Control of mRNA stability in higher plants

Plant Molecular Biology

Volumn 32, Issue 1-2, 1996, Pages 63-78

  Abler, Michael L ^a   Green, Pamela J ^a  

^a Michigan State University ^*  (United States)

Author keywords

instability sequences; mRNA decay mechanisms; mRNA degradation; mRNA half life measurements; mRNA turnover; RNA binding proteins; translation

Indexed keywords

EID: 0030267492     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF00039377     Document Type: Article

References (100)

1. Bariola PA, Green PJ: Plant Ribonucleases. In: Riordan JF, D'Alessio G (eds) Ribonucleases: Structure and Function, Academic Press, Orlando, FL (1996), In press.
2. Belanger FC, Brodl MR, Ho TD: Heat shock causes destabilization of specific mRNAs and destruction of endoplasmic reticulum in barley aleurone cells. Proc Natl Acad Sci USA 83: 1354-1358 (1986).
3. Belostotsky DA, Meagher RB: Differential organ-specific expression of three poly(A)-binding-protein genes from Arabidopsis thaliana. Proc Natl Acad Sci USA 90: 6686-6690 (1993).
4. Binder R, Horowitz JA, Basilion JP, Koeller DM, Klausner RD, Harford JB: Evidence that the pathway of transferrin receptor mRNA degradation involves an endonucleolytic cleavage within the 3′ UTR and does not involve poly(A) tail shortening. EMBO J 13: 1969-1980 (1994).
5. Bourque JE: Antisense strategies for genetic manipulations in plants. Plant Sci 105: 125-149 (1995).
6. Brock ML, Shapiro DJ: Estrogen stabilizes vitellogenin mRNA against cytoplasmic degradation. Cell 34: 207-214 (1983).
7. Brodl MR, Ho TD: Heat shock causes selective destabilization of secretory protein mRNAs in barley aleurone cells. Plant Physiol 96: 1048-1052 (1991).
8. Brodl MR, Ho TD: Heat shock in mechanically wounded carrot root disks causes destabilization of stable secretory protein mRNA and dissociation of endoplasmic reticulum lamellae. Physiol Plant 86: 253-262 (1992).
9. Byrne DH, Seeley KA, Colbert JT: Half-lives of oat mRNAs in vivo and in a polysome-based in-vitro system. Planta 189: 249-256 (1993).
10. Caponigro G, Parker R: Multiple functions for poly (A)-binding protein in mRNA decapping and deadenylation in yeast. Genes Devel 9: 2421-2432 (1995).
11. De Rocher EJ, Bohnert HJ: Development and environmental stress employ different mechanisms in the expression of a plant gene family. Plant Cell 5: 1611-1625 (1993).
12. Dean C, Favreau M, Bond-Nutter D, Bedbrook J, Dunsmuir P: Sequences downstream of translation start regulate quantitative expression of two petunia rbcS genes. Plant Cell 1: 201-208 (1989).
13. Decker CJ, Parker R: A turnover pathway for both stable and unstable mRNAs in yeast: evidence for a requirement for deadenylation. Genes Devel 7: 1632-1643 (1993).
14. Decker CJ, Parker R: Mechanisms of mRNA degradation in eukaryotes. Trends Biochem Sci 19: 336-340 (1994).
15. Dickey LF, Gallo-Meagher M, Thompson WF: Light regulatory sequences are located within the 5′ portion of the Fed-1 message sequence. EMBO J 11: 2311-2317 (1992).
16. Dickey LF, Nguyen T-T, Allen GC, Thompson WF: Light modulation of ferredoxin mRNA abundance requires an open reading frame. Plant Cell 6: 1171-1176 (1994).
17. Diehn SH, De Rocher EJ, Green PJ: Problems that can limit the expression of foreign genes in plants: lessons to be learned from B.t. toxin genes. In: Setlow JK (ed) Genetic Engineering: Principles and Methods, Plenum Press, New York (1996), In press.
