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First published online August 17, 2007; 10.1104/pp.107.104794 Plant Physiology 145:1031-1042 (2007) © 2007 American Society of Plant Biologists OPEN ACCESS ARTICLE
Genetic and Molecular Regulation by DELLA Proteins of Trichome Development in Arabidopsis1,[W],[OA]Centre for Novel Agricultural Products, Department of Biology, University of York, York YO10 5YW, United Kingdom (Y.G., P.B.); Department of Biological Sciences and Temasek Life Sciences Laboratory, National University of Singapore, Singapore 117543 (H.Y.); and Functional Genomics Laboratory, Institute of Molecular and Cell Biology, Protesos, Singapore 138673 (J.P.)
Gibberellins (GA) are known to influence phase change in Arabidopsis (Arabidopsis thaliana) as well as the development of trichomes, which are faithful epidermal markers of shoot maturation. They modulate these developmental programs in part by antagonizing DELLA repressors of growth, GIBBERELLIC ACID INSENSITIVE (GAI) and REPRESSOR OF ga1-3 (RGA). In this study, we have probed the relative roles played by RGA, GAI, and two homologs, RGA-LIKE1 (RGL1) and RGL2, in these processes and investigated molecular mechanisms through which they influence epidermal differentiation. We found that the DELLAs act collectively to regulate trichome initiation on all aerial organs and that the onset of their activity is accompanied by the repression of most genes known to regulate trichome production. These effects are consistent with the results of genetic analysis, which conclusively place theses genes downstream of the DELLAs. We find that repression of trichome regulatory genes is rapid, but involves an indirect, rather than a direct, molecular mechanism, which requires de novo protein synthesis. DELLA activity also influences postinitiation events and we show that GAI is a major repressor of trichome branching, a role in which it is antagonized by RGL1 and RGL2. Finally, we report that, in contrast to most other effects, the repression by GA applications of flower trichome initiation is not dependent on RGA, GAI, RGL1, or RGL2. In summary, our data show that DELLA proteins are central to trichome development in Arabidopsis and that their effect can be largely explained by their transcriptional influence on trichome initiation activators.
The initiation of trichomes, which are large unicellular epidermal structures on the aerial organs of many plant species, has long been a model for the study of cell-fate determination in plants. In Arabidopsis (Arabidopsis thaliana), trichomes decorate stems, sepals, and leaves, where they first appear on the adaxial side, early in leaf development (Larkin et al., 1994  ; Hülskamp et al., 1999). Genetic analyses have identified at least three regulatory proteins that promote trichome initiation: GLABROUS1 (GL1), an R2R3-Myb-type transcription factor; TRANSPARENT TESTA GLABRA1 (TTG1), a protein containing WD-40 repeats; and GLABRA3 (GL3), a basic helix-loop-helix-type transcription factor. Loss-of-function mutations in the GL1 and TTG1 genes nearly abolish trichome initiation on leaves (Larkin et al., 1994; Walker et al., 1999; Payne et al., 2000). GL3 has been shown to self-associate and assemble with GL1 and TTG1 in yeast (Saccharomyces cerevisiae) two-hybrid experiments, but GL1 and TTG1 are not known to interact (Larkin et al., 1994; Walker et al., 1999; Payne et al., 2000; Zhang et al., 2003).
Trichome initiation is dependent on GA signaling in Arabidopsis: The GA biosynthesis mutant ga1-3 is almost completely glabrous and GA applications stimulate initiation in both ga1-3 and wild-type plants (Chien and Sussex, 1996
RGA and GAI are known to repress trichome formation on leaves because loss-of-function mutations in RGA and GAI can rescue leaf trichome initiation in ga1-3 mutants (Dill and Sun, 2001 In this study, we have used a combination of DELLA loss-of-function mutants and inducible overexpressors to examine these issues. We found that the different repressors act synergistically in the control of trichome development, but that specific DELLA proteins play predominant roles in the control of either initiation or branching. We also found that the effect of DELLA repression is associated with profound changes in the expression of trichome initiation regulators, which are an indirect, rather than a direct, consequence of DELLA action.
