Evolutionary Aspects of Translation Regulation During Abiotic Stress and Development in Plants

  • René Toribio
  • Alfonso Muñoz
  • Ana B. Castro-Sanz
  • Alejandro Ferrando
  • Marta Berrocal-Lobo
  • M. Mar CastellanoEmail author


In the last decade, different studies have highlighted the importance translational control in plant development and in response to environmental cues. Although most translation factors are conserved in plants, our current knowledge about translation regulation in this kingdom is still scarce. This chapter will outline the mechanisms controlling the selective translation of mRNAs under different abiotic stresses and developmental conditions in several eukaryotic model systems, discussing whether similar or specific mechanisms exist in plants.


Translational Repression Translation Regulation Translation Elongation Factor Translation Factor Wheat Germ Extract 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    Hernandez G, Vazquez-Pianzola P. Functional diversity of the eukaryotic translation initiation factors belonging to eIF4 families. Mech Dev. 2005;122:865–76. doi: 10.1016/j.mod.2005.04.002.CrossRefPubMedGoogle Scholar
  2. 2.
    Hernandez G, Altmann M, Lasko P. Origins and evolution of the mechanisms regulating translation initiation in eukaryotes. Trends Biochem Sci. 2010;35:63–73. doi: 10.1016/j.tibs.2009.10.009.CrossRefPubMedGoogle Scholar
  3. 3.
    Hernandez G, Proud CG, Preiss T, Parsyan A. On the diversification of the translation apparatus across eukaryotes. Comp Funct Genomics. 2012;2012:256848. doi: 10.1155/2012/256848.PubMedPubMedCentralGoogle Scholar
  4. 4.
    Browning KS, Bailey-Serres J. Mechanism of cytoplasmic mRNA translation. The Arabidopsis book/Am Soc Plant Biol. 2015;13:e0176. doi: 10.1199/tab.0176.Google Scholar
  5. 5.
    Sonenberg N, Hinnebusch AG. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell. 2009;136:731–45. doi: 10.1016/j.cell.2009.01.042.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Jackson RJ, Hellen CU, Pestova TV. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol. 2010;11:113–27. doi: 10.1038/nrm2838.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Aitken CE, Lorsch JR. A mechanistic overview of translation initiation in eukaryotes. Nat Struct Mol Biol. 2012;19:568–76. doi: 10.1038/nsmb.2303.CrossRefPubMedGoogle Scholar
  8. 8.
    Hershey JW, Sonenberg N, Mathews MB. Principles of translational control: an overview. Cold Spring Harbor perspectives in biology. 2012; 4. doi: 10.1101/cshperspect.a011528.Google Scholar
  9. 9.
    Lomakin IB, Steitz TA. The initiation of mammalian protein synthesis and mRNA scanning mechanism. Nature. 2013;500:307–11. doi: 10.1038/nature12355.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Mead EJ, Masterton RJ, von der Haar T, Tuite MF, Smales CM. Control and regulation of mRNA translation. Biochem Soc Trans. 2014;42:151–4. doi: 10.1042/BST20130259.CrossRefPubMedGoogle Scholar
  11. 11.
    Muñoz A, Castellano MM. Regulation of translation initiation under abiotic stress conditions in plants: is it a conserved or not so conserved process among eukaryotes? Comp Funct Genomics. 2012;2012:8. doi: 10.1155/2012/406357.CrossRefGoogle Scholar
  12. 12.
    Echevarria-Zomeno S, Yanguez E, Fernandez-Bautista N, Castro-Sanz AB, Ferrando A, Castellano MM. Regulation of Translation Initiation under Biotic and Abiotic Stresses. Int J Mol Sci. 14:4670–4683. doi: 10.3390/ijms14034670.Google Scholar
  13. 13.
    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;. doi: 10.1074/jbc.M111.280099.PubMedPubMedCentralGoogle Scholar
  14. 14.
    Patrick RM, Browning KS. The eIF4F and eIFiso4F Complexes of plants: an evolutionary perspective. Comp Funct Genomics. 2012;2012:287814. doi: 10.1155/2012/287814.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    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. doi: 10.1074/jbc.M111.280099.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    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. doi: 10.1104/pp.109.138438.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    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. doi: 10.1074/jbc.M103869200.CrossRefPubMedGoogle Scholar
  18. 18.
