Author: klasfeld

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SWI/SNF chromatin remodeling ATPases control accessibility of the information stored in the genome. However, the in vivo role of these remodelers has remained poorly understood because null mutations in these result in embryonic lethality in most organisms. Recently, the study of conditional mutants in mammals and viable null mutants in plants, combined with genome wide expression studies in mammals, flies and plants, have implicated chromatin remodeling ATPases in the regulation of many developmental pathways in multicellular eukaryotes. In addition, these studies reveal striking functional specificity for chromatin remodeling in individual developmental processes.

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R01 gm064650-01/gm/nigmsJournal ArticleResearch Support, N.I.H., ExtramuralResearch Support, Non-U.S. Gov’tReviewEnglandTig

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Chromatin remodeling is emerging as a central mechanism for patterning and differentiation in multicellular eukaryotes. SWI/SNF chromatin remodeling ATPases are conserved in the animal and plant kingdom and regulate transcriptional programs in response to endogenous and exogenous cues. In contrast with their metazoan orthologs, null mutants in two Arabidopsis thaliana SWI/SNF ATPases, BRAHMA (BRM) and SPLAYED (SYD), are viable, facilitating investigation of their role in the organism. Previous analyses revealed that syd and brm null mutants exhibit both similar and distinct developmental defects, yet the functional relationship between the two closely related ATPases is not understood. Another central question is whether these proteins act as general or specific transcriptional regulators. Using global expression studies, double mutant analysis, and protein interaction assays, we find overlapping functions for the two SWI/SNF ATPases. This partial diversification may have allowed expansion of the SWI/SNF ATPase regulatory repertoire, while preserving essential ancestral functions. Moreover, only a small fraction of all genes depends on SYD or BRM for expression, indicating that these SWI/SNF ATPases exhibit remarkable regulatory specificity. Our studies provide a conceptual framework for understanding the role of SWI/SNF chromatin remodeling in regulation of Arabidopsis development.

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1040-4651 (Print)Journal article

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Wang, L-S, Wagner D, Kwon CS, Su Y, Kim J.  2006.  Transcriptional target prediction using qualitative reasoning. Proceedings of the 28th Annual International Conference of the IEEE Engineering in Medicine and Biology Society. :pp.3138-3141.

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The CUP-SHAPED COTYLEDON (CUC) genes CUC1, CUC2 and CUC3 act redundantly to control cotyledon separation in Arabidopsis. In order to identify novel regulators of this process, we have performed a phenotypical enhancer screen using a null allele of cuc2, cuc2-1. We identified three nonsense alleles of AtBRM, an Arabidopsis SWI/SNF chromatin remodeling ATPase, that result in strong cotyledon fusion in cuc2-1. atbrm also enhances cotyledon fusion in loss-of-function cuc1 and cuc3 mutants, suggesting a general requirement for this ATPase in cotyledon separation. By contrast, a null allele of SPLAYED (SYD), the closest homolog of AtBRM in Arabidopsis, enhances only the loss-of-function cuc1 mutant. By investigating the activities of the CUC promoters in the cotyledon boundary during embryogenesis in sensitized backgrounds, we demonstrate that AtBRM upregulates the transcription of all three CUC genes, whereas SYD upregulates the expression of CUC2. Our results uncover a specific role for both chromatin remodeling ATPases in the formation and/or maintenance of boundary cells during embryogenesis.

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0950-1991 (Print)Journal article

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Su, Y, Kwon CS, Bezhani S, Huvermann B, Chen C, Peragine A, Kennedy JF, Wagner D.  2006.  The N-terminal ATPase AT-hook-containing region of the Arabidopsis chromatin-remodeling protein SPLAYED is sufficient for biological activity, May. Plant J. 46:685-99., Number 4

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The SNF2-like chromatin-remodeling ATPase SPLAYED (SYD) was identified as a co-activator of floral homeotic gene expression in Arabidopsis. SYD is also required for meristem maintenance and regulates flowering under a non-inductive photoperiod. SNF2 ATPases are structurally and functionally conserved from yeast to humans. In addition to the conserved protein features, SYD has a large unique C-terminal domain. We show here that SYD is present as two forms in the nucleus, full-length and truncated, with the latter apparently lacking the C-terminal domain. The ratio of the two forms of endogenous SYD differs in juvenile and in adult tissues. Furthermore, an SYD variant lacking the C-terminal domain (SYDDeltaC) rescues the syd null mutant, indicating that the N-terminal ATPase AT-hook-containing region of SYD is sufficient for biological activity. Plants expressing SYDDeltaC show molecular and morphological phenotypes opposite to those of the null mutant, suggesting that the construct results in increased activity. This increased activity is at least in part due to elevated SYD protein levels in these lines. We propose that the C-terminal domain may control SYD accumulation and/or specific activity in the context of the full-length protein. The presence of the C-terminal domain in rice SYD suggests that its role is probably conserved in the two classes of flowering plants.