DELLA Proteins Act as Repressors of Most Known Positive Regulators of Trichome Initiation in Arabidopsis
In GA-treated plants, higher trichome production is associated with the induction of GIS, ZFP8, and GIS2 and with an increase in the expression of GL1, which is itself dependent on GIS activity. In addition, GL1 and GIS are strongly down-regulated in the ga1-3 mutant (Perazza et al., 1998 We first compared the levels of TTG1, GL3, ZFP8, and GIS2 expression in ga1-3 and in wild-type plants. We found that decreased GA levels in the mutant resulted in the down-regulation of GL3, ZFP8, and GIS2, but that the expression of TTG1 was not affected (Supplemental Fig. S1). This response indicated that reductions in GA signaling negatively impact the expression of multiple genes encoding regulators of trichome initiation. To assess the role played by DELLA proteins in this transcriptional response, we examined the effects of loss-of-function mutations in RGA, GAI, RGL1, and RGL2 on the expression of GL1, GL3, GIS, ZFP8, and GIS2 in the ga1-3 background (Fig. 1 ). We found that, in every case, loss of all DELLA function restored gene expression to wild-type levels or higher, which indicated that, collectively, DELLA repressors play a prominent role in the regulation of these genes by GA. Whereas the impact of DELLA activity on gene expression was generally similar to its effects on trichome initiation, DELLA proteins differed in their overall influence and in their effects on individual genes. For example, RGA loss of function strongly stimulated the expression of GL1, GL3, GIS, and ZFP8, but had little effect on GIS2 expression. GIS2 was only significantly induced when the functions of both RGA and GAI were abolished (Fig. 1). Similarly, the combination of gai-t6, rgl1, and rgl2 mutations strongly promoted ZFP8 expression, but not expression of other genes. The influence of RGL1 and RGL2 on gene expression was clearly detectable in the case of GL1 and ZFP8, although it was most marked when the function of other DELLA proteins had been abolished. Similarly, loss-of-function mutations in both RGL1 and RGL2 boosted GL3 expression above wild-type levels, but only if both RGA and GAI had been knocked out. In all other cases, the influence of individual DELLA proteins was limited and dependent on the activity of all the others (Fig. 1).
In summary, our findings indicated that DELLA proteins are essential in the control by GA of the expression of genes encoding activators of trichome initiation. They also suggested that, whereas RGA generally plays a predominant role in this process, GAI, RGL1, and RGL2 also participate, sometimes in a critical way, in the regulation of downstream gene expression.
To further investigate regulation by DELLA proteins of downstream regulators and, in particular, assess whether their role in this process is direct or indirect, we examined the expression of GL1, GL3, GIS, GIS2, and ZFP8 in DELLA mutants that overexpress RGA-GR, which encodes a functional fusion of RGA to the receptor domain of the rat glucocorticoid receptor. In these plants, RGA (RGA-GR) activity is inducible by dexamethasone (DEX; Yu et al., 2004 We found that, in most cases, RGA-GR strongly and rapidly repressed the expression of trichome regulatory genes and that this effect was detectable as early as 2 h after DEX application (Fig. 2 ). In the case of ZFP8, repression was faster in 35S:RGA-GR rga-t2 rgl2 ga1-3 than in 35S:RGA-GR rga-t2 gai-t6 ga1-3 plants, possibly because the amplitude of the response was more limited in the latter background. In all cases, the repression of gene expression by RGA-GR was found to be temporary and was no longer detectable 8 h after treatment (Fig. 2).
Because DEX induction of RGA-GR activity does not require protein synthesis, it is possible to determine whether its effects are direct or indirect by examining the influence of protein synthesis inhibitors on induced gene expression changes. To determine whether RGA-GR directly or indirectly represses trichome regulators, we repeated DEX applications to 35S:RGA-GR rga-t2 rgl2 ga1-3 in the presence of the protein synthesis inhibitor cycloheximide. We found that cycloheximide strongly inhibited the repression by DEX of all genes (Fig. 3 ). The transcriptional effect of RGA-GR activity was abolished or strongly attenuated and we never measured down-regulation in the first 6 h following application.
Based on the above results, we concluded that, although RGA-GR activity rapidly triggers repression of trichome initiation activators, the corresponding genes are indirect, rather than direct, targets and repression is therefore likely to require the production of additional, yet unidentified, factors.
To investigate whether the roles of RGA, GAI, RGL1, and RGL2 in repressing trichome activators reflect their influence on trichome initiation throughout the plant, we examined the effect of DELLA loss-of-function mutations in the absence of GA in the ga1-3 background.
