Structure-based mutational analysis of eIF4E in relation to sbm1 resistance to Pea seed-borne mosaic virus in Pea

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Ashby, Jamie A ^b   Stevenson, Clare E M ^a   Jarvis, Gavin E ^c   Lawson, David M ^a   Maule, Andrew J ^a  

^a NORWICH RESEARCH PARK   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATE; INITIATION FACTOR 4E;

ALLELE; ARTICLE; CRYSTALLOGRAPHY; GENE EXPRESSION; GENETIC COMPLEMENTATION; GENETIC CONSERVATION; GENETIC POLYMORPHISM; GENETIC RESISTANCE; MOSAIC VIRUS; MUTATIONAL ANALYSIS; NONHUMAN; ORTHOLOGY; PEA; PHENOTYPE; PLANT DISEASE; PLANT TISSUE; POINT MUTATION; POTYVIRUS; PROTEIN BINDING; PROTEIN STRUCTURE; SPECIES DIFFERENCE; VIROGENESIS; VIRUS INHIBITION; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; NUCLEOTIDE SEQUENCE; PLANT IMMUNITY; PLANT SEED; PROTEIN TERTIARY STRUCTURE; STRUCTURAL HOMOLOGY; VIROLOGY; X RAY CRYSTALLOGRAPHY;

EUKARYOTA; PEA SEED-BORNE MOSAIC VIRUS; PISUM SATIVUM; POTYVIRUS;

CRYSTALLOGRAPHY, X-RAY; DNA MUTATIONAL ANALYSIS; EUKARYOTIC INITIATION FACTOR-4E; IMMUNITY, INNATE; MODELS, MOLECULAR; MOSAIC VIRUSES; PEAS; PLANT DISEASES; PLANT IMMUNITY; POINT MUTATION; POTYVIRUS; PROTEIN STRUCTURE, TERTIARY; SEEDS; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 79551524986     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015873     Document Type: Article

References (68)

