The Late Flowering Phenotype of fwa Mutants Is Caused by Gain-of-Function Epigenetic Alleles of a Homeodomain Gene

Soppe, Wim J. J.; Jacobsen, Steven E.; Alonso‐Blanco, Carlos; Jackson, James P.; Kakutani, Tetsuji; Koornneef, M.; Peeters, Anton J. M.

doi:10.1016/s1097-2765(05)00090-0

Cited by 535 publications

(345 citation statements)

References 47 publications

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“…3B, panel FWA tr; Lippman et al 2004). The promoter region of FWA in wild-type plants has been shown to be methylated in all sequence contexts (CG, CNG, and CNN) within the two direct repeats region, causing FWA to be silenced (Soppe et al 2000). In this regard, FWA activation in our mutants suggested a possible loss of cytosine methylation and con- sequent heterochromatin disruption.…”

Section: Rnapiva and Rnapivb Act In The Same Pathway And Direct Silenmentioning

confidence: 82%

“…While the regulation of most genes analyzed was not affected, as exemplified by the floral gene regulator FLC, all independent mutants showed significant expression of the imprinted FWA gene, whose ectopic expression has been shown to induce a late flowering phenotype in Arabidopsis (Fig. 3B, see panels FLC and FWA; Soppe et al 2000). Consistent with the ectopic activation of FWA, we found that the long tandem repeat that encompasses the FWA promoter and the first two untranslated exons is transcriptionally active in all mutants analyzed (Fig.…”

Section: Rnapiva and Rnapivb Act In The Same Pathway And Direct Silenmentioning

confidence: 98%

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Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis

Pontier¹,

Yahubyan²,

Véga³

et al. 2005

Genes Dev.

359

441

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Recent genetic and biochemical studies have revealed the existence in plants of a fourth RNA polymerase, RNAPIV, which mediates siRNA accumulation and DNA methylation-dependent silencing of endogenous repeated sequences. Here, we show that Arabidopsis expresses, in fact, two evolutionarily related forms of RNAPIV, hereafter referred to as RNAPIVa and RNAPIVb. These two forms contain the same second-largest subunit (NRPD2), but differ at least by their largest subunit, termed NRPD1a and NRPD1b. Unlike NRPD1a, NRPD1b possesses a reiterated CTD, a feature that also characterizes the largest subunit of RNAPII. Our data indicate that RNAPIVb is the most abundant form of RNAPIV in Arabidopsis. Selective disruption of either form of RNAPIV indicates that RNAPIVa-dependent siRNA accumulation is not sufficient per se to drive robust silencing at endogenous loci and that high levels of DNA methylation and silencing depend on siRNA that are accumulated through a pathway involving the concerted action of both RNAPIV forms. Taken together, our results imply the existence of a novel two-step mechanism in siRNA synthesis at highly methylated loci, with RNAPIVb being an essential component of a self-reinforcing loop coupling de novo DNA methylation to siRNA production. A major evolutionary distinction separating prokaryotes from eukaryotes is the passage from a unique multisubunit DNA-dependent RNA polymerase enzyme (RNAP) to three complexes (Roeder and Rutter 1969), each responsible for the transcription of a subclass of nuclear DNA sequences (Sentenac 1985). RNA polymerase I (RNAPI) transcribes the repeated genes encoding the large ribosomal RNAs, which represent up to four-fifths of total RNA. RNA polymerase II (RNAPII) transcribes all of the cell protein-coding messenger RNAs (mRNAs) as well as some small nuclear RNAs (snRNAs). RNA polymerase III (RNAPIII) is dedicated to the transcription of a collection of genes whose main common feature is that they encode structural or catalytic RNAs (tRNAs, 5S RNA, snRNA) that are components of protein synthesis, splicing, and tRNA processing apparatuses. It is believed that this triplication event provided the eukaryotic cell with a greater flexibility toward energy-consuming cellular functions such as ribosome synthesis, as well as with more sophisticated means for the regulation of gene expression.Prokaryotic and eukaryotic RNA polymerases are multisubunit enzymes that are evolutionarily related to each other through their largest and second-largest subunits (Ebright 2000;Cramer 2002). The largest subunit (≈160 kDa: ␤Ј; A; RPA1; RPB1; RPC1) contains eight regions conserved in order and sequence (A to H), while the second-largest subunit (≈150 kDa: ␤; B; RPA2; RPB2; RPC2), contains nine such regions (A to I) (Allison et al. 1985;Sweetser et al. 1987). Although the role of these conserved domains is not yet fully understood, the structure determination of RNAPII suggests that they cooperate in the formation of a single fold cleft containing the active site of the enzyme (Cramer et al....

