Download Functional aspects of cell patterning in aerial epidermis

Functional aspects of cell patterning in aerial epidermis
Cathie Martin1 and Beverley J Glover2
Plants have evolved epidermal cells that have specialized
functions as adaptations to life on land. Many of the functions of
these specialized cells are dependent, to a significant extent,
on their arrangement within the aerial epidermis. Considerable
progress has been made over the past two years in
understanding the patterning mechanisms of trichomes and
stomata in Arabidopsis leaves at the molecular level. How
universal are these patterning programmes, and how are they
adjusted to meet the changing functions of specialized
epidermal cells in different plant organs? In this review, we
compare the patterning of stomata and trichomes in different
plant species, describe environmental and developmental
factors that alter cell patterning, and discuss how changes in
patterning might relate to cell function. Patterning is an
important aspect to the functioning of aerial epidermal cells,
and a greater understanding of the processes that are involved
will significantly enhance our understanding of how cellular
activities are integrated in multicellular plants.
Addresses
1
Department of Cell and Developmental Biology, John Innes Centre,
Norwich Research Park, Colney NR4 7UH, UK
2
Department of Plant Sciences, University of Cambridge, Downing St,
Cambridge CB2 3EA, UK
Corresponding author: Martin, Cathie ([email protected])
Current Opinion in Plant Biology 2007, 10:70–82
This review comes from a themed issue on
Growth and development
Edited by Cris Kuhlemeier and Neelima Sinha
Available online 30th November 2006
1369-5266/$ – see front matter
# 2006 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2006.11.004
Introduction
The epidermis is common to almost all multicellular land
plants. Many typical epidermal features evolved during
the colonisation of land, when the acquisition of water and
the restriction of water loss from aerial tissues became
priorities. These requirements led to the development of
specialized cell types within the epidermis; rhizoids and
later root hairs for the acquisition of water, and stomata
within a cuticularised aerial epidermis for the control of
water loss.
Another specialized cell type of the aerial epidermis is the
trichome or hair, found in ferns and higher plants. The
functions of trichomes are usually less obvious than those
Current Opinion in Plant Biology 2007, 10:70–82
of stomata and might be very diverged, depending on the
plant species and the organ on which the trichome develops. Ontologically, the relationship between aerial trichomes and root hairs is not entirely clear. Although
trichomes and root hairs share components of a common
regulatory mechanism that governs their patterning and
initiation in Arabidopsis, it is unlikely that these structures
are homologous over the entire plant kingdom. The very
earliest land plants had rhizoids [1] whereas aerial trichomes evolved after the divergence of bryophytes.
Trichomes have probably evolved independently on
multiple occasions [2]. Consequently, the patterning
mechanisms for trichomes across the plant kingdom are
likely to be multi-fold as might be the molecular-genetic
mechanisms of their initiation and determination [3].
Other types of specialized epidermal cell are gland cells,
which are often considered to be a type of trichome [4],
and papillate cells, which have outgrowths from their
surfaces.
Stomata serve essential functions in land plants, including
the control of water loss, the acquisition of CO2, cooling
and nutrient accumulation [5]. The relative importance of
these functions might vary between stomata in different
organs and different plant species, but the functions
themselves are invariant. The only extant examples of
astomatous plants are parasites, which do not fix their
own carbon from CO2, or submerged aquatics, which
have lost their requirements for homoiohydry (i.e. the
capacity to maintain an equitable water balance under
changing environmental conditions) and obtain their
CO2 through root systems. Trichomes, on the other hand,
are largely dispensable for life and their functions and
patterning might be much more diverged than those of
stomata.
Functional aspects of epidermal cell
patterning in leaves
Stomata
The original function of stomata was the limitation of
water loss in land plants and the maintenance of homoiohydry, while allowing gas exchange. Their other roles
(cooling, xylem integrity and nutrient accumulation)
probably evolved later [5]. All of these roles place constraints on stomatal patterning within epidermal sheets;
most notably the requirement that they should be relatively evenly distributed. There are a limited number of
species that have clustered stomata, but the functional
significance of this is not obvious. Often, stomatal density
is far greater on abaxial leaf surfaces than on adaxial ones.
This is believed to relate to the role of stomata in
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Cell patterning in aerial epidermis Martin and Glover 71
controlling water loss. The heating of leaves is less on the
abaxial surface, so the loss of water through transpiration
can be reduced by placing the stomata on the lower side
of the leaf. In plants such as Eucalyptus that have
isobilateral leaf anatomy in their adult leaves (i.e. palisade mesophyll on both adaxial and abaxial sides of the
leaf), the stomatal densities of adult leaves resemble
those on the adaxial surfaces of the bilateral juvenile
leaves. Isobilateral leaf anatomy is an adaptation to hot
dry conditions. Differences in stomatal density between
abaxial and adaxial surfaces are likely to be under the
control of polarity-determining genes, such as those
encoding the homeodomain zipper (HD-ZIP) proteins
PHABULOSA, PHAVOLUTA and REVOLUTA and
the YABBY proteins YABBY3 and FILAMENTOUS
FLOWER [6,7].
Although even distribution of stomata over planar surfaces assists in water conservation and CO2 assimilation,
stomata tend to be absent from epidermal tissues that
overlie leaf veins (Figure 1). Any proximity of stomata to
vascular tissue is likely to short-circuit internal water
distribution, and to be ineffectual in CO2 distribution
because palisade mesophyll cells are generally less frequent close to veins. The exclusion of stomata from
epidermal tissues that overlie vascular strands might be
strong enough to constitute a pre-pattern in monocot
leaves and conifer needles (Figure 1a,b). From a functional perspective, it is also significant that stomatal
density is sensitive to environmental conditions. The
sensitivity of stomatal numbers to atmospheric CO2 concentrations is widespread. Most plants show reduced
numbers of stomata at elevated CO2 levels and stomatal
density has been used as a means of estimating past
atmospheric CO2 concentrations [8].
