specification of stomatal fate in arabidopsis: evidences for cellular interactions
TRANSCRIPT
©
New Phytologist
(2002)
153
: 399–404
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Review
Blackwell Science Ltd
Research review
Research review
Specification of stomatal fate in
Arabidopsis
: evidences for cellular
interactions
Laura Serna, Javier Torres-Contreras and Carmen Fenoll
Facultad de Ciencias del Medio Ambiente, Universidad de Castilla-La Mancha, E-45071 Toledo, Spain
Summary
Stomata are bi-celled epidermal structures distributed in predictable patterns pro-viding plants with pathways for gas exchange with the atmosphere. In
Arabidopsisthaliana
, stomatal formation is emerging as an elegant and powerful model systemto study the genetic and molecular control of cell fate specification and pattern forma-tion in multicellular organisms. In this review, we describe the mechanisms thatregulate stomatal distribution in this model plant. The emerging view indicates thatcellular interactions play a relevant role during stomatal pattern formation. Thesecellular interactions are not restricted to a cell layer and signalling within the epidermis,between the epidermis and the underlying tissues and between organs seem toplay a relevant role during stomatal formation. Whatever the nature of the differentsignals, the stomatal pattern must arise as the result of the integration by the epi-dermal cells of multiple inputs. Uncovering the molecular nature of such signals andunderstanding the specific role during stomatal development provides a formidabletask for the future.
©
New Phytologist
(2002)
153
: 399–404
Author for correspondence:
Carmen Fenoll and Laura Serna Tel: +34 925 265715 Fax: +34 925 268840 Email: [email protected]/[email protected]
Received:
30 July 2001
Accepted:
22 October 2001
Key words:
Arabidopsis
, cellular interactions, lineage, pattern, stoma.
Introduction
The control of spatial pattern formation in multicellularorganisms can be reduced to the question of how cell fate isdetermined. Two mechanisms explain the acquisition of alarge variety of cell fates in all multicellular organisms (see forexample Knoblich, 1997; Jan & Jan, 1998, Fig. 1), and theycan thence be used to explain pattern formation. Unequaldistribution of cell fate determinants during a given cell divi-sion pattern might result in the acquisition of different cellfates (an intrinsic or lineage-based mechanism). Alternatively,cells that arise from a given cell division pattern might beidentical, and they might adopt different fates as the result of
interactions with neighbouring cells (an extrinsic or position-based mechanism). Obviously, intrinsic and extrinsic mechan-isms are not mutually exclusive and, in combination, theymight be used to produce a large number of cell types arrangedin particular patterns.
Stomata are bi-celled epidermal structures providing plantswith pathways for gas exchange with the atmosphere. Theyare arranged in nonrandom and beautiful patterns. How isstomatal fate determined? This article reviews the latestprogress in understanding stomatal pattern formation in
Arabidopsis
by describing observations that indicate that aposition-based mechanism plays a relevant role during cellfate determination.
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Three-dimensional stomatal pattern
In all plant species studied, stomata are surrounded by a fullcomplement of nonstomatal epidermal cells (Larkin
et al.
,1997).
Arabidopsis
is not an exception to this general rule: atleast one nonstomatal cell is interposed between neighbour-ing stomata (Yang & Sack, 1995; Berger & Altmann, 2000;Fig. 2a). This universal principle is disturbed in the mutants
too many mouth
(
tmm
) and
four lips
(
flp
), which exhibit stomatalclusters in several plant organs (Yang & Sack, 1995; Geisler
et al.
, 1998), and in the
stomatal density and distribution1–1
(
sdd1–1
) mutant, which shows stomatal clusters in thecotyledons (Berger & Altmann, 2000). Mutants affected in
other developmental processes, such as
ectopic root hair 3
(
erh3
)(Schneider
et al.
, 1997) and
constitutive photomorphogenic 10–1
(
cop 10–1
) (Wei
et al.
, 1994) also develop adjacent stomata. Inaddition, specific growth conditions induce the formation ofstomatal clusters in
Arabidopsis
leaves (Serna & Fenoll, 1997).A recent study has shown that elevated atmospheric CO
2
levels (720 ppm) and reduced light intensity induce a decreasein the stomatal density and index (Lake
et al.
