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First published online August 28, 2009; 10.1105/tpc.109.068387 The Plant Cell 21:2307-2322 (2009) © 2009 American Society of Plant Biologists OPEN ACCESS ARTICLE
The Trihelix Transcription Factor GTL1 Regulates Ploidy-Dependent Cell Growth in the Arabidopsis Trichome[W],[OA]
a RIKEN Plant Science Center, Yokohama, Kanagawa 230-0045, Japan 3 Address correspondence to sugimoto{at}psc.riken.jp.
Leaf trichomes in Arabidopsis thaliana develop through several distinct cellular processes, such as patterning, differentiation, and growth. Although recent studies have identified several key transcription factors as regulating early patterning and differentiation steps, it is still largely unknown how these regulatory proteins mediate subsequent trichome development, which is accompanied by rapid cell growth and branching. Here, we report a novel trichome mutation in Arabidopsis, which in contrast with previously identified mutants, increases trichome cell size without altering its overall patterning or branching. We show that the corresponding gene encodes a GT-2-LIKE1 (GTL1) protein, a member of the trihelix transcription factor family. GTL1 is present within the nucleus during the postbranching stages of trichome development, and its loss of function leads to an increase in the nuclear DNA content only in trichomes that have completed branching. Our data further demonstrate that the gtl1 mutation modifies the expression of several cell cycle genes and partially rescues the ploidy defects in the cyclin-dependent kinase inhibitor mutant siamese. Taken together, this study provides the genetic evidence for the requirement of transcriptional regulation in the repression of ploidy-dependent plant cell growth as well as for an involvement of GTL trihelix proteins in this regulation.
Plant trichomes are highly specialized epidermal cells implicated in several important functions, including transpiration control, freezing tolerance, and protection against insects, diseases, and UV light (Johnson, 1975  ; Mauricio and Rausher, 1997). Trichomes are also of special commercial interest because they have a unique secondary metabolism, allowing the production and secretion of various useful natural compounds (Wang et al., 2008; Besser et al., 2009). Leaf trichomes in Arabidopsis thaliana develop through several distinct cellular processes, and over the last decade, they have become an ideal model system to study various developmental processes, such as cell patterning, differentiation, and morphogenesis, at the single cell level (Hulskamp et al., 1994).
Trichomes are the first epidermal cells that undergo cell specification in the Arabidopsis leaf primordia (Hulskamp et al., 1994
After cell fate specification, trichome cells enter a highly complex differentiation program that proceeds through two major growth phases (Melaragno et al., 1993
The tight coupling between endocycling and trichome development is also supported by several lines of experimental evidence demonstrating that the up- or downregulation of key cell cycle genes directly modifies the trichome patterning and/or morphogenesis. For example, mutations in the SIAMESE (SIM) gene, encoding a plant-specific cyclin-dependent kinase (CDK) inhibitor, result in clustered multicellular trichomes with individual nuclei having reduced ploidy levels (Walker et al., 2000 In this study, we identified a novel trichome mutant in Arabidopsis, which unlike all other previously described trichome mutants, only affects trichome size without altering their overall patterning or branching. We demonstrate that the corresponding gene encodes a plant-specific trihelix transcription factor, GT-2-LIKE1 (GTL1), and that it functions as a negative regulator of ploidy-dependent cell growth during postbranching phases of trichome development.
Cauliflower Mosaic Virus 35S Promoter–Driven Expression of Full-Length or Truncated GTL1 cDNA Leads to an Increase in Trichome Cell Size In a screen of the Arabidopsis FOX (full-length cDNA overexpression) collection (Ichikawa et al., 2006 ) for gain-of-function mutants that display aberrant sizes of trichome cells, we identified a transgenic line, F26519, that shows substantial increase in trichome cell size (Figure 1A
). The observed phenotype segregated dominantly within the original T2 population (43 seedlings with large trichomes and 14 seedlings with wild-type trichomes, n = 57,  2 = 0.003, P > 0.9), and PCR genotyping using primers specific for FOX vectors revealed cosegregation of the genotype and the phenotype, suggesting that the observed phenotype is caused by the overexpression of F26519 cDNA in the FOX vector. Furthermore, the cauliflower mosaic virus 35S promoter (CaMV35S)–driven expression of F26519 cDNA in wild-type background recapitulated the large trichome phenotype among all selected transformants (Figure 1A, R26519), confirming the identity of the causal gene. Sequencing analysis revealed that F26519 cDNA corresponds to a truncated version of the Arabidopsis GTL1 cDNA that lacks 750 bp in the central region and 4 bp in the C-terminal region. These deletions are likely to be an artifact caused during the construction of the full-length cDNA library (Seki et al., 2002), rather than the products derived from alternative splicing in vivo, since the borders of the deleted cDNA fragments do not match conventional eukaryotic splice sites. Consistently, our RT-PCR using RNA from 2-week-old wild-type seedlings amplified a 2010-bp cDNA that corresponds to the annotated full-length GTL1.
