Genic and Global Functions for Paf1C in Chromatin Modification and Gene Expression in Arabidopsis

Overview

Journal PLoS Genet

Specialty Genetics

Date 2008 Aug 30

PMID 18725930

Citations 82

Authors

Sookyung Oh

Sunchung Park

Steven van Nocker

Affiliations

Soon will be listed here.

Abstract

In budding yeast, intragenic histone modification is linked with transcriptional elongation through the conserved regulator Paf1C. To investigate Paf1C-related function in higher eukaryotes, we analyzed the effects of loss of Paf1C on histone H3 density and patterns of H3 methylated at K4, K27, and K36 in Arabidopsis genes, and integrated this with existing gene expression data. Loss of Paf1C did not change global abundance of H3K4me3 or H3K36me2 within chromatin, but instead led to a 3' shift in the distribution of H3K4me3 and a 5' shift in the distribution of H3K36me2 within genes. We found that genes regulated by plant Paf1C showed strong enrichment for both H3K4me3 and H3K27me3 and also showed a high degree of tissue-specific expression. At the Paf1C- and PcG-regulated gene FLC, transcriptional silencing and loss of H3K4me3 and H3K36me2 were accompanied by expansion of H3K27me3 into the promoter and transcriptional start regions and further enrichment of H3K27me3 within the transcribed region. These results highlight both genic and global functions for plant Paf1C in histone modification and gene expression, and link transcriptional activity with cellular memory.

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References

Pokholok D, Hannett N, Young R . Exchange of RNA polymerase II initiation and elongation factors during gene expression in vivo. Mol Cell. 2002; 9(4):799-809. DOI: 10.1016/s1097-2765(02)00502-6. View

Schwartz Y, Kahn T, Nix D, Li X, Bourgon R, Biggin M . Genome-wide analysis of Polycomb targets in Drosophila melanogaster. Nat Genet. 2006; 38(6):700-5. DOI: 10.1038/ng1817. View

Oh S, Zhang H, Ludwig P, van Nocker S . A mechanism related to the yeast transcriptional regulator Paf1c is required for expression of the Arabidopsis FLC/MAF MADS box gene family. Plant Cell. 2004; 16(11):2940-53. PMC: 527190. DOI: 10.1105/tpc.104.026062. View

Schwartz Y, Pirrotta V . Polycomb silencing mechanisms and the management of genomic programmes. Nat Rev Genet. 2006; 8(1):9-22. DOI: 10.1038/nrg1981. View

Squazzo S, Costa P, Lindstrom D, Kumer K, Simic R, Jennings J . The Paf1 complex physically and functionally associates with transcription elongation factors in vivo. EMBO J. 2002; 21(7):1764-74. PMC: 125365. DOI: 10.1093/emboj/21.7.1764. View

Zhang H, Ransom C, Ludwig P, van Nocker S . Genetic analysis of early flowering mutants in Arabidopsis defines a class of pleiotropic developmental regulator required for expression of the flowering-time switch flowering locus C. Genetics. 2003; 164(1):347-58. PMC: 1462564. DOI: 10.1093/genetics/164.1.347. View

Keogh M, Kurdistani S, Morris S, Ahn S, Podolny V, Collins S . Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell. 2005; 123(4):593-605. DOI: 10.1016/j.cell.2005.10.025. View

Rozenblatt-Rosen O, Hughes C, Nannepaga S, Shanmugam K, Copeland T, Guszczynski T . The parafibromin tumor suppressor protein is part of a human Paf1 complex. Mol Cell Biol. 2005; 25(2):612-20. PMC: 543415. DOI: 10.1128/MCB.25.2.612-620.2005. View

Adelman K, Wei W, Ardehali M, Werner J, Zhu B, Reinberg D . Drosophila Paf1 modulates chromatin structure at actively transcribed genes. Mol Cell Biol. 2005; 26(1):250-60. PMC: 1317635. DOI: 10.1128/MCB.26.1.250-260.2006. View

10.

Tenney K, Gerber M, Ilvarsonn A, Schneider J, Gause M, Dorsett D . Drosophila Rtf1 functions in histone methylation, gene expression, and Notch signaling. Proc Natl Acad Sci U S A. 2006; 103(32):11970-4. PMC: 1567682. DOI: 10.1073/pnas.0603620103. View

11.

Carrozza M, Li B, Florens L, Suganuma T, Swanson S, Lee K . Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell. 2005; 123(4):581-92. DOI: 10.1016/j.cell.2005.10.023. View

12.

Dennis E, Peacock W . Epigenetic regulation of flowering. Curr Opin Plant Biol. 2007; 10(5):520-7. DOI: 10.1016/j.pbi.2007.06.009. View

13.

Li X, Wang X, He K, Ma Y, Su N, He H . High-resolution mapping of epigenetic modifications of the rice genome uncovers interplay between DNA methylation, histone methylation, and gene expression. Plant Cell. 2008; 20(2):259-76. PMC: 2276441. DOI: 10.1105/tpc.107.056879. View

14.

Zhang X, Clarenz O, Cokus S, Bernatavichute Y, Pellegrini M, Goodrich J . Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol. 2007; 5(5):e129. PMC: 1852588. DOI: 10.1371/journal.pbio.0050129. View

15.

Koch C, Andrews R, Flicek P, Dillon S, Karaoz U, Clelland G . The landscape of histone modifications across 1% of the human genome in five human cell lines. Genome Res. 2007; 17(6):691-707. PMC: 1891331. DOI: 10.1101/gr.5704207. View

16.

Lindroth A, Shultis D, Jasencakova Z, Fuchs J, Johnson L, Schubert D . Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMETHYLASE3. EMBO J. 2004; 23(21):4286-96. PMC: 524394. DOI: 10.1038/sj.emboj.7600430. View

17.

Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P . Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science. 2002; 298(5595):1039-43. DOI: 10.1126/science.1076997. View

18.

Porter S, Washburn T, Chang M, Jaehning J . The yeast pafl-rNA polymerase II complex is required for full expression of a subset of cell cycle-regulated genes. Eukaryot Cell. 2002; 1(5):830-42. PMC: 126743. DOI: 10.1128/EC.1.5.830-842.2002. View

19.

Schmid M, Davison T, Henz S, Pape U, Demar M, Vingron M . A gene expression map of Arabidopsis thaliana development. Nat Genet. 2005; 37(5):501-6. DOI: 10.1038/ng1543. View

20.

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