The Arabidopsis Mediator CDK8 module genes CCT (MED12) and GCT (MED13) are global regulators of developmental phase transitions

Development (Cambridge)

Volumn 141, Issue 23, 2014, Pages 4580-4589

  Stewart Gillmor, C ^b   Silva Ortega, Claudia O ^a   Willmann, Matthew R ^b   Buendía Monreal, Manuel ^a   Poethig, R Scott ^b  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Arabidopsis thaliana; FLC; MED12; MED13; Mediator; miR156

Indexed keywords

GIBBERELLIC ACID; MICRORNA; MICRORNA 156; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; CENTRAL CITY PROTEIN, ARABIDOPSIS; FLF PROTEIN, ARABIDOPSIS; GRAND CENTRAL PROTEIN, ARABIDOPSIS; MADS DOMAIN PROTEIN; MIRN156 MICRORNA, ARABIDOPSIS; PRIMER DNA; REPRESSOR PROTEIN;

ARABIDOPSIS THALIANA; ARTICLE; BRACT; CCT GENE; CDK8 GENE; CONTROLLED STUDY; DEVELOPMENTAL GENE; DEVELOPMENTAL STAGE; EMBRYO DEVELOPMENT; FLOWERING; GCT GENE; GENE EXPRESSION; GENE REPRESSION; GENETIC REGULATION; GENOTYPE; GERMINATION; MICROARRAY ANALYSIS; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHASE TRANSITION; PHENOTYPE; PLANT DEVELOPMENT; PLANT GENE; PLANT GROWTH; PLANT LEAF; REGULATOR GENE; REPRESSOR GENE; SEEDLING; TRICHOME; UPREGULATION; ARABIDOPSIS; EMBRYOLOGY; FLOWER; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA PRIMERS; FLOWERS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GERMINATION; MADS DOMAIN PROTEINS; MICROARRAY ANALYSIS; MICRORNAS; PLANT DEVELOPMENT; REAL-TIME POLYMERASE CHAIN REACTION; REPRESSOR PROTEINS;

EID: 84911490418     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.111229     Document Type: Article

References (61)

