RESEARCH REPORT 1919
Development 140, 1919-1923 (2013) doi:10.1242/dev.094417
© 2013. Published by The Company of Biologists Ltd
ATML1 promotes epidermal cell differentiation in
Arabidopsis shoots
Shinobu Takada*, Nozomi Takada and Ayaka Yoshida
SUMMARY
Molecular mechanisms that generate distinct tissue layers in plant shoots are not well understood. ATML1, an Arabidopsis homeobox
gene, is expressed in the outermost cell layer, beginning at an early stage of development. The promoters of many epidermis-specific
genes, including ATML1, contain an ATML1-binding site called an L1 box, suggesting that ATML1 regulates epidermal cell fate. Here,
we show that overexpression of ATML1 was sufficient to activate the expression of epidermal genes and to induce epidermis-related
traits such as the formation of stomatal guard cells and trichome-like cells in non-epidermal seedling tissues. Detailed observation of
the division planes of these ectopic stomatal cells suggested that a near-surface position, as well as epidermal cell identity, were
required for regular anticlinal cell division, as seen in wild-type epidermis. Moreover, analyses of a loss-of-function mutant and
overexpressors implied that differentiation of epidermal cells was associated with repression of mesophyll cell fate. Collectively, our
studies contribute new information about the molecular basis of cell fate determination in different layers of plant aerial organs.
KEY WORDS: Epidermal cell differentiation, Mesophyll cell differentiation, HD-ZIP class IV transcription factor
Department of Biological Sciences, Graduate School of Science, Osaka University,
1-1 Machikaneyama-cho, Toyonaka, Osaka 560-0043, Japan.
*Author for correspondence ([email protected])
Accepted 25 February 2013
shown to bind to the L1 box in vitro, suggesting that ATML1 and
its homologues may promote epidermis differentiation through the
regulation of the L1 box-containing genes (Abe et al., 2001;
Nakamura et al., 2006). However, it is unclear whether ATML1
alone is sufficient to confer epidermis identity to non-epidermal
cells.
To gain further insight into the mechanisms of ATML1-mediated
regulation of epidermal cell fate, we performed gain-of-function
experiments in combination with analyses of a loss-of-function
mutant and provided evidence that ATML1 is a master regulator for
shoot epidermis identity.
MATERIALS AND METHODS
Plant materials and growth conditions
proATML1-nls-3xGFP, atml1-1;pdf2-1 carrying proATML1-nls-3xGFP,
STOMAGEN-GUS, GL2-GUS (CS8851) and KAT1-GUS (CS3763) lines
have been described previously (Nakamura et al., 1995; Szymanski et al.,
1998; Takada and Jürgens, 2007; Kondo et al., 2010). proATML1-nls3xGFP was used as the wild type.
For estradiol treatment, plants were germinated and grown on Murashige
and Skoog (MS)-Phytagel plates containing 10 µM β-estradiol. β-Estradiol
was dissolved in dimethyl sulphoxide (DMSO). The same volume of
DMSO was added to MS media for control experiments.
Plasmid construction and transgenic plants
The G10 promoter in the pER8 vector was replaced with the promoter
region of AtRPS5A from −1571 to +113 relative to the transcription start
site (RPS5A/pER8) (Zuo et al., 2000; Weijers et al., 2001). The ATML1coding sequence was amplified by PCR using primers 4925 and 4926
(primer sequences are listed in supplementary material Table S1) and
inserted into the XhoI and SpeI sites of the RPS5A/pER8 vector
(proRPS5A-ATML1/pER8).
proRPS5A-ATML1/pER8 was used to transform a proATML1-nls3xGFP line (Takada and Jürgens, 2007). Eight of 35 transgenic lines
exhibited abnormal phenotypes when grown in the presence of 10 µM
estradiol. Four of the eight lines carried T-DNA insertions at a single locus.
Three of the four lines, which showed overexpression of ATML1, were used
for expression analysis. The three lines chosen for subsequent analyses were
designated lines #7, #24 and #35. These transgenic plants did not show an
abnormal phenotype in the absence of estradiol.