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Section: Rnapiva and Rnapivb Act In The Same Pathway And Direct Silenmentioning

confidence: 82%

Section: Rnapiva and Rnapivb Act In The Same Pathway And Direct Silenmentioning

confidence: 98%

Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis

Pontier¹,

Yahubyan²,

Véga³

et al. 2005

Genes Dev.

359

441

View full text Add to dashboard Cite

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“…Recent work has shown that FPA, FCA, and homologs of FLD are also required for the repression of loci that are normally associated with high levels of DNA methylation. In fpa fca double mutants, the expression of both AtSN1 and AtMu1 is up-regulated (Baurle et al, 2007) and mutations in the FLD homologs lsd1-like1 (ldl1) and ldl2 lead to ectopic expression of FWA (Jiang et al, 2007), a gene whose DNA is highly methylated and transcriptionally inactive in the sporophyte (FWA is normally expressed the central cell and in endosperm; Soppe et al, 2000;Kinoshita et al, 2004;Ikeda et al, 2007). In some cases, the activation of these normally silenced loci is accompanied by a decrease in DNA methylation, particularly at asymmetric sites (AtMu1 in fpa fca mutants and FWA in ldl1 and ldl2 mutants), whereas, in other cases (AtSN1 in fpa fca mutants), no change in DNA methylation is observed (Baurle et al, 2007;Jiang et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

Functional Redundancy and New Roles for Genes of the Autonomous Floral-Promotion Pathway

Veley

Michaels

2008

Plant Physiology

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The early-flowering habit of rapid-cycling accessions of Arabidopsis (Arabidopsis thaliana) is, in part, due to the genes of the autonomous floral-promotion pathway (AP). The AP promotes flowering by repressing expression of the floral inhibitor FLOWERING LOCUS C (FLC). AP mutants are therefore late flowering due to elevated levels of FLC, and this late-flowering phenotype is eliminated by loss-of-function mutations in FLC. To further investigate the role of the AP, we created a series of double mutants. In contrast to the phenotypes of single mutants, which are largely limited to delayed flowering, a subset of AP double mutants show a range of defects in growth and development. These phenotypes include reduced size, chlorophyll content, growth rate, and fertility. Unlike the effects of the AP on flowering time, these phenotypes are FLC independent. Recent work has also shown that two AP genes, FCA and FPA, are required for the repression and, in some cases, proper DNA methylation of two transposons. We show that similar effects are seen for all AP genes tested. Microarray analysis of gene expression in AP single and double mutants, however, suggests that the AP is not likely to play a broad role in the repression of gene expression through DNA methylation: very few of the genes that have been reported to be up-regulated in DNA methylation mutants are misexpressed in AP mutants. Together, these data indicate that the genes of the AP play important and sometimes functionally redundant roles in aspects of development in addition to flowering time.A fundamental question in biology is how differentiating cells make decisions between alternative fates. The change from vegetative to reproductive development in Arabidopsis (Arabidopsis thaliana) is an attractive model for studying the factors that regulate such developmental transitions. Early in the life cycle, the undifferentiated stem cells of the shoot apical meristem give rise to organ primordia that will produce the vegetative portions of the plant (e.g. leaves). Later, the shoot apical meristem switches to producing primordia that will form the reproductive organs (e.g. flowers). Proper timing of this transition is critical for successful reproduction. Therefore, plants have evolved mechanisms to regulate flowering in response to both endogenous and environmental factors (Boss et al., 2004). These mechanisms help to ensure that plants flower at a suitable time in their development and a favorable time of year.

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“…Further examples of naturally occurring epialleles are the Colorless nonripening (Cnr) locus in tomato (Manning et al 2006), the transcription factor CmWIP controlling sex determination in melon (Martin et al 2009), the FLOWERING WAGENINGEN (FWA) (Kakutani 1997;Soppe et al 2000;Fujimoto et al 2008Fujimoto et al , 2011 and FOLT1 loci (Durand et al 2012) in Arabidopsis thaliana, and selected SP11 alleles at the complex S locus responsible for self-incompatibility in Brassica rapa (Shiba et al 2006;Tarutani et al 2010). Although no changes in the underlying DNA sequence of the Lcyc and Cnr region have been observed, the epigenetic variants at CmWIP, FWA, FOLT1, and SP11 originate from structural genetic variation.…”

Section: The Molecular Basis Of Epigenetic Variationmentioning

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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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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The Late Flowering Phenotype of fwa Mutants Is Caused by Gain-of-Function Epigenetic Alleles of a Homeodomain Gene

Cited by 535 publications

References 47 publications

Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis

Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis

Functional Redundancy and New Roles for Genes of the Autonomous Floral-Promotion Pathway

Epigenetic Variation, Inheritance, and Selection in Plant Populations

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