1 Department of Molecular, Cellular, and Developmental Biology, University of
Michigan, 830 North University Avenue, Ann Arbor, MI 48109, USA
2 Department of Biology, Yonsei University, Sinchon 134, Seoul 120-749,
Korea
3 Institute for Cellular and Molecular Biology, University of Texas, Austin, TX
78712, USA
* Author for correspondence (e-mail: schiefel{at}umich.edu)
Accepted 19 September 2003
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SUMMARY |
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Key words: Epidermis, Pattern formation, Cell differentiation, Root development, Transcriptional regulation
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Introduction |
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Molecular genetic studies have led to the identification of a suite of
putative transcription factors that regulate the epidermal cell pattern. These
include gene products required for specification of the non-hair cell type,
such as the homeodomain protein GLABRA2 (GL2)
(Masucci et al., 1996;
Rerie et al., 1994
), the R2R3
MYB-type transcription factor WEREWOLF (WER)
(Lee and Schiefelbein, 1999
),
and the WD-repeat protein TRANSPARENT TESTA GLABRA (TTG)
(Galway et al., 1994
;
Walker et al., 1999
). Other
regulators are involved in specifying the hair cell fate, including CAPRICE
(CPC) and TRYPTICHON (TRY), which are small one-repeat MYB proteins that lack
a transcriptional activation domain and exhibit partially redundant functions
(Schellmann et al., 2002
;
Wada et al., 2002
;
Wada et al., 1997
). The final
cell pattern appears to result from positive and negative regulatory
interactions between these components
(Schiefelbein, 2003
).
Specifically, WER promotes transcription of GL2 and CPC (and
probably TRY) in the N position, GL2 inhibits hair cell specification
in the N position, and CPC (and probably TRY) act in lateral inhibition by
moving to the H cell and repressing transcription of WER, GL2 and its
own gene (Lee and Schiefelbein,
2002
; Schellmann et al.,
2002
; Schiefelbein,
2003
; Wada et al.,
2002
).
Several lines of indirect evidence have suggested that a basic
helix-loop-helix (bHLH) transcription factor may also be a component of the
cell specification pathway in the root epidermis. This evidence includes (1)
the ability of the maize R bHLH protein to induce ectopic non-hair cells when
expressed in wild type Arabidopsis
(Galway et al., 1994); (2) the
ability of the maize R bHLH protein to restore non-hair cell production when
expressed in the hairy ttg mutant
(Galway et al., 1994
); (3) the
ability of the maize R bHLH protein to promote GL2 gene expression
(Hung et al., 1998
); (4) the
ability of the wer mutations to block the effect of the maize R bHLH
protein on non-hair cell specification
(Lee and Schiefelbein, 1999
);
and (5) the ability of the R bHLH protein to interact with the WER protein and
with the CPC protein in the yeast two-hybrid assay
(Lee and Schiefelbein, 1999
;
Wada et al., 2002
). Together,
these findings have led to the suggestion that an Arabidopsis bHLH
protein is likely to exist that interacts with WER to induce cells in the N
position to adopt a non-hair fate (Larkin
et al., 2003
; Lee and
Schiefelbein, 1999
).
In this study, we confirm this long-standing hypothesis. We find that two
Arabidopsis bHLH genes, GLABRA3 (GL3) and
ENHANCER OF GLABRA3 (EGL3), are important regulators of root
epidermal cell specification. These two genes encode bHLH proteins related to
the maize R protein and influence trichome development and other TTG-related
processes in Arabidopsis
(Koornneef et al., 1982;
Payne et al., 2000
;
Zhang et al., 2003
). We show
that GL3 and EGL3 have largely redundant functions in the
specification of the non-hair cell fate and also participate in specifying the
hair cell fate. We propose that the GL3 and EGL3 bHLH proteins act as binding
partners for the WER or the CPC MYB proteins and thereby mediate the cell fate
decision during root epidermis development.
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Materials and methods |
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Arabidopsis seeds were surface sterilized and grown on
agarose-solidified nutrient medium in vertically oriented petri plates as
previously described (Schiefelbein and
Somerville, 1990).
