The plant Mediator and its role in noncoding RNA production

Yun Ju KIM, Xuemei CHEN

PDF(196 KB)
PDF(196 KB)
Front. Biol. ›› 2011, Vol. 6 ›› Issue (2) : 125-132. DOI: 10.1007/s11515-011-1133-7
REVIEW

The plant Mediator and its role in noncoding RNA production

Author information +
History +

Abstract

Mediator, a conserved multiprotein complex in animals, plants, and fungi, is a cofactor of RNA polymerase II (Pol II). It is known to promote basal Pol II-mediated transcription as well as bridge sequence-specific transcriptional regulators and Pol II to integrate regulatory information. Pol II transcribes not only protein-coding genes but also intergenic regions to generate noncoding RNAs such as small RNAs (microRNAs and small interfering RNAs) and long noncoding RNAs. Intriguingly, two plant-specific polymerases, Pol IV and Pol V, have evolved from Pol II and play a role in the production of small interfering RNAs and long noncoding RNAs at heterochromatic regions to maintain genome stability through transcriptional gene silencing (TGS). Recent studies have defined the composition of the plant Mediator and evaluated its role in noncoding RNA production in relationship to Pol II, Pol IV and Pol V. Here, we review the functions of Mediator and that of noncoding RNAs generated by Pol II, Pol IV and Pol V in plants, and discuss a role of Mediator in epigenetic regulation via noncoding RNA production.

Keywords

small RNA / noncoding RNA / Mediator / Pol II / Pol IV / Pol V

Cite this article

Download citation ▾
Yun Ju KIM, Xuemei CHEN. The plant Mediator and its role in noncoding RNA production. Front Biol, 2011, 6(2): 125‒132 https://doi.org/10.1007/s11515-011-1133-7

