Transcriptome-wide analysis of uncapped mRNAs in Arabidopsis reveals regulation of mRNA degradation

Plant Cell

Volumn 20, Issue 10, 2008, Pages 2571-2585

  Jiao, Yuling ^a   Riechmann, José Luis ^a,b   Meyerowitz, Elliot M ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b CENTRE FOR RESEARCH IN AGRICULTURAL GENOMICS CRAG   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA;

EID: 57749084495     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.108.062786     Document Type: Article

References (85)

1. Addo-Quaye, C., Eshoo, T.W., Bartel, D.P., and Axtell, M.J. (2008). Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr. Biol. 18: 758-762.
2. Amrani, N., Sachs, M.S., and Jacobson, A. (2006). Early nonsense: mRNA decay solves a translational problem. Nat. Rev. Mol. Cell Biol. 7: 415-425.
3. Arava, Y., Wang, Y., Storey, J.D., Liu, C.L., Brown, P.O., and Herschlag, D. (2003). Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 100: 3889-3894.
4. Arciga-Reyes, L., Wootton, L., Kieffer, M., and Davies, B. (2006). UPF1 is required for nonsense-mediated mRNA decay (NMD) and RNAi in Arabidopsis. Plant J. 47: 480-489.
5. Aukerman, M.J., and Sakai, H. (2003). Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15: 2730-2741.
6. Barkoulas, M., Galinha, C., Grigg, S.P., and Tsiantis, M. (2007). From genes to shape: Regulatory interactions in leaf development. Curr. Opin. Plant Biol. 10: 660-666.
7. Belostotsky, D.A. (2008). State of decay: An update on plant mRNA turnover. Curr. Top. Microbiol. Immunol. 326: 179-199.
8. Belostotsky, D.A., and Rose, A.B. (2005). Plant gene expression in the age of systems biology: Integrating transcriptional and posttranscriptional events. Trends Plant Sci. 10: 347-353.
9. Berardini, T.Z., et al. (2004). Functional annotation of the Arabidopsis genome using controlled vocabularies. Plant Physiol. 135: 1-11.
10. Borsani, O., Zhu, J., Verslues, P.E., Sunkar, R., and Zhu, J.K. (2005). Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123: 1279-1291.
11. Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., Dunoyer, P., Yamamoto, Y.Y., Sieburth, L., and Voinnet, O. (2008). Widespread translational inhibition by plant miRNAs and siRNAs. Science 320: 1185-1190.
12. Chekanova, J.A., et al. (2007). Genome-wide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell 131: 1340-1353.
13. Chen, X. (2004). A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303: 2022-2025.
14. Chiba, Y., Johnson, M.A., Lidder, P., Vogel, J.T., van Erp, H., and Green, P.J. (2004). AtPARN is an essential poly(A) ribonuclease in Arabidopsis. Gene 328: 95-102.
15. Clark, S.E., Williams, R.W., and Meyerowitz, E.M. (1997). The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89: 575-585.
16. Coller, J., and Parker, R. (2004). Eukaryotic mRNA decapping. Annu. Rev. Biochem. 73: 861-890.
17. Couttet, P., Fromont-Racine, M., Steel, D., Pictet, R., and Grange, T. (1997). Messenger RNA deadenylylation precedes decapping in mammalian cells. Proc. Natl. Acad. Sci. USA 94: 5628-5633.
18. Dabney, A.R., and Storey, J.D. (2007). Normalization of two-channel microarrays accounting for experimental design and intensity-dependent relationships. Genome Biol. 8: R44.
19. Fahlgren, N., Howell, M.D., Kasschau, K.D., Chapman, E.J., Sullivan, C.M., Cumbie, J.S., Givan, S.A., Law, T.F., Grant, S.R., Dangl, J.L., and Carrington, J.C. (2007). High-throughput sequencing of Arabidopsis microRNAs: Evidence for frequent birth and death of MIRNA genes. PLoS ONE 2: e219.
20. Gallie, D.R. (2002). Protein-protein interactions required during translation. Plant Mol. Biol. 50: 949-970.
21. Gallie, D.R., and Bailey-Serres, J. (1997). Eyes off transcription! The wonderful world of post-transcriptional regulation. Plant Cell 9: 667-673.
22. Gandikota, M., Birkenbihl, R.P., Hohmann, S., Cardon, G.H., Saedler, H., and Huijser, P. (2007). The miRNA156/157 recognition element in the 3′ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J. 49: 683-693.