    Mader S, Lee H, Pause A, Sonenberg N. The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4 gamma and the translational repressors 4E-binding proteins. Mol Cell Biol. 1995;15:4990–7.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK. Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G. Mol Cell. 1999;3:707–16.CrossRefPubMedGoogle Scholar
  20. 20.
    Altmann M, Schmitz N, Berset C, Trachsel H. A novel inhibitor of cap-dependent translation initiation in yeast: p20 competes with eIF4G for binding to eIF4E. The EMBO journal. 1997;16:1114–21. doi: 10.1093/emboj/16.5.1114.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Matsuo H, Li H, McGuire AM, Fletcher CM, Gingras AC, Sonenberg N, Wagner G. Structure of translation factor eIF4E bound to m7GDP and interaction with 4E-binding protein. Nature structural biology. 1997;4:717–24.CrossRefPubMedGoogle Scholar
  22. 22.
    Siddiqui N, Sonenberg N. Signalling to eIF4E in cancer. Biochem Soc Trans. 2015;43:763–72. doi: 10.1042/BST20150126.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Clemens MJ. Translational regulation in cell stress and apoptosis. Roles of the eIF4E binding proteins. J Cell Mol Med. 2001; 5:221–239. doi:005.003.01Google Scholar
  24. 24.
    Rhoads RE. eIF4E: new family members, new binding partners, new roles. J Biol Chem. 2009;284:16711–5. doi: 10.1074/jbc.R900002200.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Carrera AC. TOR signaling in mammals. J Cell Sci. 2004;117:4615–6. doi: 10.1242/jcs.01311.CrossRefPubMedGoogle Scholar
  26. 26.
    Kneller EL, Rakotondrafara AM, Miller WA. Cap-independent translation of plant viral RNAs. Virus Res. 2006;119:63–75. doi: 10.1016/j.virusres.2005.10.010.CrossRefPubMedGoogle Scholar
  27. 27.
    Mardanova ES, Zamchuk LA, Skulachev MV, Ravin NV. The 5′ untranslated region of the maize alcohol dehydrogenase gene contains an internal ribosome entry site. Gene. 2008;420:11–6. doi: 10.1016/j.gene.2008.04.008.CrossRefPubMedGoogle Scholar
  28. 28.
    Dinkova TD, Zepeda H, Martinez-Salas E, Martinez LM, Nieto-Sotelo J, de Jimenez ES. Cap-independent translation of maize Hsp101. Plant J. 2005;41:722–31. doi: 10.1111/j.1365-313X.2005.02333.x.CrossRefPubMedGoogle Scholar
  29. 29.
    Cui Y, Rao S, Chang B, Wang X, Zhang K, Hou X, Zhu X, Wu H, Tian Z, Zhao Z, Yang C, Huang T. AtLa1 protein initiates IRES-dependent translation of WUSCHEL mRNA and regulates the stem cell homeostasis of Arabidopsis in response to environmental hazards. Plant, Cell Environ. 2015;38:2098–114. doi: 10.1111/pce.12535.CrossRefGoogle Scholar
  30. 30.
    Deprost D, Yao L, Sormani R, Moreau M, Leterreux G, Nicolai M, Bedu M, Robaglia C, Meyer C. The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Rep. 2007;8:864–70. doi: 10.1038/sj.embor.7401043.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Caldana C, Li Y, Leisse A, Zhang Y, Bartholomaeus L, Fernie AR, Willmitzer L, Giavalisco P. Systemic analysis of inducible target of rapamycin mutants reveal a general metabolic switch controlling growth in Arabidopsis thaliana. Plant J. 2013;73:897–909. doi: 10.1111/tpj.12080.CrossRefPubMedGoogle Scholar
  32. 32.
    Dobrenel T, Marchive C, Azzopardi M, Clement G, Moreau M, Sormani R, Robaglia C, Meyer C. Sugar metabolism and the plant target of rapamycin kinase: a sweet operaTOR? Front Plant Sci. 2013;4:93. doi: 10.3389/fpls.2013.00093.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Robaglia C, Thomas M, Meyer C. Sensing nutrient and energy status by SnRK1 and TOR kinases. Curr Opin Plant Biol. 2012;15:301–7. doi: 10.1016/j.pbi.2012.01.012.CrossRefPubMedGoogle Scholar
  34. 34.
