Specific requirement for translation initiation factor 4E or its isoform drives plant host susceptibility to Tobacco etch virus

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Estevan, Joan ^a   Maréna, Aramata ^a   Callot, Caroline ^a   Lacombe, Séverine ^a   Moretti, André ^a   Caranta, Carole ^a   Gallois, Jean Luc ^a  

^a CEMAGREF   (France)

Author keywords

Arabidopsis thaliana; Capsicum annuum; eIF4E; Potyvirus; Translation initiation factor

Indexed keywords

VEGETABLE PROTEIN;

ALLELE; ARABIDOPSIS; ARTICLE; GENETICS; METABOLISM; PATHOGENICITY; PLANT VIRUS; TOBACCO; VIROLOGY;

ALLELES; ARABIDOPSIS; PLANT PROTEINS; PLANT VIRUSES; TOBACCO;

EID: 84899143956     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-14-67     Document Type: Article

References (41)

1. Hernandez G, Altmann M, Lasko P. Origins and evolution of the mechanisms regulating translation initiation in eukaryotes. Trends Biochem Sci 2010, 35(2):63-73. 10.1016/j.tibs.2009.10.009, 19926289.
2. Patrick RM, Browning KS. The eIF4F and eIFiso4F Complexes of Plants: An Evolutionary Perspective. Comp Funct Genomics 2012, 2012:287814. 3352336, 22611336.
3. Robaglia C, Caranta C. Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 2006, 11(1):40-45. 10.1016/j.tplants.2005.11.004, 16343979.
4. Wang A, Krishnaswamy S. Eukaryotic translation initiation factor 4E-mediated recessive resistance to plant viruses and its utility in crop improvement. Mol Plant Pathol 2012, 13(7):795-803. 10.1111/j.1364-3703.2012.00791.x, 22379950.
5. Ruffel S, Dussault MH, Palloix A, Moury B, Bendahmane A, Robaglia C, Caranta C. A natural recessive resistance gene against Potato virus Y in pepper corresponds to the eukaryotic initiation factor 4E (eIF4E). Plant J 2002, 32(6):1067-1075. 10.1046/j.1365-313X.2002.01499.x, 12492847.
6. Duprat A, Caranta C, Revers F, Menand B, Browning KS, Robaglia C. The Arabidopsis eukaryotic initiation factor (iso)4E is dispensable for plant growth but required for susceptibility to potyviruses. Plant J 2002, 32(6):927-934. 10.1046/j.1365-313X.2002.01481.x, 12492835.
7. Lellis A, Kasschau K, Whitham S, Carrington J. Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during potyvirus infection. Curr Biol 2002, 12:1046-1051. 10.1016/S0960-9822(02)00898-9, 12123581.
8. Gao Z, Johansen E, Eyers S, Thomas C, Ellis T, Maule A. The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell-to-cell trafficking. Plant J 2004, 40:376-385. 10.1111/j.1365-313X.2004.02215.x, 15469495.
9. Nicaise V, German-Retana S, Sanjuan R, Dubrana MP, Mazier M, Maisonneuve B, Candresse T, Caranta C, Le Gall O. The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the potyvirus Lettuce mosaic virus. Plant Physiol 2003, 132(3):1272-1282. 10.1104/pp.102.017855, 167067, 12857809.
10. Wang X, Kohalmi SE, Svircev A, Wang A, Sanfacon H, Tian L. Silencing of the host factor eIF(iso)4E gene confers plum pox virus resistance in plum. PLoS One 2013, 8(1):e50627. 10.1371/journal.pone.0050627, 3557289, 23382802.
11. Ruffel S, Gallois JL, Moury B, Robaglia C, Palloix A, Caranta C. Simultaneous mutations in translation initiation factors eIF4E and eIF(iso)4E are required to prevent Pepper veinal mottle virus infection of pepper. J Gen Virol 2006, 87(Pt 7):2089-2098.
12. Hwang J, Li J, Liu WY, An SJ, Cho H, Her NH, Yeam I, Kim D, Kang BC. Double mutations in eIF4E and eIFiso4E confer recessive resistance to Chilli veinal mottle virus in pepper. Mol Cells 2009, 27(3):329-336. 10.1007/s10059-009-0042-y, 19326080.
