Posttranscriptional control of photosynthetic mRNA decay under stress conditions requires 3′ and 5′ untranslated regions and correlates with differential polysome association in rice

Plant Physiology

Volumn 159, Issue 3, 2012, Pages 1111-1124

  Park, Su Hyun ^a   Chung, Pil Joong ^a,b   Juntawong, Piyada ^c   Bailey Serres, Julia ^c   Kim, Youn Shic ^a   Jung, Harin ^a   Bang, Seung Woon ^a   Kim, Yeon Ki ^a   Choi, Yang Do ^d   Kim, Ju Kon ^a  

^a Myong Ji University   (South Korea)

^b ROCKEFELLER UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ORYZA SATIVA;

EID: 84863641060     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.194928     Document Type: Article

References (81)

1. An G, Mitra A, Choi HK, Costa MA, An K, Thornburg RW, Ryan CA (1989) Functional analysis of the 39 control region of the potato woundinducible proteinase inhibitor II gene Plant Cell 1: 115-122.
2. Anderson P, Kedersha N (2008) Stress granules: the Tao of RNA triage Trends Biochem Sci 33: 141-150.
3. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions Plant Physiol 141: 391-396.
4. Bailey-Serres J (1998) Selective translation of cytoplasmic mRNAs in plants Trends Plant Sci 4: 1360-1385.
5. Bailey-Serres J, Sorenson R, Juntawong P (2009) Getting the message across: cytoplasmic ribonucleoprotein complexes Trends Plant Sci 14: 443-453.
6. Balagopal V, Parker R (2009) Plysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs Curr Opin Plant Biol 21: 403-408.
7. Belostotsky DA, Sieburth LE (2009) Kill the messenger: mRNA decay and plant development Curr Opin Plant Biol 12: 96-102.
8. Bensen RJ, Boyer JS, Mullet JE (1988) Water deficit-induced changes in abscisic acid, growth, polysomes, and translatable RNA in soybean hypocotyls Plant Physiol 88: 289-294.
9. Bevilacqua A, Ceriani MC, Capaccioli S, Nicolin A (2003) Post-transcriptional regulation of gene expression by degradation of messenger RNAs J Cell Physiol 195: 356-372.
10. Bowler C, Benvenuto G, Laflamme P, Molino D, Probst AV, Tariq M, Paszkowski J (2004) Chromatin techniques for plant cells Plant J 39: 776-789.
11. Chaves MM (1991) Effects of water deficits on carbon assimilation J Exp Bot 42: 1-16.
12. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell Ann Bot (Lond) 103: 551-560.
13. Chaves MM, Oliveira MM (2004) Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture J Exp Bot 55: 2365-2384.
14. Chiba Y, Green PJ (2009) mRNA degradation machinery in plants J Plant Biol 52: 114-124.
15. Chiu WL, Niwa Y, Zeng W, Hirano T, Kobayashi H, Sheen J (1996) Engineered GFP as a vital reporter in plants Curr Biol 6: 325-330.
16. +-induced SOS1 mRNA stability in Arabidopsis Plant J 53: 554-565.
17. Chung PJ, Kim YS, Jeong JS, Park S-H, Nahm BH, Kim J-K (2009) The histone deacetylase OsHDAC1 epigenetically regulates the OsNAC6 gene that controls seedling root growth in rice Plant J 59: 764-776.
18. Claes B, Dekeyser R, Villarroel R, Van den Bulcke M, Bauw G, Van Montagu M, Caplan A (1990) Characterization of a rice gene showing organ-specific expression in response to salt stress and drought Plant Cell 2: 19-27.
19. Cohen A, Moses MS, Plant AL, Bray EA (1999) Multiple mechanisms control the expression of abscisic acid (ABA)-requiring genes in tomato plants exposed to soil water deficit Plant Cell Environ 22: 989-998.
20. Cushman JC, Michalowski CB, Bohnert HJ (1990) Developmental control of Crassulacean acid metabolism inducibility by salt stress in the common ice plant Plant Physiol 94: 1137-1142.
21. Dhindsa RS, Cleland RE (1975) Water stress and protein synthesis I Differential inhibition of protein synthesis Plant Physiol 55: 778-781.
22. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns Proc Natl Acad Sci USA 95: 14863-14868.
23. Feldbrügge M, Arizti P, Sullivan ML, Zamore PD, Belasco JG, Green PJ (2002) Comparative analysis of the plant mRNA-destabilizing element, DST, in mammalian and tobacco cells Plant Mol Biol 49: 215-223.
24. Flexas J, Bota J, Loreto F, Cornic G, Sharkey TD (2004) Diffusive and metabolic limitations to photosynthesis under drought and salinity in C (3) plants Plant Biol (Stuttg) 6: 269-279.
25. Flexas J, Diaz-Espejo A, Galmés J, Kaldenhoff R, Medrano H, Ribas-Carbo M (2007) Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves Plant Cell Environ 30: 1284-1298.
