Components of the Arabidopsis mRNA decapping complex are required for early seedling development

Plant Cell

Volumn 19, Issue 5, 2007, Pages 1549-1564

  Goeres, David C ^a   Van Norman, Jaimie M ^a   Zhang, Weiping ^a   Fauver, Nellie A ^a   Spencer, Mary Lou ^a   Sieburth, Leslie E ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEXATION; MUTAGENESIS; RNA;

ARABIDOPSIS MRNA DECAPPING COMPLEX; ARABIDOPSIS THALIANA;

PLANTS (BOTANY);

MUTAGENS; NUCLEIC ACIDS; PLANTS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 34347398218     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.106.047621     Document Type: Article

References (79)

1. Adenot, X., Elmayan, T., Lauressergues, D., Boutet, S., Bouché, N., Gasciolli, V., and Vaucheret, H. (2006). DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr. Biol. 16: 927-932.
2. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
3. Badis, G., Saveanu, C., Fromont-Racine, M., and Jacquier, A. (2004). Targeted mRNA degradation by deadenylation-independent decapping. Mol. Cell 15: 5-15.
4. Baima, S., Nobili, F., Sessa, G., Lucchetti, S., Ruberti, I., and Morelli, G. (1995). The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. Development 121: 4171-4182.
5. Barton, M.K., and Poethig, R.S. (1993). Formation of the shoot apical meristem in Arabidopsis thaliana: An analysis of development in the wild type and in the shoot meristemless mutant. Development 119: 823-831.
6. Beelman, C.A., Stevens, A., Caponigro, G., LaGrandeur, T.E., Hatfield, L., Fortner, D.M., and Parker, R. (1996). An essential component of the decapping enzyme required for normal rates of mRNA turnover. Nature 382: 642-646.
7. Behm-Ansmant, I., Rehwinkel, J., Doerks, T., Stark, A., Bork, P., and Izaurralde, E. (2006). mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev. 20: 1885-1895.
8. Bougourd, S., Marrison, J., and Haseloff, J. (2000). An aniline blue staining procedure for confocal microscopy and 3D imaging of normal and perturbed cellular phenotypes in mature Arabidopsis embryos. Plant J. 24: 543-550.
9. Brengues, M., Teixeira, D., and Parker, R. (2005). Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310: 486-489.
10. Bruno, I., and Wilkinson, M.F. (2006). P-bodies react to stress and nonsense. Cell 125: 1036-1038.
11. Busse, J.S., and Evert, R.F. (1999). Vascular differentiation and transition in the seedling of Arabidopsis thaliana (Brassicaceae). Int. J. Plant Sci. 160: 241-251.
12. Carland, F.M., Fujioka, S., Takatsuto, S., Yoshida, S., and Nelson, T. (2002). The identification of CVP1 reveals a role for sterols in vascular patterning. Plant Cell 14: 2045-2058.
13. Carland, F.M., and Nelson, T. (2004). COTYLEDON VASCULAR PATTERN2-mediated inositol (1.4.5) triphosphate signal transduction is essential for closed venation patterns of Arabidopsis foliar organs. Plant Cell 16: 1263-1275.
14. Carrington, J.C., and Ambros, V. (2003). Role of microRNAs in plant and animal development. Science 301: 336-338.
15. 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.
16. Clay, N.K., and Nelson, T. (2002). VH1, a provascular cell-specific receptor kinase that influences leaf cell patterns in Arabidopsis. Plant Cell 14: 2707-2722.
17. Clay, N.K., and Nelson, T. (2005). Arabidopsis thickvein mutation affects vein thickness and organ vascularization, and resides in a provascular cell-specific spermine synthase involved in vein definition and in polar auxin transport. Plant Physiol. 138: 767-777.
18. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
19. Cougot, N., Babajko, S., and Séraphin, B. (2004). Cytoplasmic foci are sites of mRNA decay in human cells. J. Cell Biol. 165: 31-40.
20. 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.
21. Cutler, S.R., Ehrhardt, D.W., Griffitts, J.S., and Somerville, C.R. (2000). Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc. Natl. Acad. Sci. USA 97: 3718-3723.
22. Deyholos, M.K., Cavaness, G.F., Hall, B., King, E., Punwani, J., Van Norman, J., and Sieburth, L.E. (2003). VARICOSE, a WD-domain protein, is required for leaf blade development. Development 130: 6577-6588.
23. Dunckley, T., and Parker, R. (1999). The DCP2 protein is required for mRNA decapping in Saccharomyces cerevisiae and contains a functional MutT motif. EMBO J. 18: 5411-5422.