GTL1 belongs to the GT-2 gene family, a subfamily of the plant-specific trihelix transcription factor family (Smalle et al., 1998 ; Zhou, 1999). The Arabidopsis genome encodes 29 trihelix proteins, each of which contains at least one trihelix DNA binding domain, and depending on additional conserved motifs, they are classified into several subfamilies (Gao et al., 2009). In addition to GTL1, six other trihelix proteins, including previously described GT-2, DF1, and PETAL LOSS (PTL), are designated within the GT-2 subfamily in Arabidopsis. Phylogenetic analysis of the five genes most closely related in the GT-2 family demonstrates that GT-2, GTL1, and DF1 form a small clade, while two other homologs encoded by At5g28300 and At5g47660 are more distantly related (Smalle et al., 1998; Nagano et al., 2001; Figure 2
; see Supplemental Data Set 1 online). All five proteins, however, share common features with highly conserved N- and C-terminal trihelix DNA binding domains, which are unique to the GT-2 family, and another well-conserved domain of unknown function in the central region (Figures 1B and 2A). Further sequence analysis using a bioinformatic tool (http://www.at.embnet.org/toolbox/9aatad/) also identified, in the C-terminal region of the GTL1 protein, a potential 9–amino acid transactivation domain (DLVMRELIQ, Figure 1B), which gives a 100% match to 9–amino acid transactivation domains previously identified in eukaryotic and viral transcription factors (Piskacek et al., 2007). Alignment of the deduced amino acid sequences of wild-type GTL1 and GTL1F26519 proteins revealed that the deletions in GTL1F26519 proteins cause a truncation of 250 amino acids within the central region and a frame shift in the C-terminal region, resulting in a triple amino acid substitution from PED to KTL and a premature translational stop codon that removes the C-terminal 82 amino acids (Figure 1B). These large truncations are expected to remove the entire central domain and the putative transactivation domain of GTL1 proteins, while leaving their two trihelix domains intact.
Intriguingly, our RT-PCR analysis using RNA isolated from trichome-enriched plant materials (Jakoby et al., 2008 ) revealed that while the CaMV35S promoter–driven expression of the GTL1F26519 cDNA causes  50-fold overexpression of GTL1F26519, it also leads to strong downregulation of endogenous GTL1 expression with only 10% of wild-type GTL1 transcripts present in F26519 trichomes (Figure 1C). Furthermore, we found that the CaMV35S promoter–driven expression of full-length GTL1 cDNA also results in the reduction of total GTL1 levels in trichomes (Figure 1D) and increased trichome cell size (34 out of 36 selected T1 transformants showed large trichome phenotypes). These results suggest that 35S-driven expression of full-length GTL1 or GTL1F26519 may cause knockdown phenotypes with respect to trichome development.
GTL1 Represses Trichome Cell Growth Our phenotypic observation reveals that homozygous mutations for all three alleles lead to an increase in trichome size indistinguishable from original F26519 plants (Figures 1A and 3A ). Further quantitative analysis using trichomes isolated from the fourth and fifth leaves of 24-d-old plants indeed demonstrates that the trichome branch length is increased to very similar degrees in gtl1-1, gtl1-2, and F26519 (Figure 3B). Although all previously described large trichome mutants, including try, kak, rfi, and pym, also have over-branching phenotypes, gtl1 trichomes do not show significant alterations in their branching patterns (Figure 3A), and, as in the wild type, the majority of trichomes possess three branches (Figure 3C). Quantification of epidermal cell numbers and trichome numbers in individual leaves also demonstrates that the gtl1 mutations do not affect their relative frequencies (Table 1 ). These results suggest that GTL1 is involved in the regulation of trichome cell growth through pathways uncoupled from those mediating trichome initiation or branching. The third and fourth leaves of 21-d-old gtl1 plants, which are still expanding, appear to be slightly smaller than those of the wild type (Table 1), but after their full development, we do not find significant differences in their sizes (see Supplemental Figure 2A online).
