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doi: 10.1111/j.1440-169X.2011.01309.x
Review Article
Transposons are highly conserved in plants and have created a symbiotic relationship with the host genome. An important factor of the successful communication between transposons and host plants is epigenetic modications including DNA methylation and the modications of the histone tail. In plants, small interfering RNAs (siRNAs) are responsible for RNA-directed DNA methylation (RdDM) that suppresses transposon activities. Although most transposons are silent in their host plants, certain genomic shocks, such as an environmental stress or a hybridization event, might trigger transposon activation. Further, since transposons can affect the regulation mechanisms of host genes, it is possible that transposons have co-evolved as an important mechanism for plant development and adaptation. Recent new ndings reveal that siRNAs control not only transcriptional activation, but also suppress transgenerational transposition of mobile elements making siRNAs critically important towards maintaining genome stability. Together these data suggest host-mediated siRNA regulation of transposons appears to have been adapted for controlling essential systems of plant development, morphogenesis, and reproduction. Key words: epigenetics, evolution, plants, siRNAs, stress, transposon.
Introduction
Transposons of various classes, including both DNA transposons and retrotransposons, are abundant in plant genomes (Feschotte et al. 2002). The copy number of transposons inuences the genome size. For example, a massive number of transposons make up more than 85% of the approximately 2300 MB maize genome (Wilson et al. 2009). The most abundant families of transposons in higher plants are long terminal repeat (LTR)-type retrotransposons (Kumar & Bennetzen 1999). In contrast to the cut and paste mechanism of DNA transposons use for transposition, retrotransposons transpose via an RNA intermediate that is reverse transcribed into extrachromosomal DNA and inserted into the genome. In addition to LTR-type families, Non-LTR retrotransposons were identied as ubiquitous components of nuclear genomes in many species. Non-LTR retrotransposons are divided into long interspersed nuclear elements (LINEs) and short interspersed nuclear elements (SINEs). LINEs are able
*Author to whom all correspondence should be addressed. Email: hito@mail.sci.hokudai.ac.jp Received 18 August 2011; revised 28 September 2011; accepted 28 September 2011. 2011 The Author Development, Growth & Differentiation 2011 Japanese Society of Developmental Biologists
to transpose autonomously while non-autonomous SINEs depend on the reverse transcription machinery of other retrotransposons. Although a large number of retrotransposons are conserved in intergenic regions (SanMiguel et al. 1996; Kumar & Bennetzen 1999) several families are conserved in gene rich regions (Kumar 1996; Kumar & Bennetzen 1999) possibly indicating an insertion preference of the retrotransposon or an evolutionary advantage at integration sites. This is surprising since active transposons are highly mutagenic and not only change gene expression, but also cause chromosome breakage and recombination leading to genomic instability. Some insertions, however, may favorably affect gene splicing or act as an enhancer or a promoter to nearby genes (Girard & Freeling 1999). Despite the potential to either harm or benet the host genome, in nature most transposons are silent and rarely transpose due to the point mutations, deletions, or recombination that abolish their activities. In the event that full-length autonomous transposons are intact and can potentially transpose, host plants have evolved various types of epigenetic regulation to defend from transposition. DNA methylation is one regulatory mechanism that suppresses transcriptional activation, which is established by the RNA directed DNA methylation (RdDM) pathway guided by small RNAs (Lister et al. 2008). Indeed, about 37% of the methylated loci were associated with siRNA clusters
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(Zhang et al. 2006) in the Arabidopsis genome. Recently, siRNAs have also been revealed to play important roles for transposon inactivation, not only at the transcriptional level, but also at the transpositional level. The recent discoveries of plant-specic transposon regulation involving small RNAs in plants are reviewed in this article.
et al. 2004). The inserted transposon also makes FLC subject to repressive chromatin modications mediated by siRNAs generated from unlinked, homologous transposable elements elsewhere in the genome. Another example is the imprinted gene FLOWERING WAGENINGEN (FWA) that is specically expressed in the endosperm but is silent in vegetative tissues of A. thaliana. The tissue-specic imprinted expression of FWA depends on DNA demethylation of the FWA promoter, which is comprised of two direct repeats containing a sequence related to a short interspersed nuclear (SINE) retrotransposon (Kakutani et al. 2007). If the FWA promoter is methylated, localized heterochromatin is established leading to transcriptional silencing and the biogenesis of small interfering RNAs from these SINE-related tandem repeats (Lippman et al. 2004; Chan et al. 2006). Similar to the inserted transposon of FLC described above, these siRNA can also target the RdDM activity to establish de novo silencing at unmethylated FWA transgenes (Cao & Jacobsen 2002; Chan et al. 2004).
