Arabidopsis thaliana RNase H2 deficiency counteracts the needs for the WEE1 checkpoint kinase but triggers genome instability

Plant Cell

Volumn 26, Issue 9, 2014, Pages 3680-3692

  Kalhorzadeh, Pooneh ^a,b   Hu, Zhubing ^a,b   Cools, Toon ^a,b   Amiard, Simon ^c   Willing, Eva Maria ^d   De Winne, Nancy ^a,b   Gevaert, Kris ^a,b   Schneeberger, Korbinian ^d   White, Charles I ^c   De Veyldera, Lieven ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c UNIVERSITÉ CLERMONT AUVERGNE   (France)

^d MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; HYDROXYUREA; PROTEIN SERINE THREONINE KINASE; RIBONUCLEASE H; RIBONUCLEASE HII; RIBONUCLEOTIDE; WEE1 PROTEIN, ARABIDOPSIS;

AMINO ACID SEQUENCE; ARABIDOPSIS; BASE PAIRING; CELL CYCLE CHECKPOINT; CHEMISTRY; DEFICIENCY; DRUG EFFECTS; ENZYME ACTIVE SITE; ENZYMOLOGY; GENETIC RECOMBINATION; GENETICS; GENOMIC INSTABILITY; METABOLISM; MOLECULAR GENETICS; MUTATION; MUTATION RATE; NUCLEOTIDE SEQUENCE; PLANT GENE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE PAIRING; BASE SEQUENCE; CATALYTIC DOMAIN; CELL CYCLE CHECKPOINTS; GENES, PLANT; GENOMIC INSTABILITY; HYDROXYUREA; MOLECULAR SEQUENCE DATA; MUTATION; MUTATION RATE; PROTEIN-SERINE-THREONINE KINASES; RECOMBINATION, GENETIC; RIBONUCLEASE H; RIBONUCLEOTIDES;

EID: 84908223252     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.128108     Document Type: Article

References (62)

