Analysis of the Transcription Factor WUSCHEL and Its Functional Homologue in<i>Antirrhinum</i>Reveals a Potential Mechanism for Their Roles in Meristem Maintenance

Kieffer, Martin; Stern, Yaniv; Cook, Holly; Clerici, Elena; Maulbetsch, Christoph; Laux, Thomas; Davies, Brendan

doi:10.1105/tpc.105.039107

Cited by 203 publications

(209 citation statements)

References 55 publications

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“…The C-terminal region of WUS is necessary for its biological function and includes an acidic region, a WUS box, and an EARlike motif (Kieffer et al, 2006). The EAR motif is a repression domain that is conserved in plants (Ohta et al, 2001), and its presence supported the proposed role of WUS as a repressor.…”

Section: Introductionmentioning

confidence: 90%

“…The C-terminal region of WUS, which is required for WUS activity (Kieffer et al, 2006), contains an acidic region, a WUS box (TLPLFPMH) and an EAR-like (SLELRLN) motif ( Figure 1B). Since the EAR motif is a repression domain that is conserved in plant transcription factors (Ohta et al, 2001), we mutated the EAR-like motif and replaced the two Leu residues in SLELRLN by Ala residues (to yield SLEARAN in a mutant protein designated WUSm2; Figures 1A and 1B).…”

Section: Functional Analysis and Identification Of Functional Domainsmentioning

confidence: 99%

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ArabidopsisWUSCHEL Is a Bifunctional Transcription Factor That Acts as a Repressor in Stem Cell Regulation and as an Activator in Floral Patterning

2009

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Most transcription factors act either as activators or repressors, and no such factors with dual function have been unequivocally identified and characterized in plants. We demonstrate here that the Arabidopsis thaliana protein WUSCHEL (WUS), which regulates the maintenance of stem cell populations in shoot meristems, is a bifunctional transcription factor that acts mainly as a repressor but becomes an activator when involved in the regulation of the AGAMOUS (AG) gene. We show that the WUS box, which is conserved among WOX genes, is the domain that is essential for all the activities of WUS, namely, for regulation of stem cell identity and size of floral meristem. All the known activities of WUS were eliminated by mutation of the WUS box, including the ability of WUS to induce the expression of AG. The mutation of the WUS box was complemented by fusion of an exogenous repression domain, with resultant induction of somatic embryogenesis in roots and expansion of floral meristems as observed upon ectopic expression of WUS. By contrast, fusion of an exogenous activation domain did not result in expanded floral meristems but induced flowers similar to those induced by the ectopic expression of AG. Our results demonstrate that WUS acts mainly as a repressor and that its function changes from that of a repressor to that of an activator in the case of regulation of the expression of AG.

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Section: Introductionmentioning

confidence: 90%

Section: Functional Analysis and Identification Of Functional Domainsmentioning

confidence: 99%

ArabidopsisWUSCHEL Is a Bifunctional Transcription Factor That Acts as a Repressor in Stem Cell Regulation and as an Activator in Floral Patterning

2009

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“…In addition to specifying stamen and carpel identities, Arabidopsis AG controls floral determinacy by repressing the expression of WUS, a gene that maintains stem cell fates (Laux et al 1996;Schoof et al 2000;Lenhard et al 2001;Lohmann et al 2001;Baurle and Laux 2005;Kieffer et al 2006). To determine if the loss of floral determinacy in 35S∷AP2m3 lines could be due to reduced expression of NbAG, we identified NbAG and studied its mRNA levels by semi-quantitative RT-PCR (Fig.…”

Section: Arabidopsis Ap2 Induces Floral Patterning Defects In N Bentmentioning

confidence: 99%

Floral patterning defects induced by Arabidopsis APETALA2 and microRNA172 expression in Nicotiana benthamiana

