MHF1 plays Fanconi anaemia complementation group M protein (FANCM)-dependent and FANCM-independent roles in DNA repair and homologous recombination in plants

Plant Journal

Volumn 78, Issue 5, 2014, Pages 822-833

  Dangel, Natalie J ^a   Knoll, Alexander ^a   Puchta, Holger ^a  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

Arabidopsis thaliana; DNA repair; Fanconi anaemia complementation group M protein; homologous recombination; MHF1

Indexed keywords

CHROMOSOMES; DNA; PROTEINS; REPAIR;

ARABIDOPSIS THALIANA; COMPLEMENTATION; DNA REPAIR; HOMOLOGOUS RECOMBINATION; MHF1;

PLANTS (BOTANY);

ARABIDOPSIS PROTEIN; DNA HELICASE; FANCM PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; DNA REPAIR; GENETICS; HOMOLOGOUS RECOMBINATION; METABOLISM; PHYSIOLOGY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA HELICASES; DNA REPAIR; HOMOLOGOUS RECOMBINATION;

EID: 84901399642     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12507     Document Type: Article

References (43)

1. Alonso, J.M., Stepanova, A.N., Leisse, T.J., et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657.
2. Amano, M., Suzuki, A., Hori, T., Backer, C., Okawa, K., Cheeseman, I.M., and, Fukagawa, T., (2009) The CENP-S complex is essential for the stable assembly of outer kinetochore structure. J. Cell Biol. 186, 173-182.
3. Arents, G., and, Moudrianakis, E.N., (1993) Topography of the histone octamer surface: repeating structural motifs utilized in the docking of nucleosomal DNA. Proc. Natl Acad. Sci. USA, 90, 10489-10493.
4. Armstrong, S.J., Sanchez-Moran, E., and, Franklin, F.C., (2009) Cytological analysis of Arabidopsis thaliana meiotic chromosomes. Methods Mol. Biol. 558, 131-145.
5. Bhattacharjee, S., Osman, F., Feeney, L., Lorenz, A., Bryer, C., and, Whitby, M.C., (2013) MHF1-2/CENP-S-X performs distinct roles in centromere metabolism and genetic recombination. Open Biology, 3, 130102.
6. Boddy, M.N., Gaillard, P.H., McDonald, W.H., Shanahan, P., Yates, J.R., and, Russell, P., (2001) Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell, 107, 537-548.
7. Bonnet, S., Knoll, A., Hartung, F., and, Puchta, H., (2013) Different functions for the domains of the Arabidopsis thaliana RMI1 protein in DNA cross-link repair, somatic and meiotic recombination. Nucleic Acids Res. 41, 9349-9360.
8. Boulikas, T., and, Vougiouka, M., (2003) Cisplatin and platinum drugs at the molecular level. Oncol. Rep. 10, 1663-1682.
9. Chen, X.B., Melchionna, R., Denis, C.M., Gaillard, P.H., Blasina, A., van de Weyer, I., Boddy, M.N., Russell, P., Vialard, J., and, McGowan, C.H., (2001) Human Mus81-associated endonuclease cleaves Holliday junctions in vitro. Mol. Cell, 8, 1117-1127.
10. Crismani, W., Girard, C., Froger, N., Pradillo, M., Santos, J.L., Chelysheva, L., Copenhaver, G.P., Horlow, C., and, Mercier, R., (2012) FANCM limits meiotic crossovers. Science, 336, 1588-1590.
11. Deans, A.J., and, West, S.C., (2009) FANCM connects the genome instability disorders Bloom's syndrome and Fanconi anemia. Mol. Cell, 36, 943-953.
12. Ellis, N.A., Groden, J., Ye, T.Z., Straughen, J., Lennon, D.J., Ciocci, S., Proytcheva, M., and, German, J., (1995) The Bloom's syndrome gene product is homologous to RecQ helicases. Cell, 83, 655-666.
13. Epstein, C.J., Martin, G.M., Schultz, A.L., and, Motulsky, A.G., (1966) Werner's syndrome a review of its symptomatology, natural history, pathologic features, genetics and relationship to the natural aging process. Medicine, 45, 177-221.
14. Fanconi, G., (1927) Familiäre infantile perniziosaartige Anämie (perniziöses Blutbild und Konstitution). Jahrbuch für Kinderheilkunde (Wien); 117, 257-280.
15. German, J., Archibald, R., and, Bloom, D., (1965) Chromosomal breakage in a rare and probably genetically determined syndrome of man. Science, 148, 506-507.
16. Hartung, F., Suer, S., Bergmann, T., and, Puchta, H., (2006) The role of AtMUS81 in DNA repair and its genetic interaction with the helicase AtRecQ4A. Nucleic Acids Res. 34, 4438-4448.
17. 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.
18. Hirano, S., Yamamoto, K., Ishiai, M., et al. (2005) Functional relationships of FANCC to homologous recombination, translesion synthesis, and BLM. EMBO J. 24, 418-427.
19. Hoadley, K.A., Xue, Y., Ling, C., Takata, M., Wang, W., and, Keck, J.L., (2012) Defining the molecular interface that connects the Fanconi anemia protein FANCM to the Bloom syndrome dissolvasome. Proc. Natl Acad. Sci. USA, 109, 4437-4442.