Pre-patterning of stomata in leaves
In many species, stomata are organized in regular arrangements, particularly as files of alternating guard cells and
pavement epidermal cells. This restricted arrangement of
stomata has been referred to as pre-patterning and is
common in monocotyledonous plants and conifer needles
[9]. Epidermal cells mature first at the tip of the monocot
leaf. In those files of cells determined to form stomata,
asymmetric divisions occur to produce a single stomatal
initial positioned towards the leaf tip and a larger epidermal cell positioned towards the leaf base. The stomatal initial then divides asymmetrically to form two
subsidiary cells and then symmetrically to form the two
central guard cells. The divisions of the stomatal initial in
monocot leaves resemble the orientated divisions that
define the patterning of guard cells in dicot leaves, but the
initial organization of cells in rows that develop the
competence to form stomata represents a pre-pattern that
constrains the lineage-based patterning process. In maize,
clonal analysis has shown that this pre-pattern is nonclonal, and defined by positional information. An inhibiwww.sciencedirect.com
tory signal that emanates from the veins of the leaf would
be adequate to explain the ordered patterning of stomata
in rows in maize leaves [10]. In other monocots such as
Tradescantia, however, additional positional cues must be
used to establish the pre-pattern [11].
The functional significance of the pre-patterning of stomata away from the veins is particularly obvious in maize.
Maize is a C4 plant in which the fixation of CO2 by
Rubisco is separated physically by Kranz anatomy from
the light reactions of photosynthesis. CO2 enters through
stomata overlying the mesophyll cells and is incorporated
into phosphoenol pyruvate (PEP) to form malate. Malate
is shuttled from the mesophyll to the bundle sheath cells
that surround the veins where it is converted back to PEP,
releasing the CO2, which is then fixed by Rubisco. This
mechanism increases the CO2 concentration in the bundle sheath cells, which remain free from the O2 present in
the atmosphere. This frees the carboxylase activity of
Rubisco from its normal accompanying oxygenase activity, making the carbon fixation of C4 plants more efficient
than that of C3 plants. Central to the effective operation
of C4 metabolism is the insulation of the bundle sheath
chloroplasts from the normal atmospheric levels of O2.
Consequently, the exclusion of stomata from the regions
around the veins is of considerable functional significance
in maize (Figure 1c).
In Arabidopsis, no obvious pre-pattern determines stomatal distribution in leaves, but there is a pre-pattern in
hypocotyls. There, files of cells that overlie the junctions
between the mesophyll cells are competent to form
stomata [12]. In the roots of Arabidopsis, these same cell
files form root hairs. Although the pre-pattern imposes
constraints on the cell files that can form stomata, the
same orientated divisions that position the guard cells
surrounded by subsidiary cells in leaves also occur within
the determined cell files of the hypocotyls. The prepattern constraining stomatal development in the hypocotyl is determined by at least some of the genes that also
define root hair patterning in Arabidopsis (WEREWOLF
[WER], TRANSPARENT TESTA GLABRA 1 [TTG1] and
GLABRA2 [GL2]). Furthermore, it is thought that the
same transcriptional complex controls the expression of
GL2 in non-stomatal files to inhibit the formation of
meristemoids [12]. If this is indeed the case, then it is
likely that the small one-repeat MYB inhibitors TRIPTYCHON (TRY) and CAPRICE (CPC), which effect
lateral inhibition in root hair development, also function
in lateral inhibition of the non-stomatal fate [13–15]. It is
possible that it is the position of the mesophyll cell
junctions that provides the initial signal defining the
pre-patterning of the hypocotyls as it might also do in
roots [16]. Signals emanating from mesophyll cells are also
likely to be important in determining the patterning of
stomata in leaves. In Arabidopsis, 93% of leaf stomata
overlie junctions between mesophyll cells [17].
Current Opinion in Plant Biology 2007, 10:70–82
72 Growth and development
Figure 1
Patterning within the epidermis of leaves. (a) Scanning electron micrograph (SEM) of the abaxial surface of an adult maize leaf. The stomata (S)
are produced in rows of alternating guard cells (arrowed) and epidermal cells. They are excluded from the epidermal region overlying the veins
(MV, major vein). Scale bar indicates 200 mm. (b) SEM of the adaxial surface of an adult maize leaf. The visible trichomes are of two types: prickle
hairs (PH) and macrohairs (MH). These are arranged in rows of bulliform cells (BC) that are sited mid-way between the veins (V) and are separate
from the rows of stomata. Scale bar indicates 200 mm. (c) Diagram of the arrangement of the epidermal cells in a maize leaf in relation to the
underlying photosynthetic cells. The stomata are positioned over spaces between the mesophyll cells (M), which fix CO2 into malate in C4
Current Opinion in Plant Biology 2007, 10:70–82
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Cell patterning in aerial epidermis Martin and Glover 73
Patterning of stomata following the determination of
stomatal initials
Tremendous progress has been made over the past two
years in understanding the signalling pathway that
defines the pattern of cell divisions and the satellite
stomata once the initial meristemoid mother cells
(MMCs) have been determined. Most of the mutations
that affect stomatal patterning in Arabidopsis affect these
orientated asymmetric divisions. The phenotypes of most
of the mutants involve the proliferation and clustering of
stomata, indicating that the wildtype signalling pathway
negatively regulates the development of guard cells and
orientates the divisions that create guard mother cells
(GMCs) and subsidiary cells.
MMCs arise relatively late in leaf development through
an initial asymmetric cell division (Figure 2). MMCs
might initiate adjacent to each other, so there is no strong
patterning of these cell types. Nevertheless, recent examination of the mutant phenotypes of three receptor-like
kinase (RLK) genes, ERECTA (ER), ERECTA-LIKE1
(ERL1) and ERL2, showed that collectively these genes
act as negative regulators of stomatal development [18].
