Peptide aptamers that bind to geminivirus replication proteins confer a resistance phenotype to tomato yellow leaf curl virus and tomato mottle virus infection in tomato

Journal of Virology

Volumn 87, Issue 17, 2013, Pages 9691-9706

  Reyes, Maria Ines ^a   Nash Tara E , T E ^a   Dallas, Mary M ^a   Ascencio Ibáñez, J Trinidad ^a   Hanley Bowdoin, Linda ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APTAMER; HELICASE; VIRUS DNA;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; GEMINIVIRUS; INFECTION RESISTANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SYMPTOM; TOMATO; TOMATO MOTTLE VIRUS; TOMATO YELLOW LEAF CURL VIRUS; VIRAL PLANT DISEASE;

AMINO ACID SEQUENCE; APTAMERS, PEPTIDE; BEGOMOVIRUS; DNA, VIRAL; GEMINIVIRIDAE; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; PHENOTYPE; PLANT DISEASES; PLANTS, GENETICALLY MODIFIED; PROTEIN BINDING; TWO-HYBRID SYSTEM TECHNIQUES; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84883265477     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01095-13     Document Type: Article

References (85)

1. Gutierrez C. 2000. Geminiviruses and the plant cell cycle. Plant Mol. Biol. 43:763-772.
2. Hanley-Bowdoin L, Settlage SB, Orozco BM, Nagar S, Robertson D. 2000. Geminiviruses: models for plant DNA replication, transcription, and cell cycle regulation. Crit. Rev. Biochem. Mol. Biol. 35:105-140.
3. Gutierrez C. 1999. Geminivirus DNA replication. Cell. Mol. Life Sci. 56:313-329.
4. Anderson PK, Cunningham AA, Patel NG, Morales FJ, Epstein PR, Daszak P.2004. Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol. Evol. 19:535-544.
5. Morales FJ, Jones PG. 2004. The ecology and epidemiology of whiteflytransmitted viruses in Latin America. Virus Res. 100:57-65.
6. Moffat A. 1999. Geminiviruses emerge as serious crop threat. Science 286:1835.
7. Rojas Hagen C, Lucas WJ, Gilbertson RL. 2005. Exploiting chinks in the plant's armor: evolution and emergence of geminiviruses. Annu. Rev. Phytopathol. 43:361-394.
8. Shepherd DN, Martin DP, Thomson JA. 2009. Transgenic strategies for developing crops resistant to geminiviruses. Plant Sci. 176:1-11.
9. Vanderschuren H, Stupak M, Futterer J, Gruissem W, Zhang P. 2007. Engineering resistance to geminiviruses-review and perspectives. Plant Biotechnol. J. 5:207-220.
10. Mansoor S, Zafar Y, Briddon RW. 2006. Geminivirus disease complexes: the threat is spreading. Trends Plant Sci. 11:209-212.
11. Duffy S, Holmes EC. 2008. Phylogenetic evidence for rapid rates of molecular evolution in the single-stranded DNA begomovirus Tomato yellow leaf curl virus. J. Virol. 82:957-965.
12. Jeske H, Lutgemeier M, Preiss W. 2001. DNA forms indicate rolling circle and recombination-dependent replication of Abutilon mosaic virus. EMBO J. 20:6158-6167.
13. Briddon RW, Brown JK, Moriones E, Stanley J, Zerbini M, Zhou X, Fauquet CM. 2008. Recommendations for the classification and nomenclature of the DNA-β satellites of begomoviruses. Arch. Virol. 153:763-781.
14. Melgarejo TA, Kon T, Rojas MR, Paz-Carrasco L, Zerbini FM, Gilbertson RL. 2013. Characterization of a New World monopartite begomovirus causing leaf curl disease of tomato in Ecuador and Peru reveals a new direction in geminivirus evolution. J. Virol. 87:5397-5413.
15. Lapidot M, Friedmann M. 2002. Breeding for resistance to whiteflytransmitted geminiviruses. Ann. Appl. Biol. 140:109-127.
