1887

Abstract

Geminiviruses are a group of small plant viruses responsible for devastating crop damage worldwide. The emergence of agricultural diseases caused by geminiviruses is attributed in part to their high rates of recombination, leading to complementary function between viral components across species and genera. We have developed a mastreviral reporter system based on bean yellow dwarf virus (BeYDV) that replicates to high levels in the plant nucleus, expressing very high levels of GFP. To investigate the potential for complementation of movement function by other geminivirus genera, the movement protein (MP) and nuclear shuttle protein (NSP) from the bipartite begomovirus Bean dwarf mosaic virus (BDMV) were produced and characterized in Nicotiana benthamiana leaves. While overexpression of MP and NSP strongly inhibited GFP expression from the mastreviral reporter and caused adverse plant symptoms, optimizing the expression levels of MP and NSP allowed functional cell-to-cell movement. Hybrid virus vectors were created that express BDMV MP and NSP from mastreviral replicons, allowing efficient cell-to-cell movement comparable to native BDMV replicons. We find that the expression levels of MP and NSP must be fine-tuned to provide sufficient MP/NSP for movement without eliciting the plant hypersensitive response or adversely impacting gene expression from viral replicons. The ability to confer cell-to-cell movement to mastrevirus replicons depended strongly on replicon size: 2.1-2.7 kb replicons were efficiently moved, while 3 kb replicons were inhibited, and 3.9 kb replicons were very strongly inhibited. Optimized expression of MP/NSP from the normally phloem-limited Abutilon mosaic virus (AbMV) allows efficient movement in non-phloem cells.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001275
2019-05-20
2019-10-22
Loading full text...

Full text loading...

References

  1. Scholthof K-BG, Adkins S, Czosnek H, Palukaitis P, Jacquot E et al. Top 10 plant viruses in molecular plant pathology. Mol Plant Pathol 2011;12:938–954 [CrossRef]
    [Google Scholar]
  2. Waigmann E, Ueki S, Trutnyeva K, Citovsky V. The ins and outs of nondestructive cell-to-cell and systemic movement of plant viruses. CRC Crit Rev Plant Sci 2004;23:195–250 [CrossRef]
    [Google Scholar]
  3. Krichevsky A, Kozlovsky SV, Gafni Y, Citovsky V. Nuclear import and export of plant virus proteins and genomes. Mol Plant Pathol 2006;7:131–146 [CrossRef]
    [Google Scholar]
  4. Lucas WJ. Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 2006;344:169–184 [CrossRef]
    [Google Scholar]
  5. Jeske H. Geminiviruses. Curr Top Microbiol Immunol 2009;331:185–226
    [Google Scholar]
  6. Gilbertson RL, Sudarshana M, Jiang H, Rojas MR, Lucas WJ. Limitations on geminivirus genome size imposed by plasmodesmata and virus-encoded movement protein: insights into DNA trafficking. Plant Cell 2003;15:2578–2591 [CrossRef]
    [Google Scholar]
  7. Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor S. Geminiviruses: masters at redirecting and reprogramming plant processes. Nat Rev Microbiol 2013;11:777–788 [CrossRef]
    [Google Scholar]
  8. Rojas MR, Noueiry AO, Lucas WJ, Gilbertson RL. Bean dwarf mosaic geminivirus movement proteins recognize DNA in a form- and size-specific manner. Cell 1998;95:105–113 [CrossRef]
    [Google Scholar]
  9. Hehnle S, Wege C, Jeske H. Interaction of DNA with the movement proteins of geminiviruses revisited. J Virol 2004;78:7698–7706 [CrossRef]
    [Google Scholar]
  10. Zhou Y-C, Garrido-Ramirez ER, Sudarshana MR, Yendluri S, Gilbertson RL. The N-terminus of the begomovirus nuclear shuttle protein (BV1) determines virulence or avirulence in Phaseolus vulgaris. Mol Plant Microbe Interact 2007;20:1523–1534 [CrossRef]