An Increase in Trichome Cell Size Is Accompanied by an Increase in Nuclear DNA Content in gtl1 Mutants Many recent studies have shown that trichome cell size is often positively linked with their ploidy level (Hulskamp et al., 1994 ; Perazza et al., 1999; Sugimoto-Shirasu et al., 2005; Breuer et al., 2007). To test whether an increase in trichome cell size in gtl1 is accompanied by an increase in trichome ploidy, we visualized the nuclear DNA of fully mature trichomes isolated from the fourth and fifth leaves of 24-d-old plants using 4',6-diamidino-2-phenylindole (DAPI) staining. As shown in Figure 3D, our fluorescence microscopy shows that the DAPI-stained nuclear size in these trichomes is significantly increased in gtl1-1, gtl1-2, and F26519 trichome cells compared with wild-type trichomes at the equivalent developmental stage. Quantitative analysis of the nuclear DNA content indeed demonstrates that endoreduplication proceeds beyond wild-type levels in gtl1-1, gtl1-2, and F26519 trichome cells (Figure 3E). Our flow cytometry analysis using the whole third and fourth leaves of 26-d-old wild-type, gtl1-1, and gtl1-2 plants did not reveal major differences in the overall ploidy distributions (see Supplemental Figure 2B online), further supporting that GTL1 mainly functions in trichome development in leaves.
GTL1 Is Required for the Repression of Endocycles after Trichomes Complete Branching
GTL1 Is a Nuclear Protein Expressed during the Postbranching Stages of Trichome Development To investigate whether the expression pattern of the GTL1 gene supports its predicted function in postbranching stages of trichome development, we first generated transgenic lines carrying GTL1pro:β-glucuronidase (GUS) reporter constructs. All examined transgenic lines, derived from at least 10 independent T1 transformants, show strong GUS expression in developing trichomes (Figure 5A ). Interestingly, we do not detect any GUS signal in small trichomes that have just initiated or in those that are still undergoing the branching process at the base of developing young leaves. The GUS signal becomes visible, however, in large trichomes with three branches and appears to peak as trichomes reach their final size. To test whether GTL1 proteins also show developmental-specific expression patterns, we expressed GTL1:green fluorescent protein (GFP) or GFP:GTL1 fusion proteins under the same GTL1 promoter. We recovered multiple independent transgenic lines that show full complementation of the gtl1 mutant phenotypes by expression of either GTL1:GFP or GFP:GTL1 proteins, indicating that both N and C terminus fusion proteins are functional in planta. Our fluorescence microscopy further demonstrates that, as with its promoter activity, GFP:GTL1 proteins are expressed only after trichomes complete their second branching event (Figure 5B), supporting our hypothesis that GTL1 acts in postbranching processes of trichome development. Once trichomes complete their full growth, GTL1 expression declines and eventually ceases since we do not detect any GFP signals in older trichomes (Figure 5C). As expected for a putative transcription factor, we found that GFP:GTL1 proteins are localized exclusively within the nucleus (Figure 5D).
We also explored whether GFP:GTL1 proteins are expressed in any other cell types in leaves, but we did not detect any GFP signals in cells other than trichomes under our standard growth conditions. By contrast, we did detect some weak nuclear accumulation of GFP:GTL1 in developing roots and petals (see Supplemental Figure 3 online). Interestingly, GFP:GTL1 proteins do not accumulate in proliferating cells at the root meristem, and its expression is induced as cells start expanding (see Supplemental Figures 3A and 3B online). We found that GFP:GTL1 proteins are also expressed in growing root hairs (see Supplemental Figures 3C and 3D online). Within young petals, GFP:GTL1 proteins are present in a gradient fashion, with its highest expression level being detected at the tip of petals (see Supplemental Figures 3E and 3F online). In fully expanded petals, GFP:GTL1 proteins can be found in all epidermal cells (see Supplemental Figures 3E and 3F online).
The Expression and Function of GTL1 Require the Progression of Trichome Differentiation, Which Is Largely Dependent on TTG1 and GL2
To further explore the functional relationship between GTL1 and TTG1 or GL2, we introduced the GTL1pro:GUS reporter construct into the ttg1-10 or gl2-130213 mutant backgrounds and asked whether these mutations modify the promoter activity of the GTL1 gene. As shown in Figure 6E, GTL1 promoter activity is completely abolished by the ttg1-10 or gl2-130213 mutations in almost all leaf epidermal cells of 16-d-old plants, although some GUS signals can be detected in ttg1-10 trichomes that occasionally form at the leaf margins. The leaves of 24-d-old gl2-130213 plants sometimes develop one or two unbranched trichomes, and we detected GUS signals in a fraction of these unbranched trichomes (Figure 6F). While our data are largely consistent with our hypothesis that GTL1 acts downstream of TTG1 and GL2, the GUS activity detected in the ttg1-10 and gl2-130213 trichomes suggests that the expression of GTL1 is not absolutely dependent on TTG1 or GL2 function. An alternative scenario that can explain these observations is that GTL1 expression requires a certain stage of trichome development, which usually depends on TTG1 or GL2. As the ttg1-10 and gl2-130213 mutant phenotypes show (Figure 6A), both of these mutations are leaky, and trichomes that manage to initiate in the absence of TTG1 or GL2 appear to proceed to the developmental stage where GTL1 expression is induced. We found that the trichomes in gtl1-1 ttg1-10 double mutants are slightly larger and have higher ploidy than those in ttg1-10 (Figure 6A; see Supplemental Figure 4 online), indicating that the GTL1 proteins expressed in ttg1-10 trichomes do function to repress cell growth and endocycles. These results support the idea that the progression of trichome development to a certain stage is the prerequisite for the expression and function of GTL1.
