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508
Plant cells — young at heart?
Arp Schnittger*, Swen Schellmann† and Martin Hülskamp‡
Dolly has become a synonym for one of the greatest
breakthroughs in animal reproductive biology: the regeneration of
a whole mammal from a somatic cell nucleus. The equivalent
experiments in plants — the regeneration of whole plants from
single differentiated cells — are comparatively easy. Does this
apparent difference in the developmental potential of animal and
plant somatic cells reflect mechanistic differences in the
regulation and maintenance of their respective cell differentiation?
Addresses
ZMBP, Entwicklungsgenetik, Universität Tübingen, Auf der
Morgenstelle 1, D-72076 Tübingen, Germany
*e-mail: arp.schnittger@uni-tuebingen.de
†e-mail: swen.schellman@uni-tuebingen.de
‡e-mail: martin.huelskamp@uni-tuebingen.de
Current Opinion in Plant Biology 1999, 2:508–512
1369-5266/99/$ — see front matter © 1999 Elsevier Science Ltd.
All rights reserved.
Abbreviation
GFP
green fluorescent protein
Introduction
During normal development, most cells enter specific differentiation programs that change their physiological and
morphological properties. As cell differentiation progresses
it is believed that the potential of cells to change their
developmental specialization is increasingly restricted
(Figure 1). To understand differences in the developmental potential of animal and plant cells it is therefore
important to explore the role of the mechanisms that initiate and maintain cell differentiation.
Most of our knowledge about the regulation of cell differentiation comes from animal studies. In animal cells,
differentiation is controlled by the interplay of intrinsic
systems that operate in a cell-autonomous manner and
extrinsic signals that are received from the surrounding tissue [1] (Figure 1). In some cases, such as the stem cells,
continuous extrinsic signaling is necessary to maintain differentiation throughout development [2]. Usually, cell
differentiation is maintained by intrinsic systems, such as
the cell-cycle machinery or chromatin-dependent gene
silencing. During recent years evidence has accumulated
to suggest that the mechanisms underlying the regulation
of cell differentiation in plants are similar to those already
known in animals. Our review discusses examples of the
respective roles of intrinsic and extrinsic signals in the regulation of cell differentiation in plants.
Extrinsic control of cell differentiation states
A well-studied example of the extrinsic control of cell differentiation in plants is the specification of stem cells. In
plants, stem cells are found in small populations in the
shoot and root meristems where they remain in an undifferentiated state before undergoing differentiation to give
rise to most tissues of the mature plant [3,4].
In the root meristem, stem cells are located in immediate
contact with a group of four nondividing cells, which are
collectively known as the quiescent center, and that are
the initials of different cell types [5] (Figure 2a). In a series
of ablation experiments it was demonstrated that the
removal of a single quiescent center cell resulted in the
differentiation of those stem cells that had been in immediate contact with it [6]. This finding indicates that
differentiation in root stem cells is inhibited by short-range
signaling from the quiescent center cells.
As in the root, stem cells in the shoot meristem are also
specified nonautonomously. Maintaining shoot stem cells
requires the activity of WUSCHEL (WUS), a gene that
encodes a homeodomain protein [7••]. WUS is expressed
in a small group of cells that are found immediately below
the stem cells, the WUS domain (Figure 2b). A second
gene involved in stem cell specification is ZWILLE (ZLL)
[8•], which is allelic to PINHEAD [9]. ZLL encodes a
protein that is homologous to the translation initiation
factor eIF2C. During the initial stages of shoot meristem
formation in embryogenesis, and also during postembryonic development, ZLL is expressed in the
vascular precursor cells, which are found below the WUS
domain (Figure 2b). In zll mutants all apical cells differentiate, suggesting that ZLL-dependent long-range
signaling is required for the maintenance of stem cells.
One possibility is that ZLL positions the WUS expression
domain correctly (T Laux, personal communication).
Interestingly, the ZLL homolog in Drosophila, the PIWI
gene, is required for the nonautonomous maintenance of
stem cells in the germ line [10]. A ZLL homolog in
Caenorhabditis elegans has also been implicated in germ
cell maintenance [10].
