On the role of some ARGONAUTE proteins in meiosis and DNA repair in Arabidopsis thaliana

Frontiers in Plant Science

Volumn 5, Issue MAY, 2014, Pages

  Oliver, Cecilia ^a   Santos, Juan L ^a   Pradillo, Mónica ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Arabidopsis; ARGONAUTE proteins; DNA repair; Meiosis; Small RNAs

Indexed keywords

EID: 84902287755     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00177     Document Type: Article

References (64)

1. Alonso, J. M., Stepanova, A. N., Leisse, T. J., Kim, C. J., Chen, H., Shinn, P., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657. doi: 10.1126/science.1086391
2. Amiard, S., Charbonnel, C., Allain, E., Depeiges, A., and White, C. I. (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. doi: 10.1105/tpc.110.078527
3. Baumberger, N., and Baulcombe, D. C. (2005). Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc. Natl. Acad. Sci. U.S.A. 102, 11928-11933. doi: 10.1073/pnas.0505461102
4. Blevins, T., Rajeswaran, R., Shivaprasad, P. V., Beknazariants, D., Si-Ammour, A., Park, H. S., et al. (2006). Four plant Dicers mediate viral small RNA biogenesis and DNA virus induced silencing. Nucleic Acids Res. 34, 6233-6246. doi: 10.1093/nar/gkl886
5. Bohmert, K., Camus, I., Bellini, C., Bouchez, D., Caboche, M., and Benning, C. (1998). AGO1 defines a novel locus ofArabidopsis controlling leaf development. EMBO J. 17, 170-180. doi: 10.1093/emboj/17.1.170
6. Borges, F., Gomes, G., Gardner, R., Moreno, N., McCormick, S., Feijó, J. A., et al. (2008). Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol. 148, 1168-1181. doi: 10.1104/pp.108.125229
7. Borges, F., Pereira, P. A., Slotkin, R. K., Martienssen, R., and Becker, J. D. (2011). MicroRNA activity in theArabidopsis male germline. J. Exp. Bot. 62, 1611-1620. doi: 10.1093/jxb/erq452
8. Borsani, O., Zhu, J., Verslues, P. E., Sunkar, R., and Zhu, J. K. (2005). Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123, 1279-1291. doi: 10.1016/j.cell.2005.11.035
9. Campell, B. R., Song, Y., Posch, T. E., Cullis, C. A., and Town, C. D. (1992). Sequence and organization of 5S ribosomal RNA-encoding genes of Arabidopsis thaliana. Gene 112, 225-228. doi: 10.1016/0378-1119(92)90380-8
10. Castel, S. E., and Martienssen, A. (2013). RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat. Rev. Genet. 14, 100-112. doi: 10.1038/nrg3355
11. Chen, I., Haehnel, U., Altschmied, L., Schubert, I., and Puchta, H. (2003). The transcriptional response ofArabidopsis to genotoxic stress-a high density colony array study (HDCA). Plant J. 35, 771-786. doi: 10.1046/j.1365-313X.2003.01847.x
12. Conrad, M. N., Lee, C. Y., Chao, G., Shinohara, M., Kosaka, H., Shinohara, A., et al. (2008). Rapid telomere movement in meiotic prophase is promoted by NDJ1, MPS3, CSM4 and is modulated by recombination. Cell 133, 1175-1187. doi: 10.1016/j.cell.2008.04.047
13. Crismani, W., Girard, C., Froger, N., Pradillo, M., Santos, J. L., Chelysheva, L., et al. (2012). FANCM limits meiotic crossovers. Science 336, 1588-1590. doi: 10.1126/science.1220381
14. Culligan, K. M., and Britt, A. B. (2008). Both ATM and ATR promote the efficient and accurate processing of programmed meiotic double-strand breaks. Plant J. 55, 629-638. doi: 10.1111/j.1365-313X.2008.03530.x
15. 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. doi: 10.1111/j.1365-313X.2006.02931.x
16. Deans, A. J., and West, S. C. (2011). DNA interstrand crosslink repair and cancer. Nat. Rev. Cancer 11, 467-480. doi: 10.1038/nrc3088