, 2001). Further-more, the mutant
high carbon dioxide
(
hic
) exhibits a largeincrease in both parameters when grown at high CO
2
levels(Gray
et al.
, 2000). The
sdd1–1
mutant also shows increasesin both stomatal density and index at current CO
2
levels(Berger & Altmann, 2000).
Predictable stomatal patterns are not restricted to theepidermal tissue. In
Arabidopsis
leaves, stomata and theirprecursors (meristemoids, Ms) are located over the junctionsof palisade mesophyll cells and they do not develop above themain vein (Serna & Fenoll, 2000a; Fig. 2b). In the hypocotyl,a strict relationship between the epidermis and the inner celllayer has been described (Berger
et al.
, 1998; Hung
et al.
, 1998;Benfey, 1999): stomatal complexes develop preferentially fromepidermal cells overlying an anticlinal cortical cell wall. Inaddition, the
TRANSPARENT TESTA GLABRA
(
TTG
) and
GLABRA2
(
GL2
) genes are negative regulators of stomataldevelopment in epidermal cells located over a periclinal corticalwall (Berger
et al.
, 1998; Hung
et al.
, 1998; Benfey, 1999).
Cellular interactions in the epidermal tissue
In the Columbia ecotype, Geisler
et al
. (2000) have compileda number of interesting observations, pointing out that extra-cellular spatial cues play an essential role during stomatal fatedetermination. Stomatal lineages start with the acquisition ofmeristemoid mother cell (MMC) identity. This cell identityis forbidden for cells that contact two stomata or precursors(Fig. 3a), but it can be assumed by other epidermal cells,including those making direct contact with one MMC, M,guard mother cell or stoma. This finding provides evidencefor cellular interactions, which are regulated by the
TMM
gene, prohibiting cells making contact with two stomata orprecursors entering the stomatal pathway (Geisler
et al.
, 2000).
Fig. 1 Mechanisms for cell fate specification. (a) Intrinsic or lineage-based mechanism. Unequal distribution of cell fate determinants (black star) between sister cells determines the acquisition of different cell fates. (b) Extrinsic or position-based mechanism. Two identical sister cells adopt different fates as the result of cell interactions with neighbouring cells (bi-directional black arrow). (c) Cell position coupled with autonomously acting factors. Both cellular interactions and unequally distributed cell fate determinants guide a cell fate decision.
Fig. 2 Three-dimensional stomatal pattern. (a) Stomatal patterning in the epidermal tissue. Stomata are surrounded by a stomata-free region. (b) Relationship between epidermal and mesophyll cells. Stomata and meristemoids (upper, epidermal plane in the picture) are placed above the junctions of several mesophyll cells (lower plane in the picture) rather than over their periclinal walls. Micrographs from the adaxial side of first sets of Landsberg erecta leaves. Bars, 20 µm.
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MMCs divide unequally, producing a smaller and usuallytriangular M, and a larger sister cell (subsidiary cell, SC). Doesthe placement of this first cell division plane follow any gen-eral rule? Geisler
et al
. (2000) have shown that this dependson the MMC position relative to neighbouring epidermalcells. MMCs making contact with a M, guard mother cell orstoma divide so that the new M is placed away from them(Fig. 3b). This is the main spacing mechanism, ensuring aminimal distance – one cell – between nearby stomata and itis regulated by the
TMM
gene (Geisler
et al.
, 2000). By con-trast, cell division planes of MMCs located in other positions,such as next to other MMCs, are randomly oriented. Thissuggests that stomata or their precursors (Ms or guard mothercells) might produce a signal that regulates the orientation ofthe MMC division plane. If the signal is absent, the cell divisionplane will be randomly oriented. Specific cell–cell contacts haveproved important during the orientation of some cell divisionaxes in
Caenorhabditis elegans
embryo (Goldstein, 1995).As a consequence of the random positioning of the cell
division plane in MMCs placed next to other MMCs, twoMs occasionally arise in direct contact (Geisler
et al.