Cell proliferation occurs only along the central-peripheral axis
of the meristem where stem cells form a core of slowly dividing undifferentiated cells. On leaving the core, cells
proliferate more rapidly and begin to differentiate. The
dynamic of this system poses the question of how the balance
between stem cell self-renewal and differentiation might be
maintained. Two recent findings suggest that a group of three
genes, the CLAVATA (CLV) genes, are involved in this process.
The CLV genes encode components of a receptor–ligand system that controls the size of the meristem [11,12,13••]. The
increased meristem size of clv mutants is mainly due to their
enlarged stem cell population. The central domain of slowly
dividing cells, one of the main characteristics of stem cells, has
Plant cells — young at heart? Schnittger, Schellmann and Hülskamp
509
Figure 1
(a)
(b)
Undifferentiated cell
Stem cell
WUS, ZLL, CLV
Differentiated cell
Protodermal cell
?
Tissue-layer signals
e.g. GL1
expression,
endoreduplication,
branching
elongation
GL1
Trichome cell
Extrinsic signals
Intrinsic signals
e.g. Gene
expression,
morphological
changes,
physiological
changes
Extrinsic signals
Intrinsic signals
e.g. AtML1
expression [43]
Tissue-layer signals
Current Opinion in Plant Biology
The regulation of cell differentiation. (a) The progression from an
undifferentiated cell to a differentiated cell involves changes in
properties such as gene expression, morphology and physiology.
These changes are associated with a loss of potential for cells to
change their developmental specialization. Both of these aspects are
controlled by the combination of extrinsic and intrinsic signals.
Generally, intrinsic signals become more important in later stages of
development. (b) The progression from stem cells to trichome cells as
an example of the progression of cell differentiation. Note, that during
trichome differentiation intrinsic factors, as exemplified by GL1
expression, become more important than extrinsic signals.
been shown to be larger in clv3 mutants than in wildtypes
[14•]. In addition, it was shown that CLV3 is specifically
expressed in the presumptive stem cells, and hence it can be
considered as a molecular stem cell marker [13••] (Figure 2b).
In clv1 and clv3 mutants the expression domain of CLV3expressing cells is expanded, supporting the idea that the
number of stem cells is greatly increased by these mutations
[13••]. Thus, the CLV group seems to play a vital role in promoting the transition from stem to non-stem cells. The links
between the CLV and WUS-dependent control of stem cell
maintenance are not understood. It will be interesting
to know whether CLV-dependent stem cell control acts
independently of WUS, or whether the CLV genes are
involved in the regulation of WUS.
Intrinsic control of cell differentiation states
In animals, the onset of cell differentiation is closely associated with changes to intrinsic systems, such as the cell
cycle or chromatin-dependent gene silencing [1].
The role of the cell cycle and endoreduplication in cell
differentiation
A correlation between cell differentiation and cell cycle
regulation is also observed during leaf hair (trichome)
Figure 2
(a)
(b)
L1
stele
L2
end
cort
epi
CLV3
Models for stem-cell maintenance in the root
and shoot meristem. (a) In the root meristem,
the quiescent center (QC) functions as an
organizing center. Those cells in immediate
contact with the QC are stem cells (dark
shading), which are initials for all cell files:
endodermis (end), cortex (cort), epidermis
(epi), lateral root cap (lrc) and columella (col).
(b) In the shoot meristem, WUS is functionally
equivalent to the QC in the root meristem in
maintaining the presence of stem cells (dark
shading). Long-range signaling for stem cell
maintenance is also postulated for ZLL, which
is expressed in the vascular cells. CLV3 is
expressed in the presumptive stem cells that
are the initials for the L1 (epidermis), L2
(subepidermal tissues, i.e. mesophyll cells)
and L3 (subepidermal tissues, i.e. vascular
cells) tissue layers.