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than 1% of the Arabidopsis genome, including repetitive elements and transposons (Zhang et al. 2007; Mosher et al. 2008) can accumulate in specic tissues, such as the developing endosperm (Mosher et al. 2009). Interestingly, the expression of p4-siRNAs in developing endosperm specically originates from maternal chromosomes indicating genome imprinting (Mosher et al. 2009). The siRNAs produced in the endosperm have been reported to move into the egg cell to guide DNA methylation, seemingly to reinforce silencing in the germ cells (Feng et al. 2010). While this mechanism likely functions in suppressing transposon activity in the embryo, the derepression of transposons is not considered harmful since the endosperm is not inherited by the next generation. Another important role of silencing in the control of female gamete formation was revealed by the action of ARGONAUTE 9 (AGO9) in Arabidopsis. AGO9 is highly expressed in ovules and anthers of Arabidopsis (Olmedo-Monl et al. 2010). Interestingly, AGO9 expresses in cytoplasmic foci of somatic companion cells both outside and before differentiation of the gamete lineage (Olmedo-Monl et al. 2010). In ago9 mutants, some transposons are activated indicating that AGO9 is necessary for transposon silencing in the ovule and an endogenous 24 nt siRNA biosynthetic pathway may play an important role for AGO9-dependent transposon suppression. In this model, epidermal cells in the young ovule primordium produce p4-siRNAs that are templates for AGO9 to generate siRNA signals. These signals may be channeled into a secondary siRNA pathway involving RDR6 and SGS3 to move the siRNA to sub-epidermal nucellar cells to inactivate transposons. Additionally, this function restricts the surrounding cells from ectopic development of a gamete lineage (Olmedo-Monl et al. 2010). Thus, AGO9 controls gametic cell commitment by acting in a non-cellautonomous small RNA-dependent pathway in the developing ovule where transposon regulation remains of central importance. In Arabidopsis, epigenetic reprogramming also plays an important role for the transposon silencing in pollen (Slotkin et al. 2009). Many of the genes involved in siRNA biogenesis and silencing are either not expressed or expressed at low levels in pollen; however, the chromatin remodeling ATPase DECREASE IN DNA METHYLATION 1 (DDM1) (Brzeski & Jerzmanowski 2003) accumulates specically in sperm cells, but not in the vegetative nucleus of mature pollen (Slotkin et al. 2009). In wild type vegetative nuclei, the reduction of DDM1 correlates with DNA demethylation and transposon reactivation. Much like the endosperm, transposon activation in pollen vegetative nuclei does not impair tness of the next generation since the veg-
etative nucleus does not contribute DNA to the fertilized embryo or endosperm. It has been postulated that the benet of deregulation within the vegetative nucleus occurs when small RNA are transported from the pollen grain cytoplasm to within the sperm cells resulting in siRNA accumulation to reinforce silencing of transposons in the gametes (Slotkin et al. 2009).
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impaired in the siRNA biogenesis (Ito et al. 2011). Importantly, no transposition was observed in vegetative tissues of either the wild type or the siRNA biogenesis mutant, however, a high frequency of new insertions was observed in the progeny of stressed plants decient in siRNAs (Ito et al. 2011). Analysis of the insertion patterns revealed that the transgenerational transposition occurred during ower development, with evidence for mobilization before gametogenesis, demonstrating that siRNA-mediated transpositional suppression is important not only in reproductive cells, but also in the somatic tissue that will produce the gametes (Ito et al. 2011). Although the exact spatial and temporal regulation of ONSEN transposition in ower requires further analysis, it is likely that siRNA inhibition of transposition occurs in a developmental or tissue-specic manner (Fig. 1).