DEVELOPMENT
INTRODUCTION
In plants, cotyledons and leaves consist of different cell layers that
include the epidermis, mesophyll and vascular tissues. The
epidermis is a single layer of cells that covers the plant body. Leaf
epidermal cells produce the cuticle, a hydrophobic barrier composed
of lipids and waxes, that reduces water loss and protects plants
against entry of pathogens (reviewed by Samuels et al., 2008). There
are three types of leaf epidermal cells: jigsaw-puzzle-shaped
pavement cells, hair cells (trichomes) and guard cells. These
epidermal cells exhibit mostly anticlinal cell divisions, where the
plane of division is perpendicular to the organ surface. Most
epidermal cells except for guard cells lack chloroplasts, whereas
inner green mesophyll cells develop chloroplasts and
photosynthesize. Despite their important roles in plant development,
the molecular mechanisms that generate distinct tissue layers in
plant shoots are not well understood.
ARABIDOPSIS THALIANA MERISTEM LAYER 1
(ATML1) was the first transcription factor whose expression was
shown to mark the outermost cell layer of the shoot (Lu et al.,
1996; Sessions et al., 1999). ATML1 belongs to the HD-ZIP class
IV homeodomain protein family, which is characterized by a
StAR-related lipid-transfer (START) domain and a zipper-loopzipper (ZLZ) motif (Schrick et al., 2004). Mutations in ATML1
and its closest homologue PROTODERMAL FACTOR 2 (PDF2)
caused the formation of leaves that lack an epidermis, suggesting
that they are required for epidermal cell differentiation (Abe et al.,
2003). Importantly, several ATML1 homologues, as well as other
epidermis-specific genes involved in cuticle biosynthesis,
contained a cis-regulatory element called the L1 box in their
promoters. The L1 box was first discovered as an ATML1-binding
site, and other HD-ZIP class IV transcription factors were also
In situ hybridization
In situ hybridization using digoxigenin-labeled RNA probes was performed
as described previously (Lincoln et al., 1994). The templates for RNA probes
were constructed by cloning a 598 bp region of ATML1 and a 502 bp region
of FDH that were amplified by PCR using primers 6895 and 7021 for ATML1,
and primers 7614 and 7615 for FDH into the EcoRV site of pBluescript
(Stratagene, La Jolla, USA). RNA probes were synthesized using DIG RNA
labeling mix reagent (Roche, Basel, Switzerland). Control experiments using
sense probes gave no signal above background (data not shown).
Histological analysis
For histological sections, samples were embedded in Technovit 7100
(Heraeus Kulzer, Wehrheim, Germany) and cut with a microtome.
For the observation of unfixed tissues in sections, seedlings or leaves
were embedded in 5% agar, and 40-60 µm sections were prepared on
LinearSlicer PRO7 (Dosaka EM, Kyoto, Japan).
Analysis of division planes
Division planes were examined in the mature leaves of 14-day-old line #7
seedlings. Forty-eight sections from seven independent leaves were
observed, and division planes of ectopic stomata were categorized as either
‘anticlinal’, ‘periclinal’ or ‘oblique’, judging from their angles relative to
the nearest adaxial or abaxial surface of the leaves (anticlinal, 0-30° relative
to the surface; periclinal, 60-90°; oblique, 30-60°).
Quantitative RT-PCR analysis
Total RNA was extracted from 7-day-old seedlings using the RNeasy Plant
Mini kit (Qiagen, Venlo, The Netherlands). Total RNA was treated with
amplification grade DNase I (Invitrogen, Carlsbad, USA) and reversetranscribed using Superscript II reverse transcriptase (Invitrogen, Carlsbad,
USA). Real-time PCR reactions were performed using FastStart Universal
SYBR Green Master (Roche, Basel, Switzerland) on an ABI 7300 RealTime PCR System (Applied Biosystems, Foster City, USA). IPT9 and/or
PP2A were used as reference genes (Miyawaki et al., 2004; Czechowski et
al., 2005). No significant signal was detected in the minus reverse
transcriptase control (data not shown). Primer sequences used for real-time
RT-PCR are listed in supplementary material Table S1.
