Transgenerational Inheritance and Resetting of Stress-Induced Loss of Epigenetic Gene Silencing in Arabidopsis

Lang-Mladek, Christina; Popova, Olga V.; Kiok, Kathrin; Berlinger, Marc; Rakic, Branislava; Aufsatz, Werner; Jonak, Claudia; Hauser, Marie‐Theres; Luschnig, Christian

doi:10.1093/mp/ssq014

Cited by 254 publications

(220 citation statements)

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“…For instance, it was shown that abiotic stress can cause the release of transgene silencing and the reactivation of endogenous heterochromatic loci in Arabidopsis (Lang-Mladek et al 2010;Pecinka et al 2010;TittelElmer et al 2010). Interestingly, this stress-mediated transcriptional activation is not associated with DNA demethylation or changes in repressive histone modifications, two epigenetic marks that are characteristic for the release of transcriptional gene silencing (Lang-Mladek et al 2010;Pecinka et al 2010;Tittel-Elmer et al 2010). Instead, heat stress led to a dramatic reduction in nucleosome loading and affected chromatin organization (Pecinka et al 2010).…”

Section: Epigenetic Stress Responses and Their Potential Inheritancementioning

confidence: 99%

“…Such epialleles contribute to the phenotypic diversity of a population and, hence, may have a role in adaptation and evolution. Moreover, the formation of certain epialleles may be triggered by the environment, as suggested in several recent plant studies (Molinier et al 2006;Hauben et al 2009;Boyko et al 2010;Kathiria et al 2010;Lang-Mladek et al 2010;Verhoeven and van Gurp 2012). If such effects last for several generations, the modern evolutionary synthesis will have to be expanded.…”

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confidence: 99%

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Epigenetic Variation, Inheritance, and Selection in Plant Populations

Hirsch

Baumberger

Grossniklaus

2012

Cold Spring Harbor Symposia on Quantitative Biology

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Plant populations show phenotypic diversity, which may be caused by genetic and epigenetic variation. It has recently been shown that new epigenetic variants are generated at a higher rate than genetic variants and several studies have shown that epigenetic variation can be influenced by the environment. Although the heritability of environmentally induced epigenetic traits has gained increasing interest in past years, it is still not clear whether and to what extent induced epigenetic changes have a role in ecology and evolution. Some reports on model and nonmodel species support the possibility of adaptive epigenetic alleles, indicating that epigenetic variants are subject to natural selection. However, most of these studies rely solely on phenotypic data and no information is available about the underlying mechanisms. Thus, the role of inherited epigenetic variation for plant adaptation is unclear and further investigations are required to gain insights into the significance of epigenetic variation for ecological and evolutionary processes. Here, we review mechanisms of epigenetic regulation, epigenetic responses to environmental challenges, their inheritance, and their implication for adaptation and plant evolution.

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Section: Epigenetic Stress Responses and Their Potential Inheritancementioning

confidence: 99%

mentioning

confidence: 99%

Epigenetic Variation, Inheritance, and Selection in Plant Populations

Hirsch

Baumberger

Grossniklaus

2012

Cold Spring Harbor Symposia on Quantitative Biology

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“…The first evidence that epigenetic marks could indeed be inherited across more than one generation involved transgenes (Allen et al, 1990, Sapienza et al, 1987, Swain et al, 1987. More recently, Lang-Mladek et al, showed in plants that, after extreme temperature or UV-B stress, a silent transgene and several transposable elements were activated, and these changes were heritable for two generations (Lang-Mladek et al, 2010). This suggests that some epigenetic marks may avoid erasure during early development, including the germ line.…”

Section: Epigenetic Memory and Inheritancementioning

confidence: 99%

“…Environmental factors can influence epigenetic processes, and may therefore be related to cancer development (Brait et al, 2009, Lang-Mladek et al, 2010. There are indications that endogenous factors such as the hormonal balance between estrogens and androgens might play a role (Godmann et al, 2009).…”

Section: Environmental Factors In the Pathogenesis Of Gccmentioning

confidence: 99%

Role of epigenetics in the etiology of germ cell cancer

Zwan¹,

Stoop²,

Rossello³

et al. 2013

Int. J. Dev. Biol.