The gtl1 gl3 and gtl1 try Mutants Display Additive Trichome Cell Size and Ploidy Phenotypes
The gl3 and try mutations also disrupt trichome initiation and/or patterning, leading to alterations in trichome number and/or spacing (Schnittger et al., 1999 ; Payne et al., 2000). The gtl1-1 mutation does not appear to enhance or rescue either of these phenotypes in gl3-7454 or try-29760 plants (Figure 7E), further demonstrating that GTL1 does not play profound roles in trichome initiation or patterning.
The gtl1 Mutation Modifies the Expression of Cell Cycle Genes and Partially Rescues the Ploidy Defects in sim1 Mutants
To further investigate the possibility that GTL1 functions in endocycle control, we introduced the gtl1-1 mutation into the sim-1 mutant background and tested whether the function of GTL1 interferes with that of SIM. Although many trichomes in sim-1 are multicellular (Walker et al., 2000 ), their overall size is comparable with that of wild-type trichomes (Figure 9A
). By contrast, the majority of trichomes in the gtl1-1 sim-1 double mutants appear to be slightly larger than those in sim-1 (Figure 9A), although we cannot accurately measure the trichome size of gtl1-1 sim-1 plants due to the irregular branching patterns of trichome in these plants (Churchman et al., 2006). As previously reported, the DNA content of individual nuclei in sim-1 trichomes is strongly reduced compared with that in wild-type trichomes (Walker et al., 2000; Figure 9B). We found that the average nuclear DNA content in gtl1-1 sim-1 trichomes is significantly greater than in wild-type trichomes (Figure 9B), demonstrating that the gtl1-1 mutation can partially bypass the endocycle defects caused by the sim-1 mutation. These results strongly support our hypothesis that GTL1 participates in the regulation of successive endocyling in trichome development.
GTL1 Is a Repressor of Cell Growth and Endocycling in Trichome Development We have demonstrated that a novel Arabidopsis trihelix protein, GTL1, participates in the repression of ploidy-dependent cellular growth in trichome development. Recent molecular and genetic studies have uncovered the transcriptional networks involved in trichome patterning and differentiation, but the mechanism underlying subsequent growth and development is still poorly understood. Two trichome patterning transcription factors, TRY and GL3, are also implicated in the control of cell growth and branching (Hulskamp et al., 1994 ; Folkers et al., 1997; Schnittger et al., 1998; Perazza et al., 1999), indicating that some of the early acting transcriptional regulators also participate in trichome development beyond the differentiation stage. Our data show that the expression of GTL1 largely depends on the early patterning/differentiation genes, TTG1 and GL2, strongly suggesting that GTL1 acts as part of the regulatory mechanisms linking early trichome differentiation to final growth and development. Given that we occasionally detect some GTL1 expression in ttg1 or gl2 trichomes, TTG1 or GL2 itself is not likely to be the absolute requirement for GTL1 expression. Our data, instead, suggest it is the progression of trichome development to a certain stage that induces the expression of GTL1. We do not yet know what specifies the developmental stage to allow GTL1 expression, but at least our data suggest that the level of trichome branching is not the prerequisite for this, since unbranched or under-branched trichomes can express GTL1 in ttg1 or gl2.
A key difference between GTL1 and previously identified trichome growth regulators, such as KAK, RFI, PYM, and SPY, is that GTL1 represses trichome cell growth without altering its branching pattern. The tight coupling between cell size and branching in many trichome mutants previously led to the idea that the pathways regulating these two cellular features are closely linked. Our new data, however, clearly demonstrate that at least part of these regulatory pathways can be uncoupled. One possible mechanism that can uncouple trichome cell growth from branching is that trichome cells continue to have growth potential when they reach their normal maximum size while their branching potential ceases much earlier during their development (Figure 10
). Unlike TRY and GL3, which are both expressed throughout trichome development, GTL1 is expressed only after trichome cells complete branching, allowing its specific repression of trichome cell growth at the late stage of trichome development. In agreement with this idea, young three-branched trichomes in gtl1 have not undergone additional rounds of endocycling as opposed to those in try, which already possess significantly greater nuclear DNA content than the wild type. Thus, TRY and GTL1 appear to exert their function at different stages of trichome development, with TRY acting early, while cells are still undergoing branching and GTL1 only after cells complete branching. It is worth noting that 35S promoter–driven overexpression of GL1 is previously reported to increase trichome ploidy levels without modifying its branching (Larkin et al., 1994
How 35S:GTL1 or 35S:GTL1F26519 expression leads to the trichome phenotype resembling the loss-of-function mutants is not clear, but our data show that 35S-driven expression of either GTL1 or GTL1F26519 leads to the downregulation of full-length GTL1 expression (Figure 1). It is plausible that the ectopic expression of a growth repressor in cell types essential for the plant survival (e.g., meristem cells) leads to lethality, preventing the recovery of transgenic plants with high GTL1 expression. It is intriguing that 35S:GTL1F26519 expression, by contrast, allows 50-fold accumulation of GTL1F26519 cDNA in F26519 trichomes. Overexpression of these heavily truncated variants may cause dominant-negative or potentially gain-of-function phenotypes, and these possibilities should be investigated in future studies.
