The fanconi anemia ortholog FANCM ensures ordered homologous recombination in both somatic and meiotic Cells in Arabidopsis

Plant Cell

Volumn 24, Issue 4, 2012, Pages 1448-1464

  Knoll, Alexander ^a   Higgins, James D ^b   Seeliger, Katharina ^a   Reha, Sarah J ^a   Dangel, Natalie J ^a   Bauknecht, Markus ^a   Schröpfer, Susan ^a   Franklin, F Christopher H ^b   Puchta, Holger ^a  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; SYNAPSIS;

EID: 84861675090     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.096644     Document Type: Article

References (86)

1. Allers, T., and Lichten, M. (2001). Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106: 47-57.
2. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
3. Armstrong, S.J., Caryl, A.P., Jones, G.H., and Franklin, F.C. (2002). Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J. Cell Sci. 115: 3645-3655.
4. Armstrong, S.J., Sanchez-Moran, E., and Franklin, F.C. (2009). Cytological analysis of Arabidopsis thaliana meiotic chromosomes. In Methods in Molecular Biology: Meiosis: Cytological Methods, Vol. 2, S. Keeney, ed (New York: Humana Press; Springer), pp. 131-145.
5. Bakker, S.T., van de Vrugt, H.J., Rooimans, M.A., Oostra, A.B., Steltenpool, J., Delzenne-Goette, E., van der Wal, A., van der Valk, M., Joenje, H., te Riele, H., and de Winter, J.P. (2009). Fancm-deficient mice reveal unique features of Fanconi anemia complementation group M. Hum. Mol. Genet. 18: 3484-3495.
6. Berchowitz, L.E., and Copenhaver, G.P. (2010). Genetic interference: Don't stand so close to me. Curr. Genomics 11: 91-102.
7. Börner, G.V., Kleckner, N., and Hunter, N. (2004). Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117: 29-45.
8. Chelysheva, L., Grandont, L., Vrielynck, N., le Guin, S., Mercier, R., and Grelon, M. (2010). An easy protocol for studying chromatin and recombination protein dynamics during Arabidopsis thaliana meiosis: Immunodetection of cohesins, histones and MLH1. Cytogenet. Genome Res. 129: 143-153.
9. Chelysheva, L., Vezon, D., Belcram, K., Gendrot, G., and Grelon, M. (2008). The Arabidopsis BLAP75/Rmi1 homologue plays crucial roles in meiotic double-strand break repair. PLoS Genet. 4: e1000309.
10. Clark, K.A., and Krysan, P.J. (2010). Chromosomal translocations are a common phenomenon in Arabidopsis thaliana T-DNA insertion lines. Plant J. 64: 990-1001.
11. Collis, S.J., Ciccia, A., Deans, A.J., Horejsí, Z., Martin, J.S., Maslen, S.L., Skehel, J.M., Elledge, S.J., West, S.C., and Boulton, S.J. (2008). FANCM and FAAP24 function in ATR-mediated checkpoint signaling independently of the Fanconi anemia core complex. Mol. Cell 32: 313-324.
12. Curtis, M.J., Belcram, K., Bollmann, S.R., Tominey, C.M., Hoffman, P.D., Mercier, R., and Hays, J.B. (2009). Reciprocal chromosome translocation associated with TDNA-insertion mutation in Arabidopsis: Genetic and cytological analyses of consequences for gametophyte development and for construction of doubly mutant lines. Planta 229: 731-745.
13. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K., and Scheible, W.R. (2005). Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139: 5-17.
14. De Silva, I.U., McHugh, P.J., Clingen, P.H., and Hartley, J.A. (2000). Defining the roles of nucleotide excision repair and recombination in the repair of DNA interstrand cross-links in mammalian cells. Mol. Cell. Biol. 20: 7980-7990.
15. de Winter, J.P., and Joenje, H. (2009). The genetic and molecular basis of Fanconi anemia. Mutat. Res. 668: 11-19.
16. Ede, C., Rudolph, C.J., Lehmann, S., Schürer, K.A., and Kramer, W. (2011). Budding yeast Mph1 promotes sister chromatid interactions by a mechanism involving strand invasion. DNA Repair (Amst.) 10: 45-55.
17. Fanconi, G. (1927). Familiäre infantile perniziosaartige Anämie (perniziöses Blutbild und Konstitution). In Jahrbuch für Kinderheilkunde (Berlin: Karger), pp. 257-280.
18. Ferdous, M., Higgins, J.D., Osman, K., Lambing, C., Roitinger, E., Mechtler, K., Armstrong, S.J., Perry, R., Pradillo, M., Cuñado, N., and Franklin, F.C.H. (2012). Inter-homolog crossing-over and synapsis in Arabidopsis meiosis are dependent on the chromosome axis protein AtASY3. PLoS Genet. 8: e1002507.
