Mapping the nuclear localization signal in the matrix protein of potato yellow dwarf virus Free

Abstract

The ability of the matrix (M) protein of potato yellow dwarf virus (PYDV) to remodel nuclear membranes is controlled by a di-leucine motif located at residues 223 and 224 of its primary structure. This function can be uncoupled from that of its nuclear localization signal (NLS), which is controlled primarily by lysine and arginine residues immediately downstream of the LL motif. localization of green fluorescent protein fusions, bimolecular fluorescence complementation assays with nuclear import receptor importin-α1 and yeast-based nuclear import assays provided three independent experimental approaches to validate the authenticity of the M-NLS. The carboxy terminus of M is predicted to contain a nuclear export signal, which is belived to be functional, given the ability of M to bind the nuclear export receptor 1 (XPO1). The nuclear shuttle activity of M has implications for the cell-to-cell movement of PYDV nucleocapsids, based upon its interaction with the N and Y proteins.

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2018-05-01
2024-03-29
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References

  1. Amarasinghe GK, Bào Y, Basler CF, Bavari S, Beer M et al. Taxonomy of the order Mononegavirales: update 2017. Arch Virol 2017; 162:2493–2504 [View Article][PubMed]
    [Google Scholar]
  2. Bandyopadhyay A, Kopperud K, Anderson G, Martin K, Goodin M. An integrated protein localization and interaction map for Potato yellow dwarf virus, type species of the genus Nucleorhabdovirus. Virology 2010; 402:61–71 [View Article][PubMed]
    [Google Scholar]
  3. Black LM. Strains of potato yellow-dwarf virus. Am J Bot 1940; 27:386–392 [View Article]
    [Google Scholar]
  4. Hsu HT, Black LM. Inoculation of vector cell monolayers with potato yellow dwarf virus. Virology 1973; 52:187–198 [View Article][PubMed]
    [Google Scholar]
  5. Black LM. Genetic variation in the clover leafhopper's ability to transmit potato yellow-dwarf virus. Genetics 1943; 28:200–209[PubMed]
    [Google Scholar]
  6. Jang C, Wang R, Wells J, Leon F, Farman M et al. Genome sequence variation in the constricta strain dramatically alters the protein interaction and localization map of Potato yellow dwarf virus. J Gen Virol 2017; 98:1526–1536 [View Article][PubMed]
    [Google Scholar]
  7. Black LM, Smith KM, Hills GJ, Markham R. Ultrastructure of potato yellow-dwarf virus. Virology 1965; 27:446–449 [View Article][PubMed]
    [Google Scholar]
  8. Macleod R, Black LM, Moyer FH. The fine structure and intracellular localization of potato yellow dwarf virus. Virology 1966; 29:540–552 [View Article][PubMed]
    [Google Scholar]
  9. Reeder GS, Knudson DL, Macleod R. The ribonucleic acid of potato yellow dwarf virus. Virology 1972; 50:301–304 [View Article][PubMed]
    [Google Scholar]
  10. Brakke MK, van Pelt N. Linear-log sucrose gradients for estimating sedimentation coefficients of plant viruses and nucleic acids. Anal Biochem 1970; 38:56–64 [View Article][PubMed]
    [Google Scholar]
  11. Nagy PD. Tombusvirus-host interactions: co-opted evolutionarily conserved host factors take center court. Annu Rev Virol 2016; 3:491–515 [View Article][PubMed]
    [Google Scholar]
  12. Bejerman N, Mann KS, Dietzgen RG. Alfalfa dwarf cytorhabdovirus P protein is a local and systemic RNA silencing supressor which inhibits programmed RISC activity and prevents transitive amplification of RNA silencing. Virus Res 2016; 224:19–28 [View Article][PubMed]
    [Google Scholar]
  13. Mann KS, Johnson KN, Carroll BJ, Dietzgen RG. Cytorhabdovirus P protein suppresses RISC-mediated cleavage and RNA silencing amplification in planta. Virology 2016; 490:27–40 [View Article][PubMed]
    [Google Scholar]
  14. Harries PA, Palanichelvam K, Bhat S, Nelson RS. Tobacco mosaic virus 126-kDa protein increases the susceptibility of Nicotiana tabacum to other viruses and its dosage affects virus-induced gene silencing. Mol Plant Microbe Interact 2008; 21:1539–1548 [View Article][PubMed]
    [Google Scholar]
  15. Petersen JM, Her LS, Varvel V, Lund E, Dahlberg JE. The matrix protein of vesicular stomatitis virus inhibits nucleocytoplasmic transport when it is in the nucleus and associated with nuclear pore complexes. Mol Cell Biol 2000; 20:8590–8601 [View Article][PubMed]
    [Google Scholar]