Transcriptional Regulation of Growth Repression and Its Link to Endocycling
An important next question is whether other plant cell types also require similar transcriptional regulation to repress their growth. Because many plant cell types have unique, and often very constant, final cell sizes, the extent of their growth and/or the timing of growth cessation are likely to be tightly controlled. Although we know very little about these controls, one recent study reports that a basic helix-loop-helix transcription factor, BIGPETALp, is required to limit petal cell growth in Arabidopsis (Szecsi et al., 2006
Role of GT-2 Family Trihelix Proteins in Plant Development
Plant Material and Growth Conditions The original FOX mutant collection, and the gl3-7454 and try-29760 mutants (Col background), were described previously (Ichikawa et al., 2006 ; Ishida et al., 2007; Tominaga et al., 2008). The three gtl1 mutant alleles and gl2-130213 (SALK_130213) were obtained from the ABRC Stock Center (Ohio State University), and ttg1-10 (Col background; Larkin et al., 1994) and sim-1 (Col background; Walker et al., 2000) were provided by John Larkin (Louisiana State University). Plants were either germinated and grown on plates containing Murashige and Skoog salts, pH 5.7, 1% sucrose (w/v), and 0.5% phytogel (w/v) or on a 1:1 mixture of soil Supermix A (SAKATA) and vermiculite (VS Kako) in continuous light at 22°C.
Amino Acid Sequence Alignment and Phylogenetic Analysis
Genotype Determination of Mutants
Vector Constructions and Arabidopsis Transformation
RNA Extraction and Gene Expression Analyses
GUS Staining and Microscopy
Fluorescence Microscopy and Ploidy Measurements
Accession Numbers
Supplemental Data
We thank John Larkin for ttg1-10 and sim-1 mutants, the ABRC stock center for T-DNA insertion mutants, and Tsuyoshi Nakagawa for pGWB1 vectors. We thank Keith Roberts and members of the Sugimoto Lab for their critical comments on the manuscript. This work was supported by the Japan Society for the Promotion of Science Grants 20061028 and 20687004 to K.S. C.B. was a recipient of a Japan Society for the Promotion of Science postdoctoral fellowship and subsequently of a RIKEN postdoctoral fellowship.
1 Current address: University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan. 
2 Current address: National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan. 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.plantcell.org) is: Keiko Sugimoto (sugimoto{at}psc.riken.jp).
[W] Online version contains Web-only data.
[OA] Open access articles can be viewed online without a subscription. www.plantcell.org/cgi/doi/10.1105/tpc.109.068387 Received April 30, 2009; Revision received July 16, 2009. accepted August 14, 2009.