19. Fung, J.C., Rockmill, B., Odell, M., and Roeder, G.S. (2004). Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116: 795-802.
20. Gangloff, S., McDonald, J.P., Bendixen, C., Arthur, L., and Rothstein, R. (1994). The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: A potential eukaryotic reverse gyrase. Mol. Cell. Biol. 14: 8391-8398.
21. Gari, K., Décaillet, C., Delannoy, M., Wu, L., and Constantinou, A. (2008b). Remodeling of DNA replication structures by the branch point translocase FANCM. Proc. Natl. Acad. Sci. USA 105: 16107-16112.
22. Gari, K., Décaillet, C., Stasiak, A.Z., Stasiak, A., and Constantinou, A. (2008a). The Fanconi anemia protein FANCM can promote branch migration of Holliday junctions and replication forks. Mol. Cell 29: 141-148.
23. Geuting, V., Kobbe, D., Hartung, F., Dürr, J., Focke, M., and Puchta, H. (2009). Two distinct MUS81-EME1 complexes from Arabidopsis process Holliday junctions. Plant Physiol. 150: 1062-1071.
24. Grelon, M., Vezon, D., Gendrot, G., and Pelletier, G. (2001). At- SPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J. 20: 589-600.
25. Hartung, F., and Puchta, H. (2000). Molecular characterisation of two paralogous SPO11 homologues in Arabidopsis thaliana. Nucleic Acids Res. 28: 1548-1554.
26. 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.
27. Hartung, F., Suer, S., Knoll, A., Wurz-Wildersinn, R., and Puchta, H. (2008). Topoisomerase 3alpha and RMI1 suppress somatic crossovers and are essential for resolution of meiotic recombination intermediates in Arabidopsis thaliana. PLoS Genet. 4: e1000285.
28. Hartung, F., Suer, S., and Puchta, H. (2007a). 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.
29. Hartung, F., Wurz-Wildersinn, R., Fuchs, J., Schubert, I., Suer, S., and Puchta, H. (2007b). The catalytically active tyrosine residues of both SPO11-1 and SPO11-2 are required for meiotic double-strand break induction in Arabidopsis. Plant Cell 19: 3090-3099.
30. Heslop-Harrison, J., and Heslop-Harrison, Y. (1970). Evaluation of pollen viability by enzymatically induced fluorescence; intracellular hydrolysis of fluorescein diacetate. Stain Technol. 45: 115-120.
31. Higgins, J.D., Armstrong, S.J., Franklin, F.C., and Jones, G.H. (2004). The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: Evidence for two classes of recombination in Arabidopsis. Genes Dev. 18: 2557-2570.
32. Higgins, J.D., Buckling, E.F., Franklin, F.C., and Jones, G.H. (2008a). Expression and functional analysis of AtMUS81 in Arabidopsis meiosis reveals a role in the second pathway of crossingover. Plant J. 54: 152-162.
33. Higgins, J.D., Ferdous, M., Osman, K., and Franklin, F.C. (2011). The RecQ helicase AtRECQ4A is required to remove inter-chromosomal telomeric connections that arise during meiotic recombination in Arabidopsis. Plant J. 65: 492-502.
34. Higgins, J.D., Sanchez-Moran, E., Armstrong, S.J., Jones, G.H., and Franklin, F.C. (2005). The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev. 19: 2488-2500.
35. Higgins, J.D., Vignard, J., Mercier, R., Pugh, A.G., Franklin, F.C., and Jones, G.H. (2008b). AtMSH5 partners AtMSH4 in the class I meiotic crossover pathway in Arabidopsis thaliana, but is not required for synapsis. Plant J. 55: 28-39.
36. Hirayama, T., Fujishige, N., Kunii, T., Nishimura, N., Iuchi, S., and Shinozaki, K. (2004). A novel ethanol-hypersensitive mutant of Arabidopsis. Plant Cell Physiol. 45: 703-711.
37. Jackson, N., Sanchez-Moran, E., Buckling, E., Armstrong, S.J., Jones, G.H., and Franklin, F.C. (2006). Reduced meiotic crossovers and delayed prophase I progression in AtMLH3-deficient Arabidopsis. EMBO J. 25: 1315-1323.
38. Jessop, L., Rockmill, B., Roeder, G.S., and Lichten, M. (2006). Meiotic chromosome synapsis-promoting proteins antagonize the anti-crossover activity of sgs1. PLoS Genet. 2: e155.
