Plant Molecular Biology

, Volume 32, Issue 1–2, pp 145–158 | Cite as

Translational control of cellular and viral mRNAs

  • Daniel R. Gallie


We are becoming increasingly aware of the role that translational control plays in regulating gene expression in plants. There are now many examples in which specific mechanisms have evolved at the translational level that directly impact the amount of protein produced from an mRNA. All regions of an mRNA, i.e., the 5′ leader, the coding region, and the 3′-untranslated region, have the potential to influence translation. The 5′-terminal cap structure and the poly(A) tail at the 3′ terminus serve as additional elements controlling translation. Many viral mRNAs have evolved alternatives to the cap and poly(A) tail that are functionally equivalent. Nevertheless, for both cellular and viral mRNAs, a co-dependent interaction between the terminal controlling elements appears to be the universal basis for efficient translation.

Key words

5′leader 3′-untranslated region plant virus poly(A) tail cap, initiation factors 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Arrigo A-P: Cellular localization of HSP23 during Drosophila development and following subsequent heat shock. Devel Biol 122: 39–48 (1987).Google Scholar
  2. 2.
    Basso J, Dallaire P, Charest PJ, Devantier Y, Laliberte J-F: Evidence for an internal ribosome entry site within the 5′ non-translated region of turnip mosaic potyvirus RNA. J Gen Virol 75: 3157–3165 (1994).Google Scholar
  3. 3.
    Bienz M: Developmental control of the heat shock response in Xenopus. Proc Natl Acad Sci 81: 3138–3142 (1984).Google Scholar
  4. 4.
    Bienz M, Gurdon JB: The heat shock response in Xenopus oocytes is controlled at the translational level. Cell 29: 811–819 (1982).Google Scholar
  5. 5.
    Bond UM, Yario TA, Steitz JA: Multiple processing-defective mutations in a mammalian histone pre-mRNA are suppressed by compensatory changes in U7RNA both in vivo and in vitro. Genes Devel 5: 1709–1722 (1991).Google Scholar
  6. 6.
    Brault V, Miller WA: Translational frameshifting mediated by a viral sequence in plant cells. Proc Natl Acad Sci USA 89: 2262–2266 (1992).Google Scholar
  7. 7.
    Breiteneder H, Michalowski CB, Bohnert HJ: Environmental stress-mediated differential 3′ end formation of chloroplast RNA-binding protein transcripts. Plant Mol Biol 26: 833–849 (1994).Google Scholar
  8. 8.
    Browning KS, Lax SR, Humphreys J, Ravel JM, Jobling SA, Gehrke L: Evidence that the 5′-untranslated leader of mRNA affects the requirement for wheat germ initiation factors 4A, 4F, and 4G. J Biol Chem 263: 9630–9634 (1988).Google Scholar
  9. 9.
    Capasso O, Bleecker GC, Heintz N: Sequences controlling histone H4 mRNA abundance. EMBO J 6: 1825–1831 (1987).Google Scholar
  10. 10.
    Carrington JC, Freed DD: Cap-independent enhancement of translation by a plant potyvirus 5′ nontranslated region. J Virol 64: 1590–1597 (1990).Google Scholar
  11. 11.
    Chaboute M-E, Chaubet N, Clement B, Gigot C, Philipps G: Polyadenylation of histone H3 and H4 mRNAs in dicotyledonous plants. Gene 71: 217–223 (1988).Google Scholar
  12. 12.
    Chaubet N, Chaboute M-E, Clement B, Ehling M, Philipps G, Gigot C: The histone H3 and H4 mRNAs are polyadenylated in maize. Nucl Acids Res 16: 1295–1304 (1988).Google Scholar
  13. 13.
    Collier NC, Schlesinger MJ: The dynamic state of heat shock proteins in chicken embryo fibroblasts. J Cell Biol 103: 1495–1507 (1986).Google Scholar
  14. 14.