, 2000;Fig. 3(c)). Cell divisions occurring later during stomataldevelopment can also produce clustered M (Geisler
et al.
,2000). Two main mechanisms prevent the formation of
stomatal clusters in these cases (Geisler
et al.
, 2000): cell divi-sions of one or both Ms are oriented so that at least one SCis produced between the adjacent Ms; and one of the Msapparently experiences a change in its fate and differentiates asa pavement cell. These interesting observations indicate that
Arabidopsis
is equipped with a mechanism that supervises everyepidermal cell division, identifying and correcting potentialmistakes during development. This ability to amend develop-mental faults has been previously detected during stomataldevelopment in other plant species, and it provides clear evid-ence for cellular interactions (Sachs, 1978; Kagan
et al.
, 1992).Correct stomatal movements are crucial for plant survival
in a terrestrial environment and they depend on the presenceof a region free of stomata. As described above, it is likelythat at least two mechanisms ensure the absence of adjacentstomata: distribution of Ms away from stomata (or theirprecursors); and correction of pattern mistakes (Ms in directcontact). It seems logical that the two mechanism should beindependently regulated, so that a failure in the first mechan-ism could be corrected by the second one. If this is true,mutants displaying adjacent Ms must be able to form stomatasurrounded by a stomata-free region. But ‘logic’ is not alwaysfollowed during stomatal development: the adjacent Ms in the
tmm
mutant are not corrected during development, resultingin the formation of stomatal clusters (Geisler
et al.
, 2000).Although MMCs in the C24 ecotype undergo a stereo-
typed pattern of three unequal divisions followed by a finalequal one that produces a stoma surrounded by a full com-plement of SCs (Berger & Altmann, 2000; Brownlee, 2000;Serna & Fenoll, 2000b; Fig. 4), MMCs in the Columbia
Fig. 3 Evidence for cell interactions in the epidermal tissue. (a) Epidermal cells in contact with two stomata (or meristemoids) cannot assume meristemoid mother cell identity. (b) Meristemoid mother cells adjacent to stomata (or to meristemoids) divide so that the new meristemoid is placed away from the pre-existing stomata (or meristemoids). (c) Stomatal lineages can produce potential mistakes, such as adjacent meristemoids. Oriented cell divisions (upper part) or change in the cell fate -from meristemoid to pavement cell- (lower part) correct these mistakes.
Fig. 4 Stomatal development in C24 ecotype. (a) The first step towards the generation of a stomatal complex is the acquisition of meristemoid mother cell (MMC) identity from a protodermal cell. The MMC divides unequally, producing the first subsidiary cell (SC1) and the first meristemoid (M1). An unequal cell division from the M1 gives rise to the second SC and to the M2. The M2 undergoes the last unequal division producing the third SC and the M3. A change in the M3 fate yields a guard mother cell that divides equally producing the stoma surrounded by three closely clonally related SCs. (b) A SC of the primary complex undergoes the developmental program of the MMC producing a secondary complex. Note that this SC divides in such a way that the new M is placed away from the pre-existing stoma, which is evidence for cellular interactions.
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ecotype do not (Geisler
et al.
, 2000; Fig. 5). All MMCs inColumbia undergo a first unequal division, but the number ofsubsequent cell divisions that precede stomatal formation isnot fixed, and it varies from zero to three (Geisler
et al.
, 2000).As a direct consequence, Geisler
et al
. (2000) have shown thatin two-thirds of the stomata at least two lineages contribute tothe formation of the full complement of SCs. Since stomataare not in direct contact, this variability in the stomatal line-ages is indirect evidence for the existence of spatial cuesregulating stomatal pattern.
The stereotyped stomatal lineages in C24 suggest thatintracellular events guide stomatal fate in this ecotype. How-ever, the observation that MMCs in contact with stomatadivide so that the new M does not make contact with thepre-existing stoma (Berger & Altmann, 2000; Fig. 4b) indic-ates that intracellular events are not the entire story, and thatcellular interactions must also be considered in this ecotype.These cellular interactions are, in part, regulated by
SDD1
, agene that potentially codes for a subtilisin-like serine protease(Berger & Altmann, 2000).
