A Gene Essential for De Novo Methylation and Development in Ascobolus Reveals a Novel Type of Eukaryotic DNA Methyltransferase Structure

Malagnac, Fabienne; Wendel, Birgit; Goyon, Christophe; Faugeron, Godeleine; Zickler, Denise; Rossignol, Jean‐Luc; Noyer-Weidner, Mario; Vollmayr, Peter; Trautner, Thomas A.; Walter, Jörn

doi:10.1016/s0092-8674(00)80410-9

Cited by 135 publications

(129 citation statements)

References 36 publications

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“…Despite the common outcome, usually termed gene silencing or cosuppression, there seems to be considerable heterogeneity in the underlying molecular mechanisms. In no case is the mechanism completely understood; however, transgene-induced silencing can involve DNA methylation (Malagnac et al, 1997), the establishment of stably repressed chromatin (Pal-Bhadra et al, 1997), or RNA-mediated RNA deg-radation (Cogoni and Macino, 1997;Metzlaff et al, 1997).…”

Section: Introductionmentioning

confidence: 99%

Homology-dependent Gene Silencing inParamecium

Ruiz

Vayssié

Klotz

et al. 1998

MBoC

151

122

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Microinjection at high copy number of plasmids containing only the coding region of a gene into the Paramecium somatic macronucleus led to a marked reduction in the expression of the corresponding endogenous gene(s). The silencing effect, which is stably maintained throughout vegetative growth, has been observed for allParamecium genes examined so far: a single-copy gene (ND7), as well as members of multigene families (centrin genes and trichocyst matrix protein genes) in which all closely related paralogous genes appeared to be affected. This phenomenon may be related to posttranscriptional gene silencing in transgenic plants and quelling in Neurospora and allows the efficient creation of specific mutant phenotypes thus providing a potentially powerful tool to study gene function in Paramecium. For the two multigene families that encode proteins that coassemble to build up complex subcellular structures the analysis presented herein provides the first experimental evidence that the members of these gene families are not functionally redundant.

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Section: Introductionmentioning

confidence: 99%

Homology-dependent Gene Silencing inParamecium

Ruiz

Vayssié

Klotz

et al. 1998

MBoC

151

122

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“…Plasticity of DNA methylation during the life cycle of an organism, and heritability of methylation patterns over generations are crucial for normal development (Schob and Grossniklaus 2006). Genetic manipulations that alter DNA methylation cause various developmental abnormalities in plants (Finnegan et al 1996;Ronemus et al 1996;Cao and Jacobsen 2002), mice (Li et al 1992;Okano et al 1999), humans (Hansen et al 1999;Xu et al 1999), and fungi (Foss et al 1993;Malagnac et al 1997).…”

mentioning

confidence: 99%

Progressive Loss of DNA Methylation Releases Epigenetic Gene Silencing From a Tandemly Repeated Maize Myb Gene

Sekhon¹,

Chopra

2009

Genetics

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Maize pericarp color1 (p1) gene, which regulates phlobaphene biosynthesis in kernel pericarp and cob glumes, offers an excellent genetic system to study tissue-specific gene regulation. A multicopy p1 allele, P1-wr (white pericarp/red cob) is epigenetically regulated. Hypomethylation of P1-wr in the presence of Unstable factor for orange1 (Ufo1), leads to ectopic pigmentation of pericarp and other organs. The Ufo1-induced phenotypes show incomplete penetrance and poor expressivity: gain of pigmentation is observed only in a subset of plants carrying Ufo1 mutation, and the extent of pigmentation is highly variable. We show that Ufo1 induces progressive hypomethylation of P1-wr repeats over generations. After five generations of exposure to Ufo1, a 30-40% decrease in CG and CNG methylation was observed in an upstream enhancer and an intron region of P1-wr. Interestingly, such hypomethylation correlated with an increase in penetrance of the Ufo1-induced pigmentation phenotype from $27 to 61%. Expressivity of the Ufo1-induced phenotype also improved markedly as indicated by increased uniformity of pericarp pigmentation in the later generations. Furthermore, the poor expressivity of the Uo1 is associated with mosaic methylation patterns of the P1-wr upstream enhancer in individual cells and distinct P1-wr gene copies. Finally, comparison of methylation among different tissues indicated that Ufo1 induces rapid CG and CNG hypomethylation of P1-wr repeats during plant development. Together, these data indicate that the poor penetrance and expressivity of Ufo1-induced phenotypes is caused by mosaicism of methylation, and progressive mitotic hypomethylation leads to improved meiotic heritability of the mutant phenotype. In duplicated genomes like maize, loss of an epigenetic regulator may produce mosaic patterns due to redundancy of epigenetic regulators and their target sequences. We show here that multiple developmental cycles may be required for complete disruption of suppressed epigenetic states and appearance of heritable phenotypes.