Among all single DELLA mutants (in ga1-3), rgl1-1 ga1-3 and rgl2-1 ga1-3 displayed the lowest trichome density. Despite the importance of RGL1 in flower development (Cheng et al., 2004
GAI loss of function also had a significant, although lesser, impact on trichome initiation: gai-t6 ga1-3 mutants were glabrous, but gai-t6 rga-t2 ga1-3 produced more trichomes than rga-t2 ga1-3 mutants on stems and, to a lesser degree, on leaves (P = 0.07; Fig. 4, B and C). The gai-t6 mutation had the greatest effect on stems of rga-t2 ga1-3, where it nearly doubled trichome production (Fig. 4B). Interestingly, the quadruple DELLA rga-t2 gai-t6 rgl1 rgl2 ga1-3 mutant produced significantly more leaf and stem trichomes than gai-t6 rga-t2 ga1-3 mutants. These observations indicated that RGL1 and RGL2 also play a significant role in the regulation of trichome initiation. Their influence was, however, greatest when the repression exerted by other redundant DELLA proteins had been lifted. We also observed that rga-t2 gai-t6 rgl1-1 rgl2-1 ga1-3 produces a higher number of trichomes than wild-type plants on both vegetative and inflorescence organs (Fig. 4). This phenotype suggested that four DELLA proteins exert a repressive effect on trichome initiation even in wild-type plants. In summary, our data indicated that GAI, RGA, RGL1, and RGL2 are all involved, albeit to different degrees, in regulation by GA of trichome initiation and that they act collectively in their repressive role. The gene expression and phenotypic data together suggest that the DELLAs are major gatekeepers in the control by GA of trichome initiation acting mainly through a repressive transcriptional mechanism.
GA treatments are known to stimulate trichome branching on leaves and the trichomes of spy mutants, which display a constitutive GA response, are more highly branched than those of wild-type plants (Perazza et al., 1998 Our first observation was that, whereas RGA loss of function restored trichome initiation in ga1-3 mutants, rga-t2 ga1-3 was strongly deficient in branching. For example, mutant stems harbored only 4.4% branched trichomes, as compared to 38.8% in wild-type plants (Fig. 5A ). The ga1-3 rga-t2 rgl1 and ga1-3 rga-t2 rgl2 mutants presented a similar phenotype, indicating that lifting the repression exerted by RGA, RGL1, and/or RGL2 repression is not sufficient to restore branching. In contrast, we found that GAI loss of function strongly stimulated branching, restoring the number of branched trichomes to about 30% of the total (Fig. 5A). A similar situation was found in leaves: Whereas the rga-t2, rgl1, and rgl2 mutations had little influence on branching in the ga1-3 background, the gai-t6 mutation restored branching to wild-type levels or above (Fig. 5B).
Interestingly, loss of RGL1 and/or RGL2 function antagonized the effect of the gai-t6 mutation, an effect that was most dramatic in the quintuple mutant. This negative effect of rgl1 and rgl2 in the ga1-3 rga-t2 gai-t6 background was visible both on leaves and on stems (Fig. 5, A and B). The positive influence of RGL1 and RGL2 on branching was dependent on GAI activity because we could not detect any decrease in trichome branching in rgl1 and rgl2 (Fig. 5C) or in the ga1-3 rga-t2 rgl1 and ga1-3 rga-t2 rgl2 mutants. In contrast, the single gai-t6 mutant displayed significantly more branched trichomes on leaves and stems, which indicated that the stimulation of trichome branching by GAI loss of function is not dependent on other DELLA proteins (Fig. 5C). In summary, our analysis revealed an essential role for GAI in trichome branching and indicated that the repressors are antagonized by RGL1 and RGL2 in this process.
We previously reported that overexpressing GIS is not sufficient for restoring trichome initiation in the gai or ga1-3 mutants even though GIS, GIS2, and ZFP8 are required in the positive regulation of trichome initiation by GA (Gan et al., 2006
These observations therefore indicated that GIS2 is required for trichome initiation in the absence of DELLA repression. They also indicated that GIS2 (GIS/ZFP8) activity is limiting to trichome initiation when repression by RGA and GAI or RGL2 is lifted and that derepression is sufficient to restore the ability of GIS clade members to induce trichome proliferation in the ga1-3 background. These findings provided conclusive evidence that GIS2 and, in all likelihood, GIS and ZFP8 act downstream of the DELLA proteins.
In Arabidopsis, GAs are required for the transition between juvenile and adult stages and for flowering under short days, processes in which RGA and GAI play a major role (Wilson et al., 1992 Our observations confirmed that only RGA loss of function can restore abaxial trichome production in ga1-3 and that GAI loss of function further accelerates both vegetative and reproductive phase change, although the gai-t6 mutation alone has no effect (data not shown). Similarly, the effects of the rgl1 and rgl2 mutations were not detectable unless the function of other DELLA proteins was compromised. Loss of RGA function was required for the influence of RGL1 and RGL2 to be measurable and the effect was most pronounced when the activities of both RGA and GAI were abolished (Supplemental Fig. S3). Loss of RGL1 and/or RGL2 function in the rga-t2 gai-t6 ga1-3 background also resulted in earlier adult leaf production and flowering than in wild-type plants. In comparison, the combination of rga-t2 and gai-t6 mutations only restored a normal shoot maturation program in the ga1-3 mutant (Supplemental Fig. S3). The above findings indicated that both RGL1 and RGL2 play a role in the regulation by GAs of vegetative phase change and flowering and that their influence is conditional on RGA and GAI function. Interestingly, there was, overall, a strong correlation between the effects of DELLA loss of function on vegetative and reproductive phase change, which suggested that the mechanisms through which they control the two processes may be similar (Supplemental Fig. S3).