L3
L1
L2
L3
WUS
QC
Irc
ZLL
col
Current Opinion in Plant Biology
510
Cell biology
development. Trichomes are initiated at the base of young
leaves in a field of dividing cells [15,16]. In experiments in
which trichome formation was induced by the overexpression of known positive regulators of trichome initiation, it
was shown that trichome initiation is only possible in tissues that are proliferating. This was demonstrated in
Arabidopsis by plants overexpressing the maize R gene [17]
and in tobacco plants overexpressing the Anthirrinum
MIXTA gene [18].
Trichome initiation is closely coupled with the onset of
endoreduplication [19]. Trichome precursor cells stop dividing but continue DNA replication. In addition, it has been
shown that two genes that are involved in trichome initiation
are also important in regulating the number of endoreduplication cycles. Overexpression of GLABRA1 (GL1), a positive
regulator of trichome initiation, promotes further endoreduplication cycles in trichome cells [20••]. Mutations in the
TRIPTYCHON (TRY) gene, a negative regulator of trichome
initiation, also result in an increased DNA content [20••].
Although GL1 and TRY may have independent functions in
trichome patterning and endoreduplication, an attractive
hypothesis is that the initiation of trichome development by
these two genes is directly linked to the cell cycle machinery.
An expanding role of cell cycle regulators in plants?
During recent years evidence has accumulated to show
that, in animals, various cell cycle genes are involved not
only in the regulation of the cell cycle, but also directly in
cell differentiation [21]. For example, proteins encoded by
p21 CKI, an inhibitor of mitosis, and that encoded by
Retinoblastoma (Rb), an inhibitor of cell cycle progression,
also affect the cell differentiation of keratinocytes and
myoblasts, respectively [22,23]. There is scant evidence of
a direct role of cell cycle genes in plant cell differentiation.
Some observations, however, now suggest a connection
between cell cycle regulation and cell differentiation in
plants. In Arabidopsis, leaf aging and differentiation are
associated with increased expression of CYCLIN DEPENDENT KINASE INHIBITOR1 (ICK1) [24], which shows
homology to p21 CKI. Similarly, in maize, leaf tissues containing older, differentiated cells show higher
concentrations of Rb than do younger leaf tissues [25]. It is
tempting to speculate that these plant homologs are also
directly involved in cell differentiation. More direct evidence of an additional role for a cell cycle gene in
differentiation was found for CycD3 in Arabidopsis [26••].
Expression of CycD3 activates cell divisions at the G1–S
cell cycle phase transition. Plants overexpressing CycD3
have abnormal meristems and leaves. Calli that have been
transformed so that they express CycD3 differentiate,
become green and cannot be regenerated to form shoots.
These findings suggest that CycD3 has an additional role in
the regulation of cell differentiation.
Chromatin-dependent gene silencing
In animals, chromatin-dependent gene silencing is a common mechanism for maintaining cell differentiation. In
Drosophila, a large number of genes, known collectively as
the Polycomb (Pc) group, regulate the accessibility of chromosomal regions, and as a consequence transcriptionally
repress gene expression in particular chromosomal
regions [27].
The first Pc-like gene described in plants is the CURLY
LEAF (CLF) gene of Arabidopsis. clf mutants display a wide
range of morphological defects in their leaves and flowers
[28]. Most of these defects are caused by the ectopic expression of the floral homeotic gene AGAMOUS (AG), indicating
that CLF represses the expression of AG. Pc genes also play
an important role in suppressing the development of unfertilized seeds. In medea (mea) and fertilization-independent
endosperm (fie) mutants endosperm and sometimes also
embryo development is initiated without fertilization
[29•,30,31]. The two proteins which are defective in these
mutants contain motifs found in the Pc-group proteins of
Drosophila: MEA contains a SET domain similar to enhancer
of zeste [29•,32•,33•], and FIE shares a sequence identity
with the WD domain of extra sex combs [34•].
On the basis of homology with their animal counterparts,
Pc-like proteins are thought to function as chromatin regulators in plants. The current data, however, are consistent
with the involvement of Pc-like proteins in three different
mechanisms of gene regulation.
