Repeat elements and the Arabidopsis DNA methylation landscape

Abstract

DNA methylation is an epigenetic mark that has key roles in the control of genome activity in plants and mammals. It is critical for the stable silencing of repeat elements and is also involved in the epigenetic regulation of some genes. Despite similarities in the controlling functions of DNA methylation, its dynamics and deposition patterns differ in several respects between plants and mammals. One of the most striking differences is that plants tend to propagate pre-existing DNA methylation states across generations, whereas mammals re-establish them genome wide at every generation. Here, we review our current understanding of DNA methylation in the flowering plant Arabidopsis. We discuss in particular the role of RNAi in the incremental methylation and silencing of repeat elements over successive generations. We argue that paramutation, an epigenetic phenomenon first described in maize, is an extreme manifestation of this RNAi-dependent pathway. Heredity (2010) 105, 14-23; doi:10.1038/hdy.2010.52; published online 12 May 2010Keywords: DNA methylation; repeat elements; Arabidopsis; RNAi; paramutation Introduction DNA methylation refers to the enzymatic transfer of a methyl group to specific nucleotides within the DNA sequence. In eukaryotes, this modification almost exclusively affects cytosines. Although clearly ancestral, cytosine methylation is not universally present in the eukaryotic tree of life. Thus, the yeasts Saccharomyces cerevisiae and Schizosaccharomyces pombe, as well as the nematode Caenorhabditis elegans have no DNA methyltransferases (DNA MTases;Goll and Bestor, 2005). Furthermore, Drosophila contains a single, enigmatic DNA MTase-like protein (Goll and Bestor, 2005) and it is unclear if this species actually methylates DNA. By contrast, DNA methylation is readily detected in plants and mammals, where it is critical for normal development and genome stability. Although numerous hypotheses have been proposed (Bird, 1995;Yoder et al., 1997;Martienssen, 1998;Regev et al., 1998;Colot and Rossignol, 1999;Suzuki and Bird, 2008), it is still a mystery as to why these organisms cannot dispense with cytosine methylation when many lower eukaryotes can.In plants and mammals, most methylated cytosines are found over repeat elements (Goll and Bestor, 2005;Suzuki and Bird, 2008;Law and Jacobsen, 2010) and loss of this modification is associated with transcriptional reactivation as well as increased mobilization of transposable elements (TEs; Slotkin and Martienssen, 2007). These observations likely reflect the ancestral role of cytosine methylation in the defence against invasive DNA. Methylation of repeat elements is also thought to have been exapted recurrently during eukaryotic evolution to exert other essential functions, notably in the epigenetic regulation of genes. Thus, genomic imprinting, which results in parent-of-origin-dependent expression, may have evolved in plants and mammals from situations in which methylation of repeat elements influences the activity of neighbouring genes (Barlow, 1993;M...

Changes in 24-nt siRNA levels in Arabidopsis hybrids suggest an epigenetic contribution to hybrid vigor

“…For instance, loci with lower than expected siRNA production in the F1 may show increased levels in subsequent generations as reported in interspecies Arabidopsis hybrids (22). These altered siRNA levels could then allow reestablishment of methylation levels at loci altered in the F1 hybrids in a manner similar to that seen in hypo-methylated recombinant lines (23). Furthermore, in generations beyond the F1, an increasing number of loci may show "balancing" interactions between parental epialleles, leading to loss of epiallelic diversity.…”

“…If it were possible to trace parental contributions at each 24-nt siRNA locus, it might show that such transinteractions could be one reason for the reduced 24-nt siRNA levels observed in the hybrids. Variations in the chromatin states, sequence composition, abundance of siRNA, and/or the feedback between methylation and siRNA production (23), may all account for why certain loci retain parental contributions, whereas others exhibit transeffects.…”

Targeting of Arabidopsis KNL2 to Centromeres Depends on the Conserved CENPC-k Motif in Its C Terminus

“…Incorporation of cenH3 is anticorrelated with other epigenetic marks such as DNA methylation and some histone modifications (Zhang et al, 2008). It was shown for Arabidopsis that the centromeric transcripts and corresponding small interfering RNAs might be involved in methylation of centromeric/pericentromeric DNA (Teixeira and Colot, 2010). Single-stranded centromeric transcripts can bind centromeric chromatin and may serve as a structural template to help in recruiting kinetochore proteins (Wong et al, 2007;Du et al, 2010).…”

required to maintain repression2 Is a Novel Protein That Facilitates Locus-Specific Paramutation in Maize

“…It has been proposed that small RNAs (sRNAs) acting in an RNAdirected DNA methylation (RdDM) pathway (Haag and Pikaard, 2011;Zhang and Zhu, 2011) mediate the trans-homolog interactions that typify paramutation behaviors (Chandler, 2010;Teixeira and Colot, 2010). This model is attractive because both RNA polymerase IV (Pol IV) catalytic subunits (RPD1 and RPD2a) and a putative RNA-dependent RNA polymerase (RDR2), presumably orthologous to the Arabidopsis thaliana RdDM-related proteins NUCLEAR RNA POLYMERASE D1 (NRPD1), NRPD2, and RNA-DEPENDENT RNA POLYMERASE2 (RDR2), respectively, have been identified by mutations affecting paramutation at pl1 (Dorweiler et al, 2000;Hollick et al, 2005;Alleman et al, 2006;Woodhouse et al, 2006;Erhard et al, 2009;Stonaker et al, 2009).…”