Diversification of the core RNA interference machinery in Chlamydomonas reinhardtii and the role of DCL1 in transposon silencing

Genetics

Volumn 179, Issue 1, 2008, Pages 69-81

  Casas Mollano, J Armando ^a   Rohr, Jennifer ^a   Kim, Eun Jeong ^a   Balassa, Eniko ^a   Van Dijk, Karin ^a,b   Cerutti, Heriberto ^a  

^a UNIVERSITY OF NEBRASKA   (United States)

^b CREIGHTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 1 PROTEIN; ARGONAUTE PROTEIN; DICER; DICER LIKE 1; TRANSFER RNA; UNCLASSIFIED DRUG; PRIMER DNA; RIBONUCLEASE; RIBONUCLEASE III;

ARTICLE; CHLAMYDOMONAS REINHARDTII; CONTROLLED STUDY; GENE SILENCING; GENETIC ORGANIZATION; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; POSTTRANSCRIPTIONAL GENE SILENCING; PRIORITY JOURNAL; RETROPOSON; RNA INTERFERENCE; TRANSPOSON; UNINDEXED SEQUENCE; WILD TYPE; ANIMAL; CHROMATIN IMMUNOPRECIPITATION; CLUSTER ANALYSIS; COMPARATIVE STUDY; DNA SEQUENCE; ENZYMOLOGY; GENETIC VARIABILITY; GENETICS; IMMUNOBLOTTING; MOLECULAR GENETICS; PHYLOGENY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA; EMBRYOPHYTA; EUKARYOTA; PROTISTA;

ANIMALS; BASE SEQUENCE; CHLAMYDOMONAS REINHARDTII; CHROMATIN IMMUNOPRECIPITATION; CLUSTER ANALYSIS; DNA PRIMERS; DNA TRANSPOSABLE ELEMENTS; ENDORIBONUCLEASES; IMMUNOBLOTTING; MOLECULAR SEQUENCE DATA; PHYLOGENY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBONUCLEASE III; RNA INTERFERENCE; SEQUENCE ANALYSIS, DNA; VARIATION (GENETICS);

EID: 52049104255     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.107.086546     Document Type: Article

References (92)

