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4.3. How does phosphorylation affect transcription factor function?
5. Regulation of Stomatal Asymmetric Cell Division
5.1. Models of asymmetric cell division
5.2. Stomatal asymmetric cell division
5.3. Polarized receptor protein: PAN1 from maize
5.4. Polarized and segregated novel protein: BASL in Arabidopsis
6. Concluding Remarks
7. Key Conclusions
References
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Abstract
Stomata are epidermal pores used for water and gas exchange between a plant
and the atmosphere. Both the entry of carbon dioxide for photosynthesis and
the evaporation of water that drives transpiration and temperature regulation
are modulated by the activities of stomata. Each stomatal pore is surrounded by
Department of Biology, Stanford University, Stanford, California, USA
Current Topics in Developmental Biology, Volume 91
ISSN 0070-2153, DOI 10.1016/S0070-2153(10)91009-0
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two highly specialized cells called guard cells (GCs), and may also be asso
ciated with neighboring subsidiary cells; this entire unit is referred to as the
stomatal complex. Generation of GCs requires stereotyped asymmetric and
symmetric cell divisions, and the pattern of stomatal complexes in the epider
mis follows a one-cell-spacing rule (one complex almost never touches
another one). Both stomatal formation and patterning are highly regulated by
a number of genetic components identified in the last decade, including, but not
limited to, secreted peptide ligands, plasma membrane receptors and receptorlike kinases, a MAP kinase module, and a series of transcription factors.
This review will elaborate on the current state of knowledge about compo
nents in signaling pathways required for cell fate and pattern, with emphasis on
(1) a family of extracellular peptide ligands and their relationship to the TOO
MANY MOUTHS receptor-like protein and/or members of the ERECTA receptorlike kinase family, (2) three tiers of a MAP kinase module and the kinases that
confer novel regulatory effects in specific stomatal cell types, and (3) transcrip
tion factors that generate specific stomatal cell types and the regulatory
mechanisms for modulating their activities. We will then consider two new
proteins (BASL and PAN1, from Arabidopsis and maize, respectively) that
regulate stomatal asymmetric divisions by establishing cell polarity.
1. Introduction
Stomata (mouths in Greek) are pores used for water and gas
exchange between a plant and the atmosphere. Each stomatal pore is
surrounded by two highly specialized cells called guard cells (GCs), and
may also be associated with neighboring subsidiary cells (SCs); this entire
unit is referred to as the stomatal complex. Stomata are found in different
aerial organs and in species-specific patterns; nonetheless, in nearly all plants
studied, the generation of stomata requires asymmetric and symmetric cell
divisions, and the pattern of stomatal complexes in the epidermis follows a
spacing rule whereby two stomatal complexes are always separated by at
least one intervening epidermal cell.
Stomatal development in Arabidopsis thaliana requires a dedicated series
of asymmetric cell divisions (ACDs) followed by a single symmetric cell
division to form a pair of mature GCs (Fig. 9.1; Geisler et al., 2003; Nadeau
and Sack, 2003). In the developing epidermis of young leaves, the stomatal
lineage is initiated from a subset of committed protodermal (Pr) cells called
meristemoid mother cells (MMCs). ACD of an MMC generates two
daughter cells: a small, triangular cell called a meristemoid and a larger cell
called a stomatal lineage ground cell (SLGC). This type of division is also
referred to as an entry division, because it creates stomatal lineage cells.
Meristemoids may follow either of two paths (Fig. 9.1); they may transition
into a round-shaped guard mother cell (GMC) and divide once to make
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ERL2
TMM
TMM
ER
Amplifying
ERL1
ERL2
MMC
Pr
ER
Entry
GC
Transition GMC
Differentiation
SLGC
ERL1, ERL2
PC
TMM
ER
ERL1
ERL2
Spacing
TMM
GMC
Figure 9.1 Schematic for stomatal development and regulation by TMM and members
of the ERECTA family (ERf) receptors. Stomatal development initiates from
meristemoid mother cells (MMCs), a set of committed protodermal (Pr) cells. In the
stomatal entry division, asymmetric cell division of an MMC generates a small daughter
cell, the meristemoid (M), and a larger daughter cell, the stomatal lineage ground cell
(SLGC). A meristemoid may immediately transition into a guard mother cell (GMC) and
further divide and differentiate into guard cells (GC), or it may divide again
asymmetrically, up to three times, amplifying the number of cells in the stomatal
lineage, before transitioning into a GMC. SLGCs may divide asymmetrically in a
spacing division to generate secondary meristemoids, which are always spaced away
from the existing stomatal precursor cell. Regulation of developmental progression by
TMM ER, ERL1, and ERL2 is marked at each step where they function, with positive
effects labeled with black arrows and negative effects labeled with gray T-bars. Font
size used for TMM and ERf indicates the relative strength of each genes effect, with
larger fonts signifying stronger effects.
