Diverse Groups of Plant RNA and DNA Viruses Share Related Movement Proteins that may Possess Chaperone-like Activity Free

Abstract

Amino acid sequences of plant virus proteins mediating cell-to-cell movement were compared to each other and to protein sequences in databases. Two families of movement proteins have been identified, the members of which show statistically significant sequence similarity. The first, larger family (I) encompasses the movement proteins of tobamo-, tobra-, caulimo- and comoviruses, apple chlorotic leaf spot virus (ACLSV) and geminiviruses with bipartite genomes. Thus this family includes viruses which move by two methods, those requiring the coat protein for the cell-to-cell spread (comoviruses) and those not having this requirement (tobamoviruses). The previously unsuspected relationship between the movement proteins of RNA and DNA viruses having no RNA stage in their life cycle (geminiviruses) suggested that their movement mechanisms might be similar. The second, smaller family (II) consists of the movement proteins of tricornaviruses (bromoviruses, cucumoviruses, alfalfa mosaic virus and tobacco streak virus) and dianthoviruses. Alignment of the sequences of family I movement proteins highlighted two motifs, centred at conserved Gly and Asp residues, respectively, which are assumed to be crucial for the movement protein function(s). Screening the amino acid sequence database revealed another conserved motif that is shared by a large subset of family I movement proteins (those of caulimo- and comoviruses, and ACLSV) and the family of cellular 90K heat shock proteins (HSP90). Based on the analogy to HSP90, it is speculated that many plant virus movement proteins may mediate virus transport in a chaperone-like manner.

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1991-12-01
2024-03-29
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References

  1. Agranovsky A. A., Boyko V. P., Karasev A. V., Lunina N. A., Koonin E. V., Dolja V. V. 1991a; Nucleotide sequence of the 3′-terminal half of beet yellows closterovirus RNA genome: unique arrangement of eight virus genes. Journal of General Virology 72:15–23
    [Google Scholar]
  2. Agranovsky A. A., Boyko V. P., Karasev A. V., Koonin E. V., Dolja V. V. 1991b; The putative 65K protein of beet yellows closterovirus is a homologue of HSP70 heat shock proteins. Journal of Molecular Biology 217:603–610
    [Google Scholar]
  3. Allison R. F., Janda M., Ahlquist P. 1989; Sequence of cowpea chlorotic mottle virus RNA 2 and 3 and evidence of a recombination event during bromovirus evolution. Virology 172:321–330
    [Google Scholar]
  4. Allison R., Thompson C., Ahlquist P. 1990; Regeneration of a functional RNA virus genome by recombination between deletion mutants and requirement for cowpea chlorotic mottle virus 3a and coat genes for systemic infection. Proceedings of the National Academy of Sciences, U.S.A. 87:1820–1824
    [Google Scholar]
  5. Atabekov J. G., Taliansky M. E. 1990; Expression of plant virus-specific transport function by various viral genomes. Advances in Virus Research 38:201–248
    [Google Scholar]
  6. Beck D. L., Guilford P. J., Voot D. M., Andersen M. T., Forster R. L. S. 1991; Triple gene block proteins of white clover mosaic potexvirus are required for transport. Virology 183:695–702
    [Google Scholar]
  7. Beckman R. P., Mizzen L. A., Welch W. J. 1990; Interaction of HSP70 with newly synthesized proteins: implications for protein folding and assembly. Science 38:850–853
    [Google Scholar]
  8. Boccara M., Hamilton W. D. O., Baulcombe D. C. 1986; The organization and interviral homologies of genes at the 3′ end of tobacco rattle virus. EMBO Journal 5:223–229
