Skip to main content

The Diversification of eIF4E Family Members in Plants and Their Role in the Plant-Virus Interaction

  • Chapter
  • First Online:
Book cover Evolution of the Protein Synthesis Machinery and Its Regulation

Abstract

Recruitment of eukaryotic mRNAs by the translation machinery requires binding of their 5′ end (cap) to eIF4E in complex with the bridge protein eIF4G (eIF4F). Plant eIF(iso)4E and eIF(iso)4G form the eIF(iso)4F complex, distinct from eIF4F (formed by eIF4E and eIF4G). Separate eIF(iso)4E and eIF4E clades are detected upon seed plants’ arrival in evolution, while eIF(iso)4G has been present since green algae. Strong preference is observed between eIF(iso)4G and eIF(iso)4E, as well as between eIF4E and eIF4G in vitro and in vivo, suggesting that these complexes exert functionally distinct roles in seed plants. However, the regulatory mechanisms underlying their role in translation or other cellular processes remain mainly unknown, with the notable exception of plant-virus interaction. Individual isoforms are required in a specific way for successful virus infection in a range of plant species. The isolation of resistance-associated mutations in eIF4E family members pinpointed their role through direct interaction with the viral genome-linked protein VPg. In this chapter we review recent research on eIF4E diversification with emphasis on their cellular function and roles in the specificity of plant-virus interaction.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Browning KS, Bailey-Serres J. Mechanism of Cytoplasmic mRNA Translation. In: The Arabidopsis book. doi:10.1199/tab.0176; 2015.

    Google Scholar 

  2. Joshi B, Lee K, Maeder DL, Jagus R. Phylogenetic analysis of eIF4E-family members. BMC Evol Biol. 2005;5:48.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Mayberry LK, Allen ML, Dennis MD, Browning KS. Evidence for variation in the optimal translation initiation complex: plant eIF4B, eIF4F, and eIF(iso)4F differentially promote translation of mRNAs. Plant Physiol. 2009;150:1844–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Kaye NM, Emmett KJ, Merrick WC, Jankowsky E. Intrinsic RNA binding by the eukaryotic initiation factor 4F depends on a minimal RNA length but not on the m7G cap. J Biol Chem. 2009;284:17742–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Rhoads RE. eIF4E: new family members, new binding partners, new roles. J Biol Chem. 2009;284:16711–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Hernández G, Vazquez-Pianzola P. Functional diversity of the eukaryotic translation initiation factors belonging to eIF4 families. Mech Dev. 2005;122:865–76.

    Article  CAS  PubMed  Google Scholar 

  7. Amiri A, Keiper BD, Kawasaki I, Fan Y, Kohara Y, Rhoads RE, Strome S. An isoform of eIF4E is a component of germ granules and is required for spermatogenesis in C. elegans. Development. 2001;128:3899–912.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Ptushkina M, Malys N, McCarthy JE. eIF4E isoform 2 in Schizosaccharomyces pombe is a novel stress-response factor. EMBO Rep. 2004;5:311–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Dinkova TD, Keiper BD, Korneeva NL, Aamodt EJ, Rhoads RE. Translation of a small subset of Caenorhabditis elegans mRNAs is dependent on a specific eukaryotic translation initiation factor 4E isoform. Mol Cell Biol. 2005;25:100–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Cho PF, Poulin F, Cho-Park YA, Cho-Park IB, Chicoine JD, Lasko P, Sonenberg N. A new paradigm for translational control: inhibition via mRNA tethering by Bicoid and the eIF4E cognate 4EHP. Cell. 2005;121:411–23.

    Article  CAS  PubMed  Google Scholar 

  11. Syntichaki P, Troulinaki K, Tavernarakis N. eIF4E function in somatic cells modulates ageing in Caenorhabditis elegans. Nature. 2007;445:922–6.

    Article  CAS  PubMed  Google Scholar 

  12. Hernández G, Proud CG, Preiss T, Parsyan A. On the diversification of the translation apparatus across eukaryotes. Comp Funct Genomics. 2012;2012:256848.

    PubMed  PubMed Central  Google Scholar 

  13. Sanfaçon H. Plant translation factors and virus resistance. Viruses. 2015;7:3392–419.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Patrick RM, Browning KS. The eIF4F and eIFiso4F complexes of plants: an evolutionary perspective. Comp Funct Genomics. 2012;2012:287814.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Rhoads RE, Dinkova TD, Jagus R. Approaches for analyzing the differential activities and functions of eIF4E family members. Methods Enzymol. 2007;429:261–97.