    Damiani RD, Wessler S: An upstream open reading frame represses expression of Lc, a member of the R/B family of maize transcriptional activators. Proc Natl Acad Sci USA 90: 8244–8248 (1993).Google Scholar
  15. 15.
    Danthinne X, Seurinck J, Meulewaeter F, Van Montagu M, Cornelissen M: The 3′ untranslated region of satellite tobacco necrosis virus RNA stimulates translation in vitro. Mol Cell Biol 13: 3340–3349 (1993).Google Scholar
  16. 16.
    De Haan P, Gielen JJL, Prins M, Wijkamp IG, van Schepen A, Peters D, van Grinsven MQJM, Goldbach R: Characterization of RNA-mediated resistance to tomato spotted wilt virus in transgenic tobacco plants. Bio/Technology 10: 1133–1137 (1992).Google Scholar
  17. 17.
    Dowson Day MJ, Ashurst JL, Mathias SF, Watts JW, Wilson TMA, Dixon RA. Plant viral leaders influence expression of a reporter gene in tobacco. Plant Mol Biol 23: 97–109 (1993).Google Scholar
  18. 18.
    Duncan R, Milburn SC, Hershey JWB: Regulated phosphorylation and low abundance of HeLa cell initiation factor eIF-4F suggest a role in translational control. J Biol Chem 262: 380–388 (1987).Google Scholar
  19. 19.
    Duncan R, Hershey JWB: Protein synthesis and protein phosphorylation during heat stress; recovery, and adaptation. J Cell Biol 109: 1467–1481 (1989).Google Scholar
  20. 20.
    Eckner R, Ellmeier W, Birnstiel ML: Mature mRNA 3′ end formation stimulates RNA export from the nucleus. EMBO J 10: 3513–3522 (1991).Google Scholar
  21. 21.
    Fabbri BJ, Hershey JWB: Comparison of in vivo and in vitro phosphorylation patterns of eIF-4B. In: Translational Control, p. 66. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1996).Google Scholar
  22. 22.
    Fabry S, Muller K, Lindauer A, Park PB, Cornelius T, Schmitt R: The organization, structure, and controlling elements of Chlamydomonas histone genes reveal features linking plant and animal genes. Curr Genet 28: 333–345 (1995).Google Scholar
  23. 23.
    Fennoy SL, Bailey-Serres J. Post-transcriptional regulation of gene expression in oxygen-deprived roots of maize. Plant J 7: 287–295 (1995).Google Scholar
  24. 24.
    Fletcher L, Corbin SD, Browning KS, Ravel JM: The absence of a m7G cap on β-globin mRNA and alfalfa mosaic virus RNA 4 increases the amounts of initiation factor 4F required for translation. J Biol Chem 265: 19582–19587 (1990).Google Scholar
  25. 25.
    Fütterer J, Hohn T: Translation of a polycistronic mRNA in the presence of the cauliflower mosaic virus transactivator protein. EMBO J 10: 3887–3896 (1991).Google Scholar
  26. 26.
    Gallie DR: The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes Devel 5: 2108–2116 (1991).Google Scholar
  27. 27.
    Gallie DR, Caldwell C, Pitto L: Heat shock disrupts cap and poly(A) tail function during translation and increases mRNA stability of introduced reporter mRNA. Plant Physiol 108: 1703–1713 (1995).Google Scholar
  28. 28.
    Gallie DR, Feder JN, Schimke RT, Walbot V: Posttranscriptional regulation in higher eukaryotes: the role of the reporter gene in controlling expression. Mol Gen Genet 228: 258–264 (1991).Google Scholar
  29. 29.
    Gallie DR, Kobayashi M: The role of the 3′-untranslated region of non-polyadenylated plant viral mRNAs in regulating translational efficiency. Gene 142: 159–165 (1994).Google Scholar
  30. 29a.
    Gallie DR, Lewis NJ, Marzluff WF: The histone 3′-terminal stem-loop is necessary for translation in Chinese hamster ovary cells. Nucl Acids Res, in press (1996).Google Scholar
  31. 30.
