An AP Endonuclease Functions in Active DNA Dimethylation and Gene Imprinting in Arabidopsis

PLoS Genetics

Volumn 11, Issue 1, 2015, Pages

  Li, Yan ^a,b   Córdoba Cañero, Dolores ^c   Qian, Weiqiang ^b   Zhu, Xiaohong ^d   Tang, Kai ^d   Zhang, Huiming ^a   Ariza, Rafael R ^c   Roldán Arjona, Teresa ^c   Zhu, Jian Kang ^a,d  

^a Chinese Academy of Sciences   (China)

^b PEKING UNIVERSITY   (China)

^c UNIVERSITY OF CÓRDOBA   (Spain)

^d PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; DNA GLYCOSYLASE DEMETER; DNA GLYCOSYLTRANSFERASE; DNA PHOSPHATASE ZDP; MESSENGER RNA; PHOSPHATASE; REPRESSOR OF SILENCING 1; UNCLASSIFIED DRUG; APE1L PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; ENDONUCLEASE; FWA PROTEIN, ARABIDOPSIS; HOMEODOMAIN PROTEIN; MEA PROTEIN, ARABIDOPSIS; NUCLEAR PROTEIN; ROS1 PROTEIN, ARABIDOPSIS; TRANSCRIPTION FACTOR;

AMINO ACID SUBSTITUTION; APE1L GENE; ARABIDOPSIS; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA DEMETHYLATION; DNA METHYLATION; DNA PROTEIN COMPLEX; DNA REPAIR; DOWN REGULATION; ENDOSPERM; ENZYME ACTIVITY; ENZYME METABOLISM; ENZYME SUBSTRATE COMPLEX; EXCISION REPAIR; FEMALE GAMETOPHYTE; FWA GENE; GENE EXPRESSION REGULATION; GENE SEQUENCE; GENOME IMPRINTING; IN VITRO STUDY; IN VIVO STUDY; LETHALITY; MEA GENE; MOLECULAR DYNAMICS; MUTATIONAL ANALYSIS; NICOTIANA BENTHAMIANA; NONHUMAN; PHENOTYPE; PLANT GENE; PLANT LEAF; PLANT PARAMETERS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; SEED ABORTION; SEED DEVELOPMENT; WHOLE GENOME BISULFITE SEQUENCING; ZDP GENE; ANIMAL; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGH THROUGHPUT SEQUENCING; METABOLISM; PLANT GENOME; PLANT SEED;

ANIMALIA; ARABIDOPSIS;

ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA METHYLATION; ENDONUCLEASES; ENDOSPERM; GENE SILENCING; GENOME, PLANT; GENOMIC IMPRINTING; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HOMEODOMAIN PROTEINS; NUCLEAR PROTEINS; SEEDS; TRANSCRIPTION FACTORS;

EID: 84924366668     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004905     Document Type: Article

References (46)