    Article  CAS  PubMed  Google Scholar 

  16. Browning KS. Plant translation initiation factors: it is not easy to be green. Biochem Soc Trans. 2004;32:589–91.

    Article  CAS  PubMed  Google Scholar 

  17. Carberry SE, Goss DJ. Wheat germ initiation factors 4F and (iso)4F interact differently with oligoribonucleotide analogues of rabbit α-globin mRNA. Biochemistry. 1991;30:4542–5.

    Article  CAS  PubMed  Google Scholar 

  18. Gallie DR, Browning KS. eIF4G functionally differs from eIFiso4G in promoting internal initiation, cap-independent translation, and translation of structured mRNAs. J Biol Chem. 2001;276:36951–60.

    Article  CAS  PubMed  Google Scholar 

  19. Dinkova TD. Sanchez de Jimenez E. Differential expression and regulation of translation initiation factors -4E and -iso4E during maize germination. Physiol Plant. 1999;107:419–25.

    Article  CAS  Google Scholar 

  20. Bush MS, Hutchins AP, Jones AM, Naldrett MJ, Jarmolowski A, Lloyd CW, Doonan JH. Selective recruitment of proteins to 5’ cap complexes during the growth cycle in Arabidopsis. Plant J. 2009;59:400–12.

    Article  CAS  PubMed  Google Scholar 

  21. Ruud KA, Kuhlow C, Goss DJ, Browning KS. Identification and characterization of a novel cap-binding protein from Arabidopsis thaliana. J Biol Chem. 1998;273:10325–30.

    Article  CAS  PubMed  Google Scholar 

  22. Morita M, Ler LW, Fabian MR, Siddiqui N, Mullin M, Henderson VC, Alain T, Fonseca BD, Karashchuk G, Bennett CF, Kabuta T, Higashi S, Larsson O, Topisirovic I, Smith RJ, Gingras AC, Sonenberg N. A novel 4EHP-GIGYF2 translational repressor complex is essential for mammalian development. Mol Cell Biol. 2012;32:3585–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Patrick RM, Mayberry LK, Choy G, Woodard LE, Liu JS, White A, Mullen RA, Tanavin TM, Latz CA, Browning KS. Two Arabidopsis loci encode novel eukaryotic initiation factor 4E isoforms that are functionally distinct from the conserved plant eukaryotic initiation factor 4E. Plant Physiol. 2014;164:1820–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. 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;32:927–34.

    Article  CAS  PubMed  Google Scholar 

  25. Combe JP, Petracek ME, van Eldik G, Meulewaeter F, Twell D. Translation initiation factors eIF4E and eIFiso4E are required for polysome formation and regulate plant growth in tobacco. Plant Mol Biol. 2005;57:749–60.

    Article  CAS  PubMed  Google Scholar 

  26. Mayberry LK, Allen ML, Nitka KR, Campbell L, Murphy PA. Browning KS Plant cap-binding complexes eukaryotic initiation factors eIF4F and eIFiso4F: molecular specificity of subunit binding. J Biol Chem. 2011;286:42566–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Robaglia C, Caranta C. Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci. 2006;11:40–5.

    Article  CAS  PubMed  Google Scholar 

  28. Lellis AD, Allen ML, Aertker AW, Tran JK, Hillis DM, Harbin CR, Caldwell C, Gallie DR, Browning KS. Deletion of the eIFiso4G subunit of the Arabidopsis eIFiso4F translation initiation complex impairs health and viability. Plant Mol Biol. 2010;74:249–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Gallie DR. Cap-independent translation conferred by the 5’ leader of tobacco etch virus is eukaryotic initiation factor 4G dependent. J Virol. 2001;75:12141–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Gallie DR. Eukaryotic initiation factor eIFiso4G1 and eIFiso4G2 are isoforms exhibiting distinct functional differences in supporting translation in Arabidopsis. J Biol Chem. 2016;291:1501–13.

    Article  CAS  PubMed  Google Scholar 

  31. Yoshii M, Nishikiori M, Tomita K, Yoshioka N, Kozuka R, Naito S, Ishikawa M. The Arabidopsis cucumovirus multiplication 1 and 2 loci encode translation initiation factors 4E and 4G. J Virol. 2004;78:6102–11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. 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;581:1041–6.