26. Gallie DR (1996) Translational control of cellular and viral mRNAs Plant Mol Biol 32: 145-158.
27. Gil P, Green PJ (1996) Multiple regions of the Arabidopsis SAUR-AC1 gene control transcript abundance: the 39 untranslated region functions as an mRNA instability determinant EMBO J 15: 1678-1686.
28. Gil P, Liu Y, Orbović V, Verkamp E, Poff KL, Green PJ (1994) Characterization of the auxin-inducible SAUR-AC1 gene for use as a molecular genetic tool in Arabidopsis Plant Physiol 104: 777-784.
29. Gray JC, Sullivan JA, Wang JH, Jerome CA, MacLean D (2003) Coordination of plastid and nuclear gene expression Philos Trans R Soc Lond B Biol Sci 358: 135-144, discussion 144-145.
30. Guhaniyogi J, Brewer G (2001) Regulation of mRNA stability in mammalian cells Gene 265: 11-23.
31. Gutierrez RA, Ewing RM, Cherry JM, Green PJ (2002) Identification of unstable transcripts in Arabidopsis by cDNA microarray analysis: rapid decay is associated with a group of touch- and specific clock-controlled genes Proc Natl Acad Sci USA 99: 11513-11518.
32. Higgs DC, Colbert JT (1994) Oat phytochrome A mRNA degradation appears to occur via two distinct pathways Plant Cell 6: 1007-1019.
33. Hsiao TC (1970) Rapid changes in levels of polyribosomes in Zea mays in response to water stress Plant Physiol 46: 281-285.
34. Hua XJ, Van de Cotte B, Van Montagu M, Verbruggen N (2001) The 59 untranslated region of the At-P5R gene is involved in both transcriptional and post-transcriptional regulation Plant J 26: 157-169.
35. Hughes TA (2006) Regulation of gene expression by alternative untranslated regions Trends Genet 22: 119-122.
36. Jang I-C, Choi W-B, Lee K-H, Song SI, Nahm BH, Kim J-K (2002) Highlevel and ubiquitous expression of the rice cytochrome c gene OsCc1 and its promoter activity in transgenic plants provides a useful promoter for transgenesis of monocots Plant Physiol 129: 1473-1481.
37. Jang I-C, Nahm BH, Kim J-K (1999) Subcellular targeting of green fluorescent protein to plastids in transgenic rice plants provides a high-level expression system Mol Breed 5: 453-461.
38. Jeong JS, Kim YS, Baek K-H, Jung H, Ha SH, Do Choi Y, Kim M, Reuzeau C, Kim J-K (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions Plant Physiol 153: 185-197.
39. Kawaguchi R, Bailey-Serres J (2005) mRNA sequence features that contribute to translational regulation in Arabidopsis Nucleic Acids Res 33: 955-965.
40. Kawaguchi R, Girke T, Bray EA, Bailey-Serres J (2004) Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana Plant J 38: 823-839.
41. Kawaguchi R, William AJ, Bray EA, Bailey-Serres J (2003) Water-deficitinduced translational control in Nicotiana tabacum Plant Cell Environ 26: 211-229.
42. Kim YM, Kim JK, Hwang YS (1994) Isolation and characterization of a rice fulllength cDNA clone encoding a polyubiquitin Plant Physiol 106: 791-792.
43. Kleine T, Voigt C, Leister D (2009) Plastid signalling to the nucleus: messengers still lost in the mists? Trends Genet 25: 185-192.
44. Koshiba T, Ballas N, Wong LM, Theologis A (1995) 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.
45. Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants Plant Cell Environ 25: 275-294.
46. Lidder P, Gutiérrez RA, Salomé PA, McClung CR, Green PJ (2005) Circadian control of messenger RNA stability: association with a sequencespecific messenger RNA decay pathway Plant Physiol 138: 2374-2385.
47. Liu J-H, Hill RD (1995) Post-transcriptional regulation of bifunctional a-amylase/subtilisin inhibitor expression in barley embryos by abscisic acid Plant Mol Biol 29: 1087-1091.
48. Mason HS, Mullet JE, Boyer JS (1988) Polysomes, messenger RNA, and growth in soybean stems during development and water-deficit Plant Physiol 86: 725-733.
49. Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals J Exp Bot 57: 1025-1043.
50. Mustroph A, Juntawong P, Bailey-Serres J (2009) Isolation of plant polysomal mRNA by differential centrifugation and ribosome immunopurification methods Methods Mol Biol Plant Syst Biol 553: 109-126.
51. Narsai R, Howell KA, Millar AH, O'Toole N, Small I, Whelan J (2007) Genome-wide analysis of mRNA decay rates and their determinants in Arabidopsis thaliana Plant Cell 19: 3418-3436.
52. Oh SJ, Kim YS, Kwon CW, Park HK, Jeong JS, Kim J-K (2009) Overexpression of the transcription factor AP37 in rice improves grain yield under drought conditions Plant Physiol 150: 1368-1379.
