Genetic framework for flowering-time regulation by ambient temperature-responsive miRNAs in Arabidopsis

Nucleic Acids Research

Volumn 38, Issue 9, 2010, Pages 3081-3093

  Lee, Hanna ^a   Yoo, Seong Jeon ^a   Lee, Jeong Hwan ^a   Kim, Wanhui ^a   Yoo, Seung Kwan ^a   Fitzgerald, Heather ^b   Carrington, James C ^b   Ahn, Ji Hoon ^a  

^a Korea University   (South Korea)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA;

ARABIDOPSIS; ARTICLE; CONTROLLED STUDY; ENVIRONMENTAL TEMPERATURE; FLOWER DEVELOPMENT; FLOWER MORPHOLOGY; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; MICROARRAY ANALYSIS; NONHUMAN; NORTHERN BLOTTING; PHENOTYPE; PLANT GENETICS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TEMPERATURE SENSITIVITY; TEMPERATURE STRESS; VEGETATIVE STAGE; FLOWER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; TEMPERATURE;

ARABIDOPSIS;

ARABIDOPSIS; FLOWERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; MICRORNAS; MUTATION; TEMPERATURE;

EID: 77953245655     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp1240     Document Type: Article

References (71)

1. Carrington, J.C. and Ambros, V. (2003) Role of microRNAs in plant and animal development. Science, 301, 336-338.
2. Schauer, S.E., Jacobsen, S.E., Meinke, D.W. and Ray, A. (2002) DICER-LIKE1: blind men and elephants in Arabidopsis development. Trends Plant Sci., 7, 487-491.
3. 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.
4. 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.
5. Chen, X. (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science, 303, 2022-2025.
6. Guo, H.S., Xie, Q., Fei, J.F. and Chua, N.H. (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for arabidopsis lateral root development. Plant Cell, 17, 1376-1386.
7. Lauter, N., Kampani, A., Carlson, S., Goebel, M. and Moose, S.P. (2005) microRNA172 down-regulates glossy15 to promote vegetative phase change in maize. Proc. Natl Acad. Sci. USA, 102, 9412-9417.
8. Aukerman, M.J. and Sakai, H. (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. The Plant Cell Online, 15, 2730.
9. 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. et al. (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS One, 2, e219.
10. Barakat, A., Wall, K., Leebens-Mack, J., Wang, Y.J., Carlson, J.E. and Depamphilis, C.W. (2007) Large-scale identification of microRNAs from a basal eudicot (Eschscholzia californica) and conservation in flowering plants. Plant J., 51, 991-1003.
11. Long, S.P. and Woodward, F.I. (1988) Company of Biologists and Society for Experimental Biology (Great Britain). Plants and Temperature. Company of Biologists Ltd., Department of Zoology, University of Cambridge, Cambridge, UK.
12. Penfield, S. (2008) Temperature perception and signal transduction in plants. New Phytol., 179, 615-628.
13. Lee, J.H., Lee, J.S. and Ahn, J.H. (2008) Ambient temperature signaling in plants: an emerging field in the regulation of flowering time. J. Plant Biol., 51, 321-326.
14. Samach, A. and Wigge, P.A. (2005) Ambient temperature perception in plants. Curr. Opin. Plant Biol., 8, 483-486.
15. Blazquez, M.A., Ahn, J.H. and Weigel, D. (2003) A thermosensory pathway controlling flowering time in Arabidopsis thaliana. Nat. Genet., 33, 168-171.
16. Macknight, R., Bancroft, I., Page, T., Lister, C., Schmidt, R., Love, K., Westphal, L., Murphy, G., Sherson, S., Cobbett, C. et al. (1997) FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell, 89, 737-745.
17. Kim, H.J., Hyun, Y., Park, J.Y., Park, M.J., Park, M.K., Kim, M.D., Kim, H.J., Lee, M.H., Moon, J., Lee, I. et al. (2004) A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana. Nat. Genet., 36, 167-171.
18. Ausin, I., Alonso-Blanco, C., Jarillo, J.A., Ruiz-Garcia, L. and Martinez-Zapater, J.M. (2004) Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat. Genet., 36, 162-166.
19. Hartmann, U., Hohmann, S., Nettesheim, K., Wisman, E., Saedler, H. and Huijser, P. (2000) Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J., 21, 351-360.