    Xiong Y, Sheen J. Rapamycin and glucose-target of rapamycin (TOR) protein signaling in plants. J Biol Chem. 2012;287:2836–42. doi: 10.1074/jbc.M111.300749.CrossRefPubMedGoogle Scholar
  35. 35.
    Richter JD, Sonenberg N. Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature. 2005;433:477–80. doi: 10.1038/nature03205.CrossRefPubMedGoogle Scholar
  36. 36.
    Vardy L, Orr-Weaver TL. Regulating translation of maternal messages: multiple repression mechanisms. Trends Cell Biol. 2007;17:547–54. doi: 10.1016/j.tcb.2007.09.002.CrossRefPubMedGoogle Scholar
  37. 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.CrossRefPubMedGoogle Scholar
  38. 38.
    Richter JD. CPEB: a life in translation. Trends Biochem Sci. 2007;32:279–85. doi: 10.1016/j.tibs.2007.04.004.CrossRefPubMedGoogle Scholar
  39. 39.
    Wells DG. RNA-binding proteins: a lesson in repression. J Neurosci Official J Soc Neurosci. 2006;26:7135–8. doi: 10.1523/JNEUROSCI.1795-06.2006.CrossRefGoogle Scholar
  40. 40.
    Jung MY, Lorenz L, Richter JD. Translational control by neuroguidin, a eukaryotic initiation factor 4E and CPEB binding protein. Mol Cell Biol. 2006;26:4277–87. doi: 10.1128/MCB.02470-05.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Nelson MR, Leidal AM, Smibert CA. Drosophila Cup is an eIF4E-binding protein that functions in Smaug-mediated translational repression. The EMBO J. 2004;23:150–9. doi: 10.1038/sj.emboj.7600026.CrossRefPubMedGoogle Scholar
  42. 42.
    Nakamura A, Sato K, Hanyu-Nakamura K. Drosophila cup is an eIF4E binding protein that associates with Bruno and regulates oskar mRNA translation in oogenesis. Dev Cell. 2004;6:69–78.CrossRefPubMedGoogle Scholar
  43. 43.
    Napoli I, Mercaldo V, Boyl PP, Eleuteri B, Zalfa F, De Rubeis S, Di Marino D, Mohr E, Massimi M, Falconi M, Witke W, Costa-Mattioli M, Sonenberg N, Achsel T, Bagni C. The fragile X syndrome protein represses activity-dependent translation through CYFIP1, a new 4E-BP. Cell. 2008;134:1042–54. doi: 10.1016/j.cell.2008.07.031.CrossRefPubMedGoogle Scholar
  44. 44.
    Rom E, Kim HC, Gingras AC, Marcotrigiano J, Favre D, Olsen H, Burley SK, Sonenberg N. Cloning and characterization of 4EHP, a novel mammalian eIF4E-related cap-binding protein. J Biol Chem. 1998;273:13104–9.CrossRefPubMedGoogle Scholar
  45. 45.
    Cho PF, Poulin F, Cho-Park YA, Cho-Park IB, Chicoine JD, Lasko P, Sonenberg N. A new paradigm for translational control: inhibition via 5’-3’ mRNA tethering by Bicoid and the eIF4E cognate 4EHP. Cell. 2005;121:411–23. doi: 10.1016/j.cell.2005.02.024.CrossRefPubMedGoogle Scholar
  46. 46.
    Cho PF, Gamberi C, Cho-Park YA, Cho-Park IB, Lasko P, Sonenberg N. Cap-dependent translational inhibition establishes two opposing morphogen gradients in Drosophila embryos. Current Biol CB. 2006;16:2035–41. doi: 10.1016/j.cub.2006.08.093.CrossRefGoogle Scholar
  47. 47.
    Kim HS, Abbasi N, Choi SB. Bruno-like proteins modulate flowering time via 3’ UTR-dependent decay of SOC1 mRNA. New Phytol. 2013;198:747–56. doi: 10.1111/nph.12181.CrossRefPubMedGoogle Scholar
  48. 48.
    Francischini CW, Quaggio RB. Molecular characterization of Arabidopsis thaliana PUF proteins–binding specificity and target candidates. The FEBS J. 2009;276:5456–70. doi: 10.1111/j.1742-4658.2009.07230.x.CrossRefPubMedGoogle Scholar
  49. 49.