    Gallie DR, Lucas WJ, Walbot V: Visualizing mRNA expression in plant protoplasts: factors influencing efficient mRNA uptake and translation. Plant Cell 1: 301–311 (1989).Google Scholar
  32. 31.
    Gallie DR, Sleat DE, Watts JW, Turner PC, Wilson TMA: The 5′-leader sequence of tobacco mosaic virus RNA enhances the expression of foreign gene transcripts in vitro and it in vivo. Nucl Acids Res 15: 3257–3273 (1987).Google Scholar
  33. 32.
    Gallie DR, Sleat DE, Watts JW, Turner PC, Wilson TMA: A comparison of eukaryotic viral 5′-leader sequences as enhancers of mRNA expression in vivo. Nucl Acids Res 15: 8693–8711 (1987).Google Scholar
  34. 33.
    Gallie DR, Tanguay R: Poly(A) binds to initiation factors and increases cap-dependent translation in vitro. J Biol Chem 269: 17166–17173 (1994).Google Scholar
  35. 34.
    Gallie DR, Tanguay R, Leathers V: The tobacco etch viral 5′ leader and poly(A) tail are functionally synergistic regulators of translation. Gene 165: 233 (1995).Google Scholar
  36. 35.
    Gallie DR, Walbot V: RNA pseudoknot domain of tobacco mosaic virus can functionally substitute for a poly(A) tail in plant and animal cells. Genes Devel 4: 1149–1157 (1990).Google Scholar
  37. 36.
    Gallie DR, Walbot V: Identification of the motifs within the tobacco mosaic virus 5′-leader responsible for enhancing translation. Nucl Acids Res 20: 4631–4638 (1992).Google Scholar
  38. 37.
    Gallie DR, Young TE: The regulation of gene expression in transformed maize aleurone and endosperm protoplasts. Plant Physiol 106: 929–939 (1994).Google Scholar
  39. 38.
    Gielen JJL, de Haan P, Kool AJ, Peters D, van Grinsven MQIM, Goldbach RW: Engineered resistance to tomato spotted wilt virus, a negative-strand RNA virus. Bio/technology 9: 1363–1367 (1991).Google Scholar
  40. 39.
    Harris ME, Bohni R, Schneiderman MH, Ramamurthy L, Schumperli D, Marzluff WF: Regulation of histone mRNA in the unperturbed cell cycle: evidence suggesting control at two posttranscriptional steps. Mol Cell Biol 11: 2416–2424 (1991).Google Scholar
  41. 40.
    Hentschel CC, Birnstiel ML: The organization and expression of histone gene families. Cell 25: 301–313 (1981).Google Scholar
  42. 41.
    Hinnebusch AG: Translational control of GCN4: an in vivo barometer of initiation-factor activity. Trends Biochem Sci 19: 409–414 (1994).Google Scholar
  43. 42.
    Jagus R, Anderson WF, Safer B: The regulation of initiation of mammalian protein synthesis. Prog Nucl Acids Res Mol Biol 25: 127–185 (1981).Google Scholar
  44. 43.
    Jobling SA, Cuthbert CM, Rogers SG, Fraley RT, Gehrke L: In vitro transcription and translational efficiency of chimeric SP6 messenger RNAs devoid of 5′ vector nucleotides. Nucl Acids Res 16: 4483–4498 (1988).Google Scholar
  45. 44.
    Jobling SA, Gehrke L: Enhanced translation of chimaeric messenger RNAs containing a plant viral untranslated leader sequence. Nature 325: 622–625 (1987).Google Scholar
  46. 45.
    Joshi CP: An inspection of the domain between putative TATA box and translation start site in 79 plant genes. Nucl Acids Res 16: 6643–6653 (1987).Google Scholar
  47. 46.
    Joshi CP, Nguyen HT: 5′ untranslated leader sequences of eukaryotic mRNAs encoding heat shock induced proteins. Nucl Acids Res 23: 541–549 (1995).Google Scholar
  48. 47.
    Key JL, Lin CY, Chen YM: Heat shock proteins of higher plants. Proc Natl Acad Sci USA 78: 3526–3530 (1981).Google Scholar
  49. 48.