Besser, K., Harper, A., Welsby, N., Schauvinhold, I., Slocombe, S., Li, Y., Dixon, R.A., and Broun, P. (2009). Divergent regulation of terpenoid metabolism in the trichomes of wild and cultivated tomato species. Plant Physiol. 149: 499–514. Breuer, C., Stacey, N.J., West, C.E., Zhao, Y., Chory, J., Tsukaya, H., Azumi, Y., Maxwell, A., Roberts, K., and Sugimoto-Shirasu, K. (2007). BIN4, a novel component of the plant DNA topoisomerase VI complex, is required for endoreduplication in Arabidopsis. Plant Cell 19: 3655–3668. Brewer, P.B., Howles, P.A., Dorian, K., Griffith, M.E., Ishida, T., Kaplan-Levy, R.N., Kilinc, A., and Smyth, D.R. (2004). PETAL LOSS, a trihelix transcription factor gene, regulates perianth architecture in the Arabidopsis flower. Development 131: 4035–4045. Castellano, M.M., del Pozo, J.C., Ramirez-Parra, E., Brown, S., and Gutierrez, C. (2001). Expression and stability of Arabidopsis CDC6 are associated with endoreplication. Plant Cell 13: 2671–2686. Cebolla, A., Vinardell, J.M., Kiss, E., Olah, B., Roudier, F., Kondorosi, A., and Kondorosi, E. (1999). The mitotic inhibitor ccs52 is required for endoreduplication and ploidy-dependent cell enlargement in plants. EMBO J. 18: 4476–4484.[CrossRef][Web of Science][Medline] Churchman, M.L., et al. (2006). SIAMESE, a plant-specific cell cycle regulator, controls endoreplication onset in Arabidopsis thaliana. Plant Cell 18: 3145–3157. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735–743.[CrossRef][Web of Science][Medline] Corpet, F. (1988). Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16: 10881–10890. Dehesh, K., Bruce, W.B., and Quail, P.H. (1990). A trans-acting factor that binds to a GT-motif in a phytochrome gene promoter. Science 250: 1397–1399. Esch, J.J., Chen, M.A., Hillestad, M., and Marks, M.D. (2004). Comparison of TRY and the closely related At1g01380 gene in controlling Arabidopsis trichome patterning. Plant J. 40: 860–869.[CrossRef][Web of Science][Medline] Folkers, U., Berger, J., and Hulskamp, M. (1997). Cell morphogenesis of trichomes in Arabidopsis: Differential control of primary and secondary branching by branch initiation regulators and cell growth. Development 124: 3779–3786.[Abstract] Galway, M.E., Masucci, J.D., Lloyd, A.M., Walbot, V., Davis, R.W., and Schiefelbein, J.W. (1994). The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root. Dev. Biol. 166: 740–754.[CrossRef][Web of Science][Medline] Gao, M.-J., Lydiate, D.J., Li, X., Lui, H., Gjetvaj, B., Hegedus, D.D., and Rozwadowski, K. (2009). Repression of seed maturation genes by a trihelix transcriptional repressor in Arabidopsis seedlings. Plant Cell 21: 54–71. Hulskamp, M., Misra, S., and Jurgens, G. (1994). Genetic dissection of trichome cell development in Arabidopsis. Cell 76: 555–566.[CrossRef][Web of Science][Medline] Hulskamp, M., Schnittger, A., and Folkers, U. (1999). Pattern formation and cell differentiation: trichomes in Arabidopsis as a genetic model system. Int. Rev. Cytol. 186: 147–178.[Web of Science][Medline] Ichikawa, T., et al. (2006). The FOX hunting system: An alternative gain-of-function gene hunting technique. Plant J. 48: 974–985.[CrossRef][Web of Science][Medline] Ilgenfritz, H., Bouyer, D., Schnittger, A., Mathur, J., Kirik, V., Schwab, B., Chua, N.H., Jurgens, G., and Hulskamp, M. (2003). The Arabidopsis STICHEL gene is a regulator of trichome branch number and encodes a novel protein. Plant Physiol. 131: 643–655. Imai, K.K., Ohashi, Y., Tsuge, T., Yoshizumi, T., Matsui, M., Oka, A., and Aoyama, T. (2006). The A-type cyclin CYCA2;3 is a key regulator of ploidy levels in Arabidopsis endoreduplication. Plant Cell 18: 382–396. Ishida, T., Hattori, S., Sano, R., Inoue, K., Shirano, Y., Hayashi, H., Shibata, D., Sato, S., Kato, T., Tabata, S., Okada, K., and Wada, T. (2007). Arabidopsis TRANSPARENT TESTA GLABRA2 is directly regulated by R2R3 MYB transcription factors and is involved in regulation of GLABRA2 transcription in epidermal differentiation. Plant Cell 19: 2531–2543. Ishida, T., Kurata, T., Okada, K., and Wada, T. (2008). A genetic regulatory network in the development of trichomes and root hairs. Annu. Rev. Plant Biol. 59: 365–386.[CrossRef][Medline] Jakoby, M.J., Falkenhan, D., Mader, M.T., Brininstool, G., Wischnitzki, E., Platz, N., Hudson, A., Hulskamp, M., Larkin, J., and Schnittger, A. (2008). Transcriptional profiling of mature Arabidopsis trichomes reveals that NOECK encodes the MIXTA-like transcriptional regulator MYB106. Plant Physiol. 