Epigenetic Reprogramming and Small RNA Silencing of Transposable Elements in Pollen

Cell

Volumn 136, Issue 3, 2009, Pages 461-472

  Slotkin, R Keith ^a   Vaughn, Matthew ^a   Borges, Filipe ^b   Tanurdžić, Miloš ^a   Becker, Jörg D ^b   Feijó, José A ^b,c   Martienssen, Robert A ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^c UNIVERSITY OF LISBON   (Portugal)

Author keywords

DEVBIO; DNA; RNA

Indexed keywords

DNA; SMALL INTERFERING RNA;

ARTICLE; DNA METHYLATION; EPIGENETICS; GAMETE; GENE EXPRESSION; GENE SILENCING; GENE TARGETING; PRIORITY JOURNAL; TRANSPOSON;

ARABIDOPSIS; HEXAPODA;

EID: 59349118366     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2008.12.038     Document Type: Article

References (60)

1. Aravin A.A., Hannon G.J., and Brennecke J. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318 (2007) 761-764
2. Becker J.D., and Feijo J.A. How many genes are needed to make a pollen tube? Lessons from transcriptomics. Ann. Bot. (Lond.) 100 (2007) 1117-1123
3. Becker J.D., Boavida L.C., Carneiro J., Haury M., and Feijo J.A. Transcriptional profiling of Arabidopsis tissues reveals the unique characteristics of the pollen transcriptome. Plant Physiol. 133 (2003) 713-725
4. Borges F., Gomes G., Gardner R., Moreno N., McCormick S., Feijo J.A., and Becker J.D. Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol. 148 (2008) 1168-1181
5. Brennecke J., Aravin A.A., Stark A., Dus M., Kellis M., Sachidanandam R., and Hannon G.J. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128 (2007) 1089-1103
6. Brennecke J., Malone C.D., Aravin A.A., Sachidanandam R., Stark A., and Hannon G.J. An epigenetic role for maternally inherited piRNAs in transposon silencing. Science 322 (2008) 1387-1392
7. Brower-Toland B., Findley S.D., Jiang L., Liu L., Yin H., Dus M., Zhou P., Elgin S.C., and Lin H. Drosophila PIWI associates with chromatin and interacts directly with HP1a. Genes Dev. 21 (2007) 2300-2311
8. Calvi B.R., and Gelbart W.M. The basis for germline specificity of the hobo transposable element in Drosophila melanogaster. EMBO J. 13 (1994) 1636-1644
9. Carmell M.A., Girard A., van de Kant H.J., Bourc'his D., Bestor T.H., de Rooij D.G., and Hannon G.J. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev. Cell 12 (2007) 503-514
10. Casa A.M., Nagel A., and Wessler S.R. MITE display. Methods Mol. Biol. 260 (2004) 175-188
11. Chambeyron S., Popkova A., Payen-Groschene G., Brun C., Laouini D., Pelisson A., and Bucheton A. piRNA-mediated nuclear accumulation of retrotransposon transcripts in the Drosophila female germline. Proc. Natl. Acad. Sci. USA 105 (2008) 14964-14969
12. Dunoyer P., Himber C., and Voinnet O. DICER-LIKE 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal. Nat. Genet. 37 (2005) 1356-1360
13. Dupressoir A., and Heidmann T. Germ line-specific expression of intracisternal A-particle retrotransposons in transgenic mice. Mol. Cell. Biol. 16 (1996) 4495-4503
14. Eady C., Lindsey K., and Twell D. The Significance of microspore division and division symmetry for vegetative cell-specific transcription and generative cell differentiation. Plant Cell 7 (1995) 65-74
15. Engel M.L., Holmes-Davis R., and McCormick S. Green sperm. Identification of male gamete promoters in Arabidopsis. Plant Physiol. 138 (2005) 2124-2133
16. Friedman W.E. Expression of the cell cycle in sperm of Arabidopsis: implications for understanding patterns of gametogenesis and fertilization in plants and other eukaryotes. Development 126 (1999) 1065-1075
17. Galli M., Theriault A., Liu D., and Crawford N.M. Expression of the Arabidopsis transposable element Tag1 is targeted to developing gametophytes. Genetics 165 (2003) 2093-2105