    [Google Scholar]
  11. Sudarshana MR, Wang HL, Lucas WJ, Gilbertson RL. Dynamics of bean dwarf mosaic geminivirus cell-to-cell and long-distance movement in Phaseolus vulgaris revealed, using the green fluorescent protein. MPMI 1998;11:277–291 [CrossRef]
    [Google Scholar]
  12. Hou Y-M, Paplomatas EJ, Gilbertson RL. Host adaptation and replication properties of two bipartite geminiviruses and their pseudorecombinants. MPMI 1998;11:208–217 [CrossRef]
    [Google Scholar]
  13. Zhou Y, Rojas MR, Park MR, Seo YS, Lucas WJ et al. Histone H3 interacts and colocalizes with the nuclear shuttle protein and the movement protein of a geminivirus. J Virol 2011;85:11821–11832 [CrossRef]
    [Google Scholar]
  14. Krenz B, Windeisen V, Wege C, Jeske H, Kleinow T. A plastid-targeted heat shock cognate 70kDa protein interacts with the Abutilon mosaic virus movement protein. Virology 2010;401:6–17 [CrossRef]
    [Google Scholar]
  15. Krenz B, Jeske H, Kleinow T. The induction of stromule formation by a plant DNA-virus in epidermal leaf tissues suggests a novel intra- and intercellular macromolecular trafficking route. Front Plant Sci 2012;3:291 [CrossRef]
    [Google Scholar]
  16. Shepherd DN, Mangwende T, Martin DP, Bezuidenhout M, Kloppers FJ et al. Maize streak virus-resistant transgenic maize: a first for Africa. Plant Biotechnol J 2007;5:759–767 [CrossRef]
    [Google Scholar]
  17. Liu H, Boulton MI, Thomas CL, Prior DA, Oparka KJ et al. Maize streak virus coat protein is karyophyllic and facilitates nuclear transport of viral DNA. Mol Plant Microbe Interact 1999;12:894–900 [CrossRef]
    [Google Scholar]
  18. Azzam O, Frazer J, de la Rosa D, Beaver JS, Ahlquist P et al. Whitefly transmission and efficient ssDNA accumulation of bean golden mosaic geminivirus require functional coat protein. Virology 1994;204:289–296 [CrossRef]
    [Google Scholar]
  19. Jeffrey JL, Pooma W, Petty ITD. Genetic requirements for local and systemic movement of tomato golden mosaic virus in infected plants. Virology 1996;223:208–218 [CrossRef]
    [Google Scholar]
  20. Rojas MR, Hagen C, Lucas WJ, Gilbertson RL. Exploiting chinks in the plant's armor: evolution and emergence of geminiviruses. Annu Rev Phytopathol 2005;43:361–394 [CrossRef]
    [Google Scholar]
  21. Legg JP, Fauquet CM. Cassava mosaic geminiviruses in Africa. Plant Mol Biol 2004;56:585–599 [CrossRef]
    [Google Scholar]
  22. García-Andrés S, Monci F, Navas-Castillo J, Moriones E. Begomovirus genetic diversity in the native plant reservoir solanum nigrum: evidence for the presence of a new virus species of recombinant nature. Virology 2006;350:433–442 [CrossRef]
    [Google Scholar]
  23. Briddon RW, Pinner MS, Stanley J, Markham PG. Geminivirus coat protein gene replacement alters insect specificity. Virology 1990;177:85–94 [CrossRef]
    [Google Scholar]
  24. Kraberger S, Harkins GW, Kumari SG, Thomas JE, Schwinghamer MW et al. Evidence that dicot-infecting mastreviruses are particularly prone to inter-species recombination and have likely been circulating in Australia for longer than in Africa and the Middle East. Virology 2013;444:282–291 [CrossRef]
    [Google Scholar]
  25. Liu L, Pinner MS, Davies JW, Stanley J. Adaptation of the geminivirus bean yellow dwarf virus to dicotyledonous hosts involves both virion-sense and complementary-sense genes. J Gen Virol 1999;80:501–506 [CrossRef]
    [Google Scholar]
  26. van der Walt E, Palmer KE, Martin DP, Rybicki EP. Viable chimaeric viruses confirm the biological importance of sequence specific maize streak virus movement protein and coat protein interactions. Virol J 2008;5:61 [CrossRef]