    Kim J-K, Hollingsworth MJ: Localization of in vivo ribosome pause sites. Anal Biochem 206: 183–188 (1992).Google Scholar
  50. 49.
    Kim J, Klein PG, Mullet JE: Ribosomes pause at specific sites during synthesis of membrane-bound chloroplast reaction center protein D1. J Biol Chem 266: 14931–14938 (1991).Google Scholar
  51. 50.
    Koning AJ, Tanimoto EY, Kiehne K, Rost T, Comai L: Cell-specific expression of plant histone H2A genes. Plant Cell 3: 657–665 (1991).Google Scholar
  52. 51.
    Kozak M: Influences of mRNA secondary structure on initiation by eukaryotic ribosomes. Proc Natl Acad Sci USA 83: 2850–2854 (1986).Google Scholar
  53. 52.
    Kozak M: Circumstances and mechanisms of inhibition of translation by secondary structure in eucaryotic mRNAs. Mol Cell Biol 9: 5134–5142 (1989).Google Scholar
  54. 53.
    Kozak M: A short leader sequence impairs the fidelity of initiation by eukaryotic ribosomes. Gene Expression 1: 111–115 (1991).Google Scholar
  55. 54.
    Lamphear BJ, Panniers R: Heat shock impairs the interaction of cap-binding protein complex with 5′ mRNA cap. J Biol Chem 266: 2789–2794 (1991).Google Scholar
  56. 55.
    Leicht BG, Biessmann H, Palter KB, Bonner JJ: Small heat shock proteins of Drosophila associate with the cytoskeleton. Proc Natl Acad Sci USA 83: 90–94 (1986).Google Scholar
  57. 56.
    Leathers V, Tanguay R, Kobayashi M, Gallie DR: A phylogenetically conserved sequence within viral 3′ untranslated RNA pseudoknots regulates translation. Mol Cell Biol 13: 5331–5347 (1993).Google Scholar
  58. 57.
    Lee SW, Heinz R, Robb J, Nazar RN: Differential utilization of alternate initiation sites in a plant defense gene responding to environmental stimuli. Eur J Biochem 226: 109–114 (1994).Google Scholar
  59. 58.
    Levine BJ, Chodchoy N, Marzluff WF, Skoultchi AI: Coupling of replication type histone mRNA levels to DNA synthesis requires the stem-loop sequence at the 3′ end of the mRNA. Proc Natl Acad Sci USA 84: 6189–6193 (1987).Google Scholar
  60. 59.
    Levis C, Astier-Manifacier S: The 5′ untranslated region of PVY RNA even located in an internal position enables initiation of translation. Virus Genes 7: 367–379 (1993).Google Scholar
  61. 60.
    Lingelbach K, Dobberstein B: An extended RNA/RNA duplex structure within the coding region of mRNA does not block translational elongation. Nucl Acids Res 16: 3405–3414 (1988).Google Scholar
  62. 61.
    Lindquist S: The heat shock response. Annu Rev Biochem 55: 1151–1191 (1986).Google Scholar
  63. 62.
    Lohmer S, Maddaloni M, Motto M, Salamini F, Thompson RD: Translation of the mRNA of the maize transcriptional activator Opaque-2 is inhibited by upstream open reading frames present in the leader sequence. Plant Cell 5: 65–73 (1993).Google Scholar
  64. 63.
    Marzluff WF: Histone 3′ ends: essential and regulatory fuctions. Gene Exp 2: 93–97 (1992).Google Scholar
  65. 64.
    Melin L, Soldati D, Mital R, Streit A, Schumperli D: Biochemical demonstration of complex formation of histone pre-mRNA with U7 small nuclear ribonucleoprotein and hairpin binding factors. EMBO J 11: 691–697 (1992).Google Scholar
  66. 65.
    Michelet B, Lukaszewicz M, Dupriez V, Boutry M: A plant plasma membrane protein-ATPase gene is regulated by development and environment and shows signs of a translational regulation. Plant Cell 6: 1375–1389 (1994).Google Scholar
  67. 66.