    [Google Scholar]
  9. Brodsky L. I., Drachev A. L., Tatuzov R. L., Chumakov K. M. 1991; GENEBEE: a package of computer programs for biopolymer sequence analysis. Biopolimery i Kletka 7: (in press)
    [Google Scholar]
  10. Brough C. L., Hayes R. J., Morgan A. J., Coutts R. H. A., Buck K. W. 1988; Effect of mutagenesis in vitro on the ability of cloned tomato golden mosaic virus DNA to infect Nicotiana benthamiana plants. Journal of General Virology 69:503–514
    [Google Scholar]
  11. Burke J. M. 1988; Molecular genetics of group I introns – RNA structures and protein factors required for splicing. A review. Gene 73:273–294
    [Google Scholar]
  12. Citovsky V., Zambryski P. 1991; How do plant virus nucleic acids move across plasmodesmata?. BioEssays (in press)
    [Google Scholar]
  13. Citovsky V., Knorr D., Shuster G., Zambryski P. 1990; The P30 movement protein of tobacco mosaic virus is a single-strand nucleic acid binding protein. Cell 60:637–647
    [Google Scholar]
  14. Citovsky V., Knorr D., Zambryski P. 1991; Gene I, a potential cell-to-cell movement locus of cauliflower mosaic virus, encodes an RNA binding protein. Proceedings of the National Academy of Sciences, U.S.A. 88:2476–2480
    [Google Scholar]
  15. Davies J. W., Stanley J. 1989; Geminivirus genes and vectors. Trends in Genetics 5:77–81
    [Google Scholar]
  16. Dayhoff M. O., Barker W. C., Hunt L. T. 1983; Establishing homologies in protein sequences. Methods in Enzymology 91:524–549
    [Google Scholar]
  17. Deom C. M., Oliver M. J., Beachy R. N. 1987; The 30 kilodalton gene product of tobacco mosaic virus potentiates virus movement. Science 237:389–394
    [Google Scholar]
  18. Domier L. L., Shaw J. G., Rhoads R. E. 1987; Potyviral proteins share amino acid sequence homology with picoma-, como- and caulimoviral proteins. Virology 158:20–27
    [Google Scholar]
  19. Doolittle R. F. 1986 On URFs and ORFs Mill Valley: University Science Books;
    [Google Scholar]
  20. Etessami P., Callis R., Ellwood S., Stanley J. 1988; Delimitation of essential genes of cassava latent virus DNA 2. Nucleic Acids Research 16:4811–4829
    [Google Scholar]
  21. Feng D. F., Johnson M. S., Doolittle R. F. 1985; Aligning amino acid sequences: comparison of commonly used methods. Journal of Molecular Evolution 21:112–125
    [Google Scholar]
  22. German S., Candresse T., Lanneau M., Huet J. C., Pernolet J. C., Dunez J. 1990; Nucleotide sequence and genomic organization of apple chlorotic leaf spot virus. Virology 179:104–112
    [Google Scholar]
  23. Gibrat J.-F., Garnier J., Robson B. 1987; Further developments of protein secondary structure predictions using information theory. New parameters and consideration of residue pairs. Journal of Molecular Biology 198:425–443
    [Google Scholar]
  24. Gorbalenya A. E., Blinov V. M., Donchenko A. P., Koonin E. V. 1989; An NTP-binding motif is the most conserved sequence in a highly diverged monophyletic group of proteins involved in positive strand RNA viral replication. Journal of Molecular Evolution 28:256–268
    [Google Scholar]
  25. Hasegawa A., Verver J., Shimada A., Saito M., Goldbach R., van Kammen A. 1989; The complete nucleotide sequence of soybean chlorotic mottle virus DNA and the identification of a novel promoter. Nucleic Acids Research 17:9993–10013
    [Google Scholar]
  26. Hull R. 1989; The movement of viruses in plants. Annual Review of Phytopathology 27:213–240
    [Google Scholar]
  27. Hull R., Saedler J., Longstaff M. 1986; The sequence of carnation etched ring virus DNA: comparison with cauliflower mosaic virus and retroviruses. EMBO Journal 5:3083–3090
    [Google Scholar]
