Skip to main content
Log in

C4 protein of Beet severe curly top virus is a pathomorphogenetic factor in Arabidopsis

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

The Curtovirus C4 protein is required for symptom development during infection of Arabidopsis. Transgenic Arabidopsis plants expressing C4 from either Beet curly top virus or Beet severe curly top virus produced phenotypes that were similar to symptoms seen during infection with wild-type viruses. The pseudosymptoms caused by C4 protein alone were novel to transgenic Arabidopsis and included bumpy trichomes, severe enations, disorientation of vascular bundles and stomata, swelling, callus-like structure formation, and twisted siliques. C4 induced abnormal cell division and altered cell fate in a variety of tissues depending on the C4 expression level. C4 protein expression increased the expression levels of cell-cycle-related genes CYCs, CDKs and PCNA, and suppressed ICK1 and the retinoblastoma-related gene RBR1, resulting in activation of host cell division. These results suggest that the Curtovirus C4 proteins are involved actively in host cell-cycle regulation to recruit host factors for virus replication and symptom development.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ascencio-Ibanez JT, Settlage SB (2007) DNA abrasion onto plants is an effective method for geminivirus infection and virus-induced gene silencing. J Virol Methods 142:198–203

    Article  CAS  PubMed  Google Scholar 

  • Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (1987) Current protocols in molecular biology. Wiley, New York

    Google Scholar 

  • Bechtold N, Pelletier G (1998) In planta agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol Biol 82:259–266

    Google Scholar 

  • Bishopa GJ, Konczb C (2002) Brassinosteroids and plant steroid hormone signaling. Plant Cell 14:S97–S110

    Google Scholar 

  • Briddon RW, Watts J, Markham PG, Stanley J (1989) The coat protein of beet curly top virus is essential for infectivity. Virology 172:628

    Article  CAS  PubMed  Google Scholar 

  • Cano-Delgado A, Yin Y, Yu C, Vafeados D, Mora-Garcia S, Cheng JC, Nam KH, Li J, Chory J (2004) BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131:5341–5351

    Article  CAS  PubMed  Google Scholar 

  • Castillo AG, Collinet D, Deret S, Kashoggi A, Bejarano ER (2003) Dual interaction of plant PCNA with geminivirus replication accessory protein (Ren) and viral replication protein (Rep). Virology 312:381–394

    Article  CAS  PubMed  Google Scholar 

  • Collin S, Fernandez-Lobato M, Gooding PS, Mullineaux PM, Fenoll C (1996) The two nonstructural proteins from wheat dwarf virus involved in viral gene expression and replication are retinoblastoma-binding proteins. Virology 219:324–329

    Article  CAS  PubMed  Google Scholar 

  • Davis KR, Ausubel FM (1989) Characterization of elicitor-induced defense responses in suspension-cultured cells of Arabidopsis. Mol Plant Microbe Interact 2:363–368

    Google Scholar 

  • Duan YP, Powell CA, Purcifull DE, Broglio P, Hiebert E (1997) Phenotypic variation in transgenic tobacco expressing mutated geminivirus movement/pathogenicity (BC1) proteins. Mol Plant Microbe Interact 10:1065–1074

    Article  CAS  PubMed  Google Scholar 

  • Dykstra MJ (1993) A manual of applied techniques for biological electron microscopy. Kluwer Academic Publishers

  • Esau K, Hoefert LL (1978) Hyperplastic phloem in sugarbeet leaves infected with the beet curly top virus. Am J Bot 65:772–783

    Article  Google Scholar 

  • Fauquet CM, Stanley J (2005) Revising the way we conceive and name viruses below the species level: a review of geminivirus taxonomy calls for new standardized isolate descriptors. Arch Virol 150:2151–2179

    Article  CAS  PubMed  Google Scholar 

  • Frischmuth S, Frischmuth T, Latham JR, Stanley J (1993) Transcriptional analysis of the virion-sense genes of the geminivirus beet curly top virus. Virology 197:312

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez C (2000) Geminiviruses and the plant cell cycle. Plant Mol Biol 43:763–772

    Article  CAS  PubMed  Google Scholar 

  • Hanley-Bowdoin L, Settlage SB, Orozco BM, Nagar S, Robertson D (1999) Geminiviruses: models for plant DNA replication, transcription, and cell cycle regulation. Crit Rev Plant Sci 18:71–106