    Millar AJ, Short SR, Hiratsuka K, Chua N-C, Kay SA: Firefly luciferase as a reporter of regulated gene expression in higher plants. Plant Mol Biol Rep 10: 324–337 (1992).Google Scholar
  68. 67.
    Millar AJ, Carre IA, Strayer CA, Chua N-C, Kay SA: Circadian clock mutants in Arabidopsis identified by luciferase imaging. Sci 267: 1161–1163 (1995).Google Scholar
  69. 68.
    Mowry KL, Oh R, Steitz JA: Each of the conserved sequence elements flanking the cleavage site of mammalian histone pre-mRNAs has a distinct role in the 3′-end processing reaction. Mol Cell Biol 9: 3105–3108 (1989).Google Scholar
  70. 69.
    Mowry KL, Steitz JA: Both conserved signals on mammalian histone pre-mRNAs associate with small nuclear ribonucleo-proteins during 3′-end formation in vitro. Mol Cell Biol 7: 1663–1672 (1987).Google Scholar
  71. 70.
    Mowry KL, Steitz JA: Identification of the human U7 snRNP as one of several factors involved in the 3′-end maturation of histone premessenger RNA's. Science 238: 1682–1687 (1987).Google Scholar
  72. 71.
    Muller K, Lindauer A, Bruderlein M, Schmitt R: Organization and transcription of Volvox histone-encoding genes: similarities between algal and animal genes. Gene 93: 167–175 (1990).Google Scholar
  73. 72.
    Muller K, Schmitt R: Histone genes of Volvox carteri: DNA sequence and organization of two H3-H4 gene loci. Nucl Acids Res 16: 4121–4136 (1988).Google Scholar
  74. 73.
    Murtha-Riel P, Davies MV, Scherer BJ, Choi S-Y, Hershey JWB, Kaufman RJ: Expression of a phosphorylation-resistant eukaryotic initiation factor 2 α-subunit mitigates heat shock inhibition of protein synthesis. J Biol Chem 268: 12946–12951 (1993).Google Scholar
  75. 74.
    Nicolaisen M, Johansen E, Poulsen GP, Borkhardt B: The 5′ untranslated region from pea seedborne mosaic potyvirus RNA as a translational enhancer in pea and tobacco protoplasts. FEBS Lett 303: 169–172 (1992).Google Scholar
  76. 75.
    Nover L, Scharf K-D, Neumann D: Formation of cytoplasmic heat shock granules in tomato cell cultures and leaves. Mol Cell Biol 3: 1648–1655 (1983).Google Scholar
  77. 76.
    Nover L, Scharf K-D, Neumann D: Cytoplasmic heat shock granules are formed from precursor particles and are associated with a specific set of mRNAs. Mol Cell Biol 9: 1298–1308 (1989).Google Scholar
  78. 77.
    Oliver MJ, Bewley JD: Plant desiccation and protein synthesis. V. Stability of poly(A)- and poly(A)+ RNA during desiccation and their synthesis upon rehydration in the desiccation-tolerant moss Tortula ruralis and the intolerant moss Cratoneuron filicinum. Plant Physiol 74: 917–922 (1984).Google Scholar
  79. 78.
    Oliver MJ, Bewley JD: Plant desiccation and protein synthesis. VI. Changes in protein synthesis elicited by desiccation of the moss Tortula ruralis are effected at the translational level. Plant Physiol 74: 923–927 (1984).Google Scholar
  80. 79.
    Oliver MJ: Influence of protoplasmic water loss on the control of protein synthesis in the desiccation-tolerant moss Tortula ruralis. Plant Physiol 97: 1501–1511 (1991).Google Scholar
  81. 80.
    Pandey NB, Marzluff WF: The stem-loop Structure at the 3′ end of histone mRNA is necessary and sufficient for regulation of histone mRNA stability. Mol Cell Biol 7: 4557–4559 (1987).Google Scholar
  82. 81.