  28. Kitajima E. W., Lauritis J. A. 1969; Plant virions in plasmodesmata. Virology 37:681–685
    [Google Scholar]
  29. Kost S. S., Smith D. F., Sullivan W. P., Welch W. J., Toft O. O. 1989; Binding of heat shock proteins to the avian progesterone receptor. Molecular and Cellular Biology 9:3829–3838
    [Google Scholar]
  30. Koyatsu S., Nishida E., Kadowaki T., Matsuzaki F., Iida K., Harada F., Kasuga M., Sakai H., Yahara L. 1986; Two mammalian heat shock proteins, HSP90 and HSP100, are actin-binding proteins. Proceedings of the National Academy of Sciences, U.S.A. 83:8054–8058
    [Google Scholar]
  31. Lazarowitz S. G., Pinder A. J., Darmsteegt V. D., Rogers S. G. 1989; Maize streak virus genes essentia] for systemic spread and symptom development. EMBO Journal 8:1023–1032
    [Google Scholar]
  32. Leontovich A. M., Gorbalenya A. E., Brodsky L. I. 1990; Generation of a complete local similarity map for two biopolymer sequences (DOTHELIX program of the GENEBEE package). Biopolymery i Kletka 6:12–17
    [Google Scholar]
  33. Linstead P. J., Hills G. J., Plaskitt K. A., Wilson I. G., Harker C. L., Maule A. J. 1988; The subcellular location of the gene 1 product of cauliflower mosaic virus is consistent with a function associated with virus spread. Journal of General Virology 69:1809–1818
    [Google Scholar]
  34. Malyshenko S. I., Kondakova O. A., Taliansky M. E., Atabekov J. G. 1989; Plant virus transport function: complementation by helper viruses is non-specific. Journal of General Virology 70:2751–2757
    [Google Scholar]
  35. Martinez-Izquierdo J. A., Futterer J., Hohn T. 1987; Protein encoded by ORF 1 of cauliflower mosaic virus is part of viral inclusion body. Virology 160:527–530
    [Google Scholar]
  36. Melcher U. 1990; Similarities between putative transport proteins of plant viruses. Journal of General Virology 71:1009–1018
    [Google Scholar]
  37. Meshi T., Watanabe J., Saito T., Sugimoto A., Maeda T., Okada Y. 1987; Function of the 30 kD protein of tobacco mosaic virus: involvement in cell-to-cell movement and dispensability for replication. EMBO Journal 6:2557–2563
    [Google Scholar]
  38. Meshi T., Motoyoshi F., Maeda T., Yoshiowoka S., Watanabe Y. 1989; Mutations in the tobacco mosaic virus 30 kD protein gene overcome Tm-2 resistance in tomato. The Plant Celt 1:515–522
    [Google Scholar]
  39. Meyer M., Hemmer O., Mayo M. A., Fritsch C. 1986; The nucleotide sequence of tobacco black ring virus RNA-2. Journal of General Virology 67:1257–1271
    [Google Scholar]
  40. Morozov S. Yu., Dolja V. V., Atabekov J. G. 1989; Probable reassortment of genetic elements among elongated RNA-containing plant viruses. Journal of Molecular Evolution 29:52–62
    [Google Scholar]
  41. Moser O., Gagey M. -J., Godefroy-Colburn T., Stussi-Garaud G., Ellwart-Tschurtz M., Nitschko H., Mundry K. -W. 1988; The fate of the transport protein of tobacco mosaic virus in systemic and hypersensitive tobacco hosts. Journal of General Virology 69:1367–1373
    [Google Scholar]
  42. Pelham H. R. B. 1990; Function of the Hsp70 protein family: an overview. In Stress Proteins in Biology and Medicine pp 287–289 Edited by Morimoto R. I., Tissieres A., Georgopulos G. New York: Cold Spring Harbor Laboratory;
    [Google Scholar]
  43. Petty I. T. D., Jackson A. O. 1990; Mutational analysis of barley stripe mosaic virus RNA β. Virology 179:712–718
    [Google Scholar]
  44. Prasad B. V. V., Chiu W. 1987; Sequence comparison of single-stranded DNA binding proteins and its structural implications. Journal of Molecular Biology 193:579–584
    [Google Scholar]
  45. Rothman J. E. 1989; Polypeptide chain binding proteins: catalysis of protein folding and related processes in cells. Cell 59:591–601
