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Plant Signal Behav. Jan 1, 2012; 7(1): 86–92.
PMCID: PMC3357377

Diverse roles of Groucho/Tup1 co-repressors in plant growth and development

Abstract

Transcriptional regulation involves coordinated and often complex interactions between activators and repressors that together dictate the temporal and spatial activity of target genes. While the study of developmental regulation has often focused on positively acting transcription factors, it is becoming increasingly clear that transcriptional repression is a key regulatory mechanism underpinning many developmental processes in both plants and animals. In this review, we focus on the plant Groucho (Gro)/Tup1-like co-repressors and discuss their roles in establishing the apical-basal axis of the developing embryo, maintaining the stem cell population in the shoot apex and determining floral organ identity. As well as being developmental regulators, recent studies have shown that these co-repressors play a central role in regulating auxin and jasmonate signaling pathways and are also linked to the regulation of pectin structure in the seed coat. These latest findings point to the Gro/Tup1-like co-repressors playing a much broader role in plant growth and development than previously thought, an observation that underlines the central importance of transcriptional repression in plant gene regulation.

Introduction

Plants, like other organisms, employ both transcriptional and post-transcriptional mechanisms to generate precise patterns of gene expression in response to developmental cues and environmental fluctuations. At the transcriptional level, spatio-temporal patterns of gene activity are largely determined by the recruitment of activators and repressors to cis-sites of target genes. In animal systems, the role of transcriptional repression or context-specific switching between activation and repression has long been recognized as a key mechanism underpinning developmental regulation.1 Recent studies in plants have also established the importance of this mode of transcriptional control during various developmental processes, with many plant proteins employing similar regulatory mechanisms to those observed in animal systems.

Repressors can be broadly categorized according to whether they bind DNA directly, or, as is the case with co-repressors, indirectly via physical interactions with DNA-binding co-factors. Differences are also apparent in their mode of repression, with some repressors actively regulating transcription, while others function passively. Passive interference occurs when a repressor competes with an activator for a shared binding site within a regulatory element. Alternatively, it may form an inactive heterodimer with an activator. In contrast, active repression involves the repressor directly inhibiting transcription through interactions with either the basal transcriptional machinery or positively acting transcription factors. Repressors may also function by recruiting chromatin-modifying enzymes such as histone deacetylases (HDACs) to target loci. The resulting change in chromatin state may limit or prevent positively acting regulators from reaching their target cis-elements, leading to reduced transcriptional activity of the target gene.

The Groucho/Tup1 Family of Co-repressors

The Groucho/Tup1 family of co-repressors is an evolutionarily conserved group of regulators found in animals, plants and fungi, which all share a similar domain structure and mechanism of action. As co-repressors, they lack intrinsic DNA-binding activity, instead relying on interactions with DNA-binding cofactors to ensure their recruitment to the regulatory elements of target genes. The Drosophila protein Groucho (Gro) was the first metazoan co-repressor to be identified and, like its mammalian Transducin-Like Enhancer of split (TLE) homologs, has a characteristic N-terminal glutamine (Q)-rich domain and a C-terminal region containing multiple ~40 amino acid repeats enriched for tryptophan (W) and aspartate (D). The WD-40 repeats form a distinctive β-propeller structure that facilitates protein–protein interactions, whereas the Q-rich domain is linked to homotetramerization. Separating these domains is a less-conserved region that is associated with the recruitment of histone-modifying enzymes.2

Although the yeast co-repressor Tup1 has only the WD-40 repeats in common with Gro (Fig. 1), similarities in domain organization and mechanisms of repression suggest that these proteins perform analogous functions.3 In most cases, interaction of Tup1 tetramers with transcription factors requires Ssn6, an adaptor protein that can simultaneously bind to the N-terminal region of Tup1 as well as to a range of DNA-binding co-factors.4 The resulting Tup1-Ssn6 complex targets ~3% of the total number of genes in the yeast genome, many of which are regulated in response to altered growth conditions.5,6

figure psb-7-86-g1
Figure 1. Domain organization of Gro, Tup1, LUG and TPL co-repressors. All four proteins contain C-terminal WD-40 repeats (green) but have different conserved N-terminal domains. LUG and TPL both contain an N-terminal LisH motif (gold), but in ...