17. Durán-Figueroa, N., and Vielle-Calzada, J. P. (2010). ARGONAUTE9-dependent silencing of transposable elements in pericentromeric regions of Arabidopsis. Plant Signal. Behav. 5, 1476-1479. doi: 10.4161/psb.5.11.13548
18. Eastman, A. (1985). Interstrand cross-links and sequence specificity in the reaction of cis-dichloro (ethylenediamine) platinum (II) with DNA. Biochemistry 24, 5027-5032. doi: 10.1021/bi00340a011
19. Gao, M., Wei, W., Li, M. M., Wu, Y. S., Ba, Z., Jin, K. X., et al. (2014). Ago2 facilitates Rad51 recruitment and DNA double-strand break repair by homologous recombination. Cell Res. doi: 10.1038/cr.2014.36. [Epub ahead of print].
20. Gerlach, W. L., and Bedbrook, J. R. (1979). Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucleic Acids Res. 7, 1869-1885. doi: 10.1093/nar/7.7.1869
21. Grant-Downton, R., Le Trionnaire, G., Schmid, R., Rodriguez-Enriquez, J., Hafidh, S., Mehdi, S., et al. (2009). MicroRNA and tasiRNA diversity in mature pollen of Arabidopsis thaliana. BMC Genomics 10:643. doi: 10.1186/1471-2164-10-643
22. Harvey, J. J., Lewsey, M. G., Patel, K., Westwood, J., Hemstädt, S., Carr, J. P., et al. (2011). An antiviral defense role of AGO2 in plants. PLoS ONE 6:e14639. doi: 10.1371/journal.pone.0014639
23. Havecker, E. R., Wallbridge, L. M., Hardcastle, T. J., Bush, M. S., Kelly, K. A., Dunn, R. M., et al. (2010). TheArabidopsis RNA-directed DNA methylation argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell 22, 321-334. doi: 10.1105/tpc.109.072199
24. Jamalkandi, S. A., and Masoudi-Nejad, A. (2009). Reconstruction of Arabidopsis thaliana fully integrated small RNA pathway. Funct. Integr. Genomics 9, 419-432. doi: 10.1007/s10142-009-0141-z
25. Ji, L., Liu, X., Yan, J., Wang, W., Yumul, R. E., Kim, Y. J., et al. (2011). ARGONAUTE10 and ARGONAUTE1 regulate the termination of floral stem cells through two microRNAs in Arabidopsis. PLoS Genet. 7:e1001358. doi: 10.1371/journal.pgen.1001358
26. Jin, H., Vacic, V., Girke, T., Lonardi, S., and Zhu, J. K. (2008). Small RNAs and the regulation of cis-natural antisense transcripts in Arabidopsis. BMC Mol. Biol. 9:6. doi: 10.1186/1471-2199-9-6
27. Kapoor, M., Arora, R., Lama, T., Nijhawan, A., Khurana, J. P., Tyagi, A. K., et al. (2008). Genome-wide identification, organization and phylogenetic analysis of Dicer-like, Argonaute and RNA-dependent RNA Polymerase gene families and their expression analysis during reproductive development and stress in rice. BMC Genomics 9:451. doi: 10.1186/1471-2164-9-451
28. Knoll, A., Higgins, J. D., Seeliger, K., Reha, S. J., Dangel, N. J., Bauknecht, M., et al. (2012). The Fanconi anemia ortholog FANCM ensures ordered homologous recombination in both somatic and meiotic cells in Arabidopsis. Plant Cell 24, 1448-1464. doi: 10.1105/tpc.112.096644
29. Koszul, R., Kim, K. P., Prentiss, M., Kleckner, N., and Kameoka, S. (2008). Meiotic chromosome move by linkage to dynamic actin cables with transduction of force the nuclear envelope. Cell 133, 1188-1201. doi: 10.1016/j.cell.2008.04.050
30. López, E., Pradillo, M., Oliver, C., Romero, C., Cuñado, N., and Santos, J. L. (2012). Looking for natural variation in chiasma frequency in Arabidopsis thaliana. J. Exp. Bot. 63, 887-894. doi: 10.1093/jxb/err319
31. López, E., Pradillo, M., Romero, C., Santos, J. L., and Cuñado, N. (2008). Pairing and synapsis in wild typeArabidopsis thaliana. Chromosome Res. 16, 701-708. doi: 10.1007/s10577-008-1220-z
