Skip to main content
Log in

Structural properties of potexvirus coat proteins detected by optical methods

  • Regular Papers
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

It has been shown by X-ray analysis that cores of coat proteins (CPs) from three potexviruses, flexible helical RNA-containing plant viruses, have similar α-helical structure. However, this similarity cannot explain structural lability of potexvirus virions, which is believed to determine their biological activity. Here, we used circular dichroism (CD) spectroscopy in the far UV region to compare optical properties of CPs from three potexviruses with the same morphology and similar structure. CPs from Alternanthera mosaic virus (AltMV), potato aucuba mosaic virus (PAMV), and potato virus X (PVX) have been studied in a free state and in virions. The CD spectrum of AltMV virions was similar to the previously obtained CD spectrum of papaya mosaic virus (PapMV) virions, but differed significantly from the CD spectrum of PAMV virions. The CD spectrum of PAMV virions resembled in its basic characteristics the CD spectrum of PVX virions characterized by molar ellipticity that is abnormally low for α-helical proteins. Homology modeling of the CP structures in AltMV, PAMV, and PVX virions was based on the known high-resolution structures of CPs from papaya mosaic virus and bamboo mosaic virus and confirmed that the structures of the CP cores in all three viruses were nearly identical. Comparison of amino acid sequences of different potexvirus CPs and prediction of unstructured regions in these proteins revealed a possible correlation between specific features in the virion CD spectra and the presence of disordered N-terminal segments in the CPs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

AltMV:

Alternanthera mosaic virus

BaMV:

bamboo mosaic virus

CD:

circular dichroism

CP:

coat protein

PAMV:

potato aucuba mosaic virus

PapMV:

papaya mosaic virus

PepMV:

pepino mosaic virus

PVX:

potato virus X

TMV:

tobacco mosaic virus

UV:

ultraviolet

References

  1. Harrison, S. C. (2007) Principles of Virus Structure. Fields Virology (Knipe, D. M., and Howley, P. M., eds.) 5th Edn., Lippincott Williams & Wilkins, pp. 59–98.

  2. Holmes, K., Stubbs, J., Mandelkow, E., and Gallwitz, U. (1975) Structure of tobacco mosaic virus at 6.7 Å resolution, Nature, 254, 192–196.

    Article  CAS  PubMed  Google Scholar 

  3. Bloomer, A. C., Champness, J. N., Bricogne, G., Staden, R., and Klug, A. (1978) Protein disk of tobacco mosaic virus at 2.8 Å resolution showing the interactions within and between subunits, Nature, 276, 362–368.

    Article  CAS  PubMed  Google Scholar 

  4. Namba, K., Pattanayek, R., and Stubbs, G. (1989) Visualization of protein-nucleic acid interactions in a virus. Refined structure of intact tobacco mosaic virus at 2.9 Å resolution by X-ray fiber diffraction, J. Mol. Biol., 208, 307–325.

    Article  CAS  PubMed  Google Scholar 

  5. Kendall, A., McDonald, M., Bian, W., Bowles, T., Baumgarten, S., Shi, J., Stewart, P., Bullitt, E., Gore, D., Irving, T., Havens, W., Ghabrial, S., Wall, J., and Stubbs, G. (2008) Structure of flexible filamentous plant viruses, J. Virol., 82, 9546–9554.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Parker, L., Kendall, A., and Stubbs, G. (2002) Surface features of potato virus X from fiber diffraction, Virology, 300, 291–295.

    Article  CAS  PubMed  Google Scholar 

  7. Nemykh, M. A., Efimov, A. V., Novikov, V. K., Orlov, V. N., Arutyunyan, A. M., Drachev, V. A., Lukashina, E. V., Baratova, L. A., and Dobrov, E. N. (2008) One more probable structural transition in potato virus X virions and a revised model of the virus coat protein structure, Virology, 373, 61–71.

    Article  CAS  PubMed  Google Scholar 

  8. Baratova, L. A., Grebenshchikov, N. I., Dobrov, E. N., Gedrovich, A. V., Kashirin, I. A., Shishkov, A. V., Efimov, A. V., Jarvekulg, L., Radavsky, Y. L., and Saarma, M. (1992) The organization of potato virus X coat proteins in virus particles studied by tritium planigraphy and model building, Virology, 188, 175–180.

