Silencing of the Host Factor eIF(iso)4E Gene Confers Plum Pox Virus Resistance in Plum

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Wang, Xinhua ^a,b   Kohalmi, Susanne E ^a   Svircev, Antonet ^b   Wang, Aiming ^b   Sanfaçon, Hélène ^c   Tian, Lining ^a,b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^c SUMMERLAND RESEARCH AND DEVELOPMENT CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 4E; SHORT HAIRPIN RNA; VIRUS RNA;

ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOWN REGULATION; EUKARYOTIC TRANSLATION INITIATION FACTOR 4E GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSFORMATION; MOLECULAR CLONING; MOLECULAR INTERACTION; MOSAIC VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PLUM; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RHIZOBIUM; SEQUENCE ANALYSIS; TRANSGENIC PLANT; VIRUS RESISTANCE; VIRUS STRAIN;

EUKARYOTIC INITIATION FACTOR-4E; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; PLANT DISEASES; PLANTS, GENETICALLY MODIFIED; PLUM POX VIRUS; PRUNUS;

EID: 84873861617     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050627     Document Type: Article

References (74)

1. Németh MV (1986) Plum Pox (Sharka). In: Németh MV, editor. Virus, Mycoplasma and Rickettsia Disases. Boston: Martinus Nijhoff Publishers. pp. 463-479.
2. Lopez-Moya JJ, Fernandez-Fernandez MR, Cambra M, Garcia JA, (2000) Biotechnological aspects of plum pox virus. J Biotechnol 76: 121-136.
3. Kegler H, Fuchs E, Gruntzig M, Schwartz S, (1998) Some results of 50 years' research on resistance to plum pox potyvirus. Arch Phytopathol Pflanzenschutz 31: 479-506.
4. Atanassov D, (1932) Plum pox. A new virus disease. Ann Univ Sofia Fac Agric Silvic 11: 49-69.
5. Németh M, (1994) History and importance of plum pox in stone-fruit production. EPPO Bull 24: 525-536.
6. Laín S, Riechmann JL, Méndez E, García JA, (1988) Nucleotide sequence of the 3 terminal region of plum pox potyvirus RNA. Virus Research 10: 325-342.
7. Riechmann JL, Laín S, García JA, (1989) The genome-linked protein and 5 end RNA sequence of plum pox potyvirus. J Gen Virol 70: 2785-2789.
8. Glasa M, Palkovics L, Komínek P, Labonne G, Pittnerová S, et al. (2004) Geographically and temporally distant natural recombinant isolates of Plum pox virus (PPV) are genetically very similar and form a unique PPV subgroup. J Gen Virol 85: 2671-2681.
9. James D, Varga A, (2005) Nucleotide sequence analysis of Plum pox virus isolate W3174: evidence of a new strain. Virus Research 110: 143-150.
10. Serçe ÇU, Candresse T, Svanella-Dumas L, Krizbai L, Gazel M, et al. (2009) Further characterization of a new recombinant group of Plum pox virus isolates, PPV-T, found in orchards in the Ankara province of Turkey. Virus Research 142: 121-126.
11. Cambra M, Capote N, Myrta A, Llácer G, (2006) Plum pox virus and the estimated costs associated with sharka disease. EPPO Bulletin 36: 202-204.
12. Thakur PD, Bhardwaj SV, Garg ID, Sharma DR, Khosla K, (1994) Plum pox virus on stone fruits from India- a new record. Plant Disease Research 9: 100-102.
13. Navratil M, Safarova D, Karesova R, Petrzik K, (2005) First Incidence of Plum Pox Virus on Apricot Trees in China. Plant Dis 89: 338-338.
14. Maejima K, Hoshi H, Hashimoto M, Himeno M, Kawanishi T, et al. (2010) First report of plum pox virus infecting Japanese apricot (Prunus mume Sieb. et Zucc.) in Japan. J Gen Plant Pathol 76: 229-231.
15. Levy L, Damsteegt V, Welliver R, (2000) First Report of Plum pox virus (Sharka Disease) in Prunus persica in the United States. Plant Disease 84: 202-202.
16. Thompson D, McCann M, MacLeod M, Lye D, Green M, et al. (2001) First Report of Plum Pox Potyvirus in Ontario, Canada. Plant Disease 85: 97-97.
17. Tian L, Svircev A, Helene S, Brown DC, Schneider KE, et al. (2010) Development of Plum Pox Virus Resistance in Plum via Expression of an Intron-Spliced Hairpin HC-Pro Transgene. Nageswara-Rao M,Soneji JR (Eds) Focus on Tree and Forest Genetics Genes, Genomes and Genomics 4 (Special Issue 1). pp. 28-31.