1. ALLEN, E., Z. XIE, A. M. GUSTAFSON and J. C. CARRINGTON, 2005 microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121: 207-221.
2. AOKI, K., H. MORIGUCHI, T. YOSHIOKA, K. OKAWA and H. TABARA, 2007 In vitro analyses of the production and activity of secondary small interfering RNAs in C. elegans. EMBO J. 26: 5007-5019.
3. ARAVIN, A. A., G. J. HANNON and J. BRENNECKE, 2007 The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318: 761-764.
4. BARTEL, D. P., 2004 MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 282-297.
5. BAULCOMBE, D., 2004 RNA silencing in plants. Nature 431: 356-363.
6. BAUMBERGER, N., and D. C. BAULCOMBE, 2005 Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits micro-RNAs and short interfering RNAs. Proc. Natl. Acad. Sci. USA 102: 11928-11933.
7. BERNSTEIN, E., A. A. CAUDY, S. M. HAMMOND and G. J. HANNON, 2001 Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409: 363-366.
8. BESTOR, T. H., 2003 Cytosine methylation mediates sexual conflict. Trends Genet. 19: 185-190.
9. BRODERSEN, P., and O. VOINNET, 2006 The diversity of RNA silencing pathways in plants. Trends Genet. 22: 268-280.
10. CARMELL, M. A., Z. XUAN, M. Q. ZHANG and G. J. HANNON, 2002 The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev. 16: 2733-2742.
11. CASAS-MOLLANO, J. A., K. VAN DIJK, J. EISENHART and H. CERUTTI, 2007 SET3p monomethylates histone H3 on lysine 9 and is required for the silencing of tandemly repeated transgenes in Chlamydomonas. Nucleic Acids Res. 35: 939-950.
12. CERUTTI, H., 2003 RNA interference: Traveling in the cell and gaining functions? Trends Genet. 19: 39-46.
13. CERUTTI, H., and J. A. CASAS-MOLLANO, 2006 On the origin and functions of RNA-mediated silencing: from protists to man. Curr. Genet. 50: 81-99.
14. CERUTTI, H., A. M. JOHNSON, N. W. GILLHAM and J. E. BOYNTON, 1997a A eubacterial gene conferring spectinomycin resistance on Chlamydomonas reinhardtii: integration into the nuclear genome and gene expression. Genetics 145: 97-110.
15. CERUTTI, H., A. M. JOHNSON, N. W. GILLHAM and J. E. BOYNTON, 1997b Epigenetic silencing of a foreign gene in nuclear transformants of Chlamydomonas. Plant Cell 9: 925-945.
16. CERUTTI, L., N. MIAN and A. BATEMAN, 2000 Domains in gene silencing and cell differentiation proteins: the novel PAZ domain and redefinition of the Piwi domain. Trends Biochem. Sci. 25: 481-482.
17. CHAN, S. W., D. ZILBERMAN, Z. XIE, L. K. JOHANSEN, J. C. CARRINGTON et al., 2004 RNA silencing genes control de novo DNA methylation. Science 303: 1336.
18. CHAPMAN, E. J., and J. C. CARRINGTON, 2007 Specialization and evolution of endogenous small RNA pathways. Nat. Rev. Genet. 8: 884-896.
19. CHICAS, A., C. COGONI and G. MACINO, 2004 RNAi-dependent and RNAi-independent mechanisms contribute to the silencing of RIPed sequences in Neurospora crassa. Nucleic Acids Res. 32: 4237-4243.
20. COGONI, C., and G. MACINO, 2000 Post-transcriptional gene silencing across kingdoms. Curr. Opin. Genet. Dev. 10: 638-643.
21. DAY, A., and J. D. ROCHAIX, 1991 Structure and inheritance of sense and anti-sense transcripts from a transposon in the green alga Chlamydomonas reinhardtii. J. Mol. Biol. 218: 273-291.
22. DAY, A., M. SCHIRMER-RAHIRE, M. R. KUCHKA, S. P. MAYFIELD and J. D. ROCHAIX, 1988 A transposon with an unusual arrangement of long terminal repeats in the green alga Chlamydomonas reinhardtii. EMBO J. 7: 1917-1927.
23. DING, S.-W., and O. VOINNET, 2007 Antiviral immunity directed by small RNAs. Cell 130: 413-426.