20. Scortecci, K., Michaels, S.D. and Amasino, R.M. (2003) Genetic interactions between FLM and other flowering-time genes in Arabidopsis thaliana. Plant Mol. Biol., 52, 915-922.
21. Balasubramanian, S., Sureshkumar, S., Lempe, J. and Weigel, D. (2006) Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet., 2, e106.
22. Lee, J.H., Yoo, S.J., Park, S.H., Hwang, I., Lee, J.S. and Ahn, J.H. (2007) Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev., 21, 397-402.
23. Kobayashi, Y., Kaya, H., Goto, K., Iwabuchi, M. and Araki, T. (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science, 286, 1960-1962.
24. Kardailsky, I., Shukla, V.K., Ahn, J.H., Dagenais, N., Christensen, S.K., Nguyen, J.T., Chory, J., Harrison, M.J. and Weigel, D. (1999) Activation tagging of the floral inducer FT. Science, 286, 1962-1965.
25. Michaels, S.D. and Amasino, R.M. (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell, 11, 949-956.
26. Sheldon, C.C., Burn, J.E., Perez, P.P., Metzger, J., Edwards, J.A., Peacock, W.J. and Dennis, E.S. (1999) The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell, 11, 445-458.
27. Searle, I., He, Y., Turck, F., Vincent, C., Fornara, F., Krober, S., Amasino, R.A. and Coupland, G. (2006) The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev., 20, 898-912.
28. Helliwell, C.A., Wood, C.C., Robertson, M., James Peacock, W. and Dennis, E.S. (2006) The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex. Plant J., 46, 183-192.
29. Halliday, K.J., Salter, M.G., Thingnaes, E. and Whitelam, G.C. (2003) Phytochrome control of flowering is temperature sensitive and correlates with expression of the floral integrator FT. Plant J., 33, 875-885.
30. Strasser, B., Alvarez, M.J., Califano, A. and Cerdan, P.D. (2009) A complementary role for ELF3 and TFL1 in the regulation of flowering time by ambient temperature. Plant J., 58, 629-640.
31. Franklin, K.A. (2009) Light and temperature signal crosstalk in plant development. Curr. Opin. Plant Biol., 12, 63-68.
32. Zhang, B.H., Pan, X.P., Wang, Q.L., Cobb, G.P. and Anderson, T.A. (2005) Identification and characterization of new plant microRNAs using EST analysis. Cell Res., 15, 336-360.
33. Sunkar, R. and Zhu, J.K. (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell, 16, 2001-2019.
34. Zhou, X., Wang, G., Sutoh, K., Zhu, J.K. and Zhang, W. (2008) Identification of cold-inducible microRNAs in plants by transcriptome analysis. Biochim. Biophys. Acta, 1779, 780-788.
35. 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.
36. Pall, G.S., Codony-Servat, C., Byrne, J., Ritchie, L. and Hamilton, A. (2007) Carbodiimide-mediated cross-linking of RNA to nylon membranes improves the detection of siRNA, miRNA and piRNA by northern blot. Nucleic Acids Res., 35, e60.
37. 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.
38. Pall, G.S. and Hamilton, A.J. (2008) Improved northern blot method for enhanced detection of small RNA. Nat. Protoc., 3, 1077-1084.
39. Ascencio-Ibanez, J.T., Sozzani, R., Lee, T.J., Chu, T.M., Wolfinger, R.D., Cella, R. and Hanley-Bowdoin, L. (2008) Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol., 148, 436-454.
40. Chen, F., D'Auria, J.C., Tholl, D., Ross, J.R., Gershenzon, J., Noel, J.P. and Pichersky, E. (2003) An Arabidopsis thaliana gene for methylsalicylate biosynthesis, identified by a biochemical genomics approach, has a role in defense. Plant J., 36, 577-588.
41. Martinez, C., Pons, E., Prats, G. and Leon, J. (2004) Salicylic acid regulates flowering time and links defence responses and reproductive development. Plant J., 37, 209-217.
42. Jung, J.H., Seo, Y.H., Seo, P.J., Reyes, J.L., Yun, J., Chua, N.H. and Park, C.M. (2007) The GIGANTEA-regulated microRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. Plant Cell, 19, 2736-2748.
43. Mathieu, J., Yant, L.J., Murdter, F., Kuttner, F. and Schmid, M. (2009) Repression of flowering by the miR172 target SMZ. PLoS Biol., 7, e1000148.
44. 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.
45. Yamaguchi, A., Kobayashi, Y., Goto, K., Abe, M. and Araki, T. (2005) TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol., 46, 1175-1189.
