A Role for RNAi in the Selective Correction of DNA Methylation Defects

Teixeira, Felipe Karam; Herédia, Fabiana; Sarazin, Alexis; Roudier, François; Boccara, Martine; Ciaudo, Constance; Cruaud, Corinne; Poulain, Julie; Berdasco, María; Fraga, Mario F.; Voinnet, Olivier; Wincker, Patrick; Esteller, Manel; Colot, Vincent

doi:10.1126/science.1165313

Cited by 348 publications

(334 citation statements)

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“…Moreover, plants seem more prone to the inheritance of DNA methylation defects than mammals (Richards, 2006;Whitelaw and Whitelaw, 2008). Collectively, these observations indicate that DNA methylation patterns tend to be propagated across generations in plants, rather than re-established anew at each generation like in mammals.Nonetheless, DNA methylation and silencing can be restored in an RNAi-dependent manner over a subset of repeat sequences following ddm1-induced hypomethylation (Johannes et al, 2009;Teixeira et al, 2009). Typically, restoration takes place over several generations , which is consistent with the frequent progressivity of TE inactivation in maize and transgene silencing in many plant species (Chandler and Stam, 2004;Slotkin and Martienssen, 2007).…”

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confidence: 69%

“…As mentioned earlier, DNA methylation of repeat elements is mostly constant among Arabidopsis accessions (Vaughn et al, 2007;Zhai et al, 2008;Zhang et al, 2008), yet some highly methylated repeat elements seem to produce hardly any siRNAs (Kasschau et al, 2007;Lister et al, 2008;Teixeira et al, 2009). This raises the question of how such repeat elements maintain DNA methylation over evolutionary time.…”

Section: Transgenerational Inheritance Of Dna Methylation Patternsmentioning

confidence: 98%

“…Furthermore, CHH methylation is not completely abolished in drm1drm2cmt3 triple mutants (Cokus et al, 2008;Lister et al, 2008). This and other observations suggest that some CHH methylation is in fact laid down by MET1 or additional DNA MTases, presumably in an RNAi-independent manner ( In addition to the factors listed above, the ATPase SWI2/SNF2 chromatin remodeler DECREASE IN DNA METHYLATION 1 (DDM1) has an essential role in the maintenance of high DNA methylation levels over repeat elements (Vongs et al, 1993;Jeddeloh et al, 1999;Lippman et al, 2004;Teixeira et al, 2009). Although the mechanism of action of DDM1 remains mysterious, studies carried out on the mammalian homolog lymphoid-specific helicase (LSH) suggest that it may serve as a recruiting factor for DNA MTases and histone deacetylases at target loci (Myant and Stancheva, 2008).…”

Section: Dna Methylation Maintenance Mechanismsmentioning

confidence: 99%

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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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confidence: 69%

Section: Transgenerational Inheritance Of Dna Methylation Patternsmentioning

confidence: 98%

Section: Dna Methylation Maintenance Mechanismsmentioning

confidence: 99%

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Repeat elements and the Arabidopsis DNA methylation landscape

Teixeira

Colot

2010

Heredity

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“…In the cellular epigenetic scenario, the presence or absence of methyl, acetyl or phosphate groups to the DNA or histones can transiently or permanently modify gene expression by altering the local chromatin structure (Johannes et al 2008 Jacobsen 2009). These cellular epigenetic changes can be induced by environmental and/or genetic factors, and can remain relatively stable over several generations (Teixeira et al 2009;Reinders et al 2009). Phenotype can also be changed by mechanisms other than (epi)genome variation (Fig.…”

Section: Microevolution Of Contrasting Seasonally Changing Phenotypesmentioning

confidence: 99%

Flyway evolution is too fast to be explained by the modern synthesis: proposals for an ‘extended’ evolutionary research agenda

Piersma

2011

J Ornithol

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In this paper, I argue that to fully grasp the generation and maintenance of variation in the migratory phenotypes of (shore-)birds we need to expand our scientific search image and include developmental processes and non-genetic pathways of inheritance in the explanatory frameworks. Traditionally, studies of micro-evolution of migratory phenotypes were restricted to comparative studies on migratory versus non-migratory taxa, and artificial selection and heritability experiments on quantitative behavioural traits related to migration. Such studies had a focus on the genetic axis of inheritance and were restricted to songbirds. In avian groups such as the shorebird families Scolopacidae and Charadriidae, all but a few island species are migrants, which precludes comparative studies at the species level. Like other taxa, shorebirds have geographically separate breeding populations (either or not recognized as subspecies on the basis of morphological differences) which differentiate with respect to the length, general direction and timing of migration, including the use of fuelling at staging sites and the timing of moult. However, their breeding systems preclude artificial selection and heritability experiments on quantitative traits. This would seem to limit the prospects of evolutionary analysis until one realizes that the speed of evolutionary innovation in shorebird migratory life-histories may be so fast as to necessitate other avenues of explanation and investigation. According to our best current estimates based on mitochondrial gene sequence variation, in Red Knots Calidris canutus considerable phenotypic variation has evolved since the Last Glacial Maximum ca. 20,000 years ago, to the extent that six subspecies are currently recognized. This would be too short a time for the origin of the qualitatively and quantitatively distinct and non-overlapping traits to be explained by random point mutations followed by natural selection, although we cannot dismiss the possibility of previously unexpressed (standing) genetic variation followed by selection. I argue that, to understand the flyway evolution of such shorebirds in the 'extended' evolutionary framework, we need to give due attention to developmental versatility and broad-sense epigenetic evolutionary mechanisms. This means that experimental studies at the phenotypic level are now necessary. This could involve a combination of observational studies in our rapidly changing world, common garden experiments, and even experiments involving global-scale displacements of particular migratory phenotypes at different phases of development. I provide suggestions on how such experiments could be carried out.

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“…Variation of DNA methylation can affect plant phenotypes [1] and impact some important agricultural traits, such as resistance to rice bacterial blight (BB) [2,3], plant height [4] and yield [5]. Allelic variation in DNA methylation appears to be inheritable in subsequent generations [68], and inheritance of DNA methylation may be due to RNAi [9]. In Arabidopsis, large regions of contiguous methylation remain as stable DNA sequences across 30 generations [1].…”

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confidence: 99%

DNA methylation polymorphism and stability in Chinese indica hybrid rice

Peng

Jiang

Zhang

et al. 2013

Sci. China Life Sci.

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Conventional rice breeding has long focused on exploiting the DNA sequence diversity. However, epigenetic diversity, reflected particularly in DNA methylation, can also contribute to phenotypic variation and should not be overlooked in rice breeding. In this study, 20 parental lines of indica rice, which are widely used in hybrid rice breeding in China, were analyzed to investigate variations of DNA methylation and its inheritance. The results revealed a wide diversity in DNA methylation among these breeding lines. A positive correlation was seen between DNA methylation and genetic diversity. Furthermore, some of the methylated DNA was inherited in the subsequent generation, regardless of whether they were produced by selfing or hybrid-crossing. This study provides insight into the methylation patterns in rice, and suggests the importance of epigenetic diversity in rice breeding. epigenetic diversity, genetic diversity, rice breeding line

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A Role for RNAi in the Selective Correction of DNA Methylation Defects

Cited by 348 publications

References 21 publications

Repeat elements and the Arabidopsis DNA methylation landscape

Repeat elements and the Arabidopsis DNA methylation landscape

Flyway evolution is too fast to be explained by the modern synthesis: proposals for an ‘extended’ evolutionary research agenda

DNA methylation polymorphism and stability in Chinese indica hybrid rice

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