24. DLAKIC, M., 2006 DUF283 domain of Dicer proteins has a double-stranded RNA-binding fold. Bioinformatics 22: 2711-2714.
25. FERRIS, P. J., 1989 Characterization of a Chlamydomonas transposon, Gulliver, resembling those in higher plants. Genetics 122: 363-377.
26. FESCHOTTE, C., N. JIANG and S. R. WESSLER, 2002 Plant transposable elements: where genetics meets genomics. Nat. Rev. Genet. 3: 329-341.
27. FIRE, A., S. XU, M. K. MONTGOMERY, S. A. KOSTAS, S. E. DRIVER et al., 1998 Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806-811.
28. FORTIER, E., and J. M. BELOTE, 2000 Temperature-dependent gene silencing by an expressed inverted repeat in Drosophila. Genesis 26: 240-244.
29. FREITAG, M., D. W. LEE, G. O. KOTHE, R. J. PRATT, R. ARAMAYO et al., 2004 DNA methylation is independent of RNA interference in Neurospora. Science 304: 1939.
30. HALL, J. L., and D. J. L. LUCK, 1995 Basal body-associated DNA: in situ studies in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 92: 5129-5133.
31. HARRIS, E. H., 1989 The Chlamydomonas Sourcebook. Academic Press, San Diego.
32. HINAS, A., J. REIMEGÅRD, E. G. WAGNER, W. NELLEN, V. R. AMBROS et al., 2007 The small RNA repertoire of Dictyostelium discoideum and its regulation by components of the RNAi pathway. Nucleic Acids Res. 35: 6714-6726.
33. IBRAHIM, F., J. ROHR, W-J. JEONG, J. HESSON and H. CERUTTI, 2006 Untemplated oligoadenylation promotes degradation of RISC-cleaved transcripts. Science 314: 1893.
34. JANOWSKI, B. A., S. T. YOUNGER, D. B. HARDY, R. RAM, K. E. HUFFMAN et al., 2007 Activating gene expression in mammalian cells with promoter-targeted duplex RNAs. Nat. Chem. Biol. 3: 166-173.
35. JEONG, B. R., D. WU-SCHARF, C. ZHANG and H. CERUTTI, 2002 Suppressors of transcriptional transgenic silencing in Chlamydomonas are sensitive to DNA-damaging agents and reactivate transposable elements. Proc. Natl. Acad. Sci. USA 99: 1076-1081.
36. JOSSE, T., L. TEYSSET, A. L. TODESCHINI, C. M. SIDOR, D. ANXOLABEHERE et al., 2007 Telomeric trans-silencing: an epigenetic repression combining RNA silencing and heterochromatin formation. PLoS Genet. 3: 1633-1643.
37. KELLER, L. R., J. A. SCHLOSS, C. D. SILFLOW and J. L. ROSENBAUM, 1984 Transcription of α- and β-tubulin genes in vitro in isolated Chlamydomonas reinhardtii nuclei. J. Cell Biol. 98: 1138-1143.
38. KIM, K. S., S. KUSTU and W. INWOOD, 2006 Natural history of transposition in the green alga Chlamydomonas reinhardtii: use of the AMT4 locus as an experimental system. Genetics 173: 2005-2019.
39. KINDLE, K. L., 1990 High-frequency nuclear transformation of Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 87: 1228-1232.
40. KUMAR, S., K. TAMURA and M. NEI, 2004 MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief. Bioinform. 2: 150-163.
41. LEE, S. R., and K. COLLINS, 2006 Two classes of endogenous small RNAs in Tetrahymena thermophila. Genes Dev. 20: 28-33.
42. LI, L. C., S. T. OKINO, H. ZHAO, D. POOKOT, R. F. PLACE et al., 2006 Small dsRNAs induce transcriptional activation in human cells. Proc. Natl. Acad. Sci. USA 103: 17337-17342.
43. LIPPMAN, Z., and R. MARTIENSSEN, 2004 The role of RNA interference in heterochromatic silencing. Nature 431: 364-370.
44. LIPPMAN, Z., B. MAY, C. YORDAN, T. SINGER and R. MARTIENSSEN, 2003 Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification. PLoS Biol. 1: E67.
45. LIU, J., M. A. CARMELL, F. V. RIVAS, C. G. MARSDEN, J. M. THOMSON et al., 2004 Argonaute2 is the catalytic engine of mammalian RNAi. Science 305: 1437-1441.