The mutant phenotypes have been interpreted to show
two levels of patterning activity by the products of these
genes. The first is negative regulation of the initiation of
stomatal meristemoids, which is conferred by all three
receptors. The second is conferred by ERL1 and ERL2
and involves the negative regulation of the transition of
meristemoids to GMCs.
The smaller cell produced by the asymmetric division of
the MMC is termed the meristemoid. This cell might
differentiate directly into a GMC and thence form a pair
of guard cells by a symmetric division (Figure 2). Alternatively, the meristemoid might divide again asymmetrically to form satellite meristemoids. The larger cell
produced by the asymmetric division of the MMC might
also undergo further asymmetric divisions to form satellite meristemoids. It is the orientation of these subsequent divisions that ensures that all guard cell pairs are
separated by at least one epidermal cell (Figure 2). As
guard cell activity is dependent on the exchange of ions
and the bulk flow of water with subsidiary cells to allow
changes in turgor, this patterning is absolutely essential to
effective stomatal functioning.
The first gene in the signalling pathway that patterns the
distribution of stomata is STOMATAL DENSITY AND
DISTRIBUTION 1 (SDD1), which orients the asymmetric
divisions of the satellite meristemoids ([19,20]; Figure 2).
SDD1 is highly expressed in meristemoids. It encodes
a subtilisin-like protease and it has been suggested
that this protein might operate extracellularly to cleave
an inactive precursor peptide, producing an active form
that serves as the ligand for the receptors that signal
the oriented cell divisions. The second identified component of the signalling pathway is the TOO MANY
MOUTHS (TMM) gene [21]. TMM encodes a receptorlike protein (RLP) in the plasma membrane of meristemoids and neighbouring cells. Its leucine-rich repeats
(LRR) are positioned extracellularly. Genetic analysis
suggests that TMM detects the signal generated by
SDD1. TMM has a role in suppressing satellite meristemoid identity and a second role in the orientation of the
asymmetric divisions that produce satellite meristemoids
[22]. The LRR–RLP encoded by TMM lacks a kinase
domain. In other examples of LRR receptors that regulate stem cell identity in plants, RLPs interact with
RLKs to modulate signalling through phosphorylation
cascades. ER, ERL1 and ERL2 encode RLKs that modulate stomatal development [18] suggesting that these
might be the RLKs that partner TMM in stomatal
patterning (Figure 2).
A potential target for the information produced from the
TMM–RLK interactions is YODA (YDA). This protein is
a mitogen-activated protein (MAP) kinase kinase kinase
(MAPKKK) that negatively regulates guard cell fate [23].
Constitutively active YDA causes the complete inhibition
of stomatal development, and yda mutants have elevated
numbers of stomata. YDA has other functions in regulating cell fate decisions, for example in the zygote [24], but
signalling in multiple pathways is a common feature of
MAPKKKs. The interaction of TMM with its RLK
partner(s) might activate YDA by phosphorylation. Activated YDA then negatively regulates the adoption of
guard cell fate or guard cell differentiation, presumably
through a MAP kinase phosphorylation cascade. One of
the genes that are upregulated in yda mutants is FAMA,
which encodes a basic helix–loop–helix (bHLH) transcription factor. fama mutants produce no mature guard
cells, so FAMA positively controls the competence of
(Figure Legend 1 continued) photosynthesis. The malate is transported to the bundle sheath cells (BS), which surround the veins. In the
bundle sheath cells, the CO2 is released and re-fixed by Rubisco. The fixed carbon is then exported from the veins in the form of sugars. This
arrangement of cells means that the concentration of O2 is kept low in the vicinity of the bundle sheath cells so that photorespiration is limited.
(d) SEM of the abaxial surface of tobacco leaf. Tobacco produces glandular trichomes (GT) and exuding trichomes (ET) that are dispersed
relatively evenly over the blade but are concentrated in the epidermis over the veins (especially the mid vein as shown). Stomata are distributed
over the blade but are excluded from the epidermal tissue over the veins. Scale bar indicates 500 mm. (e) SEM of the adaxial epidermis of a
leaf of Solanum dulcamara (woody nightshade). Trichomes of two types are produced: non-glandular trichomes (NGT) and glandular trichomes.
The glandular trichomes are produced mostly in the tissue that overlies the veins. Stomata are distributed over the leaf except in the tissue
overlying the veins. Scale bar indicates 500 mm. (f) SEM of the adaxial epidermis of an Arabidopsis leaf (Colombia), showing trichomes (T) with
supporting socket cells. Stomatal complexes (SC) are distributed within the epidermis but the guard cells are kept separate by the asymmetric
divisions that determine the position of the satellite meristemoids. Stomata are not formed in the trichome socket cells. Scale bar indicates 500 mm.
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Current Opinion in Plant Biology 2007, 10:70–82
74 Growth and development
Figure 2
GMCs to divide and form guard cells [23]. This phenotype has been suggested to be analogous to that resulting
from mutation of the FOURLIPS (FLP) gene, which
encodes a MYB-related transcription factor [25]. FLP,
in combination with a very closely related MYB protein,
AtMYB88, regulates the transition between GMCs and
differentiated guard cells. Because FAMA encodes a
bHLH protein and FLP/AtMYB88 encode R2R3MYB
proteins, it has been suggested that these proteins might
form a transcriptional complex that positively regulates
the differentiation of GMCs [23,25]. However, neither
FAMA nor FLP/AtMYB88 have any of the signature
motifs that are essential for MYB–bHLH interactions
in other well-established transcriptional complexes in
plants [26]. Indeed, the parallels between the phenotype
of the fama mutant (no stomata) and the flp mutant
(clustered stomatal pairs) are difficult to appreciate,
and proof of the interaction between these proteins
and establishment of its significance to patterning will
require considerable further experimentation.