(Perez-Hormaeche et al. 2008). In one study, the LTR retrotransposon Tnt1 in tobacco (Nicotiana tabacum) was introduced into Arabidopsis. As a result, 24 nt siRNAs were produced that targeted the promoter in the LTR region to establish non-CG methylation and transcriptional silencing. The suppression of Tnt1 was dependent on copy number given that the stable reversion of silencing was obtained when the number of Tnt1 elements was reduced by genetic segregation to two copies (Perez-Hormaeche et al. 2008). This suggests that the maintenance of transposon silencing established by a copy number threshold can be released in some circumstances. A natural situation in which transposon copy number variation may occur is when newly formed interspecic hybrids or resynthesized allopolyploids are produced, which can cause a genomic shock. Such a shock can lead to genome-wide alteration of gene expression, including transposon activation (Ha et al. 2009). The distribution of siRNA in two closely related species, Arabidopsis thaliana and Arabidopsis arenosa, a natural allotetraploid of Arabidopsis suecica, and resynthesized allotetraploid lines derived from A. thaliana and A. arenosa were analyzed (Ha et al. 2009). The
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Fig. 1. A model of double lock regulation in transposon activity by siRNAs in Arabidopsis. Transposon-related RNAs transcribed by Pol IV subsequently produce siRNAs with RDR and DCL proteins. An RNAi pathway degrades the transcription of transposons as indicated by the production of 21 nt siRNA. Binding of 24 nt siRNA to the AGO4-containing RNA induced silencing complex (RISC) targets RNAdirected DNA methylation (RdDM) to the chromatin. RdDM introduces de novo cytosine methylation and suppresses transcription of transposons. Previous observations indicated that siRNA function to regulate transposition of mobile elements in Arabidopsis (Mirouze et al. 2009; Ito et al. 2011), yet it remains unclear if the siRNAs target extrachromosomal DNA for degradation or inhibit integration into the host genome, or some combination therein. 2011 The Author Development, Growth & Differentiation 2011 Japanese Society of Developmental Biologists
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results suggested that small RNAs produced during interspecic hybridization or polyploidization serve as a buffer against the genomic shock occurring in interspecic hybrids and allopolyploids. Among 6000 siRNA-generating transposons in A. thaliana, 5123 (85%) also produced siRNAs in one or more allotetraploids. A. thaliana siRNA populations underwent rapid changes in nascent F1 allotetraploids, but were stably maintained through the seventh generation (F7) indicating that stable inheritance of transposon-associated siRNA maintains chromatin and genome stability. How such stable inheritance might affect genome evolution was also examined in Arabidopsis thaliana and Arabidopsis lyrata, two related species, yet with major transposon families having more copies in A. lyrata (Hollister et al. 2011). The difference indicates that most transposons have either been more active in A. lyrata or that selection against gene expression patterns modied by transposons is more stringent in A. thaliana (Hollister et al. 2011). A comparison of the 24 nt siRNA complement between the two species revealed that siRNA-targeted transposons were associated with reduced gene expression within both species, but also created gene expression differences between the orthologues (Hollister et al. 2011). In addition, A. lyrata transposons were targeted by a lower fraction of uniquely matching siRNAs, which are associated with more effective silencing of the expression. These results indicate that the efcacy of RdDM silencing and transposon proliferation clearly differ between the two species. What remains to be determined is whether this indicates genome evolution requires tolerance to modied gene expression patterns induced by proliferating transposons, or conversely, evolution requires an ability to purge new insertions from the genome, or some combination of these two functions. A locus-specic example of natural variation comes from the analysis of highly abundant 24 nt siRNAs found in the ecotype Ler that could direct RdDM and heterochromatinization towards hobo, Activator, Tam3 (hAT) (Rubin et al. 2001) transposons adjacent to the promoter of FLC (Zhai et al. 2008). Despite the same hAT element in ecotype Columbia (Col) with almost the identical DNA sequence, the low amount of siRNAs detected did not affect FLC activities. A genomewide comparison of Ler and Col small RNAs identied at least 68 loci matched by a signicant level of the 24 nt siRNAs present specically in Ler, but not Col, with nearly half of the loci being related to repeat or transposon sequences. The analysis suggested that the same region could be led to a different epigenetic status because of the difference in their corresponding small RNA abundance and between the two closely
related Arabidopsis ecotypes, supporting the model that small RNA-directed epigenetic differences may exist among natural populations.