Microscopy
Root hair cell production and cell type pattern analysis were determined
from Toluidine Blue-stained roots as previously described
(Lee and Schiefelbein, 2002)
from at least 24 four-day-old seedling roots for each strain. The upper region
of the root was defined as the segment containing 10 epidermal cells whose
upper boundary is four cells below the hairy collet region. The lower region
of the root is a larger zone representing approximately the lower half of a
four-dayold root and occupied by epidermal cells that differentiate during
days 3-4. An epidermal cell was scored as a root-hair cell if any protrusion
was visible, regardless of its length.
Plastic transverse sections were obtained from four- to five-day-old roots
embedded in JB-4 resin and stained with 0.05% Toluidine Blue O, as previously
described (Masucci and Schiefelbein,
1996). The relative cell division rate in the H and N cell
positions of the epidermis was determined by counting the number of cells in
clones derived from rare longitudinal divisions, using a method previously
described (Berger et al.,
1998a
), and by counting the number of cells in adjacent N and H
cell files.
The histochemical analysis of plants containing the GUS reporter
constructs was performed essentially as described
(Masucci et al., 1996).
Molecular biology methods
For RT-PCR assays, tissue of wild-type (Columbia) plants was ground in
liquid nitrogen and total RNA was extracted as described
(Weigel and Glazebrook, 2002).
Tissue from roots and hypocotyl/cotyledons was obtained from four-day-old
seedling grown on nutrient plates as described above. All other tissues were
obtained from soil grown plants. RT-PCR was performed using the Superscript
One-Step RTPCR Kit (Invitrogen) according to manufacturer instructions. Total
RNA template (500 ng) was used for each reaction and a total of 40 PCR cycles
was performed. UBQ10 gene-specific primers
(Weigel and Glazebrook, 2002
)
were used in control reactions. The length of the gene-specific products
obtained for GL3, EGL3 and UBQ was 581 bp, 516 bp and 483
bp, respectively.
Yeast two-hybrid assays were performed essentially as described
(Lee and Schiefelbein, 1999).
The entire coding regions of the GL3 or EGL3 cDNA were joined as C-terminal
fusion to the yeast GAL4 DNA-binding domain in pGBT9 to generate the in-frame
protein fusions BD-GL3 and BD-EGL3. The GAL4 transcriptional activation domain
in pGAD424 was fused to the full-length WER-coding region to generate AD-WER
(Lee and Schiefelbein, 1999
)
and it was fused to the full-length CPC coding region to generate AD-CPC.
After transformation into yeast strain HF7c, the ß-galactosidase assays
were performed on at least six individual transformants for each combination
of constructs.
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Results |
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To determine whether either of these R-like bHLH genes from
Arabidopsis are normally expressed in the developing root, we
conducted RT-PCR analyses using GL3- and EGL3-specific
primers on RNA isolated from roots and other organs. GL3 and
EGL3 amplified fragments were detected from each RNA sample
(Fig. 1), indicating that each
bHLH gene is expressed in all of these plant organs. This is consistent with
the recent finding that GL3 and EGL3 participate in multiple
pathways in the above-ground organs (Zhang
et al., 2003). Furthermore, the substantial amplification of
GL3 and EGL3 from root RNA samples
(Fig. 1) suggests that these
genes are expressed in developing Arabidopsis seedling roots.