20. Kaliraman, V., Mullen, J.R., Fricke, W.M., Bastin-Shanower, S.A., and, Brill, S.J., (2001) Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes Dev. 15, 2730-2740.
21. Kim, H., and, D'Andrea, A.D., (2012) Regulation of DNA cross-link repair by the Fanconi anemia/BRCA pathway. Genes Dev. 26, 1393-1408.
22. Kitao, S., Shimamoto, A., Goto, M., Miller, R.W., Smithson, W.A., Lindor, N.M., and, Furuichi, Y., (1999) Mutations in RECQL4 cause a subset of cases of Rothmund-Thomson syndrome. Nat. Genet. 22, 82-84.
23. Knoll, A., and, Puchta, H., (2011) The role of DNA helicases and their interaction partners in genome stability and meiotic recombination in plants. J. Exp. Bot. 62, 1565-1579.
24. Knoll, A., Higgins, J.D., Seeliger, K., Reha, S.J., Dangel, N.J., Bauknecht, M., Schropfer, S., Franklin, F.C., and, Puchta, H., (2012) The Fanconi anemia ortholog FANCM ensures ordered homologous recombination in both somatic and meiotic cells in Arabidopsis. Plant Cell, 24, 1448-1464.
25. Kottemann, M.C., and, Smogorzewska, A., (2013) Fanconi anaemia and the repair of Watson and Crick DNA crosslinks. Nature, 493, 356-363.
26. Lorenz, A., Osman, F., Sun, W., Nandi, S., Steinacher, R., and, Whitby, M.C., (2012) The fission yeast FANCM ortholog directs non-crossover recombination during meiosis. Science, 336, 1585-1588.
27. 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.
28. Moldovan, G.-L., and, D'Andrea, A.D., (2009) How the Fanconi anemia pathway guards the genome. Annu. Rev. Genet. 43, 223-249.
29. Molinier, J., Ries, G., Bonhoeffer, S., and, Hohn, B., (2004) Interchromatid and interhomolog recombination in Arabidopsis thaliana. Plant Cell, 16, 342-352.
30. Nishino, T., Takeuchi, K., Gascoigne, K.E., Suzuki, A., Hori, T., Oyama, T., Morikawa, K., Cheeseman, I.M., and, Fukagawa, T., (2012) CENP-T-W-S-X forms a unique centromeric chromatin structure with a histone-like fold. Cell, 148, 487-501.
31. Patel, K.J., and, Joenje, H., (2007) Fanconi anemia and DNA replication repair. DNA Repair, 6, 885-890.
32. Pichierri, P., Franchitto, A., and, Rosselli, F., (2004) BLM and the FANC proteins collaborate in a common pathway in response to stalled replication forks. EMBO J. 23, 3154-3163.
33. Puchta, H., and, Hohn, B., (2012) In planta somatic homologous recombination assay revisited: a successful and versatile, but delicate tool. Plant Cell, 24, 4324-4331.
34. Punta, M., Coggill, P.C., Eberhardt, R.Y., et al. (2012) The Pfam protein families database. Nucleic Acids Res. 40, D290-D301.
35. Rink, S.M., Lipman, R., Alley, S.C., Hopkins, P.B., and, Tomasz, M., (1996) Bending of DNA by the mitomycin C-induced, GpG intrastrand cross-link. Chem. Res. Toxicol. 9, 382-389.
36. Scheller, J., Schürer, A., Rudolph, C., Hettwer, S., and, Kramer, W., (2000) MPH1, a yeast gene encoding a DEAH protein, plays a role in protection of the genome from spontaneous and chemically induced damage. Genetics, 155, 1069-1081.
37. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Scholkopf, B., Weigel, D., and, Lohmann, J.U., (2005) A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37, 501-506.
38. Schröpfer, S., Kobbe, D., Hartung, F., Knoll, A., and, Puchta, H., (2013) Defining the roles of the N-terminal region and the helicase activity of RECQ4A in DNA repair and homologous recombination in Arabidopsis. Nucleic Acids Res. 42 (3), 1684-1697.
39. Singh, T.R., Saro, D., Ali, A.M., et al. (2010) MHF1-MHF2, a histone-fold-containing protein complex, participates in the Fanconi anemia pathway via FANCM. Mol. Cell, 37, 879-886.
40. Sugahara, R., Mon, H., Lee, J.M., and, Kusakabe, T., (2013) Middle region of FancM interacts with Mhf and Rmi1 in silkworms, a species lacking the Fanconi anaemia (FA) core complex. Insect Mol. Biol. 23 (2), 185-198.
41. Tao, Y., Jin, C., Li, X., Qi, S., Chu, L., Niu, L., Yao, X., and, Teng, M., (2012) The structure of the FANCM-MHF complex reveals physical features for functional assembly. Nat. Commun. 3, 782.
42. Woody, S.T., Austin-Phillips, S., Amasino, R.M., and, Krysan, P.J., (2007) The WiscDsLox T-DNA collection: an Arabidopsis community resource generated by using an improved high-throughput T-DNA sequencing pipeline. J. Plant. Res. 120, 157-165.
43. Yan, Z., Delannoy, M., Ling, C., et al. (2010) A histone-fold complex and FANCM form a conserved DNA-remodeling complex to maintain genome stability. Mol. Cell, 37, 865-878.