Genome-wide Excision Repair in Arabidopsis is Coupled to Transcription and Reflects Circadian Gene Expression Patterns

Overview

Journal Nat Commun

Specialty Biology

Date 2018 Apr 19

PMID 29666379

Citations 36

Authors

Onur Oztas

Christopher P Selby

Aziz Sancar

Ogun Adebali

Affiliations

Soon will be listed here.

Abstract

Plants are exposed to numerous DNA-damaging stresses including the exposure to ultraviolet (UV) component of solar radiation. They employ nucleotide excision repair to remove DNA-bulky adducts and to help eliminate UV-induced DNA lesions, so as to maintain their genome integrity and their fitness. Here, we generated genome-wide single-nucleotide resolution excision repair maps of UV-induced DNA damage in Arabidopsis at different circadian time points. Our data show that the repair of UV lesions for a large fraction of the genome is controlled by the joint actions of the circadian clock and transcription by RNA polymerase II. Our findings reveal very strong repair preference for the transcribed strands of active genes in Arabidopsis, and 10-30% of the transcription-coupled repair is circadian time-dependent. This dynamic range in nucleotide excision repair levels throughout the day enables Arabidopsis to cope with the bulky DNA lesion-inducing environmental factors including UV.

Citing Articles

Exploring the Relationship Between Gene Expression and Low-Frequency Somatic Mutations in Arabidopsis with Duplex Sequencing.

Waneka G, Pate B, Monroe J, Sloan D Genome Biol Evol. 2024; 16(10).

PMID: 39365161 PMC: 11489876. DOI: 10.1093/gbe/evae213.

Nucleotide excision repair of aflatoxin-induced DNA damage within the 3D human genome organization.

Wu Y, Adeel M, Xia D, Sancar A, Li W Nucleic Acids Res. 2024; 52(19):11704-11719.

PMID: 39258558 PMC: 11514448. DOI: 10.1093/nar/gkae755.

Genome-wide analysis of transcription-coupled repair reveals novel transcription events in Caenorhabditis elegans.

Kose C, Lindsey-Boltz L, Sancar A, Jiang Y PLoS Genet. 2024; 20(7):e1011365.

PMID: 39028758 PMC: 11290646. DOI: 10.1371/journal.pgen.1011365.

UV damage induces production of mitochondrial DNA fragments with specific length profiles.

Waneka G, Stewart J, Anderson J, Li W, Wilusz J, Argueso J Genetics. 2024; 227(3.

PMID: 38722894 PMC: 11228841. DOI: 10.1093/genetics/iyae070.

Chromatin dynamics and RNA metabolism are double-edged swords for the maintenance of plant genome integrity.

Bergis-Ser C, Reji M, Latrasse D, Bergounioux C, Benhamed M, Raynaud C Nat Plants. 2024; 10(6):857-873.

PMID: 38658791 DOI: 10.1038/s41477-024-01678-z.

References

Harmer S, Hogenesch J, Straume M, Chang H, Han B, Zhu T . Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science. 2000; 290(5499):2110-3. DOI: 10.1126/science.290.5499.2110. View

Hsu P, Harmer S . Wheels within wheels: the plant circadian system. Trends Plant Sci. 2013; 19(4):240-9. PMC: 3976767. DOI: 10.1016/j.tplants.2013.11.007. View

Lu F, Cui X, Zhang S, Liu C, Cao X . JMJ14 is an H3K4 demethylase regulating flowering time in Arabidopsis. Cell Res. 2010; 20(3):387-90. DOI: 10.1038/cr.2010.27. View

Biedermann S, Hellmann H . The DDB1a interacting proteins ATCSA-1 and DDB2 are critical factors for UV-B tolerance and genomic integrity in Arabidopsis thaliana. Plant J. 2010; 62(3):404-15. DOI: 10.1111/j.1365-313X.2010.04157.x. View