Environmental influences on stomatal patterning
Stomatal density and function are very sensitive to environmental conditions. Land plants evolved in atmospheres
that had considerably higher CO2 levels than currently
prevail, and the role of stomata in providing leaf mesophyll cells with access to CO2 might have become more
important as atmospheric levels dropped. Stomatal density in megaphylls is significantly higher than that in
microphylls [27]. Increased stomatal densities might also
have contributed to the evolution of additional roles for
stomata in nutrient accumulation, transpirational cooling
and the prevention of xylem embolism [5].
Diagram of the lineage-based mechanism for the patterning and
determination of stomata in Arabidopsis. The positions of the activities of
known players in the patterning mechanism are shown. Stomatal
development begins with an unequal cell division of a protodermal cell.
The fate of this cell could be determined by RLK activity and by
positional signals from the underlying mesophyll. In some tissues (e.g.
hypocotyls), TMM also regulates this step. The products of this division
are a subsidiary cell (green) and a meristemoid (red). The meristemoid
divides to give a new subsidiary cell and a new meristemoid; then the
meristemoid divides again to give a further subsidiary cell and another
meristemoid. The meristemoid rounds and becomes a GMC. The GMC
divides equally to form two guard cells. This step is positively regulated
by the transcription factors encoded by FAMA, FLP and AtMYB88. The
stomatal complex enters the stomatal pathway, producing a secondary
complex. The orientation of the divisions at this stage are controlled by
the SDD1–TMM–YDA signalling pathway, which involves a MAP kinase
cascade. This pathway also negatively regulates the expression of
FAMA, FLP and AtMYB88 to control the transition to guard cell fate.
Current Opinion in Plant Biology 2007, 10:70–82
Stomatal densities are sensitive to atmospheric CO2 concentrations: as the concentration of CO2 increases, stomatal density decreases. This is a universal response of
plants, although it might not always occur through the
same developmental mechanisms. In dicot leaves, stomatal density decreases as atmospheric CO2 levels
increase, but in conifers, the number of rows of cells that
are determined to form stomata is decreased rather than
the microscale stomatal density [28]. The response of
conifers suggests that it is the degree of reiteration of the
pre-pattern rather than the patterning mechanism itself
that is adjusted in response to changes in atmospheric
CO2. By contrast, Serna and Fenoll [29] showed that
growing Arabidopsis plants in enclosed environments
(i.e. at high humidity) could significantly affect the lineage-based patterning mechanism and give rise to clustered stomata that phenocopied the tmm and flp mutant
phenotypes. Perhaps environmental conditions influence
both the pre-patterning mechanisms and the lineagebased patterning mechanisms once the MMCs have been
determined. Stomatal densities are influenced by several
other environmental conditions, including light quality,
UV-B, drought, ozone and shade [30].
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Cell patterning in aerial epidermis Martin and Glover 75
Both elevated CO2 levels and shading can generate longdistance signals to decrease stomatal densities [31]. Thus,
if mature leaves are shaded or exposed to elevated CO2,
the developing leaves on the same plant show reductions
in stomatal density. Because both atmospheric CO2 and
shading influence the rates of photosynthetic carbon
fixation, it has been thought that these long-distance
signals might involve sugars. However, empirical data
suggest that sugars are unlikely signals [32,33].
Mutants have also been identified in which the stomatal
density responses to environmental conditions are
affected. The high in carbon dioxide (hic) mutant of Arabidopsis increases stomatal density in response to elevated
CO2 [34]. HIC encodes a 3-keto acyl CoA synthetase that
is involved in synthesizing the long chain fatty acids of
epicuticular waxes. HIC is expressed only in guard cells,
implying that its effects on CO2 signalling are through the
transmission of a signal that affects the differentiation of
satellite meristemoids. It has been suggested that HIC
affects the permeability of the guard cell walls to a mobile
signal, influencing stomatal density, or that the signal
itself might be a product or by-product of wax biosynthesis [30]. The influence of epicuticular waxes on signal
transmission and stomatal patterning must be qualitative
rather than quantitative because although some other wax
mutants affect stomatal density, they do not affect the
responses to elevated CO2 concentrations or to decreased
light. Another possibility is that the mobile signal that
affects stomatal density is a plant hormone. Decreased
stomatal conductance, which is probably the primary
response to increases in atmospheric CO2 levels or to
decreased light, might affect transpirational water flow
significantly. Changes in the rate of transpiration might in
turn affect the flux of hormones (abscisic acid [ABA] and
cytokinins [CK]) to the leaves from the roots. Application
of either ABA or CK can increase stomatal densities in a
variety of plant species [33,35–37].
Trichomes
The functions of trichomes in plants are very diverse.
Trichomes can be glandular or non-glandular. The nature
of the products that glandular trichomes exude or secrete
affects their functions and consequently their distribution
and patterning. For example, some glandular trichomes
produce volatiles that are attractive to insect pollinators.
These are usually positioned strategically to attract pollinatorstothereproductiveorgansoftheflower.Theproducts
of other glandular trichomes are used defensively, often as
anti-feedants against herbivores, and these trichomes are
usually distributed over the surfaces of the leaves.
Many plants produce more than one type of trichome. A
classic example is maize, which produces three structurally distinct types: macrohairs, prickle hairs and bicellular microhairs. Different trichome types that are
produced within a single species are probably determined
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by different developmental pathways; mutations that
affect the production of one type of trichome have no
effect on the distribution of the others. The macrohairless
(mhl) mutation of maize affects the production of macrohairs on the adaxial surface of the leaves, but does not
affect the formation of prickle hairs or microhairs [38]. It
seems likely that trichomes that are initiated by different
developmental programmes are probably also patterned
by different mechanisms. It is also likely, however, that
there is some cross-talk between the patterning mechanisms for different types of trichomes that co-exist within
the same epidermis, because clusters of different trichome types do not arise. Nothing is known about interactions between trichome patterning mechanisms,
although in densely pubescent epidermis, where clustering might be problematic, cross-talk could involve the
transmission of short-range inhibition by cell-to-cell communication [39].