23. Gazzani, S., Lawrenson, T., Woodward, C., Headon, D., and Sablowski, R. (2004). A link between mRNA turnover and RNA interference in Arabidopsis. Science 306: 1046-1048.
24. German, M.A., et al. (2008). Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat. Biotechnol. 26: 941-946.
25. Goeres, D.C., Van Norman, J.M., Zhang, W., Fauver, N.A., Spencer, M.L., and Sieburth, L.E. (2007). Components of the Arabidopsis mRNA decapping complex are required for early seedling development. Plant Cell 19: 1549-1564.
26. Gregory, B.D., O'Malley, R.C., Lister, R., Urich, M.A., Tonti-Filippini, J., Chen, H., Millar, A.H., and Ecker, J.R. (2008). A link between RNA metabolism and silencing affecting Arabidopsis development. Dev. Cell 14: 854-866.
27. Gunawardana, D., Cheng, H.C., and Gayler, K.R. (2008). Identification of functional domains in Arabidopsis thaliana mRNA decapping enzyme (AtDcp2). Nucleic Acids Res. 36: 203-216.
28. Guo, A., He, K., Liu, D., Bai, S., Gu, X., Wei, L., and Luo, J. (2005). DATF: A database of Arabidopsis transcription factors. Bioinformatics 21: 2568-2569.
29. Gustafson, A.M., Allen, E., Givan, S., Smith, D., Carrington, J.C., and Kasschau, K.D. (2005). ASRP: The Arabidopsis Small RNA Project Database. Nucleic Acids Res. 33: D637-D640.
30. Gutierrez, R.A., Ewing, R.M., Cherry, J.M., and Green, P.J. (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.
31. Gutierrez, R.A., MacIntosh, G.C., and Green, P.J. (1999). Current perspectives on mRNA stability in plants: Multiple levels and mechanisms of control. Trends Plant Sci. 4: 429-438.
32. Halbeisen, R.E., Galgano, A., Scherrer, T., and Gerber, A.P. (2008). Post-transcriptional gene regulation: From genome-wide studies to principles. Cell. Mol. Life Sci. 65: 798-813.
33. Henz, S.R., Cumbie, J.S., Kasschau, K.D., Lohmann, J.U., Carrington, J.C., Weigel, D., and Schmid, M. (2007). Distinct expression patterns of natural antisense transcripts in Arabidopsis. Plant Physiol. 144: 1247-1255.
34. Higgs, D.C., and Colbert, J.T. (1994). Oat phytochrome A mRNA degradation appears to occur via two distinct pathways. Plant Cell 6: 1007-1019.
35. Hofacker, I.L., Fontana, W., Stadler, P.F., Bonhoeffer, L.S., Tacker, M., and Schuster, P. (1994). Fast folding and comparison of RNA secondary structures. Monatsh. Chem. 125: 167-188.
36. Hori, K., and Watanabe, Y. (2005). UPF3 suppresses aberrant spliced mRNA in Arabidopsis. Plant J. 43: 530-540.
37. Houseley, J., LaCava, J., and Tollervey, D. (2006). RNA-quality control by the exosome. Nat. Rev. Mol. Cell Biol. 7: 529-539.
38. Iwasaki, S., Takeda, A., Motose, H., and Watanabe, Y. (2007). Characterization of Arabidopsis decapping proteins AtDCP1 and AtDCP2, which are essential for post-embryonic development. FEBS Lett. 581: 2455-2459.
39. Jen, C.H., Michalopoulos, I., Westhead, D.R., and Meyer, P. (2005). Natural antisense transcripts with coding capacity in Arabidopsis may have a regulatory role that is not linked to double-stranded RNA degradation. Genome Biol. 6: R51.
40. Jiao, Y., Lau, O.S., and Deng, X.W. (2007). Light-regulated transcriptional networks in higher plants. Nat. Rev. Genet. 8: 217-230.
41. Jin, H., Vacic, V., Girke, T., Lonardi, S., and Zhu, J.K. (2008). Small RNAs and the regulation of cis-natural antisense transcripts in Arabidopsis. BMC Mol. Biol. 9: 6.
42. Jinn, T.L., Stone, J.M., and Walker, J.C. (2000). HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission. Genes Dev. 14: 108-117.
43. Kasschau, K.D., Fahlgren, N., Chapman, E.J., Sullivan, C.M., Cumbie, J.S., Givan, S.A., and Carrington, J.C. (2007). Genomewide profiling and analysis of Arabidopsis siRNAs. PLoS Biol. 5: e57.
