Abstract
Beijerinck's (1898) recognition that the cause of tobacco mosaic disease was a novel kind of pathogen became the breakthrough which eventually led to the establishment of virology as a science. Research on this agent, tobacco mosaic virus (TMV), has continued to be at the forefront of virology for the past century. After an initial phase, in which numerous biological properties of TMV were discovered, its particles were the first shown to consist of RNA and protein, and X-ray diffraction analysis of their structure was the first of a helical nucleoprotein. In the molecular biological phase of research, TMV RNA was the first plant virus genome to be sequenced completely, its genes were found to be expressed by cotranslational particle disassembly and the use of subgenomic mRNA, and the mechanism of assembly of progeny particles from their separate parts was discovered. Molecular genetical and cell biological techniques were then used to clarify the roles and modes of action of the TMV non-structural proteins: the 126 kDa and 183 kDa replicase components and the 30 kDa cell-to-cell movement protein. Three different TMV genes were found to act as avirulence genes, eliciting hypersensitive responses controlled by specific, but different, plant genes. One of these (the N gene) was the first plant gene controlling virus resistance to be isolated and sequenced. In the biotechnological sphere, TMV has found several applications: as the first source of transgene sequences conferring virus resistance, in vaccines consisting of TMV particles genetically engineered to carry foreign epitopes, and in systems for expressing foreign genes. TMV owes much of its popularity as a research mode to the great stability and high yield of its particles. Although modern methods have much decreased the need for such properties, and TMV may have a less dominant role in the future, it continues to occupy a prominent position in both fundamental and applied research.
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- ANDERER F. A. Preparation and properties of an artificial antigen immunologically related to tobacco mosaic virus. Biochim Biophys Acta. 1963 Apr 2;71:246–248. doi: 10.1016/0006-3002(63)91077-1. [DOI] [PubMed] [Google Scholar]
- ANDERER F. A., UHLIG H., WEBER E., SCHRAMM G. Primary structure of the protein of tobacco mosaic virus. Nature. 1960 Jun 18;186:922–925. doi: 10.1038/186922a0. [DOI] [PubMed] [Google Scholar]
- Abel P. P., Nelson R. S., De B., Hoffmann N., Rogers S. G., Fraley R. T., Beachy R. N. Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science. 1986 May 9;232(4751):738–743. doi: 10.1126/science.3457472. [DOI] [PubMed] [Google Scholar]
- Butler P. J., Finch J. T., Zimmern D. Configuration of tobacco mosaic virus, RNA during virus assembly. Nature. 1977 Jan 20;265(5591):217–219. doi: 10.1038/265217a0. [DOI] [PubMed] [Google Scholar]
- Butler P. J., Klug A. Assembly of the particle of tobacco mosaic virus from RNA and disks of protein. Nat New Biol. 1971 Jan 13;229(2):47–50. doi: 10.1038/newbio229047a0. [DOI] [PubMed] [Google Scholar]
- Citovsky V., Knorr D., Schuster G., Zambryski P. The P30 movement protein of tobacco mosaic virus is a single-strand nucleic acid binding protein. Cell. 1990 Feb 23;60(4):637–647. doi: 10.1016/0092-8674(90)90667-4. [DOI] [PubMed] [Google Scholar]
- Dawson W. O., Beck D. L., Knorr D. A., Grantham G. L. cDNA cloning of the complete genome of tobacco mosaic virus and production of infectious transcripts. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1832–1836. doi: 10.1073/pnas.83.6.1832. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fraenkel-Conrat H., Williams R. C. RECONSTITUTION OF ACTIVE TOBACCO MOSAIC VIRUS FROM ITS INACTIVE PROTEIN AND NUCLEIC ACID COMPONENTS. Proc Natl Acad Sci U S A. 1955 Oct 15;41(10):690–698. doi: 10.1073/pnas.41.10.690. [DOI] [PMC free article] [PubMed] [Google Scholar]