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maintaining a constant size to the stem cell pool. Peptide ligands, such as the
ones containing the conserved CLAVATA/ESR (CLE) motif, are secreted
from the meristematic cells and perceived by a set of receptors in the
neighboring cells (Fiers et al., 2007). The receptors are typically Leucine
rich repeat (LRR) receptor-like proteins and/or kinases (LRR-RLPs and/
or LRR-RLKs). Ligand binding is thought to activate the receptors and their
downstream signaling cascade to promote differentiation and thereby prevent
the neighbor cells from adopting stem cell fate and expanding the pool
(chapters 3 and 4; Fletcher et al., 1999; Ito et al., 2006).
Two types of cells in the stomatal lineage population, MMCs and
meristemoids, behave in a stem cell-like manner, such that these cells
produces two daughter cells, one of which can maintain its MMC property
of further division potential and the other which will generally differentiate
into a pavement cell. In contrast to the stem cells in the apical meristems,
however, stomatal MMCs and meristemoids are not in niches. Instead, they
are dispersed on the leaf epidermis and their stem cell activity is transient.
Therefore, it is not surprising that signaling components, including ligands
and receptors, modulate stomatal development and patterning, but the
exact ligands and receptors are distinct from those previously described in
apical meristems. Newly discovered intercellular signals include the small
secreted proteins EPIDERMAL PATTERNING FACTOR 1 (EPF1)
(Hara et al., 2007), EPF2 (Hara et al., 2009; Hunt and Gray, 2009),
CHALLAH (CHAL) (Abrash and Bergmann, 2010), and STOMAGEN
(Kondo et al., 2009; Sugano et al., 2009), all of which belong to a small
subfamily only distantly related to the CLE family.
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ERL1 in a tmm mutant background restores stomata to the tmm stems, but
elimination of ER in tmm siliques nearly eliminates stomatal production,
although each single mutant tends to increase the number of stomata in
this organ (Shpak et al., 2005). A model derived from phenotypic
analysis of various TMM and ERf mutant combinations in various organs
was published by Shpak et al. (2005); we will revisit this model, incor
porating new information from studies of ligands, in a later section of
this review.
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(A)
Stem
Leaf
Leaf
Internal
cell
M
MMC
EPF2
STOMAGEN
(Mesophyll)
EPF1
Epidermal cells
MMC/M
EPF1 EPF2
STOMAGEN
(Mesophyll)
STOMAGEN
Pr
CHAL
(B)
Signal
EPF1/2
SLGC
STOMAGEN
TMM
Signal
Signal
Stomatal
lineage
production
CHAL
Stomatal lineage
Orien
production
tated
division
SLGC
Stomatal lineage
production
ERf
Signal
No signal No signal
Stomata
production
Figure 9.2 Speculative models for interactions among stomatal ligands and receptors.
(A) In leaves and stems, ligands differentially regulate stomatal cell fates. Protodermal
(Pr) cells or the stomatal lineage ground cell (SLGCs) in leaves receive EPF1 and EPF2
signals from the neighboring MMC or meristemoid, inhibiting the acquisition of
stomatal lineage fate. These cells also receive the STOMAGEN signal from the
underlying mesophyll that promotes stomatal lineage cell fate. In stems, SLGCs are
additionally subject to inhibitory CHAL signals coming from internal tissues. (B)
Possible regulatory interactions among ligands and receptors. If the receptors all act as
negative regulators of stomatal development, then EPF1 and EPF2 could activate
homo- or heterodimers of the ERf and TMM. TMM could dampen the CHALERf
inhibition of stomatal production activity in stems by sequestering CHAL in a
nonfunctional complex, or by the CHALTMM complex antagonizing active
CHALERfs. STOMAGEN, as a positive regulator, might compete with negative
regulators, EPF1 and EPF2, to bind receptor complexes. However, if TMMERf
receptors also act as positive regulators, then STOMAGEN could stimulate stomatal
production by associating directly with the TMMERf complexes.