24. Emery, J.F., Floyd, S.K., Alvarez, J., Eshed, Y., Hawker, N.P., Izhaki, A., Baum, S.F., and Bowman, J.L. (2003). Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr. Biol. 13: 1768-1774.
25. Esau, K. (1965). Plant Anatomy. (New York: John Wiley & Sons).
26. Fahlgren, N., Montgomery, T.A., Howell, M.D., Allen, E., Dvorak, S.K., Alexander, A.L., and Carrington, J.C. (2006). Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr. Biol. 16: 939-944.
27. Fenger-Grøn, M., Fillman, C., Norrild, B., and Lykke-Andersen, J. (2005). Multiple processing body factors and the ARE binding protein TTP activate mRNA decapping. Mol. Cell 20: 905-915.
28. Fujii, H., Chiou, T.-J., Lin, S.-I., Aung, K., and Zhu, J.-K. (2005). A miRNA involved in phosphate-starvation response in Arabidopsis. Curr. Biol. 15: 2038-2043.
29. Fukuda, H. (2004). Signals that control plant vascular cell differentiation. Nat. Rev. Mol. Cell Biol. 5: 379-391.
30. Garcia, D., Collier, S.A., Byrne, M.E., and Martienssen, R.A. (2006). Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Curr. Biol. 16: 933-938.
31. 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.
32. Geldner, N., Richter, S., Vieten, A., Marquardt, S., Torres-Ruiz, R.A., Mayer, U., and Jürgens, G. (2003). Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis. Development 131: 389-400.
33. Giraldez, A.J., Mishima, Y., Rihel, J., Grocock, R.J., Van Dongen, S., Inoue, K., Enright, A.J., and Schier, A.F. (2006). Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 312: 75-79.
34. Gutiérrez, 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.
35. Hanzawa, Y., Takahashi, T., Michael, A.J., Burtin, D., Long, D., Pineiro, M., Coupland, G., and Komeda, Y. (2000). ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO J. 19: 4248-4256.
36. Hughes, D.W., and Galau, G.A. (1989). Temporally modular gene expression during cotyledon development. Genes Dev. 3: 358-369.
37. Johanson, U., West, J., Lister, C., Michaels, S., Amasino, R., and Dean, C. (2000). Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290: 344-347.
38. 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.
39. Kim, J., Jung, J.H., Reyes, J.L., Kim, Y.S., Kim, S.Y., Chung, K.S., Kim, J.A., Lee, M., Lee, Y., Kim, V.N., Chua, N.H., and Park, C.M. (2005). MicroRNA-directed cleavage of ATHB15 mRNA regulates vascular development in Arabidopsis inflorescence stems. Plant J. 42: 84-94.
40. Koizumi, K., Naramoto, S., Sawa, S., Yahara, N., Ueda, T., Nakano, A., Sugiyama, M., and Fukuda, H. (2005). VAN3 ARF-GAP-mediated vesicle transport is involved in leaf vascular network formation. Development 132: 1699-1711.
41. Kotak, S., Vierling, E., Bäumlein, H., and von Koskull-Döring, P. (2007). A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. Plant Cell 19: 182-195.
42. Larimer, F.W., and Stevens, A. (1990). Disruption of the gene XRN1, coding for a 5′-3′ exoribonuclease, restricts yeast cell growth. Gene 95: 85-90.
43. Li, H., Xu, L., Wang, H., Yuan, Z., Cao, X., Yang, Z., Zhang, D., Xu, Y., and Huang, H. (2005). The putative RNA-dependent RNA polymerase RDR6 acts synergistically with ASYMMETRIC LEAVES1 and 2 to repress BREVIPEDICELLUS and microRNA 165/166 in Arabidopsis leaf development. Plant Cell 17: 2157-2171.
44. Liu, J., Rivas, F.V., Wohlschlegel, J., Yates, J.R., Parker, R., and Hannon, G.J. (2005a). A role for the P-body component GW182 in microRNA function. Nat. Cell Biol. 7: 1261-1266.
45. Liu, J., Valencia-Sanchez, M.A., Hannon, G.J., and Parker, R. (2005b). MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat. Cell Biol. 7: 719-723.
46. Liu, P.-P., Koizuka, N., Martin, R.C., and Nonogaki, H. (2005c). The BME3 (Blue Micropylar End 3) GATA zinc finger transcription factor is a positive regulator of Arabidopsis seed germination. Plant J. 44: 960-971.
47. Lotan, T., Ohto, M., Yee, K.M., West, M.A., Lo, R., Kwong, R.W., Yarnagishi, K., Fischer, R.L., Goldberg, R.B., and Harada, J.J. (1998). Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93: 1195-1205.
48. Maloof, J.N., Borevitz, J.O., Dabi, T., Lutes, J., Nehring, R.B., Redfern, J.L., Trainer, G.T., Wilson, J.M., Asami, T., Berry, C.C., Weigel, D., and Chory, J. (2001). Natural variation in light sensitivity of Arabidopsis. Nat. Genet. 29: 441-446.
49. Mattsson, J., Ckurshumova, W., and Berleth, T. (2003). Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol. 131: 1327-1339.