- GIERER A., MUNDRY K. W. Production of mutants of tobacco mosaic virus by chemical alteration of its ribonucleic acid in vitro. Nature. 1958 Nov 22;182(4647):1457–1458. doi: 10.1038/1821457a0. [DOI] [PubMed] [Google Scholar]
- GIERER A., SCHRAMM G. Infectivity of ribonucleic acid from tobacco mosaic virus. Nature. 1956 Apr 14;177(4511):702–703. doi: 10.1038/177702a0. [DOI] [PubMed] [Google Scholar]
- Gallie D. R., Sleat D. E., Watts J. W., Turner P. C., Wilson T. M. The 5'-leader sequence of tobacco mosaic virus RNA enhances the expression of foreign gene transcripts in vitro and in vivo. Nucleic Acids Res. 1987 Apr 24;15(8):3257–3273. doi: 10.1093/nar/15.8.3257. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gianinazzi S., Martin C., Vallée J. C. Hypersensibilité aux virus, température et protéines soubles chez le Nicotiana Xanthi n.c. Apparition de nouvelles macromolécules lors de la répression de la synthèse virale. C R Acad Sci Hebd Seances Acad Sci D. 1970 May 11;270(19):2383–2386. [PubMed] [Google Scholar]
- Goelet P., Lomonossoff G. P., Butler P. J., Akam M. E., Gait M. J., Karn J. Nucleotide sequence of tobacco mosaic virus RNA. Proc Natl Acad Sci U S A. 1982 Oct;79(19):5818–5822. doi: 10.1073/pnas.79.19.5818. [DOI] [PMC free article] [PubMed] [Google Scholar]
- HARRIS J. I., KNIGHT C. A. Action of carboxypeptidase on tobacco mosaic virus. Nature. 1952 Oct 11;170(4328):613–614. doi: 10.1038/170613a0. [DOI] [PubMed] [Google Scholar]
- Harrison B. D., Finch J. T., Gibbs A. J., Hollings M., Shepherd R. J., Valenta V., Wetter C. Sixteen groups of plant viruses. Virology. 1971 Aug;45(2):356–363. doi: 10.1016/0042-6822(71)90336-9. [DOI] [PubMed] [Google Scholar]
- Hunter T. R., Hunt T., Knowland J., Zimmern D. Messenger RNA for the coat protein of tobacco mosaic virus. Nature. 1976 Apr 29;260(5554):759–764. doi: 10.1038/260759a0. [DOI] [PubMed] [Google Scholar]
- Jackson A. O., Zaitlin M., Siegel A., Francki R. I. Replication of tobacco mosaic virus. 3. Viral RNA metabolism in separated leaf cells. Virology. 1972 Jun;48(3):655–665. doi: 10.1016/0042-6822(72)90150-x. [DOI] [PubMed] [Google Scholar]
- Lebeurier G., Nicolaieff A., Richards K. E. Inside-out model for self-assembly of tobacco mosaic virus. Proc Natl Acad Sci U S A. 1977 Jan;74(1):149–153. doi: 10.1073/pnas.74.1.149. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Legrand M., Kauffmann S., Geoffroy P., Fritig B. Biological function of pathogenesis-related proteins: Four tobacco pathogenesis-related proteins are chitinases. Proc Natl Acad Sci U S A. 1987 Oct;84(19):6750–6754. doi: 10.1073/pnas.84.19.6750. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meshi T., Ishikawa M., Motoyoshi F., Semba K., Okada Y. In vitro transcription of infectious RNAs from full-length cDNAs of tobacco mosaic virus. Proc Natl Acad Sci U S A. 1986 Jul;83(14):5043–5047. doi: 10.1073/pnas.83.14.5043. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Namba K., Stubbs G. Structure of tobacco mosaic virus at 3.6 A resolution: implications for assembly. Science. 1986 Mar 21;231(4744):1401–1406. doi: 10.1126/science.3952490. [DOI] [PubMed] [Google Scholar]
- Ohno T., Takamatsu N., Meshi T., Okada Y., Nishiguchi M., Kiho Y. Single amino acid substitution in 30K protein of TMV defective in virus transport function. Virology. 1983 Nov;131(1):255–258. doi: 10.1016/0042-6822(83)90551-2. [DOI] [PubMed] [Google Scholar]
- Osman T. A., Buck K. W. The tobacco mosaic virus RNA polymerase complex contains a plant protein related to the RNA-binding subunit of yeast eIF-3. J Virol. 1997 Aug;71(8):6075–6082. doi: 10.1128/jvi.71.8.6075-6082.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pelham H. R. Leaky UAG termination codon in tobacco mosaic virus RNA. Nature. 1978 Mar 30;272(5652):469–471. doi: 10.1038/272469a0. [DOI] [PubMed] [Google Scholar]