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0960-7412 (Print)Journal Article

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The timing of the switch from vegetative to reproductive development is crucial for species survival. The plant-specific transcription factor and meristem identity regulator LEAFY (LFY) controls this switch in Arabidopsis, in part via the direct activation of two other meristem identity genes, APETALA1 (AP1) and CAULIFLOWER (CAL). We recently identified five new direct LFY targets as candidates for the missing meristem identity regulators that act downstream of LFY. Here, we demonstrate that one of these, the class I homeodomain leucine-zipper transcription factor LMI1, is a meristem identity regulator. LMI1 acts together with LFY to activate CAL expression. The interaction between LFY, LMI1 and CAL resembles a feed-forward loop transcriptional network motif. LMI1 has additional LFY-independent roles in the formation of simple serrated leaves and in the suppression of bract formation. The temporal and spatial expression of LMI1 supports a role in meristem identity and leaf/bract morphogenesis.

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0950-1991 (Print)Journal article

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SNF2 chromatin-remodeling ATPases play an important role in ensuring proper development in higher eukaryotes by controlling accessibility of cis-regulatory DNA regions to transcription factors and to the transcriptional machinery. However, the biological targets controlled by these ATPases are largely unknown. Using genetic and molecular analyses we have identified WUSCHEL (WUS) as a biologically important target of the SNF2-class ATPase SPLAYED (SYD) in the shoot apical meristem of Arabidopsis. We present evidence that SYD is recruited to the WUS promoter and that it is involved in regulation of the stem cell pool maintenance via direct transcriptional control of this master regulator.

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0890-9369Journal Article

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We have developed a versatile floral induction system that is based on ectopic overexpression of the transcription factor LEAFY (LFY) in callus. During shoot regeneration, flowers or floral organs are formed directly from root explants without prior formation of rosette leaves. Morphological and reporter gene analyses show that leaf-like structures are converted to floral organs in response to LFY activity. Thus, increased levels of LFY activity are sufficient to bypass normal vegetative development and to direct formation of flowers in tissue culture. We found that about half of the cultured cells respond to inducible LFY activity with a rapid upregulation of the known direct target gene of LFY, APETALA1 (AP1). This dramatic increase in the number of LFY-responsive cells compared to whole plants suggested that the tissue culture system could greatly facilitate the analysis of LFY-dependent gene regulation by genomic approaches. To test this, we monitored the gene expression changes that occur in tissue culture after activation of LFY using a flower-specific cDNA microarray. Induction of known LFY target genes was readily detected in these experiments. In addition, several other genes were identified that had not been implicated in signaling downstream of LFY before. Thus, the floral induction system is suitable for the detection of low abundance transcripts whose expression is controlled in an LFY-dependent manner.

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0960-7412Journal Article

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Abstract:

The switch from vegetative to reproductive development in plants necessitates a switch in the developmental program of the descendents of the stem cells in the shoot apical meristem. Genetic and molecular investigations have demonstrated that the plant-specific transcription factor and meristem identity regulator LEAFY (LFY) controls this developmental transition by inducing expression of a second transcription factor, APETALA1, and by regulating the expression of additional, as yet unknown, genes. Here we show that the additional LFY targets include the APETALA1-related factor, CAULI-FLOWER, as well as three transcription factors and two putative signal transduction pathway components. These genes are up-regulated by LFY even when protein synthesis is inhibited and, hence, appear to be direct targets of LFY. Supporting this conclusion, cis-regulatory regions upstream of these genes are bound by LFY in vivo. The newly identified LFY targets likely initiate the transcriptional changes that are required for the switch from vegetative to reproductive development in Arabidopsis.

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0027-8424Journal Article

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