Home LiteratureArticle Details
PMID: 10880461 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

A geminivirus replication protein interacts with the retinoblastoma protein through a novel domain to determine symptoms and tissue specificity of infection in plants.

The EMBO journal ·Vol. 19 ·No. 13 ·2000-07-03 ·Pages 3485-95

Kong LJ, Orozco BM, Roe JL, Nagar S, Ou S, Feiler HS, Durfee T, Miller AB, Gruissem W, Robertson D, Hanley-Bowdoin L

Abstract

Geminiviruses replicate in nuclei of mature plant cells after inducing the accumulation of host DNA replication machinery. Earlier studies showed that the viral replication factor, AL1, is sufficient for host induction and interacts with the cell cycle regulator, retinoblastoma (pRb). Unlike other DNA virus proteins, AL1 does not contain the pRb binding consensus, LXCXE, and interacts with plant pRb homo logues (pRBR) through a novel amino acid sequence. We mapped the pRBR binding domain of AL1 between amino acids 101 and 180 and identified two mutants that are differentially impacted for AL1-pRBR interactions. Plants infected with the E-N140 mutant, which is wild-type for pRBR binding, developed wild-type symptoms and accumulated viral DNA and AL1 protein in epidermal, mesophyll and vascular cells of mature leaves. Plants inoculated with the KEE146 mutant, which retains 16% pRBR binding activity, only developed chlorosis along the veins, and viral DNA, AL1 protein and the host DNA synthesis factor, proliferating cell nuclear antigen, were localized to vascular tissue. These results established the importance of AL1-pRBR interactions during geminivirus infection of plants.