16. Morales FJ. 2001. Conventional breeding for resistance to Bemisia tabacitransmitted geminiviruses. Crop Prot. 20:825-834.
17. Briddon RW, Stanley J. 15 March 2009. Geminiviridae. Encyclopedia of life science. John Wiley & Sons, Ltd., Chichester, United Kingdom. http://www.els.net. doi:10.1002/9780470015902.a0000750.pub2.
18. Vu TV, Roy Choudhury N, Mukherjee SK. 2013. Transgenic tomato plants expressing artificial microRNAs for silencing the pre-coat and coat proteins of a begomovirus, Tomato leaf curl New Delhi virus, show tolerance to virus infection. Virus Res. 172:35-45.
19. Saxena S, Singh N, Ranade SA, Babu SG. 2011. Strategy for a generic resistance to geminiviruses infecting tomato and papaya through in silico siRNA search. Virus Genes 43:409-434.
20. Pakniat-Jahromy A, Behjatnia SA, Dry IB, Izadpanah K, Rezaian MA. 2010. A new strategy for generating geminivirus resistant plants using a DNA betasatellite/split barnase construct. J. Virol. Methods 170:57-66.
21. Sera T. 2005. Inhibition of virus DNA replication by artificial zinc finger proteins. J. Virol. 79:2614-2619.
22. Takenaka K, Koshino-Kimura Y, Aoyama Y, Sera T. 2007. Inhibition of tomato yellow leaf curl virus replication by artificial zinc-finger proteins. Nucleic Acids Symp. Ser. (Oxf.) 51:429-430.
23. Edelbaum D, Gorovits R, Sasaki S, Ikegami M, Czosnek H. 2009. Expressing a whitefly GroEL protein in Nicotiana benthamiana plants confers tolerance to tomato yellow leaf curl virus and cucumber mosaic virus, but not to grapevine virus A or tobacco mosaic virus. Arch. Virol. 154:399-407.
24. Elmer JS, Brand L, Sunter G, Gardiner WE, Bisaro DM, Rogers SG. 1988. Genetic analysis of the tomato golden mosaic virus. II. The product of the AL1 coding sequence is required for replication. Nucleic Acids Res. 16:7043-7060.
25. Fontes EP, Eagle PA, Sipe PS, Luckow VA, Hanley-Bowdoin L. 1994. Interaction between a geminivirus replication protein and origin DNA is essential for viral replication. J. Biol. Chem. 269:8459-8465.
26. Laufs J, Traut W, Heyraud F, Matzeit V, Rogers SG, Schell J, Gronenborn B. 1995. 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. 92:3879-3883.
27. Orozco BM, Hanley-Bowdoin L. 1996. A DNA structure is required for geminivirus replication origin function. J. Virol. 70:148-158.
28. Clerot D, Bernardi F. 2006. DNA helicase activity is associated with the replication initiator protein Rep of Tomato yellow leaf curl geminivirus. J. Virol. 80:11322-11330.
29. Desbiez C, David C, Mettouchi A, Laufs J, Gronenborn B. 1995. Rep protein of Tomato yellow leaf curl geminivirus has an ATPase activity required for viralDNAreplication. Proc. Natl. Acad. Sci. U. S. A. 92:5640-5644.
30. Singh DK, Malik PS, Choudhury NR, Mukherjee SK. 2008. MYMIV replication initiator protein (Rep): roles at the initiation and elongation steps of MYMIV DNA replication. Virology 380:75-83.
31. Ascencio-Ibañez JT, Sozzani R, Lee TJ, Chu TM, Wolfinger RD, Cella R, Hanley-Bowdoin L. 2008. Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol. 148:436-454.
32. Nagar S, Pedersen TJ, Carrick KM, Hanley-Bowdoin L, Robertson D. 1995.Ageminivirus induces expression of a hostDNAsynthesis protein in terminally differentiated plant cells. Plant Cell 7:705-719.