1. Amiard, S., Charbonnel, C., Allain, E., Depeiges, A., White, C. I., and Gallego, M. E. (2010). Distinct roles of the ATR kinase and the Mre11-Rad50-Nbs1 complex in the maintenance of chromosomal stability in Arabidopsis. Plant Cell 22: 3020-3033.
2. Arana, M. E., Kerns, R. T., Wharey, L., Gerrish, K. E., Bushel, P. R., and Kunkel, T. A. (2012). Transcriptional responses to loss of RNase H2 in Saccharomyces cerevisiae. DNA Repair (Amst.) 11: 933-941.
3. Bendixen, C., Gangloff, S., and Rothstein, R. (1994). A yeast matingselection scheme for detection of protein-protein interactions. Nucleic Acids Res. 22: 1778-1779.
4. Bleuyard, J. Y., Gallego, M. E., Savigny, F., and White, C. I. (2005). Differing requirements for the Arabidopsis Rad51 paralogs in meiosis and DNA repair. Plant J. 41: 533-545.
5. Boudolf, V., Inzé, D., and De Veylder, L. (2006). What if higher plants lack a CDC25 phosphatase? Trends Plant Sci. 11: 474-479.
6. Branzei, D., and Foiani, M. (2010). Maintaining genome stability at the replication fork. Nat. Rev. Mol. Cell Biol. 11: 208-219.
7. Brown, J. A., and Suo, Z. (2011). Unlocking the sugar "steric gate" of DNA polymerases. Biochemistry 50: 1135-1142.
8. Bubeck, D., Reijns, M. A., Graham, S. C., Astell, K. R., Jones, E. Y., and Jackson, A. P. (2011). PCNA directs type 2 RNase H activity on DNA replication and repair substrates. Nucleic Acids Res. 39: 3652-3666.
9. Cuéllar Pérez, A., Nagels Durand, A., Vanden Bossche, R., De Clercq, R., Persiau, G., Van Wees, S. C. M., Pieterse, C. M. J., Gevaert, K., De Jaeger, G., Goossens, A., and Pauwels, L. (2014). The non-JAZ TIFY protein TIFY8 from Arabidopsis thaliana is a transcriptional repressor. PLoS ONE 9: e84891.
10. Cerritelli, S. M., and Crouch, R. J. (2009). Ribonuclease H: the enzymes in eukaryotes. FEBS J. 276: 1494-1505.
11. Ciccia, A., and Elledge, S. J. (2010). The DNA damage response: making it safe to play with knives. Mol. Cell 40: 179-204.
12. Clausen, A. R., Zhang, S., Burgers, P. M., Lee, M. Y., and Kunkel, T. A. (2013). Ribonucleotide incorporation, proofreading and bypass by human DNA polymerase δ. DNA Repair (Amst.) 12: 121-127.
13. Cook, J. G. (2009). Replication licensing and the DNA damage checkpoint. Front Biosci (Landmark Ed) 14: 5013-5030.
14. Cools, T., Iantcheva, A., Weimer, A. K., Boens, S., Takahashi, N., Maes, S., Van den Daele, H., Van Isterdael, G., Schnittger, A., and De Veylder, L. (2011). The Arabidopsis thaliana checkpoint kinase WEE1 protects against premature vascular differentiation during replication stress. Plant Cell 23: 1435-1448.
15. Culligan, K., Tissier, A., and Britt, A. (2004). ATR regulates a G2-phase cell-cycle checkpoint in Arabidopsis thaliana. Plant Cell 16: 1091-1104.
16. Culligan, K. M., Robertson, C. E., Foreman, J., Doerner, P., and Britt, A. B. (2006). ATR and ATM play both distinct and additive roles in response to ionizing radiation. Plant J. 48: 947-961.
17. De Schutter, K., Joubès, J., Cools, T., Verkest, A., Corellou, F., Babiychuk, E., Van Der Schueren, E., Beeckman, T., Kushnir, S., Inzé, D., and De Veylder, L. (2007). Arabidopsis WEE1 kinase controls cell cycle arrest in response to activation of the DNA integrity checkpoint. Plant Cell 19: 211-225.
18. Ferraro, P., Franzolin, E., Pontarin, G., Reichard, P., and Bianchi, V. (2010). Quantitation of cellular deoxynucleoside triphosphates. Nucleic Acids Res. 38: e85.
19. Garcia, V., Bruchet, H., Camescasse, D., Granier, F., Bouchez, D., and Tissier, A. (2003). AtATM is essential for meiosis and the somatic response to DNA damage in plants. Plant Cell 15: 119-132.
20. Gietz, D., St Jean, A., Woods, R. A., and Schiestl, R. H. (1992). Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20: 1425.