First, evidence of the conservation of a function for Pclike proteins in the regulation of chromatin comes from
recent experiments in which a green fluorescent protein
(GFP) that had been fused with the Drosophila Pc-chromodomain was expressed in tobacco [35•]. In Drosophila,
the chromodomain mediates the targeting of Pc to specific chromosomal regions through protein–protein
interactions [36]. The Drosophila chromodomain has been
shown to bind to distinct chromosomal regions in tobacco,
and its overexpression caused a variety of morphological
defects during the development of tobacco, including
curly leaves or abnormal flower development. The data
suggest that the heterologous chromodomain interferes
with an endogenous chromatin-regulating mechanism.
Because the Drosophila chromodomain is thought to function only as part of a large protein complex, these findings
suggest that the underlying molecular mechanisms
involved in regulating chromatin are conserved in both
animals and plants.
Second, the methylation of DNA is a mechanism which is
involved in the control of gene transcription in both animals
and plants. Although there is no evidence of a link between
Pc-regulated chromatin silencing and the methylationdependent regulation of gene expression in animals, two
observations suggest a connection in plants. Plants containing an antisense construct of the Arabidopsis cytosine DNA
methyltransferase, MET1, display a phenotype that resembles that of clf mutants: the leaves are curled and two floral
homeotic genes, AG and APETALA3, are ectopically
Plant cells — young at heart? Schnittger, Schellmann and Hülskamp
expressed [37,38]. The recent identification of CMT1, a
DNA methyltransferase containing a chromodomain in
Arabidopsis, also suggests that chromodomain-targeted
repression of downstream genes can result from DNA
methylation [39•].
Third, the suppression of seed development by MEA and
FIE could involve transcriptional regulation via DNA binding, rather than chromatin regulation. fertilization independent
seed (fis2) mutants show the same phenotype as mea and fie
mutants and FIS2 encodes a putative zinc-finger transcription factor [34•]. Although it is possible that FIS2
transcriptionally activates MEA and FIE, an alternative
explanation is that FIS2 forms a complex with MEA and
FIE and targets them to particular promotor regions, which
regulate the transcriptional activation of downstream genes.
Intrinsic programs versus extrinsic cues
It is difficult to determine the extent to which differentiated cells are kept in their differentiated state by intrinsic
programs, or by continuous tissue-specific signaling. Some
information that relates to tissue-layer-specific cell differentiation is available. Three distinct tissue layers are
established during embryogenesis and remain separate
throughout development [40]. Each tissue layer gives rise
to specific cell types. The analysis of chimeras has shown
that cells that are displaced from the epidermal cell layer to
a subepidermal layer change their fate according to their
new position [41]. This implies that tissue-layer-specific
positional information continuously determines the fate of
cells according to their position. It was therefore surprising
to find that tissue-layer-specific restrictions can be overriden by manipulating the expression of genes required for
the initiation of one epidermis-specific cell type.
Overexpression of one key positive regulator of trichome
initiation, GL1, a myb-homolog transcription factor, in the
absence of the important negative regulator, TRY, is sufficient to trigger trichome formation in the subepidermal
tissue layers [20••,42••]. As GL1 and TRY are both cell-typespecific regulators, they can be considered as intrinsic
factors that can overcome extrinsic cues (Figure 1b). This
result is remarkable because it lacks a counterpart in animal
systems suggesting that, in animals, tissue-layer-specific
signals impose tighter restrictions on the fate of cells.
Conclusions
Plant development is evidently more flexible than animal
development in many respects. It is conceivable that this difference in flexibility is due to the fact that cell differentiation
in plants is based more on extrinsic regulation than that in
animals. However, plants and animals clearly share various
mechanisms that control their differentiation state. This, in
turn, implies that the difference between animal and plant
cells is in the extent to which commitment is irreversible.
Acknowledgements
We thank members of the Zentrum für Molekularbiologie der Pflanzen
(Center of Plant Molecular Biology) for reading this manuscript critically.
511
Work in the authors’ laboratory is supported by the Volkswagen Stiftung and
by grants from the Deutsche Forschungsgemeinschaft.