RESULTS AND DISCUSSION
Constitutive expression of ATML1 increased the
expression of epidermis-specific genes
To examine the effects of ATML1 expression on epidermal cell
specification, we generated transgenic lines for estradiol-
Development 140 (9)
inducible overexpression of ATML1 (Fig. 1B,C). We generated
seven lines showing arrested seedling development when
germinated and grown in the presence of 10 µM β-estradiol
(Fig. 1B,C). In these plants, root growth was arrested and shoot
apical meristem activity was also impaired with seedlings only
producing small leaf primordia (Fig. 1B,C). The majority of the
seedlings were small and accumulated anthocyanin. Three
representative lines, carrying T-DNA insertions at a single locus,
had relatively stronger (lines #7 and #24) or weaker (line #35)
expression of ATML1 in the presence of β-estradiol (Fig. 1D;
supplementary material Fig. S1A,B). We examined the
expression of representative L1 box-containing genes that were
uniformly expressed in the shoot epidermis (Fig. 1E;
supplementary material Fig. S1C,D). In these three lines,
transcript
levels
of
endogenous
ATML1,
PDF2,
HOMEODOMAIN GLABROUS2 (HDG2), FIDDLEHEAD
(FDH) and ECERIFERUM 5 (CER5) were increased with
estradiol treatment compared with the wild-type (Fig. 1E;
supplementary material Fig. S1C,D) (Yephremov et al., 1999;
Pruitt et al., 2000; Pighin et al., 2004; Nakamura et al., 2006).
Transcript levels of PROTODERMAL FACTOR 1 (PDF1) did not
increase significantly in lines #7 and #35 (Abe et al., 1999).
Next, we examined the spatial pattern of ATML1 promoter
activity using the proATML1-nls-3xGFP reporter line (Takada and
Jürgens, 2007). Ectopic ATML1 promoter activity was detected in
the inner cells of cotyledons and hypocotyls of the ATML1overexpressing seedlings, indicating that ATML1 induced its
promoter activity in internal tissues (5 out of 5 seedlings for line #7
and 7 out of 7 for line #35; Fig. 2A,B). In situ hybridization
experiments also revealed that epidermis-specific FDH expression
expanded to the inner tissues of cotyledons and hypocotyls in
ATML1-overexpressing plants (5 out of 7 samples for line #7;
Fig. 2E,F). These results showed that constitutive overexpression
of ATML1 induced epidermis-specific genes in the inner tissues of
the seedlings. Conversely, expression of epidermis-specific genes
decreased in the atml1;pdf2 mutant, whereas expression of the
central domain-specific ZWILLE (ZLL) was not significantly
changed (Moussian et al., 1998; Lynn et al., 1999; supplementary
material Fig. S2).
Fig. 1. Estradiol induced constitutive expression of ATML1.
(A-C) Phenotypes of 7-day-old seedlings of the wild type (A),
and inducible lines #7 (B) and #35 (C), grown in the presence of
10 μM estradiol. Scale bars: 0.5 mm. (D,E) Real-time RT-PCR
analysis of L1 box-containing genes. Values are the mean±s.e.m.
of three biological replicates. Data are normalized to the amount
of IPT9 (Miyawaki et al., 2004). (D) ATML1 expression in 7-day-old
seedlings of estradiol-inducible lines (#7 and #35) and the wild
type (WT) grown in the absence (−) or presence (+) of 10 μM
estradiol. (E) Expression of endogenous ATML1, PDF2, HDG2, FDH,
CER5 and PDF1 in 7-day-old seedlings of estradiol-inducible lines
(#7 and #35) and the wild type (WT) grown in the presence of
10 μM estradiol. Expression in the wild type was set to 1.
Asterisks indicate a statistically significant increase relative to the
wild type (unpaired one-tailed t-test; P≤0.05).
