Transcriptional Control of a Plant Stem Cell Niche

Busch, Wolfgang; Miotk, Andrej; Ariel, Federico; Zhao, Zhong; Forner, Joachim; Daum, Gabor; Suzaki, Takuya; Schuster, Christoph; Schultheiß, Sebastian J.; Leibfried, Andrea; Haubeiß, Silke; Ha, Nati; Chan, Raquel L.; Lohmann, Jan U.

doi:10.1016/j.devcel.2010.03.012

Cited by 191 publications

(234 citation statements)

References 76 publications

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“…Nonetheless, it is interesting to note that the transcriptional repression functions of both STF and WUS are required to activate cell proliferation. In the Arabidopsis shoot apical meristem, WUS has several direct targets (23), including the well-studied CLAVATA regulatory feedback loop (7), in which WUS directly represses CLV1 (23), and cytokinin signaling, in which WUS directly represses A-type two-component response regulators (24). Whether STF shares any of these regulatory modules to promote cell proliferation in leaf primordia is not known.…”

Section: Discussionmentioning

confidence: 99%

Evolutionarily conserved repressive activity of WOX proteins mediates leaf blade outgrowth and floral organ development in plants

Lin

Niu

McHale

et al. 2012

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

139

180

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The WUSCHEL related homeobox (WOX) genes play key roles in stem cell maintenance, embryonic patterning, and lateral organ development. WOX genes have been categorized into three clades-ancient, intermediate, and modern/WUS-based on phylogenetic analysis, but a functional basis for this classification has not been established. Using the classical bladeless lam1 mutant of Nicotiana sylvestris as a genetic tool, we examined the function of the Medicago truncatula WOX gene, STENOFOLIA (STF), in controlling leaf blade outgrowth. STF and LAM1 are functional orthologs. We found that the introduction of mutations into the WUS-box of STF (STFm1) reduces its ability to complement the lam1 mutant. Fusion of an exogenous repressor domain to STFm1 restores complementation, whereas fusion of an exogenous activator domain to STFm1 enhances the narrow leaf phenotype. These results indicate that transcriptional repressor activity mediated by the WUSbox of STF acts to promote blade outgrowth. With the exception of WOX7, the WUS-box is conserved in the modern clade WOX genes, but is not found in members of the intermediate or ancient clades. Consistent with this, all members of the modern clade except WOX7 can complement the lam1 mutant when expressed using the STF promoter, but members of the intermediate and ancient clades cannot. Furthermore, we found that fusion of either the WUS-box or an exogenous repressor domain to WOX7 or to members of intermediate and ancient WOX clades results in a gain-of-function ability to complement lam1 blade outgrowth. These results suggest that modern clade WOX genes have evolved for repressor activity through acquisition of the WUS-box.T he WUSCHEL related homeobox (WOX) genes form a plantspecific family of the eukaryotic homeobox transcription factor superfamily (1, 2). In Arabidopsis, the WOX family consists of 15 members, including the founding member WUSCHEL (WUS) and WOX1-WOX14 (3), which are involved in the regulation of key developmental processes, including stem cell maintenance in shoot and root meristems, embryo apical-basal polarity patterning, and development of lateral organs (1, 4-7). Based on phylogenetic analysis and their distribution in the plant kingdom, WOX genes have been classified into three clades: modern/WUS (found in seed plants), intermediate (found in vascular plants including lycophytes), and ancient (found in vascular and nonvascular plants, including mosses and green algae) (1,8). WOX genes have been proposed to have a common mechanism of action, as demonstrated by complementation of the wox5 and pressed flower (prs/wox3) mutant phenotypes by WUS, as well as by the partial complementation of prs with WOX4 (5, 9, 10). However, the extent to which the functions of WOX family members are conserved remains unclear.The critical requirement of WOX genes for the development of lateral organs, including leaves and flowers, has become increasingly apparent from the identification of several mutant phenotypes in angiosperms. In maize, the narrowsheath1 and 2 (ns1/ns2) double...

