1887

Abstract

P1a and P1b are two serine proteases of (an ipomovirus). They belong to the group of P1 factors present at the N terminus of the polyproteins of most members of the family . The present work compares the protease activities of P1a and P1b in different experimental systems. The findings made regarding how these two proteases work, such as the requirement for a host factor by P1a but not by P1b, underscore important differences in their catalytic activity that point towards their undergoing divergent evolution involving the acquisition of mechanistic variations. The expression of several truncated forms of P1b and helped define the protease domain of P1b, along with other important features such as its apparently mode of action. Recent phylogenetic data, together with the present results, allow an appealing hypothesis to be proposed regarding P1 evolution and its involvement in potyvirid speciation.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.050781-0
2013-06-01
2019-10-15
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/6/1407.html?itemId=/content/journal/jgv/10.1099/vir.0.050781-0&mimeType=html&fmt=ahah

References

  1. Abraham A. , Menzel W. , Vetten H. J. , Winter S. . ( 2012; ). Analysis of the tomato mild mottle virus genome indicates that it is the most divergent member of the genus Ipomovirus (family Potyviridae). . Arch Virol 157:, 353–357. [CrossRef] [PubMed]
    [Google Scholar]
  2. Adams M. J. , Zerbini F. M. , French R. , Rabenstein F. , Stenger D. C. , Valkonen J. P. T. . ( 2012; ). Family Potyviridae . . In Virus Taxonomy, pp. 1069–1090. Edited by King A. M. Q. , Adams M. J. , Carstens E. B. , Lefkowitz E. J. . . Oxford:: Elsevier;.
    [Google Scholar]
  3. Anandalakshmi R. , Pruss G. J. , Ge X. , Marathe R. , Mallory A. C. , Smith T. H. , Vance V. B. . ( 1998; ). A viral suppressor of gene silencing in plants. . Proc Natl Acad Sci U S A 95:, 13079–13084. [CrossRef] [PubMed]
    [Google Scholar]
  4. Berger P. H. , Hunt A. G. , Domier L. L. , Hellmann G. M. , Stram Y. , Thornbury D. W. , Pirone T. P. . ( 1989; ). Expression in transgenic plants of a viral gene product that mediates insect transmission of potyviruses. . Proc Natl Acad Sci U S A 86:, 8402–8406. [CrossRef] [PubMed]
    [Google Scholar]
  5. Brigneti G. , Voinnet O. , Li W. X. , Ji L. H. , Ding S. W. , Baulcombe D. C. . ( 1998; ). Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. . EMBO J 17:, 6739–6746. [CrossRef] [PubMed]
    [Google Scholar]
  6. Carbonell A. , Dujovny G. , García J. A. , Valli A. . ( 2012; ). The Cucumber vein yellowing virus silencing suppressor P1b can functionally replace HCPro in Plum pox virus infection in a host-specific manner. . Mol Plant Microbe Interact 25:, 151–164. [CrossRef] [PubMed]
    [Google Scholar]
  7. Carrington J. C. , Freed D. D. , Sanders T. C. . ( 1989; ). Autocatalytic processing of the potyvirus helper component proteinase in Escherichia coli and in vitro. . J Virol 63:, 4459–4463.[PubMed]
    [Google Scholar]
  8. Carrington J. C. , Freed D. D. , Oh C. S. . ( 1990; ). Expression of potyviral polyproteins in transgenic plants reveals three proteolytic activities required for complete processing. . EMBO J 9:, 1347–1353.[PubMed]
    [Google Scholar]
  9. Cronin S. , Verchot J. , Haldeman-Cahill R. , Schaad M. C. , Carrington J. C. . ( 1995; ). Long-distance movement factor: a transport function of the potyvirus helper component proteinase. . Plant Cell 7:, 549–559.[PubMed] [CrossRef]
    [Google Scholar]
  10. Curtis M. D. , Grossniklaus U. . ( 2003; ). A gateway cloning vector set for high-throughput functional analysis of genes in planta. . Plant Physiol 133:, 462–469. [CrossRef] [PubMed]
    [Google Scholar]
  11. Felsenstein J. . ( 1985; ). Confidence limits on phylogenies: An approach using the bootstrap. . Evolution 39:, 783–791. [CrossRef]
    [Google Scholar]
  12. García J. A. , Cervera M. T. , Riechmann J. L. , López-Otín C. . ( 1993; ). Inhibitory effects of human cystatin C on plum pox potyvirus proteases. . Plant Mol Biol 22:, 697–701. [CrossRef] [PubMed]
    [Google Scholar]