    Article  CAS  PubMed  Google Scholar 

  9. Yang, S., Wang, T., Bohon, J., Gagne, M. E., and Bolduc, M. (2012) Crystal structure of the coat protein of the flexible filamentous papaya mosaic virus, J. Mol. Biol., 422, 263–273.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. DiMaio, F., Chen, C. C., Yu, X., Frenz, B., Hsu, Y. H., Lin, N. S., and Egelman, E. H. (2015) The molecular basis for flexibility in the flexible filamentous plant viruses, Nat. Struct. Mol. Biol., 22, 642–644.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Agirrezabala, X., Mendez-Lopez, E., Lasso, G., Sanchez-Pina, M. A., Aranda, M., and Valle, M. (2015) The nearatomic cryoEM structure of a flexible filamentous plant virus shows homology of its coat protein with nucleoproteins of animal viruses, eLife, 4, e11795.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Homer, R., and Goodman, R. (1975) Circular dichroism and fluorescence studies on potato virus X and its structural components, Biochim. Biophys. Acta, 378, 296–304.

    Article  CAS  PubMed  Google Scholar 

  13. Lecours, K., Tremblay, M. H., Gagne, M. E., Gagne, S. M., and Leclerc, D. (2006) Purification and biochemical characterization of a monomeric form of papaya mosaic potexvirus coat protein, Protein Expr. Purif., 47, 273–280.

    Article  CAS  PubMed  Google Scholar 

  14. Tremblay, M., Majeau, N., Gagne, M., Lecours, K., Morin, H., Duvignaud, J., Bolduc, M., Chouinard, N., Pare, C., Gagne, S., and Leclerc, D. (2006) Effect of mutations K97A and E128A on RNA binding and self-assembly of papaya mosaic Potexvirus coat protein, FEBS J., 273, 14–25.

    Article  CAS  PubMed  Google Scholar 

  15. Ivanov, P. A., Mukhamedzhanova, A. A., Smirnov, A. A., Rodionova, N. P., Karpova, O. V., and Atabekov, J. G. (2011) The complete nucleotide sequence of Alternanthera mosaic virus infecting Portulaca grandiflora represents a new strain distinct from phlox isolates, Virus Genes, 42, 268–271.

    Article  CAS  PubMed  Google Scholar 

  16. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M., Appel, R., and Bairoch, R. (2005) Protein identification and analysis tools on the ExPASy Server, in The Proteomics Protocols Handbook (Walker, J. M., ed.) Humana Press, pp. 571–607.

    Chapter  Google Scholar 

  17. Nemykh, M., Novikov, V., Arutyunyan, A., Kalmykov, P., Drachev, V., and Dobrov, E. (2007) Comparative structural stability of subunits of the potato virus X coat protein in solution and in virus particles, Mol. Biol. (Moscow), 41, 630–637.

    Article  CAS  Google Scholar 

  18. Ksenofontov, A., Kozlovsky, V., Kordiukova, L., Radiukhin, V., Timofeeva, A., and Dobrov, E. (2006) Determination of concentration and aggregate size in influenza virus preparations using the true UV-absorption spectra, Mol. Biol. (Moscow), 40, 152–158.

    Article  CAS  Google Scholar 

  19. Sievers, F., Wilm, A., Dineen, D., Gibson, K., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Soding, J., Thompson, J. D., and Higgins, D. G. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega, Mol. Syst. Biol., 7, 539.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Webb, B., and Sali, V. (2014) Comparative protein structure modeling using MODELLER, Curr. Protoc. Bioinformatics, 47, 5.6.1–5.6.32.

    Article  Google Scholar 

  21. Andrade, M., Chacon, P., Merelo, J., and Moran, F. (1993) Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network, Protein Eng., 6, 383–390.

    Article  CAS  PubMed  Google Scholar 

  22. Dobrov, E., Kust, S., Yakovleva, O., and Tikchonenko, T. (1977) Structure of single-stranded virus RNA in situ: II. Optical activity of five tobacco mosaic-like viruses and their components, Biochim. Biophys. Acta, 475, 623–637.

    Article  CAS  PubMed  Google Scholar 

  23. Ward, J., McGuffin, L., Bryson, R., Buxton, B., Jones, D., Prilusky, J., Felder, C., Zeev-Ben-Mordehai, T., Rydberg, E., Man, O., Beckmann, J., Silman, I., and Sussman, J. (2004) The DISOPRED server for the prediction of protein, Bioinformatics, 20, 2138–2139.