    Article  CAS  Google Scholar 

  • Hormuzdi SG, Bisaro DM (1993) Genetic analysis of beet curly top virus: evidence for three virion sense genes involved in movement and regulation of single- and double-stranded DNA levels. Virology(New York, NY) 193:900–909

    CAS  Google Scholar 

  • Hormuzdi SG, Bisaro DM (1995) Genetic analysis of beet curly top virus: examination of the roles of L2 and L3 genes in viral pathogenesis. Virology 206:1044–1054

    Article  CAS  PubMed  Google Scholar 

  • Hunter T (1991) Cooperation between oncogenes. Cell 64:249–270

    Article  CAS  PubMed  Google Scholar 

  • Jeske H (2009) Geminiviruses. Curr Top Microbiol Immunol 331:185

    Article  CAS  PubMed  Google Scholar 

  • Junghans H, Metzlaff M (1990) A simple and rapid method for the preparation of total plant DNA. Biotechniques 8:176

    CAS  PubMed  Google Scholar 

  • Kelman Z, Hurwitz J (1998) Protein PCNA interactions: a DNA-scanning mechanism? Trends Biochem Sci 23:236–238

    Article  CAS  PubMed  Google Scholar 

  • Koncz C, Schell J (1986) The promoter of T L-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet MGG 204:383–396

    Article  CAS  Google Scholar 

  • Lai J, Chen H, Teng K, Zhao Q, Zhang Z, Li Y, Liang L, Xia R, Wu Y, Guo H (2009) RKP, a RING finger E3 ligase induced by BSCTV C4 protein, affects geminivirus infection by regulation of the plant cell cycle. Plant J 57:905–917

    Article  CAS  PubMed  Google Scholar 

  • Larebeke N, Engler G, Holsters M, den Elsacker SV, Zaenen I, Schilperoort RA, Schell J (1974) Large plasmid in Agrobacterium tumefaciens essential for crown gall-inducing ability. Nature 252:169–170

    Google Scholar 

  • Latham JR, Saunders K, Pinner MS, Stanley J (1997) Induction of plant cell division by beet curly top virus gene C4. Plant J 11:1273–1283

    Article  CAS  Google Scholar 

  • Lazarowitz SG (1992) Geminiviruses: genome structure and gene function. Crit Rev Plant Sci 11:327–349

    CAS  Google Scholar 

  • Lee S, Stenger DC, Bisaro DM, Davis KR (1994) Identification of loci in Arabidopsis that confer resistance to geminivirus infection. Plant J 6:525–535

    Article  CAS  PubMed  Google Scholar 

  • Mills-Lujan K, Deom C (2010) Geminivirus C4 protein alters Arabidopsis development. Protoplasma 239:95–110

    Article  CAS  PubMed  Google Scholar 

  • Nagar S, Pedersen TJ, Carrick KM, Hanley-Bowdoin L, Robertson D (1995) A geminivirus induces expression of a host DNA synthesis protein in terminally differentiated plant cells. Plant Cell Online 7:705–719

    Article  CAS  Google Scholar 

  • Park J, Hwang H, Shim H, Im K, Auh CK, Lee S, Davis KR (2004) Altered cell shapes, hyperplasia, and secondary growth in Arabidopsis caused by beet curly top geminivirus infection. Mol Cells 17:117–124

    CAS  PubMed  Google Scholar 

  • Pascal E, Goodlove PE, Wu LC, Lazarowitz SG (1993) Transgenic tobacco plants expressing the geminivirus BL1 protein exhibit symptoms of viral disease. Plant Cell Online 5:795–807

    Article  CAS  Google Scholar 

  • Piroux N, Saunders K, Page A, Stanley J (2007) Geminivirus pathogenicity protein C4 interacts with Arabidopsis thaliana shaggy-related protein kinase AtSKη, a component of the brassinosteroid signalling pathway. Virology 362:428–440

    Article  CAS  PubMed  Google Scholar 

  • Pooma W, Petty IT (1996) Tomato golden mosaic virus open reading frame AL4 is genetically distinct from its C4 analogue in monopartite geminiviruses. J Gen Virol 77:1947–1951