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methylation level in LTDT is regulated by Tam3 activity and that at low temperatures when siRNA-mediated methylation might decrease, re-expression of silenced transposons may occur. More direct evidence of siRNA-mediated regulation has come from the ONSEN transposition. ONSEN was activated in heat-stress and transposed to the next generation in a mutant of siRNA biogenesis. It is notable that ONSEN was not activated in the plants treated with DNA methylation inhibitor 5-azacytidine or within ddm1 mutant plants (Ito et al. 2011). Although the activation of ONSEN is likely independent of DNA methylation, siRNA is required for the immobilization. The experiments demonstrated that the heat-induced retrotransposition in the second generation of stressed pol IV mutant had an impact on the transcriptional regulation of endogenous loci harboring new ONSEN insertion. The insertions under heat stress may drive adaptation towards developing new expression variants with ONSEN acting as a heat responsive promoter element at new insertion sites. Also a gene in the Columbia accession harboring a natural insertion of ONSEN was heat activated. To determine the physiological relevance of the activation, heat responsiveness was analyzed on the gene in the Zurich accession where ONSEN is absent at the location. The result showed that heat-induced activation in the Columbia accession was much more pronounced than in the Zurich accession (Ito et al. 2011). Together, these results provide multiple examples of rapid host responses to a range of environmental stresses that can allow transposons to alter genome structure and or gene regulation, thereby inuencing future generations, which is of great importance to further study the connection between the stability of acquired epigenetic states and natural selection.
remove unt variants if adjacent host genes become dysregulated due to transposon-derived siRNAs via the RdDM pathway. How these adaptation forces are balanced in nature remains poorly understood; however, we are now in a better position to reveal the relationship between siRNAs and transposon regulation in plant development and genome evolution.
Acknowledgments
I would like to thank Jon Reinders for reviewing the manuscript. This work was supported by JST, PRESTO, Grant-in-Aid for Scientic Research on Innovative Areas (23119501), Grant-in-Aid for Young Scientists (B) (23770034), and the Akiyama Life Science Foundation.
References
Baroux, C., Raissig, M. T. & Grossniklaus, U. 2011. Epigenetic regulation and reprogramming during gamete formation in plants. Curr. Opin. Genet. Dev. 21, 124133. Boss, P. K., Bastow, R. M., Mylne, J. S. & Dean, C. 2004. Multiple pathways in the decision to ower: enabling, promoting, and resetting. Plant Cell 16(Suppl), S18S31. Brzeski, J. & Jerzmanowski, A. 2003. Decient in DNA methylation 1 (DDM1) denes a novel family of chromatin-remodeling factors. J. Biol. Chem. 278, 823828. Cao, X. & Jacobsen, S. E. 2002. Role of the arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr. Biol. 12, 11381144. Carpenter, R., Martin, C. & Coen, E. S. 1987. Comparison of genetic behavior of the transposable element Tam3 at 2 unlinked pigment loci in Antirrhinum-Majus. Mol. Gen. Genet. 207, 8289. Chan, S. W., Zhang, X., Bernatavichute, Y. V. & Jacobsen, S. E. 2006. Two-step recruitment of RNA-directed DNA methylation to tandem repeats. PLoS Biol. 4, e363. Chan, S. W., Zilberman, D., Xie, Z., Johansen, L. K. & Jacobsen, S. E. 2004. RNA silencing genes control de novo DNA methylation. Science 303, 1336. Dumas, C. & Rogowsky, P. 2008. Fertilization and early seed formation. C. R. Biol. 331, 715725. Feng, S., Jacobsen, S. E. & Reik, W. 2010. Epigenetic reprogramming in plant and animal development. Science 330, 622627. Feschotte, C., Jiang, N. & Wessler, S. R. 2002. Plant transposable elements: where genetics meets genomics. Nat. Rev. Genet. 3, 329341. Gazzani, S., Gendall, A. R., Lister, C. & Dean, C. 2003. Analysis of the molecular basis of owering time variation in Arabidopsis accessions. Plant Physiol. 132, 11071114. Gendrel, A. V., Lippman, Z., Yordan, C., Colot, V. & Martienssen, R. A. 2002. Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297, 18711873. Girard, L. & Freeling, M. 1999. Regulatory changes as a consequence of transposon insertion. Dev. Genet. 25, 291296. Ha, M., Lu, J., Tian, L., Ramachandran, V., Kasschau, K. D., Chapman, E. J., Carrington, J. C., Chen, X., Wang, X. J. & Chen, Z. J. 2009. Small RNAs serve as a genetic buffer
