Expression of the floral repressor miRNA156 is positively regulated by the AGAMOUS-like proteins AGL15 and AGL18

Molecules and Cells

Volumn 38, Issue 3, 2015, Pages 259-266

  Serivichyaswat, Phanu ^a   Ryu, Hak Seung ^a   Kim, Wanhui ^a   Kim, Soonkap ^a   Chung, Kyung Sook ^a   Kim, Jae Joon ^a   Ahn, Ji Hoon ^a  

^a Korea University   (South Korea)

Author keywords

AGAMOUS like 15; AGAMOUS like 18; CArG motifs; Floral transition; MiRNA156

Indexed keywords

AGAMOUS LIKE PROTEIN 15; AGAMOUS LIKE PROTEIN 18; GLUTATHIONE TRANSFERASE; GREEN FLUORESCENT PROTEIN; HETERODIMER; MICRORNA; MICRORNA 156; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; AGL15 PROTEIN, ARABIDOPSIS; AGL18 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; MADS DOMAIN PROTEIN; MIRN156 MICRORNA, ARABIDOPSIS; PROTEIN BINDING;

ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; BIMOLECULAR FLUORESCENCE COMPLEMENTATION; BINDING AFFINITY; FLOWER; FLOWERING; FLUORESCENCE ANALYSIS; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; HISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; NORTHERN BLOTTING; PHASE TRANSITION; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REPRESSOR GENE; YEAST; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; RNA INTERFERENCE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; GENE EXPRESSION REGULATION, PLANT; MADS DOMAIN PROTEINS; MICRORNAS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RNA INTERFERENCE;

EID: 84925040125     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.14348/molcells.2015.2311     Document Type: Article

References (43)