1. Abedon, B. G., Hatfield, R. D. and Tracy, W. F. (2006). Cell wall composition in juvenile and adult leaves of maize (Zea mays L.). J. Agric. Food Chem. 54, 3896-3900.
2. Amasino, R. (2010). Seasonal and developmental timing of flowering. Plant J. 61, 1001-1013.
3. 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.
4. Bassel, G. W., Lan, H., Glaab, E., Gibbs, D. J., Gerjets, T., Krasnogor, N., Bonner, A. J., Holdsworth, M. J. and Provart, N. J. (2011). Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. Proc. Natl. Acad. Sci. USA 108, 9709-9714.
5. Bastow, R., Mylne, J. S., Lister, C., Lippman, Z., Martienssen, R. A. and Dean, C. (2004). Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427, 164-167.
6. Boege, K. and Marquis, R. J. (2005). Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol. Evol. 20, 441-448.
7. Bourbon, H.-M. (2008). Comparative genomics supports a deep evolutionary origin for the large, four-module transcriptional mediator complex. Nucleic Acids Res. 36, 3993-4008.
8. Bouyer, D., Roudier, F., Heese, M., Andersen, E. D., Gey, D., Nowack, M. K., Goodrich, J., Renou, J.-P., Grini, P. E., Colot, V. et al. (2011). Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLoS Genet. 7, e1002014.
9. Carlsten, J. O. P., Zhu, X. and Gustafsson, C. M. (2013). The multitalented Mediator complex. Trends Biochem. Sci. 38, 531-537.
10. Carrera, I., Janody, F., Leeds, N., Duveau, F. and Treisman, J. E. (2008). Pygopus activates Wingless target gene transcription through the mediator complex subunits Med12 and Med13. Proc. Natl. Acad. Sci. USA 105, 6644-6649.
11. Chandler, M. A., Riedeman, E. S. and Tracy, W. F. (2011). Vegetative phase change in maize: biotic resistance and agronomic performance. Plant Breed. Rev. 34, 131-160.
12. Chaturvedi, C.-P., Hosey, A. M., Palii, C., Perez-Iratxeta, C., Nakatani, Y., Ranish, J. A., Dilworth, F. J. and Brand, M. (2009). Dual role for the methyltransferase G9a in the maintenance of β-globin gene transcription in adult erythroid cells. Proc. Natl. Acad. Sci. USA 106, 18303-18308.
13. Chaturvedi, C.-P., Somasundaram, B., Singh, K., Carpenedo, R. L., Stanford, W. L., Dilworth, F. J. and Brand, M. (2012). Maintenance of gene silencing by the coordinate action of the H3K9 methyltransferase G9a/KMT1C and the H3K4 demethylase Jarid1a/KDM5A. Proc. Natl. Acad. Sci. USA 109, 18845-18850.
14. Chien, J. C. and Sussex, I. M. (1996). Differential regulation of trichome formation on the adaxial and abaxial leaf surfaces by gibberellins and photoperiod in Arabidopsis thaliana (L.) Heynh. Plant Physiol. 111, 1321-1328.
15. Chuck, G., Cigan, A. M., Saeteurn, K. and Hake, S. (2007). The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat. Genet. 39, 544-549.
16. Crevillén, P. and Dean, C. (2011). Regulation of the floral repressor gene FLC: the complexity of transcription in a chromatin context. Curr. Opin. Plant Biol. 14, 38-44.
17. Dennis, G., Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C. and Lempicki, R. A. (2003). DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4, P3.
18. Ding, N., Zhou, H., Esteve, P.-O., Chin, H. G., Kim, S., Xu, X., Joseph, S. M., Friez, M. J., Schwartz, C. E., Pradham, S. et al. (2008). Mediator links epigenetic silencing of neuronal gene expression with x-linked mental retardation. Mol. Cell 31, 347-359.
19. Donner, A. J., Szostek, S., Hoover, J. M. and Espinosa, J. M. (2007). CDK8 is a stimulus-specific positive coregulator of p53 target genes. Mol. Cell 27, 121-133.
20. Elmlund, H., Baraznenok, V., Lindahl, M., Samuelsen, C. O., Koeck, P. J. B., Holmberg, S., Hebert, H. and Gustafsson, C. M. (2006). The cyclin-dependent kinase 8 module sterically blocks Mediator interactions with RNA polymerase II. Proc. Natl. Acad. Sci. USA 103, 15788-15793.
21. Evans, M. M. S. and Poethig, R. S. (1995). Gibberellins promote vegetative phase change and reproductive maturity in maize. Plant Physiol. 108, 475-487.
22. Franco-Zorrilla, J. M., Valli, A., Todesco, M., Mateos, I., Puga, M. I., Rubio- Somoza, I., Leyva, A.,Weigel, D., García, J. A. and Paz-Ares, J. (2007). Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 39, 1033-1037.
23. Geuten, K. and Coenen, H. (2013). Heterochronic genes in plant evolution and development. Front. Plant Sci. 4, 381.
24. Gillmor, C. S., Park, M. Y., Smith, M. R., Pepitone, R., Kerstetter, R. A. and Poethig, R. S. (2010). The MED12-MED13 module of Mediator regulates the timing of embryo patterning in Arabidopsis. Development 137, 113-122.
25. Gould, S. J. (1977). Ontogeny and Phylogeny. Cambridge, MA, USA: Belknap Press of Harvard University Press.
26. Han, S. and Kim, D. (2006). AtRTPrimer: database for Arabidopsis genome-wide homogeneous and specific RT-PCR primer-pairs. BMC Bioinformatics 7, 179.
27. Huang, D. W., Sherman, B. T. and Lempicki, R. A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57.
28. Huijser, P. and Schmid, M. (2011). The control of developmental phase transitions in plants. Development 138, 4117-4129.
29. Imura, Y., Kobayashi, Y., Yamamoto, S., Furutani, M., Tasaka, M., Abe, M. and Araki, T. (2012). CRYPTIC PRECOCIOUS/MED12 is a novel flowering regulator with multiple target steps in Arabidopsis. Plant Cell Physiol. 53, 287-303.
30. Ito, J., Sono, T., Tasaka, M. and Furutani, M. (2011). MACCHI-BOU2 is required for early embryo patterning and cotyledon organogenesis in Arabidopsis. Plant Cell Physiol. 52, 539-552.
31. Janody, F., Martirosyan, Z., Benlali, A. and Treisman, J. E. (2003). Two subunits of the Drosophila Mediator complex act together to control cell affinity. Development 130, 3691-3701.
