DNA methylation signature of intergenic region involves in nucleosome remodeler DDM1-mediated repression of aberrant gene transcriptional read-through

Xiaojing Yan; Xiaomei Dong; Lei Liu; Yongqing Yang; Jinsheng Lai; Yan Guo

doi:10.1016/j.jgg.2016.03.010

Volume 43 Issue 8

Aug. 2016

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Article Navigation > Journal of Genetics and Genomics > 2016 > 43(8): 513-523

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DNA methylation signature of intergenic region involves in nucleosome remodeler DDM1-mediated repression of aberrant gene transcriptional read-through

doi: 10.1016/j.jgg.2016.03.010

State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100193, China

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Corresponding author: E-mail address: guoyan@cau.edu.cn (Yan Guo)
Received Date: 2015-12-22
Accepted Date: 2016-03-30
Rev Recd Date: 2016-03-28

Available Online: 2016-06-25

Publish Date: 2016-08-20

Abstract

Abstract

The strict and efficient transcription termination is required to prevent production of aberrant read-through transcripts that may cause transcriptional interference at neighboring genes. However, the exact regulatory mechanism remains poorly understood. Through a genetic screening of a LUCIFERASE (LUC) reporter system, we found that Arabidopsis nucleosome remodeler DECREASE IN DNA METHYLATION1 (DDM1) is a key component of this regulatory machinery and plays an important role in transcription termination, thus limiting transcriptional read-through (TRT). By whole-genome strand-specific RNA sequencing, we identified and confirmed 43 endogenous TRTs between genes, transposable elements (TEs), or genes and TEs in theddm1-10 mutant, which mainly occurred at heterochromatin regions. The DNA methylation analysis of these TRT regions revealed that TRT occurred frequently at the intergenic regions with a higher methylation level in wild type comparing to the regions where TRT did not occur. Our results suggest that the level of intergenic DNA methylation may involve in preventing aberrant gene TRT or producing new gene during evolution.
- DNA methylation,
- Intergenic region,
- DDM1,
- Transcriptional read-through

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References(37)