33. Lozano-Durán R, Rosas-Díaz T, Luna AP, Bejarano ER. 2011. Identification of host genes involved in geminivirus infection using a reverse genetics approach. PLoS One 6:e22383. doi:10.1371/journal.pone .0022383.
34. Orozco BM, Kong LJ, Batts LA, Elledge S, Hanley-Bowdoin L. 2000. The multifunctional character of a geminivirus replication protein is reflected by its complex oligomerization properties. J. Biol. Chem. 275:6114-6122.
35. Malik PS, Kumar V, Bagewadi B, Mukherjee SK. 2005. Interaction between coat protein and replication initiation protein of Mung bean yellow mosaic India virus might lead to control of viral DNA replication. Virology 337:273-283.
36. Pasumarthy KK, Choudhury NR, Mukherjee SK. 2010. Tomato leaf curl Kerala virus (ToLCKeV) AC3 protein forms a higher order oligomer and enhances ATPase activity of replication initiator protein (Rep/AC1). Virol. J. 7:128. doi:10.1186/1743-422X-7-128.
37. Pasumarthy KK, Mukherjee SK, Choudhury NR. 2011. The presence of tomato leaf curl Kerala virus AC3 protein enhances viral DNA replication and modulates virus induced gene-silencing mechanism in tomato plants. Virol. J. 8:178. doi:10.1186/1743-422X-8-178.
38. Settlage SB, Miller AB, Gruissem W, Hanley-Bowdoin L. 2001. Dual interaction of a geminivirus replication accessory factor with a viral replication protein and a plant cell cycle regulator. Virology 279:570-576.
39. Settlage SB, Miller AB, Hanley-Bowdoin L. 1996. Interactions between geminivirus replication proteins. J. Virol. 70:6790-6795.
40. Settlage SB, See RG, Hanley-Bowdoin L. 2005. Geminivirus C3 protein: replication enhancement and protein interactions. J. Virol. 79:9885-9895.
41. Fondong VN. 25 April 2013. Geminivirus protein structure and function. Mol. Plant Pathol. [Epub ahead of print.] doi:10.1111/mpp.12032.
42. Nash TE, Dallas MB, Reyes MI, Buhrman GK, Ascencio-Ibáñez JT, Hanley-Bowdoin L. 2011. Functional analysis of a novel motif conserved across geminivirus Rep proteins. J. Virol. 85: 1182-1192.
43. Ilyina TV, Koonin EV. 1992. Conserved sequence motifs in the initiator proteins for rolling circle DNA replication encoded by diverse replicons from eubacteria, eucaryotes and archaebacteria. Nucleic Acids Res. 20: 3279-3285.
44. Koonin EV, Ilyina TV. 1992. Geminivirus replication proteins are related to prokaryotic plasmid rolling circle DNA replication initiator proteins. J. Gen. Virol. 73:2763-2766.
45. Argüello-Astorga GR, Ruiz-Medrano R. 2001. An iteron-related domain is associated to Motif 1 in the replication proteins of geminiviruses: identification of potential interacting amino acid-base pairs by a comparative approach. Arch. Virol. 146:1465-1485.
46. Colas P. 2000. Combinatorial protein reagents to manipulate protein function. Curr. Opin. Chem. Biol. 4:54-59.
47. Crawford M, Woodman R, Ko Ferrigno P. 2003. Peptide aptamers: tools for biology and drug discovery. Brief. Funct. Genomic. Proteomic. 2:72-79.
48. Hoppe-Seyler F, Crnkovic-Mertens I, Tomai E, Butz K. 2004. Peptide aptamers: specific inhibitors of protein function. Curr. Mol. Med. 4:529- 538.
49. Lopez-Ochoa L, Ramirez-Prado J, Hanley-Bowdoin L. 2006. Peptide aptamers that bind to a geminivirus replication protein interfere with viral replication in plant cells. J. Virol. 80:5841-5853.
50. Geyer CR, Brent R. 2000. Selection of genetic agents from random peptide aptamer expression libraries. Methods Enzymol. 328:171-208.