    Article  CAS  PubMed  Google Scholar 

  • Rigden JE, Krake LR, Rezaian MA, Dry IB (1994) ORF C4 of tomato leaf curl geminivirus is a determinant of symptom severity. Virology 204:847–850

    Article  CAS  PubMed  Google Scholar 

  • Rybicki EP (1994) A phylogenetic and evolutionary justification for three genera of Geminiviridae. Arch Virol 139:49–77

    Article  CAS  PubMed  Google Scholar 

  • Stanley J (1991) The molecular determinants of geminivirus pathogenesis. Semin Virol 2(2):139–149

    Google Scholar 

  • Stanley J, Latham JR, Pinner MS, Bedford I, Markham PG (1992) Mutational analysis of the monopartite geminivirus beet curly top virus. Virology (USA)

  • Stenger DC (1998) Replication specificity elements of the worland strain of beet curly top virus are compatible with those of the CFH strain but not those of the Cal/Logan strain. Phytopathology 88:1174–1178

    Article  CAS  PubMed  Google Scholar 

  • Stenger DC, Carbonaro D, Duffus JE (1990) Genomic characterization of phenotypic variants of beet curly top virus. J Gen Virol 71:2211–2215

    Article  CAS  PubMed  Google Scholar 

  • Stenger DC, Stevenson MC, Hormuzdi SG, Bisaro DM (1992) A number of subgenomic DNAs are produced following agroinoculation of plants with beet curly top virus. J Gen Virol 73:237–242

    Article  CAS  PubMed  Google Scholar 

  • Teng K, Chen H, Lai J, Zhang Z, Fang Y, Xia R, Zhou X, Guo H, Xie Q (2010) Involvement of C4 protein of beet severe curly top virus (Family Geminiviridae) in virus movement

  • Vert G, Chory J (2006) Downstream nuclear events in brassinosteroid signalling. Nature 441:96–100

    Google Scholar 

  • Wang X, Chory J (2006) Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 313:1118–1122

    Google Scholar 

  • Weinberg RA (1995) The retinoblastoma protein and cell cycle control. Cell 81:323–330

    Article  CAS  PubMed  Google Scholar 

  • Weinberg RA (1997) The cat and mouse games that genes, viruses, and cells play. Cell 88:573–576

    Article  CAS  PubMed  Google Scholar 

  • Xie Q, Sanz-Burgos AP, Hannon GJ, Gutierrez C (1996) Plant cells contain a novel member of the retinoblastoma family of growth regulatory proteins. EMBO J 15:4900

    CAS  PubMed  Google Scholar 

  • Yan Z, Zhao J, Peng P, Chihara R, Li J (2009) BIN2 functions redundantly with other Arabidopsis GSK3-like kinases to regulate brassinosteroid signaling. Plant Physiol 150:710–721

    Google Scholar 

  • Yeom CH, Lee G, Park JH, Yu J, Park S, Yi SY, Lee HR, Hong YS, Yang J, Lee S (2009) High dose concentration administration of ascorbic acid inhibits tumor growth in BALB/C mice implanted with sarcoma 180 cancer cells via the restriction of angiogenesis. J Transl Med 7:70

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the BioGreen 21 program (No.20070401034028) of Rural Development Administration, Republic of Korea.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Sukchan Lee or Keith R. Davis.

Additional information

Communicated by J. R. Liu.

J. Park and H. S. Hwang contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

299_2010_923_MOESM1_ESM.jpg

Supplementary Fig. 1 Induction of cell cycle related genes expression by BSCTV infection of Arabidopsis. The time-course expression of genes in different organs after BSCTV infection was analyzed by quantitative real-time RT-PCR. The organs of infection origins and inflorescence stems were chosen from virus accumulation data (Fig. 1C). (A) cdc2a, (B) cdc2b, (C) cyc1b, (D) cyc2b, (E) myb and (F) pcna1 (JPEG 125 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Park, J., Hwang, HS., Buckley, K.J. et al. C4 protein of Beet severe curly top virus is a pathomorphogenetic factor in Arabidopsis . Plant Cell Rep 29, 1377–1389 (2010). https://doi.org/10.1007/s00299-010-0923-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-010-0923-8

Keywords

Navigation