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no, and surprisingly, the ligand responsible is part of the same EPF family.
STOMAGEN/EPFL9 was identified in a co-expression analysis with TMM,
STOMATAL DENSITY AND DISTRIBUTION-1 (SDD1), and EPF1
(Sugano et al., 2009) and by its overexpression phenotypes (Kondo et al.,
2009). When ubiquitously overexpressed with the 35S promoter, STOMA
GEN can generate extra stomata in the epidermis (Kondo et al., 2009; Sugano
et al., 2009) and the loss-of-function phenotype of STOMAGEN obtained by
RNA silencing is greatly reduced stomatal production, both consistent with a
positive role of STOMAGEN in stomata formation (Sugano et al., 2009).
Biochemical analysis and peptide sequencing of the mature form of
STOMAGEN suggest that the protein is secreted and that it acts as a
45-amino-acid peptide. The STOMAGEN cDNA encodes a protein of
120 amino acids (aa) in length, including an N-terminal signal peptide
and a second proteolytic cleavage site indicating the need for multiple
processing events. A chemically synthesized 45-aa STOMAGEN pep
tide is sufficient to induce stomatal production when applied to plants
(Kondo et al., 2009; Sugano et al., 2009), indicating that this ligand
could work without any of the typical post-translational modifications
found in other plant ligands (Kondo et al., 2006). Interestingly, the
sequences around the cleavage sites are highly conserved between
STOMAGEN, EPF1, EPF2, and CHAL, suggesting that all of these
proteins may be processed to yield an active ligand of 4560 aa derived
from the C-terminus.
The phenotypes of STOMAGEN-OXhigher density and clustered
stomataresemble that of tmm (and to a lesser extent er;erl1;erl2 triple
mutants). Increasing and decreasing expression levels of STOMAGEN in
a tmm background no longer changes stomatal densities, indicating that tmm
is epistatic to STOMAGEN and that STOMAGEN is likely to act through
this receptor (Kondo et al., 2009; Sugano et al., 2009). Since the negative
regulators EPF1 and EPF2 also require TMM, the genetic relationships
between STOMAGEN and EPF1/EPF2 were also tested. STOMAGEN
OX in a epf1;epf2 background does not further increase stomatal density
(Kondo et al., 2009), and reduction of STOMAGEN levels can reduce the
number of stomata produced in an epf1;epf2 background, suggesting that
STOMAGEN could compete with EPF1 and EPF2 for signaling through
TMM (Fig. 9.2B, Sugano et al., 2009).
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It is exciting that secreted peptide ligands from the same subfamily are
stomatal regulators with a range of signaling properties. This greatly
improves our understanding of how cellcell communication determines
cell fate. But there are still quite a few pieces missing from the puzzle, for
example, the genetic interaction between STOMAGEN and the ERfs has
not yet been investigated, nor have all combinations of receptors been
tested with EPF1, EPF2, or CHAL. Other questions of future interest are:
Do the characterized ligands indeed physically interact with TMM and/or
ERf, as CLV3 does with CLV1? How many (if any) versions of receptor
complexes are formed among TMM and the ERf? What are the preferred
partners? Biochemical methods, such as in vitro assays for binding of CLV3
to CLV1 (Ogawa et al., 2008), or cell-based assays such as FRET may be
needed to rigorously identify and test the relevant physical associations.
Are all of these peptide ligands post-translationally processed and modified?
If so, how? The functional domains of some CLE proteins can be restricted
to the short conserved CLE motif, itself hydroxylated at two proline residues
(Ito et al., 2006; Kondo et al., 2006). The mature forms of CHAL, EPF1, and
EPF2 have not been elucidated yet, but biochemical methods used on
STOMAGEN would be ideal for characterizing these ligands.
Do other EPFs or other ligand classes participate in stomatal development?
SDD1, a subtilisin-like serine protease, has been known for many years to
regulate stomatal development and pattern (Berger and Altmann, 2000;
Von Groll et al., 2002). This class of subtilases has been shown, in other
cases, to process extracellular ligands. However, based on genetic analysis,
EPF1, EPF2, STOMAGEN, and CHAL act independently of SDD1
(Abrash and Bergmann, 2010; Hara et al., 2007, 2009; Kondo et al.,
2009). It would be intriguing to uncover the substrates of SDD1, some
of which could represent new ligands acting through TMM and ERf, and
may also provide some hints about ligand processing.