In Arabidopsis, Gro/Tup1 co-repressors form a small family that includes the closely related LEUNIG (LUG) and LEUNIG_HOMOLOG (LUH), TOPLESS (TPL) and the TOPLESS-RELATED (TPR1–4) proteins, and several uncharacterised proteins.7 While C-terminal WD-40 repeats and an N-terminal LisH (lissencephaly homology) domain are common to all members of this family, substantial differences outside of these regions distinguish LUG/LUH from TPL/TPRs (Fig. 1). For example, TPL/TPR proteins contain central as well as C-terminal WD-40 repeats and a conserved C-terminal to LisH (CTLH) domain, which are not present in LUG/LUH,8 while the central region of LUG and LUH lacks any distinguishable motifs but has multiple Q-rich regions.9

Role of LUG in Regulating Floral Organ Identity

LUG was first identified in a screen looking for second-site enhancers of the floral homeotic mutant apetala2 (ap2).10 As well as enhancing ap2, lug single mutant flowers display partial homeotic transformations of organs in whorl 1 (sepals) and whorl 2 (petals). While these transformations are correlated with ectopic expression of several floral homeotic genes, genetic analysis points to the class C gene AGAMOUS (AG) being the main factor repressed by LUG in the outer whorls of the flower.10 Cloning of LUG identified it as the founding member of the Gro/Tup1 family of co-repressors in plants, which is consistent with the protein functioning as a transcriptional repressor.11 Somewhat counter-intuitively, LUG is expressed in the inner AG-expressing floral whorls, as well as the outer whorls. To reconcile this observation, it has been suggested that whorl-specific factors are required for LUG-mediated repression of AG in the outer whorls of the developing flower.11

In addition to the characteristic C-terminal WD-40 repeats found in all Gro/Tup1 proteins, both LUG and the closely related LUH possess an N-terminal LUFS (named after LUG, LUH, the yeast Flo8, and human SSDP) domain that is not found in TPL/TPR co-repressors. This domain is required for physical interaction with SEUSS (SEU), a Q-rich adaptor protein that together with the related SEUSS-LIKEs (SLK1–3), links LUG/LUH to specific transcription factors in the same way that Ssn6 recruits Tup1 to its targets in yeast.12

Studies investigating SEU function have shown that it binds to the transcription factors SEPALLATA3 (SEP3) and APETALA1 (AP1), and that these interactions direct LUG to a regulatory sequence present in the second intron of AG (Fig. 2A).13 Subsequent studies have also implicated the floral regulators AGAMOUS-LIKE 24 (AGL24) and SHORT VEGETATIVE PHASE (SVP) in this recruitment, as they form dimers with AP1 and together bind to LUG-SEU.14 While AP1 expression is limited to the outer two whorls of the flower due to the repressive activity of AG,15 SEP3 accumulates in the inner whorls along with LUG. While the LUG-SEU-SEP3 complex is presumably formed in these tissues, it has been argued that the strong AG activators LEAFY (LFY), WUSCHEL (WUS) and the autoregulatory SEP3-AG complex successfully antagonise LUG function in these whorls.13

figure psb-7-86-g2
Figure 2. Roles of LUG in regulation of floral organ identity through class A–class C antagonism. (A) In whorls 1 and 2, interactions with API-AGL24/SVP and SEP3 recruit LUG-SEU to the regulatory region of intron II in AG, a C function ...

A recent study has expanded the role of LUG in floral patterning to include the regulation of miR172, a microRNA that targets the class A floral organ identity gene AP2.16 Although AP2 is expressed in all four floral whorls, AP2 protein accumulates only in the first and second whorls, whereas miR172 expression is only detected in the inner whorls.17 Analysis of AP2 and miR172 regulation has revealed that their complementary expression patterns are the product of mutual repression. For instance, interactions between AP2 and SEU lead to the recruitment of LUG to regulatory elements of miR172 loci, resulting in miR172 repression in the outer whorls. In the inner whorls, AP2 accumulation and activity is prevented by miR172-mediated post-transcriptional repression (Fig. 2B).16 In both cases, self-reinforcing feedback loops maintain AP2 and miR172 expression in their respective whorls, although how this pattern is initially established has not yet been resolved. Interestingly, AP2 is known to directly repress AG expression,17,18 although at present it is not known if LUG and SEU are required for this repressive activity.