    [Google Scholar]
  27. Palmer KE, Rybicki EP. Investigation of the potential of maize streak virus to act as an infectious gene vector in maize plants. Arch Virol 2001;146:1089–1104 [CrossRef]
    [Google Scholar]
  28. Mor TS, Moon Y-S, Palmer KE, Mason HS. Geminivirus vectors for high-level expression of foreign proteins in plant cells. Biotechnol Bioeng 2003;81:430–437 [CrossRef]
    [Google Scholar]
  29. Huang Z, Chen Q, Hjelm B, Arntzen C, Mason H. A DNA replicon system for rapid high-level production of virus-like particles in plants. Biotechnol Bioeng 2009;103:706–714 [CrossRef]
    [Google Scholar]
  30. Rosenthal SH, Diamos AG, Mason HS. An intronless form of the tobacco extensin gene terminator strongly enhances transient gene expression in plant leaves. Plant Mol Biol 2018;96:429–443 [CrossRef]
    [Google Scholar]
  31. Diamos AG, Rosenthal SH, Mason HS. 5' and 3' untranslated regions strongly enhance performance of geminiviral replicons in nicotiana benthamiana leaves. Front Plant Sci 2016;7:200 [CrossRef]
    [Google Scholar]
  32. Richter LJ, Thanavala Y, Arntzen CJ, Mason HS. Production of hepatitis B surface antigen in transgenic plants for oral immunization. Nat Biotechnol 2000;18:1167–1171 [CrossRef]
    [Google Scholar]
  33. Huang Z, Mason HS. Conformational analysis of hepatitis B surface antigen fusions in an Agrobacterium-mediated transient expression system. Plant Biotechnol J 2004;2:241–249 [CrossRef]
    [Google Scholar]
  34. Gassmann M, Grenacher B, Rohde B, Vogel J. Quantifying Western blots: pitfalls of densitometry. Electrophoresis 2009;30:1845–1855 [CrossRef]
    [Google Scholar]
  35. Grimsley N, Hohn T, Davies JW, Hohn B. Agrobacterium-mediated delivery of infectious maize streak virus into maize plants. Nature 1987;325:177–179 [CrossRef]
    [Google Scholar]
  36. Diamos AG, Mason HS. Modifying the replication of Geminiviral vectors reduces cell death and enhances expression of biopharmaceutical proteins in nicotiana benthamiana leaves. Front Plant Sci 1974;2018:9
    [Google Scholar]
  37. Diamos AG, Mason HS. Chimeric 3' flanking regions strongly enhance gene expression in plants. Plant Biotechnol J 2018;16:1971–1982 [CrossRef]
    [Google Scholar]
  38. Huang Z, Phoolcharoen W, Lai H, Piensook K, Cardineau G et al. High-level rapid production of full-size monoclonal antibodies in plants by a single-vector DNA replicon system. Biotechnol Bioeng 2010;83:9–17 [CrossRef]
    [Google Scholar]
  39. Varsani A, Shepherd DN, Monjane AL, Owor BE, Erdmann JB et al. Recombination, decreased host specificity and increased mobility may have driven the emergence of maize streak virus as an agricultural pathogen. J Gen Virol 2008;89:2063–2074 [CrossRef]
    [Google Scholar]
  40. Duffy S, Shackelton LA, Holmes EC. Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 2008;9:267–276 [CrossRef]
    [Google Scholar]
  41. Lefeuvre P, Moriones E. Recombination as a motor of host switches and virus emergence: geminiviruses as case studies. Curr Opin Virol 2015;10:14–19 [CrossRef]
    [Google Scholar]
  42. Comai L, Moran P, Maslyar D. Novel and useful properties of a chimeric plant promoter combining CaMV 35S and Mas elements. Plant Mol Biol 1990;15:373–381 [CrossRef]
    [Google Scholar]
  43. Levy A, Czosnek H. The DNA-B of the non-phloem-limited bean dwarf mosaic virus (BDMV) is able to move the phloem-limited Abutilon mosaic virus (AbMV) out of the phloem, but DNA-B of AbMV is unable to confine BDMV to the phloem. Plant Mol Biol 2003;53:789–803 [CrossRef]
    [Google Scholar]
  44. Monjane AL, Pande D, Lakay F, Shepherd DN, van der Walt E et al. Adaptive evolution by recombination is not associated with increased mutation rates in Maize streak virus. BMC Evol Biol 2012;12:252 [CrossRef]