  13. Gibbs A. , Ohshima K. . ( 2010; ). Potyviruses and the digital revolution. . Annu Rev Phytopathol 48:, 205–223. [CrossRef] [PubMed]
    [Google Scholar]
  14. Gibbs A. J. , Ohshima K. , Phillips M. J. , Gibbs M. J. . ( 2008; ). The prehistory of potyviruses: their initial radiation was during the dawn of agriculture. . PLoS ONE 3:, e2523. [CrossRef] [PubMed]
    [Google Scholar]
  15. Giner A. , Lakatos L. , García-Chapa M. , López-Moya J. J. , Burgyán J. . ( 2010; ). Viral protein inhibits RISC activity by argonaute binding through conserved WG/GW motifs. . PLoS Pathog 6:, e1000996. [CrossRef] [PubMed]
    [Google Scholar]
  16. Goujon M. , McWilliam H. , Li W. , Valentin F. , Squizzato S. , Paern J. , Lopez R. . ( 2010; ). A new bioinformatics analysis tools framework at EMBL-EBI. . Nucleic Acids Res 38: (Web Server issue), W695–W699. [CrossRef] [PubMed]
    [Google Scholar]
  17. Guo B. , Lin J. , Ye K. . ( 2011; ). Structure of the autocatalytic cysteine protease domain of potyvirus helper-component proteinase. . J Biol Chem 286:, 21937–21943. [CrossRef] [PubMed]
    [Google Scholar]
  18. Janssen D. , Martín G. , Velasco L. , Gómez P. , Segundo E. , Ruiz L. , Cuadrado I. M. . ( 2005; ). Absence of a coding region for the helper component-proteinase in the genome of cucumber vein yellowing virus, a whitefly-transmitted member of the Potyviridae. . Arch Virol 150:, 1439–1447. [CrossRef] [PubMed]
    [Google Scholar]
  19. Kasschau K. D. , Carrington J. C. . ( 1998; ). A counterdefensive strategy of plant viruses: suppression of posttranscriptional gene silencing. . Cell 95:, 461–470. [CrossRef] [PubMed]
    [Google Scholar]
  20. Kasschau K. D. , Cronin S. , Carrington J. C. . ( 1997; ). Genome amplification and long-distance movement functions associated with the central domain of tobacco etch potyvirus helper component-proteinase. . Virology 228:, 251–262. [CrossRef] [PubMed]
    [Google Scholar]
  21. Kondo T. , Fujita T. . ( 2012; ). Complete nucleotide sequence and construction of an infectious clone of Chinese yam necrotic mosaic virus suggest that macluraviruses have the smallest genome among members of the family Potyviridae. . Arch Virol 157:, 2299–2307. [CrossRef] [PubMed]
    [Google Scholar]
  22. Larkin M. A. , Blackshields G. , Brown N. P. , Chenna R. , McGettigan P. A. , McWilliam H. , Valentin F. , Wallace I. M. , Wilm A. . & other authors ( 2007; ). Clustal W and Clustal X version 2.0. . Bioinformatics 23:, 2947–2948. [CrossRef] [PubMed]
    [Google Scholar]
  23. Li W. , Hilf M. E. , Webb S. E. , Baker C. A. , Adkins S. . ( 2008; ). Presence of P1b and absence of HC-Pro in Squash vein yellowing virus suggests a general feature of the genus Ipomovirus in the family Potyviridae. . Virus Res 135:, 213–219. [CrossRef] [PubMed]
    [Google Scholar]
  24. Mbanzibwa D. R. , Tian Y. , Mukasa S. B. , Valkonen J. P. . ( 2009a; ). Cassava brown streak virus (Potyviridae) encodes a putative Maf/HAM1 pyrophosphatase implicated in reduction of mutations and a P1 proteinase that suppresses RNA silencing but contains no HC-Pro. . J Virol 83:, 6934–6940. [CrossRef] [PubMed]
    [Google Scholar]
  25. Mbanzibwa D. R. , Tian Y. P. , Tugume A. K. , Mukasa S. B. , Tairo F. , Kyamanywa S. , Kullaya A. , Valkonen J. P. . ( 2009b; ). Genetically distinct strains of Cassava brown streak virus in the Lake Victoria basin and the Indian Ocean coastal area of East Africa. . Arch Virol 154:, 353–359. [CrossRef] [PubMed]
    [Google Scholar]
  26. OEPP/EPPO ( 2005; ). Cucumber vein yellowing ipomovirus. . OEPP/EPPO Bul 35:, 419–421.[CrossRef]
    [Google Scholar]
  27. Puig O. , Caspary F. , Rigaut G. , Rutz B. , Bouveret E. , Bragado-Nilsson E. , Wilm M. , Séraphin B. . ( 2001; ). The tandem affinity purification (TAP) method: a general procedure of protein complex purification. . Methods 24:, 218–229. [CrossRef] [PubMed]
    [Google Scholar]
  28. Rigaut G. , Shevchenko A. , Rutz B. , Wilm M. , Mann M. , Séraphin B. . ( 1999; ). A generic protein purification method for protein complex characterization and proteome exploration. . Nat Biotechnol 17:, 1030–1032. [CrossRef] [PubMed]
    [Google Scholar]
