Targeted Recruitment of the Basal Transcriptional Machinery by LNK Clock Components Controls the Circadian Rhythms of Nascent RNAs in Arabidopsis

Overview

Journal Plant Cell

Publisher Oxford University Press

Specialties Biology
Cell Biology

Date 2018 Apr 6

PMID 29618629

Citations 33

Authors

Yuan Ma

Sergio Gil

Klaus D Grasser

Paloma Mas

Affiliations

Soon will be listed here.

Abstract

The rhythms of steady-state mRNA expression pervade nearly all circadian systems. However, the mechanisms behind the rhythmic transcriptional synthesis and its correlation with circadian expression remain fully unexplored, particularly in plants. Here, we discovered a multifunctional protein complex that orchestrates the rhythms of transcriptional activity in The expression of the circadian oscillator genes and initially relies on the modular function of the clock-related factor REVEILLE8: its MYB domain provides the DNA binding specificity, while its LCL domain recruits the clock components, NIGHT LIGHT-INDUCIBLE AND CLOCK-REGULATED proteins (LNKs), to target promoters. LNKs, in turn, specifically interact with RNA Polymerase II and the transcript elongation FACT complex to rhythmically co-occupy the target loci. The functional interaction of these components is central for chromatin status, transcript initiation, and elongation as well as for proper rhythms in nascent RNAs. Thus, our findings explain how genome readout of environmental information ultimately results in rhythmic changes of gene expression.

Citing Articles

Forward genetic approach identifies a phylogenetically conserved serine residue critical for the catalytic activity of UBIQUITIN-SPECIFIC PROTEASE 12 in Arabidopsis.

Hajdu A, Nyari D, Adam E, Kim Y, Somers D, Silhavy D Sci Rep. 2024; 14(1):25273.

PMID: 39455703 PMC: 11511944. DOI: 10.1038/s41598-024-77232-w.

LIP1 Regulates the Plant Circadian Oscillator by Modulating the Function of the Clock Component GIGANTEA.

Hajdu A, Nyari D, Terecskei K, Gyula P, Adam E, Dobos O Cells. 2024; 13(17.

PMID: 39273073 PMC: 11394198. DOI: 10.3390/cells13171503.

Decoding the plant clock: a review of mathematical models for the circadian regulatory network.

Singh S, Srivastava A Plant Mol Biol. 2024; 114(5):93.

PMID: 39207587 DOI: 10.1007/s11103-024-01493-2.

Regulatory networks in plant responses to drought and cold stress.

Kim J, Kidokoro S, Yamaguchi-Shinozaki K, Shinozaki K Plant Physiol. 2024; 195(1):170-189.

PMID: 38514098 PMC: 11060690. DOI: 10.1093/plphys/kiae105.

Different elongation factors distinctly modulate RNA polymerase II transcription in Arabidopsis.

Obermeyer S, Schrettenbrunner L, Stockl R, Schwartz U, Grasser K Nucleic Acids Res. 2023; 51(21):11518-11533.

PMID: 37819035 PMC: 10681736. DOI: 10.1093/nar/gkad825.

References

Vermeulen M, Mulder K, Denissov S, Pijnappel W, Van Schaik F, Varier R . Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell. 2007; 131(1):58-69. DOI: 10.1016/j.cell.2007.08.016. View

Buratowski S . Progression through the RNA polymerase II CTD cycle. Mol Cell. 2009; 36(4):541-6. PMC: 3232742. DOI: 10.1016/j.molcel.2009.10.019. View

Perales M, Mas P . A functional link between rhythmic changes in chromatin structure and the Arabidopsis biological clock. Plant Cell. 2007; 19(7):2111-23. PMC: 1955692. DOI: 10.1105/tpc.107.050807. View

Ng H, Robert F, Young R, Struhl K . Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell. 2003; 11(3):709-19. DOI: 10.1016/s1097-2765(03)00092-3. View

Zielinski T, Moore A, Troup E, Halliday K, Millar A . Strengths and limitations of period estimation methods for circadian data. PLoS One. 2014; 9(5):e96462. PMC: 4014635. DOI: 10.1371/journal.pone.0096462. View

Gardner K, Allis C, Strahl B . Operating on chromatin, a colorful language where context matters. J Mol Biol. 2011; 409(1):36-46. PMC: 3085666. DOI: 10.1016/j.jmb.2011.01.040. View

Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, Niwa Y . Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng. 2007; 104(1):34-41. DOI: 10.1263/jbb.104.34. View

Margaritis T, Holstege F . Poised RNA polymerase II gives pause for thought. Cell. 2008; 133(4):581-4. DOI: 10.1016/j.cell.2008.04.027. View

Smolle M, Workman J . Transcription-associated histone modifications and cryptic transcription. Biochim Biophys Acta. 2012; 1829(1):84-97. PMC: 5854953. DOI: 10.1016/j.bbagrm.2012.08.008. View

10.

Xie Z, Grotewold E . Serial ChIP as a tool to investigate the co-localization or exclusion of proteins on plant genes. Plant Methods. 2008; 4:25. PMC: 2584005. DOI: 10.1186/1746-4811-4-25. View

11.

Nallamsetty S, Austin B, Penrose K, Waugh D . Gateway vectors for the production of combinatorially-tagged His6-MBP fusion proteins in the cytoplasm and periplasm of Escherichia coli. Protein Sci. 2005; 14(12):2964-71. PMC: 2253240. DOI: 10.1110/ps.051718605. View

12.

Lolas I, Himanen K, Gronlund J, Lynggaard C, Houben A, Melzer M . The transcript elongation factor FACT affects Arabidopsis vegetative and reproductive development and genetically interacts with HUB1/2. Plant J. 2009; 61(4):686-97. DOI: 10.1111/j.1365-313X.2009.04096.x. View

13.

Bogomolovas J, Simon B, Sattler M, Stier G . Screening of fusion partners for high yield expression and purification of bioactive viscotoxins. Protein Expr Purif. 2008; 64(1):16-23. DOI: 10.1016/j.pep.2008.10.003. View

14.

Yakir E, Hassidim M, Melamed-Book N, Hilman D, Kron I, Green R . Cell autonomous and cell-type specific circadian rhythms in Arabidopsis. Plant J. 2011; 68(3):520-31. DOI: 10.1111/j.1365-313X.2011.04707.x. View

15.

Clough S, Bent A . Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1999; 16(6):735-43. DOI: 10.1046/j.1365-313x.1998.00343.x. View

16.

Livak K, Schmittgen T . Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2002; 25(4):402-8. DOI: 10.1006/meth.2001.1262. View

17.

Wenden B, Toner D, Hodge S, Grima R, Millar A . Spontaneous spatiotemporal waves of gene expression from biological clocks in the leaf. Proc Natl Acad Sci U S A. 2012; 109(17):6757-62. PMC: 3340055. DOI: 10.1073/pnas.1118814109. View

18.

Perez-Garcia P, Ma Y, Yanovsky M, Mas P . Time-dependent sequestration of RVE8 by LNK proteins shapes the diurnal oscillation of anthocyanin biosynthesis. Proc Natl Acad Sci U S A. 2015; 112(16):5249-53. PMC: 4413292. DOI: 10.1073/pnas.1420792112. View

19.

Hajheidari M, Koncz C, Eick D . Emerging roles for RNA polymerase II CTD in Arabidopsis. Trends Plant Sci. 2013; 18(11):633-43. DOI: 10.1016/j.tplants.2013.07.001. View

20.

Jones D, Taylor W, Thornton J . The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 1992; 8(3):275-82. DOI: 10.1093/bioinformatics/8.3.275. View