18. Dietrich RA, Radke SE, Harada JJ: Downstream DNA sequences are required to activate a gene expressed in the root cortex of embryos and seedlings. Plant Cell 4: 1371-1382 (1992).
19. Flores S, Tobin EM: Cytokinin modulation of LHCP mRNA levels: the involvement of post-transcriptional regulation. Plant Mol Biol 11: 409-415 (1988).
20. Franco AR, Gee MA, Guilfoyle TJ: Induction and superinduction of auxin-responsive mRNAs with auxin and protein synthesis inhibitors. J Biol Chem 265: 15845-15849 (1990).
21. Fritz CC, Herget T, Wolter FP, Schell J, Schreier PH: Reduced steady-state levels of rbcS mRNA in plants kept in the dark are due to differential degradation. Proc Natl Acad Sci USA 88: 4458-4462 (1991).
22. Fu H, Kim SY, Park WD: High-level tuber expression and sucrose inducibility of a potato Sus4 sucrose synthase gene require 5′ and 3′ flanking sequences and the leader intron. Plant Cell 7: 1387-1394 (1995).
23. Gallie DR: The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes Devel 5: 2108-2116 (1991).
24. Gallie DR: Posttranscriptional regulation of gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 44: 77-105 (1993).
25. Gallie DR, Feder JN, Schimke RT, Walbot V: Postranscriptional regulation in higher eukaryotes: the role of the reporter gene in controlling expression. Mol Gen Genet 228: 258-264 (1991).
26. 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).
27. Gil P, Green PJ. Multiple regions of the Arabidopsis SAUR-AC1 gene control transcript abundance: the 3′ untranslated region functions as an mRNA instability determinant. EMBO J 15: 1678-1686 (1996).
28. Gil P, Liu Y, Orbovic V, Verkamp E, Poff KL, Green PJ: Characterization of the auxin-inducible SAUR-AC1 gene for use as a molecular genetic tool in Arabidopsis. Plant Physiol 104: 777-784 (1994).
29. Gossen M, Bujard H: Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc Natl Acad Sci USA 89: 5547-5551 (1992).
30. Green PJ: Control of mRNA stability in higher plants. Plant Physiol 102: 1065-1070 (1993).
31. Green PJ: The ribonucleases of higher plants. Annu Rev Plant Physiol Plant Mol Biol 45: 421-445 (1994).
32. Greenberg JR: High stability of messenger RNA in growing cultured cells. Nature 240: 102-104 (1972).
33. Greenberg ME, Belasco JG: Control of the decay of labile protooncogene and cytokine mRNAs. In: Belasco JG, Brawerman G (eds) Control of Messenger RNA Stability, pp. 199-218. Academic Press, San Diego, CA (1993).
34. Hargrove JL, Hulsey MG, Beale EG: The kinetics of mammalian gene expression. BioEssays 13: 667-674 (1991).
35. Higgs DC, Barnes LJ, Colbert JT: Abundance and half-life of the distinct oat phytochrome A3 and A4 mRNAs. Plant Mol Biol 29: 367-377 (1995).
36. Higgs DC, Colbert JT: Oat phytochrome A mRNA degradation appears to occur via two distinct pathways. Plant Cell 6: 1007-1019 (1994).
37. Hilson P, Carroll KL, Masson PH: Molecular characterization of PAB2, a member of the multigene family coding for poly(A)-binding proteins in Arabidopsis thaliana. Plant Physiol 103: 525-533 (1993).
38. Ho TD: On the mechanism of hormone controlled enzyme formation in barley aleurone layers. Ph.D. thesis, Michigan State University, East Lansing, MI (1976).
39. Ho TD, Varner JE: Response of barley aleurone layers to abscisic acid. Plant Physiol 57: 175-178 (1976).