    [Google Scholar]
  46. Sacher R., Ahlquist P. 1989; Effects of deletions in the N-terminal basic arm of brome mosaic virus coat protein on RNA packaging and systemic infection. Journal of Virology 63:4545–4552
    [Google Scholar]
  47. Saito T., Imai Y., Meshi T., Okada Y. 1988; Interviral homologies of the 30K proteins of tobamoviruses. Virology 167:653–656
    [Google Scholar]
  48. Sanchez E. R., Redmond T., Scherrer L. C., Bresnick E. H., Welch W. J., Pratt W. B. 1988; Evidence that the 90-kilodalton heat shock protein is associated with tubulin-containing complex in L cell cytosol and in intact PtK cells. Molecular Endocrinology 2:756–760
    [Google Scholar]
  49. Savitry H. S., Murthy M. R. N. 1983; Evolutionary relationship of alfalfa mosaic virus with cucumber mosaic virus and brome mosaic virus. Journal of Bioscience 5:183–187
    [Google Scholar]
  50. Stratford R., Covey S. N. 1989; Segregation of cauliflower mosaic virus symptom genetic determinants. Virology 172:451–459
    [Google Scholar]
  51. Taliansky M. E., Malyshenko S. I., Pshennikova E. S., Kaplan I. B., Ulanova E. F., Atabekov J. G. 1982; Plant virus-specific transport function. I. Virus genetic control required for systemic spread. Virology 122:318–326
    [Google Scholar]
  52. Tomenius K., Clapham D., Meshi T. 1987; Localization by immunogold cytochemistry of the virus-coded 30 kD protein in plasmodesmata of leaves infected with tobacco mosaic virus. Virology 160:363–371
    [Google Scholar]
  53. Traynor P., Young B. M., Ahlquist P. 1991; Deletion analysis of brome mosaic virus 2a protein: effects on RNA replication and systemic spread. Journal of Virology 65:2807–2815
    [Google Scholar]
  54. van Lent J., Wellink J., Goldbach R. 1990; Evidence for the involvement of the 58K and 48K proteins in the intercellular movement of cowpea mosaic virus. Journal of General Virology 71:219–223
    [Google Scholar]
  55. Weintraub M., Ragetti H. W. V., Leung E. 1976; Elongated virus particles in plasmodesmata. Journal of Ultrastructure Research 56:351–364
    [Google Scholar]
  56. Welch W. J. 1990; The mammalian stress response: cell physiology and biochemistry of stress proteins. In Stress Proteins in Biology and Medicine pp 101–167 Edited by Morimoto R. I., Tissieres A., Georgopulos G. New York: Cold Spring Harbor Laboratory;
    [Google Scholar]
  57. Wellink J., van Kammen A. 1989; Cell-to-cell transport of cowpea mosaic virus requires both the 58K/48K proteins and the capsid proteins. Journal of General Virology 70:2279–2286
    [Google Scholar]
  58. Wolf S., Deom C. M., Beachy R. N., Lucas W. J. 1989; Movement protein of tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science 246:377–379
    [Google Scholar]
  59. Xiong Z., Lommel S. A. 1989; The complete nucleotide sequence and genome organization of red clover necrotic mosaic virus RNA 1. Virology 171:543–554
    [Google Scholar]
  60. Ziemecky A., Catelli M. G., Joab I., Moncharmont B. 1986; Association of the heat shock protein HSP90 with steroid hormone receptors and tyrosine kinase oncogene product. Biochemical and Biophysical Research Communications 138:1298–1307
    [Google Scholar]
  61. Zimmern D. 1983; Homologous proteins encoded by yeast mitochondrial genome and by a group of RNA viruses from plants. Journal of Molecular Biology 171:345–352
    [Google Scholar]
  62. Zimmern D., Hunter T. 1983; Point mutation in the 30 kD open reading frame of TMV implicated in temperature sensitive assembly and local lesion spreading of mutant Ni2519. EMBO Journal 1:1893–1990
    [Google Scholar]
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