Based on these studies, LUG is clearly part of the regulatory machinery that establishes mutual antagonism between class A and C homeotic genes within the developing flower, as it directly represses the class C gene AG and indirectly promotes accumulation of the class A protein AP2 via repression of miR172 in outer whorl organs. While the precise mechanism involved in AG and miR172 repression has yet to be resolved, genetic and in vitro studies together with pharmacological data point to LUG functioning through recruitment of histone deacetylases (HDACs);12,19,20 thus, one mechanism of LUG-mediated repression involves the formation of repressive chromatin. In addition, physical interactions observed between LUG and components of the Mediator complex suggest that LUG may also influence transcription directly by preventing RNA Pol II recruitment to target promoters.19 Future studies will no doubt address whether these two mechanisms operate sequentially or independently and to what extent the target dictates the mechanism involved in repression.

Redundant Functions of LUG and LUH in Vegetative Development

In order to determine the extent of redundancy between LUG and the closely related LUH, several studies have attempted to generate lug luh double mutants. Where crosses involved strong or null lug and luh alleles, the resulting double mutants were embryonic lethal, suggesting that these co-repressors are redundant regulators of early embryonic development.9,21 Despite the lack of viable double mutants, plant homozygous for lug and heterozygous for luh (lug luh/+) display numerous vegetative and floral defects not apparent in lug single mutants.9,21 Haploinsufficiency of LUH in a lug mutant background is consistent with these genes regulating overlapping pathways during post-embryonic development, and thus functioning redundantly to some extent. Since many of the developmental defects observed in lug luh/+ mutants are further exacerbated when the activity of vegetatively expressed YABBYs (YABs) is reduced, it has been proposed that LUG/LUH function in the YAB pathway.21,22 Consistent with this possibility, physical interactions between YAB transcription factors and LUG, LUH, SEU and SLKs imply that a LUG-SEU-YAB complex is formed in plants.21,22 As YAB expression is exclusively confined to the abaxial (lower) side of developing leaves,23 it seems likely that some functions of the LUG-SEU-YAB complex, particularly those promoting shoot apical meristem (SAM) activity, involve the regulation of cell signaling pathways.21 Although further work is still needed to characterize these pathways, LATERAL SUPPRESSOR (LAS), a GRAS protein expressed in the boundary region between organ primordia and the SAM, has recently been implicated in relaying YAB signals to the meristem.23

LUH Regulates Pectin Structure

In a surprising departure from developmental regulation, a pair of recent publications has identified a role for LUH in regulating pectin structure.24,25 Pectin is a complex polysaccharide that is found predominantly in the plant cell wall along with cellulose and hemicellulose. It is also the main component of mucilage, a gelatinous substance released from the epidermal cells of the mature Arabidopsis seed coat following contact with water.26,27 A link between LUH and pectin was established following the discovery that imbibed luh seeds fail to release mucilage.24,25 This extrusion defect was not caused by a failure to produce mucilage, as examination of developing luh seeds revealed normal mucilage synthesis and secretion by the epidermal cells of the seed coat.25,28 However, examination of mucilage release following chemical weakening of the cell wall of the luh seed coat clearly demonstrated a reduced capacity to swell. As swelling of the mucilage generates the force necessary to rupture the epidermal cell wall of the seed coat, it is likely that the altered hydration properties of luh mucilage account for its failure to be released from the seed.24,25 Analysis of luh pectin structure in extracted mucilage identified an increase in the number of single galactose residues attached to the pectin backbone; this change is also observed in mucilage extracted from mutants lacking activity of the β-galactosidase MUCILAGE MODIFIED 2 (MUM2).29,30 This similarity, together with the observation that MUM2 expression is dramatically reduced in the developing seed coat of luh mutants, suggests that LUH is a positive regulator of MUM2. As LUG and LUH are both thought to function as repressors,9 this regulation is presumably indirect, with LUH targeting a repressor that limits MUM2 expression. According to this model luh mutants have increased activity of the MUM2 repressor, which in turn reduces MUM2 expression.25 This regulatory relationship is similar to that observed between LUG and AP2, where LUG regulates the AP2 repressor miR172.16 An alternative and somewhat more speculative possibility is that LUH functions as a transcriptional activator, directly promoting MUM2 expression in the seed coat.24 While transactivation assays support this possibility,24 the activation properties of LUH have not been unequivocally demonstrated in planta.

Role of TPL and TPRs in Apical-Basal Fate Determination

TPL and TPRs constitute the other characterized group of Gro/Tup1-like co-repressors in plants. Their role in development was first established through the characterization of the temperature-sensitive, dominant negative tpl-1 mutation. When grown at the non-permissive temperature of 29°C, tpl-1 mutants display a dramatic homeotic conversion leading to the entire embryonic apical pole (shoot) being replaced with a second basal pole (root).31 This phenotype can be recapitulated only when the activity of TPL and all four TPRs is abolished, indicating that tpl-1 probably encodes a protein that dominantly suppresses the activity of all family members.32 These observations suggest that the apical and basal-promoting pathways are mutually exclusive, and that loss of TPL/TPR activity causes a complete shift from a shoot- to a root-promoting pathway.

