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 Journal

Volumn 49, Issue 4, 2007, Pages 683-693

  Gandikota, Madhuri ^a   Birkenbihl, Rainer P ^a   Höhmann, Susanne ^a   Cardon, Guillermo H ^a,b   Saedler, Heinz ^a   Huijser, Peter ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^b EUROPEAN COMMISSION   (Belgium)

Author keywords

Flowering; microRNA; miR156; Post transcriptional regulation; SBP box gene; SPL3

Indexed keywords

GENES; PLANTS (BOTANY); RNA;

FLOWERING; MICRORNA; MIR156; POST TRANSCRIPTIONAL REGULATION; SBP BOX GENE; SPL3;

PLANT CELL CULTURE;

ARABIDOPSIS PROTEIN; MICRORNA;

ARABIDOPSIS; ARTICLE; FLOWER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; SEEDLING; TRANSGENIC PLANT; ULTRASTRUCTURE; UNTRANSLATED REGION; WESTERN BLOTTING;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; BLOTTING, WESTERN; FLOWERS; GENE EXPRESSION REGULATION, PLANT; MICRORNAS; MICROSCOPY, ELECTRON, SCANNING; MOLECULAR SEQUENCE DATA; MUTATION; PLANTS, GENETICALLY MODIFIED; POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEEDLING; UNTRANSLATED REGIONS;

CELLS; GENES; NUCLEIC ACIDS; PLANTS;

ARABIDOPSIS;

EID: 33846904347     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2006.02983.x     Document Type: Article

References (51)

