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DNA Methylation and the Formation of Heterochromatin in Neurospora Crassa

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DNA Methylation and the Formation of Heterochromatin in Neurospora Crassa Heredity (2010) 105, 38–44 & 2010 Macmillan Publishers Limited All rights reserved 0018-067X/10 $32.00 www.nature.com/hdy REVIEW DNA methylation and the formation of heterochromatin in Neurospora crassa MR Rountree and EU Selker Institute of Molecular Biology, University of Oregon, Eugene, OR, USA Studies of the control and function of DNA methylation and recruits the DNA methyltransferase, DIM-2. Although in Neurospora crassa have led to a greater understand- HP1 links H3K9me3 to DNA methylation, it also serves ing of heterochromatin formation. DNA methylation in to recruit the DNA methylation modifier complex to Neurospora is dependent on trimethylation of histone the edges of heterochromatin regions, where it serves to H3 lysine 9 (H3K9me3) by the histone methyltransferase, limit the spreading of the heterochromatin by countering DIM-5. The linkage between these two methyl marks H3K9me3. is facilitated by heterochromatin protein 1 (HP1), which Heredity (2010) 105, 38–44; doi:10.1038/hdy.2010.44; serves as an adapter protein. HP1 binds to the H3K9me3 published online 21 April 2010 Keywords: heterochromatin; DNA methylation; histone methylation; RIP; Neurospora Introduction The use of simple model organisms, such as yeasts, filamentous fungi, flies, and Arabidopsis, has greatly Constitutive heterochromatin, the densely staining frac- aided our understanding of chromatin modifications and tion of the eukaryotic genome, has been historically will continue to be invaluable in deciphering the regarded as an unimportant component of the genome. chromatin modification ‘code’. However, some powerful Compared with euchromatin, the fraction of the genome model systems lack chromatin modifications that are containing most of the genes, heterochromatin is present in higher eukaryotes, such as DNA methylation. regarded as a more ‘closed’ or ‘condensed’ chromatin Neurospora crassa is the simplest model organism to sport state, which is refractory to DNA-based processes such most of the chromatin modifications seen in higher as recombination and transcription. Recently, however, eukaryotes and offers many advantages for their study. heterochromatin has attracted attention, in part because Some of the heterochromatin markers, such as DNA it has been implicated in human diseases, most notably methylation, are not essential in Neurospora, facilitating cancer (Sharma et al., 2010). Moreover, there is increasing dissection of the processes involved in the establishment evidence that heterochromatin has roles in normal cells, and maintenance of heterochromatin. for example promoting genome stability by preventing illegitimate recombination between repeats, serving to DNA methylation and repeat-induced point silence invasive elements and participating in centro- mere function (Grewal and Jia, 2007; Peng and Karpen, mutation in Neurospora 2008; Rountree and Selker, 2009). Thus, there is consider- Much of what has been learned about heterochromatin in able interest in how regions of heterochromatin are Neurospora resulted from studies on DNA methylation. formed and maintained. Recent research implicates an Approximately 1.5% of cytosines are methylated in the intricate interplay of covalent modifications of histones Neurospora genome (Selker and Stevens, 1987; Foss et al., and a variety of nuclear proteins that are positively or 1993). None of this DNA methylation has been found in negatively influenced by these modifications. Covalent protein-coding genes; rather, nearly all is found within modifications of histones include methylation, acetyla- transposon relics found in the centromere regions, near tion, phosphorylation, and/or ubiquitination of various the, telomeres and elsewhere. Essentially all of these residues. In addition to histone modifications, in many sequences are relics of a genome defense system called eukaryotes chromatin can be modified by methylation of repeat-induced point mutation (RIP) (Foss et al., 1993; cytosines in the DNA. Modifications of histones and Selker et al., 2003; Lewis et al., 2009). RIP apparently DNA should provide a virtually limitless combination of protects the genome from the assault of invasive DNAs chromatin modifications that could be used for regula- (transposons, retrotransposons, viruses, and so on) tory control. Unfortunately, our understanding of these (Rountree and Selker, 2009). RIP is a potent genome modifications and their interplay is still in its infancy. defense system, leaving duplicated sequences both mutated and methylated. The effectiveness of RIP is illustrated by the fact that no recognizable transposon Correspondence: Dr EU Selker, Institute of Molecular Biology, University is