    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.CrossRefPubMedGoogle Scholar
  50. 50.
    Zhang P, McGrath BC, Reinert J, Olsen DS, Lei L, Gill S, Wek SA, Vattem KM, Wek RC, Kimball SR, Jefferson LS, Cavener DR. The GCN2 eIF2alpha kinase is required for adaptation to amino acid deprivation in mice. Mol Cell Biol. 2002;22:6681–8.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Harding HP, Calfon M, Urano F, Novoa I, Ron D. Transcriptional and translational control in the Mammalian unfolded protein response. Annu Rev Cell Dev Biol. 2002;18:575–99. doi: 10.1146/annurev.cellbio.18.011402.160624.CrossRefPubMedGoogle Scholar
  52. 52.
    Clemens MJ. PKR–a protein kinase regulated by double-stranded RNA. Int J Biochem Cell Biol. 1997; 29:945–949. doi:S1357-2725(96)00169-0Google Scholar
  53. 53.
    Chen JJ. Regulation of protein synthesis by the heme-regulated eIF2alpha kinase: relevance to anemias. Blood. 2007;109:2693–9. doi: 10.1182/blood-2006-08-041830.PubMedPubMedCentralGoogle Scholar
  54. 54.
    Zhan K, Narasimhan J, Wek RC. Differential activation of eIF2 kinases in response to cellular stresses in Schizosaccharomyces pombe. Genetics. 2004;168:1867–75. doi: 10.1534/genetics.104.031443.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Lageix S, Lanet E, Pouch-Pelissier MN, Espagnol MC, Robaglia C, Deragon JM, Pelissier T. Arabidopsis eIF2alpha kinase GCN2 is essential for growth in stress conditions and is activated by wounding. BMC Plant Biol. 2008;8:134. doi: 10.1186/1471-2229-8-134.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Zhang Y, Wang Y, Kanyuka K, Parry MA, Powers SJ, Halford NG. GCN2-dependent phosphorylation of eukaryotic translation initiation factor-2alpha in Arabidopsis. J Exp Bot. 2008;59:3131–41. doi: 10.1093/jxb/ern169.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Shaikhin SM, Smailov SK, Lee AV, Kozhanov EV, Iskakov BK. Interaction of wheat germ translation initiation factor 2 with GDP and GTP. Biochimie. 1992;74:447–54.CrossRefPubMedGoogle Scholar
  58. 58.
    Gilks N, Kedersha N, Ayodele M, Shen L, Stoecklin G, Dember LM, Anderson P. Stress Granule Assembly Is Mediated by Prion-like Aggregation of TIA-1. Mol Biol Cell. 2004;15:5383–98. doi: 10.1091/mbc.E04-08-0715.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Juntawong P, Sorenson R, Bailey-Serres J. Cold shock protein 1 chaperones mRNAs during translation in Arabidopsis thaliana. Plant J. 2013;74:1016–28. doi: 10.1111/tpj.12187.CrossRefPubMedGoogle Scholar
  60. 60.
    Li CH, Ohn T, Ivanov P, Tisdale S, Anderson P. eIF5A promotes translation elongation, polysome disassembly and stress granule assembly. PLoS ONE. 2010;5:e9942. doi: 10.1371/journal.pone.0009942.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Thomas A, Goumans H, Amesz H, Benne R, Voorma HO. A Comparison of the Initiation Factors of Eukaryotic Protein Synthesis from Ribosomes and from the Postribosomal Supernatant. Eur J Biochem. 1979;98:329–37. doi: 10.1111/j.1432-1033.1979.tb13192.x.CrossRefPubMedGoogle Scholar
  62. 62.
    Saini P, Eyler DE, Green R, Dever TE. Hypusine-containing protein eIF5A promotes translation elongation. Nature. 2009;459:118–21.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Dever TE, Gutierrez E, Shin B-S. The hypusine-containing translation factor eIF5A. Crit Rev Biochem Mol Biol. 2014;49:413–25. doi: 10.3109/10409238.2014.939608.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Park M. The post-translational synthesis of a polyamine-derived amino acid, hypusine, in the eukaryotic translation initiation factor 5A (eIF5A). J Biochem. 2006;139:161–9.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Shiba T, Mizote H, Kaneko T, Nakajima T, Yasuo K, sano I. Hypusine, a new amino acid occurring in bovine brain: Isolation and structural determination. Biochim Biophys Acta (BBA)- General Subjects. 1971; 244:523–531.Google Scholar
  66. 66.