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Embryonic development is strictly controlled by functionality of genes in which the existing networks can act both on transcription and translation regulation. Germ cell cancers (GCC) are unique because of a number of characteristics. In spite of their clinical presentation, i.e., predominantly after puberty, they arise from primordial germ cells/gonocytes that have failed appropriate maturation to either pre-spermatogonia or oogonia. GCC mimic embryonal development to a certain extent, including capacity for totipotency. This knowledge has allowed the identification of informative diagnostic markers, including OCT3/4 (POU5F1), SOX2 and SOX17. An additional marker is the overall demethylated status of the genome. Genetic mutations in GCC are rare, which is exceptional for solid cancers. Our hypothesis is that a disturbed epigenetic regulation (through combined interaction of genetic or environmental parameters; referred to as genvironment) affect embryonic germ cell development, resulting in delayed or blocked maturation, and potentially progression to GCC. In this respect, studies of patients with Disorders of Sex Development (DSD) have increased our knowledge significantly. Genvironmental influences can lead to retention of existence of embryonic germ cells, the first step in the pathogenesis of GCC, resulting into the precursor lesions gonadoblastoma or carcinoma in situ. Identification of epigenetic alterations could lead to better understanding these processes and development of specific markers for early detection, eventually leading to development of targeted treatment. This review describes an interactive model related to the role of epigenetics in GCC pathogenesis, focusing on DNA methylation, histone modifications, epigenetic memory and inheritance, as well as environmental factors.

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“…A possible mechanism via which the 2245 site could become differentially methylated may involve an interaction between the site and either small or lncRNAs. In plants, small (21-24 nt) RNAs are known to trigger epigenetic gene silencing (Lang-Mladek et al 2010;Hauser et al 2011). The cly1 locus includes four sites, including the 2245 site, which could in principle be targeted by siRNAs ( Figure 5A).…”

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confidence: 99%

An Epiallele at cly1 Affects the Expression of Floret Closing (Cleistogamy) in Barley

Wang

Ning

et al. 2014

Genetics

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The swelling of the lodicule is responsible for floret opening in many grass species, allowing for pollen dispersal and crosspollination. In barley, the closed floret habit (cleistogamy) is under the control of cly1, a gene that operates by inhibiting the development of the lodicule. In non-cleistogamous cultivars, cly1 mRNA is degraded by miR172-directed cleavage, allowing the lodicules to swell; however, in cultivars carrying the recessive allele cly1.b, a single-nucleotide substitution destroys the miR172 target site preventing mRNA cleavage. Barley cv. SV235 is cleistogamous; its cly1 coding sequence is identical to that of cly1.b, but its lodicules do develop, although insufficiently to produce a non-cleistogamous flower. In this cultivar, the downregulation of cly1 is unrelated to miR172-directed mRNA degradation, but rather is caused by an epiallele that represses transcription. Allelic relationships between known cly1 alleles were explored by the quantification of lodicule vascularization and an assessment of the response of the spike to the supply of exogenous auxin. The SV235 phenotype can be manipulated by a pre-anthesis application of 2,4-D, a feature that could be of interest in the context of hybrid barley grain production based on cleistogamy.T HE swelling of the lodicule, a structure found in the floret of many grass species and functionally related to the petal in the hermaphroditic angiosperm flower, drives apart the palea and lemma, thereby opening the floret so that it can release its pollen and be readily cross-pollinated (Briggs 1978). In barley, closed flowering (cleistogamous) variants are known. In some of these, the lodicule fails to swell (Kurauchi et al. 1994;Turuspekov et al. 2004;Honda et al. 2005;Wang et al. 2013). The cleistogamy 1 gene (cly1) has been shown to encode an AP2-protein and is a paralog of HvAP2-like in barley and Q in bread wheat (Simons et al. 2006;Nair et al. 2010;Simonov and Pshenichnikova 2012;Ning et al. 2013). In noncleistogamous barleys, cly1 mRNA is cleaved by an miRNA, with the result that the abundance of full-length gene product remains at a low level. Two cleistogamy alleles are known, cly1.b and cly1.c; in both cases, cly1 mRNA is not cleaved by miR172, resulting in the failure of the lodicule to swell. Exceptionally, in cv. SV235, although its cly1 coding sequence is identical to that of cly1.b, its lodicules do swell at anthesis, although insufficiently to force open the floret. Here, we show the genetic and epigenetic basis of the unusual lodicule development seen in cv. SV235. Materials and Methods Plant materialsGrain of the barley cultivars SV002 (OUA008, "Sanalta"), SV223 (OUU059, "Tammi"), SV230 (OUU305, "Badajoy"), SV235 (OUU326, "France 1"), SV237 (OUU329, "Cygne"), SV241 (OUU351, "Plumage"), SV242 (OUU352, "Imperial"), and SV255 (OUU613, "Otello"), along with the Hordeum vulgare subsp. spontaneum accession OUH602 (the OU numbers relate to the Barley and Wild Plant Resource Center collection, http://www.rib.okayama-u.ac.jp/barley/index...

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Transgenerational Inheritance and Resetting of Stress-Induced Loss of Epigenetic Gene Silencing in Arabidopsis

Cited by 254 publications

References 50 publications

Epigenetic Variation, Inheritance, and Selection in Plant Populations

Epigenetic Variation, Inheritance, and Selection in Plant Populations

Role of epigenetics in the etiology of germ cell cancer

An Epiallele at cly1 Affects the Expression of Floret Closing (Cleistogamy) in Barley

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