1. Law JA, Jacobsen SE, (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11: 204–220.
2. Zhu JK, (2009) Active DNA demethylation mediated by DNA glycosylases. Annu Rev Genet 43: 143–166.
3. Zilberman D, (2008) The evolving functions of DNA methylation. Curr Opin Plant Biol 11: 554–559.
4. Haag JR, Pikaard CS, (2011) Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nat Rev Mol Cell Biol 12: 483–492.
5. Tariq M, Paszkowski J, (2004) DNA and histone methylation in plants. Trends Genet 20: 244–251.
6. Borges F, Calarco JP, Martienssen RA, (2012) Reprogramming the epigenome in Arabidopsis pollen. Cold Spring Harb Symp Quant Biol 77: 1–5.
7. Matzke M, Kanno T, Daxinger L, Huettel B, Matzke AJ, (2009) RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol 21: 367–376.
8. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW, et al. (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 126: 1189–1201.
9. Pikaard CS, (2013) Methylating the DNA of the most repressed: special access required. Mol Cell 49: 1021–1022.
10. Zhang H, Zhu JK, (2012) Active DNA demethylation in plants and animals. Cold Spring Harb Symp Quant Biol 77: 161–173.
11. Gehring M, Henikoff S, (2008) DNA methylation and demethylation in Arabidopsis. Arabidopsis Book 6: e0102.
12. Gehring M, Huh JH, Hsieh TF, Penterman J, Choi Y, et al. (2006) DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell 124: 495–506.
13. Gong Z, Morales-Ruiz T, Ariza RR, Roldan-Arjona T, David L, et al. (2002) ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 111: 803–814.
14. Ortega-Galisteo AP, Morales-Ruiz T, Ariza RR, Roldan-Arjona T, (2008) Arabidopsis DEMETER-LIKE proteins DML2 and DML3 are required for appropriate distribution of DNA methylation marks. Plant Mol Biol 67: 671–681.
15. Morales-Ruiz T, Ortega-Galisteo AP, Ponferrada-Marin MI, Martinez-Macias MI, Ariza RR, et al. (2006) DEMETER and REPRESSOR OF SILENCING 1 encode 5-methylcytosine DNA glycosylases. Proc Natl Acad Sci U S A 103: 6853–6858.
16. Agius F, Kapoor A, Zhu JK, (2006) Role of the Arabidopsis DNA glycosylase/lyase ROS1 in active DNA demethylation. Proc Natl Acad Sci U S A 103: 11796–11801.
17. Martinez-Macias MI, Qian W, Miki D, Pontes O, Liu Y, et al. (2012) A DNA 3′ phosphatase functions in active DNA demethylation in Arabidopsis. Mol Cell 45: 357–370.
18. Cordoba-Canero D, Morales-Ruiz T, Roldan-Arjona T, Ariza RR, (2009) Single-nucleotide and long-patch base excision repair of DNA damage in plants. Plant J 60: 716–728.
19. Qian W, Miki D, Zhang H, Liu Y, Zhang X, et al. (2012) A histone acetyltransferase regulates active DNA demethylation in Arabidopsis. Science 336: 1445–1448.
20. Huh JH, Bauer MJ, Hsieh TF, Fischer RL, (2008) Cellular programming of plant gene imprinting. Cell 132: 735–744.
21. Gehring M, Bubb KL, Henikoff S, (2009) Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 324: 1447–1451.
22. Hsieh TF, Ibarra CA, Silva P, Zemach A, Eshed-Williams L, et al. (2009) Genome-wide demethylation of Arabidopsis endosperm. Science 324: 1451–1454.
23. Kinoshita T, Miura A, Choi Y, Kinoshita Y, Cao X, et al. (2004) One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303: 521–523.
24. Xiao W, Gehring M, Choi Y, Margossian L, Pu H, et al. (2003) Imprinting of the MEA Polycomb gene is controlled by antagonism between MET1 methyltransferase and DME glycosylase. Dev Cell 5: 891–901.
25. Ikeda Y, (2012) Plant imprinted genes identified by genome-wide approaches and their regulatory mechanisms. Plant Cell Physiol 53: 809–816.
26. Choi Y, Gehring M, Johnson L, Hannon M, Harada JJ, et al. (2002) DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in arabidopsis. Cell 110: 33–42.
27. Schoft VK, Chumak N, Choi Y, Hannon M, Garcia-Aguilar M, et al. (2011) Function of the DEMETER DNA glycosylase in the Arabidopsis thaliana male gametophyte. Proc Natl Acad Sci U S A 108: 8042–8047.
28. Calarco JP, Borges F, Donoghue MT, Van Ex F, Jullien PE, et al. (2012) Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151: 194–205.
29. Ibarra CA, Feng X, Schoft VK, Hsieh TF, Uzawa R, et al. (2012) Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 337: 1360–1364.
30. Ikeda Y, Kinoshita Y, Susaki D, Ikeda Y, Iwano M, et al. (2011) HMG domain containing SSRP1 is required for DNA demethylation and genomic imprinting in Arabidopsis. Dev Cell 21: 589–596.
31. Murphy TM, Belmonte M, Shu S, Britt AB, Hatteroth J, (2009) Requirement for abasic endonuclease gene homologues in Arabidopsis seed development. PLoS One 4: e4297.
32. Zilberman MV, Karpawich PP, (2007) Alternate site atrial pacing in the young: conventional echocardiography and tissue Doppler analysis of the effects on atrial function and ventricular filling. Pacing Clin Electrophysiol 30: 755–760.
33. Rothwell DG, Hickson ID, (1996) Asparagine 212 is essential for abasic site recognition by the human DNA repair endonuclease HAP1. Nucleic Acids Res 24: 4217–4221.
34. Ponferrada-Marin MI, Roldan-Arjona T, Ariza RR, (2009) ROS1 5-methylcytosine DNA glycosylase is a slow-turnover catalyst that initiates DNA demethylation in a distributive fashion. Nucleic Acids Res 37: 4264–4274.
35. Chen H, Zou Y, Shang Y, Lin H, Wang Y, Cai R, Tang X, Zhou JM, (2008) Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol. 146: 368–376.
36. Buzas DM, Nakamura M, Kinoshita T, (2014) Epigenetic role for the conserved Fe-S cluster biogenesis protein AtDRE2 in Arabidopsis thaliana. Proc Natl Acad Sci U S A 111: 13565–13570.
37. Roldan-Arjona T, Ariza RR, (2009) Repair and tolerance of oxidative DNA damage in plants. Mutat Res 681: 169–179.
38. Martinez-Macias MI, Cordoba-Canero D, Ariza RR, Roldan-Arjona T, (2013) The DNA repair protein XRCC1 functions in the plant DNA demethylation pathway by stimulating cytosine methylation (5-meC) excision, gap tailoring, and DNA ligation. J Biol Chem 288: 5496–5505.
39. Joldybayeva B, Prorok P, Grin IR, Zharkov DO, Ishenko AA, et al. (2014) Cloning and characterization of a wheat homologue of apurinic/apyrimidinic endonuclease Ape1L. PLoS One 9: e92963.
40. Wu H, Zhang Y, (2014) Reversing DNA methylation: mechanisms, genomics, and biological functions. Cell 156: 45–68.
41. Cortellino S, Xu J, Sannai M, Moore R, Caretti E, et al. (2011) Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 146: 67–79.
42. Rai K, Huggins IJ, James SR, Karpf AR, Jones DA, et al. (2008) DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45. Cell 135: 1201–1212.
43. Joldybayeva B, Prorok P, Grin IR, Zharkov DO, Ishenko AA, et al. (2014) Cloning and characterization of a wheat homologue of apurinic/apyrimidinic endonuclease Ape1L. PLoS One 9: e92963.
44. Buzas DM, Nakamura M, Kinoshita T, (2014) Epigenetic role for the conserved Fe-S cluster biogenesis protein AtDRE2 in Arabidopsis thaliana. Proc Natl Acad Sci U S A 111: 13565–13570.
45. Wohrmann HJ, Gagliardini V, Raissig MT, Wehrle W, Arand J, et al. (2012) Identification of a DNA methylation-independent imprinting control region at the Arabidopsis MEDEA locus. Genes Dev 26: 1837–1850.
46. Pontes O, Li CF, Costa Nunes P, Haag J, Ream T, et al. (2006) The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell 126: 79–92.