In addition, a suggestion for cellular interactions comesfrom the study of stomatal pattern establishment in responseto atmospheric CO
2
levels. Gray
et al
. (2000) have cloned agene,
HIC
, required for preventing an increase in the stomatalindex and density in response to doubled CO
2
levels. Thegene shares a very high homology with the
Arabidopsis KSC1
gene. The
KSC1
gene codes for a 3-ketoacyl-CoA synthase(KSC; Todd
et al.
, 1999); these enzymes are involved in verylong chain fatty acid synthesis during the formation of cutic-ular waxes (Post-Beittenmiller, 1996). The molecular natureof the
HIC
gene suggests that cuticular waxes compositionmight play a relevant role during stomatal pattern establish-ment in response to CO
2
. Gray
et al
. (2000) proposed that amechanism based on the classical lateral inhibition may explainthe increase of stomatal index (and density) in response toCO
2
levels observed in the
hic
mutant: the alterations in thecuticle composition of the mutant may interfere with itspermeability to a inhibitory factor that is stimulated bydoubled CO
2
levels, thus blocking its inhibitory effect onstomatal fate.
Other mutants that show alterations in wax composition
-eceriferum-1
and
eceriferum-6
- ( Jenks
et al.
, 1995) exhibit higherstomatal index than the wild-type when grown at currentCO
2
levels (Gray
et al.
, 2000). Alterations in the diffusion ofan inhibitory factor might induce the stomatal phenotype of
eceriferum
mutants. If this is true, and considering that the
hic
mutant exhibits a wild-type stomatal pattern at current CO
2
levels, this inhibitory factor should show a normal diffusion inthe
hic
cuticle.
Signalling between cell layers
Stomatal position with respect to mesophyll cells also followpatterns that cannot be explained by random placementmechanisms (Serna & Fenoll, 2000a). Since epidermis andmesophyll tissues derive from two different cell layers (L1 andL2, respectively) that become determined at a very early stageof embryo development (Poethig, 1989), cell lineage cannotexplain the observed relationship between epidermis-mesophyllpatterns. Therefore, cellular interactions are necessary to estab-lish specific cell patterns between these two layers.
On the adaxial side of the leaf, cellular interactions maytake place between epidermal and mesophyll cells, and theymay ensure that Ms be placed over junctions of mesophyllcells rather than over their periclinal walls (Serna & Fenoll,2000a). Once the meristemoid-mesophyll pattern has beenestablished, the precise orientation of subsequent cell divisionsduring stomatal development ensures that the stoma remainsin the same relative position with respect to mesophyll cells(Serna & Fenoll, 2000a). The direction of the signal(s) con-necting the two tissues can only be a matter of speculation(Serna & Fenoll, 2000a): either the M might signal the innercells immediately below to divide and grow in such a way thatan air space is produced; or the junction with mesophyll cellsmight dictate the position of the M by determining the MMCcell division plane. In the hypocotyl, the ordered arrangementof cortical cell files before stomatal formation indicates thatthe signal is transmitted from the internal tissues to the epi-dermis, prohibiting stomatal pathway entry in those epidermalcells that do not overly an anticlinal cortical cell wall.
Fig. 5 Stomatal development in the Columbia ecotype. (a) All stomatal lineages start with a unequal cell division, producing a subsidiary cell and a meristemoid. However, no stereotyped cell division pattern follows this first division. Stoma formation can take place after the first, second, or third unequal division. As a direct consequence, many stomata are surrounded by cells that arise from at least two different lineages. (b) A subsidiary cell of the primary complex, not necessarily clonally related with the adjacent stoma, assumes meristemoid mother cell identity and produces a new stomatal complex. Note that formation of stomata can take place after the first, second, or third unequal division.
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A relationship between epidermis and inner tissues is alsorevealed by the lack of stomata over the main veins (Larkin
et al.
