APURINIC/APYRIMIDINIC ENDONUCLEASE2 and ZINC FINGER DNA 3'-PHOSPHOESTERASE Play Overlapping Roles in the Maintenance of Epigenome and Genome Stability

Overview

Journal Plant Cell

Publisher Oxford University Press

Specialties Biology
Cell Biology

Date 2018 Aug 24

PMID 30135084

Citations 15

Authors

Jinchao Li

Wenjie Liang

Yan Li

Weiqiang Qian

Affiliations

Soon will be listed here.

Abstract

Base excision repair (BER) is essential for active DNA demethylation and DNA damage repair in mammals and plants. Here, we provide genetic and biochemical evidence that APURINIC/APYRIMIDINIC ENDONUCLEASE2 (APE2) plays overlapping roles with ZINC FINGER DNA 3'-PHOSPHOESTERASE (ZDP) in active DNA demethylation and DNA damage repair in Simultaneous mutation of and causes DNA hypermethylation at more than 2000 loci, most of which are not hypermethylated in or single mutants. The and single mutants exhibit normal development, but the double mutants display pleiotropic developmental defects and are supersensitive to the DNA alkylating reagent methyl methanesulfonate. The gradual accumulation of DNA lesions in the seedlings is accompanied by constitutive activation of the DNA damage response and alteration of the cell cycle. Interestingly, knockout of the key DNA demethylase REPRESSOR OF SILENCING1 reduces the magnitude of DNA lesion accumulation and the DNA damage response in the mutants, suggesting that a proportion of the DNA damage in the mutants arises from incomplete active DNA demethylation. Lastly, we find that APE2 has 3'-phosphatase activity and strong 3'-5' exonuclease activity in vitro. Together, our results suggest that APE2 and ZDP, two BER proteins, play overlapping roles in the maintenance of epigenome and genome stability in plants.

Citing Articles

Divergent evolution of opposite base specificity and single-stranded DNA activity in animal and plant AP endonucleases.

Jordano-Raya M, Schrader C, Ariza R, Roldan-Arjona T, Cordoba-Canero D Nucleic Acids Res. 2025; 53(1.

PMID: 39778867 PMC: 11707538. DOI: 10.1093/nar/gkae1297.

Epigenetic gene regulation in plants and its potential applications in crop improvement.

Zhang H, Zhu J Nat Rev Mol Cell Biol. 2024; 26(1):51-67.

PMID: 39192154 DOI: 10.1038/s41580-024-00769-1.

Assessing Transcriptomic Responses to Oxidative Stress: Contrasting Wild-Type Arabidopsis Seedlings with and Gene Knockout Mutants.

Nikolic I, Milisavljevic M, Timotijevic G Int J Mol Sci. 2024; 25(12).

PMID: 38927997 PMC: 11203560. DOI: 10.3390/ijms25126291.

Genetic dissection of Brassica napus seed vigor after aging.

Ding Y, Hou D, Yin Y, Chen K, He J, Yan S Theor Appl Genet. 2024; 137(6):141.

PMID: 38789698 DOI: 10.1007/s00122-024-04648-3.

Base Excision DNA Repair in Plants: and Beyond.

Grin I, Petrova D, Endutkin A, Ma C, Yu B, Li H Int J Mol Sci. 2023; 24(19).

PMID: 37834194 PMC: 10573277. DOI: 10.3390/ijms241914746.

References

Krokan H, Bjoras M . Base excision repair. Cold Spring Harb Perspect Biol. 2013; 5(4):a012583. PMC: 3683898. DOI: 10.1101/cshperspect.a012583. View

Jilani A, Ramotar D, Slack C, Ong C, Yang X, Scherer S . Molecular cloning of the human gene, PNKP, encoding a polynucleotide kinase 3'-phosphatase and evidence for its role in repair of DNA strand breaks caused by oxidative damage. J Biol Chem. 1999; 274(34):24176-86. DOI: 10.1074/jbc.274.34.24176. View

Wallace B, Berman Z, Mueller G, Lin Y, Chang T, Andres S . APE2 Zf-GRF facilitates 3'-5' resection of DNA damage following oxidative stress. Proc Natl Acad Sci U S A. 2016; 114(2):304-309. PMC: 5240719. DOI: 10.1073/pnas.1610011114. View

Liu J, Ren X, Yin H, Wang Y, Xia R, Wang Y . Mutation in the catalytic subunit of DNA polymerase alpha influences transcriptional gene silencing and homologous recombination in Arabidopsis. Plant J. 2009; 61(1):36-45. DOI: 10.1111/j.1365-313X.2009.04026.x. View