51. Rudolph C, Schreier PH, Uhrig JF. 2003. Peptide-mediated broadspectrum plant resistance to tospoviruses. Proc. Natl. Acad. Sci. U. S. A. 100:4429-4434.
52. Butz K, Denk C, Ullmann A, Scheffner M, Hoppe-Seyler F. 2000. Induction of apoptosis in human papillomavirus-positive cancer cells by peptide aptamers targeting the viral E6 oncoprotein. Proc. Natl. Acad. Sci. U. S. A. 97:6693-6697.
53. Butz K, Denk C, Fitscher B, Crnkovic-Mertens I, Ullmann A, Schroder CH, Hoppe-Seyler F. 2001. Peptide aptamers targeting the hepatitis B virus core protein: a new class of molecules with antiviral activity. Oncogene 20:6579-6586.
54. Colas P, Cohen B, Jessen T, Grishina I, McCoy J, Brent R. 1996. Genetic selection of peptide aptamers that recognize and inhibit cyclin-dependent kinase 2. Nature 380:548-550.
55. Golemis EA, Brent R. 1992. Fused protein domains inhibit DNA binding by LexA. Mol. Cell. Biol. 12:3006-3014.
56. Lanahan MB, Yen H-C, Giovannoni JJ, Klee HJ. 1994. The never ripe mutation blocks ethylene perception in tomato. Plant Cell 6:521-530.
57. Clontech. 2001. Yeast protocols handbook. PT3024-1. Clontech, Mountain View, CA.
58. Cortina C, Culiáñez-Maciá FA. 2004. Tomato transformation and transgenic plant production. Plant Cell Tissue Organ Culture 76:269-275.
59. Egelkrout EM, Robertson D, Hanley-Bowdoin L. 2001. Proliferating cell nuclear antigen transcription is repressed through an E2F consensus element and activated by geminivirus infection in mature leaves. Plant Cell 13:1437-1452.
60. Ascencio-Ibáñez 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.
61. Lopez-Ochoa L, Nash TE, Ramirez-Prado J, Hanley-Bowdoin L. 2009. Isolation of peptide aptamers to target protein function. Methods Mol. Biol. 535:333-360.
62. Lu Z, Murray KS, Van Cleave V, LaVallie ER, Stahl ML, McCoy JM. 1995. Expression of thioredoxin random peptide libraries on the Escherichia coli cell surface as functional fusions to flagellin: a system designed for exploring protein-protein interactions. Biotechnology 13:366-372.
63. Legg JP, Fauquet CM. 2004. Cassava mosaic geminiviruses in Africa. Plant Mol. Biol. 56:585-599.
64. Shepherd DN, Martin DP, Van Der Walt E, Dent K, Varsani A, Rybicki EP. 2010. Maize streak virus: an old and complex 'emerging' pathogen. Mol. Plant Pathol. 11:1-12.
65. Amrao L, Amin I, Shahid MS, Briddon RW, Mansoor S. 2010. Cotton leaf curl disease in resistant cotton is associated with a single begomovirus that lacks an intact transcriptional activator protein. Virus Res. 152:153-163.
66. Mandal B, Langston DB, Pappu HR, Beard GH, Kucharek TA, Flanders JT, Whiddon JP, Smith JE, Kelley WT. 2001. First report of Cabbage leaf curl virus (family Geminiviridae) in Georgia. Plant Dis. 85:561.
67. Polston JE. 1993. Host range of Tomato mottle virus, a new geminivirus infecting tomato in Florida. Plant Dis. 77:1181-1184.
68. Polston JE, Bois D, Keinath AP, Chellemi DO. 1995. Occurrence of Tomato mottle geminivirus in South Carolina, Tennessee and Virginia. Plant Dis. 79:539.
69. Strausbaugh CA, Wintermantel WM, Gillen AM, Eujayl IA. 2008. Curly top survey in the western United States. Phytopathology 98:1212-1217.
70. Czosnek H. 2007. Tomato yellow leaf curl disease: management, molecular biology, breeding for resistance, vol 1. Springer, Dordrecht, The Netherlands.