Exogenous GA application counteracts the repression by DELLA proteins of floral development and stem elongation (Peng and Harberd, 1997
In this study, we have shown that GA-mediated control over trichome initiation in Arabidopsis involves repression of most known trichome initiation activators by DELLA proteins RGA, GAI, RGL1, and RGL2. The onset of DELLA activity results in the rapid, but indirect, down-regulation of the corresponding genes, in particular of GL1, GL3, GIS, GIS2, and ZFP8. Consistently with these observations, we find that RGA, GAI, RGL1, and RGL2 collectively repress trichome initiation in Arabidopsis, RGA having the largest influence on this process. In contrast to its secondary role in initiation, GAI is the key repressor of trichome branching, antagonized in this process by RGL1 and RGL2. In addition to their role in epidermal differentiation, GAI, RGL1, and RGL2 act synergistically with RGA to repress vegetative and reproductive phase change. Finally, we show that GA applications generally recapitulate the effects of RGA/GAI/RGL1/RGL2 loss of function, except for their negative effect on flower trichome initiation, which suggests that other developmental signals and alternative regulators are implicated in this response.
GAs are known to influence GL1 expression and, upstream, the expression of GIS, GIS2, and ZFP8 (Gan et al., 2007
Whereas the repressive effects on GL1, GL3, GIS, and GIS2 of the DELLA proteins are clear, the results of our experiments with RGA-GR argue against a direct interaction between the repressors and their downstream targets. This situation is reminiscent of the interaction between RGA and homeotic genes, which is also indirect (Yu et al., 2004 ). An alternative interpretation of our results could be that cycloheximide treatments inhibited all responses in treated tissues and that the absence of a transcriptional effect on trichome regulatory genes was unspecific. We discount this possibility, although we cannot rule it out, on the basis that APETALA1 could be activated by LEAFY factor under similar conditions in similar tissues (Wagner et al., 1999). Regardless, it will be interesting to define the transcriptional networks acting immediately downstream of the DELLAs in the epidermis to start delineating the pathway leading from DELLA repression to trichome initiation.
Whereas GA applications are known to promote trichome branching (Perazza et al., 1998 The antagonism between RLG1/RGL2 and GAI with respect to branching is also surprising because the three proteins repress, although to differing degrees, the initiation process. One possible interpretation is that the mode of GAI action during trichome development is unusual and opposite to that of RGL1 and RGL2. Alternatively, a minimal level of DELLA activity may be required for branching to occur.
Previous studies have indicated that RGA plays a central role in leaf trichome initiation, flowering, and postgerminative growth (Silverstone et al., 1997
Loss of function of the four DELLA proteins generally results in trichome and shoot maturation phenotypes that are similar to those obtained with GA treatments. It does not, however, inhibit trichome formation on flowers, an effect that is observed when high doses of GA are applied, or in spy mutants (Greenboim-Wainberg et al., 2005
Our study highlights the importance of repressive mechanisms modulating the action of transcriptional activators in the control by GAs of epidermal differentiation in Arabidopsis. We show that these mechanisms are complex and are likely to involve multiple steps, including the intervention of growth repressors of the DELLA family. These regulatory proteins play a central role in this developmental process as part of their larger control over shoot maturation, regulating both trichome initiation and development. Their influence may, however, be more limited in trichome production on flowers, where other regulators are likely to play a central role. It is expected that elucidating the molecular steps linking the DELLAs to downstream activators and the role played by other direct and indirect regulators will be facilitated by multifaceted approaches drawing from genetics, gene expression profiling, and protein biochemistry.
Plant Material and Growth Conditions
All Arabidopsis (Arabidopsis thaliana) mutants used in this study are in the Ler background unless otherwise stated. The DELLA mutant combinations in the ga1-3 background have been described before (Lee et al., 2002
Plasmid Constructs
Analysis of Gene Expression
GA3 (Sigma) was used in all experiments that involved exogenous GA treatments and GA solutions were applied twice per week by spraying as previously described (Gan et al., 2006
The following materials are available in the online version of this article.
We thank Nicholas Welsby and Katchan Thacker for their technical assistance. Received June 27, 2007; accepted August 8, 2007; published August 17, 2007.
1 This work was supported by a grant from the Garfield Weston Foundation.  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Pierre Broun (pierre.broun{at}rdto.nestle.com).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.107.104794 * Corresponding author; e-mail pierre.broun{at}rdto.nestle.com.
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