mediator of paramutation1 Is Required for Establishment and Maintenance of Paramutation at Multiple Maize Loci

Dorweiler, Jane E.; Carey, Charles C.; Kubo, Kenneth M.; Hollick, Jay B.; Kermicle, Jerry L.; Chandler, Vicki L.

doi:10.2307/3871108

Cited by 51 publications

(124 citation statements)

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“…The paramutated form of B-I, designated B 0 *, is stably inherited independently of B 0 and is itself paramutagenic, which makes it indistinguishable from B 0 (Chandler and Stam, 2004). Moreover, whereas B-I reverts spontaneously to B 0 at high frequency (1-10%) and can thus be considered a metastable epiallele, B 0 is highly stable and only becomes more active in RNAi mutant backgrounds (Dorweiler et al, 2000;Alleman et al, 2006;Woodhouse et al, 2006). These findings suggest that the tandem repeats of B-I and B 0 are, respectively, just below and well above the threshold required for RNAi-dependent chromatin targeting, presumably as a consequence of differences in chromatin states ( (Arteaga-Vazquez and Chandler, 2010), it is also reasonable to assume that the tandem repeats of B 0 and B-I produce distinct amount of siRNAs, at least during the reproductive phase, when the RNAi-dependent chromatin targeting pathway could be most active, as in Arabidopsis (Figure 2).…”

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Repeat elements and the Arabidopsis DNA methylation landscape

Teixeira

Colot

2010

Heredity

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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...

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Repeat elements and the Arabidopsis DNA methylation landscape

Teixeira

Colot

2010

Heredity

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“…Because these small RNAs are involved in controlling transposons and other repeated regions of the genome, they could potentially play a bigger role in plants such as rice and maize that have large genomes with a high proportion of repeated sequences. Furthermore, Arabidopsis plants having a mutation in RDR2 display virtually no developmental defects, whereas mutation of the maize homolog of RDR2 (MOP1) results in a number of developmental anomalies (Dorweiler et al 2000;Alleman et al 2006;Woodhouse et al 2006). These observations raise the possibility that some aspects of Pol IV/V siRNA-mediated transcriptional silencing have a greater role in regulating development in cereals than in Arabidopsis.…”

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Clusters and superclusters of phased small RNAs in the developing inflorescence of rice

Johnson¹,

Kasprzewska²,

Tennessen³

et al. 2009

Genome Res.

293

319

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To address the role of small regulatory RNAs in rice development, we generated a large data set of small RNAs from mature leaves and developing roots, shoots, and inflorescences. Using a spatial clustering algorithm, we identified 36,780 genomic groups of small RNAs. Most consisted of 24-nt RNAs that are expressed in all four tissues and enriched in repeat regions of the genome; 1029 clusters were composed primarily of 21-nt small RNAs and, strikingly, 831 of these contained phased RNAs and were preferentially expressed in developing inflorescences. Thirty-eight of the 24-mer clusters were also phased and preferentially expressed in inflorescences. The phased 21-mer clusters derive from nonprotein coding, nonrepeat regions of the genome and are grouped together into superclusters containing 10-46 clusters. The majority of these 21-mer clusters (705/831) are flanked by a degenerate 22-nt motif that is offset by 12 nt from the main phase of the cluster. Small RNAs complementary to these flanking 22-nt motifs define a new miRNA family, which is conserved in maize and expressed in developing reproductive tissues in both plants. These results suggest that the biogenesis of phased inflorescence RNAs resembles that of tasiRNAs and raise the possibility that these novel small RNAs function in early reproductive development in rice and other monocots.

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“…Recently, a protein that binds to the b1 tandem repeat (b1TR) sequences was identified, and expression of this protein as a transgene can establish a paramutagenic state in B-I (11). The mop1 gene, which is the focus of this study, encodes a protein with high similarity to RNA-dependent RNA polymerases (RDRs) and is the predicted ortholog of RDR2 in Arabidopsis thaliana (Arabidopsis) (4,5,7). Activity of mop1 is required for paramutation at the b1 locus and other loci (5,6,12), and it is required to maintain the silent B′ state (5).…”

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“…The mediator of paramutation (mop) genes (1,(4)(5)(6) and the required to maintain repression (rmr) genes (6,(8)(9)(10) have been isolated using the b1 and pl1 systems, respectively. To date, all characterized genes required for paramutation identified through forward genetic screens encode proteins that have been associated with siRNA biogenesis in other species (1).…”

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RNA-mediated trans -communication can establish paramutation at the b1 locus in maize

Arteaga-Vázquez

Сидоренко

Rabanal

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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Paramutation is the epigenetic transfer of information between alleles that leads to the heritable change of expression of one allele. Paramutation at the b1 locus in maize requires seven noncoding tandem repeat (b1TR) sequences located ∼100 kb upstream of the transcription start site of b1, and mutations in several genes required for paramutation implicate an RNA-mediated mechanism. The mediator of paramutation (mop1) gene, which encodes a protein closely related to RNA-dependent RNA polymerases, is absolutely required for paramutation. Herein, we investigate the potential function of mop1 and the siRNAs that are produced from the b1TR sequences. Production of siRNAs from the b1TR sequences depends on a functional mop1 gene, but transcription of the repeats is not dependent on mop1. Further nuclear transcription assays suggest that the b1TR sequences are likely transcribed predominantly by RNA polymerase II. To address whether production of b1TR-siRNAs correlated with paramutation, we examined siRNA production in alleles that cannot undergo paramutation. Alleles that cannot participate in paramutation also produce b1TR-siRNAs, suggesting that b1TR-siRNAs are not sufficient for paramutation in the tissues analyzed. However, when b1TR-siRNAs are produced from a transgene expressing a hairpin RNA, b1 paramutation can be recapitulated. We hypothesize that either the b1TR-siRNAs or the dsRNA template mediates the trans-communication between the alleles that establishes paramutation. In addition, we uncovered a role for mop1 in the biogenesis of a subset of microRNAs (miRNAs) and show that it functions at the level of production of the primary miRNA transcripts.interchromosomal | transfer | epigenetic | information | trans-generational

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mediator of paramutation1 Is Required for Establishment and Maintenance of Paramutation at Multiple Maize Loci

Cited by 51 publications

References 50 publications

Repeat elements and the Arabidopsis DNA methylation landscape

Repeat elements and the Arabidopsis DNA methylation landscape

Clusters and superclusters of phased small RNAs in the developing inflorescence of rice

RNA-mediated trans -communication can establish paramutation at the b1 locus in maize

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