    Article  CAS  PubMed  Google Scholar 

  33. Lee JH, Muhsin M, Atienza GA, Kwak DY, Kim SM, De Leon TB, Angeles ER, Coloquio E, Kondoh H, Satoh K, Cabunagan RC, Cabauatan PQ, Kikuchi S, Leung H, Choi IR. Single nucleotide polymorphisms in a gene for translation initiation factor (eIF4G) of rice (Oryza sativa) associated with resistance to Rice tungro spherical virus. Mol Plant Microbe Interact. 2010;23:29–38.

    Article  CAS  PubMed  Google Scholar 

  34. Martinez-Silva AV, Aguirre-Martinez C, Flores-Tinoco CE, Alejandri-Ramirez ND, Dinkova TD. Translation initiation factor AteIF(iso)4E is involved in selective mRNA translation in Arabidopsis thaliana seedlings. PLoS ONE. 2012;7:e31606.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Jackson RJ, Hellen CU, Pestova TV. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev. 2010;10:113–27.

    Article  CAS  Google Scholar 

  36. Sonenberg N, Hinnebusch AG. New modes of translational control in development, behavior, and disease. Mol Cell. 2007;28:721–9.

    Article  CAS  PubMed  Google Scholar 

  37. Stebbins-Boaz B, Cao Q, de Moor CH, Mendez R, Richter JD. Maskin is a CPEB-associated factor that transiently interacts with elF-4E. Mol Cell. 1999;4:1017–27.

    Article  CAS  PubMed  Google Scholar 

  38. John F, Roffler S, Wicker T, Ringli C. Plant TOR signaling components. Plant Signal Behav. 2011;6:1700–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Robaglia C, Thomas M, Meyer C. Sensing nutrient and energy status by SnRK1 and TOR kinases. Curr Opin Plant Biol. 2012;15:301–7.

    Article  CAS  PubMed  Google Scholar 

  40. Xiong Y, Sheen J. The role of target of rapamycin signaling networks in plant growth and metabolism. Plant Physiol. 2014;164:499–512.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Dinkova TD, Aguilar R, Sánchez de Jiménez E. Expression of maize eukaryotic initiation factor (eIF) iso4E is regulated at the translational level. Biochem J. 2000;351:825–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Dinkova TD, Reyes de la Cruz H, Garcia-Flores C, Aguilar R, Jimenez-Garcia LF, Sanchez de Jimenez E. Dissecting the TOR-S6K signal transduction pathway in maize seedlings: relevance on cell growth regulation. Physiol Plant 2007;130:1–10.

    Google Scholar 

  43. Rodriguez CM, Freire MA, Camilleri C, Robaglia C. 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. 1998;13:465–73.

    Article  CAS  PubMed  Google Scholar 

  44. Freire MA, Tourneur C, Granier F, Camonis J, El Amrani A, Browning KS, Robaglia C. Plant lipoxygenase 2 is a translation initiation factor-4E-binding protein. Plant Mol Biol. 2002;44:129–40.

    Article  Google Scholar 

  45. Freire MA. Translation initiation factor (iso) 4E interacts with BTF3, the β-subunit of the nascent polypeptide-associated complex. Gene. 2005;345:271–7.

    Article  CAS  PubMed  Google Scholar 

  46. Lazaro-Mixteco PE, Dinkova TD. Identification of proteins from Cap-binding complexes by mass spectrometry during maize (Zea mays L.) germination. J Mex Chem Soc. 2012;56:36–50.

    Google Scholar 

  47. Yeam I, Cavatorta JR, Ripoll DR, Kang BC, Jahn MM. Functional dissection of naturally occurring amino acid substitutions in eIF4E that confers recessive potyvirus resistance in plants. Plant Cell. 2007;19:2913–28.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. 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;132:1272–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. 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;40:376–85.

    Article  CAS  PubMed  Google Scholar 

  50. 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;12:1046–51.

    Article  CAS  PubMed  Google Scholar 

  51. 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;27:329–36.

    Article  CAS  PubMed  Google Scholar 

  52. 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:e50627.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. 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;87:2089–98.

    Article  CAS  PubMed  Google Scholar 

  54. Walsh JA, Rusholme RL, Hughes SL, Jenner CE, Bambridge JM, Lydiate DJ, Green SK. Different classes of resistance to Turnip mosaic virus in Brassica rapa. Eur J Plant Pathol. 2002;108:15–20.