148: 1583–1602. Johnson, C.S., Kolevski, B., and Smyth, D.R. (2002). TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. Plant Cell 14: 1359–1375. Johnson, H.B. (1975). Plant pubescence - Ecological perspective. Bot. Rev. 41: 233–258.[CrossRef] Kirik, V., Simon, M., Huelskamp, M., and Schiefelbein, J. (2004a). The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. Dev. Biol. 268: 506–513.[CrossRef][Web of Science][Medline] Kirik, V., Simon, M., Wester, K., Schiefelbein, J., and Hulskamp, M. (2004b). ENHANCER of TRY and CPC 2 (ETC2) reveals redundancy in the region-specific control of trichome development of Arabidopsis. Plant Mol. Biol. 55: 389–398.[CrossRef][Web of Science][Medline] Lammens, T., Boudolf, V., Kheibarshekan, L., Zalmas, L.P., Gaamouche, T., Maes, S., Vanstraelen, M., Kondorosi, E., La Thangue, N.B., Govaerts, W., Inze, D., and De Veylder, L. (2008). Atypical E2F activity restrains APC/CCCS52A2 function obligatory for endocycle onset. Proc. Natl. Acad. Sci. USA 105: 14721–14726. Larkin, J.C., Oppenheimer, D.G., Lloyd, A.M., Paparozzi, E.T., and Marks, M.D. (1994). Roles of the GLABROUS1 and TRANSPARENT TESTA GLABRA genes in Arabidopsis trichome development. Plant Cell 6: 1065–1076.[Abstract] Larkin, J.C., Young, N., Prigge, M., and Marks, M.D. (1996). The control of trichome spacing and number in Arabidopsis. Development 122: 997–1005.[Abstract] Larson-Rabin, Z., Li, Z., Masson, P.H., and Day, C.D. (2009). FZR2/CCS52A1 expression is a determinant of endoreduplication and cell expansion in Arabidopsis. Plant Physiol. 149: 874–884. Malamy, J., and Benfey, P. (1997). Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124: 33–44.[Abstract] Marks, M.D. (1997). Molecular genetic analysis of trichome development in Arabidopsis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 137–163.[CrossRef][Web of Science] Mauricio, R., and Rausher, M.D. (1997). Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution 51: 1435–1444.[CrossRef][Web of Science] Melaragno, J.E., Mehrotra, B., and Coleman, A.W. (1993). Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5: 1661–1668.[Abstract] Morohashi, K., Zhao, M., Yang, M., Read, B., Lloyd, A., Lamb, R., and Grotewold, E. (2007). Participation of the Arabidopsis bHLH factor GL3 in trichome initiation regulatory events. Plant Physiol. 145: 736–746. Nagano, Y., Inaba, T., Furuhashi, H., and Sasaki, Y. (2001). Trihelix DNA-binding protein with specificities for two distinct cis-elements: Both important for light down-regulated and dark-inducible gene expression in higher plants. J. Biol. Chem. 276: 22238–22243. Nakagawa, T., Kurose, T., Hino, T., Tanaka, K., Kawamukai, M., Niwa, Y., Toyooka, K., Matsuoka, K., Jinbo, T., and Kimura, T. (2007). Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104: 34–41.[CrossRef][Web of Science][Medline] Oppenheimer, D.G., Herman, P.L., Sivakumaran, S., Esch, J., and Marks, M.D. (1991). A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules. Cell 67: 483–493.[CrossRef][Web of Science][Medline] Payne, C.T., Zhang, F., and Lloyd, A.M. (2000). GL3 encodes a bHLH protein that regulates trichome development in Arabidopsis through interaction with GL1 and TTG1. Genetics 156: 1349–1362. Perazza, D., Herzog, M., Hulskamp, M., Brown, S., Dorne, A.M., and Bonneville, J.M. (1999). Trichome cell growth in Arabidopsis thaliana can be derepressed by mutations in at least five genes. Genetics 152: 461–476. Piskacek, S., Gregor, M., Nemethova, M., Grabner, M., Kovarik, P., and Piskacek, M. (2007). Nine-amino-acid transactivation domain: Establishment and prediction utilities. Genomics 89: 756–768.[CrossRef][Web of Science][Medline] Rerie, W.G., Feldmann, K.A., and Marks, M.D. (1994). The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev. 8: 1388–1399. Schellmann, S., Hulskamp, M., and Uhrig, J. (2007). Epidermal pattern formation in the root and shoot of Arabidopsis. Biochem. Soc. Trans. 35: 146–148.[CrossRef][Web of Science][Medline] Schellmann, S., Schnittger, A., Kirik, V., Wada, T., Okada, K., Beermann, A., Thumfahrt, J., Jurgens, G., and Hulskamp, M. (2002). TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J. 21: 5036–5046.