53. Ort DR (2001) When there is too much light Plant Physiol 125: 29-32.
54. Parker R, Sheth U (2007) P bodies and the control of mRNA translation and degradation Mol Cell 25: 635-646.
55. Peltz SW, Jacobson A (1992) mRNA stability: in trans-it Curr Opin Cell Biol 4: 979-983.
56. Pérez-Ortín JE, Alepuz PM, Moreno J (2007) Genomics and gene transcription kinetics in yeast Trends Genet 23: 250-257.
57. Redillas MC, Kim YS, Jeong JS, Strasser RJ, Kim J-K (2011) The use of JIP test to evaluate drought-tolerance of transgenic rice overexpressing OsNAC10 Plant Biotechnol Rep 5: 169-176.
58. Reznik B, Lykke-Andersen J (2010) Regulated and quality-control mRNA turnover pathways in eukaryotes Biochem Soc Trans 38: 1506-1510.
59. Rhodes PR, Matsuda K (1976) Water stress, rapid polyribosome reductions and growth Plant Physiol 58: 631-635.
60. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms Annu Rev Plant Biol 57: 675-709.
61. Ross J (1995) mRNA stability in mammalian cells Microbiol Rev 59: 423-450.
62. Sandoval J, Rodríguez JL, Tur G, Serviddio G, Pereda J, Boukaba A, Sastre J, Torres L, Franco L, López-Rodas G (2004) RNAPol-ChIP: a novel application of chromatin immunoprecipitation to the analysis of real-time gene transcription Nucleic Acids Res 32: e88.
63. Sathish P, Withana N, Biswas M, Bryant C, Templeton K, Al-Wahb M, Smith-Espinoza C, Roche JR, Elborough KM, Phillips JR (2007) Transcriptome analysis reveals season-specific rbcS gene expression profiles in diploid perennial ryegrass (Lolium perenne L.) Plant Biotechnol J 5: 146-161.
64. Seeley KA, Byrne DH, Colbert JT (1992) Red light-independent instability of oat phytochrome mRNA in vivo Plant Cell 4: 29-38.
65. + antiporter gene improves salt tolerance in Arabidopsis thaliana Nat Biotechnol 21: 81-85.
66. Shim J, Karin M (2002) The control of mRNA stability in response to extracellular stimuli Mol Cells 14: 323-331.
67. Sonenberg N, Hinnebusch AG (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets Cell 136: 731-745.
68. Stitt M, Gibon Y, Lunn JE, Piques M (2007) Multilevel genomics analysis of carbon signalling during low carbon availability: coordinating the supply and utilisation of carbon in a fluctuating environment Funct Plant Biol 34: 526-549.
69. Streatfield SJ (2007) Approaches to achieve high-level heterologous protein production in plants Plant Biotechnol J 5: 2-15.
70. Sullivan ML, Green PJ (1996) Mutational analysis of the DST element in tobacco cells and transgenic plants: identification of residues critical for mRNA instability RNA 2: 308-315.
71. Tanzer MM, Meagher RB (1994) Faithful degradation of soybean rbcS mRNA in vitro Mol Cell Biol 14: 2640-2650.
72. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, et al (2003) The COG database: an updated version includes eukaryotes BMC Bioinformatics 4: 41.
73. Tatusov RL, Koonin EV, Lipman DJ (1997) A genomic perspective on protein families Science 278: 631-637.
74. Thompson DM, Tanzer MM, Meagher RB (1992) 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.
75. Tsuji H, Saika H, Tsutsumi N, Hirai A, Nakazono M (2006) Dynamic and reversible changes in histone H3-Lys4 methylation and H3 acetylation occurring at submergence-inducible genes in rice Plant Cell Physiol 47: 995-1003.
76. Vasudevan S, Peltz SW (2001) Regulated ARE-mediated mRNA decay in Saccharomyces cerevisiae Mol Cell 7: 1191-1200.
77. Warpeha KM, Upadhyay S, Yeh J, Adamiak J, Hawkins SI, Lapik YR, Anderson MB, Kaufman LS (2007) The GCR1, GPA1, PRN1, NF-Y signal chain mediates both blue light and abscisic acid responses in Arabidopsis Plant Physiol 143: 1590-1600.
78. Wilkie GS, Dickson KS, Gray NK (2003) Regulation of mRNA translation by 59- and 39-UTR-binding factors Trends Biochem Sci 28: 182-188.
79. Williams AJ, Werner-Fraczek J, Chang IF, Bailey-Serres J (2003) Regulated phosphorylation of 40S ribosomal protein S6 in root tips of maize Plant Physiol 132: 2086-2097.
80. Xu J, Chua N-H (2009) Arabidopsis decapping 5 is required for mRNA decapping, P-body formation, and translational repression during postembryonic development Plant Cell 21: 3270-3279.
81. Yearling MN, Radebaugh CA, Stargell LA (2011) The transition of poised RNA polymerase II to an actively elongating state is a "complex" affair Genet Res Int 2011: Article 206290.