40. Hoekema A, Kastelein RA, Yasser M, DeBoer HA: Codon replacement in the PGK1 gene of Saccharomyces cerevisiae: experimental approach to study the role of biased codon usage in gene expression. Mol Cell Biol 7: 2914-2924 (1987).
41. Hsu CL, Stevens A: Yeast cells lacking 5′ → 3′ exoribonuclease 1 contain mRNA species that are poly(A) deficient and partially lack the 5′ cap structure. Mol Cell Biol 13: 4826-4835 (1993).
42. Ingelbrecht IW, Herman LMF, Dekeyser RA, Van Montagu MC, Depicker AG: Different 3′ end regions strongly influence the level of gene expression in plant cells. Plant Cell 1: 671-680 (1989).
43. Jiang C-Z, Kliebenstein D, Ke N, Rodermel S: Destabilization of rbcS sense transcripts by antisense RNA. Plant Mol Biol 25: 569-576 (1994).
44. Jofuku KD, Schipper RD, Goldberg RB: A frameshift mutation prevents Kunitz trypsin inhibitor mRNA accumulation in soybean embryos. Plant Cell 1: 427-435 (1989).
45. Koshiba T, Ballas N, Wong LM, Theologis A: Transcriptional regulation of PS-IAA4/5 and PS-IAA6 early gene expression by indoleacetic acid and protein synthesis inhibitors in pea (Pisum sativum). J Mol Biol 253: 396-413 (1995).
46. Lagnado CA, Brown CY, Goodall GJ: AUUUA is not sufficient to promote poly(A) shortening and degradation of an mRNA: the functional sequence within AU-rich elements may be UUAUUUA(U/A)(U/A). Mol Cell Biol 14: 7984-7995 (1994).
47. Larkin JC, Oppenheimer DG, Pollock S, Marks MD: Arabidopsis GLABROUS1 gene requires downstream sequences for function. Plant Cell 5: 1739-1748 (1993).
48. Lincoln JE, Fischer RL: Diverse mechanisms for the regulation of ethylene-inducible gene expression. Mol Gen Genet 212: 71-75 (1988).
49. Lowell JE, Rudner DZ, Sachs AB: 3′-UTR-dependent deadenylation by the yeast poly(A) nuclease. Genes Devel 6: 2088-2099 (1992).
50. Marcotte WRJ, Russell SH, Quatrano RS: Abscisic acid-responsive sequences from the Em gene of wheat. Plant Cell 1: 969-976 (1989).
51. Margossian LJ, Federman AD, Giovannoni JJ, Fischer RL: Ethylene-regulated expression of a tomato fruit ripening gene encoding a proteinase inhibitor I with a glutamic residue at the reactive site. Proc Natl Acad Sci USA 85: 8012-8016 (1988).
52. McClure BA, Hagen G, Brown CS, Gee MA, Guilfoyle TJ: Transcription, organization, and sequence of an auxin-regulated gene cluster in soybean. Plant Cell 1: 229-239 (1989).
53. Muhlrad D, Decker CJ, Parker R: Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 5′ → 3′ digestion of the transcript. Genes Devel 8: 855-866 (1994).
54. Muhlrad D, Parker R: Mutations affecting stability and deadenylation of the yeast MFA2 transcript. Genes Devel 6: 2100-2111 (1992).
55. Muhlrad D, Parker R: Premature translational termination triggers mRNA decapping. Nature 370: 578-581 (1994).
56. Murray EE, Rocheleau T, Eberle M, Stock C, Sekar V, Adang M: Analysis of unstable RNA transcripts of insecticidal crystal protein genes of Bacillus thuringiensis in transgenic plants and electroporated protoplasts. Plant Mol Biol 16: 1035-1050 (1991).
57. Newman TC, Ohme-Takagi M, Taylor CB, Green PJ: DST sequences, highly conserved among plant SAUR genes, target reporter transcripts for rapid decay in tobacco. Plant Cell 5: 701-714(1993).
58. Nolan RC, Ho TD: Hormonal regulation of α-amylase expression in barley aleurone layers. Plant Physiol 88: 588-593 (1988).
59. Nolan RC, Ho TD: Hormonal regulation of gene expression in barley aleurone layers. Planta 174: 551-560 (1988).