21. Gonzalez, N., Hernould, M., Delmas, F., Gévaudant, F., Duffe, P., Causse, M., Mouras, A., and Chevalier, C. (2004). Molecular characterization of a WEE1 gene homologue in tomato (Lycopersicon esculentum Mill.). Plant Mol. Biol. 56: 849-861.
22. Harper, J. W., and Elledge, S. J. (2007). The DNA damage response: ten years after. Mol. Cell 28: 739-745.
23. Hartung, F., Suer, S., and Puchta, H. (2007). Two closely related RecQ helicases have antagonistic roles in homologous recombination and DNA repair in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 104: 18836-18841.
24. Hiller, B., Achleitner, M., Glage, S., Naumann, R., Behrendt, R., and Roers, A. (2012). Mammalian RNase H2 removes ribonucleotides from DNA to maintain genome integrity. J. Exp. Med. 209: 1419-1426.
25. Ii, M., Ii, T., Mironova, L. I., and Brill, S. J. (2011). Epistasis analysis between homologous recombination genes in Saccharomyces cerevisiae identifies multiple repair pathways for Sgs1, Mus81-Mms4 and RNase H2. Mutat. Res. 714: 33-43.
26. Jefferson, R. A., Kavanagh, T. A., and Bevan, M. W. (1987). GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 3901-3907.
27. Kim, N., Huang, S. N., Williams, J. S., Li, Y. C., Clark, A. B., Cho, J. E., Kunkel, T. A., Pommier, Y., and Jinks-Robertson, S. (2011). Mutagenic processing of ribonucleotides in DNA by yeast topoisomerase I. Science 332: 1561-1564.
28. Kinner, A., Wu, W., Staudt, C., and Iliakis, G. (2008). Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res. 36: 5678-5694.
29. Li, Y., Rosso, M. G., Strizhov, N., Viehoever, P., and Weisshaar, B. (2003). GABI-Kat SimpleSearch: a flanking sequence tag (FST) database for the identification of T-DNA insertion mutants in Arabidopsis thaliana. Bioinformatics 19: 1441-1442.
30. Lopes, M., Cotta-Ramusino, C., Pellicioli, A., Liberi, G., Plevani, P., Muzi-Falconi, M., Newlon, C. S., and Foiani, M. (2001). The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412: 557-561.
31. Mannuss, A., Dukowic-Schulze, S., Suer, S., Hartung, F., Pacher, M., and Puchta, H. (2010). RAD5A, RECQ4A, and MUS81 have specific functions in homologous recombination and define different pathways of DNA repair in Arabidopsis thaliana. Plant Cell 22: 3318-3330.
32. Miyabe, I., Kunkel, T. A., and Carr, A. M. (2011). The major roles of DNA polymerases epsilon and delta at the eukaryotic replication fork are evolutionarily conserved. PLoS Genet. 7: e1002407.
33. Molinier, J., Ries, G., Bonhoeffer, S., and Hohn, B. (2004). Interchromatid and interhomolog recombination in Arabidopsis thaliana. Plant Cell 16: 342-352.
34. Nick McElhinny, S. A., Kumar, D., Clark, A. B., Watt, D. L., Watts, B. E., Lundström, E. B., Johansson, E., Chabes, A., and Kunkel, T. A. (2010a). Genome instability due to ribonucleotide incorporation into DNA. Nat. Chem. Biol. 6: 774-781.
35. Nick McElhinny, S. A., Watts, B. E., Kumar, D., Watt, D. L., Lundström, E. B., Burgers, P. M. J., Johansson, E., Chabes, A., and Kunkel, T. A. (2010b). Abundant ribonucleotide incorporation into DNA by yeast replicative polymerases. Proc. Natl. Acad. Sci. USA 107: 4949-4954.
36. Ossowski, S., Schneeberger, K., Clark, R. M., Lanz, C., Warthmann, N., and Weigel, D. (2008). Sequencing of natural strains of Arabidopsis thaliana with short reads. Genome Res. 18: 2024-2033.
37. Reijns, M. A. M., et al. (2012). Enzymatic removal of ribonucleotides from DNA is essential for mammalian genome integrity and development. Cell 149: 1008-1022.
38. Ricaud, L., Proux, C., Renou, J. P., Pichon, O., Fochesato, S., Ortet, P., and Montané, M. H. (2007). ATM-mediated transcriptional and developmental responses to gamma-rays in Arabidopsis. PLoS ONE 2: e430.
39. Rychlik, M. P., Chon, H., Cerritelli, S. M., Klimek, P., Crouch, R. J., and Nowotny, M. (2010). Crystal structures of RNase H2 in complex with nucleic acid reveal the mechanism of RNA-DNA junction recognition and cleavage. Mol. Cell 40: 658-670.