50. McClure, B.A., Hagen, G., Brown, C.S., Geen, M.A., and Guilfoyle, T.J. (1989). Transcription, organization, and sequence of an auxin-regulated gene cluster in soybean. Plant Cell 1: 229-239.
51. McConnell, J.R., and Barton, M.K. (1998). Leaf polarity and meristem formation in Arabidopsis. Development 125: 2935-2942.
52. Muhlrad, D., and Parker, R. (1994). Premature translational termination triggers mRNA decapping. Nature 370: 578-581.
53. Ogas, J., Kaufmann, S., Henderson, J., and Somerville, C. (1999). PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc. Natl. Acad. Sci. USA 96: 13839-13844.
54. 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 EIN3-targeting F-box proteins EBF1/2. Proc. Natl. Acad. Sci. USA 103: 13286-13293.
55. Parker, R., and Song, H. (2004). The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol. 11: 121-127.
56. 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.
57. Prigge, M.J., Otsuga, D., Alonso, J.M., Ecker, J.R., Drews, G.N., and Clark, S.E. (2004). Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17: 61-76.
58. Quint, M., and Gray, W.M. (2006). Auxin signaling. Curr. Opin. Plant Biol. 9: 448-453.
59. Reinhart, B.J., Weinstein, E.G., Rhoades, M.W., Bartel, B., and Bartel, D.P. (2002). MicroRNAs in plants. Genes Dev. 16: 1616-1626.
60. 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.
61. Scarpella, E., Francis, P., and Berleth, T. (2004). Stage-specific markers define early steps of procambium development in Arabidopsis leaves and correlate termination of vein formation with mesophyll differentiation. Development 131: 3445-3455.
62. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Schölkopf, B., Weigel, D., and Lohmann, J. (2005). A gene expression map of Arabidopsis development. Nat. Genet. 37: 501-506.
63. Sen, G.L., and Blau, H.M. (2005). Argonaute 2/RISC resides in sites of mammalian mRNA decay known as cytoplasmic bodies. Nat. Cell Biol. 7: 633-636.
64. She, M., Decker, C.J., Chen, N., Tumati, S., Parker, R., and Song, H. (2006). Crystal structure and functional analysis of Dcp2p from Schizosaccharomyces pombe. Nat. Struct. Mol. Biol. 13: 63-70.
65. Sheth, U., and Parker, R. (2003). Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300: 805-808.
66. Sieburth, L.E., and Deyholos, M.K. (2006). Vascular development: The long and winding road. Curr. Opin. Plant Biol. 9: 48-54.
67. Sieburth, L.E., Muday, G.K., King, E.J., Benton, G., Kim, S., Metcalf, K.E., Meyers, L., Seamen, E., and Van Norman, J.M. (2006). SCARFACE encodes an ARF-GAP that is required for normal auxin efflux and vein patterning in Arabidopsis. Plant Cell 18: 1396-1411.
68. 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.
69. Tusher, V.G., Tibshirani, R., and Chu, G. (2001). Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98: 5116-5121.
70. Ulmasov, T., Murfett, J., Hagen, G., and Guilfoyle, T.J. (1997). Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9: 1963-1971.
71. van Dijk, E., Cougot, N., Meyer, S., Babajko, S., Wahle, E., and Séraphin, B. (2002). Human Dcp2: A catalytically active mRNA decapping enzyme located in specific cytoplasmic structures. EMBO J. 21: 6915-6924.
72. Van Norman, J.M., Frederick, R., and Sieburth, L.E. (2004). BYPASS1 negatively regulates a root-derived signal that controls plant architecture. Curr. Biol. 14: 1739-1746.
73. Van Norman, J.M., and Sieburth, L.E. (2007). Dissecting the biosynthetic pathway for the bypass1 root-derived signal. Plant J. 49: 619-628.
74. Vaucheret, H., Vazquez, F., Crete, P., and Bartel, D.P. (2004). The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev. 18: 1187-1197.
75. Vazquez, F., Gasciolli, V., Crete, P., and Vaucheret, H. (2004). The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Curr. Biol. 14: 346-351.
76. Wehmeyer, N., and Vierling, E. (2000). The expression of small heat shock proteins in seeds responds to discrete developmental signals and suggests a general protective role in desiccation tolerance. Plant Physiol. 122: 1099-1108.
77. Williams, L., Grigg, S.P., Xie, M., Christensen, X., and Fletcher, J.C. (2005). Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development 132: 3657-3668.
78. 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.
79. Yu, J.H., Yang, W.H., Gulick, T., Bloch, K.D., and Bloch, D.B. (2005). Ge-1 is a central component of the mammalian cytoplasmic mRNA processing body. RNA 11: 1795-1802.