Like the other members of the plant Gro/Tup1-like co-repressor family, TPL/TPRs are thought to act through histone modification. Genetic analysis has shown that the tpl-1 mutant phenotype can be enhanced by mutations in HISTONE DEACETYLASE19 (HDA19), which itself displays a tpl-1-like phenotype when grown at 29°C.32 In addition, TPR1 has been shown to directly bind to HDA19 in vivo.33 Conversely, mutations in histone acetyl transferase GCN5 suppress the shoot-root transformations observed in tpl-1 mutants when grown at a non-permissive temperature.32

As the root-promoting PLETHORA genes (PLT1 and 2) are misexpressed in tpl-1 embryos, it has been proposed that the TPL/TPR co-repressors prevent the activity of these master regulators in the apical region of the embryo.34 Interestingly, recent studies suggest that TPL/TPRs achieve this through multiple pathways: TPL has been shown to bind sites in the promoters of PLT1 and PLT2 indicating that it represses them directly,34 but TPL also appears to affect PLT expression via a separate, auxin-regulated pathway.

During early embryogenesis, basal accumulation of auxin triggers root specification,35 a process that is critically dependent on the transcription factor MONOPTEROS (MP).36,37 MP is a member of the AUXIN RESPONSE FACTOR (ARF) family and activates gene expression in response to auxin,38 but under low auxin conditions its activity is inhibited by physical interaction with BODENLOS (BDL), a member of the AUX/IAA family of transcriptional repressors.39,40 Since auxin triggers ubiquitination and proteolytic cleavage of AUX/IAA proteins,41 it has been proposed that accumulation of auxin at the basal pole frees MP from the repressive activity of BDL and allows it to activate a root developmental program (Fig. 3A and C).42 TPL has been implicated in this system based on the observations that it physically interacts with BDL and is required for the repressive activity of BDL.43 While PLT expression is dependent on ARF activity, and in particular on MP,44 this regulation is likely to be indirect, since MP/BDL are thought to regulate root initiation genes in a non-cell-autonomous manner through intercellular signaling.42,45 Consistent with this idea is the observation that auxin-induced PLT expression occurs significantly later than that of primary auxin response genes.44 Thus, TPL/TPRs may regulate PLT expression both through auxin signaling and through direct repression.

figure psb-7-86-g3
Figure 3. Roles of TPL in regulation of auxin- and jasmonate-induced gene expression. (A and B) Under low hormone conditions, TPL is recruited to the promoters of auxin- or jasmonate-induced genes through interaction with repressor proteins (BDL ...

Interestingly, the interaction between the TPL co-repressor and BDL occurs through the CTLH domain of TPL and the ERF-associated amphiphilic repression (EAR) domain of BDL, a region common to all AUX/IAA proteins.46 If the mechanism of BDL-mediated repression is extended to other AUX/IAAs, it seems likely that TPL/TPRs will be involved in many other auxin-related processes.

Role of TPL and TPRs in Jasmonate Signaling

The TPL/TPR family has also recently been implicated in jasmonate signaling, which has roles in pathogen defense and developmental regulation.47,48 Mechanistically, jasmonate signaling has a striking similarity to auxin signaling pathways, with jasmonate ZIM-domain (JAZ) transcriptional repressors binding to the transcription factors MYC2–4 to form inactive complexes under low jasmonate conditions.49-52 Elevation of jasmonate levels induces degradation of the JAZ repressors, thereby allowing jasmonate-responsive genes to be activated (Fig. 3B, D).49,52 Like BDL, JAZ proteins repress their target genes through recruitment of TPL/TPRs, although in this case the interaction is mediated by the adaptor protein NOVEL INTERACTOR OF JAZ (NINJA).53 Like the AUX/IAAs, NINJA possesses an EAR motif, and it is required for the interaction with TPL.53