The density and diversity of trichomes within aerial
epidermal layers expanded dramatically with the radiation of the Angiosperms [40]. In a very interesting recent
study of basal Angiosperms, Carpenter [2] concluded
that trichomes might have evolved independently several
times within these groups. In the Nymphaeales and
Austrobaileyales, trichomes were lost or modified to form
hydropotes and ethereal oil glands, respectively. Hydropotes are multicellular structures in which the hair-like
extension excises at maturity to leave a basal set of cells.
These cells are a specialisation of this group of water
plants and are believed to have secretary or absorbative
functions. There are considerable similarities between
the organization of the cells of the modified trichomes in
complexes and the cells that are associated with the
stomata in these basal Angiosperms. This has led to
the suggestion that trichomes, hydropotes and ethereal
oil glands might have evolved from stomata [2]. A
common evolutionary origin could have significant implications for the mechanisms used to pattern trichomes in
basal Angiosperms, and for the interactions between
mechanisms that govern the distribution of stomata
and trichomes in these species.
Pre-patterning of trichomes on leaves
Pre-patterns influence the distribution of trichomes in
broad expanses of epidermis in ways that are analogous to
their influence on stomatal distribution. Trichomes are
often unequally distributed between the adaxial and
abaxial sides of leaves. They reflect light and can significantly reduce the heat load of leaves, a role often seen
in the silvery pubescent leaves of Mediterranean species.
The concentration of trichomes on the adaxial epidermis
of leaves reduces the heat load because this surface
receives most incident radiation.
In contrast to stomata, trichomes are often concentrated
in the epidermal layers that overlie the vascular strands in
Current Opinion in Plant Biology 2007, 10:70–82
76 Growth and development
leaves (Figure 1d,e). In maize, however, two of the three
trichome types (i.e. macrohairs and prickle hairs) are
formed in rows between the vascular strands
(Figure 1b). Macrohairs and prickle hairs are formed only
on the adaxial surface of maize leaves and they form
within or adjacent to rows of bulliform cells (Figure 1b).
Bulliform cells have a distinct cuticular structure and
contract in width when the leaf is dehydrated. This
contributes to leaf rolling, which is believed to reduce
water loss under drought stress [4]. Bulliform cells,
although organized in rows, are not defined exclusively
by lineage [10]; they are determined by a pre-pattern of
positional information that could involve signals from the
vascular tissue. Stomata do not form in the rows of bulliform cells, so if both cell types use positional information
from the veins, this common pre-pattern must be interpreted in different ways in the determination of the two
types of epidermal structure.
Most plant species undergo a significant amount of vegetative growth before reproductive development. Vegetative growth may be divided into juvenile and adult
phases, which are recognizable by distinct anatomical
features. Changes in trichome density or type are often
associated with the shift from the juvenile to the adult
vegetative phase. In maize, for example, macrohairs and
bulliform cells are present only on leaves formed during
the adult phase; juvenile leaves have no trichomes. The
glossy15 (gl15) gene of maize encodes an APETALA2
(AP2)-type transcription factor [41,42]. This gene promotes the juvenile growth phase; gl15 mutants show
precocious formation of several adult characters, including macrohairs. Gibberellins (GAs) promote the transition
from the juvenile to the adult phase in maize and consequently promote macrohair formation. Mutants of
maize that are insensitive to GAs, such as dwarf1 (d1),
show delayed macrohair formation. GAs work in antagonism to gl15 in the induction of adult phase vegetative
growth and macrohair formation, and macrohair formation
is more sensitive to the GA signal than to the inhibitory
influence of gl15 [38].
In Arabidopsis, vegetative phase change also influences
trichome production. In rosette leaves, trichome number
increases on the adaxial side in each new leaf, and after a
delay, trichomes form on the abaxial side [43]. The
density of trichomes in later leaves decreases on the
adaxial surface. This changing pattern continues into
the cauline leaves on the inflorescence stem. GAs promote the transition from juvenile to adult vegetative
growth and the production of leaf trichomes. GAs might
stimulate the expression of genes that are involved in
trichome initiation, particularly GLABROUS 1 (GL1) [44].
Recently, the GLABROUS INFLORESCENCE STEMS
(GIS) gene, which affects trichome production in the
adult vegetative phase in Arabidopsis, was identified
Current Opinion in Plant Biology 2007, 10:70–82
[45]. Loss of function of GIS causes premature
decreases in trichome production on successive leaves
and stem internodes, whereas GIS overexpression promotes trichome formation on inflorescence organs and
maintains high levels of trichomes on the adaxial surfaces
of cauline leaves. GIS has no effect, however, on trichome
production in rosette leaves. GIS encodes a C2H2 zincfinger protein that might operate as a transcriptional
regulator. The expression of some of the genes that are
involved in trichome initiation (i.e. GL1, GLABRA 3 [GL3]
and ENHANCER OF GLABRA 3 [EGL3]) is positively
regulated by GIS, although the expression of TTG1 is
unaffected by GIS activity.
GAs also modify trichome production as growth phases
change in Arabidopsis. Constitutive GA response mutants,
such as spindly (spy), cause earlier production of abaxial
trichomes on leaves and increase trichome production on
stems [46]. The GA signal seems to work through the
induction of GIS, although GA signalling can induce
trichome formation locally and independently of GIS
[45]. The activity of GIS in Arabidopsis is somewhat
analogous to that of gl15 in maize, although gl15 works to
repress the transition to the adult vegetative phase
whereas GIS works to promote the adult growth phase.