    [Google Scholar]
  45. Monjane AL, Martin DP, Lakay F, Muhire BM, Pande D et al. Extensive recombination-induced disruption of genetic interactions is highly deleterious but can be partially reversed by small numbers of secondary recombination events. J Virol 2014;88:7843–7851 [CrossRef]
    [Google Scholar]
  46. Shen WH, Hohn B. Vectors based on Maize streak virus can replicate to high copy numbers in maize plants. J Gen Virol 1995;76:965–969 [CrossRef]
    [Google Scholar]
  47. Wright EA, Heckel T, Groenendijk J, Davies JW, Boulton MI. Splicing features in Maize streak virus virion- and complementary-sense gene expression. Plant J 1997;12:1285–1297 [CrossRef]
    [Google Scholar]
  48. Dekker EL, Woolston CJ, Xue YB, Cox B, Mullineaux PM. Transcript mapping reveals different expression strategies for the bicistronic RNAs of the geminivirus wheat dwarf virus. Nucleic Acids Res 1991;19:4075–4081 [CrossRef]
    [Google Scholar]
  49. Sugio T, Matsuura H, Matsui T, Matsunaga M, Nosho T et al. Effect of the sequence context of the AUG initiation codon on the rate of translation in dicotyledonous and monocotyledonous plant cells. J Biosci Bioeng 2010;109:170–173 [CrossRef]
    [Google Scholar]
  50. Gallie DR. The 5'-leader of tobacco mosaic virus promotes translation through enhanced recruitment of eIF4F. Nucleic Acids Res 2002;30:3401–3411 [CrossRef]
    [Google Scholar]
  51. Zorzatto C, Machado JPB, Lopes KVG, Nascimento KJT, Pereira WA et al. NIK1-mediated translation suppression functions as a plant antiviral immunity mechanism. Nature 2015;520:679–682 [CrossRef]
    [Google Scholar]
  52. Muñoz-Martín A, Collin S, Herreros E, Mullineaux PM, Fernández-Lobato M et al. Regulation of MSV and WDV virion-sense promoters by WDV nonstructural proteins: a role for their retinoblastoma protein-binding motifs. Virology 2003;306:313–323 [CrossRef]
    [Google Scholar]
  53. Berger MR, Sunter G. Identification of sequences required for AL2-mediated activation of the tomato golden mosaic virus-yellow vein BR1 promoter. J Gen Virol 2013;94:1398–1406 [CrossRef]
    [Google Scholar]
  54. Beyene G, Buenrostro-Nava MT, Damaj MB, Gao S-J, Molina J et al. Unprecedented enhancement of transient gene expression from minimal cassettes using a double terminator. Plant Cell Rep 2011;30:13–25 [CrossRef]
    [Google Scholar]
  55. Hussain M, Mansoor S, Iram S, Fatima AN, Zafar Y. The nuclear shuttle protein of tomato leaf curl New Delhi virus is a pathogenicity determinant. J Virol 2005;79:4434–4439 [CrossRef]
    [Google Scholar]
  56. Wang H, Gilbertson RL, Lucas WJ. Spatial and temporal distribution of bean dwarf mosaic geminivirus in Phaseolus vulgaris and Nicotiana benthamiana. Phytopathology 1996;86:1204–1214 [CrossRef]
    [Google Scholar]
  57. Wege C, Gotthardt RD, Frischmuth T, Jeske H. Fulfilling Koch's postulates for Abutilon mosaic virus. Arch Virol 2000;145:2217–2225 [CrossRef]
    [Google Scholar]
  58. Kleinow T, Tanwir F, Kocher C, Krenz B, Wege C et al. Expression dynamics and ultrastructural localization of epitope-tagged Abutilon mosaic virus nuclear shuttle and movement proteins in Nicotiana benthamiana cells. Virology 2009;391:212–220 [CrossRef]
    [Google Scholar]
  59. Briddon RW, Markham PG. Complementation of bipartite begomovirus movement functions by topocuviruses and curtoviruses. Arch Virol 2001;146:1811–1819 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001275
Loading
/content/journal/jgv/10.1099/jgv.0.001275
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 1

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error