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“…In N. crassa, Dim-2 is also dispensable for normal growth and fertilization, including RIP. In contrast, masc1 and dmtA, the homologs of rid, in A. immersus and Aspergillus nidulans, respectively, are essential for fertility (Malagnac et al 1997;Lee et al 2008). Interestingly, masc2, a dnmt1-like methyltransferase in A. immerses, was dispensable for fertility and DNA methylation of natural genomic retroelement-like repeats and tandemly repeated rDNA despite showing methyltransferase activity in vitro (Malagnac et al 1999).…”

Section: Discussionmentioning

confidence: 95%

“…Dim-2 in N. crassa (Kouzminova and Selker 2001) and Masc2 in A. immersus (Chernov et al 1997) are involved in DNA methylation and transcriptional silencing in vegetative cells. Masc1 in A. immersus is responsible for methylation induced premeiotically (MIP) during the sexual stage (Malagnac et al 1997). Rid, the N. crassa ortholog of Masc1, is required for repeat-induced point mutation (RIP) during the sexual phase (Freitag et al 2002) but whether it is an actual DNA methyltransferase is not yet known.…”

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confidence: 99%

Is the Fungus Magnaporthe Losing DNA Methylation?

Ikeda

Kadotani

et al. 2013

Genetics

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The long terminal repeat retrotransposon, Magnaporthe gypsy-like element (MAGGY), has been shown to be targeted for cytosine methylation in a subset of Magnaporthe oryzae field isolates. Analysis of the F 1 progeny from a genetic cross between methylation-proficient (Br48) and methylation-deficient (GFSI1-7-2) isolates revealed that methylation of the MAGGY element was governed by a single dominant gene. Positional cloning followed by gene disruption and complementation experiments revealed that the responsible gene was the DNA methyltransferase, MoDMT1, an ortholog of Neurospora crassa Dim-2. A survey of MAGGY methylation in 60 Magnaporthe field isolates revealed that 42 isolates from rice, common millet, wheat, finger millet, and buffelgrass were methylation proficient while 18 isolates from foxtail millet, green bristlegrass, Japanese panicgrass, torpedo grass, Guinea grass, and crabgrass were methylation deficient. Phenotypic analyses showed that MoDMT1 plays no major role in development and pathogenicity of the fungus. Quantitative polymerase chain reaction analysis showed that the average copy number of genomic MAGGY elements was not significantly different between methylation-deficient and -proficient field isolates even though the levels of MAGGY transcript were generally higher in the former group. MoDMT1 gene sequences in the methylation-deficient isolates suggested that at least three independent mutations were responsible for the loss of MoDMT1 function. Overall, our data suggest that MoDMT1 is not essential for the natural life cycle of the fungus and raise the possibility that the genus Magnaporthe may be losing the mechanism of DNA methylation on the evolutionary time scale.C YTOSINE methylation is a chemical modification of DNA and is at the heart of an epigenetic mechanism involved in the control of a variety of biological processes, such as embryogenesis, cell differentiation, X-chromosome inactivation, genomic imprinting, and gene silencing (Laird and Jaenisch 1996). Cytosine methylation occurs in all three domains of life, namely, Eubacteria, Archaebacteria, and Eukaryota, and is regarded as an ancestral mechanism that antedates the divergence of eukaryotes and prokaryotes (Tajima and Suetake 1998). Consistent with this, the catalytic enzymes of cytosine methylation, the cytosine DNA methyltransferases (DMTs), are conserved in eukaryotes and prokaryotes and contain nine well-conserved motifs arranged in the same order along their primary structure (Kumar et al. 1994;Jurkowski and Jeltsch 2011).Interestingly, however, the pattern and extent of genomic DNA methylation shows considerable diversity among eukaryotes (Yoder et al. 1997; Colot and Rossignol 1999;Rabinowicz et al. 1999). While cytosine DNA methylation is common in higher plants and vertebrates, it is virtually absent in certain lower organisms, such as Saccharomyces cerevisiae, Schizosaccharomyces pombe, and Caenorhabditis elegans (Antequera et al. 1984;Proffitt et al. 1984;Hodgkin 1994). Consistent with this observation, ...

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A Gene Essential for De Novo Methylation and Development in Ascobolus Reveals a Novel Type of Eukaryotic DNA Methyltransferase Structure

Cited by 135 publications

References 36 publications

Homology-dependent Gene Silencing inParamecium

Homology-dependent Gene Silencing inParamecium

Progressive Loss of DNA Methylation Releases Epigenetic Gene Silencing From a Tandemly Repeated Maize Myb Gene

Is the Fungus Magnaporthe Losing DNA Methylation?

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