Trichome patterning
Trichome initiation is believed to be patterned, because
adjacent or clustered trichomes rarely arise in epidermis.
Even where epidermal tissues are densely pubescent,
such as the fibres of the cotton ovule, there is evidence
for trichome patterning [39]. The pathway that governs
trichome initiation is very well understood in Arabidopsis,
both at the genetic and the biochemical levels. As a
consequence, understanding the mechanism that controls
the patterning of trichome production has advanced very
rapidly. This mechanism has been reviewed extensively
[3,13–15], but is also summarized here for clarity.
Specification of trichome cell identity requires the interaction of a group of three proteins. The WD40 repeat
(WDR) protein TTG1 provides a scaffold on which other
proteins interact. Its interaction with diverse proteins
results in a range of different developmental fates, trichome development is specified by interaction with particular bHLH and MYB proteins. The bHLH proteins
GL3 and EGL3 regulate trichome, root hair and anthocyanin development. These bHLH proteins interact with
MYB proteins that exhibit specificity for individual developmental pathways. The R2R3 MYB protein GL1 specifies trichome development, whereas the single-repeat
MYB protein TRY (and close homologues, including
CPC and ENHANCER OF TRY AND CPC [ETC])
prevents the formation of a functional WDR/bHLH/MYB
complex by competing with GL1 for bHLH binding.
Expression of TTG1, GL3 and GL1 occurs initially in
all leaf epidermal cells. This transcriptional complex
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Cell patterning in aerial epidermis Martin and Glover 77
activates TRY expression and expression of GL2, which
encodes a homeodomain protein that is required for
trichome development post-patterning. TRY is transported intercellularly and inhibits the formation of the
active TTG1–GL3–GL1 complex in neighbouring cells.
Eventually, the balance is broken causing some epidermal cells to develop into trichomes and inhibit their
neighbours, generating a pattern. It is not known what
causes the initial differences between cells that result in
varying strengths of TTG1–GL3–GL1 complex, but
suggestions have included small random differences in
transcript level and cell cycle effects.
One of the problems with the use of model systems is the
assumption that the mechanisms that operate in the
model are universally applicable. The initiation and patterning mechanisms that have been established in Arabidopsis have often been assumed to apply to trichome
patterning in plants generally, but the evidence supporting this assumption is sparce [3]. For example, just one
orthologue to GL1, GaMYB2 of cotton, has been found
[47] despite the availability of two other plant genome
sequences. It is also evident that the ancestor of the GL1
gene diverged from the MYB genes that regulate anthocyanin biosynthesis relatively recently. Amongst Angiosperms, the operation of the WDR–bHLH–MYB complex
to control trichome initiation might be limited to the
Rosids [3]. Other distinct regulatory genes have been
demonstrated to induce different types of trichome in
Asterids [3]. In addition, many species produce multiple
types of trichome that appear to be regulated independently (e.g. [38]). If trichomes have evolved independently on several occasions, it is also likely that they are
patterned by distinct mechanisms.
Functional aspects of trichome patterning
in leaves
Trichomes have very diverged functions in plants, and
their densities on particular organs might relate to specific
functions. In contrast to stomatal patterning, there do not
appear to be strong environmental effects that influence
trichome density and patterning. Where environment is
correlated with particular levels of trichome density, the
association tends to be an adaptive feature of colonising
species rather than an acclimation that is induced in
plants by particular environmental conditions. At the
level of communities, plants that grow in arid environments are more likely to be highly pubescent than those
growing in more favourable water conditions. It has been
suggested that pubescence affects transpiration directly
by creating a layer of still air next to the leaf, so that air
movement is reduced and transpiration is lowered. This
boundary layer resistance is increased in highly pubescent
leaves.
Some species of Tillandsia are ‘atmospheric epiphytes’
and have a highly specialized water uptake system that is
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based on elaborate foliar trichomes that can absorb water
from moist air. Comparison of Tillandsia species that have
different degrees of pubescence failed to show any reduction in water loss in species with higher trichome densities [48]. In fact, the most important role for trichomes
under arid conditions is probably light reflectance to
reduce the heat load of the leaves [40,48,49]. Pubescent
leaves of poplar (Populus alba) have been shown to reflect
50% of incident light, whereas glabrous leaves (achieved
by shaving) reflect only 20% [40].
Another function of leaf trichomes is defence against
biotic challenges. This can be a function of either glandular or non-glandular trichomes. Non-glandular trichomes
can inhibit the movement and survival of insect herbivores. An example of this activity is illustrated by the
traditional use of bean leaves to protect bedding against
bedbugs in Balkan countries. Richardson [50] found that
the insects became entangled in the hooked hairs on the
abaxial leaf surface and starved. Higher trichome density
might also deter the laying of insect eggs and the survival
of larvae [51].
Glandular trichomes not only offer physical resistance to
herbivory but also often produce chemical deterrents that
act as anti-feedants. The significance of trichome density
to herbivore damage and other biotic challenges (including bacterial and fungal infections) is complex. Chemical
deterrents might also deter natural predators of herbivores, so the significance of resistance conferred by trichomes is likely to depend on the balance between the
population structures within plant–herbivore–predator
communities [52].
Interactions between stomatal and trichome
patterning
Very little is known of how the patterning mechanisms
that control stomatal initiation interact with those governing trichome initiation. Many of the mutations that affect
stomatal patterning have been isolated and studied in the
glabrous C24 genetic background. However, Serna and
Fenoll [29] pointed out that satellite meristemoids form
after three asymmetric divisions of the MMC in C24, but
in Colombia (which does produce trichomes), the number
of asymmetric divisions varies from one to three. This
difference could be due to interaction between the lineage-based stomatal patterning mechanism and the trichome patterning mechanism in Colombia.