60. Ohme-Takagi M, Taylor CB, Newman TC, Green PJ: The effect of sequences with high AU content on mRNA stability in tobacco. Proc Natl Acad Sci USA 90: 11811-11815 (1993).
61. Or E, Boyer SK, Larkins BA: opaque2 modifiers act posttranscriptionally and in a polar manner on-zein gene expression in maize endosperm. Plant Cell 5: 1599-1609 (1993).
62. Peltz SW, Brewer G, Bernstein P, Hart PA, Ross J: Regulation of mRNA turnover in eukaryotic cells. Crit Rev Euk Gene Exp 1: 99-126 (1991).
63. Peltz SW, He F, Welch E, Jacobson A: Nonsense-mediated mRNA decay in yeast. Prog Nucl Acid Res Mol Biol 47: 271-298 (1994).
64. Peters JL, Silverthorne J: Organ-specific stability of two Lemna rbcS mRNAs is determined primarily in the nuclear compartment. Plant Cell 7: 131-140 (1995).
65. Pulak R, Anderson P: mRNA surveillance by the Caenorhabditis elegans smg genes. Genes Devel 7: 1885-1897 (1993).
66. Ross J: mRNA stability in mammalian cells. Microbiol Rev 59: 423-150 (1995).
67. Sachs AB: Messenger RNA degradation in eukaryotes. Cell 74: 413-421 (1993).
68. Sachs AB, Deardorff JA: Translation initiation requires the PAB-dependent poly(A) ribonuclease in yeast. Cell 70: 961-973 (1992).
69. Seeley KA, Byrne DH, Colbert JT: Red light-independent instability of oat phytochrome mRNA in vivo. Plant Cell 4: 29-38 (1992).
70. Sheu J-J, Jan S-P, Lee H-T, Yu S-M: Control of transcription and mRNA turnover as mechanisms of metabolic repression of α-amylase gene expression. Plant J 5: 655-664 (1994).
71. Shirley BW, Meagher RB: A potential role for RNA turnover in the light regulation of plant gene expression: ribulose-1,5-bisphosphate carboxylase small subunit in soybean. Nucl Acids Res 18: 3377-3385 (1990).
72. Shyu A-B, Belasco JG, Greenberg ME: Two distinct destabilizing elements in the c-fos message trigger deadenylation as a first step in rapid mRNA decay. Genes Devel 5: 221-231 (1991).
73. Shyu A-B, Greenberg ME, Belasco JG: The c-fos transcript is targeted for rapid decay by two distinct mRNA degradation pathways. Genes Dev 3: 60-72 (1989).
74. Siflow CD, Key JL: Stability of polysome-associated polyadenylated RNA from soybean suspension culture cells. Biochemistry 18: 1013-1018 (1979).
75. Silverthorne J, Tobin EM: Post-transcriptional regulation of organ-specific expression of individual rbcS mRNAs in Lemna gibba. Plant Cell 2: 1181-1190 (1990).
76. Sullivan ML, Green PJ: Post-transcriptional regulation of nuclear-encoded genes in higher plants: the roles of mRNA stability and translation. Plant Mol Biol 23: 1091-1104 (1993).
77. Surdej P, Riedl A, Jacobs-Lorena M: Regulation of mRNA stability in development. Annu Rev Genet 28: 263-282 (1994).
78. Tanzer MM, Meagher RB: Faithful degradation of soybean rbcS mRNA in vitro. Mol Cell Biol 14: 2640-2650 (1994).
79. Tanzer MM, Meagher RB: Degradation of the soybean ribulose-1,5-bisphosphate carboxylase small-subunit mRNA, SRS4, initiates with endonucleolytic cleavage. Mol Cell Biol 15: 6641-6652 (1995).
80. Taylor CB, Green PJ: Identification and characterization of genes with unstable transcripts (GUTs) in tobacco. Plant Mol Biol 28: 27-38 (1995).
81. Thompson DM, Meagher RB: Transcriptional and posttranscriptional processes regulate expression of RNA encoding the small subunit of ribulose-1,5-bisphosphate carboxylase differently in petunia and in soybean. Nucl Acids Res 18: 3621-3629 (1990).