71. Salati R, Nahkla MK, Rojas MR, Guzman P, Jaquez J, Maxwell DP, Gilbertson RL. 2002. Tomato yellow leaf curl virus in the Dominican Republic: characterization of an infectious clone, virus monitoring in whiteflies, and identification of reservoir hosts. Phytopathology 92:487-496.
72. Hanssen IM, Lapidot M, Thomma BP. 2010. Emerging viral diseases of tomato crops. Mol. Plant Microbe Interact. 23:539-548.
73. Díaz-Pendón JA, Cañizares MC, Moriones E, Bejarano ER, Czosnek H, Navas-Castillo J. 2010. Tomato yellow leaf curl viruses: ménage á trois between the virus complex, the plant and the whitefly vector. Mol. Plant Pathol. 11:441-450.
74. Benfey PN, Chua NH. 1990. The Cauliflower mosaic virus 35S promoter: combinatorial regulation of transcription in plants. Science 250:959-966.
75. Varma A, Malathi VG. 2003. Emerging geminivirus problems: a serious threat to crop production. Ann. Appl. Biol. 142:145-164.
76. Real E, Rain JC, Battaglia V, Jallet C, Perrin P, Tordo N, Chrisment P, D'Alayer J, Legrain P, Jacob Y. 2004. Antiviral drug discovery strategy using combinatorial libraries of structurally constrained peptides. J. Virol. 78:7410-7417.
77. Sun L, Ren H, Liu R, Li B, Wu T, Sun F, Liu H, Wang X, Dong H. 2010. An H-type thioredoxin functions in tobacco defense responses to two species of viruses and an abiotic oxidative stress. Mol. Plant Microbe Interact. 23:1470-1485.
78. Gutzat R, Borghi L, Gruissem W. 2012. Emerging roles of retinoblastoma- related proteins in evolution and plant development. Trends Plant Sci. 17:139-148.
79. Kong LJ, Orozco BM, Roe JL, Nagar S, Ou S, Feiler HS, Durfee T, Miller AB, Gruissem W, Robertson D, Hanley-Bowdoin L. 2000. A geminivirus replication protein interacts with the retinoblastoma protein through a novel domain to determine symptoms and tissue specificity of infection in plants. EMBO J. 19:3485-3495.
80. Argüello-Astorga G, Lopez-Ochoa L, Kong LJ, Orozco BM, Settlage SB, Hanley-Bowdoin L. 2004. A novel motif in geminivirus replication proteins interacts with the plant retinoblastoma-related protein. J. Virol. 78: 4817-4826.
81. Sánchez-Durán MA, Dallas MB, Ascencio-Ibanez JT, Reyes MI, Arroyo-Mateos M, Ruiz-Albert J, Hanley-Bowdoin L, Bejarano ER. 2011. Interaction between geminivirus replication protein and the SUMOconjugating enzyme is required for viral infection. J. Virol. 85:9789-9800.
82. Amin I, Patil BL, Briddon RW, Mansoor S, Fauquet CM. 2011. Comparison of phenotypes produced in response to transient expression of genes encoded by four distinct begomoviruses in Nicotiana benthamiana and their correlation with the levels of developmental miRNAs. Virol. J. 8:238. doi:10.1186/1743-422X-8-238.
83. Saha P, Dasgupta I, Das S. 2006. A novel approach for developing resistance in rice against phloem limited viruses by antagonizing the phloem feeding hemipteran vectors. Plant Mol. Biol. 62:735-752.
84. Singer SD, Hily JM, Cox KD. 2011. The sucrose synthase-1 promoter from Citrus sinensis directs expression of the β-glucuronidase reporter gene in phloem tissue and in response to wounding in transgenic plants. Planta 234:623-637.
85. Orozco BM, Hanley-Bowdoin L. 1998. Conserved sequence and structural motifs contribute to the DNA binding and cleavage activities of a geminivirus replication protein. J. Biol. Chem. 273:24448-24456.