    Article  Google Scholar 

  55. Rusholme RL, Higgins EE, Walsh JA, Lydiate DJ. Genetic control of broad-spectrum resistance to turnip mosaic virus in Brassica rapa (Chinese cabbage). J Gen Virol. 2007;88:3177–86.

    Article  CAS  PubMed  Google Scholar 

  56. 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. 2014;77:261–8.

    Article  CAS  PubMed  Google Scholar 

  57. 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;32:1067–75.

    Article  CAS  PubMed  Google Scholar 

  58. Ruffel S, Caranta C, Palloix A, Lefebvre V, Caboche M, Bendahmane A. Structural analysis of the eukaryotic initiation factor 4E gene controlling potyvirus resistance in pepper: exploitation of a BAC library. Gene. 2004;338:209–16.

    Article  CAS  PubMed  Google Scholar 

  59. Kang BC, Yeam I, Frantz JD, Murphy JF, Jahn MM. The pvr1 locus in Capsicum encodes a translation initiation factor eIF4E that interacts with Tobacco etch virus VPg. Plant J. 2005;42:392–405.

    Article  CAS  PubMed  Google Scholar 

  60. 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;54:56–68.

    Article  CAS  PubMed  Google Scholar 

  61. Rubio M, Nicolai M, Caranta C, Palloix A. Allele mining in the pepper gene pool provided new complementation effects between pvr2-eIF4E and pvr6-eIFISO4E alleles for resistance to pepper veinal mottle virus. J Gen Virol. 2009;90:2808–14.

    Article  CAS  PubMed  Google Scholar 

  62. Ling KS, Harris KR, Meyer JD, Levi A, Guner N, Wehner TC, Bendahmane A, Havey MJ. Non-synonymous single nucleotide polymorphisms in the watermelon eIF4E gene are closely associated with resistance to zucchini yellow mosaic virus. Theor Appl Genet. 2009;120:191–200.

    Article  CAS  PubMed  Google Scholar 

  63. Nieto C, Piron F, Dalmais M, Marco CF, Moriones E, Gomez-Guillamon ML, Truniger V, Gomez P, Garcia-Mas J, Aranda MA, Bendahmane A. EcoTILLING for the identification of allelic variants of melon eIF4E, a factor that controls virus susceptibility. BMC Plant Biol. 2007;7:34. doi:10.1186/1471-2229-7-34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Truniger V, Nieto C, Gonzalez-Ibeas D, Aranda M. 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. 2008;56:716–27.

    Article  CAS  PubMed  Google Scholar 

  65. Kanyuka K, Druka A, Caldwell DG, Tymon A, McCallum N, Waugh R, Adams MJ. Evidence that the recessive bymovirus resistance locus rym4 in barley corresponds to the eukaryotic translation initiation factor 4E gene. Mol Plant Pathol. 2005;6:449–58.

    Article  CAS  PubMed  Google Scholar 

  66. Stein N, Perovic D, Kumlehn J, Pellio B, Stracke S, Streng S, Ordon F, Graner A. The eukaryotic translation initiation factor 4E confers multiallelic recessive Bymovirus resistance in Hordeum vulgare (L.). Plant J. 2005;42:912–22.

    Article  CAS  PubMed  Google Scholar 

  67. Hofinger BJ, Russell JR, Bass CHG, Baldwin T, dos Reis M, Hedley PE, Li Y, Macaulay M, Waugh R, Hammond-Kosack KE, Kanyuka K. An exceptionally high nucleotide and haplotype diversity and a signature of positive selection for the eIF4E resistance gene in barley are revealed by allele mining and phylogenetic analyses of natural populations. Mol Ecol. 2011;20:3653–68.

    CAS  PubMed  Google Scholar 

  68. German-Retana S, Walter J, Doublet B, Roudet-Tavert G, Nicaise V, Lecampion C, Houvenaghel MC, Robaglia C, Michon T, Le Gall O. Mutational analysis of plant cap-binding protein eIF4E reveals key amino acids involved in biochemical functions and potyvirus infection. J Virol. 2008;82:7601–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. 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;274:346–53.