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Plant cells — young at heart?
Arp Schnittger*, Swen Schellmann† and Martin Hülskamp‡
Dolly has become a synonym for one of the greatest
breakthroughs in animal reproductive biology: the regeneration of
a whole mammal from a somatic cell nucleus. The equivalent
experiments in plants — the regeneration of whole plants from
single differentiated cells — are comparatively easy. Does this
apparent difference in the developmental potential of animal and
plant somatic cells reflect mechanistic differences in the
regulation and maintenance of their respective cell differentiation?
Addresses
ZMBP, Entwicklungsgenetik, Universität Tübingen, Auf der
Morgenstelle 1, D-72076 Tübingen, Germany
*e-mail: arp.schnittger@uni-tuebingen.de
†e-mail: swen.schellman@uni-tuebingen.de
‡e-mail: martin.huelskamp@uni-tuebingen.de
Current Opinion in Plant Biology 1999, 2:508–512
1369-5266/99/$ — see front matter © 1999 Elsevier Science Ltd.
All rights reserved.
Abbreviation
GFP
green fluorescent protein
Introduction
During normal development, most cells enter specific differentiation programs that change their physiological and
morphological properties. As cell differentiation progresses
it is believed that the potential of cells to change their
developmental specialization is increasingly restricted
(Figure 1). To understand differences in the developmental potential of animal and plant cells it is therefore
important to explore the role of the mechanisms that initiate and maintain cell differentiation.
Most of our knowledge about the regulation of cell differentiation comes from animal studies. In animal cells,
differentiation is controlled by the interplay of intrinsic
systems that operate in a cell-autonomous manner and
extrinsic signals that are received from the surrounding tissue [1] (Figure 1). In some cases, such as the stem cells,
continuous extrinsic signaling is necessary to maintain differentiation throughout development [2]. Usually, cell
differentiation is maintained by intrinsic systems, such as
the cell-cycle machinery or chromatin-dependent gene
silencing. During recent years evidence has accumulated
to suggest that the mechanisms underlying the regulation
of cell differentiation in plants are similar to those already
known in animals. Our review discusses examples of the
respective roles of intrinsic and extrinsic signals in the regulation of cell differentiation in plants.
Extrinsic control of cell differentiation states
A well-studied example of the extrinsic control of cell differentiation in plants is the specification of stem cells. In
plants, stem cells are found in small populations in the
shoot and root meristems where they remain in an undifferentiated state before undergoing differentiation to give
rise to most tissues of the mature plant [3,4].
In the root meristem, stem cells are located in immediate
contact with a group of four nondividing cells, which are
collectively known as the quiescent center, and that are
the initials of different cell types [5] (Figure 2a). In a series
of ablation experiments it was demonstrated that the
removal of a single quiescent center cell resulted in the
differentiation of those stem cells that had been in immediate contact with it [6]. This finding indicates that
differentiation in root stem cells is inhibited by short-range
signaling from the quiescent center cells.
As in the root, stem cells in the shoot meristem are also
specified nonautonomously. Maintaining shoot stem cells
requires the activity of WUSCHEL (WUS), a gene that
encodes a homeodomain protein [7••]. WUS is expressed
in a small group of cells that are found immediately below
the stem cells, the WUS domain (Figure 2b). A second
gene involved in stem cell specification is ZWILLE (ZLL)
[8•], which is allelic to PINHEAD [9]. ZLL encodes a
protein that is homologous to the translation initiation
factor eIF2C. During the initial stages of shoot meristem
formation in embryogenesis, and also during postembryonic development, ZLL is expressed in the
vascular precursor cells, which are found below the WUS
domain (Figure 2b). In zll mutants all apical cells differentiate, suggesting that ZLL-dependent long-range
signaling is required for the maintenance of stem cells.
One possibility is that ZLL positions the WUS expression
domain correctly (T Laux, personal communication).
Interestingly, the ZLL homolog in Drosophila, the PIWI
gene, is required for the nonautonomous maintenance of
stem cells in the germ line [10]. A ZLL homolog in
Caenorhabditis elegans has also been implicated in germ
cell maintenance [10].