Conclusion
Here, the recent discoveries of plant siRNA and transposon regulations were reviewed. Both transposons and host plants have evolved ingenious strategies for survival. Clearly, transposons have acquired special relationships with host factors to proliferate within host genomes and have greatly affected genome evolution. On the other hand, plants have developed RNA-mediated interference (RNAi) that is a genome-based defense against transposons. The cause and effect of the survival strategies has played a signicant role in shaping epigenetic regulation in plant development, natural variation, and stress responses. Transposons activated under environmental stress affecting neighbor gene expression may be a driving force of adaptation, while simultaneously creating a purging force to
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H. Ito
against genomic shock in Arabidopsis interspecic hybrids and allopolyploids. Proc. Natl Acad. Sci. USA 106, 17835 17840. Hashida, S., Kitamura, K., Mikami, T. & Kishima, Y. 2003. Temperature shift coordinately changes the activity and the methylation state of transposon Tam3 in Antirrhinum majus. Plant Physiol. 132, 12071216. Hashida, S. N., Uchiyama, T., Martin, C., Kishima, Y., Sano, Y. & Mikami, T. 2006. The temperature-dependent change in methylation of the Antirrhinum transposon Tam3 is controlled by the activity of its transposase. Plant Cell 18, 104118. Herr, A. J., Jensen, M. B., Dalmay, T. & Baulcombe, D. C. 2005. RNA polymerase IV directs silencing of endogenous DNA. Science 308, 118120. Hirochika, H., Okamoto, H. & Kakutani, T. 2000. Silencing of retrotransposons in arabidopsis and reactivation by the ddm1 mutation. Plant Cell 12, 357369. Hollister, J. D., Smith, L. M., Guo, Y. L., Ott, F., Weigel, D. & Gaut, B. S. 2011. Transposable elements and small RNAs contribute to gene expression divergence between Arabidopsis thaliana and Arabidopsis lyrata. Proc. Natl Acad. Sci. USA 108, 23222327. Hsieh, L. C., Lin, S. I., Shih, A. C., Chen, J. W., Lin, W. Y., Tseng, C. Y., Li, W. H. & Chiou, T. J. 2009. Uncovering small RNAmediated responses to phosphate deciency in Arabidopsis by deep sequencing. Plant Physiol. 151, 21202132. Ito, H., Gaubert, H., Bucher, E., Mirouze, M., Vaillant, I. & Paszkowski, J. 2011. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472, 115119. Kinoshita, Y., Saze, H., Kinoshita, T., Miura, A., Soppe, W. J., Koornneef, M. & Kakutani, T. 2007. Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. Plant J. 49, 3845. Kanno, T., Huettel, B., Mette, M. F., Aufsatz, W., Jaligot, E., Daxinger, L., Kreil, D. P., Matzke, M. & Matzke, A. J. 2005. Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nat. Genet. 37, 761765. Kato, M., Miura, A., Bender, J., Jacobsen, S. E. & Kakutani, T. 2003. Role of CG and non-CG methylation in immobilization of transposons in Arabidopsis. Curr. Biol. 13, 421426. Kumar, A. 1996. The adventures of the Ty1-copia group of retrotransposons in plants. Trends Genet. 12, 4143. Kumar, A. & Bennetzen, J. L. 1999. Plant retrotransposons. Annu. Rev. Genet. 33, 479532. Law, J. A. & Jacobsen, S. E. 2010. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11, 204220. Lippman, Z., May, B., Yordan, C., Singer, T. & Martienssen, R. 2003. Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modication. PLoS Biol. 1, E67. Lippman, Z., Gendrel, A. V., Black, M., Vaughn, M. W., Dedhia, N., McCombie, W. R., Lavine, K., Mittai, V., May, B., Kasschau, K. D., Carrington, J. C., Doerge, R. W., Colot, V. & Martienssen, R. 2004. Role of transposable elements in heterochromatin and epigenetic control. Nature 430, 471476. Lister, R., OMalley, R. C., Tonti-Filippini, J., Gregory, B. D., Berry, C. C., Millar, A. H. & Ecker, J. R. 2008. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133, 523536. Liu, J., He, Y., Amasino, R. & Chen, X. 2004. siRNAs targeting an intronic transposon in the regulation of natural owering behavior in Arabidopsis. Genes Dev. 18, 28732878.