- Register J. C., 3rd, Beachy R. N. Resistance to TMV in transgenic plants results from interference with an early event in infection. Virology. 1988 Oct;166(2):524–532. doi: 10.1016/0042-6822(88)90523-5. [DOI] [PubMed] [Google Scholar]
- Saito T., Meshi T., Takamatsu N., Okada Y. Coat protein gene sequence of tobacco mosaic virus encodes a host response determinant. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6074–6077. doi: 10.1073/pnas.84.17.6074. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stanley W. M. ISOLATION OF A CRYSTALLINE PROTEIN POSSESSING THE PROPERTIES OF TOBACCO-MOSAIC VIRUS. Science. 1935 Jun 28;81(2113):644–645. doi: 10.1126/science.81.2113.644. [DOI] [PubMed] [Google Scholar]
- TSUGITA A. The proteins of mutants of TMV: composition and structure of chemically evoked mutants of TMV RNA. J Mol Biol. 1962 Sep;5:284–292. doi: 10.1016/s0022-2836(62)80072-2. [DOI] [PubMed] [Google Scholar]
- Takamatsu N., Ishikawa M., Meshi T., Okada Y. Expression of bacterial chloramphenicol acetyltransferase gene in tobacco plants mediated by TMV-RNA. EMBO J. 1987 Feb;6(2):307–311. doi: 10.1002/j.1460-2075.1987.tb04755.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takebe I., Otsuki Y. Infection of tobacco mesophyll protoplasts by tobacco mosaic virus. Proc Natl Acad Sci U S A. 1969 Nov;64(3):843–848. doi: 10.1073/pnas.64.3.843. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tsugita A., Gish D. T., Young J., Fraenkel-Conrat H., Knight C. A., Stanley W. M. THE COMPLETE AMINO ACID SEQUENCE OF THE PROTEIN OF TOBACCO MOSAIC VIRUS. Proc Natl Acad Sci U S A. 1960 Nov;46(11):1463–1469. doi: 10.1073/pnas.46.11.1463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- WATSON J. D. The structure of tobacco mosaic virus. I. X-ray evidence of a helical arrangement of sub-units around the longitudinal axis. Biochim Biophys Acta. 1954 Jan;13(1):10–19. doi: 10.1016/0006-3002(54)90265-6. [DOI] [PubMed] [Google Scholar]
- Westhof E., Altschuh D., Moras D., Bloomer A. C., Mondragon A., Klug A., Van Regenmortel M. H. Correlation between segmental mobility and the location of antigenic determinants in proteins. Nature. 1984 Sep 13;311(5982):123–126. doi: 10.1038/311123a0. [DOI] [PubMed] [Google Scholar]
- Whitham S., Dinesh-Kumar S. P., Choi D., Hehl R., Corr C., Baker B. The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell. 1994 Sep 23;78(6):1101–1115. doi: 10.1016/0092-8674(94)90283-6. [DOI] [PubMed] [Google Scholar]
- Wilson T. M. Plant viruses: a tool-box for genetic engineering and crop protection. Bioessays. 1989 Jun;10(6):179–186. doi: 10.1002/bies.950100602. [DOI] [PubMed] [Google Scholar]
- Wolf S., Deom C. M., Beachy R. N., Lucas W. J. Movement protein of tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science. 1989 Oct 20;246(4928):377–379. doi: 10.1126/science.246.4928.377. [DOI] [PubMed] [Google Scholar]
- Wu X., Shaw J. Bidirectional uncoating of the genomic RNA of a helical virus. Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2981–2984. doi: 10.1073/pnas.93.7.2981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zimmern D. The nucleotide sequence at the origin for assembly on tobacco mosaic virus RNA. Cell. 1977 Jul;11(3):463–482. doi: 10.1016/0092-8674(77)90065-4. [DOI] [PubMed] [Google Scholar]
- van Loon L. C., van Kammen A. Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var. "Samsun" and "Samsun NN". II. Changes in protein constitution after infection with tobacco mosaic virus. Virology. 1970 Feb;40(2):190–211. doi: 10.1016/0042-6822(70)90395-8. [DOI] [PubMed] [Google Scholar]