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|
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To further explore the effect of the 35S::GL3 and
35S::EGL3 transgenes in relation to the previously characterized
35S::R, we introduced the 35S::GL3 and 35S::EGL3
into the ttg-1 mutant. The ttg-1 root specifies hair cells
in nearly every root epidermal cell, and this defect can be overcome by the
35S::R transgene (Galway et al.,
1994). We found that the 35S::GL3 ttg-1 and 35S::EGL3
ttg-1 roots exhibited a significant reduction in hair cell production,
when compared with the ttg mutant
(Fig. 2;
Table 1). This indicates that
the overexpression of either gene can restore non-hair cell production in the
ttg-1 mutant, which is similar to the effect of 35S::R on
ttg (Galway et al.,
1994
). Interestingly, each transgene exhibited a difference in
their effect on the upper and lower region of the root, with the
35S::EGL3 having its greatest impact on the lower region and the
35S::GL3 on the upper region, which is similar to their effects in
the wild-type background. Because neither of the transgenes was able to induce
non-hair cell specification in the ttg-1 mutant to the same extent as
they do in the wild-type background (Table
1), it is likely that TTG is required for the full effect of the
35S::GL3 and 35S::EGL3. To determine whether this partial
TTG dependency can be diminished by expressing both GL3 and
EGL3 in the ttg mutant, we constructed a 35S::GL3
35S::EGL3 ttg-1 line. These roots had an enhanced non-hair cell phenotype
when compared with either single transgene
(Table 1), suggesting that
increased expression of these bHLH genes can overcome the effect of the
ttg-1. Furthermore, the lack of a synergistic effect implies that the
GL3 and EGL3 provide largely similar functions, rather than interdependent
functions.
Analysis of gl3 and egl3 mutants reveal redundancy in bHLH
gene function
To directly assess the involvement of the GL3 and EGL3
genes in root epidermis development, we analyzed plants bearing homozygous
mutations in one or both of these genes. We employed gl3 mutant lines
(gl3-1 and gl3-2) and egl3 mutant lines
(egl3-1 and egl3-2) with mutations that cause premature stop
codons and probably represent null alleles
(Payne et al., 2000;
Zhang et al., 2003
). We found
that each of the single mutant lines produced a normal number and pattern of
epidermal cell types in the lower region of the root, but they show a slight
(egl3-1 and egl3-2) or moderate (gl3-1 and
gl3-2) increase in hair cell production in the upper region of the
root, owing to the misspecification of hair cells in the N (ectopic) position
(Fig. 3;
Table 2). Thus, GL3
and EGL3 are necessary to specify fully the non-hair cell fate and
generate the proper epidermal pattern in the upper region, but not the lower
region, of the root.
|
|
GL3 and EGL3 act at an early stage in epidermal development
The outgrowth of a root hair from an epidermal cell represents a relatively
late event in epidermal cell differentiation. At earlier stages, immature
epidermal cells in the H and N positions may be distinguished from one another
by their differential vacuolation rate and cytoplasmic density, and these
characteristics are controlled by WER and TTG but not GL2
(Galway et al., 1994;
Lee and Schiefelbein, 1999
;
Masucci et al., 1996
;
Schellmann et al., 2002
). To
determine whether the altered root hair production in the gl3 egl3
mutant and the 35S lines were associated with cell fate abnormalities
at an early developmental stage, we examined vacuole formation and cytoplasmic
density in developing epidermal cells from transverse sections taken from the
meristematic region of the root. In contrast to the wild type, which displayed
a greater vacuolation rate and reduced cytoplasmic density in the N cell
position relative to the H cell position, all epidermal cells in the gl3
egl3 exhibit characteristics of developing hair cells, whereas all
epidermal cells in 35S::EGL3 exhibit characteristics of developing
non-hair cells (Fig. 4).
|
|
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Given these results, we wished to investigate the possibility that GL3 and EGL3 promote the non-hair fate by acting through GL2. Therefore, we generated and analyzed 35S::GL3 gl2-1 and 35S::EGL3 gl2-1 plants. Each of these lines possessed a `hairy' root phenotype that is essentially the same as the gl2-1 mutant (Table 1). This suggests that a functional GL2 gene is required for the 35S overexpression constructs to induce non-hair epidermal cells, and therefore, is consistent with the notion that the GL3/EGL3 genes act through GL2.
GL3 and EGL3 regulate CPC transcription
The CPC gene is expressed in the N cell position, and it is
required for hair cell specification through a lateral inhibition mechanism
(Lee and Schiefelbein, 2002;
Wada et al., 2002
). To
determine whether CPC is regulated by GL3 and EGL3,
we introduced the CPC::GUS reporter construct into the various mutant
and transgene backgrounds. Like the GL2::GUS expression, the
CPC::GUS expression was reduced in the gl3-1 mutant,
unchanged in the egl3-1 mutant, and virtually eliminated in the
gl3-1 egl3-1 double mutant (Fig.