13. Sato M, Nakahara K, Yoshii M, Ishikawa M, Uyeda I. Selective involvement of members of the eukaryotic initiation factor 4E family in the infection of Arabidopsis thaliana by potyviruses. FEBS Lett 2005, 579(5):1167-1171. 10.1016/j.febslet.2004.12.086, 15710407.
14. Nicaise V, Gallois JL, Chafiai F, Allen LM, Schurdi-Levraud V, Browning KS, Candresse T, Caranta C, Le Gall O, German-Retana S. Coordinated and selective recruitment of eIF4E and eIF4G factors for potyvirus infection in Arabidopsis thaliana. FEBS Lett 2007, 581(5):1041-1046. 10.1016/j.febslet.2007.02.007, 17316629.
15. Decroocq V, Sicard O, Alamillo JM, Lansac M, Eyquard JP, Garcia JA, Candresse T, Le Gall O, Revers F. Multiple resistance traits control Plum pox virus infection in Arabidopsis thaliana. Mol Plant Microbe Interact 2006, 19(5):541-549. 10.1094/MPMI-19-0541, 16673941.
16. Bruun-Rasmussen M, Moller IS, Tulinius G, Hansen JK, Lund OS, Johansen IE. The same allele of translation initiation factor 4E mediates resistance against two Potyvirus spp. in Pisum sativum. Mol Plant Microbe Interact 2007, 20(9):1075-1082. 10.1094/MPMI-20-9-1075, 17849710.
17. Charron C, Nicolai M, Gallois JL, Robaglia C, Moury B, Palloix A, Caranta C. Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. Plant J 2008, 54(1):56-68. 10.1111/j.1365-313X.2008.03407.x, 18182024.
18. Ruffel S, Gallois JL, Lesage ML, Caranta C. The recessive potyvirus resistance gene pot-1 is the tomato orthologue of the pepper pvr2-eIF4E gene. Mol Genet Genomics 2005, 274(4):346-353. 10.1007/s00438-005-0003-x, 15971038.
19. Jiang J, Laliberte JF. The genome-linked protein VPg of plant viruses-a protein with many partners. Curr Opin Virol 2011, 1(5):347-354. 10.1016/j.coviro.2011.09.010, 22440836.
20. Gallois JL, Charron C, Sanchez F, Pagny G, Houvenaghel MC, Moretti A, Ponz F, Revers F, Caranta C, German-Retana S. Single amino acid changes in the turnip mosaic virus viral genome-linked protein (VPg) confer virulence towards Arabidopsis thaliana mutants knocked out for eukaryotic initiation factors eIF(iso)4E and eIF(iso)4G. J Gen Virol 2010, 91(Pt 1):288-293.
21. Ashby JA, Stevenson CE, Jarvis GE, Lawson DM, Maule AJ. Structure-based mutational analysis of eIF4E in relation to sbm1 resistance to pea seed-borne mosaic virus in pea. PLoS One 2011, 6(1):e15873. 10.1371/journal.pone.0015873, 3025909, 21283665.
22. Roudet-Tavert G, Michon T, Walter J, Delaunay T, Redondo E, Le Gall O. Central domain of a potyvirus VPg is involved in the interaction with the host translation initiation factor eIF4E and the viral protein HcPro. J Gen Virol 2007, 88(Pt 3):1029-1033.
23. Monzingo AF, Dhaliwal S, Dutt-Chaudhuri A, Lyon A, Sadow JH, Hoffman DW, Robertus JD, Browning KS. The structure of eukaryotic translation initiation factor-4E from wheat reveals a novel disulfide bond. Plant Physiol 2007, 143(4):1504-1518. 10.1104/pp.106.093146, 1851841, 17322339.
24. Miyoshi H, Suehiro N, Tomoo K, Muto S, Takahashi T, Tsukamoto T, Ohmori T, Natsuaki T. Binding analyses for the interaction between plant virus genome-linked protein (VPg) and plant translational initiation factors. Biochimie 2006, 88(3-4):329-340.
25. Okade H, Fujita Y, Miyamoto S, Tomoo K, Muto S, Miyoshi H, Natsuaki T, Rhoads RE, Ishida T. Turnip mosaic virus genome-linked protein VPg binds C-terminal region of cap-bound initiation factor 4E orthologue without exhibiting host cellular specificity. J Biochem 2009, 145(3):299-307. 10.1093/jb/mvn180, 19122207.