Are TMM and EPf receptors sufficient to mediate all stomatal signaling
events? Based on studies of signal transduction in the shoot apical
meristem, another class of receptors, those possessing a kinase domain
but no extracellular domains, and exemplified by CORYNE, form
complexes with the TMM-like RLPs (Mller et al., 2008). The
possibility exists for the CORYNE type (or other unknown receptors)
to also participate in stomatal development signals.
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Lampard et al., 2009), and all these factors function as negative players in
stomatal development. It is interesting to note that only YDA has a notice
able effect on stomatal development as a single mutant. The redundant
activities of MPK3 and MPK6 (as MAPKs) or MKK4 and MKK5 (as
MAPKKs) were first documented in regard to regulation of plant responses
to biotic and abiotic stresses, and it appears that this is also true for regulation
of stomatal development and patterning.
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development at this final stage, but the study revealed that MKK7 and MKK9
do (Lampard et al., 2009). MKK7/9 signaling mirrors YDA at three discrete
steps, negative for the first two transitions and positive at the last stage (Fig. 9.3
and Lampard et al., 2009).
This positive function of YDA and MKK7/9 at the final stage of
stomatal formation was unexpected however; perhaps it is not entirely
surprising. It may reflect that a stomatal lineage cell prefers to form a mature
GC once it has progressed to the GMC stage, rather than being arrested
midway through this process. From observation of mutants, meristemoids
and GMCs appear to have different commitments to becoming stomata.
TMM, ERf
?
MAPKKK
YDA
MKK4/5 MKK7/9
MKK4/5 MKK7/9
MPK3/6
MPK3/6
MKK7/9
MAPKK
MPK ?
MPK3/6
MAPK
SPCH
M
MMC
SPCH
SLGC
?
GC
GMC
MUTE
FAMA
FLP/MYB
SCRM/SCRM2
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Arrested GMCs are rarely seen, but meristemoids do not always complete
the pathway; meristemoids can arrest, as seen in the leaves of the er mutant
(Shpak et al., 2005), or dedifferentiate into a SLGC, as observed on stems of
the tmm mutant (Bhave et al., 2009). Multiple control points during stomatal
development might provide a way to naturally expand the flexibility of a
plant cell confronting environmental challenges. Many environmental stres
ses induce an elevated number of stomata (Baena-Gonzalez et al., 2007;
Baena-Gonzalez and Sheen, 2008), and it has also been known for some
time that many plant species respond to higher levels of CO2 by producing
altered numbers of stomata, suggesting both positive and negative regulators
interpret the CO2 effect for stomatal development (Woodward, 1987). It
would be intriguing to know whether YDA and MKK4/5/7/9 are reg
ulators that integrate CO2 signals with developmental control.
Like with ligandreceptor interactions, new information raises new
questions and both logical and technical challenges. In the next few years,
we imagine several new directions for MAPK signaling. These include
elucidating complete MAPK cascades in relevant cell types and monitoring
their activities in real time. Some questions of particular interest are as
follows:
What is the connection between the highest level kinase (MAPKKK
YDA) and the receptor-like kinases at the membrane? MAPKKKs are
often activated by phosphorylation and require scaffold proteins for
specificity. In the embryo, a cytoplasmic receptor-like kinase, SHORT
SUSPSENSOR (SSP), acts upstream of YDA, but does not require its
kinase activity to function (Bayer et al., 2009). Could SSP or its homologs
be a bridge between YDA and the ER family kinases?
Which of the 20 MAPKs are required downstream of identified MKKs at
the different stages of stomatal development? Are some required
redundantly? In addition, MAPKs are also regulated by phosphatases,
and again, genes encoding these proteins are numerous in plants. Using
the information from many large-scale screens such as protein arrays and
expression profiles may help reduce the candidates to a testable number.
4. Transcription Factors
How could the linear MAP kinase cascade, simply by phosphorylation
relays, oppositely promote or repress stomatal cell fate at different transitions
in the stomatal lineage? We have seen how different ligands can trigger
different responses in different tissues. It is equally plausible that the YDA
MAPK module phosphorylates distinct transcription factors, which are
differentially expressed at specific cell types or stages, thereby switching
on or off key developmental processes.
