Different Domains Control the Localization and Mobility of LIKE HETEROCHROMATIN PROTEIN1 in<i>Arabidopsis</i>Nuclei

Zemach, Assaf; Li, Yan; Ben-Meir, Hagit; Oliva, Moran; Mosquna, Assaf; Kiss, Vladimir; Avivi, Yigal; Ohad, Nir; Grafi, Gideon

doi:10.1105/tpc.105.036855

Cited by 53 publications

(58 citation statements)

References 75 publications

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“…A cyan fluorescent protein (CFP) fusion to TFL2 (HP1-like homolog in A. thaliana) colocalized with the retrotransposon YFP-CHD fusions. When transiently expressed, TFL2 localizes to the chromocenters, the primary domain of heterochromatin in A. thaliana (Fransz et al 2002;Zemach et al 2006). We confirmed this association by showing colocalization between TFL2 and a YFP fusion to CENP-C-a kinetochore protein (Supplemental Fig.…”

Section: Retroelement Chromodomains Direct Proteins To Heterochromatinsupporting

confidence: 67%

Chromodomains direct integration of retrotransposons to heterochromatin

Gao¹,

Hou²,

et al. 2008

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The enrichment of mobile genetic elements in heterochromatin may be due, in part, to targeted integration. The chromoviruses are Ty3/gypsy retrotransposons with chromodomains at their integrase C termini. Chromodomains are logical determinants for targeting to heterochromatin, because the chromodomain of heterochromatin protein 1 (HP1) typically recognizes histone H3 K9 methylation, an epigenetic mark characteristic of heterochromatin. We describe three groups of chromoviruses based on amino acid sequence relationships of their integrase C termini. Genome sequence analysis indicates that representative chromoviruses from each group are enriched in gene-poor regions of the genome relative to other retrotransposons, and when fused to fluorescent marker proteins, the chromodomains target proteins to specific subnuclear foci coincident with heterochromatin. The chromodomain of the fungal element, MAGGY, interacts with histone H3 dimethyl-and trimethyl-K9, and when the MAGGY chromodomain is fused to integrase of the Schizosaccharomyces pombe Tf1 retrotransposon, new Tf1 insertions are directed to sites of H3 K9 methylation. Repetitive sequences such as transposable elements trigger the RNAi pathway resulting in their epigenetic modification. Our results suggest a dynamic interplay between retrotransposons and heterochromatin, wherein mobile elements recognize heterochromatin at the time of integration and then perpetuate the heterochromatic mark by triggering epigenetic modification.[Supplemental material is available online at www.genome.org.] (Girard et al. 2006;Grivna et al. 2006;Vagin et al. 2006). Mobile element insertions that decorate eukaryotic genomes, therefore, frequently define unique chromatin domains. Whereas the genetic consequences of transposition in terms of mutation and genome rearrangement have long been recognized, the biological consequences of their epigenetic marks, which include effects on gene expression and the formation of heterochromatin, are only beginning to be appreciated (Slotkin and Martienssen 2007).Underlying the genetic and epigenetic impact of mobile elements is integration site choice. Although forces such as selection or recombination contribute to the nonrandom distribution of mobile elements in eukaryotic genomes, an increasing number of studies indicate that many mobile elements target integration to specific chromosomal sites (Bushman 2003). For some elements, target sites are determined by recognizing specific DNA sequences, whereas for others, including several retrotransposons and retroviruses, chromatin impacts target site choice. The Ty1 and Ty3 retrotransposons of Saccharomyces cerevisiae, for example, integrate near sites of RNA polymerase III (pol III) transcription by recognizing pol III transcription complexes or chromatin states associated with pol III transcription (Yieh et al. 2000(Yieh et al. , 2002Bachman et al. 2005;Mou et al. 2006). The Tf1 retrotransposon of Schizosaccharomyces pombe recognizes certain RNA polymerase II (pol II) promoters (Singleton and L...

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Section: Retroelement Chromodomains Direct Proteins To Heterochromatinsupporting

confidence: 67%

Chromodomains direct integration of retrotransposons to heterochromatin

Gao¹,

Hou²,

et al. 2008

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“…One characteristic of eukaryotic cell nuclei is the presence of dynamic nuclear compartments, which has been linked to nuclear and cellular processes, including chromatin remodeling, regulation of gene expression, ribosome biogenesis, splicing, postsplicing events, and cell cycle-associated mechanisms (Dundr and Misteli, 2001;Yanovsky et al, 2002;Lamond and Spector, 2003;Bernardi et al, 2004;Moriguchi et al, 2005;Zemach et al, 2006). Nowadays, the functional architecture of the nucleus has to be thought of as a dynamic steady state rather than as a static situation.…”