26. Contreras-Paredes CA, Silva-Rosales L, Daros JA, Alejandri-Ramirez ND, Dinkova TD. The absence of eukaryotic initiation factor eIF(iso)4E affects the systemic spread of a Tobacco etch virus isolate in Arabidopsis thaliana. Mol Plant Microbe Interact 2013, 26(4):461-470. 10.1094/MPMI-09-12-0225-R, 23252462.
27. Mahajan SK, Chisholm ST, Whitham SA, Carrington JC. Identification and characterization of a locus (RTM1) that restricts long-distance movement of tobacco etch virus in Arabidopsis thaliana. Plant J 1998, 14(2):177-186. 10.1046/j.1365-313X.1998.00105.x, 9628015.
28. Chisholm ST, Mahajan SK, Whitham SA, Yamamoto ML, Carrington JC. Cloning of the Arabidopsis RTM1 gene, which controls restriction of long-distance movement of tobacco etch virus. Proc Natl Acad Sci U S A 2000, 97(1):489-494. 10.1073/pnas.97.1.489, 26690, 10618445.
29. Maule AJ, Caranta C, Boulton MI. Sources of natural resistance to plant viruses: status and prospects. Mol Plant Pathol 2007, 8(2):223-231. 10.1111/j.1364-3703.2007.00386.x, 20507494.
30. Fraser RSS. The genetics of resistance to plant-viruses. Annu Rev Phytopathol 1990, 28:179-200.
31. Bedhomme S, Lafforgue G, Elena SF. Multihost experimental evolution of a plant RNA virus reveals local adaptation and host-specific mutations. Mol Biol Evol 2012, 29(5):1481-1492. 10.1093/molbev/msr314, 22319146.
32. Jenner CE, Nellist CF, Barker GC, Walsh JA. Turnip mosaic virus (TuMV) is able to use alleles of both eIF4E and eIF(iso)4E from multiple loci of the diploid Brassica rapa. Mol Plant Microbe Interact 2010, 23(11):1498-1505. 10.1094/MPMI-05-10-0104, 20672877.
33. Nellist CF, Qian W, Jenner CE, Moore JD, Zhang S, Wang X, Briggs WH, Barker GC, Sun R, Walsh JA. Multiple copies of eukaryotic translation initiation factors in Brassica rapa facilitate redundancy, enabling diversification through variation in splicing and broad-spectrum virus resistance. Plant J 2013, 77(2):261-268.
34. Nieto C, Rodriguez-Moreno L, Rodriguez-Hernandez AM, Aranda MA, Truniger V. Nicotiana benthamiana resistance to non-adapted Melon necrotic spot virus results from an incompatible interaction between virus RNA and translation initiation factor 4E. Plant J 2011, 66(3):492-501. 10.1111/j.1365-313X.2011.04507.x, 21255163.
35. Ibiza VP, Canizares J, Nuez F. EcoTILLING in Capsicum species: searching for new virus resistances. BMC Genomics 2010, 11:631. 10.1186/1471-2164-11-631, 3091766, 21073716.
36. Jeong H-J, Kwon J-K, Pandeya D, Hwang J, Hoang N, Bae J-H, Kang B-C. A survey of natural and ethyl methane sulfonate-induced variations of eIF4E using high-resolution melting analysis in Capsicum. Mol Breeding 2012, 29(2):349-360.
37. Perez-de-Castro AM, Vilanova S, Canizares J, Pascual L, Blanca JM, Diez MJ, Prohens J, Pico B. Application of genomic tools in plant breeding. Curr Genomics 2012, 13(3):179-195. 10.2174/138920212800543084, 3382273, 23115520.
38. Tanksley SD, McCouch SR. Seed banks and molecular maps: unlocking genetic potential from the wild. Science 1997, 277(5329):1063-1066. 10.1126/science.277.5329.1063, 9262467.
39. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 2008, 36:W465-469. 10.1093/nar/gkn180, 2447785, 18424797.
40. Curtis MD, Grossniklaus U. A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 2003, 133(2):462-469. 10.1104/pp.103.027979, 523872, 14555774.
41. Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 1998, 16(6):735-743. 10.1046/j.1365-313x.1998.00343.x, 10069079.