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Section: Discussionmentioning

confidence: 99%

Evolutionarily conserved repressive activity of WOX proteins mediates leaf blade outgrowth and floral organ development in plants

Lin

Niu

McHale

et al. 2012

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

139

180

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“…Furthermore, WUS has been shown to bind cis elements containing TAAT core sequences in the regulatory regions of activated target genes CLV3 (6) and AGAMOUS (24) as well as in the regulatory regions of repressed target genes (14,18,19). However, the mechanisms through which WUS can discriminate between transcriptional activation and repression by using similar cis elements are not understood.…”

Section: Significancementioning

confidence: 99%

“…Several studies have shown that WUS also represses the transcription of many genes (14,18,19), including several differentiationpromoting transcription factors, thus preventing premature differentiation of stem cell descendants (19). The transient transcriptional assays in Arabidopsis leaf protoplasts have shown that WUS can function as both an activator and a repressor (20).…”

mentioning

confidence: 99%

Threshold-dependent transcriptional discrimination underlies stem cell homeostasis

Perales

Rodriguez

Snipes

et al. 2016

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

121

157

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Transcriptional mechanisms that underlie the dose-dependent regulation of gene expression in animal development have been studied extensively. However, the mechanisms of dose-dependent transcriptional regulation in plant development have not been understood. In Arabidopsis shoot apical meristems, WUSCHEL (WUS), a stem cell-promoting transcription factor, accumulates at a higher level in the rib meristem and at a lower level in the central zone where it activates its own negative regulator, CLAVATA3 (CLV3). How WUS regulates CLV3 levels has not been understood. Here we show that WUS binds a group of cis-elements, cis-regulatory module, in the CLV3-regulatory region, with different affinities and conformations, consisting of monomers at lower concentration and as dimers at a higher level. By deleting cis elements, manipulating the WUSbinding affinity and the homodimerization threshold of cis elements, and manipulating WUS levels, we show that the same cis elements mediate both the activation and repression of CLV3 at lower and higher WUS levels, respectively. The concentrationdependent transcriptional discrimination provides a mechanistic framework to explain the regulation of CLV3 levels that is critical for stem cell homeostasis.WUSCHEL | cis-regulatory module | CLAVATA3 | shoot apical meristem | gene regulation

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“…In Arabidopsis, ChIP-chip/Seq has been applied to a range of TFs, primarily those active in flowering and development. Because of the static nature of a ChIP experiment (it is a snapshot of the biological state), the genome-wide profiling of TF-binding sites is often combined with differential expression analysis in a knockout Morohashi and Grotewold, 2009;Busch et al, 2010;Yant et al, 2010) or an inducible overexpression line (Thibaud-Nissen et al, 2006;Kaufmann et al, 2009Kaufmann et al, , 2010Mathieu et al, 2009). By combining these two data types, TF target interactions can be viewed with respect to the expression of both the TF and the target, thus transforming the static ChIP image to a set of dynamic transcriptional modules.…”

mentioning

confidence: 99%

Systematic Identification of Functional Plant Modules through the Integration of Complementary Data Sources

2012

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A major challenge is to unravel how genes interact and are regulated to exert specific biological functions. The integration of genome-wide functional genomics data, followed by the construction of gene networks, provides a powerful approach to identify functional gene modules. Large-scale expression data, functional gene annotations, experimental protein-protein interactions, and transcription factor-target interactions were integrated to delineate modules in Arabidopsis (Arabidopsis thaliana). The different experimental input data sets showed little overlap, demonstrating the advantage of combining multiple data types to study gene function and regulation. In the set of 1,563 modules covering 13,142 genes, most modules displayed strong coexpression, but functional and cis-regulatory coherence was less prevalent. Highly connected hub genes showed a significant enrichment toward embryo lethality and evidence for cross talk between different biological processes. Comparative analysis revealed that 58% of the modules showed conserved coexpression across multiple plants. Using modulebased functional predictions, 5,562 genes were annotated, and an evaluation experiment disclosed that, based on 197 recently experimentally characterized genes, 38.1% of these functions could be inferred through the module context. Examples of confirmed genes of unknown function related to cell wall biogenesis, xylem and phloem pattern formation, cell cycle, hormone stimulus, and circadian rhythm highlight the potential to identify new gene functions. The module-based predictions offer new biological hypotheses for functionally unknown genes in Arabidopsis (1,701 genes) and six other plant species (43,621 genes). Furthermore, the inferred modules provide new insights into the conservation of coexpression and coregulation as well as a starting point for comparative functional annotation.

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Transcriptional Control of a Plant Stem Cell Niche

Cited by 191 publications

References 76 publications

Evolutionarily conserved repressive activity of WOX proteins mediates leaf blade outgrowth and floral organ development in plants

Evolutionarily conserved repressive activity of WOX proteins mediates leaf blade outgrowth and floral organ development in plants

Threshold-dependent transcriptional discrimination underlies stem cell homeostasis

Systematic Identification of Functional Plant Modules through the Integration of Complementary Data Sources

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