, 1997; Serna & Fenoll, 2000a). Epidermal cells in thisarea remain rectangular in shape, they do not produce sto-mata, and they do not differentiate the lobate contour thatSCs show in the mature leaf blade. These cells therefore maybe signalled by the underlying vascular tissue to prevent theirentry in the stomatal pathway.
Signalling between organs
As described above, cellular interactions during stomataldevelopment are not restricted to a cell layer, since bothepidermal and mesophyll layers seem to interact to place Ms– and therefore stomata – in right positions. Are cellularinteractions guiding stomatal patterns restricted to a givenorgan? Or, on the contrary, does long-distance signalling playany role during stomatal pattern formation? Lake
et al
. (2001)have recently answered this question: they have elegantlydemonstrated long-distance signalling that regulates stomatalpattern in response to CO
2
and light levels. Expanding andmature leaves of the same plant were exposed to differentCO
2
concentrations. Expanding leaves exposed to 360 ppmexhibited reduced stomatal index and density when matureleaves were exposed to higher CO
2
concentration (720 ppm).When mature leaves were exposed to 360 ppm and expand-ing leaves to 720 ppm, the stomatal index and density ofleaves grown at 720 were increased. This experiment indic-ates that mature leaves perceive CO
2
levels and transmit along-distance signal which regulates stomatal developmentin developing leaves (Lake
et al.
, 2001). Either this signaloverrules any other signal produced within the developingleaves, or leaves cannot perceive/respond to this environmentalcue until they reach maturity.
Long-distance signalling in response to light was alsodemonstrated by placing developing and mature leaves underdifferent irradiances (Lake
et al.
, 2001): the stomatal indexand density of new leaves were reduced when mature leaveswere exposed to shade light conditions and developing leavesto full light ones.
These unexpected findings open many questions: how domature leaves perceive CO
2
and light levels? what types ofsystemic signals are elicited by these factors, and how arethey transmitted to developing leaves? how do younger leavesrespond to the signals induced by these environmental factorsand translate them into stomatal pattern alterations? and howcan we link the proposed short-distance signal identified byGray
et al
. (2000) with this long-range signal?
Concluding remarks
Our understanding of stomatal fate determination has pro-gressed rapidly over the last year. The main message comingfrom the different observations is that the determination of
stomatal fate depends on positional information. There isnow solid evidence that epidermal cells monitor, at least cell-autonomous checkpoints: where they come from, that is,their lineage; who their neighbours are, both in the epidermisplane and in the adjacent tissues; and long distance or holisticcheckpoints: what are the values of different environmentalfactors sensed by the plant?
As Croxdale (2000) put forward, knowing the travel routesof stomatal fate regulators would provide essential informa-tion regarding stomata pattern formation. However, at themoment, these are only a matter of speculation. Chemicalsignals would include either molecules moving through theapoplast, such as the putative inhibitory factor whose move-ment depends on HIC activity (Gray
et al.
, 2000), as well asimmobilised cell wall determinants, such as those proposedfor the control of cell division planes in
Fucus
embryos (Fowler& Quatrano, 1997). As for symplastic signals, if Ms and/orMMCs establish secondary plasmodesmata with mesophyllcells, this could be an additional pathway for (macro)molecularexchange between the two layers. Long-distance signals frommature to developing leaves might also exploit symplasticpathways: in developing leaves of tobacco, GFP producedin phloem companion cells spreads symplastically throughmesophyll and epidermal layers, including immature guardcells complexes (Oparka
et al.
, 1999). In maize, the homeoticKNOTTED protein and its mRNA passes through plas-modesmata from vascular tissue through the mesophyll to theepidermis (Lucas
et al.
, 1995).Whatever the nature of the different signals is, stomatal
pattern establishment must arise as the result of the integra-tion by the epidermal cells of multiple inputs. Understandingthe precise operation of all these signals is a formidable task forthe future.
Acknowledgements
This work was supported by a grant from the Spanish NationalFunding Agency (DGESIC, project PB97-0024) to CF andby a research aid from UCLM to LS and CF. JT is the recipientof a fellowship from the Ministry of Education.
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