Section: Discussionmentioning

confidence: 99%

Insights into Nuclear Organization in Plants as Revealed by the Dynamic Distribution ofArabidopsisSR Splicing Factors

et al. 2006

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Serine/arginine-rich (SR) proteins are splicing regulators that share a modular structure consisting of one or two N-terminal RNA recognition motif domains and a C-terminal RS-rich domain. We investigated the dynamic localization of the Arabidopsis thaliana SR protein RSZp22, which, as we showed previously, distributes in predominant speckle-like structures and in the nucleolus. To determine the role of RSZp22 diverse domains in its nucleolar distribution, we investigated the subnuclear localization of domain-deleted mutant proteins. Our results suggest that the nucleolar localization of RSZp22 does not depend on a single targeting signal but likely involves different domains/motifs. Photobleaching experiments demonstrated the unrestricted dynamics of RSZp22 between nuclear compartments. Selective inhibitor experiments of ongoing cellular phosphorylation influenced the rates of exchange of RSZp22 between the different nuclear territories, indicating that SR protein mobility is dependent on the phosphorylation state of the cell. Furthermore, based on a leptomycin B-and fluorescence loss in photobleaching-based sensitive assay, we suggest that RSZp22 is a nucleocytoplasmic shuttling protein. Finally, with electron microscopy, we confirmed that RSp31, a plant-specific SR protein, is dynamically distributed in nucleolar cap-like structures upon phosphorylation inhibition. Our findings emphasize the high mobility of Arabidopsis SR splicing factors and provide insights into the dynamic relationships between the different nuclear compartments.

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“…Hence, besides differences in their subnuclear localization patterns, functional AtMBDs differ in their subnuclear mobility as well. Furthermore, similar to many eukaryotic nuclear proteins, AtMBD5 and AtMBD6 are highly mobile proteins with a residence time in the range of seconds (11,12), whereas AtMBD7 is less mobile with a residence time of minutes, similar to that displayed by the linker histone H1 (13,14). A common feature of low mobility nuclear proteins is their interaction with chromatin via multiple binding domains (15).…”

Section: Resultsmentioning

confidence: 99%

The Three Methyl-CpG-binding Domains of AtMBD7 Control Its Subnuclear Localization and Mobility

Zemach

Gaspan

Grafi

2008

Journal of Biological Chemistry

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Three methyl-CpG-binding domain (MBD) proteins in Arabidopsis, AtMBD5, AtMBD6, and AtMBD7, are functional in binding methylated CpG dinucleotides in vitro and localize to the highly CpG-methylated chromocenters in vivo. These proteins differ, however, in their subnuclear localization pattern; AtMBD5 and AtMBD6, each containing a single MBD motif, show preference for two perinucleolar chromocenters, whereas AtMBD7, a naturally occurring poly-MBD protein containing three MBD motifs, localizes to all chromocenters. Here we studied the significance of multiple MBD motifs for subnuclear localization and mobility in living cells. We found that the number of MBD motifs determines the subnuclear localization of the MBD protein. Furthermore, live kinetic experiments showed that AtMBD7-green fluorescent protein (GFP) has lower mobility than AtMBD5-GFP and AtMBD6-GFP, which is conferred by cooperative activity of its three MBD motifs. Thus, the number of MBD motifs appears to affect not only binding affinity and mobility within the nucleus, but also the subnuclear localization of the protein. Our results suggest that poly-MBD proteins can directly affect chromatin structure by inducing intra-and interchromatin compaction via bridging over multiple methylated CpG sites.Cytosine methylation is a common epigenetic modification of most eukaryotic nuclear DNA. Intensive studies demonstrated the central role played by cytosine methylation in genome organization, gene expression, and growth and development. The way by which the methyl group is interpreted into a functional state has begun to be unraveled with the isolation and characterization of methylated DNA-binding proteins. This group of proteins includes an evolutionary conserved protein family, initially described in animals, termed methyl-CpGbinding domain (MBD) 2 proteins (1). Biochemical and molecular analyses suggest that mammalian MBDs induce the formation of a repressive chromatin structure at methylated CpG (mCpG) sites by the recruitment of various chromatin factors including histone deacetylases, histone methyltransferases, and ATPase-dependent nucleosome remodeling factors (2, 3). Thus far, of the 13 AtMBD proteins found in Arabidopsis, only AtMBD5, AtMBD6, and AtMBD7 were found to bind mCpG sites in vitro and to localize in vivo to the highly methylated chromocenters (ChCs) (reviewed in Refs. 4 and 5). This chromocenter localization is CpG methylation-dependent inasmuch as it was disrupted in the hypomethylated mutants ddm1 and met1 (6). Yet, these three AtMBDs display different localization patterns within Arabidopsis nuclei; AtMBD7 is predominantly localized at all ChCs, whereas AtMBD5 and AtMBD6 show preference for two perinucleolar ChCs adjacent to the ribosomal DNA clusters (6). A major structural feature distinguishing AtMBD7 from AtMBD5 and AtMBD6 is the presence of three MBD motifs within its protein sequence. Notably, naturally occurring poly-MBD proteins appear to be unique to plants as to date no such protein has been found in animals. Here we studied...

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Different Domains Control the Localization and Mobility of LIKE HETEROCHROMATIN PROTEIN1 inArabidopsisNuclei

Cited by 53 publications

References 75 publications

Chromodomains direct integration of retrotransposons to heterochromatin

Chromodomains direct integration of retrotransposons to heterochromatin

Insights into Nuclear Organization in Plants as Revealed by the Dynamic Distribution ofArabidopsisSR Splicing Factors

The Three Methyl-CpG-binding Domains of AtMBD7 Control Its Subnuclear Localization and Mobility

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