Interactions between TPL/TPRs and the Shoot Apical Meristem Regulator WUSCHEL

The EAR motif is conserved in plants54 and is found in over 20 different families of transcriptional regulators in Arabidopsis,55 suggesting that TPL/TPRs are likely to have widespread functions. One such EAR motif-containing protein is the homeodomain transcription factor WUSCHEL (WUS),54 a key regulator of stem cell identity that is expressed in the organizing center located beneath the stem cells of the shoot apical meristem. As a master regulator of stem cell specification, WUS activity needs to be tightly regulated to ensure the size of the stem cell pool is stably maintained throughout the life of the plant. This is achieved through a negative feedback loop in which CLAVATA signaling restricts WUS expression to the organizing center.56,57

TPL and TPR4 were identified as WUS-interacting proteins in yeast two-hybrid screens, raising the possibility that TPL/TPRs are involved in the stem cell-promoting activity of WUS.8 This hypothesis is supported by the observation that chemical inhibition of HDAC activity in wild-type plants induces meristem defects similar to those seen in wus mutants. As TPL/TPRs are known to function via HDAC-mediated chromatin modification, the meristem defect of these plants may arise from the inability of TPL/TPRs to function correctly.8 Furthermore, WUS truncations that lack the EAR domain, and are thus unable to recruit TPL/TPRs, produce a dominant meristem termination phenotype when expressed in plants. A possible explanation for this termination phenotype is that the truncated protein interferes with TPL/TPR-mediated repression of target genes associated with meristem termination. Candidates for these target genes include the cytokinin-induced type A ARABIDOPSIS RESPONSE REGULATOR (ARR) genes, which function as negative regulators of cytokinin signaling.58 It is therefore possible that repression of ARRs depends on the recruitment of TPL/TPR co-repressors.7 Alternatively, WUS-TPL/TPR interactions may point to a role for auxin signaling in regulating SAM function.

Interestingly, WUS appears to function as an activator as well as a repressor, depending on the regulatory target and/or cellular context,59,60 and a similar situation appears to hold for AP2.18 It is therefore likely that this switch between positive and negative regulation is mediated by context-dependent recruitment of co-repressors, although further work is needed to clarify how this is achieved.

TPR1 Regulates Plant Immune Responses

An additional role for TPR1 has recently been identified in immune responses, after tpr1 was found to act as a suppressor of the constitutively active disease resistance gene snc1.33 SNC1 and TPR1 were subsequently shown to physically associate in vivo, and both function to repress downstream genes that are themselves negative regulators of immunity. Consistent with these observations, increased TPR1 activity results in constitutive activation of defense responses, whereas tpl tpr1 tpr4 triple mutants are less resistant to a number of pathogens. These observations support the idea that Gro/Tup1-like co-repressors are not solely involved in developmental regulation but control a broad spectrum of processes in the plant.

Conclusion

The emerging picture of plant Gro/Tup1-like co-repressors is that they function as global regulators involved in both developmental processes and responses to biotic and abiotic stress. Mechanistically, the common mode of transcriptional repression exhibited by proteins in this family, i.e., recruitment of histone-modifying enzymes, is likely to correspond to the high degree of sequence similarity in the WD-40 repeat domains, while the ability to interact with different co-factors and thus to regulate divergent targets is due to differences in the N-terminal domain.

Although interaction partners of LUG/LUH and TPL/TPRs have been identified, there are undoubtedly many more that remain unknown; similarly, only a small number of genes targeted by the co-repressor have been identified. In coming years, the widespread application of yeast two-hybrid screening, co-immunoprecipitation, chromatin immunoprecipitation and microarray analysis will provide further insight into the function of the plant Gro/Tup1 co-repressors by providing answers to how these global regulators achieve specificity. The involvement of multiple additional proteins, such as SEU/SLKs and YABs, or NINJA, JAZ proteins and MYC2, suggests that the differential expression and/or activity of these proteins is likely to mediate the recruitment of co-repressors to different regulatory targets according to the specific developmental or cellular contexts. It is also possible that co-repressor activity can be altered through post-translational modifications such as phosphorylation and sumoylation. While these modifications affect the binding properties of Gro/Tup1 proteins in animals and fungi,61-64 it is presently not clear whether such mechanisms are also used to control plant co-repressor activity.

The variety of pathways in which they function can make it difficult to study the roles of LUG/LUH and TPL/TPRs in specific processes, but increased knowledge about their interaction partners and targets will assist with this and ultimately expand our understanding of this important group of transcriptional regulators.

Acknowledgments

We thank members of the Golz lab for their critical comments of the manuscript. J.E.L is supported by an Elizabeth and Vernon Puzey Postgraduate Scholarship.

Footnotes

References

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