Matzke, M. A. & Birchler, J. A. 2005. RNAi-mediated pathways in the nucleus. Nat. Rev. Genet. 6, 2435. Matzke, M., Aufsatz, W., Kanno, T., Daxinger, L., Papp, I., Mette, M. F. & Matzke, A. J. 2004. Genetic analysis of RNA-mediated transcriptional gene silencing. Biochim. Biophys. Acta 1677, 129141. Michaels, S. D., He, Y. H., Scortecci, K. C. & Amasino, R. M. 2003. Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual owering behavior in Arabidopsis. Proc. Natl Acad. Sci. USA 100, 1010210107. Mirouze, M., Reinders, J., Bucher, E., Nishimura, T., Schneeberger, K., Ossowski, S., Cao, J., Weigel, D., Paszkowski, J. & Mathieu, O. 2009. Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461, 427430. Miura, A., Yonebayashi, S., Watanabe, K., Shimada, H. & Kakutani, T. 2001. Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411, 212214. Mosher, R. A. & Melnyk, C. W. 2010. siRNAs and DNA methylation: seedy epigenetics. Trends Plant Sci. 15, 204210. Mosher, R. A., Schwach, F., Studholme, D. & Baulcombe, D. C. 2008. PolIVb inuences RNA-directed DNA methylation independently of its role in siRNA biogenesis. Proc. Natl Acad. Sci. USA 105, 31453150. Mosher, R. A., Melnyk, C. W., Kelly, K. A., Dunn, R. M., Studholme, D. J. & Baulcombe, D. C. 2009. Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis. Nature 460, 283286. Olmedo-Monl, V., Duran-Figueroa, N., Arteaga-Vazquez, M., Demesa-Arevalo, E., Autran, D., Grimanelli, D., Slotkin, R. K., Martienssen, R. A. & Vielle-Calzada, J. P. 2010. Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464, 628632. Onodera, Y., Haag, J. R., Ream, T., Costa Nunes, P., Pontes, O. & Pikaard, C. S. 2005. Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120, 613622. Perez-Hormaeche, J., Potet, F., Beauclair, L., Le Massin, I., Courtial, B., Bouche, N. & Lucas, H. 2008. Invasion of the Arabidopsis genome by the tobacco retrotransposon Tnt1 is controlled by reversible transcriptional gene silencing. Plant Physiol. 147, 12641278. Pontier, D., Yahubyan, G., Vega, D., Bulski, A., Saez-Vasquez, J., Hakimi, M. A., Lerbs-Mache, S., Colot, V. & Lagrange, T. 2005. Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis. Genes Dev. 19, 20302040. Qi, Y., He, X., Wang, X. J., Kohany, O., Jurka, J. & Hannon, G. J. 2006. Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature 443, 10081012. Ream, T. S., Haag, J. R., Wierzbicki, A. T., Nicora, C. D., Norbeck, A. D., Zhu, J. K., Hagen, G., Guilfoyle, T. J., Pasa-Tolic, L. & Pikaard, C. S. 2009. Subunit compositions of the RNA-silencing enzymes Pol IV and Pol V reveal their origins as specialized forms of RNA polymerase II. Mol. Cell 33, 192203. Ronemus, M. J., Galbiati, M., Ticknor, C., Chen, J. & Dellaporta, S. L. 1996. Demethylation-induced developmental pleiotropy in Arabidopsis. Science 273, 654657. Rubin, E., Lithwick, G. & Levy, A. A. 2001. Structure and evolution of the hAT transposon superfamily. Genetics 158, 949 957.