References

[1]	Alonso, J.M., Stepanova, A.N., Leisse, T.J. et al. Science, 301 (2003),pp. 653-657
[2]	Amedeo, P., Habu, Y., Afsar, K. et al. Nature, 405 (2000),pp. 203-206
[3]	Behm-Ansmant, I., Kashima, I., Rehwinkel, J. et al. mRNA quality control: an ancient machinery recognizes and degrades mRNAs with nonsense codons FEBS J., 581 (2007),pp. 2845-2853
[4]	Cao, X., Aufsatz, W., Zilberman, D. et al. Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation Curr. Biol., 13 (2003),pp. 2212-2217
[5]	Chang, Y.F., Imam, J.S., Wilkinson, M.F. The nonsense-mediated decay RNA surveillance pathway Annu. Rev. Biochem., 76 (2007),pp. 51-74
[6]	Cokus, S.J., Feng, S., Zhang, X. et al. Nature, 452 (2008),pp. 215-219
[7]	Di Giammartino, D.C., Nishida, K., Manley, J.L. Mechanisms and consequences of alternative polyadenylation Mol. Cell, 43 (2011),pp. 853-866
[8]	Duc, C., Sherstnev, A., Cole, C. et al. PLoS Genet., 9 (2013),p. e1003867
[9]	He, J., Fang, Y., Zhang, F. et al. Establishment of the methodology for quantifying lentiviral vector transcriptional read-through rate Chin. J. Biotechnol., 29 (2013),pp. 1006-1015
[10]	Herr, A.J., Molnar, A., Jones, A. et al. Proc. Natl. Acad. Sci. U. S. A., 103 (2006),pp. 14994-15001
[11]	Isken, O., Maquat, L.E. Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function Genes Dev., 21 (2007),pp. 1833-1856
[12]	Jeddeloh, J.A., Bender, J., Richards, E.J. Genes Dev., 12 (1998),pp. 1714-1725
[13]	Jeddeloh, J.A., Stokes, T.L., Richards, E.J. Maintenance of genomic methylation requires a SWI2/SNF2-like protein Nat. Genet., 22 (1999),pp. 94-97
[14]	Jordan, N.D., West, J.P., Bottley, A. et al. Plant Mol. Biol., 65 (2007),pp. 571-586
[15]	Kankel, M.W., Ramsey, D.E., Stokes, T.L. et al. Genetics, 163 (2003),pp. 1109-1122
[16]	Kim, S.H., Koroleva, O.A., Lewandowska, D. et al. Plant Cell, 21 (2009),pp. 2045-2057
[17]	Kuehner, J.N., Pearson, E.L., Moore, C. Unravelling the means to an end: RNA polymerase II transcription termination Nat. Rev. Mol. Cell Biol., 12 (2011),pp. 283-294
[18]	Law, J.A., Jacobsen, S.E. Establishing, maintaining and modifying DNA methylation patterns in plants and animals Nat. Rev. Genet., 11 (2010),pp. 204-220
[19]	Li, Y., Tessaro, M.J., Li, X. et al. Plant Physiol., 153 (2010),pp. 1425-1434
[20]	Lindroth, A.M., Cao, X., Jackson, J.P. et al. Science, 292 (2001),pp. 2077-2080
[21]	Lippman, Z., Gendrel, A.V., Black, M. et al. Role of transposable elements in heterochromatin and epigenetic control Nature, 430 (2004),pp. 471-476
[22]	Lister, R., O'Malley, R.C., Tonti-Filippini, J. et al. Cell, 133 (2008),pp. 523-536
[23]	Luo, Z., Chen, Z. Plant cell, 19 (2007),pp. 943-958
[24]	Moore, M.J., Proudfoot, N.J. Pre-mRNA processing reaches back to transcription and ahead to translation Cell, 136 (2009),pp. 688-700
[25]	Proudfoot, N.J., Furger, A., Dye, M.J. Integrating mRNA processing with transcription Cell, 108 (2002),pp. 501-512
[26]	Saze, H., Kakutani, T. EMBO J., 26 (2007),pp. 3641-3652
[27]	Sonmez, C., Baurle, I., Magusin, A. et al. Proc. Natl. Acad. Sci. U. S. A., 108 (2011),pp. 8508-8513
[28]	Stroud, H., Greenberg, M.V., Feng, S. et al. Cell, 152 (2013),pp. 352-364
[29]	Trapnell, C., Roberts, A., Goff, L. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks Nat. Protoc., 7 (2012),pp. 562-578
[30]	Trapnell, C., Williams, B.A., Pertea, G. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation Nat. Biotechnol., 28 (2010),pp. 511-515
[31]	Tsukahara, S., Kobayashi, A., Kawabe, A. et al. Nature, 461 (2009),pp. 423-426
[32]	Vaillant, I., Paszkowski, J. Role of histone and DNA methylation in gene regulation Curr. Opin. Plant Biol., 10 (2007),pp. 528-533
[33]	West, S., Proudfoot, N.J. Transcriptional termination enhances protein expression in human cells Mol. Cell, 33 (2009),pp. 354-364
[34]	Zemach, A., Kim, M.Y., Hsieh, P.H. et al. Cell, 153 (2013),pp. 193-205
[35]	Zemach, A., McDaniel, I.E., Silva, P. et al. Genome-wide evolutionary analysis of eukaryotic DNA methylation Science, 328 (2010),pp. 916-919
[36]	Zhang, H., Zhu, J.K. RNA-directed DNA methylation Curr. Opin. Plant Biol., 14 (2011),pp. 142-147
[37]	Zhou, Y., Zhang, J., Lin, H. et al. Plant Physiol., 154 (2010),pp. 1272-1280