32. Mallory, A. C., Hinze, A., Tucker, M. R., Bouché, N., Gasciolli, V., Elmayan, T., et al. (2009). Redundant and specific roles of the ARGONAUTE proteins AGO1 and ZLL in development and small RNA-directed gene silencing. PLoS Genet. 5:e1000646. doi: 10.1371/journal.pgen.1000646
33. Mannuss, A., Dukowic-Schulze, S., Suer, S., Hartung, F., Pacher, M., and Puchta, H. (2010). RAD5, RECQ4A, and MUS81 have specific functions in homologous recombination and define different pathways of DNA repair inArabidopsis thaliana. Plant Cell 22, 3318-3330. doi: 10.1105/tpc.110.078568
34. Martínez-Zapater, J. M., Estelle, M. A., and Somerville, C. (1986). A highly repeated DNA sequence in Arabidopsis thaliana. Mol. Gen. Genet. 204, 417-423. doi: 10.1007/BF00331018
35. Mathieu, O., Picard, G., and Tourmente, S. (2002). Methylation of a euchromatin-heterochromatin transition region in Arabidopsis thaliana chromosome 5 left arm. Chromosome Res. 10, 455-466. doi: 10.1023/A:1020936229771
36. Matzke, M., and Birchler, J. A. (2005). RNAi-mediated pathways in the nucleus. Nat. Rev. Genet. 6, 24-35. doi: 10.1038/nrg1500
37. Mi, S., Cai, T., Hu, Y., Chen, Y., Hodges, E., Ni, F., et al. (2008). Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133, 116-127. doi: 10.1016/j.cell.2008.02.034
38. Montgomery, T. A., Howell, M. D., Cuperus, J. T., Hansen, J. E., Alexander, A. L., Chapman, E. J., et al. (2008). Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell133, 124-141. doi: 10.1016/j.cell.2008.02.033
39. Nonomura, K. I., Morohoshi, A., Nakano, M., Eiguchi, M., Miyao, A., Hirochika, H., et al. (2007). A germ cell specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice. Plant Cell 19, 2583-2594. doi: 10.1105/tpc.107.053199
40. Olmedo-Monfil, V., Durán-Figueroa, N., Arteaga-Vázquez, M., Demesa-Arévalo, E., Autran, D., Grimanelli, D., et al. (2010). Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464, 628-632. doi: 10.1038/nature08828
41. Perrella, G., Consiglio, M. F., Aiese-Cigliano, R., Cremona, G., Sánchez-Morán, E., Barra, L., et al. (2010). Histone hyperacetylation affects meiotic recombination and chromosome segregation in Arabidopsis. Plant J. 62, 796-806. doi: 10.1111/j.1365-313X.2010.04191.x
42. Rink, S. M., Lipman, R., Alley, S. C., Hopkins, P. B., and Tomasz, M. (1996). Bending of DNA by the mitomycin C-induced, GpGintrastrand cross-link. Chem. Res. Toxicol. 9, 382-389. doi: 10.1021/tx950156q
43. Ron, M., Alandete Saez, M., Eshed Williams, L., Fletcher, J. C., and McCornick, S. (2010). Proper regulation of a sperm-specific cis-nat-siRNA is essential for double fertilization in Arabidopsis. Genes Dev. 24, 1010-1021. doi: 10.1101/gad.1882810
44. Sánchez-Morán, E., Armstrong, S. J., Santos, J. L., Franklin, F. C. H., and Jones, G. H. (2001). Chiasma formation inArabidopsis thaliana accession Wassileskija and in two meiotic mutants. Chromosome Res. 9, 121-128. doi: 10.1023/A:1009278902994
45. Sánchez-Morán, E., Armstrong, S. J., Santos, J. L., Franklin, F. C. H., and Jones, G. H. (2002). Variation in chiasma frequency among eight accessions of Arabidopsis thaliana. Genetics 162, 1415-1422.
46. Scherthan, H., Wang, H., Adelfak, C., White, F. J., Cowan, C., Cande, W. Z., et al. (2007). Chromosome mobility during meiotic prophase in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 104, 16934-16939. doi: 10.1073/pnas.0704860104
47. Schmid, M., Davison, T. S., Henz, S. R., Pape, U. J., Demar, M., Vingron, M., et al. (2005). A gene expression map ofArabidopsis thaliana development. Nat. Genet. 37, 501-506. doi: 10.1038/ng1543