18. Wang A, Tian L, Huang T-S, Brown DCW, Svircev AM, et al. (2009) Development of genetic resistance to Plum pox virus in transgenic Nicotiana benthamiana and Prunus domestica. Acta Horticulturae 839: 665-672.
19. Hily JM, Ravelonandro M, Damsteegt V, Bassett C, Petri C, et al. (2007) Plum pox virus coat protein gene intron-hairpin-RNA (ihpRNA) constructs provide resistance to plum pox virus in Nicotiana benthamiana and Prunus domestica. Journal of the American Society for Horticultural Science 132: 850-858.
20. Zhang SC, Tian L, Svircev A, Brown DCW, Sibbald S, et al. (2006) Engineering resistance to Plum pox virus (PPV) through the expression of PPV-specific hairpin RNAs in transgenic plants. Can J Plant Pathol 28: 263-270.
21. Nicola-Negri E, Brunetti A, Tavazza M, Ilardi V, (2005) Hairpin RNA-Mediated Silencing of Plum pox virus P1 and HC-Pro Genes for Efficient and Predictable Resistance to the Virus. Transgenic Research 14: 989-994.
22. Ravelonandro M, Scorza R, Bachelier JC, Labonne G, Levy L, et al. (1997) Resistance of transgenic Prunus domestica to plum pox virus infection. Plant Disease 81: 1231-1235.
23. Scorza R, Callahan A, Levy L, Damsteegt V, Webb K, et al. (2001) Post-transcriptional gene silencing in plum pox virus resistant transgenic European plum containing the plum pox potyvirus coat protein gene. Transgenic Research 10: 201-209.
24. Hily JM, Scorza R, Malinowski T, Zawadzka B, Ravelonandro M, (2004) Stability of gene silencing-based resistance to Plum pox virus in transgenic plum (Prunus domestica L.) under field conditions. Transgenic Research 13: 427-436.
25. Mayo M, Jolly C, (1991) The 5′-terminal sequence of Potato leafroll virus RNA: evidence of recombination between virus and host RNA. J Gen Virol 72: 2591.
26. Farinelli L, Malnoë P, Collet GF, (1992) Heterologous Encapsidation of Potato Virus Y Strain O (PVYO) With The Transgenic Coat Protein of PVY Strain N (PVYN) in Solanum Tuberosum Cv. Bintje. Nat Biotech 10: 1020-1025.
27. Candelier-Harvey P, Hull R, (1993) Cucumber mosaic virus genome is encapsidated in alfalfa mosaic virus coat protein expressed in transgenic tobacco plants. Transgenic Research 2: 277-285.
28. Lecoq H, Ravelonandro M, Wipf-Scheibel C, Monsion M, Raccah B, et al. (1993) Aphid transmission of a non-aphid-transmissible strain of Zucchini yellow mosaic potyvirus from transgenic plants expressing the capsid protein of Plum pox potyvirus. Mol Plant-Microbe Interact 6: 403.
29. Lellis A, Kasschau K, Whitham S, Carrington J, (2002) Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during potyvirus infection. Curr Biol 12: 1046-1051.
30. Kang BC, Yeam I, Frantz JD, Murphy JF, Jahn MM, (2005) The pvr1 locus in Capsicum encodes a translation initiation factor elF4E that interacts with Tobacco etch virus VPg. Plant Journal 42: 392-405.
31. Duprat A, Caranta C, Revers F, Menand B, Browning K, et al. (2002) The Arabidopsis eukaryotic initiation factor (iso)4E is dispensable for plant growth but required for susceptibility to potyviruses. Plant J 32: 927-934.
32. Nicaise V, German-Retana S, Sanjuan R, Dubrana MP, Mazier M, et al. (2003) The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the Potyvirus Lettuce mosaic virus. Plant Physiol 132: 1272-1282.
33. Sato M, Nakahara K, Yoshii M, Ishikawa M, Uyeda I, (2005) Selective involvement of members of the eukaryotic initiation factor 4E family in the infection of Arabidopsis thaliana by potyviruses. FEBS Lett 579: 1167-1171.
34. Nicaise V, Gallois JL, Chafiai F, Allen LM, Schurdi-Levraud V, et al. (2007) Coordinated and selective recruitment of eIF4E and eIF4G factors for potyvirus infection in Arabidopsis thaliana. FEBS Lett 581: 1041-1046.