6; data not shown). Furthermore, the CPC::GUS reporter
was expressed throughout the epidermis in the 35S::EGL3, and to a
weaker extent in the 35S::GL3
(Fig. 6). Thus, the
GL3 and EGL3 genes act in a redundant manner to promote
expression of both the non-hair-cell-specification gene GL2 and the
hair-cell-specification gene CPC in the N cell position.
|
GL3 and EGL3 interact with WER and CPC
In prior studies, the maize R bHLH protein has been found to interact with
both the WER (Lee and Schiefelbein,
1999) and with the CPC (Wada
et al., 2002
) MYB proteins. To examine the possibility that the
GL3 or EGL3 proteins physically associate with WER or CPC, we employed the
yeast two-hybrid assay (Fields and
Sternglanz, 1994
). First, we found that fusions of the GAL4 DNA
binding domain (BD) to either the GL3 or EGL3 protein alone were sufficient to
induce a significant level of lacZ reporter expression
(Table 4). This `one-hybrid'
assay shows that the GL3 and EGL3 proteins possess transcriptional activation
domains that are functional in yeast.
|
We also discovered that GL3 and EGL3 can each associate with the CPC protein in the yeast two-hybrid assay. Yeast cells expressing an AD-CPC fusion together with the BD-GL3 or the BD-EGL3 produce an increased level of lacZ reporter expression (Table 4). This implies that CPC may also interact with GL3 or EGL3 in Arabidopsis, which suggests a possible competition model for the opposite action of WER and CPC in root epidermis cell specification.
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Discussion |
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These results suggest a simple model for the action of the GL3 and EGL3
bHLH proteins in specifying cell fates in the root epidermis
(Fig. 7). This model is largely
consistent with earlier predictions based on results with the heterologous
maize R protein (Galway et al.,
1994; Lee and Schiefelbein,
1999
; Masucci et al.,
1996
). First, the GL3 and EGL3 bHLH proteins are likely to act as
transcriptional regulators in concert with the WER MYB protein. This proposal
is supported by the similar effects of WER and GL3/EGL3 on GL2 and
CPC expression, and their similar effects on early stages of cell
differentiation. Furthermore, it is consistent with the yeast two-hybrid
results showing that GL3 and EGL3 interact with WER, and it is supported by
the WER-dependent nature of the 35S::GL3 or 35S::EGL3
induction of non-hair cells. In plants, it is common for bHLH proteins to act
in a combinatorial fashion with MYB-related proteins to regulate gene
transcription (Singh, 1998
).
The best characterized example is the control of anthocyanin production in
maize, where the tissue-specific activation of the structural genes of the
anthocyanin pathway requires the expression of a bHLH protein encoded by the
maize R or B loci as well as a MYB-related protein encoded by the C1 or Pl
loci (Ludwig and Wessler,
1990
; Mol et al.,
1998
).
|
Another part of our model (Fig.
7) is that the GL3/EGL3 bHLH proteins interact with the CPC
protein in the H position, and this interaction leads to specification of the
hair cell fate. This proposal is derived from two lines of evidence. First,
CPC physically interacts with GL3 or EGL3 in yeast
(Table 4). Second, the ability
of the 35S::GL3 and 35S::EGL3 lines to induce GL2
expression, CPC expression and the non-hair cell fate in the H
position implies that a high concentration of GL3 or EGL3 is sufficient to
alter the fate of the H cells and convert them into non-hair cells.
Considering that WER is required for this effect
(Table 1) and therefore must be
produced/available in the H position, it is possible that, in wild-type roots,
the concentration of GL3/EGL3 available for interaction with WER is low
because most of it is bound to CPC. The 35S::GL3 and
35S::EGL3 phenotypes may then be explained because the excess supply
of these bHLH proteins enables a significant accumulation of the functional
WER-bHLH complex even in the presence of the CPC inhibitor. This explanation
is consistent with a competition mechanism for epidermal patterning that is
essentially similar to one proposed earlier
(Lee and Schiefelbein, 1999).