  29. Roho . ž ková J. , Navrátil M. . ( 2011; ). P1 peptidase–a mysterious protein of family Potyviridae. . J Biosci 36:, 189–200. [CrossRef] [PubMed]
    [Google Scholar]
  30. Rojas M. R. , Zerbini F. M. , Allison R. F. , Gilbertson R. L. , Lucas W. J. . ( 1997; ). Capsid protein and helper component-proteinase function as potyvirus cell-to-cell movement proteins. . Virology 237:, 283–295. [CrossRef] [PubMed]
    [Google Scholar]
  31. Salvador B. , Saénz P. , Yangüez E. , Quiot J. B. , Quiot L. , Delgadillo M. O. , García J. A. , Simón-Mateo C. . ( 2008; ). Host-specific effect of P1 exchange between two potyviruses. . Mol Plant Pathol 9:, 147–155. [CrossRef] [PubMed]
    [Google Scholar]
  32. Shukla D. D. , Ward C. W. , Brunt A. A. , Berger P. H. . ( 1998; ). Potyviridae family. AAB Description of plant viruses no. 366. . http://www.dpvweb.net/dpv/showdpv.php?dpvno = 366.
    [Google Scholar]
  33. Tatineni S. , Qu F. , Li R. , Morris T. J. , French R. . ( 2012; ). Triticum mosaic poacevirus enlists P1 rather than HC-Pro to suppress RNA silencing-mediated host defense. . Virology 433:, 104–115. [CrossRef] [PubMed]
    [Google Scholar]
  34. Thornbury D. W. , van den Heuvel J. F. , Lesnaw J. A. , Pirone T. P. . ( 1993; ). Expression of potyvirus proteins in insect cells infected with a recombinant baculovirus. . J Gen Virol 74:, 2731–2735. [CrossRef] [PubMed]
    [Google Scholar]
  35. Valli A. , Martín-Hernández A. M. , López-Moya J. J. , García J. A. . ( 2006; ). RNA silencing suppression by a second copy of the P1 serine protease of Cucumber vein yellowing ipomovirus, a member of the family Potyviridae that lacks the cysteine protease HCPro. . J Virol 80:, 10055–10063. [CrossRef] [PubMed]
    [Google Scholar]
  36. Valli A. , López-Moya J. J. , García J. A. . ( 2007; ). Recombination and gene duplication in the evolutionary diversification of P1 proteins in the family Potyviridae. . J Gen Virol 88:, 1016–1028. [CrossRef] [PubMed]
    [Google Scholar]
  37. Valli A. , Dujovny G. , García J. A. . ( 2008; ). Protease activity, self interaction, and small interfering RNA binding of the silencing suppressor p1b from cucumber vein yellowing ipomovirus. . J Virol 82:, 974–986. [CrossRef] [PubMed]
    [Google Scholar]
  38. Valli A. , Oliveros J. C. , Molnar A. , Baulcombe D. , García J. A. . ( 2011; ). The specific binding to 21-nt double-stranded RNAs is crucial for the anti-silencing activity of Cucumber vein yellowing virus P1b and perturbs endogenous small RNA populations. . RNA 17:, 1148–1158. [CrossRef] [PubMed]
    [Google Scholar]
  39. Verchot J. , Carrington J. C. . ( 1995; ). Evidence that the potyvirus P1 proteinase functions in trans as an accessory factor for genome amplification. . J Virol 69:, 3668–3674.[PubMed]
    [Google Scholar]
  40. Verchot J. , Koonin E. V. , Carrington J. C. . ( 1991; ). The 35-kDa protein from the N-terminus of the potyviral polyprotein functions as a third virus-encoded proteinase. . Virology 185:, 527–535. [CrossRef] [PubMed]
    [Google Scholar]
  41. Verchot J. , Herndon K. L. , Carrington J. C. . ( 1992; ). Mutational analysis of the tobacco etch potyviral 35-kDa proteinase: identification of essential residues and requirements for autoproteolysis. . Virology 190:, 298–306. [CrossRef] [PubMed]
    [Google Scholar]
  42. Waterhouse A. M. , Procter J. B. , Martin D. M. , Clamp M. , Barton G. J. . ( 2009; ). Jalview Version 2–a multiple sequence alignment editor and analysis workbench. . Bioinformatics 25:, 1189–1191. [CrossRef] [PubMed]
    [Google Scholar]
  43. You Y. , Shirako Y. . ( 2010; ). Bymovirus reverse genetics: requirements for RNA2-encoded proteins in systemic infection. . Mol Plant Pathol 11:, 383–394. [CrossRef] [PubMed]
    [Google Scholar]
  44. Young B. A. , Stenger D. C. , Qu F. , Morris T. J. , Tatineni S. , French R. . ( 2012; ). Tritimovirus P1 functions as a suppressor of RNA silencing and an enhancer of disease symptoms. . Virus Res 163:, 672–677. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.050781-0
Loading
/content/journal/jgv/10.1099/vir.0.050781-0
Loading

Data & Media loading...

Supplements

Supplementary material 

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