Arabidopsis DNA Replication Initiates in Intergenic, AT-Rich Open Chromatin

Overview

Journal Plant Physiol

Specialty Physiology

Date 2020 Mar 25

PMID 32205451

Citations 9

Authors

Emily Wheeler

Ashley M Brooks

Lorenzo Concia

Daniel L Vera

Emily E Wear

Chantal LeBlanc

Umamaheswari Ramu

Matthew W Vaughn

Hank W Bass

Robert A Martienssen

William F Thompson

Linda Hanley-Bowdoin

Affiliations

Soon will be listed here.

Abstract

The selection and firing of DNA replication origins play key roles in ensuring that eukaryotes accurately replicate their genomes. This process is not well documented in plants due in large measure to difficulties in working with plant systems. We developed a new functional assay to label and map very early replicating loci that must, by definition, include at least a subset of replication origins. Arabidopsis () cells were briefly labeled with 5-ethynyl-2'-deoxy-uridine, and nuclei were subjected to two-parameter flow sorting. We identified more than 5500 loci as initiation regions (IRs), the first regions to replicate in very early S phase. These were classified as strong or weak IRs based on the strength of their replication signals. Strong initiation regions were evenly spaced along chromosomal arms and depleted in centromeres, while weak initiation regions were enriched in centromeric regions. IRs are AT-rich sequences flanked by more GC-rich regions and located predominantly in intergenic regions. Nuclease sensitivity assays indicated that IRs are associated with accessible chromatin. Based on these observations, initiation of plant DNA replication shows some similarity to, but is also distinct from, initiation in other well-studied eukaryotic systems.

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References

Bass H, Hoffman G, Lee T, Wear E, Joseph S, Allen G . Defining multiple, distinct, and shared spatiotemporal patterns of DNA replication and endoreduplication from 3D image analysis of developing maize (Zea mays L.) root tip nuclei. Plant Mol Biol. 2015; 89(4-5):339-51. PMC: 4631726. DOI: 10.1007/s11103-015-0364-4. View

Taylor J . Increase in DNA replication sites in cells held at the beginning of S phase. Chromosoma. 1977; 62(4):291-300. DOI: 10.1007/BF00327029. View

Sequeira-Mendes J, Gutierrez C . Links between genome replication and chromatin landscapes. Plant J. 2015; 83(1):38-51. DOI: 10.1111/tpj.12847. View

Huala E, Dickerman A, Garcia-Hernandez M, Weems D, Reiser L, LaFond F . The Arabidopsis Information Resource (TAIR): a comprehensive database and web-based information retrieval, analysis, and visualization system for a model plant. Nucleic Acids Res. 2000; 29(1):102-5. PMC: 29827. DOI: 10.1093/nar/29.1.102. View

Gai D, Chang Y, Chen X . Origin DNA melting and unwinding in DNA replication. Curr Opin Struct Biol. 2010; 20(6):756-62. PMC: 2997676. DOI: 10.1016/j.sbi.2010.08.009. View

Sequeira-Mendes J, Vergara Z, Peiro R, Morata J, Araguez I, Costas C . Differences in firing efficiency, chromatin, and transcription underlie the developmental plasticity of the DNA replication origins. Genome Res. 2019; 29(5):784-797. PMC: 6499314. DOI: 10.1101/gr.240986.118. View

Eaton M, Prinz J, MacAlpine H, Tretyakov G, Kharchenko P, MacAlpine D . Chromatin signatures of the Drosophila replication program. Genome Res. 2010; 21(2):164-74. PMC: 3032920. DOI: 10.1101/gr.116038.110. View

Bedrat A, Lacroix L, Mergny J . Re-evaluation of G-quadruplex propensity with G4Hunter. Nucleic Acids Res. 2016; 44(4):1746-59. PMC: 4770238. DOI: 10.1093/nar/gkw006. View

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

10.

Xing Y, Liu G, Zhao X, Zhao H, Cai L . Genome-wide characterization and prediction of Arabidopsis thaliana replication origins. Biosystems. 2014; 124:1-6. DOI: 10.1016/j.biosystems.2014.07.001. View

11.

Hughes A, Jin Y, Rando O, Struhl K . A functional evolutionary approach to identify determinants of nucleosome positioning: a unifying model for establishing the genome-wide pattern. Mol Cell. 2012; 48(1):5-15. PMC: 3472102. DOI: 10.1016/j.molcel.2012.07.003. View

12.

Cayrou C, Ballester B, Peiffer I, Fenouil R, Coulombe P, Andrau J . The chromatin environment shapes DNA replication origin organization and defines origin classes. Genome Res. 2015; 25(12):1873-85. PMC: 4665008. DOI: 10.1101/gr.192799.115. View

13.

Thastrom A, Lowary P, Widlund H, Cao H, Kubista M, Widom J . Sequence motifs and free energies of selected natural and non-natural nucleosome positioning DNA sequences. J Mol Biol. 1999; 288(2):213-29. DOI: 10.1006/jmbi.1999.2686. View

14.

Banh S, Hales B . Hydroxyurea exposure triggers tissue-specific activation of p38 mitogen-activated protein kinase signaling and the DNA damage response in organogenesis-stage mouse embryos. Toxicol Sci. 2013; 133(2):298-308. PMC: 3663560. DOI: 10.1093/toxsci/kft069. View

15.

Miotto B . [How genomic approaches help the understanding of the initiation of DNA replication]. Med Sci (Paris). 2017; 33(2):143-150. DOI: 10.1051/medsci/20173302009. View

16.

Ramirez F, Ryan D, Gruning B, Bhardwaj V, Kilpert F, Richter A . deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 2016; 44(W1):W160-5. PMC: 4987876. DOI: 10.1093/nar/gkw257. View

17.

Besnard E, Babled A, Lapasset L, Milhavet O, Parrinello H, Dantec C . Unraveling cell type-specific and reprogrammable human replication origin signatures associated with G-quadruplex consensus motifs. Nat Struct Mol Biol. 2012; 19(8):837-44. DOI: 10.1038/nsmb.2339. View

18.

Krishnakumar V, Hanlon M, Contrino S, Ferlanti E, Karamycheva S, Kim M . Araport: the Arabidopsis information portal. Nucleic Acids Res. 2014; 43(Database issue):D1003-9. PMC: 4383980. DOI: 10.1093/nar/gku1200. View

19.

Picard F, Cadoret J, Audit B, Arneodo A, Alberti A, Battail C . The spatiotemporal program of DNA replication is associated with specific combinations of chromatin marks in human cells. PLoS Genet. 2014; 10(5):e1004282. PMC: 4006723. DOI: 10.1371/journal.pgen.1004282. View

20.

Lee T, Pascuzzi P, Settlage S, Shultz R, Tanurdzic M, Rabinowicz P . Arabidopsis thaliana chromosome 4 replicates in two phases that correlate with chromatin state. PLoS Genet. 2010; 6(6):e1000982. PMC: 2883604. DOI: 10.1371/journal.pgen.1000982. View