References

[1]
Ansari S A, He Q, Morse R H (2009). Mediator complex association with constitutively transcribed genes in yeast. Proc Natl Acad Sci USA, 106(39): 16734–16739
CrossRef Pubmed Google scholar
[2]
Autran D, Jonak C, Belcram K, Beemster G T, Kronenberger J, Grandjean O, Inzé D, Traas J (2002). Cell numbers and leaf development in Arabidopsis: a functional analysis of the STRUWWELPETER gene. EMBO J, 21(22): 6036–6049
CrossRef Pubmed Google scholar
[3]
Bäckström S, Elfving N, Nilsson R, Wingsle G, Björklund S (2007). Purification of a plant mediator from Arabidopsis thaliana identifies PFT1 as the Med25 subunit. Mol Cell, 26(5): 717–729
CrossRef Pubmed Google scholar
[4]
Baek H J, Kang Y K, Roeder R G (2006). Human Mediator enhances basal transcription by facilitating recruitment of transcription factor IIB during preinitiation complex assembly. J Biol Chem, 281(22): 15172–15181
CrossRef Pubmed Google scholar
[5]
Bari R, Datt Pant B, Stitt M, Scheible W R (2006). PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol, 141(3): 988–999
CrossRef Pubmed Google scholar
[6]
Black J C, Choi J E, Lombardo S R, Carey M (2006). A mechanism for coordinating chromatin modification and preinitiation complex assembly. Mol Cell, 23(6): 809–818
CrossRef Pubmed Google scholar
[7]
Carlson M, Osmond B C, Botstein D (1981). Mutants of yeast defective in sucrose utilization. Genetics, 98(1): 25–40
Pubmed
[8]
Casamassimi A, Napoli C (2007). Mediator complexes and eukaryotic transcription regulation: an overview. Biochimie, 89(12): 1439–1446
CrossRef Pubmed Google scholar
[9]
Cerdán P D, Chory J (2003). Regulation of flowering time by light quality. Nature, 423(6942): 881–885
CrossRef Pubmed Google scholar
[10]
Chen X (2009). Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol, 25(1): 21–44
CrossRef Pubmed Google scholar
[11]
Chi Y, Huddleston M J, Zhang X, Young R A, Annan R S, Carr S A, Deshaies R J (2001). Negative regulation of Gcn4 and Msn2 transcription factors by Srb10 cyclin-dependent kinase. Genes Dev, 15(9): 1078–1092
CrossRef Pubmed Google scholar
[12]
Dhawan R, Luo H, Foerster A M, Abuqamar S, Du H N, Briggs S D, Mittelsten Scheid O, Mengiste T (2009). HISTONE MONOUBIQUITINATION1 interacts with a subunit of the mediator complex and regulates defense against necrotrophic fungal pathogens in Arabidopsis. Plant Cell, 21(3): 1000–1019
CrossRef Pubmed Google scholar
[13]
Ding N, Zhou H, Esteve P O, Chin H G, Kim S, Xu X, Joseph S M, Friez M J, Schwartz C E, Pradhan S, Boyer T G (2008). Mediator links epigenetic silencing of neuronal gene expression with x-linked mental retardation. Mol Cell, 31(3): 347–359
CrossRef Pubmed Google scholar
[14]
Dotson M R, Yuan C X, Roeder R G, Myers L C, Gustafsson C M, Jiang Y W, Li Y, Kornberg R D, Asturias F J (2000). Structural organization of yeast and mammalian mediator complexes. Proc Natl Acad Sci USA, 97(26): 14307–14310
CrossRef Pubmed Google scholar
[15]
El-Shami M, Pontier D, Lahmy S, Braun L, Picart C, Vega D, Hakimi M A, Jacobsen S E, Cooke R, Lagrange T (2007). Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes Dev, 21(20): 2539–2544
CrossRef Pubmed Google scholar
[16]
Fan X, Chou D M, Struhl K (2006). Activator-specific recruitment of Mediator in vivo. Nat Struct Mol Biol, 13(2): 117–120
CrossRef Pubmed Google scholar
[17]
Fan X, Struhl K (2009). Where does mediator bind in vivo? PLoS ONE, 4(4): e5029
CrossRef Pubmed Google scholar
[18]
Gonzalez D, Bowen A J, Carroll T S, Conlan R S (2007). The transcription corepressor LEUNIG interacts with the histone deacetylase HDA19 and mediator components MED14 (SWP) and CDK8 (HEN3) to repress transcription. Mol Cell Biol, 27(15): 5306–5315
CrossRef Pubmed Google scholar
[19]
Guglielmi B, van Berkum N L, Klapholz B, Bijma T, Boube M, Boschiero C, Bourbon H M, Holstege F C, Werner M (2004). A high resolution protein interaction map of the yeast Mediator complex. Nucleic Acids Res, 32(18): 5379–5391
CrossRef Pubmed Google scholar
[20]
Hallberg M, Polozkov G V, Hu G Z, Beve J, Gustafsson C M, Ronne H, Björklund S (2004). Site-specific Srb10-dependent phosphorylation of the yeast Mediator subunit Med2 regulates gene expression from the 2-microm plasmid. Proc Natl Acad Sci USA, 101(10): 3370–3375
