Snf2 proteins in plants: gene silencing and beyond

Kniżewski, Łukasz; Ginalski, Krzysztof; Jerzmanowski, Andrzej

doi:10.1016/j.tplants.2008.08.004

Cited by 114 publications

(128 citation statements)

References 80 publications

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“…SYDN and BRMN contain two conserved regions typical of SNF2-type ATPases, a QLQ-rich region and an evolutionarily conserved helicase/SANT-associated (HSA) domain (29,30). The HSA domain of mammalian and yeast SWI2/SNF2 ATPases is important for protein-protein interaction (42).…”

Section: Resultsmentioning

confidence: 99%

“…The chromatin-remodeling ATPases are central catalytic subunits of large multiprotein complexes (27,28). Among the four SWI2/SNF2 ATPases present in the Arabidopsis genome (29), the closely related SPLAYED (SYD) and BRAHMA (BRM) are the best characterized (30,31). Both syd and brm single-mutant flowers have mild and variable floral homeotic defects, yet their role in flower patterning is not well understood (26,32).…”

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confidence: 99%

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SWI2/SNF2 chromatin remodeling ATPases overcome polycomb repression and control floral organ identity with the LEAFY and SEPALLATA3 transcription factors

Sang

Bezhani

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

198

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Patterning of the floral organs is exquisitely controlled and executed by four classes of homeotic regulators. Among these, the class B and class C floral homeotic regulators are of central importance as they specify the male and female reproductive organs. Inappropriate induction of the class B gene APETALA3 (AP3) and the class C gene AGAMOUS (AG) causes reduced reproductive fitness and is prevented by polycomb repression. At the onset of flower patterning, polycomb repression needs to be overcome to allow induction of AP3 and AG and formation of the reproductive organs. We show that the SWI2/SNF2 chromatin-remodeling ATPases SPLAYED (SYD) and BRAHMA (BRM) are redundantly required for flower patterning and for the activation of AP3 and AG. The SWI2/SNF2 ATPases are recruited to the regulatory regions of AP3 and AG during flower development and physically interact with two direct transcriptional activators of class B and class C gene expression, LEAFY (LFY) and SEPALLATA3 (SEP3). SYD and LFY association with the AP3 and AG regulatory loci peaks at the same time during flower patterning, and SYD binding to these loci is compromised in lfy and lfy sep3 mutants. This suggests a mechanism for SWI2/SNF2 ATPase recruitment to these loci at the right stage and in the correct cells. SYD and BRM act as trithorax proteins, and the requirement for SYD and BRM in flower patterning can be overcome by partial loss of polycomb activity in curly leaf (clf) mutants, implicating the SWI2/SNF2 chromatin remodelers in reversal of polycomb repression. P lant development occurs largely postembryonically (1), and, as a consequence, many cell-fate choices do not take place until long after embryogenesis. One example is flower development; in the rapid-flowering winter annual Arabidopsis the first flowers are formed 1 mo to 1 y after germination (2). Precocious activation of the floral homeotic genes required for flower patterning results in pleiotropic defects including poor seed set and is prevented by chromatin repression, which is faithfully inherited throughout cell divisions until the first flowers are formed (3-7). The repressive chromatin needs to be erased for flower patterning to be initiated in flower primordia. For class B genes, such as APETALA3 (AP3), which are required for correct patterning of the showy petals and the male reproductive organs, activation of gene expression occurs in late stage 2 flower primordia in the cells that will give rise to whorls 2 and 3 of the flower (6). For class C gene AGAMOUS (AG), which is required for patterning both the male and the female reproductive organs, induction is observed in early stage 3 flowers in the cells that will give rise to whorls 3 and 4 (6).The mitotically heritable chromatin repression of AP3 and AG before flower formation is achieved by two polycomb complexes: polycomb repressive complex 1 (PRC1) and PRC2. PRC2 is responsible for trimethylation of lysine 27 of histone H3 (H3K27me3) (7,8). Two putative H3K27 methyltransferases and PRC2 complex components, SWINGER and ...

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

SWI2/SNF2 chromatin remodeling ATPases overcome polycomb repression and control floral organ identity with the LEAFY and SEPALLATA3 transcription factors

Sang

Bezhani

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

198

194

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“…The distinctive feature of all CRMs is the presence of a central ATPase, belonging to the SWI2/SNF2 family (Bork and Koonin, 1993;Eisen et al, 1995). The Arabidopsis thaliana genome encodes 41 Snf2-related proteins distributed into six superfamilies, among which the Snf2-like family encompasses the motor subunits for SWI/ SNF complexes (Knizewski et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

“…The chromatin remodeling SWR1/SRCAP complex belongs to a different class of chromatin remodelers than SWI/SNF complexes and relies on the activity of ATPases from the SWR1-like family, comprising INO80 and SWR1 (Knizewski et al, 2008). This complex is involved in the substitution of histone H2A by the histone variant H2A.Z (March-Díaz and Reyes, 2009).…”

Section: Introductionmentioning

confidence: 99%

The BAF60 Subunit of the SWI/SNF Chromatin-Remodeling Complex Directly Controls the Formation of a Gene Loop at FLOWERING LOCUS C in Arabidopsis

et al. 2014

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SWI/SNF complexes mediate ATP-dependent chromatin remodeling to regulate gene expression. Many components of these complexes are evolutionarily conserved, and several subunits of Arabidopsis thaliana SWI/SNF complexes are involved in the control of flowering, a process that depends on the floral repressor FLOWERING LOCUS C (FLC). BAF60 is a SWI/SNF subunit, and in this work, we show that BAF60, via a direct targeting of the floral repressor FLC, induces a change at the highorder chromatin level and represses the photoperiod flowering pathway in Arabidopsis. BAF60 accumulates in the nucleus and controls the formation of the FLC gene loop by modulation of histone density, composition, and posttranslational modification. Physiological analysis of BAF60 RNA interference mutant lines allowed us to propose that this chromatinremodeling protein creates a repressive chromatin configuration at the FLC locus.