82. Thompson DM, Tanzer MM, Meagher RB: Degradation products of the mRNA encoding the small subunit of ribulose-1,5-bisphosphate carboxylase in soybean and transgenic petunia. Plant Cell 4: 47-58 (1992).
83. Thompson WF, White MJ: Physiological and molecular studies of light-regulated nuclear genes in higher plants. Annu Rev Plant Physiol Plant Mol Biol 42: 423-466 (1991).
84. Thornburg RW, An G, Cleveland TE, Johnson R, Ryan CA: Wound-inducible expression of a potato inhibitor II-chloramphenicol acetyltransferase gene fusion in transgenic tobacco plants. Proc Natl Acad Sci USA 84: 744-748 (1987).
85. Vancanneyt G, Rosahl S, Willmitzer L: Translatability of a plant-mRNA strongly influences its accumulation in transgenic plants. Nucl Acids Res 18: 2917-2921 (1990).
86. 85a. Van Hoof A, Green PJ: Premature nonsense codons decrease the stability of phytophemagglutinin mRNA in a position-dependent manner. Plant J, in press.
87. Vierling E: The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42: 579-620 (1991).
88. Voelker TA, Moreno J, Chrispeels MJ: Expression analysis of a pseudogene in transgenic tobacco: a frameshift mutation prevents mRNA accumulation. Plant Cell 2: 255-261 (1990).
89. Voelker TA, Staswick P, Chrispeels MJ: Molecular analysis of two phytohemagglutinin genes and their expression in Phaseolus vulgaris cv. Pinto, a lectin-deficient cultivar of the bean. EMBO J 5: 3075-3082 (1986).
90. Vorst O, Van Dam F, Weisbeek P, Smeekens S: Light-regulated expression of the Arabidopsis thaliana ferredoxin A gene involves both transcriptional and post-transcriptional processes. Plant J 3: 793-803 (1993).
91. Walker EL, Weeden NF, Taylor CB, Green PJ, Coruzzi GM. Molecular evolution of duplicate copies of genes encoding cytosolic glutamine synthetase in Pisum sativum. Plant Mol Biol 29: 1111-1125 (1996).
92. Weinmann P, Gossen M, Hillen W, Bujard H, Gatz C: A chimeric transactivator allows tetracycline-responsive gene expression in whole plants. Plant J 5: 559-569 (1994).
93. Weiss IM, Liebhaber SA: Erythroid cell-specific mRNA stability elements in the α2-globin 3′ nontranslated region. Mol Cell Biol 15: 2457-2465 (1995).
94. Williamson JD, Quatrano RS: ABA-regulation of two classes of embryo-specific sequences in mature wheat embryos. Plant Physiol 86: 208-215 (1988).
95. Wolfraim LA, Langis R, Tyson H, Dhindsa RS: cDNA sequence, expression, and transcript stability of a cold acclimation-specific gene, cas18, ofalfalfa (Medicago falcata) cells. Plant Physiol 101: 1275-1282 (1993).
96. Yamamoto KT, Mori H, Imaseki H: cDNA cloning of indole-3-acetic acid-regulated genes: Aux22 and SAUR from mung bean (Vigna radiata) hypocotyl tissue. Plant Cell Physiol 33: 93-97 (1992).
97. Yang J, Hunt AG: Immunological characterization of plant polyadenylate-binding proteins. Plant Sci 99: 161-170 (1994).
98. Zhang S, Mehdy MC: Binding of a 50-kD protein to a U-rich sequence in an mRNA encoding a proline-rich protein that is destabilized by fungal elicitor. Plant Cell 6: 135-145 (1994).
99. Zhang S, Sheng J, Liu Y, Mehdy MC: Fungal elicitor-induced bean proline-rich protein mRNA down-regulation is due to destabilization that is transcription and translation dependent. Plant Cell 5: 1089-1099 (1993).
100. Zubiaga AM, Belasco JG, Greenberg ME: The nonamer UUAUUUAUU is the key AU-rich sequence motif that mediates mRNA degradation. Mol Cell Biol 15: 2219-2230 (1995).