1. Adamczyk, B.J., Lehti-Shiu, M.D., and Fernandez, D.E. (2007). The MADS domain factors AGL15 and AGL18 act redundantly as repressors of the floral transition in Arabidopsis. Plant J. 50, 1007-1019.
2. Borner, R., Kampmann, G., Chandler, J., Gleissner, R., Wisman, E., Apel, K., and Melzer, S. (2000). A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J. 24, 591-599.
3. Carrington, C., and Ambros, V., (2003). Role of microRNAs in plant and animal development. Science 301, 336-338.
4. Chen, X. (2004). A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303, 2022-2025.
5. Cho, H.J., Kim, J.J., Lee, J.H., Kim, W., Jung, J., Park, C., and Ahn, J.H. (2012). SHORT VEGETATIVE PHASE (SVP) protein negatively regulates miR172 transcription via direct binding to the primiR172a promoter in Arabidopsis. FEBS Lett. 586, 2332-2337.
6. Chung, Y., Kwon, S.I., and Choe, S. (2014). Antagonistic regulation of Arabidopsis growth by brassinosteroids and abiotic stresses. Mol. Cells 37, 795-803.
7. 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.
8. Ferrandiz, C., Liljegren, S.J., and Yanofsky, M.F. (2000). Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science 289, 436-438.
9. Fernandez, D.E., Wang, C.T., Zheng, Y., Adamczyk, B.J., Singhal, R., Hall, P.K., and Perry, S.E. (2014). The MADS-domain factors AGAMOUS-LIKE15 and AGAMOUS-LIKE18, along with SHORT VEGETATIVE PHASE and AGAMOUS-LIKE24, are necessary to block floral gene expression during the vegetative phase. Plant Physiol. 165, 1591-1603.
10. Fornara, F., Montaigu, A., and Coupland, G. (2010). Snapshot: control of flowering in Arabidopsis. Cell 141, 550.e1-2.
11. Gu, X., Wang, Y., and He, Y. (2013). Photoperiodic regulation of flowering time through periodic histone deacetylation of the florigen gene FT. PLoS Biol. 11, E1001649.
12. Hehl, R., and Bülow, L. (2014). AthaMap web tools for the analysis of transcriptional and posttranscriptional regulation of gene expression in Arabidopsis thaliana. Methods Mol. Biol. 1158, 139-156.
13. Higo, K., Ugawa, Y., Iwamoto, M., and Higo, H. (1998). PLACE: a database of plant cis-acting regulatory DNA elements. Nucleic Acids Res. 26, 358-359.
14. Hill, K., Wang, H., and Perry, S.E. (2008). A transcriptional repression motif in the MADS factor AGL15 is involved in recruitment of histone deacetylase complex components. Plant J. 53, 172-185.
15. Hong, S.M., Bahn, S.C., Lyu, A., Jung, H.S., and Ahn, J.H. (2010). Identification and testing of superior reference genes for a starting pool of transcript normalization in Arabidopsis. Plant Cell Physiol. 51, 1694-1606.
16. Jack, T. (2001). Plant development going MADS. Plant Mol. Biol. 46, 515-520.
17. Jang, Y.H., Park, H., Kim, S., Lee, J.H., Suh, M.C., Chung, Y.S., Peak, K., and Kim, J. (2009) Survey of rice proteins interacting with OsFCA and OsFY proteins which are homologous to the Arabidopsis flowering time proteins, FCA and FY. Plant Cell Physiol. 5, 1479-1492.
18. Kutter, C., Schob, H., Stadler, M., Meins, F., and Si-Ammour, A. (2007). MicroRNA-mediated regulation of stomatal development in Arabidopsis. Plant Cell 19, 2417-2429.
19. 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. Gene Dev. 21, 397-402.
20. 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.
21. Lee, H., Yoo, S.J., Lee, J.H., Kim, W., Yoo, S.K., Fitzgarald, H., Carrington, J.C., and Ahn, J.H. (2010). Genetic framework for flowering-time regulation by ambient temperature-respon sivemiRNAs in Arabidopsis. Nucleic Acids Res. 38, 3081-3093.
22. Lee, J.H., Kim, J.J., and Ahn, J.H. (2012a). Role of SEPALLATA3 (SEP3) as a downstream gene of miR156-SPL3-FT circuitry in ambient temperature-responsive flowering. Plant Signal. Behav. 7, 1151-1154.
23. Lee, J.H., Park, S.H., and Ahn, J.H. (2012b). Functional conservation and diversification between rice OsMADS22/OsMADS55 and Arabidopsis SVP proteins. Plant Sci. 185-186, 97-104.
24. Nesi, N., Debeaujon I., Jond C., Stewart A.J., Jenkins G.I., Caboche M., and Lepiniec, L. (2002). The TRANSPARENT TESTA16 locus encodes the ARABIDOPSIS BSISTER MADS domain protein and is required for proper development and pigmentation of the seed coat. Plant Cell 14, 2463-2479
25. Kim, J.J., Lee, J.H., Kim, W., Jung, H.S., Huijser, P., and Ahn, J.H. (2012). The microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 module regulates ambient temperature-resp onsive flowering via FLOWERING LOCUS T in Arabidopsis thaliana. Plant Physiol. 159, 461-478.
26. Perry, S.E., Nichols, K.W., and Fernandez, D.E. (1996). The MADS domain protein AGL15 localizes to the nucleus during earlys tages of seed development. Plant Cell 8, 1977-1989.
27. Pinyopich, A., Ditta, G.S., Savidge, B., Liljegren, S.J., Baumann, E., Wisman, E., and Yanofsky, M.F. (2003). Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424, 85-88.
28. Riechmann, J.L., Krizek, B.A., and Meyerowitz, E.M. (1996). Dimerization specificity of Arabidopsis MADS domain homeotic p roteinsAPETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc. Natl. Acad. Sci. USA 93, 4793-4798.
29. Rubio-Somoza, I., and Weigel, D. (2013). Coordination of flower maturation by a regulatory circuit of three microRNAs. PLoS Genet. 9, e1003374
30. Shore, P., and Sharrocks, A.D. (1995). The MADS-box family of transcription factors. Eur. J. Biochem. 229, 1-13.
31. Tang, W., and Perry, S.E. (2003). Binding site selection for the plant MADS domain protein AGL15: an in vitro and in vivo study. J. Biol Chem. 278, 28154-28159.
32. Voinnet, O., Rivas, S., Mestre, P., and Baulcombe, D. (2003). An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949-956 .
33. Walter, M., Chaban, C., Schuutze, K., Batistic, O., Weckerma nn, K., Nake, C., Blazervic, D., Grefen, C., Schumacher, K., Oecking, C., et al. (2004). Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40, 428-438.
34. Wang, H., Tang, W., Zhu, C., and Perry, S.E. (2002). A chromatin immunoprecipitation (ChIP) approach to isolate genes regulated by AGL15, a MADS domain protein that preferentially accumulates in embryos. Plant J. 32, 831-843.
35. Wang, J., Czech, B., and Weigel, D. (2009). MiR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138, 738-749.
36. West, A.G., Shore, P., and Sharrocks, A.D. (1997). DNA binding by MADS-Box transcription factors: a molecular mechanism for differential DNA bending. Mol. Cell. Biol. 17, 2876-2887.
37. 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.
38. Xie, Z., Allen E.A., Fahlgren N., Calamar, A., Givan, S.A., and Carrington J.C. (2005). Expression of Arabidopsis MIRNA genes. Plant Physiol. 138, 2145-2154.
39. Yamaguchi, A., Wu, M., Yang, L., Wu, G., Poethig, R.S., and Wagner, D. (2009). The MicroRNA-regulated SBP-box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev. Cell 17, 268-278.
40. Yoo, S.D., Cho, Y.H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1572.
41. Yoo, S. K., Wu, X., Lee, J.S., and Ahn, J.H. (2011). AGAMOUSLIKE 6 is a floral promoter that negatively regulates the FLC/MAF clade genes and positively regulates FT in Arabidopsis. Plant J. 65, 62-76.
42. Zhang, H. and Forde, B.G. (1998). An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279, 407-409.
43. Zhang, Y., Cao G., Qu, L., and Gu, H. (2009). Characterization of Arabidopsis MYB transcription factor gene AtMYB17 and its possible regulation by LEAFY and AGL15. J. Genet. Genomics 36, 99-107.