In planta somatic homologous recombination assay revisited: A successful and versatile, but delicate tool

Plant Cell

Volumn 24, Issue 11, 2012, Pages 4324-4331

  Puchta, Holger ^a   Hohn, Barbara ^b  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS THALIANA;

EID: 84871888820     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.101824     Document Type: Article

References (47)

1. Abe, K., Osakabe, K., Nakayama, S., Endo, M., Tagiri, A., Todoriki, S., Ichikawa, H., and Toki, S. (2005). Arabidopsis RAD51C gene is important for homologous recombination in meiosis and mitosis. Plant Physiol. 139: 896-908.
2. Boyko, A., Blevins, T., Yao, Y., Golubov, A., Bilichak, A., Ilnytskyy, Y., Hollunder, J., Meins, F., Jr., and Kovalchuk, I. (2010). Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of Dicer-like proteins. PLoS ONE 5: e9514.
3. Chiurazzi, M., Ray, A., Viret, J.F., Perera, R., Wang, X.H., Lloyd, A.M., and Signer, E.R. (1996). Enhancement of somatic intrachromo-somal homologous recombination in Arabi-dopsis by the HO endonuclease. Plant Cell 8: 2057-2066.
4. Daxinger, L., Hunter, B., Sheikh, M., Jauvion, V., Gasciolli, V., Vaucheret, H., Matzke, M., and Furner, I. (2008). Unexpected silencing effects from T-DNA tags in Arabidopsis. Trends Plant Sci. 13: 4-6.
5. Endo, M., Ishikawa, Y., Osakabe, K., Nakayama, S., Kaya, H., Araki, T., Shibahara, K., Abe, K., Ichikawa, H., Valentine, L., Hohn, B., and Toki, S. (2006). Increased frequency of homologous recombination and T-DNA integration in Arabidopsis CAF-1 mutants. EMBO J. 25: 5579-5590.
6. Fauser, F., Roth, N., Pacher, M., Ilg, G., Sánchez-Fernández, R., Biesgen, C., and Puchta, H. (2012). In planta gene targeting. Proc. Natl. Acad. Sci. USA 109: 7535-7540.
7. Fritsch, O., Benvenuto, G., Bowler, C., Molinier, J., and Hohn, B. (2004). The INO80 protein controls homologous recombination in Arabidopsis thaliana. Mol. Cell 16: 479-485.
8. Gherbi, H., Gallego, M.E., Jalut, N., Lucht, J.M., Hohn, B., and White, C.I. (2001). Homologous recombination in planta is stimulated in the absence of Rad50. EMBO Rep. 2: 287-291.
9. 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 thali-ana. PLoS Genet. 4: e1000285.
10. 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.
11. Ilnytskyy, Y., Boyko, A., and Kovalchuk, I. (2004). Luciferase-based transgenic recombination assay is more sensitive than beta-glucoronidase-based. Mutat. Res. 559: 189-197.
12. Kilby, N.J., Leyser, H.M., and Furner, I.J. (1992). Promoter methylation and progressive transgene inactivation in Arabidopsis. Plant Mol. Biol. 20: 103-112.
13. Kinoshita, Y., Saze, H., Kinoshita, T., Miura, A., Soppe, W.J., Koornneef, M., and Kakutani, T. (2007). Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. Plant J. 49: 38-45.
14. Kirik, A., Pecinka, A., Wendeler, E., and Reiss, B. (2006). The chromatin assembly factor subunit FASCIATA1 is involved in homologous recombination in plants. Plant Cell 18: 2431-2442.
15. Knoll, A., Higgins, J.D., Seeliger, K., Reha, S.J., Dangel, N.J., Bauknecht, M., Schröpfer, 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.
16. 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.
17. Kovalchuk, I., Kovalchuk, O., Arkhipov, A., and Hohn, B. (1998). Transgenic plants are sensitive bioindicators of nuclear pollution caused by the Chernobyl accident. Nat. Biotechnol. 16: 1054-1059.
18. Kovalchuk, I., Kovalchuk, O., Kalck, V., Boyko, V., Filkowski, J., Heinlein, M., and Hohn, B. (2003). Pathogen-induced systemic plant signal triggers DNA rearrangements. Nature 423: 760-762.
19. Lebel, E.G., Masson, J., Bogucki, A., and Paszkowski, J. (1993). Stress-induced in-trachromosomal recombination in plant somatic cells. Proc. Natl. Acad. Sci. USA 90: 422-426.
20. Li, L., Santerre-Ayotte, S., Boivin, E.B., Jean, M., and Belzile, F. (2004). A novel reporter for intrachromosomal homoeologous recombination in Arabidopsis thaliana. Plant J. 40: 1007-1015.
21. Liang, L., Flury, S., Kalck, V., Hohn, B., and Molinier, J. (2006). CENTRIN2 interacts with the Arabidopsis homolog of the human XPC protein (AtRAD4) and contributes to efficient synthesis-dependent repair of bulky DNA lesions. Plant Mol. Biol. 61: 345-356.