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ACD
ACD
PAN1 in
maize
SMC
SMC
SMC
SMC
Entry
Amplifying
BASL
BASL
BASL
ACD
Spacing
Meristemoid (M)
(M + SLGC)
PAN1
SMC
ACD
ACD
BASL in
Arabidopsis
GCs
SC
SC
GCs
GMC
GMC
SMC
Differentiation
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Figure 9.4 Polarized proteins PAN1 and BASL in stomatal development. Asymmetric
cell divisions (ACD) are labeled and localization of PAN1 and BASL proteins are
indicated by gray shading. (Top) In maize, the guard mother cell (GMC) is generated
from an ACD in a specific lineage (first panel, dashed line). GMCs provide a positional
cue interpreted by the neighboring subsidiary mother cells (SMCs), inducing their
nuclei to migrate toward the GMC in preparation for a highly asymmetric division.
The smaller daughters of the SMC division become subsidiary cells (SCs) that, together
with the GCs, comprise the stomatal complex. In SMCs, PAN1 appears in patches at the
GMC contact sites. (Bottom) Arabidopsis BASL first appears in the nucleus of the MMC,
and then as a crescent in the cell periphery. After the MMC divides, only the larger
daughter cell inherits the peripheral BASL. The nuclear BASL initially present in both
daughter cells may disappear causing the cell to exit an asymmetric division phase; loss
of nuclear BASL from SLGCs is associated with differentiation into pavement cells. In
spacing divisions, the BASL peripheral crescent relocates to maintain its position distal
to the newly formed meristemoid.
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Cell Division
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(Fig. 9.1), external signals from GCs, GMCs, or meristemoids orient the
direction of the new ACDs, so that the newly formed meristemoid is placed
distal from them (Nadeau and Sack, 2002). In this review, we will point out
where signals and transcription factors regulate stomatal lineage ACDs, but
will consider in more depth two newly identified regulators that appear to
be critical internal polarity factors.
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crescent is always inherited by only the larger daughter cell (the SLGC,
Fig. 9.4). Immediately after division, both daughter cells have
BASLGFP in their nuclei, but nuclear BASL does not always persist.
Disappearance of BASL from the nucleus correlates with cell differentia
tion; if the cell did not inherit peripheral BASL, it will become a GMC
and eventually GCs, but if the cell does possess BASL at the cell periphery,
loss of nuclear BASL correlates with adoption of pavement cell fate
(Fig. 9.4). Interestingly, peripheral BASL is more than a convenient
asymmetrically segregated marker. This region is the site of BASL function
as demonstrated by the expression of an N-terminal-deleted variant of
BASL (BASL-IC) that is localized to a crescent in the cell periphery (but
not the nucleus), yet it fully rescues the basl mutant phenotypes (Dong
et al., 2009).
In contrast to PAN1, BASL seems to be an internal regulator of stomatal
ACDs. The orientation of the BASL crescent does not appear to respond to
external cues such as EPF1 coming from GCs, nor does BASL pattern
change in a tmm mutant. It was hypothesized that BASL may trigger local
cell expansion to induce local physical asymmetries. Indeed, when ectopi
cally expressed in nonstomatal lineage cells of the hypocotyl, the BASL
peripheral crescent overlays areas of abnormal cell outgrowth (Dong et al.,
2009). The BASL crescent, to some extent, also coordinates cell fate
determination; it is invariably in the larger daughter cell resulting from an
asymmetric division and the division and fate of each sister can be predicted
by monitoring BASL in the nucleus and at the periphery (Dong et al.,
2009). Together with evidence that BASL is polarized before any outward
physical asymmetries can be detected in stomatal lineage cells, it appears that
BASL plays a role very similar to that of the PARaPKC complexes in
animal cells.
Discovery of PAN1 and BASL, polarized proteins that regulate
asymmetric division, suggested that the establishment of cell polarity by
accumulation of proteins in distinct subcellular regions is a mechanism
used not only by animals, but by plants, for asymmetric division control.
Still, there are differences between plants and animals; the molecular
identities of BASL and PAN1 as well as the lack of genes encoding
homologs of animal polarity proteins indicate that each group recruited
a different set of proteins.