Cell proliferation occurs only along the central-peripheral axis
of the meristem where stem cells form a core of slowly dividing undifferentiated cells. On leaving the core, cells
proliferate more rapidly and begin to differentiate. The
dynamic of this system poses the question of how the balance
between stem cell self-renewal and differentiation might be
maintained. Two recent findings suggest that a group of three
genes, the CLAVATA (CLV) genes, are involved in this process.
The CLV genes encode components of a receptor–ligand system that controls the size of the meristem [11,12,13••]. The
increased meristem size of clv mutants is mainly due to their
enlarged stem cell population. The central domain of slowly
dividing cells, one of the main characteristics of stem cells, has
Plant cells — young at heart? Schnittger, Schellmann and Hülskamp
509
Figure 1
(a)
(b)
Undifferentiated cell
Stem cell
WUS, ZLL, CLV
Differentiated cell
Protodermal cell
?
Tissue-layer signals
e.g. GL1
expression,
endoreduplication,
branching
elongation
GL1
Trichome cell
Extrinsic signals
Intrinsic signals
e.g. Gene
expression,
morphological
changes,
physiological
changes
Extrinsic signals
Intrinsic signals
e.g. AtML1
expression [43]
Tissue-layer signals
Current Opinion in Plant Biology
The regulation of cell differentiation. (a) The progression from an
undifferentiated cell to a differentiated cell involves changes in
properties such as gene expression, morphology and physiology.
These changes are associated with a loss of potential for cells to
change their developmental specialization. Both of these aspects are
controlled by the combination of extrinsic and intrinsic signals.
Generally, intrinsic signals become more important in later stages of
development. (b) The progression from stem cells to trichome cells as
an example of the progression of cell differentiation. Note, that during
trichome differentiation intrinsic factors, as exemplified by GL1
expression, become more important than extrinsic signals.
been shown to be larger in clv3 mutants than in wildtypes
[14•]. In addition, it was shown that CLV3 is specifically
expressed in the presumptive stem cells, and hence it can be
considered as a molecular stem cell marker [13••] (Figure 2b).
In clv1 and clv3 mutants the expression domain of CLV3expressing cells is expanded, supporting the idea that the
number of stem cells is greatly increased by these mutations
[13••]. Thus, the CLV group seems to play a vital role in promoting the transition from stem to non-stem cells. The links
between the CLV and WUS-dependent control of stem cell
maintenance are not understood. It will be interesting
to know whether CLV-dependent stem cell control acts
independently of WUS, or whether the CLV genes are
involved in the regulation of WUS.
Intrinsic control of cell differentiation states
In animals, the onset of cell differentiation is closely associated with changes to intrinsic systems, such as the cell
cycle or chromatin-dependent gene silencing [1].
The role of the cell cycle and endoreduplication in cell
differentiation
A correlation between cell differentiation and cell cycle
regulation is also observed during leaf hair (trichome)
Figure 2
(a)
(b)
L1
stele
L2
end
cort
epi
CLV3
Models for stem-cell maintenance in the root
and shoot meristem. (a) In the root meristem,
the quiescent center (QC) functions as an
organizing center. Those cells in immediate
contact with the QC are stem cells (dark
shading), which are initials for all cell files:
endodermis (end), cortex (cort), epidermis
(epi), lateral root cap (lrc) and columella (col).
(b) In the shoot meristem, WUS is functionally
equivalent to the QC in the root meristem in
maintaining the presence of stem cells (dark
shading). Long-range signaling for stem cell
maintenance is also postulated for ZLL, which
is expressed in the vascular cells. CLV3 is
expressed in the presumptive stem cells that
are the initials for the L1 (epidermis), L2
(subepidermal tissues, i.e. mesophyll cells)
and L3 (subepidermal tissues, i.e. vascular
cells) tissue layers.