[CrossRef][Web of Science][Medline] Schnittger, A., Folkers, U., Schwab, B., Jurgens, G., and Hulskamp, M. (1999). Generation of a spacing pattern: the role of triptychon in trichome patterning in Arabidopsis. Plant Cell 11: 1105–1116. Schnittger, A., Jurgens, G., and Hulskamp, M. (1998). Tissue layer and organ specificity of trichome formation are regulated by GLABRA1 and TRIPTYCHON in Arabidopsis. Development 125: 2283–2289.[Abstract] Schnittger, A., Schobinger, U., Bouyer, D., Weinl, C., Stierhof, Y.D., and Hulskamp, M. (2002). Ectopic D-type cyclin expression induces not only DNA replication but also cell division in Arabidopsis trichomes. Proc. Natl. Acad. Sci. USA 99: 6410–6415. Seki, M., et al. (2002). Functional annotation of a full-length Arabidopsis cDNA collection. Science 296: 141–145. Smalle, J., Kurepa, J., Haegman, M., Gielen, J., Van Montagu, M., and Van Der Straeten, D. (1998). The trihelix DNA-binding motif in higher plants is not restricted to the transcription factors GT-1 and GT-2. Proc. Natl. Acad. Sci. USA 95: 3318–3322. Sugimoto-Shirasu, K., Roberts, G.R., Stacey, N.J., McCann, M.C., Maxwell, A., and Roberts, K. (2005). RHL1 is an essential component of the plant DNA topoisomerase VI complex and is required for ploidy-dependent cell growth. Proc. Natl. Acad. Sci. USA 102: 18736–18741. Sugimoto-Shirasu, K., Stacey, N.J., Corsar, J., Roberts, K., and McCann, M.C. (2002). DNA topoisomerase VI is essential for endoreduplication in Arabidopsis. Curr. Biol. 12: 1782–1786.[CrossRef][Web of Science][Medline] Szecsi, J., Joly, C., Bordji, K., Varaud, E., Cock, J.M., Dumas, C., and Bendahmane, M. (2006). BIGPETALp, a bHLH transcription factor is involved in the control of Arabidopsis petal size. EMBO J. 25: 3912–3920.[CrossRef][Web of Science][Medline] Szymanski, D.B., and Marks, M.D. (1998). GLABROUS1 overexpression and TRIPTYCHON alter the cell cycle and trichome cell fate in Arabidopsis. Plant Cell 10: 2047–2062. Szymanski, D.B., Marks, M.D., and Wick, S.M. (1999). Organized F-actin is essential for normal trichome morphogenesis in Arabidopsis. Plant Cell 11: 2331–2347. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596–1599. Tominaga, R., Iwata, M., Sano, R., Inoue, K., Okada, K., and Wada, T. (2008). Arabidopsis CAPRICE-LIKE MYB 3 (CPL3) controls endoreduplication and flowering development in addition to trichome and root hair formation. Development 135: 1335–1345. Vanstraelen, M., Baloban, M., Da Ines, O., Cultrone, A., Lammens, T., Boudolf, V., Brown, S.C., De Veylder, L., Mergaert, P., and Kondorosi, E. (2009). APC/CCCS52A complexes control meristem maintenance in the Arabidopsis root. Proc. Natl. Acad. Sci. USA 106: 11806–11811. Walker, A.R., Davison, P.A., Bolognesi-Winfield, A.C., James, C.M., Srinivasan, N., Blundell, T.L., Esch, J.J., Marks, M.D., and Gray, J.C. (1999). The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11: 1337–1350. Walker, J.D., Oppenheimer, D.G., Concienne, J., and Larkin, J.C. (2000). SIAMESE, a gene controlling the endoreduplication cell cycle in Arabidopsis thaliana trichomes. Development 127: 3931–3940.[Abstract] Wang, G., Tian, L., Aziz, N., Broun, P., Dai, X., He, J., King, A., Zhao, P.X., and Dixon, R.A. (2008). Terpene biosynthesis in glandular trichomes of hop. Plant Physiol. 148: 1254–1266. Wang, S., Kwak, S.H., Zeng, Q., Ellis, B.E., Chen, X.Y., Schiefelbein, J., and Chen, J.G. (2007). TRICHOMELESS1 regulates trichome patterning by suppressing GLABRA1 in Arabidopsis. Development 134: 3873–3882. Wester, K., Digiuni, S., Geier, F., Timmer, J., Fleck, C., and Hulskamp, M. (2009). Functional diversity of R3 single-repeat genes in trichome development. Development 136: 1487–1496. Zhang, F., Gonzalez, A., Zhao, M., Payne, C.T., and Lloyd, A. (2003). A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis. Development 130: 4859–4869. Zhang, X., and Oppenheimer, D.G. (2004). A simple and efficient method for isolating trichomes for downstream analyses. Plant Cell Physiol. 45: 221–224. Zhao, M., Morohashi, K., Hatlestad, G., Grotewold, E., and Lloyd, A. (2008). The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci. Development 135: 1991–1999. Zhou, D.X. (1999). Regulatory mechanism of plant gene transcription by GT-elements and GT-factors. Trends Plant Sci. 4: 210–214.[CrossRef][Web of Science][Medline] This article has been cited by other articles:
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