It seems likely that the way that BASL (and possibly PAN1) promotes
asymmetric division must also be different from what is known from animal
systems. Classical morphology and cell biology already showed that there
are different mechanisms for division plane specification in animals and
plants. In animal cells, the position of the centrosomes and the mitotic
spindle determine the orientation of the division plane (Cowan and
Hyman, 2004). In an animal asymmetric division, polarity proteins (such
as the PAR/aPKC complex), coordinating with microtubules, adjust the
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spindle position and the division plane is set when the membrane pinches
down from the periphery to the midzone of the spindle in a purse-string
closure cytokinesis. By contrast, the division plane of a plant cell is
predicted by a specialized ring of cortical cytoskeleton elements (micro
tubules and F-actin) named the preprophase band (PPB). The PPB appears
during interphase and is transient, being largely disassembled before mitosis;
however, a reminder of its position is maintained and the phragmoplast and
new cell wall dividing the daughter cells will form at this site. What is the
connection between PAN1 and BASL and PPB orientation? Does either
protein orient PPB placement directly, and if so, how? PAN1 appears to
establish cellular asymmetry by recruiting actin, so it is possible that it creates
a platform for orientation of the PPB through this polymer. However, the
placement of the actin patch in SMCs is not where the PPB would
assemble, so it is unlikely that PAN1 is a direct scaffold. Interphase nuclear
position also influences PPB placement (Murata and Wada, 1991), though
the precise mechanism is still unknown. Since BASL is expressed in the
nucleus before PPB formation, might nuclear BASL direct the placement of
the PPB? Alternatively, nuclear BASL might act in coordination with
polarized peripheral BASL to facilitate PPB formation at a specific site.
Polarity generation, though known from decades of morphological
studies to be a critical part of stomatal development and pattern, is just
now beginning to be studied at a molecular level. We anticipate many new
discoveries in the coming decade and that many of these will translate to
polarity issues outside of the stomatal lineage. Some of the outstanding
questions are as follows:
How are the PAN1 and BASL proteins brought to and maintained at
their polarized peripheral locations? Much work on plant cell polarity has
followed the localization of the transmembrane auxin transporters of the
PIN family. Will the trafficking elements required for PIN localization
also be used for PAN1 and BASL, or are the mechanisms different?
Experiments comparing PIN and BASL localization in roots suggest
that they are different (Dong et al., 2009), leaving open the question of
what is required for the dynamic localization of BASL.
What is the link between the presence of polarized proteins and the
generation of cellular asymmetry? Do PAN1 and BASL serve as
scaffolds for other proteins with enzymatic functions to become
localized to one region? Or do these proteins have (as yet unknown)
abilities to directly organize differential growth and division plane
orientation?
What is the functional or regulatory connection between the cell fate
regulators, including the ligands, receptors, MAPK signaling components,
and transcription factors described in previous sections and the
(presumably downstream) polarity proteins PAN1 and BASL?
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6. Concluding Remarks
In the last decade, stomatal development and pattern has emerged
from a phase where most of our information was purely descriptive to
become a maturing field in which we know the molecular identities of
key players and many of the regulatory principles. We have sought in this
review to provide a comprehensive picture of signals, receptors, transcrip
tion factors, and polarity proteins currently known and how they connect
with each other. We summarize these key points below. In describing these
recent advances, we have also tried to highlight areas in which we think
there will be new discoveries in the near future and areas where technical
advances are needed to drive the field forward.
7. Key Conclusions
1. Stomatal development has emerged as an ideal system for study of
intercellular and intracellular signaling and the underlying molecular
mechanisms for cell fate determination and patterning during plant
tissue formation and morphogenesis.
2. The intercellular communication in the stomatal lineage appears to be
mediated by a set of LRR receptor and kinases that must interpret
multiple extracelluar signals. Peptide ligands secreted from neighboring
cells (not necessarily limited to the stomatal lineage) deliver messages to
membrane receptors that can result in either negative or positive
regulation of stomatal fates.
3. Coordinated activity of transcription factors is required to regulate three
sequential cell fate transitions during stomatal development. Promoters
of some of these transcription factors, due to their cell-type specificity,
are proving useful for manipulating gene activity in restricted stomatal
lineage cell types.
4. The YDA MAPK cascade appears to link signaling initiated by
interaction of ligands with the LRR-RLKs at the plasma membrane to
responses in the nucleus by phosphorylation of transcription factors.
5. Polarly localized and segregated proteins regulate ACD in the stomatal
lineage, hinting at conserved mechanisms among plants and animals.
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