CrossRef Pubmed Google scholar
[21]
Han S J, Lee J S, Kang J S, Kim Y J (2001). Med9/Cse2 and Gal11 modules are required for transcriptional repression of distinct group of genes. J Biol Chem, 276(40): 37020–37026
CrossRef Pubmed Google scholar
[22]
Havecker E R, Wallbridge L M, Hardcastle T J, Bush M S, Kelly K A, Dunn R M, Schwach F, Doonan J H, Baulcombe D C (2010). The Arabidopsis RNA-directed DNA methylation argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell, 22(2): 321–334
CrossRef Pubmed Google scholar
[23]
Hengartner C J, Myer V E, Liao S M, Wilson C J, Koh S S, Young R A (1998). Temporal regulation of RNA polymerase II by Srb10 and Kin28 cyclin-dependent kinases. Mol Cell, 2(1): 43–53
CrossRef Pubmed Google scholar
[24]
Herr A J, Jensen M B, Dalmay T, Baulcombe D C (2005). RNA polymerase IV directs silencing of endogenous DNA. Science, 308(5718): 118–120
CrossRef Pubmed Google scholar
[25]
Hirst M, Kobor M S, Kuriakose N, Greenblatt J, Sadowski I (1999). GAL4 is regulated by the RNA polymerase II holoenzyme-associated cyclin-dependent protein kinase SRB10/CDK8. Mol Cell, 3(5): 673–678
CrossRef Pubmed Google scholar
[26]
Holstege F C, Jennings E G, Wyrick J J, Lee T I, Hengartner C J, Green M R, Golub T R, Lander E S, Young R A (1998). Dissecting the regulatory circuitry of a eukaryotic genome. Cell, 95(5): 717–728
CrossRef Pubmed Google scholar
[27]
Huang L, Jones A M, Searle I, Patel K, Vogler H, Hubner N C, Baulcombe D C (2009). An atypical RNA polymerase involved in RNA silencing shares small subunits with RNA polymerase II. Nat Struct Mol Biol, 16(1): 91–93
CrossRef Pubmed Google scholar
[28]
Kang J S, Kim S H, Hwang M S, Han S J, Lee Y C, Kim Y J (2001). The structural and functional organization of the yeast mediator complex. J Biol Chem, 276(45): 42003–42010
CrossRef Pubmed Google scholar
[29]
Kanno T, Huettel B, Mette M F, Aufsatz W, Jaligot E, Daxinger L, Kreil D P, Matzke M, Matzke A J (2005). Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nat Genet, 37(7): 761–765
CrossRef Pubmed Google scholar
[30]
Kawashima C G, Yoshimoto N, Maruyama-Nakashita A, Tsuchiya Y N, Saito K, Takahashi H, Dalmay T (2009). Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant J, 57(2): 313–321
CrossRef Pubmed Google scholar
[31]
Kidd B N, Edgar C I, Kumar K K, Aitken E A, Schenk P M, Manners J M, Kazan K (2009). The mediator complex subunit PFT1 is a key regulator of jasmonate-dependent defense in Arabidopsis. Plant Cell, 21(8): 2237–2252
CrossRef Pubmed Google scholar
[32]
Kim Y J, Zheng B, Yu Y, Won S Y, Mo B, Chen X (2011). The role of Mediator in small and long noncoding RNA production in Arabidopsis thaliana. EMBO J, (In press)
CrossRef Pubmed Google scholar
[33]
Krebs A R, Demmers J, Karmodiya K, Chang N C, Chang A C, Tora L (2010). ATAC and Mediator coactivators form a stable complex and regulate a set of non-coding RNA genes. EMBO Rep, 11(7): 541–547
CrossRef Pubmed Google scholar
[34]
Kuras L, Struhl K (1999). Binding of TBP to promoters in vivo is stimulated by activators and requires Pol II holoenzyme. Nature, 399(6736): 609–613
CrossRef Pubmed Google scholar
[35]
Lahmy S, Pontier D, Cavel E, Vega D, El-Shami M, Kanno T, Lagrange T (2009). PolV(PolIVb) function in RNA-directed DNA methylation requires the conserved active site and an additional plant-specific subunit. Proc Natl Acad Sci USA, 106(3): 941–946
CrossRef Pubmed Google scholar
[36]
Larivière L, Geiger S, Hoeppner S, Röther S, Strässer K, Cramer P (2006). Structure and TBP binding of the Mediator head subcomplex Med8-Med18-Med20. Nat Struct Mol Biol, 13(10): 895–901
CrossRef Pubmed Google scholar
[37]
Lee Y C, Park J M, Min S, Han S J, Kim Y J (1999). An activator binding module of yeast RNA polymerase II holoenzyme. Mol Cell Biol, 19(4): 2967–2976
Pubmed
[38]
Li C F, Pontes O, El-Shami M, Henderson I R, Bernatavichute Y V, Chan S W, Lagrange T, Pikaard C S, Jacobsen S E (2006). An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell, 126(1): 93–106
CrossRef Pubmed Google scholar
[39]