    Park MH, Wolff EC, Folk JE. Hypusine—its posttranslational formation in eukaryotic initiation factor-5A and its potential role in cellular-regulation. BioFactors. 1993;4:95–104.PubMedGoogle Scholar
  67. 67.
    Chattopadhyay MK, Park MH, Tabor H. Hypusine modification for growth is the major function of spermidine in Saccharomyces cerevisiae polyamine auxotrophs grown in limiting spermidine. Proc Natl Acad Sci. 2008;105:6554–9. doi: 10.1073/pnas.0710970105.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Pällmann N, Braig M, Sievert H, Preukschas M, Hermans-Borgmeyer I, Schweizer M, Nagel CH, Neumann M, Wild P, Haralambieva E, Hagel C, Bokemeyer C, Hauber J, Balabanov S. Biological relevance and therapeutic potential of the hypusine modification system. J Biol Chem. 2015;290:18343–60. doi: 10.1074/jbc.M115.664490.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Nishimura K, Lee S, Park J, Park M. Essential role of eIF5A-1 and deoxyhypusine synthase in mouse embryonic development. Amino Acids. 2012;42:703–10. doi: 10.1007/s00726-011-0986-z.CrossRefPubMedGoogle Scholar
  70. 70.
    Pagnussat GC, Yu HJ, Ngo QA, Rajani S, Mayalagu S, Johnson CS, Capron A, Xie LF, Ye D, Sundaresan V. Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development. 2005;132:603–14.CrossRefPubMedGoogle Scholar
  71. 71.
    Imai A, Matsuyama T, Hanzawa Y, Akiyama T, Tamaoki M, Saji H, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Komeda Y, Takahashi T. Spermidine synthase genes are essential for survival of arabidopsis. Plant Physiol. 2004;135:1565–73.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Wolff EC, Kang KR, Kim YS, Park MH. Posttranslational synthesis of hypusine: evolutionary progression and specificity of the hypusine modification. Amino Acids. 2007;33:341–50.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Navarre WW, Zou SB, Roy H, Xie JL, Savchenko A, Singer A, Edvokimova E, Prost LR, Kumar R, Ibba M, Fang FC. PoxA, YjeK, and elongation factor P coordinately modulate virulence and drug resistance in salmonella enterica. Mol Cell. 2010;39:209–21.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Lassak J, Keilhauer EC, Fürst M, Wuichet K, Gödeke J, Starosta AL, Chen J-M, Søgaard-Andersen L, Rohr J, Wilson DN, Häussler S, Mann M, Jung K. Arginine-rhamnosylation as new strategy to activate translation elongation factor P. Nat Chem Biol. 2015;11:266–70. doi: 10.1038/nchembio.1751.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Bullwinkle TJ, Zou SB, Rajkovic A, Hersch SJ, Elgamal S, Robinson N, Smil D, Bolshan Y, Navarre WW, Ibba M. (R)-β-Lysine-modified elongation factor P functions in translation elongation. J Biol Chem. 2013;288:4416–23. doi: 10.1074/jbc.M112.438879.CrossRefPubMedGoogle Scholar
  76. 76.
    Blaha G, Stanley RE, Steitz TA. Formation of the first peptide bond: the structure of EF-P bound to the 70S ribosome. Science. 2009;325:966–70. doi: 10.1126/science.1175800.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Gutierrez E, Shin B-S, Woolstenhulme Christopher J, Kim J-R, Saini P, Buskirk Allen R, Dever Thomas E. eIF5A Promotes Translation of Polyproline Motifs. Mol Cell. 2013; 51:35-45. doi: 10.1016/j.molcel.2013.04.021 Google Scholar
  78. 78.
    Doerfel LK, Wohlgemuth I, Kothe C, Peske F, Urlaub H, Rodnina MV. EF-P Is essential for rapid synthesis of proteins containing consecutive proline residues. Science. 2013;339:85–8. doi: 10.1126/science.1229017.CrossRefPubMedGoogle Scholar
  79. 79.