found within the wild-type Neurospora genome of Oregon, Eugene, OR 97403, USA. E-mail: [email protected] (Galagan et al., 2003). Early genetic studies showed that Received 25 January 2010; revised 22 February 2010; accepted 23 RIP senses duplicated sequences and subjects both February 2010; published online 21 April 2010 sequences to numerous polarized transition mutations Heterochromatin formation in Neurospora MR Rountree and EU Selker 39 (G:C to A:T) in the stage of the life cycle between (HP1) and DNA methylation (Bhaumik et al., 2007). To fertilization and nuclear fusion (Selker et al., 1987; Selker achieve a more thorough understanding of the relation- and Garrett, 1988). Up to B30% of the G:C pairs of ship between such heterochromatin markers in Neuro- duplicated sequences are mutated in a single passage spora, Lewis et al. (2009) used a ChIP-chip approach to through the sexual cycle (Cambareri et al., 1989; Cambar- generate a high-resolution map of these heterochromatin eri et al., 1991). Although the mechanism of RIP remains to markers along N. crassa Linkage Group VII. This analysis be elucidated, one of Neurospora’s two putative DNA demonstrated that DNA methylation, H3K9me3, and methyltransferases (DMT), RIP defective (RID), is essen- HP1 are nearly perfectly co-localized at 44 discrete tial for the process (Table 1) (Freitag et al., 2002). Sequences heterochromatic domains on this chromosome and altered by RIP are typically methylated at the remaining showed that they do not overlap with H3K4me2, a mark cytosines and this methylation is not restricted to of euchromatin (Lewis et al., 2009). All 44 of these symmetrical sequences (for example, CpG), unlike the domains appear to be relics of RIP, consistent with earlier case of DNA methylation in most vertebrate cells (Selker studies showing that virtually all DNA methylation is and Stevens, 1985). Indeed, it appears that any cytosine associated with RIP’d sequences in Neurospora (Selker residue in a methylated region can be modified and this et al., 2003; Lewis et al., 2009). methylation is typically dense but heterogeneous within a population of nuclei (Selker et al., 1993). Importantly, the DNA methylation does not depend on the sequence Establishment of heterochromatin domains duplication that originally triggered RIP and is relatively In a number of organisms, most notably Schizosacchar- independent of chromosomal position (Selker, 2004). omyces pombe (Cam and Grewal, 2004; Allshire and Treating Neurospora with the histone deacetylase Selker, 2007), RNAi-dependent mechanisms have been inhibitor, Trichostatin-A, affects DNA methylation implicated in the establishment of heterochromatin. In (Selker, 1998). Although this observation was the first contrast, known elements of Neurospora’s RNAi indication that DNA methylation is closely linked to machinery (two dicer proteins, three RNA-dependent histone modifications in this organism, genetic studies RNA polymerases, and two argonaut proteins) are not have been most important in defining a sequence of required for the initiation or maintenance of heterochro- chromatin events that lead to DNA methylation. Two matin (Freitag et al., 2004a). mutants defective in DNA methylation (dim), dim-2 and dim-5, Methylation is at the core of heterochromatin forma- completely abolish DNA methylation in vegetative tissue tion in Neurospora as both dim-2 and dim-5 encode were most informative (Foss et al., 1993; Tamaru and Selker, methyltransferases, the former for DNA methylation and 2001). Unlike DNA methylation patterns in animals and the latter for H3K9 methylation. We will use a bottom up plants, which are established by multiple DMTs in different approach, starting with the DNA sequence characteris- pathways, one DMT, encoded by the dim-2 gene, is tics that trigger heterochromatin formation, to discuss responsible for all DNA methylation found in vegetative what has been learned and what remains to be tissue of Neurospora (Table 1) (Kouzminova and Selker, discovered about how heterochromatin domains are 2001). Although the role of dim-2 in DNA methylation was established and maintained in this relatively simple obvious, the role of dim-5, which encodes a histone organism. methyltransferase, was less so, but provided a concrete link between histone modification and DNA methylation (Table 1) (Tamaru and Selker, 2001). The identification of RIP creates the signal these and other dim mutants, coupled with proteomic, The majority of sequences altered by RIP trigger de novo bioinformatics, and high-throughput approaches have methylation in vegetative tissue (Singer et al., 1995). This served to unlock the pathway that leads to heterochromatin was first shown by removing the existing methylation, formationinNeurospora. either by treatment with the methylation inhibitor 5- azacytidine or by molecular cloning followed by trans-
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