39. Jones, G.H. (1984). The control of chiasma distribution. Symp. Soc. Exp. Biol. 38: 293-320.
40. Jones, G.H., and Franklin, F.C. (2006). Meiotic crossing-over: Obligation and interference. Cell 126: 246-248.
41. Keeney, S., Giroux, C.N., and Kleckner, N. (1997). Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88: 375-384.
42. Klimyuk, V.I., and Jones, J.D. (1997). AtDMC1, the Arabidopsis homologue of the yeast DMC1 gene: Characterization, transposoninduced allelic variation and meiosis-associated expression. Plant J. 11: 1-14.
43. 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.
44. Langevin, F., Crossan, G.P., Rosado, I.V., Arends, M.J., and Patel, K.J. (2011). Fancd2 counteracts the toxic effects of naturally produced aldehydes in mice. Nature 475: 53-58.
45. Li, W., Chen, C., Markmann-Mulisch, U., Timofejeva, L., Schmelzer, E., Ma, H., and Reiss, B. (2004). The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. Proc. Natl. Acad. Sci. USA 101: 10596-10601.
46. Lu, X., Liu, X., An, L., Zhang, W., Sun, J., Pei, H., Meng, H., Fan, Y., and Zhang, C. (2008). The Arabidopsis MutS homolog AtMSH5 is required for normal meiosis. Cell Res. 18: 589-599.
47. Luke-Glaser, S., Luke, B., Grossi, S., and Constantinou, A. (2010). FANCM regulates DNA chain elongation and is stabilized by S-phase checkpoint signalling. EMBO J. 29: 795-805.
48. 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.
49. Marcon, E., and Moens, P. (2003). MLH1p and MLH3p localize to precociously induced chiasmata of okadaic-acid-treated mouse spermatocytes. Genetics 165: 2283-2287.
50. Marnett, L.J. (1999). Lipid peroxidation-DNA damage by malondialdehyde. Mutat. Res. 424: 83-95.
51. Meetei, A.R., et al. (2005). A human ortholog of archaeal DNA repair protein Hef is defective in Fanconi anemia complementation group M. Nat. Genet. 37: 958-963.
52. Mercier, R., Armstrong, S.J., Horlow, C., Jackson, N.P., Makaroff, C.A., Vezon, D., Pelletier, G., Jones, G.H., and Franklin, F.C. (2003). The meiotic protein SWI1 is required for axial element formation and recombination initiation in Arabidopsis. Development 130: 3309-3318.
53. Molinier, J., Ries, G., Bonhoeffer, S., and Hohn, B. (2004). Interchromatid and interhomolog recombination in Arabidopsis thaliana. Plant Cell 16: 342-352.
54. Neveling, K., Endt, D., Hoehn, H., and Schindler, D. (2009). Genotype-phenotype correlations in Fanconi anemia. Mutat. Res. 668: 73-91.
55. Obayashi, T., Hayashi, S., Saeki, M., Ohta, H., and Kinoshita, K. (2009). ATTED-II provides coexpressed gene networks for Arabidopsis. Nucleic Acids Res. 37(Database issue): D987-D991.
56. Oh, S.D., Lao, J.P., Hwang, P.Y., Taylor, A.F., Smith, G.R., and Hunter, N. (2007). BLM ortholog, Sgs1, prevents aberrant crossingover by suppressing formation of multichromatid joint molecules. Cell 130: 259-272.
57. Osman, K., Higgins, J.D., Sanchez-Moran, E., Armstrong, S.J., and Franklin, F.C. (2011). Pathways to meiotic recombination in Arabidopsis thaliana. New Phytol. 190: 523-544.
58. Panico, E.R., Ede, C., Schildmann, M., Schürer, K.A., and Kramer, W. (2010). Genetic evidence for a role of Saccharomyces cerevisiae Mph1 in recombinational DNA repair under replicative stress. Yeast 27: 11-27.
59. Patel, K.J., and Joenje, H. (2007). Fanconi anemia and DNA replication repair. DNA Repair (Amst.) 6: 885-890.
60. Prakash, R., Krejci, L., Van Komen, S., Anke Schürer, K., Kramer, W., and Sung, P. (2005). Saccharomyces cerevisiae MPH1 gene, required for homologous recombination-mediated mutation avoidance, encodes a 39 to 59 DNA helicase. J. Biol. Chem. 280: 7854-7860.
61. Puchta, H. (2005). The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. J. Exp. Bot. 56: 1-14.
62. Räschle, M., Knipscheer, P., Enoiu, M., Angelov, T., Sun, J., Griffith, J.D., Ellenberger, T.E., Schärer, O.D., and Walter, J.C. (2008). Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 134: 969-980. Erratum. Cell 137: 972.
63. Rockmill, B., Fung, J.C., Branda, S.S., and Roeder, G.S. (2003). The Sgs1 helicase regulates chromosome synapsis and meiotic crossing over. Curr. Biol. 13: 1954-1962.