44. Kastenmayer, J.P., and Green, P.J. (2000). Novel features of the XRN-family in Arabidopsis: Evidence that AtXRN4, one of several orthologs of nuclear Xrn2p/Rat1p, functions in the cytoplasm. Proc. Natl. Acad. Sci. USA 97: 13985-13990.
45. Katiyar-Agarwal, S., Gao, S., Vivian-Smith, A., and Jin, H. (2007). A novel class of bacteria-induced small RNAs in Arabidopsis. Genes Dev. 21: 3123-3134.
46. Katiyar-Agarwal, S., Morgan, R., Dahlbeck, D., Borsani, O., Villegas, A., Jr., Zhu, J.K., Staskawicz, B.J., and Jin, H. (2006). A pathogen-inducible endogenous siRNA in plant immunity. Proc. Natl. Acad. Sci. USA 103: 18002-18007.
47. Keene, J.D. (2007). RNA regulons: Coordination of post-transcriptional events. Nat. Rev. Genet. 8: 533-543.
48. Kerenyi, Z., Merai, Z., Hiripi, L., Benkovics, A., Gyula, P., Lacomme, C., Barta, E., Nagy, F., and Silhavy, D. (2008). Inter-kingdom conservation of mechanism of nonsense-mediated mRNA decay. EMBO J. 27: 1585-1595.
49. Kertesz, S., Kerenyi, Z., Merai, Z., Bartos, I., Palfy, T., Barta, E., and Silhavy, D. (2006). Both introns and long 3′-UTRs operate as cis-acting elements to trigger nonsense-mediated decay in plants. Nucleic Acids Res. 34: 6147-6157.
50. Krupa, A., Abhinandan, K.R., and Srinivasan, N. (2004). KinG: A database of protein kinases in genomes. Nucleic Acids Res. 32: D153-D155.
51. Lackner, D.H., Beilharz, T.H., Marguerat, S., Mata, J., Watt, S., Schubert, F., Preiss, T., and Bahler, J. (2007). A network of multiple regulatory layers shapes gene expression in fission yeast. Mol. Cell 26: 145-155.
52. Leek, J.T., Monsen, E., Dabney, A.R., and Storey, J.D. (2006). EDGE: Extraction and analysis of differential gene expression. Bioinformatics 22: 507-508.
53. Li, J., and Chory, J. (1997). A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90: 929-938.
54. Li, J., Wen, J., Lease, K.A., Doke, J.T., Tax, F.E., and Walker, J.C. (2002). BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110: 213-222.
55. Lindow, M., Jacobsen, A., Nygaard, S., Mang, Y., and Krogh, A. (2007). Intragenomic matching reveals a huge potential for miRNA-mediated regulation in plants. PLoS Comput. Biol. 3: e238.
56. Liu, H., and Kiledjian, M. (2006). Decapping the message: A beginning or an end. Biochem. Soc. Trans. 34: 35-38.
57. Liu, X., and Gorovsky, M.A. (1993). Mapping the 5′ and 3′ ends of Tetrahymena thermophila mRNAs using RNA ligase mediated amplification of cDNA ends (RLM-RACE). Nucleic Acids Res. 21: 4954-4960.
58. Llave, C., Xie, Z., Kasschau, K.D., and Carrington, J.C. (2002). Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297: 2053-2056.
59. Ma, L., Sun, N., Liu, X., Jiao, Y., Zhao, H., and Deng, X.W. (2005). Organ-specific expression of Arabidopsis genome during development. Plant Physiol. 138: 80-91.
60. Meyer, S., Temme, C., and Wahle, E. (2004). Messenger RNA turnover in eukaryotes: Pathways and enzymes. Crit. Rev. Biochem. Mol. Biol. 39: 197-216.
61. Mitchell, P., and Tollervey, D. (2000). Musing on the structural organization of the exosome complex. Nat. Struct. Biol. 7: 843-846.
62. Muhlrad, D., Decker, C.J., and Parker, R. (1995). Turnover mechanisms of the stable yeast PGK1 mRNA. Mol. Cell. Biol. 15: 2145-2156.
63. Nam, K.H., and Li, J. (2002). BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110: 203-212.
64. Narsai, R., Howell, K.A., Millar, A.H., O'Toole, N., Small, I., and Whelan, J. (2007). Genome-wide analysis of mRNA decay rates and their determinants in Arabidopsis thaliana. Plant Cell 19: 3418-3436.
65. Nishimura, N., Kitahata, N., Seki, M., Narusaka, Y., Narusaka, M., Kuromori, T., Asami, T., Shinozaki, K., and Hirayama, T. (2005). Analysis of ABA hypersensitive germination2 revealed the pivotal functions of PARN in stress response in Arabidopsis. Plant J. 44: 972-984.