Li J, Yang Z, Yu B, Liu J, Chen X (2005). Methylation protects miRNAs and siRNAs from a 3′-end uridylation activity in Arabidopsis. Curr Biol, 15(16): 1501–1507
CrossRef Pubmed Google scholar
[40]
Liu Y, Kung C, Fishburn J, Ansari A Z, Shokat K M, Hahn S (2004). Two cyclin-dependent kinases promote RNA polymerase II transcription and formation of the scaffold complex. Mol Cell Biol, 24(4): 1721–1735
CrossRef Pubmed Google scholar
[41]
Liu Z, Meyerowitz E M (1995). LEUNIG regulates AGAMOUS expression in Arabidopsis flowers. Development, 121(4): 975–991
Pubmed
[42]
Malik S, Roeder R G (2000). Transcriptional regulation through Mediator-like coactivators in yeast and metazoan cells. Trends Biochem Sci, 25(6): 277–283
CrossRef Pubmed Google scholar
[43]
Malik S, Roeder R G (2010). The metazoan Mediator co-activator complex as an integrative hub for transcriptional regulation. Nat Rev Genet, 11(11): 761–772
CrossRef Pubmed Google scholar
[44]
Megraw M, Baev V, Rusinov V, Jensen S T, Kalantidis K, Hatzigeorgiou A G (2006). MicroRNA promoter element discovery in Arabidopsis. RNA, 12(9): 1612–1619
CrossRef Pubmed Google scholar
[45]
Mittler G, Kremmer E, Timmers H T, Meisterernst M (2001). Novel critical role of a human Mediator complex for basal RNA polymerase II transcription. EMBO Rep, 2(9): 808–813
CrossRef Pubmed Google scholar
[46]
Mosher R A, Schwach F, Studholme D, Baulcombe D C (2008). PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis. Proc Natl Acad Sci USA, 105(8): 3145–3150
CrossRef Pubmed Google scholar
[47]
Näär A M, Taatjes D J, Zhai W, Nogales E, Tjian R (2002). Human CRSP interacts with RNA polymerase II CTD and adopts a specific CTD-bound conformation. Genes Dev, 16(11): 1339–1344
CrossRef Pubmed Google scholar
[48]
Neigeborn L, Carlson M (1984). Genes affecting the regulation of SUC2 gene expression by glucose repression in Saccharomyces cerevisiae. Genetics, 108(4): 845–858
Pubmed
[49]
Nelson C, Goto S, Lund K, Hung W, Sadowski I (2003). Srb10/Cdk8 regulates yeast filamentous growth by phosphorylating the transcription factor Ste12. Nature, 421(6919): 187–190
CrossRef Pubmed Google scholar
[50]
Onodera Y, Haag J R, Ream T, Nunes P C, Pontes O, Pikaard C S (2005). Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell, 120(5): 613–622
CrossRef Pubmed Google scholar
[51]
Ooi L, Wood I C (2007). Chromatin crosstalk in development and disease: lessons from REST. Nat Rev Genet, 8(7): 544–554
CrossRef Pubmed Google scholar
[52]
Park J M, Kim H S, Han S J, Hwang M S, Lee Y C, Kim Y J (2000). In vivo requirement of activator-specific binding targets of mediator. Mol Cell Biol, 20(23): 8709–8719
CrossRef Pubmed Google scholar
[53]
Ream T S, Haag J R, Wierzbicki A T, Nicora C D, Norbeck A D, Zhu J K, Hagen G, Guilfoyle T J, Pasa-Tolić L, Pikaard C S (2009). Subunit compositions of the RNA-silencing enzymes Pol IV and Pol V reveal their origins as specialized forms of RNA polymerase II. Mol Cell, 33(2): 192–203
CrossRef Pubmed Google scholar
[54]
Reese J C (2003). Basal transcription factors. Curr Opin Genet Dev, 13(2): 114–118
CrossRef Pubmed Google scholar
[55]
Sato S, Tomomori-Sato C, Banks C A, Sorokina I, Parmely T J, Kong S E, Jin J, Cai Y, Lane W S, Brower C S, Conaway R C, Conaway J W (2003). Identification of mammalian Mediator subunits with similarities to yeast Mediator subunits Srb5, Srb6, Med11, and Rox3. J Biol Chem, 278(17): 15123–15127
CrossRef Pubmed Google scholar
[56]
Sikorski T W, Buratowski S (2009). The basal initiation machinery: beyond the general transcription factors. Curr Opin Cell Biol, 21(3): 344–351
CrossRef Pubmed Google scholar
[57]
Simchen G, Winston F, Styles C A, Fink G R (1984). Ty-mediated gene expression of the LYS2 and HIS4 genes of Saccharomyces cerevisiae is controlled by the same SPT genes. Proc Natl Acad Sci USA, 81(8): 2431–2434
CrossRef Pubmed Google scholar
[58]
Stern M, Jensen R, Herskowitz I (1984). Five SWI genes are required for expression of the HO gene in yeast. J Mol Biol, 178(4): 853–868
CrossRef Pubmed Google scholar
[59]
Struhl K (1996). Chromatin structure and RNA polymerase II connection: implications for transcription. Cell, 84(2): 179–182