1. Allen, E., Xie, Z., Gustafson, A.M. and Carrington, J.C. (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell, 121, 207-221.
2. Arazi, T., Talmor-Neiman, M., Stav, R., Riese, M., Huijser, P. and Baulcombe, D.C. (2005) Cloning and characterization of microRNAs from moss. Plant J. 43, 837-848.
3. Axtell, M.J. and Bartel, D.P. (2005) Antiquity of microRNAs and their targets in land plants. Plant Cell, 17, 1658-1673.
4. Bartel, D.P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281-297.
5. Bechtold, N., Ellis, J. and Pelletier, G. (1997) In planta Agrobacterium-mediated transfer by infilteration of adult Arabidopsis plants. C.R. Acad. Sci. III Sci. Vie, 316, 1194-1199.
6. Birkenbihl, R.P., Jach, G., Saedler, H. and Huijser, P. (2005) Functional dissection of the plant-specific SBP-domain: overlap of the DNA-binding and nuclear localization domains. J. Mol. Biol. 352, 585-596.
7. Boss, P.K., Bastow, R.M., Mylne, J.S. and Dean, C. (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell, 16, S18-S31.
8. Cardon, G.H., Höhmann, S., Nettesheim, K., Saedler, H. and Huijser, P. (1997) Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3: a novel gene involved in the floral transition. Plant J. 12, 367-377.
9. Cardon, G.H., Höhmann, S., Klein, J., Nettesheim, K., Saedler, H. and Huijser, P. (1999) Molecular characterisation of the Arabidopsis SBP-box genes. Gene, 237, 91-104.
10. Chen, X. (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science, 303, 2022-2025.
11. Chen, J., Li, W.X., Xie, D., Peng, J.R. and Ding, S.W. (2004) Viral virulence protein suppresses RNA silencing-mediated defense but upregulates the role of microRNA in host gene expression. Plant Cell, 16, 1302-1313.
12. Chiou, T.J., Aung, K., Lin, S.I., Wu, C.C., Chiang, S.F. and Su, C.L. (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell, 18, 412-421.
13. Doench, J.G. and Sharp, P.A. (2004) Specificity of microRNA target selection in translational repression. Genes Dev. 18, 504-511.
14. Dreyfuss, G., Kim, V.N. and Kataoka, N. (2002) Messenger-RNA-binding proteins and the messages they carry. Nat. Rev. Mol. Cell Biol. 3, 195-205.
15. 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.
16. Humphreys, D.T., Belinda, J., Westman, B.J., Martin, D.I.K. and Preiss, T. (2005) MicroRNAs control translation initiation by inhibiting eukaryotic initiation factor 4E cap and poly(A) tail function. Proc. Natl Acad. Sci. USA, 102, 16961-16966.
17. Jones-Rhoades, M.W. and Bartel, D.P. (2004) Computational identification of plant microRNAs and their targets, including a stressinduced miRNA. Mol. Cell, 14, 787-799.
18. Kasschau, K.D., Xie, Z., Allen, E., Llave, C., Chapman, E.J., Krizan, K.A. and Carrington, J.C. (2003) P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev. Cell, 4, 205-217.
19. Kiriakidou, M., Nelson, P.T., Kouranov, A., Fitziev, P., Bouyioukos, C., Mourelatos, Z. and Hatzigeorgiou, A. (2004) A combined computational-experimental approach predicts human microRNA targets. Genes Dev. 18, 1165-1178.
20. Klein, J., Saedler, H. and Huijser, P. (1996) A new family of DNA binding proteins includes putative transcriptional regulators of the Antirrhinum majus floral meristem identity gene SQUAMOSA. Mol. Gen. Genet. 250, 7-16.
21. Lännenpää, M., Jänönen, I., Hölttä-Vuori, M., Marika Gardemeister, M., Porali, I. and Sopanen, T. (2004) A new SBP-box gene BpSPL1 in silver birch (Betula pendula). Physiol. Plant. 120, 491-500.
22. 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.
23. Lu, S., Sun, Y.H., Shi, R., Clark, C., Li, L. and Chiang, V.L. (2005) Novel and mechanical stress-responsive microRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell, 17, 2186-2203.
24. Mallory, A.C., Reinhart, B.J., Jones-Rhoades, M.W., Tang, G., Zamore, P.D., Barton, M.K. and Bartel, D.P. (2004) MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region. EMBO J. 23, 3356-3364.
25. Millar, A.A. and Waterhouse, P.M. (2005) Plant and animal microRNAs: similarities and differences. Funct. Integr. Genomics, 5, 129-135.
26. Moreno, M.A., Harper, L.C., Krueger, R.W., Dellaporta, S.L. and Freeling, M. (1997) Liguleless1 encodes a nuclear-localized protein required for induction of ligules and auricles during maize leaf organogenesis. Genes Dev. 11, 616-628.
27. Olsen, P.H. and Ambros, V. (1999) The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev. Biol. 216, 671-680.
28. Palatnik, J.F., Allen, E., Wu, X., Schommer, C., Schwab, R., Carrington, J.C. and Weigel, D. (2003) Control of leaf morphogenesis by microRNAs. Nature, 425, 257-263.
29. Panstruga, R., Kim, M.C., Cho, M.J. and Schulze-Lefert, P. (2003) Testing the efficiency of dsRNAi constructs in vivo in a transient expression assay tested on two fluorescent proteins. Mol. Biol. Rep. 30, 135-140.
30. Parizotto, E.A., Dunoyer, P., Rahm, N., Himber, C. and Voinnet, O. (2004) In vivo investigation of transcription, processing, endonucleolytic activity and functional relevance of the spatial distribution of a plant miRNA. Genes Dev. 18, 2237-2242.
31. Park, M.Y., Wu, G., Gonzalez-Sulser, A., Vaucheret, H. and Poethig, R.S. (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proc. Natl Acad. Sci. USA, 102, 3691-3696.
32. Peragine, A., Yoshikawa, M., Wu, G., Albrecht, H.L. and Poethig, R.S. (2004) SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev. 18, 2368-2379.
33. Pillai, R.S., Bhattacharyya, S.N., Artus, C.G., Zoller, T., Cougot, N., Basyuk, E., Bertrand, E. and Filipowicz, W. (2005) Inhibition of translational initiation by Let-7 microRNA in human cells. Science, 309, 1573-1576.
34. Reinhart, B.J., Weinstein, E.G., Rhoades, M.W., Bartel, B. and Bartel, D.P. (2002) MicroRNAs in plants. Genes Dev. 16, 1616-1626.
35. Rhoades, M.W., Reinhart, B.J., Lim, L.P., Burge, C.B., Bartel, B. and Bartel, D.P. (2002) Prediction of plant microRNA targets. Cell, 110, 513-520.
36. Samach, A., Onouchi, H., Gold, S.E., Ditta, G.S., Schwarz-Sommer, Z.S., Yanofsky, M.F. and Coupland, G. (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science, 288, 1613-1616.
37. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
38. Schmid, M., Uhlenhaut, M.H., Godard, F., Demar, M., Bressan, R., Weigel, D. and Lohmann, J.U. (2003) Dissection of floral induction pathways using global expression analysis. Development, 130, 6001-6012.
39. Schmid, M., Darison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Scholkopf, B., Weig, D. and Lohmann, J.U. (2005) A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37, 501-506.
40. 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.
41. Sommer, H., Beltran, J.P., Huijser, P., Pape, H., Lönnig, W.-E., Saedler, H. and Schwarz-Sommer, Z. (1990) DEFICIENS, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus - the protein shows homology to transcription factors. EMBO J. 9, 605-613.
42. Stone, J.M., Liang, X., Nekl, E.R. and Stiers, J.J. (2005) Arabidopsis AtSPL14, a plant-specific SBP-domain transcription factor, participates in plant development and sensitivity to fumonisin B1. Plant J. 41, 744-754.
43. Sunkar, R. and Zhu, J.K. (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell, 16, 2001-2019.
44. Tang, G., Reinhart, B.J., Bartel, D.P. and Zamore, P.D. (2003) A biochemical framework for RNA silencing in plants. Genes Dev., 17, 49-63.
45. Unte, U.S., Sorensen, A.-M., Pesaresi, P., Gandikota, M., Leister, D., Saedler, H. and Huijser, P. (2003) SPL8, an SBP-box gene that affects pollen sac development in Arabidopsis. Plant Cell, 15, 1009-1019.
46. Válóczi, A., Várallyay, É., Kauppinen, S., Burgyán, J. and Havelda, Z. (2006) Spatio-temporal accumulation of microRNAs is highly coordinated in developing plant tissues. Plant J. 47, 140-151.
47. Vazquez, F., Gasciolli, V., Crété, 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.
48. Wang, H., Nussbaum-Wagler, T., Li, B., Zhao, Q., Vigouroux, Y., Faller, M., Bomblies, K., Lukens, L. and Doebley, J.F. (2005) The origin of the naked grains of maize. Nature, 436, 714-719.
49. Yamasaki, K., Kigawa, T., Inoue, M. et al. (2004) A novel zinc-binding motif revealed by solution structures of DNA-binding domains of Arabidopsis SBP-family transcription factors. J. Mol. Biol. 337, 49-63.
50. Zhang, B., Pan, X., Cannon, C.H., Cobb, G.P. and Anderson, T.A. (2006) Conservation and divergence of plant microRNA genes. Plant J. 46, 243-259.
51. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L. and Gruissem, W. (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632.