35. Truniger V, Aranda MA, Gad L, John PC, (2009) Recessive Resistance to Plant Viruses. Advances in virus research 75: 119-159, 231.
36. Sonenberg N, Gingras A-C, (1998) The mRNA 5′ cap-binding protein eIF4E and control of cell growth. Current Opinion in Cell Biology 10: 268-275.
37. Gingras A-C, Raught B, Sonenberg N, (1999) eIF4 INITIATION FACTORS: Effectors of mRNA Recruitment to Ribosomes and Regulators of Translation. Annual Review of Biochemistry 68: 913-963.
38. Browning KS, (2004) Plant translation initiation factors: it is not easy to be green. Biochem Soc Trans 32: 589-591.
39. Robaglia C, Caranta C, (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11: 40-45.
40. Wittmann S, Chatel H, Fortin MG, Laliberté JF, (1997) Interaction of the viral protein genome linked of turnip mosaic potyvirus with the translational eukaryotic initiation factor (iso) 4E of Arabidopsis thaliana using the yeast two-hybrid system. Virology 234: 84-92.
41. Leonard S, Plante D, Wittmann S, Daigneault N, Fortin MG, et al. (2000) Complex formation between potyvirus VPg and translation eukaryotic initiation factor 4E correlates with virus infectivity. J Virol 74: 7730-7737.
42. Ruffel S, Gallois JL, Lesage ML, Caranta C, (2005) The recessive potyvirus resistance gene pot-1 is the tomato orthologue of the pepper pvr2-eIF4E gene. Mol Genet Genomics 274: 346-353.
43. Yoshii M, Nishikiori M, Tomita K, Yoshioka N, Kozuka R, et al. (2004) The Arabidopsis Cucumovirus Multiplication 1 and 2 Loci Encode Translation Initiation Factors 4E and 4G. Journal of Virology 78: 6102-6111.
44. Stein N, Perovic D, Kumlehn J, Pellio B, Stracke S, et al. (2005) The eukaryotic translation initiation factor 4E confers multiallelic recessive Bymovirus resistance in Hordeum vulgare (L.). The Plant Journal 42: 912-922.
45. Nieto C, Morales M, Orjeda G, Clepet C, Monfort A, et al. (2006) An eIF4E allele confers resistance to an uncapped and non-polyadenylated RNA virus in melon. The Plant Journal 48: 452-462.
46. Decroocq V, Sicard O, Alamillo JM, Lansac M, Eyquard JP, et al. (2006) Multiple resistance traits control Plum pox virus infection in Arabidopsis thaliana. Molecular Plant-Microbe Interactions 19: 541-549.
47. Marandel G, Salava J, Abbott A, Candresse T, Decroocq V, (2009) Quantitative trait loci meta-analysis of Plum pox virus resistance in apricot (Prunus armeniaca L.): new insights on the organization and the identification of genomic resistance factors. Mol Plant Pathol 10: 347-360.
48. El-Sharkawy I, Kim WS, El-Kereamy A, Jayasankar S, Svircev AM, et al. (2007) Isolation and characterization of four ethylene signal transduction elements in plums (Prunus salicina L.). J Exp Bot 58: 3631-3643.
49. Combe JP, Petracek ME, van Eldik G, Meulewaeter F, Twell D, (2005) Translation initiation factors eIF4E and eIFiso4E are required for polysome formation and regulate plant growth in tobacco. Plant Mol Biol 57: 749-760.
50. Hamilton A, Voinnet O, Chappell L, Baulcombe D, (2002) Two classes of short interfering RNA in RNA silencing. EMBO J 21: 4671-4679.
51. Kim WS, Stobbs LW, Lehman SM, James D, Suircev AM, (2008) Direct real-time PCR detection of plum pox virus in field surveys in Ontario. Can J Plant Pathol 30: 308-317.
52. Scheper GC, van Kollenburg B, Hu J, Luo Y, Goss DJ, et al. (2002) Phosphorylation of Eukaryotic Initiation Factor 4E Markedly Reduces Its Affinity for Capped mRNA. Journal of Biological Chemistry 277: 3303-3309.
53. Browning KS, Lax SR, Ravel JM, (1987) Identification of two messenger RNA cap binding proteins in wheat germ. Evidence that the 28-kDa subunit of eIF-4B and the 26-kDa subunit of eIF-4F are antigenically distinct polypeptides. J Biol Chem 262: 11228-11232.