46. MA, J. B., K. YE and D. J. PATEL, 2004 Structural basis for overhangspecific small interfering RNA recognition by the PAZ domain. Nature 429: 318-322.
47. MARGIS, R., A. F. FUSARO, N. A. SMITH, S. J. CURTIN, J. M. WATSON et al., 2006 The evolution and diversification of Dicers in plants. FEBS Lett. 580: 2442-2450.
48. MATRANGA, C., and P. ZAMORE, 2007 Small silencing RNAs. Curr. Biol. 17: R789-R793.
49. MATZKE, M. A., and J. A. BIRCHLER, 2005 RNAi-mediated pathways in the nucleus. Nat. Rev. Genet. 6: 24-35.
50. MATZKE, M., T. KANNO, B. HUETTEL, L. DAXINGER and A. J. MATZKE, 2007 Targets of RNA-directed DNA methylation. Curr. Opin. Plant Biol. 10: 512-519.
51. MEISTER, G., and T. TUSCHL, 2004 Mechanisms of gene silencing by double-stranded RNA. Nature 431: 343-349.
52. MEISTER, G., M. LANDTHALER, A. PATKANIOWSKA, Y. DORSETT, G. TENG et al., 2004 Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell 15: 185-197.
53. MERCHANT, S. S., S. E. PROCHNIK, O. VALLON, E. H. HARRIS, S. J. KARPOWICZ et al., 2007 The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245-251.
54. MOLNAR, A., F. SCHWACH, D. J. STUDHOLME, E. C. THUENEMANN and D. C. BAULCOMBE, 2007 miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447: 1126-1129.
55. NAKAYASHIKI, H., N. KADOTANI and S. MAYAMA, 2006 Evolution and diversification of RNA silencing proteins in fungi. J. Mol. Evol. 63: 127-135.
56. NOLAN, T., L. BRACCINI, G. AZZALIN, A. DE TONI, G. MACINO et al., 2005 The post-transcriptional gene silencing machinery functions independently of DNA methylation to repress a LINE1-like retrotransposon in Neurospora crassa. Nucleic Acids Res. 33: 1564-1573.
57. OBBARD, D. J., F. M. JIGGINS, D. L. HALLIGAN and T. J. LITTLE, 2006 Natural selection drives extremely rapid evolution in antiviral RNAi genes. Curr. Biol. 16: 580-585.
58. OKAMURA, K., A. ISHIZUKA, H. SIOMI and M. C. SIOMI, 2004 Distinct roles for Argonaute proteins in small RNA-directed RNA cleavage pathways. Genes Dev. 18: 1655-1666.
59. PAK, J., and A. FIRE, 2007 Distinct populations of primary and secondary effectors during RNAi in C. elegans. Science 315: 241-244.
60. PÉREZ-ALEGRE, M., A. DUBUS and E. FERNÁNDEZ, 2005 REM1, a new type of long terminal repeat transposon in Chlamydomonas reinhardtii. Mol. Cell. Biol. 25: 10628-10638.
61. RANGWALA, S. H., and E. J. RICHARDS, 2007 Differential epigenetic regulation within an Arabidopsis retroposon family. Genetics 176: 151-160.
62. RIVAS, F. V., N. H. TOLIA, J. J. SONG, J. P. ARAGON, J. LIU et al., 2005 Purified Argonaute2 and siRNA form recombinant human RISC. Nat. Struct. Mol. Biol. 12: 340-349.
63. ROHR, J., N. SARKAR, S. BALENGER, B. R. JEONG and H. CERUTTI, 2004 Tandem inverted repeat system for selection of effective transgenic RNAi strains in Chlamydomonas. Plant J. 40: 611-621.
64. RUDENKO, G. N., A. ONO and V. WALBOT, 2003 Initiation of silencing of maize MuDR/Mu transposable elements. Plant J. 33: 1013-1025.
65. SAITOU, N., and M. NEI, 1987 The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
66. SAMBROOK, J., and D. W. RUSSELL, 2001 Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
67. SCHNELL, R. A., and P. A. LEFEBVRE, 1993 Isolation of the Chlamydomonas regulatory gene NIT2 by transposon tagging. Genetics 134: 737-747.
68. SCHRODA, M., 2006 RNA silencing in Chlamydomonas: mechanisms and tools. Curr. Genet. 49: 69-84.
69. SIJEN, T., and R. H. PLASTERK, 2003 Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi. Nature 426: 310-314.
70. SIJEN, T., J. FLEENOR, F. SIMMER, K. L. THIJSSEN, S. PARRISH et al., 2001 On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107: 465-476.