66. Olmedo, G., Guo, H., Gregory, B.D., Nourizadeh, S.D., Aguilar-Henonin, L., Li, H., An, F., Guzman, P., and Ecker, J.R. (2006). ETHYLENE-INSENSITIVE5 encodes a 5′→3′ exoribonuclease required for regulation of the EIN3-targeting F-box proteins EBF1/2. Proc. Natl. Acad. Sci. USA 103: 13286-13293.
67. Parker, R., and Sheth, U. (2007). P bodies and the control of mRNA translation and degradation. Mol. Cell 25: 635-646.
68. Parker, R., and Song, H. (2004). The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol. 11: 121-127.
69. Potuschak, T., Vansiri, A., Binder, B.M., Lechner, E., Vierstra, R.D., and Genschik, P. (2006). The exoribonuclease XRN4 is a component of the ethylene response pathway in Arabidopsis. Plant Cell 18: 3047-3057.
70. Qin, X., Ahn, S., Speed, T.P., and Rubin, G.M. (2007). Global analyses of mRNA translational control during early Drosophila embryogenesis. Genome Biol. 8: R63.
71. Reverdatto, S.V., Dutko, J.A., Chekanova, J.A., Hamilton, D.A., and Belostotsky, D.A. (2004). mRNA deadenylation by PARN is essential for embryogenesis in higher plants. RNA 10: 1200-1214.
72. Schwab, R., Palatnik, J.F., Riester, M., Schommer, C., Schmid, M., and Weigel, D. (2005). Specific effects of microRNAs on the plant transcriptome. Dev. Cell 8: 517-527.
73. Shiu, S.H., and Bleecker, A.B. (2001). Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc. Natl. Acad. Sci. USA 98: 10763-10768.
74. Shyu, A.B., Wilkinson, M.F., and van Hoof, A. (2008). Messenger RNA regulation: to translate or to degrade. EMBO J. 27: 471-481.
75. Souret, F.F., Kastenmayer, J.P., and Green, P.J. (2004). AtXRN4 degrades mRNA in Arabidopsis and its substrates include selected miRNA targets. Mol. Cell 15: 173-183.
76. Staple, D.W., and Butcher, S.E. (2005). Pseudoknots: RNA structures with diverse functions. PLoS Biol. 3: e213.
77. Torii, K.U., Mitsukawa, N., Oosumi, T., Matsuura, Y., Yokoyama, R., Whittier, R.F., and Komeda, Y. (1996). The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8: 735-746.
78. Vlasova, I.A., Tahoe, N.M., Fan, D., Larsson, O., Rattenbacher, B., Sternjohn, J.R., Vasdewani, J., Karypis, G., Reilly, C.S., Bitterman, P.B., and Bohjanen, P.R. (2008). Conserved GU-rich elements mediate mRNA decay by binding to CUG-binding protein 1. Mol. Cell 29: 263-270.
79. Wang, X.J., Gaasterland, T., and Chua, N.H. (2005). Genome-wide prediction and identification of cis-natural antisense transcripts in Arabidopsis thaliana. Genome Biol. 6: R30.
80. Wellmer, F., Alves-Ferreira, M., Dubois, A., Riechmann, J.L., and Meyerowitz, E.M. (2006). Genome-wide analysis of gene expression during early Arabidopsis flower development. PLoS Genet. 2: e117.
81. Wellmer, F., and Riechmann, J.L. (2005). Gene network analysis in plant development by genomic technologies. Int. J. Dev. Biol. 49: 745-759.
82. Wellmer, F., Riechmann, J.L., Alves-Ferreira, M., and Meyerowitz, E.M. (2004). Genome-wide analysis of spatial gene expression in Arabidopsis flowers. Plant Cell 16: 1314-1326.
83. Xu, J., Yang, J.Y., Niu, Q.W., and Chua, N.H. (2006). Arabidopsis DCP2, DCP1, and VARICOSE form a decapping complex required for postembryonic development. Plant Cell 18: 3386-3398.
84. Yoine, M., Nishii, T., and Nakamura, K. (2006). Arabidopsis UPF1 RNA helicase for nonsense-mediated mRNA decay is involved in seed size control and is essential for growth. Plant Cell Physiol. 47: 572-580.
85. Yuan, J.S., Galbraith, D.W., Dai, S.Y., Griffin, P., and Stewart, C.N., Jr. (2008). Plant systems biology comes of age. Trends Plant Sci. 13: 165-171.