Hu Z, Cools T, De Veylder L . Mechanisms Used by Plants to Cope with DNA Damage. Annu Rev Plant Biol. 2015; 67:439-62. DOI: 10.1146/annurev-arplant-043015-111902. View

Zhang R, Podtelezhnikov A, Hogenesch J, Anafi R . Discovering Biology in Periodic Data through Phase Set Enrichment Analysis (PSEA). J Biol Rhythms. 2016; 31(3):244-57. DOI: 10.1177/0748730416631895. View

Saze H, Shiraishi A, Miura A, Kakutani T . Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science. 2008; 319(5862):462-5. DOI: 10.1126/science.1150987. View

Kimura S, Sakaguchi K . DNA repair in plants. Chem Rev. 2006; 106(2):753-66. DOI: 10.1021/cr040482n. View

Pikaard C, Mittelsten Scheid O . Epigenetic regulation in plants. Cold Spring Harb Perspect Biol. 2014; 6(12):a019315. PMC: 4292151. DOI: 10.1101/cshperspect.a019315. View

10.

Sancar A, Lindsey-Boltz L, Kang T, Reardon J, Lee J, Ozturk N . Circadian clock control of the cellular response to DNA damage. FEBS Lett. 2010; 584(12):2618-25. PMC: 2878924. DOI: 10.1016/j.febslet.2010.03.017. View

11.

Wu G, Anafi R, Hughes M, Kornacker K, Hogenesch J . MetaCycle: an integrated R package to evaluate periodicity in large scale data. Bioinformatics. 2016; 32(21):3351-3353. PMC: 5079475. DOI: 10.1093/bioinformatics/btw405. View

12.

Singh S, Roy S, Roy Choudhury S, Sengupta D . DNA repair and recombination in higher plants: insights from comparative genomics of Arabidopsis and rice. BMC Genomics. 2010; 11:443. PMC: 3091640. DOI: 10.1186/1471-2164-11-443. View

13.

Sequeira-Mendes J, Araguez I, Peiro R, Mendez-Giraldez R, Zhang X, Jacobsen S . The Functional Topography of the Arabidopsis Genome Is Organized in a Reduced Number of Linear Motifs of Chromatin States. Plant Cell. 2014; 26(6):2351-2366. PMC: 4114938. DOI: 10.1105/tpc.114.124578. View

14.

Trapnell C, Pachter L, Salzberg S . TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009; 25(9):1105-11. PMC: 2672628. DOI: 10.1093/bioinformatics/btp120. View

15.

Hu J, Adar S, Selby C, Lieb J, Sancar A . Genome-wide analysis of human global and transcription-coupled excision repair of UV damage at single-nucleotide resolution. Genes Dev. 2015; 29(9):948-60. PMC: 4421983. DOI: 10.1101/gad.261271.115. View

16.

Britt . Molecular genetics of DNA repair in higher plants. Trends Plant Sci. 1999; 4(1):20-25. DOI: 10.1016/s1360-1385(98)01355-7. View

17.

Hetzel J, Duttke S, Benner C, Chory J . Nascent RNA sequencing reveals distinct features in plant transcription. Proc Natl Acad Sci U S A. 2016; 113(43):12316-12321. PMC: 5087027. DOI: 10.1073/pnas.1603217113. View

18.

Rugnone M, Soverna A, Sanchez S, Schlaen R, Hernando C, Seymour D . LNK genes integrate light and clock signaling networks at the core of the Arabidopsis oscillator. Proc Natl Acad Sci U S A. 2013; 110(29):12120-5. PMC: 3718124. DOI: 10.1073/pnas.1302170110. View

19.

Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N . The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009; 25(16):2078-9. PMC: 2723002. DOI: 10.1093/bioinformatics/btp352. View

20.

Landt S, Marinov G, Kundaje A, Kheradpour P, Pauli F, Batzoglou S . ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res. 2012; 22(9):1813-31. PMC: 3431496. DOI: 10.1101/gr.136184.111. View