71. SLOTKIN, R. K., and R. MARTIENSSEN, 2007 Transposable elements and the epigenetic regulation of the genome. Nat. Rev. Genet. 8: 272-285.
72. SOIFER, H. S., and J. J. ROSSI, 2006 Small interfering RNAs to the rescue: blocking L1 retrotransposition. Nat. Struct. Mol. Biol. 13: 758-759.
73. SONG, J. J., S. K. SMITH, G. J. HANNON and L. JOSHUA-TOR, 2004 Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305: 1434-1437.
74. STANEK, D., and K. M. NEUGEBAUER, 2006 The cajal body: a meeting place for spliceosomal snRNPs in the nuclear maze. Chromosoma 115: 343-354.
75. SZITTYA, G., D. SILHAVY, A. MOLNAR, Z. HAVELDA, A. LOVAS et al., 2003 Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation. EMBO J. 22: 633-640.
76. THOMPSON, J. D., T. J. GIBSON, F. PLEWNIAK, F. JEANMOUGIN and D. G. HIGGINS, 1997 The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876-4882.
77. TRAN, R. K., D. ZILBERMAN, C. DE BUSTOS, R. F. DITT, J. G. HENIKOFF et al., 2005 Chromatin and siRNA pathways cooperate to maintain DNA methylation of small transposable elements in Arabidopsis. Genome Biol. 6: R90.
78. VAN DIJK, K., K. E. MARLEY, B. R. JEONG, J. XU, J. HESSON et al., 2005 Monomethyl histone H3 lysine 4 as an epigenetic mark for silenced euchromatin in Chlamydomonas. Plant Cell 17: 2439-2453.
79. VAN DIJK, K., H. XU and H. CERUTTI, 2006 Epigenetic silencing of transposons in the green alga Chlamydomonas reinhardtii. Nucleic Acids Mol. Biol. 17: 159-178
80. VASUDEVAN, S., Y. TONG and J. A. STEITZ, 2007 Switching from repression to activation: microRNAs can up-regulate translation. Science 318: 1931-1934.
81. VAUCHERET, H., 2006 Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev. 20: 759-771.
82. WANG, S-C., R. A. SCHNELL and P. A. LEFEBVRE, 1998 Isolation and characterization of a new transposable element in Chlamydomonas reinhardtii. Plant Mol. Biol. 38: 681-687.
83. WIENHOLDS, E., and R. H. A. PLASTERK, 2005 MicroRNA function in animal development. FEBS Lett. 579: 5911-5922.
84. WOODHOUSE, M. R., M. FREELING and D. LISCH, 2006 Initiation, establishment, and maintenance of heritable MuDR transposon silencing in maize are mediated by distinct factors. PLoS Biol. 4: e339.
85. XIE, Z., L. K. JOHANSEN, A. M. GUSTAFSON, K. D. KASSCHAU, A. D. LELLIS et al., 2004 Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2: E104.
86. YOSHIKAWA, M., A. PERAGINE, M. Y. PARK and R. S. POETHIG, 2005 A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev. 19: 2164-2175.
87. YUAN, Y-R., Y. PEI, J-B. MA, V. KURYAVYI, M. ZHADINA et al., 2005 Crystal structure of A. aeolicus argonaute, a site-specific DNA-guided endoribonuclease, provides insights into RISC-mediated mRNA cleavage. Mol. Cell 19: 405-419.
88. ZAMBON, R. A., V. N. VAKHARIA and L. P. WU, 2006 RNAi is an antiviral immune response against a dsRNA virus in Drosophila melanogaster. Cell. Microbiol. 8: 880-889.
89. ZAMORE, P. D., and B. HALEY, 2005 Ribo-gnome: the big world of small RNAs. Science 309: 1519-1524.
90. ZHANG, C., D. WU-SCHARF, B. R. JEONG and H. CERUTTI, 2002 A WD40-repeat containing protein, similar to a fungal co-repressor, is required for transcriptional gene silencing in Chlamydomonas. Plant J. 31: 25-36.
91. ZHAO, T., G. LI, S. MI, S. LI, G. J. HANNON et al., 2007 A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev. 21: 1190-1203.
92. ZILBERMAN, D., X. CAO and S. E. JACOBSEN, 2003 Argonaute4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299: 716-719.