    Pandey NB, Sun J-H, Marzluff WF: Different complexes are formed on the 3′ end of histone mRNA with nuclear and polysomal proteins. Nucl Acids Res 19: 5653–5659 (1991).Google Scholar
  83. 82.
    Pandey NB, Williams AS, Sun J-H, Brown VD, Bond U, Marzluff WF: Point mutations in the stem-loop at the 3′ end of mouse histone mRNA reduce expression by reducing the efficiency of 3′ end formation. Mol Cell Biol 14: 1709–1720 (1994).Google Scholar
  84. 83.
    Panniers R, Stewart EB, Merrick WC, Henshaw EC: Mechanism of inhibition of polypeptide chain initiation in heatshocked Ehrlich cells involves reduction of eukaryotic initiation factor 4F activity. J Biol Chem 260: 9648–9653 (1985).Google Scholar
  85. 84.
    Pelletier J, Sonenberg N: Insertion mutagenesis to increase secondary structure within the 5′ noncoding region of a eukaryotic mRNA reduces translational efficiency. Cell 40: 515–526 (1985).Google Scholar
  86. 85.
    Pitto L, Gallie DR, Walbot V: The role of the leader sequence during thermal repression of translation in maize, tobacco, and carrot protoplasts. Plant Physiol 100: 1827–1833 (1992).Google Scholar
  87. 86.
    Pooggin MM, Skryabin KG: The 5′-untranslated leader of potato virus X RNA enhances the expression of a heterologous gene in vivo. Mol Gen Genet 234: 329–331 (1992).Google Scholar
  88. 87.
    Putterill JJ, Gardner RC: Initiation of translation of the β-glucuronidase reporter gene at internal AUG codons in plant cells. Plant Sci 62: 199–205 (1989).Google Scholar
  89. 88.
    Robbins E, Borun TW: The cytoplasmic synthesis of histones in HeLa cells and its temporal relationship to DNA replication. Proc Natl Acad Sci USA 58: 1977–1983 (1967).Google Scholar
  90. 89.
    Rozen F, Edery I, Meerovitch K, Dever TE, Merrick WC, Sonenberg N: Bidirectional RNA helicase activity of eucaryotic translation initiation factors 4A and 4F. Mol Cell Biol 10: 1134–1144 (1990).Google Scholar
  91. 90.
    Sachs MM, Freeling M, Okimoto R: The anaerobic proteins of maize. Cell 20: 761–767 (1980).Google Scholar
  92. 91.
    Scholthof HB, Wu FC, Gowda S, Shepard RJ: Regulation of cauliflower gene expression and the involvement of cis-acting elements on both viral transcripts. Virology 190: 403–412 (1992).Google Scholar
  93. 92.
    Scott HB, Oliver MJ: Accumulation and polysomal recruitment of transcripts in response to dessication and rehydration of the moss Tortula ruralis. J Exp Bot 45: 577–583 (1994).Google Scholar
  94. 93.
    Shaul O, Galili G: Increased lysine synthesis in tobacco plants that express high levels of bacterial dihydrodipicolinate synthase in their chloroplasts. Plant J 2: 203–209 (1992).Google Scholar
  95. 94.
    Stollar NE, Kim J-K, Hollingsworth MJ: Ribosomes pause during the expression of the large ATP synthase gene cluster in spinach chloroplasts. Plant Physiol 105: 1167–1177 (1994).Google Scholar
  96. 95.
    Storti RV, Scott MP, Rich A, Pardue ML: Translational control of protein synthesis in response to heat shock in D. melanogaster cells. Cell 22: 825–834 (1980).Google Scholar
  97. 96.
    Tacke E, Prufer D, Salamini F, Rohde W: Characterization of a potato leafroll luteovirus subgenomic RNA: differential expression by internal translation initiation and UAG suppression. J Gen Virol 71: 2265–2272 (1990).Google Scholar
  98. 96a.