Accordingly, the epidermal pattern is determined by the relative concentration
of a functional two-repeat MYB (WER) versus an incomplete one-repeat MYB that
lacks a transcriptional activation domain (CPC and probably also TRY). Each of
these MYBs is envisioned to compete for binding to a limited supply of the
GL3/EGL3 bHLH proteins, with the WER-bHLH interaction leading to a functional
transcriptional complex that activates GL2 and CPC, whereas
the CPC-bHLH interaction generates a non-functional complex that leads to hair
cell specification by default (Fig.
7). The cell-type pattern may then result from positional cues and
gene regulatory networks that generate a relatively high concentration of WER
in the N position and a relatively high concentration of CPC (and probably
TRY) in the H position (Fig.
7). We are currently testing various predictions of this
model.
Although we have focused our attention on the seedling root, it is likely
that the action of the GL3 and EGL3 genes is initiated
during embryonic root development, because the epidermal pattern is known to
be established during embryogenesis and each of the other regulators is active
during that period (Costa and Dolan,
2003; Lin and Schiefelbein,
2001
). It is also likely that GL3 and EGL3 help
to establish epidermal cell fate in the hypocotyl because, to date, all of the
regulators that have been examined alter epidermal patterning in the root and
hypocotyl (Berger et al.,
1998b
; Hung et al.,
1998
; Lee and Schiefelbein,
1999
). Future studies will be aimed at testing these
predictions.
In this study, we detected a significant difference in the epidermal cell
pattern in the upper and lower regions of the 4-day-old seedling roots in
several of the bHLH mutants and transgenic lines (Tables
1,
2). The cells that comprise the
upper region are largely formed during embryogenesis and have been termed the
`embryonic root' (Dolan et al.,
1994; Lin and Schiefelbein,
2001
; Scheres et al.,
1994
). It is therefore possible that the GL3 and/or
EGL3 genes or gene products have a different role in epidermal
patterning during embryonic versus post-embryonic development. For example,
the GL3 and EGL3 may differ in their degree of redundancy or
their putative partner proteins in a developmentally dependent manner.
Alternatively, it is possible that epidermal patterning in this region of the
root is generally less `tightly regulated' by the position-dependent mechanism
and therefore more sensitive to genetic perturbation, owing to the proximity
of this region to the root-hypocotyl junction (collet), where every epidermal
cell adopts the hair fate (Dolan et al.,
1994
; Lin and Schiefelbein,
2001
; Scheres et al.,
1994
).
The patterning of epidermal cells in the root appears to employ a mechanism
similar to the one used in the shoot to control trichome distribution
(Larkin et al., 2003;
Schiefelbein, 2003
). This
similarity extends to the use of the GL3 and EGL3 proteins, which have been
shown to participate in trichome specification in a regulatory network
resembling the one described here (Payne
et al., 2000
; Zhang et al.,
2003
). Furthermore, these bHLH proteins participate with TTG in
seed coat development and anthocyanin production
(Zhang et al., 2003
), which
suggests that a common transcriptional cassette operates in all of these
processes and confirms predictions made from studies with the heterologous
maize R protein in Arabidopsis
(Galway et al., 1994
;
Lloyd et al., 1992
).
Our work shows that the GL3 and EGL3 bHLH genes act in a
largely redundant fashion to influence epidermal cell specification in the
root. The lack of a major effect of either single homozygous mutant and the
lack of a synergistic effect in the 35S::GL3 35S::EGL3 line indicates
that the GL3 and EGL3 proteins function in a similar manner. There are two
other Arabidopsis bHLH genes, MYC1
(Urao et al., 1996) and
TT8 (Nesi et al.,
2000
), that are related to the maize R and in the same
subgroup as GL3 and EGL3
(Heim, 2003
). In preliminary
studies, we have found that at least the MYC1 gene probably
participates in root epidermal patterning (C.B., M. Sridharan and J.S.,
unpublished). Thus, an unexpectedly large collection of bHLH genes may play a
role in the specification of epidermal cell fate in the Arabidopsis
root. This probably reflects the importance of genetic redundancy and the
complex regulatory nature of cell specification in higher plants.
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ACKNOWLEDGMENTS |
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