46. Michaels, S.D., Himelblau, E., Kim, S.Y., Schomburg, F.M. and Amasino, R.M. (2004) Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol., 137, 149-156.
47. Lee, H., Suh, S.S., Park, E., Cho, E., Ahn, J.H., Kim, S.G., Lee, J.S., Kwon, Y.M. and Lee, I. (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev., 14, 2366-2376.
48. Samach, A., Onouchi, H., Gold, S.E., Ditta, G.S., Schwarz-Sommer, Z., Yanofsky, M.F. and Coupland, G. (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science, 288, 1613-1616.
49. Liu, H.H., Tian, X., Li, Y.J., Wu, C.A. and Zheng, C.C. (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA, 14, 836-843.
50. Zhao, B., Liang, R., Ge, L., Li, W., Xiao, H., Lin, H., Ruan, K. and Jin, Y. (2007) Identification of drought-induced microRNAs in rice. Biochem. Biophys. Res. Commun., 354, 585-590.
51. Chambers, C. and Shuai, B. (2009) Profiling microRNA expression in Arabidopsis pollen using microRNA array and real-time PCR. BMC Plant Biol., 9, 87.
52. 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.
53. Xie, Z., Kasschau, K.D. and Carrington, J.C. (2003) Negative feedback regulation of Dicer-Like1 in Arabidopsis by microRNA-guided mRNA degradation. Curr. Biol., 13, 784-789.
54. 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.
55. 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.
56. Li, D., Liu, C., Shen, L., Wu, Y., Chen, H., Robertson, M., Helliwell, C.A., Ito, T., Meyerowitz, E. and Yu, H. (2008) A repressor complex governs the integration of flowering signals in Arabidopsis. Dev. Cell, 15, 110-120.
57. Jang, S., Torti, S. and Coupland, G. (2009) Genetic and spatial interactions between FT, TSF and SVP during the early stages of floral induction in Arabidopsis. Plant J., 60, 614-625.
58. Lin, S.I., Chiang, S.F., Lin, W.Y., Chen, J.W., Tseng, C.Y., Wu, P.C. and Chiou, T.J. (2008) Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol., 147, 732-746.
59. Jones-Rhoades, M.W. and Bartel, D.P. (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol. Cell, 14, 787-799.
60. Wu, G. and Poethig, R.S. (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development, 133, 3539-3547.
61. Li, W.X., Oono, Y., Zhu, J., He, X.J., Wu, J.M., Iida, K., Lu, X.Y., Cui, X., Jin, H. and Zhu, J.K. (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell, 20, 2238-2251.
62. Wang, J.W., Schwab, R., Czech, B., Mica, E. and Weigel, D. (2008) Dual effects of miR156-targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell, 20, 1231-1243.
63. Gandikota, M., Birkenbihl, R.P., Hohmann, S., Cardon, G.H., Saedler, H. and Huijser, P. (2007) The miRNA156/157 recognition element in the 30 UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J., 49, 683-693.
64. Wu, G., Park, M.Y., Conway, S.R., Wang, J.W., Weigel, D. and Poethig, R.S. (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell, 138, 750-759.
65. Wang, J.W., Czech, B. and Weigel, D. (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell, 138, 738-749.
66. Wenkel, S., Turck, F., Singer, K., Gissot, L., Le Gourrierec, J., Samach, A. and Coupland, G. (2006) CONSTANS and the CCAA T box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. Plant Cell, 18, 2971-2984.
67. Kumimoto, R.W., Adam, L., Hymus, G.J., Repetti, P.P., Reuber, T.L., Marion, C.M., Hempel, F.D. and Ratcliffe, O.J. (2008) The Nuclear Factor Y subunits NF-YB2 and NF-YB3 play additive roles in the promotion of flowering by inductive long-day photoperiods in Arabidopsis. Planta, 228, 709-723.
68. Sunkar, R., Kapoor, A. and Zhu, J.K. (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell, 18, 2051-2065.
69. Abdel-Ghany, S.E. and Pilon, M. (2008) MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J. Biol. Chem., 283, 15932-15945.
70. Pant, B.D., Buhtz, A., Kehr, J. and Scheible, W.R. (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J., 53, 731-738.
71. Zhou, X., Wang, G. and Zhang, W. (2007) UV-B responsive microRNA genes in Arabidopsis thaliana. Mol. Syst. Biol., 3, 103.