    Article  CAS  PubMed  Google Scholar 

  70. Naderpour M, Lund OS, Larsen R, Johansen E. 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. 2010;11:255–63.

    Article  CAS  PubMed  Google Scholar 

  71. Hart JP, Griffiths PD. A series of eIF4E alleles at the Bc-3 locus are associated with recessive resistance to Clover yellow vein virus in common bean. Theor Appl Genet. 2013;126:2849–63.

    Article  CAS  PubMed  Google Scholar 

  72. 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;20:1075–82.

    Article  CAS  PubMed  Google Scholar 

  73. Andrade M, Abe Y, Nakahara KS, Uyeda I. The cyv-2 resistance to clover yellow vein virus in pea is controlled by the eukaryotic initiation factor 4E. J Gen Plant Pathol. 2009;75:241–9.

    Article  CAS  Google Scholar 

  74. 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:e15873.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Konecna E, Safarova D, Navratil M, Hanacek P, Coyne C, Flavell A, Vishnyakova M, Ambrose M, Redden R, Smykal P. Geographical gradient of the eIF4E alleles conferring resistance to potyviruses in pea (Pisum) germplasm. PLoS ONE. 2014;9:e90394.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Marandel G, Salava J, Abbott A, Candresse T, Decroocq V. 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. 2009;10:347–60.

    Article  CAS  Google Scholar 

  77. 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;143:1504–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Michon T, Estevez Y, Walter J, German-Retana S, Le Gall O. 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. 2006;273:1312–22.

    Article  CAS  PubMed  Google Scholar 

  79. 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;88:329–40.

    Article  CAS  PubMed  Google Scholar 

  80. 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;88:1029–33.

    Article  CAS  PubMed  Google Scholar 

  81. Contreras-Paredes CA, Silva-Rosales L, Daros JA, Alejandri-Ramirez ND, Dinkova TD. The absence of eukaryotic initiation factor eIFISO4E affects the systemic spread of a Tobacco etch virus isolate in Arabidopsis thaliana. Mol Plant Microbe Interact. 2013;26:461–70.

    Article  CAS  PubMed  Google Scholar 

  82. Calvo M, Martinez-Turino S, Garcia JA. Resistance to Plum pox virus Strain C in Arabidopsis thaliana and Chenopodium foetidum involves genome-linked viral protein and other viral determinants and might depend on compatibility with host translation initiation factors. Mol Plant Microbe Interact. 2014;27:1291–301.

    Article  CAS  PubMed  Google Scholar 

  83. Mazier M, Flamain F, Nicolai M, Sarnette V, Caranta C. Knock-down of both eIF4E1 and eIF4E2 genes confers broad-spectrum resistance against potyviruses in tomato. PLoS ONE. 2011;6:e29595.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Albar L, Bangratz-Reyser M, Hebrard E, Ndjiondjop MN, Jones M, Ghesquiere A. Mutations in the eIFISO4G translation initiation factor confer high resistance of rice to Rice yellow mottle virus. Plant J. 2006;47:417–26.

    Article  CAS  PubMed  Google Scholar 

  85. Hebrard E, Poulicard N, Gerard C, Traore O, Wu HC, Albar L, Fargette D, Bessin Y, Vignols F. Direct interaction between the Rice yellow mottle virus (RYMV) VPg and the central domain of the rice eIFISO4G1 factor correlates with rice susceptibility and RYMV virulence. Mol Plant Microbe Interact. 2010;23:1506–13.

    Article  CAS  PubMed  Google Scholar 

  86. Leonard S, Plante D, Wittmann S, Daigneault N, Fortin MG, Laliberte JF. Complex formation between potyvirus VPg and translation eukaryotic initiation factor 4E correlates with virus infectivity. J Virol. 2000;74:7730–7.

    Google Scholar 

  87. Khan MA, Miyoshi H, Gallie DR, Goss DJ. Potyvirus genome-linked protein, VPg, directly affects wheat germ in vitro translation: Interactions with translation initiation factors eIF4F and eIFiso4F. J Biol Chem. 2008;283:1340–9.

    Article  CAS  PubMed  Google Scholar 

  88. 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;13:795–803.

    Article  CAS  PubMed  Google Scholar 

  89. Beauchemin C, Boutet N, Laliberte JF. Visualisation of the interaction between the precursors of the viral protein linked to the genome (VPg) of Turnip mosaic virus and the translation eukaryotic initiation factor iso 4E in planta. J Virol. 2007;81:775–82.