    Tanguay RL, Gallie DR: Isolation and characterization of the 102-kilodalton RNA-binding protein that binds to the 5′ and 3′ translational enhancers of tobacco mosaic virus RNA. J Biol Chem, in press (1996).Google Scholar
  99. 97.
    Thomas AAM, Ter Haar E, Wellink J, Voorma HO: Cowpea mosaic virus middle component RNA contains a sequence that allows internal binding of ribosomes and that requires eukaryotic initiation factor 4F for optimal translation. J Virol 65: 2953–2959 (1991).Google Scholar
  100. 98.
    Timmer RT, Benkowski LA, Schodin D, Lax SR, Metz AM, Ravel JM, Browning KS: The 5′ and 3′ untranslated regions of satellite tobacco necrosis virus RNA affect translational efficiency and dependence on a 5′ cap structure. J Biol Chem 268: 9504–9510 (1993).Google Scholar
  101. 99.
    Turner R, Bate N, Twell D, Foster GD: Analysis of a translational enhancer upstream from the coat protein open reading frame of potato virus S. Arch Virol 134: 321–333 (1994).Google Scholar
  102. 100.
    Vasserot AP, Schaufele FJ, Birnstiel ML: Conserved terminal hairpin sequences of histone mRNA precursors are not involved in duplex formation with the U7 RNA but act as a target site for a distinct processing factor. Proc Natl Acad Sci USA 86: 4345–4349 (1989).Google Scholar
  103. 101.
    Verver J, LeGall O, van Kammen A, Wellink J: The sequence between nucleotides 161 and 512 of cowpea mosaic virus M RNA is able to support internal initiation of translation in vitro. J Gen Virol 72: 2339–2345 (1991).Google Scholar
  104. 102.
    Wang S, Miller WA: A sequence located 4.5 to 5 kilobases from the 5′ end of the barley yellow dwarf virus (PAV) genome strongly stimulates translation of uncapped mRNA. J Biol Chem 270: 13446–13452 (1995).Google Scholar
  105. 103.
    Webster C, Gaut RL, Browning KS, Ravel JM, Roberts JKM: Hypoxia enhances phosphorylation of eukaryotic initiation factor 4A in maize root tips. J Biol Chem 266: 23341–23346 (1991).Google Scholar
  106. 104.
    Williams AS, IngledueIII TC, Kay BK, Marzluff WF: Changes in the stem-loop at the 3′ terminus of histone mRNA affects its nucleocytoplasmic transport and cytoplasmic regulation. Nucl Acids Res 22: 4660–4666 (1994).Google Scholar
  107. 105.
    Williams AS, Marzluff WF: The sequence of the stem and flanking sequences at the 3′ end of histone mRNA are critical determinants for the binding of the stem-loop binding protein. Nucl Acids Res 23: 654–662 (1995).Google Scholar
  108. 106.
    Wolin S, Walter P: Ribosome pausing and stacking during translation of a eukaryotic mRNA. EMBO J 7: 3559–3569 (1988).Google Scholar
  109. 107.
    Wu S-C, Gyorgyey J, Dudits D: Polyadenylated H3 histone transcripts and H3 histone variants in alfalfa. Nucl Acids Res 17: 3057–3063 (1989).Google Scholar
  110. 108.
    Zapata JM, Maroto FG, Sierra JM: Inactivation of mRNA cap-binding Protein complex in Drosophila melanogaster embryos under heat shock. J Biol Chem 266: 16007–16014 (1991).Google Scholar
  111. 109.
    Zelenina DA, Kulaeva OI, Smirnyagina EV, Solovyev AG, Miroshnichenko NA, Fedorkin ON, Rodionova NP, Morozov SY, Atabekov JG: Translation enhancing properties of the 5′-leader of potato virus X genomic RNA. FEBS Lett 296: 267–270 (1992).Google Scholar

Copyright information

© Kluwer Academic Publishers 1996

Authors and Affiliations

  • Daniel R. Gallie
    • 1
  1. 1.Department of BiochemistryUniversity of CaliforniaRiversideUSA

Personalised recommendations