et al. 2006

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Floral patterning and morphogenesis are controlled by many transcription factors including floral homeotic proteins, by which floral organ identity is determined. Recent studies have uncovered widespread regulation of transcription factors by microRNAs (miRNAs), ~21-nucleotide noncoding RNAs that regulate protein-coding RNAs through transcript cleavage and/or translational inhibition. The regulation of the floral homeotic gene APETALA2 (AP2) by miR172 is crucial for normal Arabidopsis flower development and is likely to be conserved across plant species. Here we probe the activity of the AP2/miR172 regulatory circuit in a heterologous Solanaceae species, Nicotiana benthamiana. We generated transgenic N. benthamiana lines expressing Arabidopsis wild type AP2 (35S∷AP2), miR172-resistant AP2 mutant (35S∷AP2m3) and MIR172a-1 (35S∷MIR172) under the control of the cauliflower mosaic virus 35S promoter. 35S∷AP2m3 plants accumulated high levels of AP2 mRNA and protein and exhibited floral patterning defects that included proliferation of numerous petals, stamens and carpels indicating loss of floral determinacy. On the other hand, nearly all 35S∷AP2 plants accumulated barely detectable levels of AP2 mRNA or protein and were essentially non-phenotypic. Overall, the data indicated that expression of the wild type Arabidopsis AP2 transgene was repressed at the mRNA level by an endogenous N. benthamiana miR172 homologue that could be detected using Arabidopsis miR172 probe. Interestingly, 35S∷MIR172 plants had sepal-to-petal transformations and/or more sepals and petals, suggesting interference with N. benthamiana normal floral homeotic gene function in perianth organs. Our studies uncover the potential utility of the Arabidopsis AP2/miR172 system as a tool for manipulation of floral architecture and flowering time in non-model plants.

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“…These genes are involved in regulating embryonic shoot-root axis determination and appear to repress auxin-mediated signaling events during embryogenesis (Szemenyei et al, 2008). The TPL/WSIP genes are also involved in mediating the effect of WUSCHEL in target gene repression to maintain the stem cell pool at the shoot apical meristem (Kieffer et al, 2006). Therefore, the plant Gro/Tup1 family corepressors are emerging as a fundamentally important class of regulators in plant development.…”

mentioning

confidence: 99%

“…In Arabidopsis, LUG belongs to a small family of about 13 genes (http://smart.embl-heidelberg.de/), including TOPLESS (TPL), TOPLESS-RELATED, and WUSCHEL-INTERACTING PROTEINs (WSIPs; Kieffer et al, 2006;Long et al, 2006;Liu and Karmarkar, 2008). These genes are involved in regulating embryonic shoot-root axis determination and appear to repress auxin-mediated signaling events during embryogenesis (Szemenyei et al, 2008).…”

mentioning

confidence: 99%

LEUNIG_HOMOLOGandLEUNIGPerform Partially Redundant Functions during Arabidopsis Embryo and Floral Development

2008

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Transcription corepressors play important roles in animal and plant development. In Arabidopsis (Arabidopsis thaliana), LEUNIG (LUG) and LEUNIG_HOMOLOG (LUH ) encode two highly homologous proteins that are similar to the animal and fungal Gro/Tup1-type corepressors. LUG was previously shown to form a putative corepressor complex with another protein, SEUSS (SEU), and to repress the transcription of AGAMOUS in floral organ identity specification. However, the function of LUH is completely unknown. Here, we show that single luh loss-of-function mutants develop normal flowers, but lug; luh double mutants are embryo lethal, uncovering a previously unknown function of LUG and LUH in embryonic development. In addition, luh/1 enhances the floral phenotype of lug, revealing a minor role of LUH in flower development. Functional diversification between LUH and LUG is evidenced by the inability of 35STLUH overexpression to rescue lug mutants and by the opposite expression trends of LUG and LUH in response to biotic and abiotic stresses. The luh-1 mutation does not enhance the defect of seu in flower development, but LUH could directly interact with SEU in yeast. We propose a model that explains the complex relationships among LUH, LUG, and SEU. As most eukaryotes have undergone at least one round of whole-genome duplication during evolution, gene duplication and functional diversification are important issues to consider in uncovering gene function. Our study provides important insights into the complexity in the relationship between two highly homologous paralogous genes.

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Analysis of the Transcription Factor WUSCHEL and Its Functional Homologue inAntirrhinumReveals a Potential Mechanism for Their Roles in Meristem Maintenance

Cited by 203 publications

References 55 publications

ArabidopsisWUSCHEL Is a Bifunctional Transcription Factor That Acts as a Repressor in Stem Cell Regulation and as an Activator in Floral Patterning

ArabidopsisWUSCHEL Is a Bifunctional Transcription Factor That Acts as a Repressor in Stem Cell Regulation and as an Activator in Floral Patterning

Floral patterning defects induced by Arabidopsis APETALA2 and microRNA172 expression in Nicotiana benthamiana

LEUNIG_HOMOLOGandLEUNIGPerform Partially Redundant Functions during Arabidopsis Embryo and Floral Development

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