10.1006/viro.1998.9030
  29. Nishida, K., Kawasaki, T., Fujie, M., Usami, S. and Yamada, T. 1999. Aminoacylation of tRNAs encoded by Chlorella virus CVK2. Virology 263:220-229 https://doi.org/10.1006/viro.1999.9949
  30. Plunkett, III, G., Rose, D. J., Durfee, T. J. and Blattner, F. R. 1999. Sequence of Shiga toxin 2 phage 933W from Escherichia coli O157:H7:Shiga toxin as a phage late-gene product. J. Bacteriol. 181:1767-1778
  31. Schuster, A. M., Graves, M., Korth, K., Ziegelbein, M., Brumbaugh, J., Grone, D. and Meints, R. H. 1990. Transcription and sequence studies of a 4.3kbp fragment from a dsDNA eukaryotic algal virus. Virology 176:515-523 https://doi.org/10.1016/0042-6822(90)90021-I
  32. Smith, M. C. M., Burns, R. N., Wilson, S. E. and Gregory, M. A. 1999. The complete genome sequence of the Streptomyces temperate phage ${\varphi}$ C31: evolutionary relationships to other viruses. Nucl. Acids Res. 27:2145-2155 https://doi.org/10.1093/nar/27.10.2145
  33. Songsri, P., Hiramatsu, S., Fujie, M. and Yamada, T. 1997. Proteolytic processing of Chlorella virus CVK2 capsid proteins. Virology 227:252-254 https://doi.org/10.1006/viro.1996.8298
  34. Sun, L., Adams, B., Gumon, J. R., Ye, Y. and Van Etten, J. L. 1999. Characterization of two chitinase genes and one chitosanase gene encoded by chlorella virus PBCV-1. Virology 263:376-387 https://doi.org/10.1006/viro.1999.9958
  35. Van Etten, J. L., Meints, R. H., Burbank, D. E., Kuczmarski, D., Cuppels, D. A. and Lane, L. C. 1981. Isolation and characterization of a virus from the intracellular green alga symbiotic with Hydra viridis. Virology 113:704-711 https://doi.org/10.1016/0042-6822(81)90199-9
  36. Van Etten, J. L., Burbank, D. E., Kuczmarski, D. and Meints, R. H. 1983. Virus infection of culturable Chlorella-like algea and development of a plaque assay. Science 219:994-996 https://doi.org/10.1126/science.219.4587.994
  37. Van Etten, J. L., Lane, L. C., and Meints, R. H. 1991. Viruses and viruslike particles of eukaryotic algae. Microbiol. Rev. 55:586-620
  38. Van Etten, J. L. 2003. Unusual life style of giant chlorella viruses. Annu. Rev. Gen. 37:153-195 https://doi.org/10.1146/annurev.genet.37.110801.143915
  39. Wilson, J. 1972. Ph.D. thesis, California Institute of Technology, Division of Biology, Pasadena, Calif
  40. Xia, Y. and Van Etten, J. L. 1986. DNA methyltransferase induced by PBCV-1 virus infection of a Chlorella-like green algea. Mol. Cell. Biol. 6:1440-1445 https://doi.org/10.1128/MCB.6.5.1440
  41. Yamada, T., Higashiyama, T. and Fukuda, T. 1991. Screening of natural waters for viruses infect Chlorella cells. Appl. Environ. Microbiol. 57:3433-3437
  42. Yamada, T., Fukuda, T., Tamura, K., Furukawa, S. and Songsri, P. 1993. Expression of the gene encoding a translational elongation factor 3 homolog of chlorella virus CVK2. Virology 197:742-750 https://doi.org/10.1006/viro.1993.1650
  43. Yamada, T., Hiramatsu, S., Songsri, P. and Fujie, M. 1997. Alternative expression of a chitosanase gene produces two different proteins in cells infected with Chlorella virus CVK2. Virology 230:361-368 https://doi.org/10.1006/viro.1997.8486
  44. Zhang, Y., Burbank, D. E. and Van Etten, J. L. 1998. Chlorella viruses isolated in China. Appl. Environ. Microbiol. 54:2170-2173

Cited by

  1. Coevolution mechanisms that adapt viruses to genetic code variations implemented in their hosts vol.95, pp.1, 2016, https://doi.org/10.1007/s12041-016-0612-7