18. Gendrel A.V., Lippman Z., Yordan C., Colot V., and Martienssen R.A. Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297 (2002) 1871-1873
19. Goldberg R.B., Beals T.P., and Sanders P.M. Anther development: basic principles and practical applications. Plant Cell 5 (1993) 1217-1229
20. Grivna S.T., Beyret E., Wang Z., and Lin H. A novel class of small RNAs in mouse spermatogenic cells. Genes Dev. 20 (2006) 1709-1714
21. Gruntman E., Qi Y., Slotkin R.K., Roeder T., Martienssen R., and Sachidanandam R. Kismeth: Analyzer of plant methylation states though bisulfite sequencing. BMC Bioinformatics 9 (2008) 371
22. Hamilton A., Voinnet O., Chappell L., and Baulcombe D. Two classes of short interfering RNA in RNA silencing. EMBO J. 21 (2002) 4671-4679
23. Himber C., Dunoyer P., Moissiard G., Ritzenthaler C., and Voinnet O. Transitivity-dependent and -independent cell-to-cell movement of RNA silencing. EMBO J. 22 (2003) 4523-4533
24. Honys D., and Twell D. Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol. 5 (2004) R85
25. Ingouff M., Hamamura Y., Gourgues M., Higashiyama T., and Berger F. Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr. Biol. 17 (2007) 1032-1037
26. Janousek B., Zluvova J., and Vyskot B. Histone H4 acetylation and DNA methylation dynamics during pollen development. Protoplasma 211 (2000) 116-122
27. Johnson-Brousseau S.A., and McCormick S. A compendium of methods useful for characterizing Arabidopsis pollen mutants and gametophytically-expressed genes. Plant J. 39 (2004) 761-775
28. Jullien P.E., Mosquna A., Ingouff M., Sakata T., Ohad N., and Berger F. Retinoblastoma and its binding partner MSI1 control imprinting in Arabidopsis. PLoS Biol. 6 (2008) e194
29. Kasschau K.D., Fahlgren N., Chapman E.J., Sullivan C.M., Cumbie J.S., Givan S.A., and Carrington J.C. Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biol. 5 (2007) e57
30. Kikuchi K., Terauchi K., Wada M., and Hirano H. The plant MITE mPing is mobilized in anther culture. Nature 421 (2003) 167-170
31. Kloc A., Zaratiegui M., Nora E., and Martienssen R. RNA interference guides histone modification during the S phase of chromosomal replication. Curr. Biol. 18 (2008) 490-495
32. Lau N.C., Seto A.G., Kim J., Kuramochi-Miyagawa S., Nakano T., Bartel D.P., and Kingston R.E. Characterization of the piRNA complex from rat testes. Science 313 (2006) 363-367
33. Lippman Z., Gendrel A.V., Black M., Vaughn M.W., Dedhia N., McCombie W.R., Lavine K., Mittal V., May B., Kasschau K.D., et al. Role of transposable elements in heterochromatin and epigenetic control. Nature 430 (2004) 471-476
34. Lippman Z., May B., Yordan C., Singer T., and Martienssen R. Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification. PLoS Biol. 1 (2003) E67
35. Lisch D. Mutator transposons. Trends Plant Sci. 7 (2002) 498-504
36. May B.P., Lippman Z.B., Fang Y., Spector D.L., and Martienssen R.A. Differential regulation of strand-specific transcripts from Arabidopsis centromeric satellite repeats. PLoS Genet. 1 (2005) e79
37. McCormick S. Male Gametophyte Development. Plant Cell 5 (1993) 1265-1275
38. McCormick S. Control of male gametophyte development. Plant Cell 16 Suppl (2004) S142-S153
39. Meyer E., and Chalker D.L. Epigenetics of Ciliates. In: Allis D.C., Jenuwein T., Reinberg D., and Caparros M.-L. (Eds). Epigenetics (2007), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 127-150
40. Miura A., Yonebayashi S., Watanabe K., Toyama T., Shimada H., and Kakutani T. Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411 (2001) 212-214