Keywords
Non-programmatic
MeSH Terms
Antigens, Polyomavirus Transforming/metabolism Base Sequence DNA Primers Geminiviridae/isolation & purification,metabolism,physiology Plants/virology Protein Binding Retinoblastoma Protein/metabolism Viral Proteins/metabolism Virus Replication
Chemicals
Antigens, Polyomavirus Transforming DNA Primers Retinoblastoma Protein Viral Proteins
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Kong L J
Departments of Biochemistry and Botany, North Carolina State University, Raleigh, NC 27695, USA.
Orozco B M
Roe J L
Nagar S
Ou S
Feiler H S
Durfee T
Miller A B
Gruissem W
Robertson D
Hanley-Bowdoin L
References (57)
57 references, click to expand
  1. The two nonstructural proteins from wheat dwarf virus involved in viral gene expression and replication are retinoblastoma-binding proteins.
    Virology. 1996 May 1;219(1):324-9 PMID: 8623550
  2. Genetic analysis of the tomato golden mosaic virus. II. The product of the AL1 coding sequence is required for replication.
    Nucleic Acids Res. 1988 Jul 25;16(14B):7043-60 PMID: 3405758
  3. The cloning of plant E2F, a retinoblastoma-binding protein, reveals unique and conserved features with animal G(1)/S regulators.
    Nucleic Acids Res. 1999 Sep 1;27(17):3527-33 PMID: 10446243
  4. Efficient generation of infectious recombinant baculoviruses by site-specific transposon-mediated insertion of foreign genes into a baculovirus genome propagated in Escherichia coli.
    J Virol. 1993 Aug;67(8):4566-79 PMID: 8392598
  5. Interactions between geminivirus replication proteins.
    J Virol. 1996 Oct;70(10):6790-5 PMID: 8794317
  6. Identification and analysis of a retinoblastoma binding motif in the replication protein of a plant DNA virus: requirement for efficient viral DNA replication.
    EMBO J. 1995 Aug 15;14(16):4073-82 PMID: 7664747
  7. Differential expression of genes for cyclin-dependent protein kinases in rice plants.
    Plant Physiol. 1999 Jan;119(1):31-40 PMID: 9880343
  8. Geminiviruses: models for plant DNA replication, transcription, and cell cycle regulation.
    Crit Rev Biochem Mol Biol. 2000;35(2):105-40 PMID: 10821479
  9. Two proteins of a plant DNA virus coordinate nuclear and plasmodesmal transport.
    Cell. 1994 Mar 11;76(5):925-32 PMID: 8124726
  10. E2F: a link between the Rb tumor suppressor protein and viral oncoproteins.
    Science. 1992 Oct 16;258(5081):424-9 PMID: 1411535
  11. Retinoblastoma-related proteins in plants: homologues or orthologues of their metazoan counterparts?
    Plant Mol Biol. 2000 Aug;43(5-6):635-42 PMID: 11089866
  12. The multifunctional character of a geminivirus replication protein is reflected by its complex oligomerization properties.
    J Biol Chem. 2000 Mar 3;275(9):6114-22 PMID: 10692401
  13. Negative regulation of DNA replication by the retinoblastoma protein is mediated by its association with MCM7.
    Mol Cell Biol. 1998 May;18(5):2748-57 PMID: 9566894
  14. In vitro cleavage and joining at the viral origin of replication by the replication initiator protein of tomato yellow leaf curl virus.
    Proc Natl Acad Sci U S A. 1995 Apr 25;92(9):3879-83 PMID: 7732000
  15. Clink, a nanovirus-encoded protein, binds both pRB and SKP1.
    J Virol. 2000 Apr;74(7):2967-72 PMID: 10708410
  16. The retinoblastoma protein and cell cycle control.
    Cell. 1995 May 5;81(3):323-30 PMID: 7736585
  17. A DNA polymerase from maize axes: its purification and possible role.
    Plant Mol Biol. 1992 Dec;20(6):1159-68 PMID: 1463849
  18. Transcriptional activation by simian virus 40 large T antigen: interactions with multiple components of the transcription complex.
    Mol Cell Biol. 1993 Feb;13(2):961-9 PMID: 8423815
  19. Regulation of the cyclin E gene by transcription factor E2F1.
    Proc Natl Acad Sci U S A. 1995 Dec 19;92(26):12146-50 PMID: 8618861
  20. Molecular cloning and functional analysis of the adenovirus E1A-associated 300-kD protein (p300) reveals a protein with properties of a transcriptional adaptor.
    Genes Dev. 1994 Apr 15;8(8):869-84 PMID: 7523245
  21. Association of human papillomavirus types 16 and 18 E6 proteins with p53.
    Science. 1990 Apr 6;248(4951):76-9 PMID: 2157286
  22. Spatial pattern of cdc2 expression in relation to meristem activity and cell proliferation during plant development.
    Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7360-4 PMID: 1502145
  23. Plant cells contain a novel member of the retinoblastoma family of growth regulatory proteins.
    EMBO J. 1996 Sep 16;15(18):4900-8 PMID: 8890163
  24. RB kinases and RB-binding proteins: new points of view.
    Trends Biochem Sci. 1997 Jan;22(1):14-7 PMID: 9020586
  25. Adenovirus E1A, simian virus 40 tumor antigen, and human papillomavirus E7 protein share the capacity to disrupt the interaction between transcription factor E2F and the retinoblastoma gene product.
    Proc Natl Acad Sci U S A. 1992 May 15;89(10):4549-53 PMID: 1316611
  26. Conserved sequence and structural motifs contribute to the DNA binding and cleavage activities of a geminivirus replication protein.
    J Biol Chem. 1998 Sep 18;273(38):24448-56 PMID: 9733736