1. Ling KS, Harris KR, Meyer JD, Levi A, Guner N, et al. (2009) Nonsynonymous single nucleotide polymorphisms in the watermelon eIF4E gene are closely associated with resistance to zucchini yellow mosaic virus. Theor Appl Genet 120: 191-200.
2. Truniger V, Aranda MA (2009) Recessive resistance to plant viruses. Adv Virus Res 75: 119-159.
3. Hwang J, Li J, Liu WY, An SJ, Cho H, et al. (2009) Double mutations in eIF4E and eIFiso4E confer recessive resistance to Chilli veinal mottle virus in pepper. Mol Cells 27: 329-336.
4. Bruun-Rasmussen M, Moller IS, Tulinius G, Hansen JK, Lund OS, et al. (2007) The same allele of translation initiation factor 4E mediates resistance against two Potyvirus spp. in Pisum sativum. Mol Plant Microbe Interact 20: 1075-1082.
5. Keller KE, Johansen IE, Martin RR, Hampton RO (1998) Potyvirus genomelinked protein (VPg) determines pea seed-borne mosaic virus pathotype-specific virulence in Pisum sativum. Mol Plant Microbe Interact 11: 124-130.
6. Johansen IE, Lund OS, Hjulsager CK, Laursen J (2001) Recessive resistance in Pisum sativum and potyvirus pathotype resolved in a gene-for-cistron correspondence between host and virus. Journal of Virology 75: 6609-6614.
7. 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.
8. 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.
9. Yeam I, Cavatorta JR, Ripoll DR, Kang BC, Jahn MM (2007) Functional dissection of naturally occurring amino acid substitutions in eIF4E that confers recessive potyvirus resistance in plants. Plant Cell 19: 2913-2928.
10. 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.
11. German-Retana S, Walter J, Doublet B, Roudet-Tavert G, Nicaise V, et al. (2008) Mutational analysis of plant cap-binding protein eIF4E reveals key amino acids involved in biochemical functions and potyvirus infection. J Virol 82: 7601-7612.
12. Kang BC, Yeam I, Frantz JD, Murphy JF, Jahn MM (2005) The pvr1 locus in Capsicum encodes a translation initiation factor eIF4E that interacts with Tobacco etch virus VPg. Plant J 42: 392-405.
13. Ruffel S, Dussault MH, Palloix A, Moury B, Bendahmane A, et al. (2002) A natural recessive resistance gene against potato virus Y in pepper corresponds to the eukaryotic initiation factor 4E (eIF4E). Plant J 32: 1067-1075.
14. 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.
15. 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.). Plant J 42: 912-922.
16. Naderpour M, Lund OS, Larsen R, Johansen E (2010) Potyviral resistance derived from cultivars of Phaseolus vulgaris carrying bc-3 is associated with the homozygotic presence of a mutated eIF4E allele. Mol Plant Pathol 11: 255-263.
17. Grzela R, Strokovska L, Andrieu JP, Dublet B, Zagorski W, et al. (2006) Potyvirus terminal protein VPg, effector of host eukaryotic initiation factor eIF4E. Biochimie 88: 887-896.
18. 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.
19. Michon T, Estevez Y, Walter J, German-Retana S, Le Gall O (2006) The potyviral virus genome-linked protein VPg forms a ternary complex with the eukaryotic initiation factors eIF4E and eIF4G and reduces eIF4E affinity for a mRNA cap analogue. FEBS J 273: 1312-1322.
20. 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.
21. Abdul-Razzak A, Guiraud T, Peypelut M, Walter J, Houvenaghel MC, et al. (2009) Involvement of the cylindrical inclusion (CI) protein in the overcoming of an eIF4E-mediated resistance against Lettuce mosaic potyvirus. Mol Plant Pathol 10: 109-113.
22. Nakahara KS, Shimada R, Choi SH, Yamamoto H, Shao J, et al. (2010) Involvement of the P1 Cistron in Overcoming eIF4E-Mediated Recessive Resistance Against Clover yellow vein virus in Pea. Molecular Plant-Microbe Interactions 23: 1460-1469.
23. Brown CJ, McNae I, Fischer PM, Walkinshaw MD (2007) Crystallographic and mass spectrometric characterisation of eIF4E with N7-alkylated cap derivatives. J Mol Biol 372: 7-15.
24. Brown CJ, Verma CS, Walkinshaw MD, Lane DP (2009) Crystallization of eIF4E complexed with eIF4GI peptide and glycerol reveals distinct structural differences around the cap-binding site. Cell Cycle 8: 1905-1911.
25. Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK (1997) Cocrystal structure of the messenger RNA 59 cap-binding protein (eIF4E) bound to 7- methyl-GDP. Cell 89: 951-961.
26. Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK (1999) Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G. Mol Cell 3: 707-716.
27. Niedzwiecka A, Marcotrigiano J, Stepinski J, Jankowska-Anyszka M, Wyslouch-Cieszynska A, et al. (2002) Biophysical studies of eIF4E cap-binding protein: recognition of mRNA 59 cap structure and synthetic fragments of eIF4G and 4EBP1 proteins. J Mol Biol 319: 615-635.
28. Tomoo K, Matsushita Y, Fujisaki H, Abiko F, Shen X, et al. (2005) Structural basis for mRNA Cap-Binding regulation of eukaryotic initiation factor 4E by 4Ebinding protein, studied by spectroscopic, X-ray crystal structural, and molecular dynamics simulation methods. Biochim Biophys Acta 1753: 191-208.
29. Liu W, Zhao R, McFarland C, Kieft J, Niedzwiecka A, et al. (2009) Structural insights into parasite eIF4E binding specificity for m7G and m2,2,7G mRNA caps. J Biol Chem 284: 31336-31349.
30. Monzingo AF, Dhaliwal S, Dutt-Chaudhuri A, Lyon A, Sadow JH, et al. (2007) The structure of eukaryotic translation initiation factor-4E from wheat reveals a novel disulfide bond. Plant Physiol 143: 1504-1518.
31. Robaglia C, Caranta C (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11: 40-45.
32. Khan MA, Miyoshi H, Ray S, Natsuaki T, Suehiro N, et al. (2006) Interaction of genome-linked protein (VPg) of turnip mosaic virus with wheat germ translation initiation factors eIFiso4E and eIFiso4F. J Biol Chem 281: 28002-28010.