Gong Z, Morales-Ruiz T, Ariza R, Roldan-Arjona T, David L, Zhu J . ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell. 2003; 111(6):803-14. DOI: 10.1016/s0092-8674(02)01133-9. View

Li Y, Cordoba-Canero D, Qian W, Zhu X, Tang K, Zhang H . An AP endonuclease functions in active DNA demethylation and gene imprinting in Arabidopsis [corrected]. PLoS Genet. 2015; 11(1):e1004905. PMC: 4287435. DOI: 10.1371/journal.pgen.1004905. View

Liu Q, Wang J, Miki D, Xia R, Yu W, He J . DNA replication factor C1 mediates genomic stability and transcriptional gene silencing in Arabidopsis. Plant Cell. 2010; 22(7):2336-52. PMC: 2929113. DOI: 10.1105/tpc.110.076349. View

Spampinato C . Protecting DNA from errors and damage: an overview of DNA repair mechanisms in plants compared to mammals. Cell Mol Life Sci. 2016; 74(9):1693-1709. PMC: 11107726. DOI: 10.1007/s00018-016-2436-2. View

He Y, Li B, Li Z, Liu P, Wang Y, Tang Q . Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science. 2011; 333(6047):1303-7. PMC: 3462231. DOI: 10.1126/science.1210944. View

10.

Zhang H, Ma Z, Zeng L, Tanaka K, Zhang C, Ma J . DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of Pol IV. Proc Natl Acad Sci U S A. 2013; 110(20):8290-5. PMC: 3657815. DOI: 10.1073/pnas.1300585110. View

11.

Stavnezer J, Linehan E, Thompson M, Habboub G, Ucher A, Kadungure T . Differential expression of APE1 and APE2 in germinal centers promotes error-prone repair and A:T mutations during somatic hypermutation. Proc Natl Acad Sci U S A. 2014; 111(25):9217-22. PMC: 4078814. DOI: 10.1073/pnas.1405590111. View

12.

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

13.

Zhang H, Li L . SQUAMOSA promoter binding protein-like7 regulated microRNA408 is required for vegetative development in Arabidopsis. Plant J. 2013; 74(1):98-109. DOI: 10.1111/tpj.12107. View

14.

Zhang J, Xie S, Cheng J, Lai J, Zhu J, Gong Z . The Second Subunit of DNA Polymerase Delta Is Required for Genomic Stability and Epigenetic Regulation. Plant Physiol. 2016; 171(2):1192-208. PMC: 4902588. DOI: 10.1104/pp.15.01976. View

15.

Akishev Z, Taipakova S, Joldybayeva B, Zutterling C, Smekenov I, Ishchenko A . The major Arabidopsis thaliana apurinic/apyrimidinic endonuclease, ARP is involved in the plant nucleotide incision repair pathway. DNA Repair (Amst). 2016; 48:30-42. DOI: 10.1016/j.dnarep.2016.10.009. View

16.

Cordoba-Canero D, Morales-Ruiz T, Roldan-Arjona T, Ariza R . Single-nucleotide and long-patch base excision repair of DNA damage in plants. Plant J. 2009; 60(4):716-28. PMC: 2954439. DOI: 10.1111/j.1365-313X.2009.03994.x. View

17.

Burkovics P, Hajdu I, Szukacsov V, Unk I, Haracska L . Role of PCNA-dependent stimulation of 3'-phosphodiesterase and 3'-5' exonuclease activities of human Ape2 in repair of oxidative DNA damage. Nucleic Acids Res. 2009; 37(13):4247-55. PMC: 2715233. DOI: 10.1093/nar/gkp357. View

18.

Sidorenko V, Nevinsky G, Zharkov D . Mechanism of interaction between human 8-oxoguanine-DNA glycosylase and AP endonuclease. DNA Repair (Amst). 2006; 6(3):317-28. DOI: 10.1016/j.dnarep.2006.10.022. View

19.

Yin H, Zhang X, Liu J, Wang Y, He J, Yang T . Epigenetic regulation, somatic homologous recombination, and abscisic acid signaling are influenced by DNA polymerase epsilon mutation in Arabidopsis. Plant Cell. 2009; 21(2):386-402. PMC: 2660612. DOI: 10.1105/tpc.108.061549. View

20.

Gehring M, Huh J, Hsieh T, Penterman J, Choi Y, Harada J . DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell. 2006; 124(3):495-506. PMC: 4106368. DOI: 10.1016/j.cell.2005.12.034. View