64. Rogakou, E.P., Boon, C., Redon, C., and Bonner, W.M. (1999). Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146: 905-916.
65. Rosado, I.V., Langevin, F., Crossan, G.P., Takata, M., and Patel, K.J. (2011). Formaldehyde catabolism is essential in cells deficient for the Fanconi anemia DNA-repair pathway. Nat. Struct. Mol. Biol. 18: 1432-1434.
66. Rosso, M.G., Li, Y., Strizhov, N., Reiss, B., Dekker, K., and Weisshaar, B. (2003). An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol. Biol. 53: 247-259.
67. Sanchez-Moran, E., Armstrong, S.J., Santos, J.L., Franklin, F.C., and Jones, G.H. (2002). Variation in chiasma frequency among eight accessions of Arabidopsis thaliana. Genetics 162: 1415-1422.
68. Sanchez-Moran, E., Santos, J.L., Jones, G.H., and Franklin, F.C. (2007). ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev. 21: 2220-2233.
69. 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.
70. Schürer, K.A., Rudolph, C., Ulrich, H.D., and Kramer, W. (2004). Yeast MPH1 gene functions in an error-free DNA damage bypass pathway that requires genes from homologous recombination, but not from postreplicative repair. Genetics 166: 1673-1686.
71. Schwab, R.A., Blackford, A.N., and Niedzwiedz, W. (2010). ATR activation and replication fork restart are defective in FANCM-deficient cells. EMBO J. 29: 806-818.
72. Schwacha, A., and Kleckner, N. (1997). Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell 90: 1123-1135.
73. Seeliger, K., Dukowic-Schulze, S., Wurz-Wildersinn, R., Pacher, M., and Puchta, H. (2012). BRCA2 is a mediator of RAD51- and DMC1-facilitated homologous recombination in Arabidopsis thaliana. New Phytol. 193: 364-375.
74. Sessions, A., et al. (2002). A high-throughput Arabidopsis reverse genetics system. Plant Cell 14: 2985-2994.
75. Shinohara, A., and Shinohara, M. (2004). Roles of RecA homologues Rad51 and Dmc1 during meiotic recombination. Cytogenet. Genome Res. 107: 201-207.
76. Siebert, R., and Puchta, H. (2002). Efficient repair of genomic doublestrand breaks by homologous recombination between directly repeated sequences in the plant genome. Plant Cell 14: 1121-1131.
77. Snowden, T., Acharya, S., Butz, C., Berardini, M., and Fishel, R. (2004). hMSH4-hMSH5 recognizes Holliday Junctions and forms a meiosis-specific sliding clamp that embraces homologous chromosomes. Mol. Cell 15: 437-451.
78. Stacey, N.J., Kuromori, T., Azumi, Y., Roberts, G., Breuer, C., Wada, T., Maxwell, A., Roberts, K., and Sugimoto-Shirasu, K. (2006). Arabidopsis SPO11-2 functions with SPO11-1 in meiotic recombination. Plant J. 48: 206-216.
79. Storlazzi, A., Gargano, S., Ruprich-Robert, G., Falque, M., David, M., Kleckner, N., and Zickler, D. (2010). Recombination proteins mediate meiotic spatial chromosome organization and pairing. Cell 141: 94-106.
80. Sun, W., Nandi, S., Osman, F., Ahn, J.S., Jakovleska, J., Lorenz, A., and Whitby, M.C. (2008). The FANCM ortholog Fml1 promotes recombination at stalled replication forks and limits crossing over during DNA double-strand break repair. Mol. Cell 32: 118-128.
81. Szostak, J.W., Orr-Weaver, T.L., Rothstein, R.J., and Stahl, F.W. (1983). The double-strand-break repair model for recombination. Cell 33: 25-35.
82. Trivin, C., Gluckman, E., Leblanc, T., Cousin, M.N., Soulier, J., and Brauner, R. (2007). Factors and markers of growth hormone secretion and gonadal function in Fanconi anemia. Growth Horm. IGF Res. 17: 122-129.
83. Wei, Y., Lin, M., Oliver, D.J., and Schnable, P.S. (2009). The roles of aldehyde dehydrogenases (ALDHs) in the PDH bypass of Arabidopsis. BMC Biochem. 10: 7.
84. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V., and Provart, N.J. (2007). An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2: e718.
85. Xu, L., Weiner, B.M., and Kleckner, N. (1997). Meiotic cells monitor the status of the interhomolog recombination complex. Genes Dev. 11: 106-118.
86. Youds, J.L., Mets, D.G., McIlwraith, M.J., Martin, J.S., Ward, J.D., ONeil, N.J., Rose, A.M., West, S.C., Meyer, B.J., and Boulton, S.J. (2010). RTEL-1 enforces meiotic crossover interference and homeostasis. Science 327: 1254-1258.