  27. Interaction between a geminivirus replication protein and origin DNA is essential for viral replication.
    J Biol Chem. 1994 Mar 18;269(11):8459-65 PMID: 8132573
  28. Getting it together in plant virus movement: cooperative interactions between bipartite geminivirus movement proteins.
    Trends Cell Biol. 1996 Sep;6(9):353-8 PMID: 15157433
  29. The retinoblastoma protein alters the phosphorylation state of polyomavirus large T antigen in murine cell extracts and inhibits polyomavirus origin DNA replication.
    J Virol. 1999 Apr;73(4):3004-13 PMID: 10074150
  30. Cell cycle regulation of the cyclin A gene promoter is mediated by a variant E2F site.
    Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):11264-8 PMID: 7479977
  31. Two domains of the AL1 protein mediate geminivirus origin recognition.
    Virology. 1997 Dec 8;239(1):186-97 PMID: 9426458
  32. Prediction of functional regions of the maize streak virus replication-associated proteins by protein-protein interaction analysis.
    Plant Mol Biol. 1998 Nov;38(5):699-712 PMID: 9862488
  33. A maize cDNA encoding a member of the retinoblastoma protein family: involvement in endoreduplication.
    Proc Natl Acad Sci U S A. 1996 Aug 20;93(17):8962-7 PMID: 8799136
  34. Activity of the retinoblastoma family proteins, pRB, p107, and p130, during cellular proliferation and differentiation.
    Crit Rev Biochem Mol Biol. 1996 Jun;31(3):237-71 PMID: 8817077
  35. DNA replication and cell cycle in plants: learning from geminiviruses.
    EMBO J. 2000 Mar 1;19(5):792-9 PMID: 10698921
  36. How viral oncogenes make the cell cycle.
    Trends Genet. 1996 Jul;12(7):270-5 PMID: 8763499
  37. cdc2a expression in Arabidopsis is linked with competence for cell division.
    Plant Cell. 1993 Dec;5(12):1711-23 PMID: 8305869
  38. The maize retinoblastoma protein homologue ZmRb-1 is regulated during leaf development and displays conserved interactions with G1/S regulators and plant cyclin D (CycD) proteins.
    Plant Mol Biol. 1998 May;37(1):155-69 PMID: 9620273
  39. Localization of abutilon mosaic virus (AbMV) DNA within leaf tissue by in situ hybridization.
    Virology. 1991 Apr;181(2):580-8 PMID: 2014637
  40. A geminivirus induces expression of a host DNA synthesis protein in terminally differentiated plant cells.
    Plant Cell. 1995 Jun;7(6):705-19 PMID: 7647562
  41. Tobacco retinoblastoma-related protein phosphorylated by a distinct cyclin-dependent kinase complex with Cdc2/cyclin D in vitro.
    Plant J. 1999 May;18(3):243-52 PMID: 10377991
  42. RRB1 and RRB2 encode maize retinoblastoma-related proteins that interact with a plant D-type cyclin and geminivirus replication protein.
    Mol Cell Biol. 1997 Sep;17(9):5077-86 PMID: 9271385
  43. A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif.
    Plant Cell. 1995 Jan;7(1):85-103 PMID: 7696881
  44. Geminivirus replication origins have a modular organization.
    Plant Cell. 1994 Mar;6(3):405-16 PMID: 8180499
  45. Structure of the retinoblastoma tumour-suppressor pocket domain bound to a peptide from HPV E7.
    Nature. 1998 Feb 26;391(6670):859-65 PMID: 9495340
  46. Protein domains connect cell cycle stimulation directly to initiation of DNA replication.
    Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):12125-9 PMID: 7991595
  47. Bean yellow dwarf virus RepA, but not rep, binds to maize retinoblastoma protein, and the virus tolerates mutations in the consensus binding motif.
    Virology. 1999 Apr 10;256(2):270-9 PMID: 10191192
  48. Isolation and characterization of the E2F-like gene in plants.
    FEBS Lett. 1999 Oct 22;460(1):117-22 PMID: 10571072
  49. Homologous sequences in adenovirus E1A and human papillomavirus E7 proteins mediate interaction with the same set of cellular proteins.
    J Virol. 1992 Dec;66(12):6893-902 PMID: 1331501
  50. A conserved family of WD-40 proteins binds to the retinoblastoma protein in both plants and animals.
    Plant Cell. 1997 Sep;9(9):1595-606 PMID: 9338962
  51. Functional domains of a geminivirus replication protein.
    J Biol Chem. 1997 Apr 11;272(15):9840-6 PMID: 9092519
  52. Chromosome condensation induced by geminivirus infection of mature plant cells.
    J Cell Sci. 2000 Apr;113 ( Pt 7):1149-60 PMID: 10704366
  53. Virus-like particles in nuclei of phloem cells in spinach leaves infected with the curly top virus.
    J Ultrastruct Res. 1977 Oct;61(1):78-88 PMID: 915977
  54. A DNA structure is required for geminivirus replication origin function.
    J Virol. 1996 Jan;70(1):148-58 PMID: 8523519
  55. Cell division in plants.
    Curr Opin Cell Biol. 1993 Apr;5(2):226-31 PMID: 8507494
  56. Rep protein of tomato yellow leaf curl geminivirus has an ATPase activity required for viral DNA replication.
    Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5640-4 PMID: 7777563
  57. The retinoblastoma protein: a master regulator of cell cycle, differentiation and apoptosis.
    Eur J Biochem. 1997 Jun 15;246(3):581-601 PMID: 9219514
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2000-07-03
Pages
3485-95
Language
English
Region
England
NLM ID
8208664
PMCID
PMC313951
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]