  16. Goodin M, Yelton S, Ghosh D, Mathews S, Lesnaw J. Live-cell imaging of rhabdovirus-induced morphological changes in plant nuclear membranes. Mol Plant Microbe Interact 2005; 18:703–709 [View Article][PubMed]
    [Google Scholar]
  17. Goodin MM, Chakrabarty R, Yelton S, Martin K, Clark A et al. Membrane and protein dynamics in live plant nuclei infected with Sonchus yellow net virus, a plant-adapted rhabdovirus. J Gen Virol 2007; 88:1810–1820 [View Article][PubMed]
    [Google Scholar]
  18. Goodin MM, Zaitlin D, Naidu RA, Lommel SA. Nicotiana benthamiana: its history and future as a model for plant-pathogen interactions. Mol Plant Microbe Interact 2008; 21:1015–1026 [View Article][PubMed]
    [Google Scholar]
  19. Anderson G, Wang R, Bandyopadhyay A, Goodin M. The nucleocapsid protein of potato yellow dwarf virus: protein interactions and nuclear import mediated by a non-canonical nuclear localization signal. Front Plant Sci 2012; 3:14 [View Article][PubMed]
    [Google Scholar]
  20. Nakai K, Kanehisa M. A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics 1992; 14:897–911 [View Article][PubMed]
    [Google Scholar]
  21. Kosugi S, Yanagawa H, Terauchi R, Tabata S. NESmapper: accurate prediction of leucine-rich nuclear export signals using activity-based profiles. PLoS Comput Biol 2014; 10:e1003841 [View Article][PubMed]
    [Google Scholar]
  22. Wang Q, Ma X, Qian S, Zhou X, Sun K et al. Rescue of a plant negative-strand RNA virus from cloned cDNA: insights into enveloped plant virus movement and morphogenesis. PLoS Pathog 2015; 11:e1005223 [View Article][PubMed]
    [Google Scholar]
  23. Kosugi S, Hasebe M, Matsumura N, Takashima H, Miyamoto-Sato E et al. Six classes of nuclear localization signals specific to different binding grooves of importin alpha. J Biol Chem 2009; 284:478–485 [View Article][PubMed]
    [Google Scholar]
  24. Wang R, Brattain MG. The maximal size of protein to diffuse through the nuclear pore is larger than 60kDa. FEBS Lett 2007; 581:3164–3170 [View Article][PubMed]
    [Google Scholar]
  25. Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD et al. ExPASy: The proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 2003; 31:3784–3788 [View Article][PubMed]
    [Google Scholar]
  26. Nakai K, Kanehisa M. Expert system for predicting protein localization sites in gram-negative bacteria. Proteins 1991; 11:95–110 [View Article][PubMed]
    [Google Scholar]
  27. La Cour T, Kiemer L, Mølgaard A, Gupta R, Skriver K et al. Analysis and prediction of leucine-rich nuclear export signals. Protein Eng Des Sel 2004; 17:527–536 [View Article][PubMed]
    [Google Scholar]
  28. Min BE, Martin K, Wang R, Tafelmeyer P, Bridges M et al. A host-factor interaction and localization map for a plant-adapted rhabdovirus implicates cytoplasm-tethered transcription activators in cell-to-cell movement. Mol Plant Microbe Interact 2010; 23:1420–1432 [View Article][PubMed]
    [Google Scholar]
  29. Ramalho TO, Figueira AR, Sotero AJ, Wang R, Geraldino Duarte PS et al. Characterization of Coffee ringspot virus-Lavras: a model for an emerging threat to coffee production and quality. Virology 2014; 464-465:385–396 [View Article][PubMed]
    [Google Scholar]
  30. Zaltsman A, Yi BY, Krichevsky A, Gafni Y, Citovsky V. Yeast-plant coupled vector system for identification of nuclear proteins. Plant Physiol 2007; 145:1264–1271 [View Article][PubMed]
    [Google Scholar]
  31. Chakrabarty R, Banerjee R, Chung SM, Farman M, Citovsky V et al. PSITE vectors for stable integration or transient expression of autofluorescent protein fusions in plants: probing Nicotiana benthamiana-virus interactions. Mol Plant Microbe Interact 2007; 20:740–750 [View Article][PubMed]
    [Google Scholar]
  32. Martin K, Kopperud K, Chakrabarty R, Banerjee R, Brooks R et al. Transient expression in Nicotiana benthamiana fluorescent marker lines provides enhanced definition of protein localization, movement and interactions in planta. Plant J 2009; 59:150–162 [View Article][PubMed]
    [Google Scholar]
  33. Martin KM, Dietzgen RG, Wang R, Goodin MM. Lettuce necrotic yellows cytorhabdovirus protein localization and interaction map, and comparison with nucleorhabdoviruses. J Gen Virol 2012; 93:906–914 [View Article][PubMed]
    [Google Scholar]
  34. Dietzgen RG, Martin KM, Anderson G, Goodin MM. In planta localization and interactions of impatiens necrotic spot tospovirus proteins. J Gen Virol 2012; 93:2490–2495 [View Article][PubMed]
    [Google Scholar]
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