L3
L1
L2
L3
WUS
QC
Irc
ZLL
col
Current Opinion in Plant Biology
510
Cell biology
development. Trichomes are initiated at the base of young
leaves in a field of dividing cells [15,16]. In experiments in
which trichome formation was induced by the overexpression of known positive regulators of trichome initiation, it
was shown that trichome initiation is only possible in tissues that are proliferating. This was demonstrated in
Arabidopsis by plants overexpressing the maize R gene [17]
and in tobacco plants overexpressing the Anthirrinum
MIXTA gene [18].
Trichome initiation is closely coupled with the onset of
endoreduplication [19]. Trichome precursor cells stop dividing but continue DNA replication. In addition, it has been
shown that two genes that are involved in trichome initiation
are also important in regulating the number of endoreduplication cycles. Overexpression of GLABRA1 (GL1), a positive
regulator of trichome initiation, promotes further endoreduplication cycles in trichome cells [20••]. Mutations in the
TRIPTYCHON (TRY) gene, a negative regulator of trichome
initiation, also result in an increased DNA content [20••].
Although GL1 and TRY may have independent functions in
trichome patterning and endoreduplication, an attractive
hypothesis is that the initiation of trichome development by
these two genes is directly linked to the cell cycle machinery.
An expanding role of cell cycle regulators in plants?
During recent years evidence has accumulated to show
that, in animals, various cell cycle genes are involved not
only in the regulation of the cell cycle, but also directly in
cell differentiation [21]. For example, proteins encoded by
p21 CKI, an inhibitor of mitosis, and that encoded by
Retinoblastoma (Rb), an inhibitor of cell cycle progression,
also affect the cell differentiation of keratinocytes and
myoblasts, respectively [22,23]. There is scant evidence of
a direct role of cell cycle genes in plant cell differentiation.
Some observations, however, now suggest a connection
between cell cycle regulation and cell differentiation in
plants. In Arabidopsis, leaf aging and differentiation are
associated with increased expression of CYCLIN DEPENDENT KINASE INHIBITOR1 (ICK1) [24], which shows
homology to p21 CKI. Similarly, in maize, leaf tissues containing older, differentiated cells show higher
concentrations of Rb than do younger leaf tissues [25]. It is
tempting to speculate that these plant homologs are also
directly involved in cell differentiation. More direct evidence of an additional role for a cell cycle gene in
differentiation was found for CycD3 in Arabidopsis [26••].
Expression of CycD3 activates cell divisions at the G1–S
cell cycle phase transition. Plants overexpressing CycD3
have abnormal meristems and leaves. Calli that have been
transformed so that they express CycD3 differentiate,
become green and cannot be regenerated to form shoots.
These findings suggest that CycD3 has an additional role in
the regulation of cell differentiation.
Chromatin-dependent gene silencing
In animals, chromatin-dependent gene silencing is a common mechanism for maintaining cell differentiation. In
Drosophila, a large number of genes, known collectively as
the Polycomb (Pc) group, regulate the accessibility of chromosomal regions, and as a consequence transcriptionally
repress gene expression in particular chromosomal
regions [27].
The first Pc-like gene described in plants is the CURLY
LEAF (CLF) gene of Arabidopsis. clf mutants display a wide
range of morphological defects in their leaves and flowers
[28]. Most of these defects are caused by the ectopic expression of the floral homeotic gene AGAMOUS (AG), indicating
that CLF represses the expression of AG. Pc genes also play
an important role in suppressing the development of unfertilized seeds. In medea (mea) and fertilization-independent
endosperm (fie) mutants endosperm and sometimes also
embryo development is initiated without fertilization
[29•,30,31]. The two proteins which are defective in these
mutants contain motifs found in the Pc-group proteins of
Drosophila: MEA contains a SET domain similar to enhancer
of zeste [29•,32•,33•], and FIE shares a sequence identity
with the WD domain of extra sex combs [34•].
On the basis of homology with their animal counterparts,
Pc-like proteins are thought to function as chromatin regulators in plants. The current data, however, are consistent
with the involvement of Pc-like proteins in three different
mechanisms of gene regulation.