54. Browning KS, (1996) The plant translational apparatus. Plant Molecular Biology 32: 107-144.
55. Gallie DR, Browning KS, (2001) eIF4G Functionally Differs from eIFiso4G in Promoting Internal Initiation, Cap-independent Translation, and Translation of Structured mRNAs. Journal of Biological Chemistry 276: 36951-36960.
56. Rodriguez CM, Freire MA, Camilleri C, Robaglia C, (1998) The Arabidopsis thaliana cDNAs coding for eIF4E and eIF(iso)4E are not functionally equivalent for yeast complementation and are differentially expressed during plant development. Plant J 13: 465-473.
57. Gao Z, Johansen E, Eyers S, Thomas CL, Noel Ellis TH, et al. (2004) The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell-to-cell trafficking. Plant J 40: 376-385.
58. Albar L, Bangratz-Reyser M, Hébrard E, Ndjiondjop M-N, Jones M, et al. (2006) Mutations in the eIF(iso)4G translation initiation factor confer high resistance of rice to Rice yellow mottle virus. The Plant Journal 47: 417-426.
59. Ruffel S, Gallois JL, Moury B, Robaglia C, Palloix A, et al. (2006) Simultaneous mutations in translation initiation factors elF4E and elF(iso)4E are required to prevent pepper veinal mottle virus infection of pepper. Journal of General Virology 87: 2089-2098.
60. Keller KE, Johansen E, Martin RR, Hampton RO, (1998) Potyvirus Genome-Linked Protein (VPg) Determines Pea Seed-Borne Mosaic Virus Pathotype-Specific Virulence in Pisum sativum. Molecular Plant-Microbe Interactions 11: 124-130.
61. Goodfellow I, Chaudhry Y, Gioldasi I, Gerondopoulos A, Natoni A, et al. (2005) Calicivirus translation initiation requires an interaction between VPg and eIF4E. EMBO Rep 6: 968-972.
62. Charron C, Nicolai M, Gallois JL, Robaglia C, Moury B, et al. (2008) Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. Plant J 54: 56-68.
63. Beauchemin C, Boutet N, Laliberte J-F, (2007) Visualization of the Interaction between the Precursors of VPg, the Viral Protein Linked to the Genome of Turnip Mosaic Virus, and the Translation Eukaryotic Initiation Factor iso 4E In Planta. Journal of Virology 81: 775-782.
64. Rodríguez-Hernández AM, Gosalvez B, Sempere RN, Burgos L, Aranda MA, et al. (2012) Melon RNA interference (RNAi) lines silenced for Cm-eIF4E show broad virus resistance. Molecular Plant Pathology.
65. Mazier M, Flamain F, Nicolaï M, Sarnette V, Caranta C, (2011) Knock-Down of Both eIF4E1 and eIF4E2 Genes Confers Broad-Spectrum Resistance against Potyviruses in Tomato. PLoS One 6: e29595.
66. Smith NA, Singh SP, Wang M-B, Stoutjesdijk PA, Green AG, et al. (2000) Gene expression: Total silencing by intron-spliced hairpin RNAs. Nature 407: 319-320.
67. Wesley SV, Christopher AH, Neil AS, MingBo W, Dean TR, et al. (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. The Plant Journal 27: 581-590.
68. Hartley JL, Temple GF, Brasch MA, (2000) DNA Cloning Using In Vitro Site-Specific Recombination. Genome Research 10: 1788-1795.
69. Hood EE, Gelvin SB, Melchers LS, Hoekema A, (1993) New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Research 2: 208-218.
70. Tian L, Canli FA, Wang X, Sibbald S, (2009) Genetic transformation of Prunus domestica L. using the hpt gene coding for hygromycin resistance as the selectable marker. Scientia Horticulturae 119: 339-343.
71. Huang T-S, Wei T, Laliberté J-F, Wang A, (2010) A Host RNA Helicase-Like Protein, AtRH8, Interacts with the Potyviral Genome-Linked Protein, VPg, Associates with the Virus Accumulation Complex, and Is Essential for Infection. Plant Physiology 152: 255-266.
72. Lu Q, Tang X, Tian G, Wang F, Liu K, et al. (2009) Arabidopsis homolog of the yeast TREX-2 mRNA export complex: components and anchoring nucleoporin. Plant J 61: 259-270.
73. Sparkes IA, Runions J, Kearns A, Hawes C, (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protocols 1: 2019-2025.
74. Henikoff S, Henikoff JG, (1992) Amino acid substitution matrices from protein blocks. Proc Natl Acad Sci U S A 89: 10915-10919.