An RNA-dependent RNA polymerase is required for paramutation in maize

Alleman, Mary; Сидоренко, Л. В.; McGinnis, Karen M.; Seshadri, Vishwas; Dorweiler, Jane E.; White, Joe L.; Sikkink, Kristin L.; Chandler, Vicki L.

doi:10.1038/nature04884

Cited by 343 publications

(322 citation statements)

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“…Mop1 encodes for an RNAdependent RNA polymerase, which, together with Rmr2 (Hollick and Chandler 2001), is required for somatic maintenance of the paramutant state of Pl' and B' but not R' allele. Mop1 is also required to establish silencing at b1 and r1 loci , Alleman et al, 2006, and is able to progressively reactivate a silenced MuDR element (Woodhouse et al, 2006). Analysis of progenies obtained by crossing the mop1-1 mutant with our lpa mutants ( Figure 6) showed that mop1-1 mutant is not involved in the maintenance of the silenced state of lpa1-241 allele.…”

Section: Discussionmentioning

confidence: 99%

“…So far, we do not know whether paramutation is also affected, and we plan to do this experiment in the near future. Mop1 is an RNAdependent RNA polymerase possibly involved in maintaining a threshold level of some kind of silencing RNA, which mediates transcriptional gene silencing (Alleman et al, 2006). Although 5-Azacytidine can significantly revert lpa1-241 phenotype, mop1 mutation cannot.…”

Section: Discussionmentioning

confidence: 99%

“…So far, paramutation in maize has been studied at four loci: r1, b1, p1 and pl1, all involved in the regulation of anthocyanin and flavonoid biosynthesis (reviewed in Chandler et al, 2000). For these genes, reduced pigmentation linked to the paramutated allele correlates with reduced mRNA level and in the case of b1 locus is associated with RNAi phenomena (Das and Messing, 1994;Lund et al, 1995;Chandler et al, 2000;Sidorenko and Peterson, 2001;Della Vedova and Cone, 2004;Chandler and Stam, 2004;Stam and Scheid, 2005;Alleman et al, 2006;Chandler, 2007).…”

Section: Introductionmentioning

confidence: 99%

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A paramutation phenomenon is involved in the genetics of maize low phytic acid1-241 (lpa1-241) trait

et al. 2008

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So far, in maize, three classes of mutants involved in phytic acid biosynthesis have been isolated: lpa1, lpa2 and lpa3. In 2007, a gene tagging experiment performed by Shi et al. found that mutations in ZmMRP4 (multidrug resistance-associated proteins 4) gene cause lpa1 phenotype. In previous studies, we isolated and described a single recessive lpa mutation (originally named lpa241), which was allelic to the lpa1-1 mutant, and was consequently renamed lpa1-241. It showed a decrease in the expression of the myo-inositol (Ins)-3-phosphate synthase gene (mips1S). In this study, we present genetic and molecular analyses of the lpa1-241 mutation that indicate an epigenetic origin of this trait, that is, a paramutagenic interaction that results in meiotically heritable changes in ZmMRP4 gene expression, causing a strong pleiotropic effect on the whole plant. The use of a 5-Azacytidine treatment provided data suggesting an association between gene methylation and the lpa1-241 phenotype. To our knowledge, this is the first report of a paramutagenic activity not involving flavonoid biosynthesis in maize, but regarding a key enzyme of an important metabolic pathway in plants.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A paramutation phenomenon is involved in the genetics of maize low phytic acid1-241 (lpa1-241) trait

et al. 2008

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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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confidence: 99%

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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“…Very little is known how the methylation "states" (epigenetic states) of these cis-regulatory regions are established. More recently, a new link between transposon activity and epigenetic phenomena such as paramutation, imprinting and gene silencing has been established in plants as well as in animals (Ketting et al 1999;Tabara et al 1999;Lippman et al 2004;Martienssen et al 2004;Alleman et al 2006). ROSINA (RSI) was isolated as a factor able to bind a speciWc promoter region of the DEFICIENS gene and to modulate petal and stamen development (Roccaro et al 2005).…”

Section: Introductionmentioning

confidence: 99%

ROSINA (RSI) is part of a CACTA transposable element, TamRSI, and links flower development to transposon activity

Roccaro¹,

Sommer³

et al. 2007

Mol Genet Genomics

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ROSINA (RSI) was isolated as a DNA binding factor able to bind to the CArG-box present in the promoter of the MADS-box gene DEFICIENS of Antirrhinum majus. The mosaic nature of RSI and its multi-copy presence in the A. majus genome indicated that RSI could be a part of a mobile genetic element. Here we show that RSI is a part of a CACTA transposable element system of A. majus, named TamRSI, which has evolved and is still evolving within the terminal inverted repeats (TIRs) of this CACTA transposon. Interestingly, RSI is always found in opposite orientation with respect to the transcription of a second gene present within the CACTA transposon, which encodes a putative TRANSPOSASE (TNP). This structural conWguration has not yet been described for any member of the CACTA transposons superfamily. Internal deletion derivatives of the TamRSI produce aberrant RSI transcripts (RSIATs) that carry parts of the RSI RNA fused to parts of the TNP RNA. In addition, an intriguing seed phenotype shown by RNAi transgenic lines generated to silence RSI, relate TamRSI to epigenetic mechanisms and associate the control of Xower development to transposon activity.

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An RNA-dependent RNA polymerase is required for paramutation in maize

Cited by 343 publications

References 31 publications

A paramutation phenomenon is involved in the genetics of maize low phytic acid1-241 (lpa1-241) trait

A paramutation phenomenon is involved in the genetics of maize low phytic acid1-241 (lpa1-241) trait

Repeat elements and the Arabidopsis DNA methylation landscape

ROSINA (RSI) is part of a CACTA transposable element, TamRSI, and links flower development to transposon activity

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