Pre-patterning mechanisms, such as those seen in maize,
keep stomatal rows separate from trichome or bulliform
cell rows; so any interactions in maize would appear to
occur at the level of the pre-patterns.
Experiments using the MIXTA gene of Antirrhinum majus
to increase trichome production on tobacco leaves also
resulted in a very significant reduction in the numbers of
Current Opinion in Plant Biology 2007, 10:70–82
78 Growth and development
stomata [53]. This was interpreted as the result of direct
competition between the mechanisms that specify trichomes and those specifying stomatal complexes. Trichomes are usually initiated earlier than stomata, and if
very high densities of trichomes are initiated then fewer
stomata are initiated later. This competition seemed to
work at the level of the stomatal meristemoid in tobacco,
because trichomes never formed on the subsidiary cells
surrounding the guard cells. The same experiment in A.
majus, however, gave rise to stomata with outgrowths on
the subsidiary cells, suggesting that competition between
trichome or papillate cell fate and stomatal cell fate occurs
at a later stage in this species [54].
Functional aspects of epidermal cell
patterning in flowers
Scientific attention has been focussed on epidermal patterning in leaves, perhaps as a result of the clear importance of stomatal function to photosynthesis. However,
epidermal cell patterning often contributes very significantly to organ function in flowers.
Conical-papillate cells
Conical-papillate cells are the simplest of the specialized
epidermal cells found on flowers, but analysis of their
function has revealed an unexpected degree of complexity. Conical-papillate cells are found on the petals of the
majority of Angiosperm species, including members of
the Austrobaileyales, and they are considered to be a
relatively ancient trait [55]. They are usually found only
on the petals, except in those species where other floral
organs have become specialized for pollinator attraction.
The production of conical-papillate cells by organs whose
primary function is to attract pollinators has led to the
hypothesis that these specialized cells play a central role
in this attraction, but their diverse effects on petal form
and function might attract different pollinators through
different mechanisms.
Conical-papillate cells on the petal lobes of A. majus are
associated with greater pollination success when compared
to the flat-cells of mixta mutants in emasculated fieldgrown plants [56]. These cells are distributed across the
lobes of the dorsal, lateral and ventral petals, but are mainly
absent from the corolla tube. Their absence from the mixta
mutant supported the suggestion of Kay et al. [57] that
conical-papillate cells might enhance the colour of the
petal [58,59]. Kevan and Lane [60] showed that bees could
distinguish between petals of different species using touch
alone. Our recent experiments have confirmed that bees
can distinguish tactilely between artificial casts of conical
and flat-celled petals (H Whitney, L Chittka, BJ Glover,
unpublished). Conical-papillate epidermal cells have also
been shown to increase intrafloral temperature [61]. Warmer flowers might provide a direct metabolic reward to
pollinators, which is likely to be particularly significant at
Current Opinion in Plant Biology 2007, 10:70–82
dawn, and have been shown to be more attractive even
when equal rewards are offered [62].
One site of scent production in A. majus is the conicalpapillate cells [63]. Although their conical shape is not
necessary for scent production (H Whitney, BJ Glover,
unpublished), their extended and angled cell walls might
enhance scent dispersal. In species in which nectar spurs
are formed from extensions of the petal tissue, conicalpapillate cells act as secretory sites, producing the nectar
that collects in the spur. Analysis of the nectar spur of the
orchid Gymnadenia odoratissima revealed that the secretary conical-papillate cells were particularly pronounced
in the distal region of the spur [64].
Recent observations in both Antirrhinum and Petunia have
shown that the production of fields of conical-papillate
epidermal cells on the inner petal epidermis also affects
the degree of reflexing of the petal, and thus the size and
shape of the petal surface presented to potential pollinators (K Baumann, M Perez-Rodriguez, C Martin, unpublished). This effect on petal form might also impact
pollinator attraction and consequent reproductive success
[65].
The MIXTA gene encodes a MYB transcription factor that
controls the development of conical-papillate cells in the
petal lobes of Antirrhinum [58]. MIXTA is expressed only
in the adaxial epidermis of the petals [53]. Antirrhinum
contains a small group of MYB proteins that have highly
significant structural similarity to MIXTA [66]. Duplication of an ancestral MIXTA-like gene, and subsequent
mutation of regulatory DNA, might thus explain the
development of conical-papillate cells and trichomes in
other regions of the petal. AmMIXTALIKE1 (ML1) is
expressed in the ventral petal tube, and in the hinge of
the Antirrhinum flower. It is involved in the development
of the elaborated conical-papillate cells of the flower’s
landing platform, and in the development of the trichomes of the tube that capture the pollen from the
surface of pollinators for redistribution to the stigmatic
surface [66].
Trichomes
The function of floral trichomes is dependent not only on
their type but also on their patterning. In flowers, trichomes are often found in fields. A field of trichomes
presents a very different surface to a surface containing
evenly dispersed trichomes, and these differences are
enhanced when the trichomes themselves differ in size,
shape and structure.
Stigmatic papillae, i.e. unicellular non-glandular trichomes, are found in both plants with dry stigmas and
plants with wet stigmas. In species that have dry stigmas,
such as Arabidopsis, the papillae themselves act as the
point of pollen capture (Figure 3a). Although no mutants
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Cell patterning in aerial epidermis Martin and Glover 79
Figure 3
Cell specialisations and patterning in flowers. (a) Stigmatic papillae (SP) on the dry stigma of Arabidopsis. Scale bar indicates 500 mm.
(b) Conical-papillate cells on the petal epidermis of Veronica dichrous. Scale bar indicates 20 mm. (c) The ‘beetle daisy’, Gorteria diffusa.