2011 The Author Development, Growth & Differentiation 2011 Japanese Society of Developmental Biologists
107
Rudall, P. J. 2006. How many nuclei make an embryo sac in owering plants? Bioessays 28, 10671071. Rudall, P. J. & Bateman, R. M. 2007. Developmental bases for key innovations in the seed-plant microgametophyte. Trends Plant Sci. 12, 317326. SanMiguel, P., Tikhonov, A., Jin, Y. K., Motchoulskaia, N., Zakharov, D., Melake-Berhan, A., Springer, P.S., Edwards, K. J., Lee, M., Avramova, Z. & Bennetzen, J. L. 1996. Nested retrotransposons in the intergenic regions of the maize genome. Science 274, 765768. Schnable, P. S., Ware, D., Fulton, R. S., Stein, J. C., Wei, F., Pasternak, S., Liang, C., Zhang, J., Fulton, L., Graves, T. A., Minx, P., Reily, A. D., Courtney, L., Kruchowski, S. S., Tomlinson, C., Strong, C., Delehaunty, K., Fronick, C., Courtney, B., Rock, S. M., Belter, E., Du, F., Kim, K., Abbott, R. M., Cotton, M., Levy, A., Marchetto, P., Ochoa, K., Jackson, S. M., Gillam, B., Chen, W., Yan, L., Higginbotham, J., Cardenas, M., Waligorski, J., Applebaum, E., Phelps, L., Falcone, J., Kanchi, K., Thane, T., Scimone, A., Thane, N., Henke, J., Wang, T., Ruppert, J., Shah, N., Rotter, K., Hodges, J., Ingenthron, E., Cordes, M., Kohlberg, S., Sgro, J., Delgado, B., Mead, K., Chinwalla, A., Leonard, S., Crouse, K., Collura, K., Kudrna, D., Currie, J., He, R., Angelova, A., Rajasekar, S., Mueller, T., Lomeli, R., Scara, G., Ko, A., Delaney, K., Wissotski, M., Lopez, G., Campos, D., Braidotti, M., Ashley, E., Golser, W., Kim, H., Lee, S., Lin, J., Dujmic, Z., Kim, W., Talag, J., Zuccolo, A., Fan, C., Sebastian, A., Kramer, M., Spiegel, L., Nascimento, L., Zutavern, T., Miller, B., Ambroise, C., Muller, S., Spooner, W., Narechania, A., Ren, L., Wei, S., Kumari, S., Faga, B., Levy, M. J., McMahan, L., Van Buren, P., Vaughn, M. W., Ying, K., Yeh, C. T., Emrich, S. J., Jia, Y., Kalyanaraman, A., Hsia, A. P., Barbazuk, W. B., Baucom, R. S., Brutnell, T. P., Carpita, N. C., Chaparro, C., Chia, J. M., Deragon, J. M., Estill, J. C., Fu, Y., Jeddeloh, J. A., Han, Y., Lee, H., Li, P., Lisch, D. R., Liu, S., Liu, Z., Nagel, D. H., McCann, M. C., SanMiguel, P., Myers, A. M., Nettleton, D., Nguyen, J., Penning, B. W., Ponnala, L., Schneider, K. L., Schwartz, D. C., Sharma, A., Soderlund,
C., Springer, N. M., Sun, Q., Wang, H., Waterman, M., Westerman, R., Wolfgruber, T. K., Yang, L., Yu, Y., Zhang, L., Zhou, S., Zhu, Q., Bennetzen, J. L., Dawe, R. K., Jiang, J., Jiang, N., Presting, G. G., Wessler, S. R., Aluru, S., Martienssen, R. A., Clifton, S. W., McCombie, W. R., Wing, R. A. & Wilson, R. K. 2009. The B73 maize genome: complexity, diversity, and dynamics. Science 326, 11121115. Slotkin, R. K., Vaughn, M., Borges, F., Tanurdzic, M., Becker, J. D., Feijo, J. A. & Martienssen, R. A. 2009. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136, 461472. Steward, N., Kusano, T. & Sano, H. 2000. Expression of ZmMET1, a gene encoding a DNA methyltransferase from maize, is associated not only with DNA replication in actively proliferating cells, but also with altered DNA methylation status in cold-stressed quiescent cells. Nucleic Acids Res. 28, 32503259. Tsukahara, S., Kobayashi, A., Kawabe, A., Mathieu, O., Miura, A. & Kakutani, T. 2009. Bursts of retrotransposition reproduced in Arabidopsis. Nature 461, 423426. Walbot, V. & Evans, M. M. S. 2003. Unique features of the plant life cycle and their consequences. Nat. Rev. Genet. 4, 369 379. Zeller, G., Henz, S. R., Widmer, C. K., Sachsenberg, T., Ratsch, G., Weigel, D. & Laubinger, S. 2009. Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. Plant J. 58, 10681082. Zhai, J., Liu, J., Liu, B., Li, P., Meyers, B. C., Chen, X. & Cao, X. 2008. Small RNA-directed epigenetic natural variation in Arabidopsis thaliana. PLoS Genet. 4, e1000056. Zhang, X., Henderson, I. R., Lu, C., Green, P. J. & Jacobsen, S. E. 2007. Role of RNA polymerase IV in plant small RNA metabolism. Proc. Natl Acad. Sci. USA 104, 45364541. Zhang, X., Yazaki, J., Sundaresan, A., Cokus, S., Chan, S. W., Chen, H., Henderson, I. R., Shinn, P., Pellegrini, M., Jacobsen, S. E. & Ecker, J. R. 2006. Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 126, 11891201.
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