40. Rydberg, B., and Game, J. (2002). Excision of misincorporated ribonucleotides in DNA by RNase H (type 2) and FEN-1 in cell-free extracts. Proc. Natl. Acad. Sci. USA 99: 16654-16659.
41. Sambrook, J., Russell, D. W., and Sambrook, J. (2006). The Condensed Protocols from Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
42. Schneeberger, K., Ossowski, S., Lanz, C., Juul, T., Petersen, A. H., Nielsen, K. L., Jørgensen, J. E., Weigel, D., and Andersen, S. U. (2009). SHOREmap: simultaneous mapping and mutation identification by deep sequencing. Nat. Methods 6: 550-551.
43. Schuermann, D., Fritsch, O., Lucht, J. M., and Hohn, B. (2009). Replication stress leads to genome instabilities in Arabidopsis DNA polymerase delta mutants. Plant Cell 21: 2700-2714.
44. Sekiguchi, J., and Shuman, S. (1997). Site-specific ribonuclease activity of eukaryotic DNA topoisomerase I. Mol. Cell 1: 89-97.
45. Sirbu, B. M., Couch, F. B., Feigerle, J. T., Bhaskara, S., Hiebert, S. W., and Cortez, D. (2011). Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev. 25: 1320-1327.
46. Sogo, J. M., Lopes, M., and Foiani, M. (2002). Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297: 599-602.
47. Sorrell, D. A., Marchbank, A., McMahon, K., Dickinson, J. R., Rogers, H. J., and Francis, D. (2002). A WEE1 homologue from Arabidopsis thaliana. Planta 215: 518-522.
48. Sparks, J. L., Chon, H., Cerritelli, S. M., Kunkel, T. A., Johansson, E., Crouch, R. J., and Burgers, P. M. (2012). RNase H2-initiated ribonucleotide excision repair. Mol. Cell 47: 980-986.
49. Stein, H., and Hausen, P. (1969). Enzyme from calf thymus degrading the RNA moiety of DNA-RNA Hybrids: effect on DNA-dependent RNA polymerase. Science 166: 393-395.
50. Sun, Y., Dilkes, B. P., Zhang, C., Dante, R. A., Carneiro, N. P., Lowe, K. S., Jung, R., Gordon-Kamm, W. J., and Larkins, B. A. (1999). Characterization of maize (Zea mays L.) Wee1 and its activity in developing endosperm. Proc. Natl. Acad. Sci. USA 96: 4180-4185.
51. Swoboda, P., Gal, S., Hohn, B., and Puchta, H. (1994). Intrachromosomal homologous recombination in whole plants. EMBO J. 13: 484-489.
52. Takahashi, N., Lammens, T., Boudolf, V., Maes, S., Yoshizumi, T., De Jaeger, G., Witters, E., Inzé, D., and De Veylder, L. (2008). The DNA replication checkpoint aids survival of plants deficient in the novel replisome factor ETG1. EMBO J. 27: 1840-1851.
53. Van Leene, J., et al. (2007). A tandem affinity purification-based technology platform to study the cell cycle interactome in Arabidopsis thaliana. Mol. Cell. Proteomics 6: 1226-1238.
54. Van Leene, J., Witters, E., Inzé, D., and De Jaeger, G. (2008). Boosting tandem affinity purification of plant protein complexes. Trends Plant Sci. 13: 517-520.
55. Van Leene, J., et al. (2010). Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol. Syst. Biol. 6: 397, 12.
56. Wang, J. C. (2002). Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell Biol. 3: 430-440.
57. Williams, J. S., and Kunkel, T. A. (2014). Ribonucleotides in DNA: origins, repair and consequences. DNA Repair (Amst.) 19: 27-37.
58. Williams, J. S., Clausen, A. R., Nick McElhinny, S. A., Watts, B. E., Johansson, E., and Kunkel, T. A. (2012). Proofreading of ribonucleotides inserted into DNA by yeast DNA polymerase ε. DNA Repair (Amst.) 11: 649-656.
59. Williams, J. S., Smith, D. J., Marjavaara, L., Lujan, S. A., Chabes, A., and Kunkel, T. A. (2013). Topoisomerase 1-mediated removal of ribonucleotides from nascent leading-strand DNA. Mol. Cell 49: 1010-1015.
60. Willis, N., and Rhind, N. (2009). Regulation of DNA replication by the S-phase DNA damage checkpoint. Cell Div. 4: 13.
61. Wu, T. D., and Nacu, S. (2010). Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26: 873-881.
62. Zegerman, P., and Diffley, J. F. X. (2009). DNA replication as a target of the DNA damage checkpoint. DNA Repair (Amst.) 8: 1077-1088.