CrossRef Pubmed Google scholar
[60]
Sun X, Zhang Y, Cho H, Rickert P, Lees E, Lane W, Reinberg D (1998). NAT, a human complex containing Srb polypeptides that functions as a negative regulator of activated transcription. Mol Cell, 2(2): 213–222
CrossRef Pubmed Google scholar
[61]
Suzuki Y, Nogi Y, Abe A, Fukasawa T (1988). GAL11 protein, an auxiliary transcription activator for genes encoding galactose-metabolizing enzymes in Saccharomyces cerevisiae. Mol Cell Biol, 8(11): 4991–4999
Pubmed
[62]
Taatjes D J, Schneider-Poetsch T, Tjian R (2004). Distinct conformational states of nuclear receptor-bound CRSP-Med complexes. Nat Struct Mol Biol, 11(7): 664–671
CrossRef Pubmed Google scholar
[63]
Takagi Y, Calero G, Komori H, Brown J A, Ehrensberger A H, Hudmon A, Asturias F, Kornberg R D (2006). Head module control of mediator interactions. Mol Cell, 23(3): 355–364
CrossRef Pubmed Google scholar
[64]
Thomas M C, Chiang C M (2006). The general transcription machinery and general cofactors. Crit Rev Biochem Mol Biol, 41(3): 105–178
CrossRef Pubmed Google scholar
[65]
Thompson C M, Young R A (1995). General requirement for RNA polymerase II holoenzymes in vivo. Proc Natl Acad Sci USA, 92(10): 4587–4590
CrossRef Pubmed Google scholar
[66]
van de Peppel J, Kettelarij N, van Bakel H, Kockelkorn T T, van Leenen D, Holstege F C (2005). Mediator expression profiling epistasis reveals a signal transduction pathway with antagonistic submodules and highly specific downstream targets. Mol Cell, 19(4): 511–522
CrossRef Pubmed Google scholar
[67]
Vincent O, Kuchin S, Hong S P, Townley R, Vyas V K, Carlson M (2001). Interaction of the Srb10 kinase with Sip4, a transcriptional activator of gluconeogenic genes in Saccharomyces cerevisiae. Mol Cell Biol, 21(17): 5790–5796
CrossRef Pubmed Google scholar
[68]
Wang W, Chen X (2004). HUA ENHANCER3 reveals a role for a cyclin-dependent protein kinase in the specification of floral organ identity in Arabidopsis. Development, 131(13): 3147–3156
CrossRef Pubmed Google scholar
[69]
Wierzbicki A T, Haag J R, Pikaard C S (2008). Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell, 135(4): 635–648
CrossRef Pubmed Google scholar
[70]
Wollenberg A C, Strasser B, Cerdán P D, Amasino R M (2008). Acceleration of flowering during shade avoidance in Arabidopsis alters the balance between FLOWERING LOCUS C-mediated repression and photoperiodic induction of flowering. Plant Physiol, 148(3): 1681–1694
CrossRef Pubmed Google scholar
[71]
Xie Z, Allen E, Fahlgren N, Calamar A, Givan S A, Carrington J C (2005). Expression of Arabidopsis MIRNA genes. Plant Physiol, 138(4): 2145–2154
CrossRef Pubmed Google scholar
[72]
Xie Z, Johansen L K, Gustafson A M, Kasschau K D, Lellis A D, Zilberman D, Jacobsen S E, Carrington J C (2004). Genetic and functional diversification of small RNA pathways in plants. PLoS Biol, 2(5): E104
CrossRef Pubmed Google scholar
[73]
Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T (2009). SQUAMOSA promoter binding protein-like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell, 21(1): 347–361
CrossRef Pubmed Google scholar
[74]
Yudkovsky N, Ranish J A, Hahn S (2000). A transcription reinitiation intermediate that is stabilized by activator. Nature, 408(6809): 225–229
CrossRef Pubmed Google scholar
[75]
Zhang X, Henderson I R, Lu C, Green P J, Jacobsen S E (2007). Role of RNA polymerase IV in plant small RNA metabolism. Proc Natl Acad Sci USA, 104(11): 4536–4541
CrossRef Pubmed Google scholar
[76]
Zheng B, Wang Z, Li S, Yu B, Liu J Y, Chen X (2009). Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev, 23(24): 2850–2860
CrossRef Pubmed Google scholar
[77]
Zheng X, Zhu J, Kapoor A, Zhu J K (2007). Role of Arabidopsis AGO6 in siRNA accumulation, DNA methylation and transcriptional gene silencing. EMBO J, 26(6): 1691–1701
CrossRef Pubmed Google scholar
[78]
Zilberman D, Cao X, Jacobsen S E (2003). ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science, 299(5607): 716–719
CrossRef Pubmed Google scholar

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg
PDF(196 KB)

Accesses

Citations

Detail

Sections
Recommended

/