DEVELOPMENT
1920 RESEARCH REPORT
Fig. 2. Expression patterns of ATML1 and FDH in the ATML1
overexpressor. (A,B) Longitudinal vibratome sections of seedlings.
proATML1-nls-3xGFP expression in a 10-day-old seedling without estradiol
treatment (A) and a 17-day-old seedling grown with 10 μM estradiol (B).
Arrows indicate ectopic proATML1-nls-3xGFP signals. (C-F) In situ detection
of ATML1 (C,D) and FDH (E,F) mRNA in 7-day-old seedlings of the wild
type (C,E) and the ATML1-overexpressor (D,F). Longitudinal sections are
shown. Scale bars: 100 μm.
Collectively, our results indicate that ATML1-mediated positive
regulation of epidermis-specific genes indeed occurs in planta.
Moreover, our results show that ATML1 does not require epidermisspecific co-factors, such as ligands and other transcription factors
for its activity.
RESEARCH REPORT 1921
Ectopic expression of ATML1 induced epidermisrelated traits in the inner tissues of the
cotyledons and leaves
Next, to examine whether ATML1 can confer epidermis identity
to non-epidermal cells, we performed histological analyses.
Overexpression of ATML1 induced stomata-like structures in the
inner cells of the cotyledons in seven independent lines (Fig. 3B,C;
supplementary material Fig. S3C,F,G,H,I). Ectopic guard cell-like
cells expressed the guard cell marker KAT1-GUS, suggesting that
these cells had guard cell identity (Fig. 3D) (Nakamura et al., 1995).
To determine the effects of overexpression of ATML1 on leaf
development, the estradiol-inducible lines were germinated on
estradiol-free MS plates and transferred to 10 µM estradiol-containing
plates after 5 days. Young leaves that developed after estradiol
treatment were narrower and malformed (data not shown). As in the
case of cotyledons, ectopic guard cells were formed in the inner
tissues of these narrow leaves (Fig. 3G,H,I; supplementary material
Fig. S3D,E). Ectopic stomata in leaves were rarely clustered,
comparable with the pattern seen for wild-type epidermis (P=0.22,
Pearson’s chi-square test), whereas clustering of ectopic stomata was
observed in the cotyledons (supplementary material Fig. S3C).
Although the typical three-branch trichomes, another characteristic
of leaf epidermis, were not found in the inner tissues, large cells
expressing the trichome marker GL2-GUS were observed in the inner
cells of these leaves (Fig. 3F,H,I; four out of six leaves from
independent plants). Surprisingly, overexpression of ATML1 induced
ectopic ATML1 promoter activity and ectopic guard-cell marker
expression in the roots (supplementary material Fig. S4), suggesting
that ATML1 was able to confer a shoot epidermal fate to root cells.
Formation of ectopic stomata and GL2-positive cells indicates that
ATML1 is not merely a positive regulator of a specific cell type in the
epidermis, in contrast to the cases of overexpression of FAMA, a
positive regulator of guard cell fate (Ohashi-Ito and Bergmann, 2006).
Rather, ATML1 appeared to induce pluripotent protodermal cells that
can produce the several different cell types found in the shoot epidermis.
Epidermal cell fate was not sufficient to induce
anticlinal cell division
One of the characteristics of epidermal cells is their anticlinal cell
division. Accordingly, epidermis-deficient mutants abolished
Fig. 3. Overexpression of ATML1 induced epidermisrelated traits in the inner tissues. (A) Transverse section
of a 14-day-old wild-type cotyledon. (B) Longitudinal
section of a cotyledon from a 14-day-old ATML1overexpressing plant. (C) Magnified view of the boxed
area in B. (D) KAT1-GUS expression in a longitudinal
section of a cotyledon from a 14-day-old ATML1overexpressing plant. Arrows indicate ectopic guard cells;
arrowhead indicates a normal guard cell. (E,F) Sections of
mature leaves from 14-day-old wild-type (E) and ATML1overexpressing (F) plants carrying GL2-GUS. Arrows
indicate GL2-GUS-positive cells in the inner tissues;
arrowheads indicate trichomes. (G-I) Transverse sections
of mature leaves from 14-day-old ATML1-overexpressing
plants carrying GL2-GUS. Arrows in G indicate stomata
that were apparently generated by anticlinal cell
divisions. Asterisks in E,H,I indicate intercellular gaps.