22. Lucht, J.M., Mauch-Mani, B., Steiner, H.Y., Metraux, J.P., Ryals, J., and Hohn, B. (2002). Pathogen stress increases somatic recombination frequency in Arabidopsis. Nat. Genet. 30: 311-314.
23. 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.
24. Molinier, J., Ries, G., Bonhoeffer, S., and Hohn, B. (2004). Interchromatid and interho-molog recombination in Arabidopsis thaliana. Plant Cell 16: 342-352.
25. Molinier, J., Ries, G., Zipfel, C., and Hohn, B. (2006). Transgeneration memory of stress in plants. Nature 442: 1046-1049.
26. Opperman, R., Emmanuel, E., and Levy, A.A. (2004). The effect of sequence divergence on recombination between direct repeats in Arab-idopsis. Genetics 168: 2207-2215.
27. Orel, N., Kyryk, A., and Puchta, H. (2003). Different pathways of homologous recombination are used for the repair of double-strand breaks within tandemly arranged sequences in the plant genome. Plant J. 35: 604-612.
28. Pâques, F., and Haber, J.E. (1999). Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63: 349-404.
29. Pecinka, A., Rosa, M., Schikora, A., Berlinger, M., Hirt, H., Luschnig, C., and Mittelsten Scheid, O. (2009). Transgenerational stress memory is not a general response in Arabi-dopsis. PLoS ONE 4: e5202.
30. Peterhans, A., Schlüpmann, H., Basse, C., and Paszkowski, J. (1990). Intrachromo-somal recombination in plants. EMBO J. 9: 3437-3445.
31. Puchta, H. (2005). The repair of double-strand breaks in plants: Mechanisms and consequences for genome evolution. J. Exp. Bot. 56: 1-14.
32. Puchta, H., Dujon, B., and Hohn, B. (1996). Two different but related mechanisms are used in plants for the repair of genomic double-strand breaks by homologous recombination. Proc. Natl. Acad. Sci. USA 93: 5055-5060.
33. Puchta, H., Swoboda, P., and Hohn, B. (1995). Induction of intrachromosomal homologous recombination in whole plants. Plant J. 7: 203-210.
34. Qin, X.F., Holuigue, L., Horvath, D.M., and Chua, N.H. (1994). Immediate early transcription activation by salicylic acid via the cauliflower mosaic virus as-1 element. Plant Cell 6: 863-874.
35. Ries, G., Heller, W., Puchta, H., Sandermann, H., Seidlitz, H.K., and Hohn, B. (2000). Elevated UV-B radiation reduces genome stability in plants. Nature 406: 98-101.
36. Roth, N., Klimesch, J., Dukowic-Schulze, S., Pacher, M., Mannuss, A., and Puchta, H. (October 1, 2012). The requirement for recombination factors differs considerably between different pathways of homologous double-strand break repair in somatic plant cells. Plant J. http://dx.doi.org/10.1111/j.1365-313X.2012.05119.x.
37. 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.
38. Schuermann, D., Molinier, J., Fritsch, O., and Hohn, B. (2005). The dual nature of homologous recombination in plants. Trends Genet. 21: 172-181.
39. 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.
40. Shalev, G., and Levy, A.A. (1997). The maize transposable element Ac induces recombination between the donor site and an homologous ectopic sequence. Genetics 146: 1143-1151.
41. Siebert, R., and Puchta, H. (2002). Efficient repair of genomic double-strand breaks by homologous recombination between directly repeated sequences in the plant genome. Plant Cell 14: 1121-1131.
42. Sun, X., Zhang, Y., Yang, S., Chen, J.Q., Hohn, B., and Tian, D. (2008). Insertion DNA promotes ectopic recombination during meiosis in Arabi-dopsis. Mol. Biol. Evol. 25: 2079-2083.
43. Swoboda, P., Gal, S., Hohn, B., and Puchta, H. (1994). Intrachromosomal homologous recombination in whole plants. EMBO J. 13: 484-489.
44. Tinland, B., Hohn, B., and Puchta, H. (1994). Agrobacterium tumefaciens transfers single-stranded transferred DNA (T-DNA) into the plant cell nucleus. Proc. Natl. Acad. Sci. USA 91: 8000-8004.
45. Ülker, B., Rahman, M., Hommelsheim, C.M., Berson, T., Thomas, S., Chandrasekar, B., Olcay, A.C., Berendzen, K.W., and Frantzeskakis, L. (2012). Re-evaluation of the reliability and usefulness of the somatic homologous recombination reporter lines. Plant Cell 24: 4314-4323.
46. Wei, W., Ba, Z., Gao, M., Wu, Y., Ma, Y., Amiard, S., White, C.I., Rendtlew Danielsen, J.M., Yang, Y.G., and Qi, Y. (2012). A role for small RNAs in DNA double-strand break repair. Cell 149: 101-112.
47. Xiao, Y.L., and Peterson, T. (2000). Intrachro-mosomal homologous recombination in Arab-idopsis induced by a maize transposon. Mol. Gen. Genet. 263: 22-29.