32. Kim, Y. J., Zheng, B., Yu, Y., Won, S. Y., Mo, B. and Chen, X. (2011). The role of Mediator in small and long noncoding RNA production in Arabidopsis thaliana. EMBO J. 30, 814-822.
33. Knuesel, M. T., Meyer, K. D., Bernecky, C. and Taatjes, D. J. (2009). The human CDK8 subcomplex is a molecular switch that controls Mediator coactivator function. Genes Dev. 23, 439-451.
34. Koornneef, M. and van der Veen, J. H. (1980). Induction and analysis of Gibberellin sensitive mutants in Arabidopsis thaliana (L.) Heynh. Theoret. Appl. Genet. 58, 257-263.
35. Kuuluvainen, E., Hakala, H., Havula, E., Estimé, M. S., Rämet, M., Hietakangas, V. and Mäkelä, T. P. (2014). Cyclin-dependent kinase 8 module expression profiling reveals requirement of Mediator subunits 12 and 13 for transcription of Serpent-dependent innate immunity genes in Drosophila. J. Biol. Chem. 289, 16252-16261.
36. Lai, Z., Schluttenhofer, C. M., Bhide, K., Shreve, J., Thimmapuram, J., Lee, S. Y., Yun, D.-J. and Mengiste, T. (2014). MED18 interaction with distinct transcription factors regulates multiple plant functions. Nat. Commun. 5, 3064.
37. 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.
38. Neff, M. M., Turk, E. and Kalishman, M. (2002). Web-based primer design for single nucleotide polymorphism analysis. Trends Genet. 18, 613-615.
39. Nemet, J., Jelicic, B., Rubelj, I. and Sopta, M. (2013). The two faces of Cdk8, a positive/negative regulator of transcription. Biochimie 97, 22-27.
40. Ogas, J., Cheng, J.-C., Sung, Z. R. and Somerville, C. (1997). Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant. Science 277, 91-94.
41. Poethig, R. S. (2013). Vegetative phase change and shoot maturation in plants. Curr. Top. Dev. Biol. 105, 125-152.
42. Röbbelen, G. (1957). Uber heterophyllie bei Arabidopsis thaliana (L.). Heynh Berichte der Deutschen Botanischen Gesellschaft 70, 39-44.
43. Samuelsen, C. O., Baraznenok, V., Khorosjutina, O., Spahr, H., Kieselbach, T., Holmberg, S. and Gustafsson, C. M. (2003). TRAP230/ARC240 and TRAP240/ ARC250 Mediator subunits are functionally conserved through evolution. Proc. Natl. Acad. Sci. USA 100, 6422-6427.
44. Schmid, M., Davison, T. S., Henz, S. R., Pape, U. J., Demar, M., Vingron, M., Schölkopf, B.,Weigel, D. and Lohmann, J. U. (2005). A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37, 501-506.
45. Telfer,A.,Bollman, K. M. andPoethig,R.S. (1997).Phase change and the regulation of trichome distribution in Arabidopsis thaliana. Development 124, 645-654.
46. Tsai, K.-L., Sato, S., Tomomori-Sato, C., Conaway, R. C., Conaway, J. W. and Asturias, F. J. (2013). A conserved Mediator-CDK8 kinase module association regulates Mediator-RNA polymerase II interaction. Nat. Struct. Mol. Biol. 20, 611-619.
47. van de Peppel, J., Kettelarij, N., van Bakel, H., Kockelkorn, T. T. J. P., van Leenen, D. and Holstege, F. C. P. (2005). Mediator expression profiling epistasis reveals a signal transduction pathway with antagonistic submodules and highly specific downstream targets. Mol. Cell 19, 511-522.
48. Wang, W. and Chen, X. (2004). HUA ENHANCER3 reveals a role for a cyclindependent protein kinase in the specification of floral organ identity in Arabidopsis. Development 131, 3147-3156.
49. Wang, J.-W., Czech, B. andWeigel, D. (2009). miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138, 738-749.
50. Willmann, M. R., Mehalick, A. J., Packer, R. L. and Jenik, P. D. (2011). MicroRNAs regulate the timing of embryo maturation in Arabidopsis. Plant Physiol. 155, 1871-1884.
51. Wilson, R. N., Heckman, J.W. and Somerville, C. R. (1992). Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiol. 100, 403-408.
52. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G. V. and Provart, N. J. (2007). An 'Electronic Fluorescent Pictograph' browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2, e718.
53. 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.
54. 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.
55. Yang, L., Conway, S. R. and Poethig, R. S. (2011). Vegetative phase change is mediated by a leaf-derived signal that represses the transcription of miR156. Development 138, 245-249.
56. Yang, L., Xu, M., Koo, Y., He, J. and Poethig, R. S. (2013). Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing the expression of MIR156A and MIR156C. eLife 2, e00260.
57. Yin, Y.-W. and Wang, G. (2014). The Mediator complex: a master coordinator of transcription and cell lineage development. Development 141, 977-987.
58. Yoda, A., Kouike, H., Okano, H. and Sawa, H. (2005). Components of the transcriptional Mediator complex are required for asymmetric cell division in C. elegans. Development 132, 1885-1893.
59. Yu, S., Galvão, V. C., Zhang, Y.-C., Horrer, D., Zhang, T.-Q., Hao, Y.-H., Feng, Y.- Q., Wang, S., Schmid, M. and Wang, J.-W. (2012). Gibberellin regulates the Arabidopsis floral transition through miR156-targeted SQUAMOSA PROMOTER BINDING-LIKE transcription factors. Plant Cell 24, 3320-3332.
60. Yu, S., Cao, L., Zhou, C.-M., Zhang, T.-Q., Lian, H., Sun, Y., Wu, J., Huang, J., Wang, G. and Wang, J.-W. (2013). Sugar is an endogenous cue for juvenile-toadult phase transition in plants. eLife 2, e00269.
61. Zhang, H., Rider, S. D., Henderson, J. T., Fountain, M., Chuang, K., Kandachar, V., Simons, A., Edenberg, H. J., Romero-Severson, J., Muir, W. M. et al. (2008). The CHD3 remodeler PICKLE promotes trimethylation of histone H3 lysine 27. J. Biol. Chem. 283, 22637-22648.