Sections are stained with Toluidine Blue in A-C and
safranin O in E-I. Scale bars: 100 μm for A,B,D-F,H,I; 20 μm
for C; 50 μm for G.
DEVELOPMENT
ATML1 specifies epidermal fate
Development 140 (9)
1922 RESEARCH REPORT
differentiation. Mesophyll-specific STOMAGEN-GUS expression
was severely depressed in the seedlings of the strong ATML1overexpressor (Kondo et al., 2010; Fig. 4B). Induction of ATML1 at
5 days after germination resulted in malformed leaves with ectopic
patches of transparent cells among the green mesophyll tissues
(Fig. 4D; supplementary material Fig. S3D).
The fact that ectopic ATML1 induction decreased mesophyll cell
differentiation led us to assume that mesophyll cell fate may be
negatively regulated by ATML1 in the outermost cell layer. In
support of this idea, atml1;pdf2 produced leaves with mesophyll
cells on the surface (Fig. 4E-G) (Abe et al., 2003). In order to
determine whether this phenotype is due to a conversion of
epidermis into mesophyll cells or due to degradation of the surface
epidermis, we carefully observed proATML1-nls-3xGFP expression
in the atml1;pdf2 leaves. Our results showed that proATML1-nls3xGFP was still expressed in some green mesophyll cells near the
surface of the atml1;pdf2 leaves (Fig. 4F,H). One interpretation of
this observation is that the outermost cells initially specified as
epidermis (and hence proATML1-nls-3xGFP positive) partially
obtained mesophyll cell identity in the absence of ATML1 and
PDF2 activities. In conclusion, these results were consistent with
the idea that ATML1 and/or epidermis identity antagonize
mesophyll cell differentiation and that loss of epidermal cell identity
is associated with ectopic mesophyll cell development in the
outermost cell layer.
regular anticlinal cell divisions in the outermost cell layer (Tanaka
et al., 2007). This observation led us to expect that overexpression
of ATML1 may cause ectopic anticlinal cell divisions in the inner
tissues. However, in the ATML1-overexpressing plants, division
planes that separate two guard cells were approximately anticlinal
(41.0%), periclinal (29.3%) or oblique (29.8%) relative to the
adaxial or abaxial surface of the organ, indicating that epidermis
identity alone was necessary, but not sufficient, for anticlinal cell
division (supplementary material Fig. S5A). By contrast, the cell
walls separating the two guard cells of ectopic stomata formed in the
subepidermal L2 cell layer were often anticlinal (Fig. 3G;
supplementary material Fig. S5B). Interestingly, we noticed that
stomatal pores had a tendency to face towards inner air spaces in the
mesophyll (Fig. 3H,I; supplementary material Fig. S5C); guard
mother cells appeared to divide anticlinally (i.e. perpendicular to
the inner surface) to form these stomatal pores. These observations
raised the fascinating possibility that ‘surface proximity’ as well as
‘epidermis identity’ is required for anticlinal cell division.
ATML1 negatively influences mesophyll cell
differentiation
To investigate whether ectopic ATML1 induction had negative
effects on inner cell fate, we examined mesophyll cell
Acknowledgements
We thank Prof. Nam-Hai Chua (Rockefeller University, USA) for providing the
pER8 vector, Prof. Tatsuo Kakimoto (Osaka University, Japan) for STOMAGENGUS seeds and the Arabidopsis Biological Resource Center for marker lines.
Funding
This work was supported by grants from the Japan Society for the Promotion
of Science [20657012, 22687003 and 23657036 to S.T.].
Competing interests statement
The authors declare no competing financial interests.
Supplementary material
Supplementary material available online at
http://dev.biologists.org/lookup/suppl/doi:10.1242/dev.094417/-/DC1
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DEVELOPMENT
ATML1 specifies epidermal fate