48. Singh, M., Goel, S., Meeley, R. B., Dantec, C., Parrinello, H., Michaud, C., et al. (2011). Production of viable gametes without meiosis in maize deficient for an ARGONAUTE protein. Plant Cell 23, 443-458. doi: 10.1105/tpc.110.079020
49. Storlazzi, A., Gargano, S., Ruprich-Robert, G., Falque, M., David, M., Kleckner, N., et al. (2010). Recombination proteins mediate meiotic spatial chromosome organization and pairing. Cell 141, 94-106. doi: 10.1016/j.cell.2010.02.041
50. Takeda, A., Iwasaki, S., Watanabe, T., Utsumi, M., and Watanabe, Y. (2008). The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins. Plant Cell Physiol. 49, 493-500. doi: 10.1093/pcp/pcn043
51. Tucker, M. R., Okada, T., Hu, Y., Scholefield, A., Taylor, J. M., and Koltunow, A. M. G. (2012). Somatic small RNA pathways promote the mitotic events of megagametogenesis during female reproductive development inArabidopsis. Development 139, 1399-1404. doi: 10.1242/dev.075390
52. Vaucheret, H. (2008). Plant ARGONAUTES. Trends Plant Sci. 13, 350-358. doi: 10.1016/j.tplants.2008.04.007
53. Vaucheret, H., Vazquez, F., Crété, P., and Bartel, D. P. (2004). The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev. 18, 1187-1197. doi: 10.1101/gad.1201404
54. Von Wettstein, D., Rasmussen, S. W., and Holm, P. B. (1984). The synaptonemal complex in genetic segregation. Annu. Rev. Genet. 18, 331-413. doi: 10.1146/annurev.genet.18.1.331
55. Wang, C. R., Carlton, P. M., Golubovskaya, I. N., and Cande, W. Z. (2009). Interlock formation and coiling of meiotic chromosome axes during synapsis. Genetics 183, 905-915. doi: 10.1534/genetics.109.108688
56. Wang, X. B., Jovel, J., Udomporn, P., Wang, Y., Wu, Q., Li, W. X., et al. (2011). The 21-nucleotide, but not 22-nucleotide, viral secondary small interfering RNAs direct potent antiviral defense by two cooperative argonautes in Arabidopsis thaliana. Plant Cell 23, 1625-1638. doi: 10.1105/tpc.110.082305
57. Wassenegger, M., Heimes, S., Riedel, L., and Sänger, H. L. (1994). RNA-directed de novo methylation of genomic sequences in plants. Cell 76, 567-576. doi: 10.1016/0092-8674(94)90119-8
58. Wei, W., Ba, Z., Gao, M., Wu, Y., Ma, Y., Amiard, S., et al. (2012). A role for small RNAs in DNA double-strand repair. Cell 149, 101-112. doi: 10.1016/j.cell.2012.03.002
59. West, C. E., Waterworth, W. M., Sunderland, P. A., and Bray, C. M. (2004). Arabidopsis DNA double-strand break repair pathways. Biochem. Soc. Trans. 32, 964-966. doi: 10.1042/BST0320964
60. Wood, V., Gwilliam, R., Rajanderam, M. A., Lyne, M., Lyne, R., Stewart, A., et al. (2002). The genome sequence ofSchizosaccharomyces pombe. Nature 415, 871-880. doi: 10.1038/nature724
61. Wuest, S. E., Vijverberg, K., Schmidt, A., Weiss, M., Gheyselinck, J., Lohr, M., et al. (2010). Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Curr. Biol. 20, 506-512. doi: 10.1016/j.cub.2010.01.051
62. Xie, Z., Johansen, L. K., Gustafson, A. M., Kasschau, K. D., Lellis, A. D., Zilberman, D., et al. (2004). Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2:E104. doi: 10.1371/journal.pbio.0020104
63. Yao, Y., Bilichak, A., Golubov, A., Blevins, T., and Kovalchuk, I. (2010). Differential sensitivity of ArabidopsissiRNA biogenesis mutants to genotoxic stress. Plant Cell Rep. 29, 1401-1410. doi: 10.1007/s00299-010-0930-9
64. Zickler, D., and Kleckner, N. (1999). Meiotic chromosomes: integrating structure and function. Annu. Rev. Genet. 33, 603-754. doi: 10.1146/annurev.genet.33.1.603