41. Nobuta K., Venu R.C., Lu C., Belo A., Vemaraju K., Kulkarni K., Wang W., Pillay M., Green P.J., Wang G.L., and Meyers B.C. An expression atlas of rice mRNAs and small RNAs. Nat. Biotechnol. 25 (2007) 473-477
42. Okada T., Singh M.B., and Bhalla P.L. Histone H3 variants in male gametic cells of lily and H3 methylation in mature pollen. Plant Mol. Biol. 62 (2006) 503-512
43. Ostertag E.M., DeBerardinis R.J., Goodier J.L., Zhang Y., Yang N., Gerton G.L., and Kazazian Jr. H.H. A mouse model of human L1 retrotransposition. Nat. Genet. 32 (2002) 655-660
44. Pasyukova E., Nuzhdin S., Li W., and Flavell A.J. Germ line transposition of the copia retrotransposon in Drosophila melanogaster is restricted to males by tissue-specific control of copia RNA levels. Mol. Gen. Genet. 255 (1997) 115-124
45. Pelisson A., Song S.U., Prud'homme N., Smith P.A., Bucheton A., and Corces V.G. Gypsy transposition correlates with the production of a retroviral envelope-like protein under the tissue-specific control of the Drosophila flamenco gene. EMBO J. 13 (1994) 4401-4411
46. Pina C., Pinto F., Feijo J.A., and Becker J.D. Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol. 138 (2005) 744-756
47. Rabinowicz P.D., Citek R., Budiman M.A., Nunberg A., Bedell J.A., Lakey N., O'Shaughnessy A.L., Nascimento L.U., McCombie W.R., and Martienssen R.A. Differential methylation of genes and repeats in land plants. Genome Res. 15 (2005) 1431-1440
48. Raizada M.N., Benito M.I., and Walbot V. The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs. Plant J. 25 (2001) 79-91
49. Sarot E., Payen-Groschene G., Bucheton A., and Pelisson A. Evidence for a piwi-dependent RNA silencing of the gypsy endogenous retrovirus by the Drosophila melanogaster flamenco gene. Genetics 166 (2004) 1313-1321
50. Schmid M., Davison T.S., Henz S.R., Pape U.J., Demar M., Vingron M., Scholkopf B., Weigel D., and Lohmann J.U. A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37 (2005) 501-506
51. Singer T., Yordan C., and Martienssen R.A. Robertson's Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1). Genes Dev. 15 (2001) 591-602
52. Smyth D.R., Bowman J.L., and Meyerowitz E.M. Early flower development in Arabidopsis. Plant Cell 2 (1990) 755-767
53. Sundaresan V., Springer P., Volpe T., Haward S., Jones J.D., Dean C., Ma H., and Martienssen R. Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev. 9 (1995) 1797-1810
54. Talbert P.B., Masuelli R., Tyagi A.P., Comai L., and Henikoff S. Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell 14 (2002) 1053-1066
55. Tanurdzic M., Vaughn M.W., Jiang H., Lee T.-J., Slotkin R.K., Sosinski B., Thompson W.F., Doerge R.W., and Martienssen R.A. Epigenomic consequences of immortalized plant cell suspension culture. PLoS Biol. 6 (2008) e302
56. Ueda K., and Tanaka I. The appearance of male gamete-specific histones gH2B and gH3 during pollen development in Lilium longiflorum. Dev. Biol. 169 (1995) 210-217
57. Vongs A., Kakutani T., Martienssen R.A., and Richards E.J. Arabidopsis thaliana DNA methylation mutants. Science 260 (1993) 1926-1928
58. Wang Y., Zhang W.Z., Song L.F., Zou J.J., Su Z., and Wu W.H. Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol. 148 (2008) 1201-1211
59. Yu S., Hu S., and Zhu C. Ultrastructure of sperm cells of the male germ unit in pollen tubes of Nicotiana tabacum. Protoplasma 152 (1989) 29-36
60. Zheng X., Pontes O., Zhu J., Miki D., Zhang F., Li W.X., Iida K., Kapoor A., Pikaard C.S., and Zhu J.K. ROS3 is an RNA-binding protein required for DNA demethylation in Arabidopsis. Nature 455 (2008) 1259-1262