First, evidence of the conservation of a function for Pclike proteins in the regulation of chromatin comes from
recent experiments in which a green fluorescent protein
(GFP) that had been fused with the Drosophila Pc-chromodomain was expressed in tobacco [35•]. In Drosophila,
the chromodomain mediates the targeting of Pc to specific chromosomal regions through protein–protein
interactions [36]. The Drosophila chromodomain has been
shown to bind to distinct chromosomal regions in tobacco,
and its overexpression caused a variety of morphological
defects during the development of tobacco, including
curly leaves or abnormal flower development. The data
suggest that the heterologous chromodomain interferes
with an endogenous chromatin-regulating mechanism.
Because the Drosophila chromodomain is thought to function only as part of a large protein complex, these findings
suggest that the underlying molecular mechanisms
involved in regulating chromatin are conserved in both
animals and plants.
Second, the methylation of DNA is a mechanism which is
involved in the control of gene transcription in both animals
and plants. Although there is no evidence of a link between
Pc-regulated chromatin silencing and the methylationdependent regulation of gene expression in animals, two
observations suggest a connection in plants. Plants containing an antisense construct of the Arabidopsis cytosine DNA
methyltransferase, MET1, display a phenotype that resembles that of clf mutants: the leaves are curled and two floral
homeotic genes, AG and APETALA3, are ectopically
Plant cells — young at heart? Schnittger, Schellmann and Hülskamp
expressed [37,38]. The recent identification of CMT1, a
DNA methyltransferase containing a chromodomain in
Arabidopsis, also suggests that chromodomain-targeted
repression of downstream genes can result from DNA
methylation [39•].
Third, the suppression of seed development by MEA and
FIE could involve transcriptional regulation via DNA binding, rather than chromatin regulation. fertilization independent
seed (fis2) mutants show the same phenotype as mea and fie
mutants and FIS2 encodes a putative zinc-finger transcription factor [34•]. Although it is possible that FIS2
transcriptionally activates MEA and FIE, an alternative
explanation is that FIS2 forms a complex with MEA and
FIE and targets them to particular promotor regions, which
regulate the transcriptional activation of downstream genes.
Intrinsic programs versus extrinsic cues
It is difficult to determine the extent to which differentiated cells are kept in their differentiated state by intrinsic
programs, or by continuous tissue-specific signaling. Some
information that relates to tissue-layer-specific cell differentiation is available. Three distinct tissue layers are
established during embryogenesis and remain separate
throughout development [40]. Each tissue layer gives rise
to specific cell types. The analysis of chimeras has shown
that cells that are displaced from the epidermal cell layer to
a subepidermal layer change their fate according to their
new position [41]. This implies that tissue-layer-specific
positional information continuously determines the fate of
cells according to their position. It was therefore surprising
to find that tissue-layer-specific restrictions can be overriden by manipulating the expression of genes required for
the initiation of one epidermis-specific cell type.
Overexpression of one key positive regulator of trichome
initiation, GL1, a myb-homolog transcription factor, in the
absence of the important negative regulator, TRY, is sufficient to trigger trichome formation in the subepidermal
tissue layers [20••,42••]. As GL1 and TRY are both cell-typespecific regulators, they can be considered as intrinsic
factors that can overcome extrinsic cues (Figure 1b). This
result is remarkable because it lacks a counterpart in animal
systems suggesting that, in animals, tissue-layer-specific
signals impose tighter restrictions on the fate of cells.
Conclusions
Plant development is evidently more flexible than animal
development in many respects. It is conceivable that this difference in flexibility is due to the fact that cell differentiation
in plants is based more on extrinsic regulation than that in
animals. However, plants and animals clearly share various
mechanisms that control their differentiation state. This, in
turn, implies that the difference between animal and plant
cells is in the extent to which commitment is irreversible.
Acknowledgements
We thank members of the Zentrum für Molekularbiologie der Pflanzen
(Center of Plant Molecular Biology) for reading this manuscript critically.
511
Work in the authors’ laboratory is supported by the Volkswagen Stiftung and
by grants from the Deutsche Forschungsgemeinschaft.
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