33. Miyoshi H, Suehiro N, Tomoo K, Muto S, Takahashi T, et al. (2006) Binding analyses for the interaction between plant virus genome-linked protein (VPg) and plant translational initiation factors. Biochimie 88: 329-340.
34. Okade H, Fujita Y, Miyamoto S, Tomoo K, Muto S, et al. (2009) 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 145: 299-307.
35. Khan MA, Miyoshi H, Gallie DR, Goss DJ (2008) Potyvirus genome-linked protein, VPg, directly affects wheat germ in vitro translation: interactions with translation initiation factors eIF4F and eIFiso4F. J Biol Chem 283: 1340-1349.
36. Gallie DR (2001) Cap-independent translation conferred by the 59 leader of tobacco etch virus is eukaryotic initiation factor 4G dependent. J Virol 75: 12141-12152.
37. Khan MA, Yumak H, Goss DJ (2009) Kinetic mechanism for the binding of eIF4F and tobacco Etch virus internal ribosome entry site rna: effects of eIF4B and poly(A)-binding protein. J Biol Chem 284: 35461-35470.
38. Carrington JC, Freed DD (1990) Cap-independent enhancement of translation by a plant potyvirus 59 nontranslated region. J Virol 64: 1590-1597.
39. Levis C, Astier-Manifacier S (1993) The 59 untranslated region of PVY RNA, even located in an internal position, enables initiation of translation. Virus Genes 7: 367-379.
40. Ashby JA, Stevenson CE, Maule AJ, Lawson DM (2009) Crystallization and preliminary X-ray analysis of eukaryotic initiation factor 4E from Pisum sativum. Acta Crystallogr Sect F Struct Biol Cryst Commun 65: 836-838.
41. Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK (1997) X-ray studies of the messenger RNA 59 cap-binding protein (eIF4E) bound to 7-methyl-GDP. Nucleic Acids Symp Ser. pp 8-11.
42. Prilusky J, Felder CE, Zeev-Ben-Mordehai T, Rydberg EH, Man O, et al. (2005) FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics 21: 3435-3438.
43. Holm L, Kaariainen S, Rosenstrom P, Schenkel A (2008) Searching protein structure databases with DaliLite v.3. Bioinformatics 24: 2780-2781.
44. Bracha-Drori K, Shichrur K, Katz A, Oliva M, Angelovici R, et al. (2004) Detection of protein-protein interactions in plants using bimolecular fluorescence complementation. Plant J 40: 419-427.
45. Walter M, Chaban C, Schutze K, Batistic O, Weckermann K, et al. (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40: 428-438.
46. Phan J, Zdanov A, Evdokimov AG, Tropea JE, Peters HK, 3rd, et al. (2002) Structural basis for the substrate specificity of tobacco etch virus protease. J Biol Chem 277: 50564-50572.
47. Hughes JMX, Ptushkina M, Karim MM, Koloteva N, von der Haar T, et al. (1999) Translational repression by human 4E-BP1 in yeast specifically requires human eIF4E as target. Journal of Biological Chemistry 274: 3261-3264.
48. Truniger V, Nieto C, Gonzalez-Ibeas D, Aranda M (2008) Mechanism of plant eIF4E-mediated resistance against a Carmovirus (Tombusviridae): cap-independent translation of a viral RNA controlled in cis by an (a)virulence determinant. Plant J 56: 716-727.
49. Hebrard E, Bessin Y, Michon T, Longhi S, Uversky VN, et al. (2009) Intrinsic disorder in Viral Proteins Genome-Linked: experimental and predictive analyses. Virol J 6: 23.
50. Rantalainen KI, Uversky VN, Permi P, Kalkkinen N, Dunker AK, et al. (2008) Potato virus A genome-linked protein VPg is an intrinsically disordered molten globule-like protein with a hydrophobic core. Virology 377: 280-288.
51. 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.
52. Hirsch S, Kim J, Munoz A, Heckmann AB, Downie JA, et al. (2009) GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21: 545-557.
53. Bailey S (1994) The Ccp4 Suite - Programs for Protein Crystallography. Acta Crystallographica Section D-Biological Crystallography 50: 760-763.
54. Stein N (2008) CHAINSAW: a program for mutating pdb files used as templates in molecular replacement. Journal of Applied Crystallography 41: 641-643.
55. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, et al. (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Research 31: 3497-3500.
56. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and clustal X version 2.0. Bioinformatics 23: 2947-2948.
57. Navaza J (1994) Amore - an Automated Package for Molecular Replacement. Acta Crystallographica Section A 50: 157-163.
58. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallographica Section D-Biological Crystallography 60: 2126-2132.
59. Krissinel E, Henrick K (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallographica Section D-Biological Crystallography 60: 2256-2268.
60. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallographica Section D-Biological Crystallography 53: 240-255.
61. Read RJ (1986) Improved Fourier Coefficients for Maps Using Phases from Partial Structures with Errors. Acta Crystallographica Section A 42: 140-149.
62. Glaser F, Pupko T, Paz I, Bell RE, Bechor-Shental D, et al. (2003) ConSurf: Identification of Functional Regions in Proteins by Surface-Mapping of Phylogenetic Information. Bioinformatics 19: 163-164.
63. Landau M, Mayrose I, Rosenberg Y, Glaser F, Martz E, et al. (2005) ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Research 33: W299-W302.
64. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402.
65. Voinnet O, Rivas S, Mestre P, Baulcombe D (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33: 949-956.
66. Witte CP, Noel LD, Gielbert J, Parker JE, Romeis T (2004) Rapid one-step protein purification from plant material using the eight-amino acid StrepII epitope. Plant Mol Biol 55: 135-147.
67. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, et al. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Research 35: W375-W383.
68. Howlin B, Butler SA, Moss DS, Harris GW, Driessen HPC (1993) Tlsanl - Tls Parameter-Analysis Program for Segmented Anisotropic Refinement of Macromolecular Structures. Journal of Applied Crystallography 26: 622-624.