    Ude S, Lassak J, Starosta AL, Kraxenberger T, Wilson DN, Jung K. Translation elongation factor EF-P alleviates ribosome stalling at polyproline stretches. Science. 2013;339:82–5. doi: 10.1126/science.1228985.CrossRefPubMedGoogle Scholar
  80. 80.
    Li T, Belda-Palazon B, Ferrando A, Alepuz P. Fertility and polarized cell growth depends on eIF5A for translation of polyproline-rich formins in saccharomyces cerevisiae. Genetics. 2014;197:1191–200. doi: 10.1534/genetics.114.166926.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Mandal A, Mandal S, Park MH. Genome-wide analyses and functional classification of proline repeat-rich proteins: potential role of eIF5A in eukaryotic evolution. PLoS ONE. 2014;9:e111800.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Ingolia NT, Ghaemmaghami S, Newman JRS, Weissman JS. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science. 2009;324:218–23. doi: 10.1126/science.1168978.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Elgamal S, Katz A, Hersch SJ, Newsom D, White P, Navarre WW, Ibba M. EF-P dependent pauses integrate proximal and distal signals during translation. PLoS Genet. 2014;10:e1004553.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Woolstenhulme C, Guydosh N, Green R, Buskirk A. High-precision analysis of translational pausing by ribosome profiling in bacteria lacking EFP. Cell Reports. 2015;11:13–21. doi: 10.1016/j.celrep.2015.03.014.CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Duguay J, Jamal S, Liu Z, Wang TW, Thompson JE. Leaf-specific suppression of deoxyhypusine synthase in Arabidopsis thaliana enhances growth without negative pleiotropic effects. J Plant Physiol. 2007;164:408–20.CrossRefPubMedGoogle Scholar
  86. 86.
    Feng H, Chen Q, Feng J, Zhang J, Yang X, Zuo J. Functional characterization of the arabidopsis eukaryotic translation initiation factor 5A-2 that plays a crucial role in plant growth and development by regulating cell division, cell growth, and cell death. Plant Physiol. 2007;144:1531–45.CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Liu Z, Duguay J, Ma F, Wang TW, Tshin R, Hopkins MT, McNamara L, Thompson JE. Modulation of eIF5A1 expression alters xylem abundance in Arabidopsis thaliana. JExpBot. 2008;59:939–50.Google Scholar
  88. 88.
    Ma F, Liu Z, Wang TW, Hopkins MT, Peterson CA, Thompson JE. Arabidopsis eIF5A3 influences growth and the response to osmotic and nutrient stress. Plant Cell Environ. 2010;33:1682–96. doi: 10.1111/j.1365-3040.2010.02173.x.CrossRefPubMedGoogle Scholar
  89. 89.
    Belda-Palazón B, Nohales MA, Rambla JL, Aceña JL, Delgado O, Fustero S, Martínez MC, Granell A, Carbonell J, Ferrando A. Biochemical quantitation of the eIF5A hypusination in Arabidopsis thaliana uncovers ABA-dependent regulation. Front Plant Sci. 2014; 5. doi: 10.3389/fpls.2014.00202.
  90. 90.
    Zuk D, Jacobson A. A single amino acid substitution in yeast eIF-5A results in mRNA stabilization. The EMBO J. 1998;17:2914–25. doi: 10.1093/emboj/17.10.2914.CrossRefPubMedGoogle Scholar
  91. 91.
    Ren B, Chen Q, Hong S, Zhao W, Feng J, Feng H, Zuo J. The arabidopsis eukaryotic translation initiation factor eIF5A-2 regulates root protoxylem development by modulating cytokinin signaling. Plant Cell. 2013;25:3841–57. doi: 10.1105/tpc.113.116236.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • René Toribio
    • 1
  • Alfonso Muñoz
    • 1
  • Ana B. Castro-Sanz
    • 1
  • Alejandro Ferrando
    • 2
  • Marta Berrocal-Lobo
    • 1
  • M. Mar Castellano
    • 1
    Email author
  1. 1.Centro de Biotecnología y Genómica de Plantas. Universidad Politécnica de Madrid (UPM) - Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA)Pozuelo de AlarcónSpain
  2. 2.Instituto de Biología Molecular y Celular de Plantas, CSIC-Universidad Politécnica de ValenciaValenciaSpain

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