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“…Phylogenetic analyses of the SNF2 superfamily in Arabidopsis place the five FRG paralogs in the family of yeast Rad5-and Rad16-related genes (22). Within this family, they show the closest homology to yeast DIS1/RIS1/ULS1, a RING-type E3 ligase that mediates ubiquitylation of small ubiquitin-like modifier-conjugated substrates (29,30) (Fig. S1).…”

Section: Eliminatedmentioning

confidence: 99%

SNF2 chromatin remodeler-family proteins FRG1 and -2 are required for RNA-directed DNA methylation

Groth

Stroud

Feng

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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DNA methylation in Arabidopsis thaliana is maintained by at least four different enzymes: DNA METHYLTRANSFERASE1 (MET1), CHROMO-METHYLASE3 (CMT3), DOMAINS REARRANGED METHYLTRANSFER-ASE2 (DRM2), and CHROMOMETHYLASE2 (CMT2). However, DNA methylation is established exclusively by the enzyme DRM2, which acts in the RNA-directed DNA methylation (RdDM) pathway. Some RdDM components belong to gene families and have partially redundant functions, such as the endoribonucleases DICER-LIKE 2, 3, and 4, and INVOLVED IN DE NOVO2 (IDN2) interactors IDN2-LIKE 1 and 2. Traditional mutagenesis screens usually fail to detect genes if they are redundant, as the loss of one gene can be compensated by a related gene. In an effort to circumvent this issue, we used coexpression data to identify closely related genes that are coregulated with genes in the RdDM pathway. Here we report the discovery of two redundant proteins, SNF2-RING-HELICASE-LIKE1 and -2 (FRG1 and -2) that are putative chromatin modifiers belonging to the SNF2 family of helicase-like proteins. Analysis of genome-wide bisulfite sequencing shows that simultaneous mutations of FRG1 and -2 cause defects in methylation at specific RdDM targeted loci. We also show that FRG1 physically associates with Su(var)3-9-related SUVR2, a known RdDM component, in vivo. Combined, our results identify FRG1 and FRG2 as previously unidentified components of the RdDM machinery.epigenetic | plant C ytosine methylation is an epigenetic mark present in many eukaryotes and is involved in silencing of transposable elements and other repetitive sequences that impose threats to genome integrity. Moreover, DNA methylation in regulatory regions suppresses the expression of genes and disturbances in methylation patterns can lead to developmental defects (1).In the model plant Arabidopsis, DNA methylation occurs at CG, CHG, and CHH sequences (H = A, T, or C) and is maintained through DNA replication by different mechanisms, depending on the sequence context: symmetric CG and CHG methylation are maintained primarily by MET1 and CMT3, respectively, whereas the asymmetric CHH methylation is maintained by either CMT2 or DRM2 (2, 3). Initial DNA methylation establishment-or de novo methylation-in any sequence context is carried out by DRM2 (4, 5). DRM2 is guided to its target loci via a complex pathway known as RNA-directed DNA methylation (RdDM). RdDM depends on the production of both small interfering RNA (siRNA), and overlapping long-noncoding transcripts. According to current knowledge, chromatin-associated proteins, including SAWADEE HOMEODOMAIN HOMOLOG1 (SHH1)/DTF1 and CLASSY1 (CLSY1), recruit and assist RNA POLYMERASE IV (Pol IV), which produces transcripts that are converted to double-stranded RNA by RNA-DEPENDENT RNA POLY-MERASE2 (RDR2) and subsequently cleaved into 24-nt siRNAs by DICER-LIKE3 (DCL3). ARGONAUTE4 (AGO4) binds siRNAs and is recruited to the RNA POLYMERASE V (Pol V) complex, as well as to long noncoding transcripts (lncRNA) produced by Pol V. AGO4 ultimately interacts with DRM2, whi...

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Snf2 proteins in plants: gene silencing and beyond

Cited by 114 publications

References 80 publications

SWI2/SNF2 chromatin remodeling ATPases overcome polycomb repression and control floral organ identity with the LEAFY and SEPALLATA3 transcription factors

SWI2/SNF2 chromatin remodeling ATPases overcome polycomb repression and control floral organ identity with the LEAFY and SEPALLATA3 transcription factors

The BAF60 Subunit of the SWI/SNF Chromatin-Remodeling Complex Directly Controls the Formation of a Gene Loop at FLOWERING LOCUS C in Arabidopsis

SNF2 chromatin remodeler-family proteins FRG1 and -2 are required for RNA-directed DNA methylation

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