(d) Close-up of the beetle spot on a petal of Gorteria diffusa. (e) The specialized epidermal cells in the beetle spot include large trichomes.
that have defects in papillar cell development have been
identified, cell ablation experiments have shown that the
stigmatic papillae are essential for pollination [67]. In
species that have wet stigmas, such as tobacco, the
papillae might still protrude from the secreted matrix,
and facilitate the capture of pollen. Their large surface
area allows faster secretion at maturity, and they may also
burst, releasing exudates swiftly [68,69]. Little is known
about the development of stigmatic papillae, but the
observation that one MIXTA-like gene is expressed in
the stigmatic papillae of Antirrhinum suggests that they
might develop through mechanisms similar to those seen
in conical-papillate cells (F Jaffe, BJ Glover, unpublished). It has also been shown that endoreduplication
is a key stage in the development of stigmatic papillae, as
it is in the development of Arabidopsis trichomes. The
stigmatic papillae of Triglochin maritimum (sea arrowgrass)
have been shown to have DNA contents of up to 64C [70].
These data suggest that proteins that are involved in
uncoupling DNA synthesis and cell division are as essential in stigmatic papillae as they are in Arabidopsis trichomes. The stigmatic surface is usually composed of a
uniform field of papillae, so patterning here is clearly
distinct from that found in most other organs and might
reflect the constitutive expression of key genes, perhaps
including MYB transcription factors.
Trichomes on the anthers may play a simple role in
deterring predatory insects from acquiring protein-rich
pollen. In certain species, however, they have also
evolved to play key roles in pollination strategies. The
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anthers of Vigna radiata (mungbean) have a network of
overlapping trichomes bent close to the surface of the
anther. These increase the stiffness of the anther, facilitating the transfer of pollen from the anther to the
emerging stigma [71]. Another unusual role for anther
trichomes has been demonstrated within the genus Solanum. Tomato (Solanum lycopersicum) and closely related
species produce anthers that have interlocking trichomes
on their margins. These trichomes cause the five anthers
to hold together as a single structure, the anther cone.
Solanum species have poricidal anthers, and attract pollen-collecting bees that release the pollen by vibrating
their flight muscles, a system known as buzz-pollination.
In the majority of Solanum species, bees grapple with each
anther separately, but in the tomato clade, the interlocking trichomes cause the five anthers to be treated as a
single structure that provides more efficient pollen dispersal. Loss of the anther trichomes in the dialytic mutant
causes the anthers to develop independently, and dramatically reduces fruit set [72].
In the petal, non-glandular trichomes can be difficult to
distinguish from conical-papillate cells. Indeed, the continuum from conical cell through papilla to short trichome
and then long trichome that is found on many petals only
serves to underline the developmental, and presumably
molecular, relationship between these cell types. Often,
the only distinguishing feature is the patterning of the
different cell types; papillae are almost always found in
fields whereas trichomes are more usually separated by
one or more pavement cells. Non-glandular trichomes of
Current Opinion in Plant Biology 2007, 10:70–82
80 Growth and development
the petal often play a major role in pollen capture and
redistribution. For example, the adaxial epidermis of the
tube portion of the ventral petal of Antirrhinum contains a
tangled mass of long, multicellular trichomes. These
trichomes trap pollen from the bodies of nectar-gathering
bees, and can then brush it onto the bodies of subsequent
visitors. In this way, pollen is spread around the flower
and between flowers, maximising the male component of
reproductive fitness. MIXTA-like genes also play a role in
the development of these non-glandular trichomes, with
AmMYBML1 being expressed in these cells. Loss of
AmMYBML1 expression is associated with loss of these
particular trichomes, supporting the hypothesis that this
MYB transcription factor is necessary for their development [66].
The diversity of roles played by conical-papillate cells
and trichomes in floral organs can be attributed to differences in their patterning mechanisms. More extreme
examples of such relationships are found in species that
use specialized epidermal cells in elaborate ways. For
example, the South African beetle daisy, Gorteria diffusa,
produces 2–4 ray florets that have dark spots which closely
mimic the pollinating fly, Megapalpus nitidus [73]. These
spots are composed of several specialized cell types,
including multicellular trichomes, that give a threedimensional appearance (Figure 3c,d,e).
Stomata
Stomata are necessary on all photosynthetic organs, and
are found in flowers in the epidermis of sepals, stamens
and carpels. Their patterning and morphogenesis in
sepals is similar to that in leaves. In the snow buttercup,
Ranunculus adoneus, the small number of stomata that
develop on the carpel are essential for the metabolism of
the entire flower [74].
Modified stomata are also essential for correct functioning
of the nectaries. Nectary position within the flower varies
greatly between species, but the majority of nectaries are
very similar in structure. Their epidermal surface is
composed of many stomata, which are interspersed with
pavement cells. The pavement cells can sometimes be so
few in number that the stomata are contiguous [75].
These stomata are modified to remain permanently open
[76,77]. Little is known about the molecular processes
that control this stomatal patterning, but nectaries
throughout the eudicots are specified by CRABS CLAW
genes, suggesting that the stomatal patterning mechanism is common to diverse species that have nectaries on
different organs [77].
Conclusions
The distribution and patterning of specialized cell types
within aerial epidermis is closely linked to their function.
Recent advances in understanding the signalling pathways mean that cell patterning is reasonably well underCurrent Opinion in Plant Biology 2007, 10:70–82
stood in Arabidopsis leaves. However, there are likely to
be multiple pathways patterning trichome production in
individual plants and across the plant kingdom. There
might also be multiple pathways patterning stomata.
Development of our understanding of epidermal cell
patterning in its widest context will significantly enhance
our appreciation of how cells function within multicellular organisms.
Acknowledgements
We thank Paula Rudall for the photograph shown in Figure 3c and Meredith
Murphy Thomas for the photographs shown in Figure 3d,e. CM
acknowledges support through the core strategic grant awarded to JIC by
the Biological and Biotechnological Science Research Council, UK.
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