    Article  CAS  PubMed  Google Scholar 

  90. Beauchemin C, Laliberte JF. The poly(A) binding protein is internalized in virus-induced vesicles or redistributed to the nucleolus during Turnip mosaic virus infection. J Virol. 2007;81:10905–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Thivierge K, Cotton S, Dufresne PJ, Mathieu I, Beauchemin C, Ide C, Fortin MG, Laliberte JF. Eukaryotic elongation factor 1A interacts with Turnip mosaic virus RNA-dependent RNA polymerase and VPg-Pro in virus-induced vesicles. Virology. 2008;377:216–25.

    Article  CAS  PubMed  Google Scholar 

  92. Ala-Poikela M, Goytia E, Haikonen T, Rajamaki ML, Valkonen JPT. Helper component proteinase of genus Potyvirus is an interaction partner of translation initiation factors eIF(iso)4E and eIF4E that contains a 4E binding motif. J Virol. 2011;85:6784–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Estevan J, Marena A, Callot C, Lacombe S, Moretti A, Caranta C, Gallois JL. Specific requirement for translation initiation factor 4E or its isoform drives plant host susceptibility to Tobacco etch virus. BMC Plant Biol. 2014;14:67.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Cavatorta JR, Savage AE, Yeam I, Gray SM, Jahn MM. Positive Darwinian selection at single amino acid sites conferring plant virus resistance. J Mol Evol. 2008;67:551–9.

    Article  CAS  PubMed  Google Scholar 

  95. Moury B, Charron C, Janzac B, Simon V, Gallois JL, Palloix A, Caranta C. Evolution of plant eukaryotic initiation factor 4E (eIF4E) and potyvirus genome-linked protein (VPg): a game of mirrors impacting resistance spectrum and durability. Infect Genet Evol. 2014;27:472–80.

    Article  CAS  PubMed  Google Scholar 

  96. Moury B, Morel C, Johansen E, Guilbaud L, Souche S, Ayme V, Caranta C, Palloix A, Jacquemond M. Mutations in Potato virus Y genome-linked protein determine virulence toward recessive resistances in Capsicum annuum and Lycopersicon hirsutum. Mol Plant Microbe Interact. 2004;17:322–9.

    Article  PubMed  Google Scholar 

  97. Quenouille J, Saint-Felix L, Moury B, Palloix A. Diversity of genetic backgrounds modulating the durability of a major resistance gene. Analysis of a core collection of pepper landraces resistant to Potato virus Y. Mol. Plant Pathol. 2016;17:296–302.

    Article  CAS  Google Scholar 

  98. Ayme V, Souche S, Caranta C, Jacquemond M, Chadoeuf J, Palloix A, Moury B. Different mutations in the genome-linked protein VPg of potato virus Y confer virulence on the pvr2(3) resistance in pepper. Mol Plant Microbe Interact. 2006;19:557–63.

    Article  CAS  PubMed  Google Scholar 

  99. Ayme V, Petit-Pierre J, Souche S, Palloix A, Moury B. Molecular dissection of the potato virus Y VPg virulence factor reveals complex adaptations to the pvr2 resistance allelic series in pepper. J Gen Virol. 2007;88:1594–601.

    Article  CAS  PubMed  Google Scholar 

  100. Quenouille J, Montarry J, Palloix A, Moury B. Farther, slower, stronger: how the plant genetic background protects a major resistance gene from breakdown. Mol Plant Pathol. 2012;14:109–18.

    Article  CAS  PubMed  Google Scholar 

  101. Stamatakis A. RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 2010;New Orleans, LA:1–8.

    Google Scholar 

Download references

Acknowledgments

Research performed in Dr. Dinkova’s laboratory is supported by grants from Consejo Nacional de Ciencia y Tecnología, CONACYT 238439, Facultad de Química PAIP 5000-9118, and Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica, PAPIIT IN211215. The authors acknowledge the help provided by Dr. Vasti T. Juárez-González in figure preparation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tzvetanka D. Dinkova .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Dinkova, T.D., Martinez-Castilla, L., Cruz-Espíndola, M.A. (2016). The Diversification of eIF4E Family Members in Plants and Their Role in the Plant-Virus Interaction. In: Hernández, G., Jagus, R. (eds) Evolution of the Protein Synthesis Machinery and Its Regulation. Springer, Cham. https://doi.org/10.1007/978-3-319-39468-8_9

Download citation

Publish with us

Policies and ethics