    Article  CAS  PubMed  Google Scholar 

  24. Koenig, R. (1972) Anomalous behavior of the coat proteins of potato virus X and cactus virus X during electrophoresis in dodecyl sulphate-containing polyacrylamide gels, Virology, 50, 263–266.

    Article  CAS  PubMed  Google Scholar 

  25. Atabekov, J., Dobrov, E., Karpova, O., and Rodionova, N. (2007) Potato virus X: structure, disassembly and reconstitution, Mol. Plant Pathol., 8, 667–675.

    Article  CAS  PubMed  Google Scholar 

  26. Karpova, O. V., Arkhipenko, M. V., Zaiakina, O. V., Nikitin, N. A., Kiseleva, O. I., Kozlovskii, S. V., Rodionova, N. P., and Atabekov, I. G. (2006) Translational regulation of potato virus X RNA–coat protein complexes: the key role of a coat protein N-terminal peptide, Mol. Biol. (Moscow), 40, 703–710.

    Article  CAS  Google Scholar 

  27. Karpova, O. V., Zayakina, O. V., Arkhipenko, M. V., Sheval, E. V., Kiselyova, O. I., Poljakov, V. Y., Yaminsky, I. V., Rodionova, N. P., and Atabekov, J. G. (2006) Potato virus X RNA-mediated assembly of single-tailed ternary “coat protein–RNA–movement protein” complexes, J. Gen. Virol., 87, 2731–2740.

    Article  CAS  PubMed  Google Scholar 

  28. Makarov, V. V., and Kalinina, N. O. (2016) Structure and noncanonical activities of coat proteins of helical plant viruses, Biochemistry (Moscow), 81, 1–18.

    Article  CAS  Google Scholar 

  29. Lukashina, E., Ksenofontov, A., Fedorova, N., Badun, G., Mukhamedzhanova, A., Karpova, O., Rodionova, N., Baratova, L., and Dobrov, E. (2011) Analysis of the role of the coat protein N-terminal segment in potato virus X virion stability and functional activity, Mol. Plant Pathol., 13, 38–45.

    Article  PubMed  Google Scholar 

  30. Baratova, L. A., Fedorova, N. V., Dobrov, E. N., Lukashina, E. V., Kharlanov, A. N., Nasonov, V. V., Serebryakova, M. V., Kozlovsky, S. V., Zayakina, O. V., and Rodionova, N. P. (2004) N-terminal segment of potato virus X coat protein subunits is glycosylated and mediates formation of a bound water shell on the virion surface, Eur. J. Biochem., 271, 3136–3145.

    Article  CAS  PubMed  Google Scholar 

  31. Kiselyova, O. I., Yaminsky, I. V., Karpova, O. V., Rodionova, N. P., Kozlovsky, S. V., Arkhipenko, M. V., and Atabekov, J. G. (2003) AFM study of potato virus X disassembly induced by movement protein, J. Mol. Biol., 332, 321–323.

    Article  CAS  PubMed  Google Scholar 

  32. Lukashina, E., Badun, G., Fedorova, N., Ksenofontov, A., Nemykh, M., Serebryakova, M., Mukhamedzhanova, A., Karpova, O., Rodionova, N., Baratova, L., and Dobrov, E. (2009) Tritium planigraphy study of structural alterations in the coat protein of potato virus X induced by binding of its triple gene block 1 protein to virions, FEBS J., 276, 7006–7015.

    Article  CAS  PubMed  Google Scholar 

  33. Clare, D. K., Pechnikova, E. V., Skurat, E. V., Makarov, V. V., Sokolova, O. S., Solovyev, A. G., and Orlova, E. V. (2015) Novel inter-subunit contacts in barley stripe mosaic virus revealed by cryo-electron microscopy, Structure, 23, 1815–1826.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to N. O. Kalinina or V. V. Makarov.

Additional information

Original Russian Text © P. I. Semenyuk, O. V. Karpova, A. L. Ksenofontov, N. O. Kalinina, E. N. Dobrov, V. V. Makarov, 2016, published in Biokhimiya, 2016, Vol. 81, No. 12, pp. 1838–1848.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Semenyuk, P.I., Karpova, O.V., Ksenofontov, A.L. et al. Structural properties of potexvirus coat proteins detected by optical methods. Biochemistry Moscow 81, 1522–1530 (2016). https://doi.org/10.1134/S0006297916120130

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297916120130

Key words

Navigation