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Stomata

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DOI: 10.1002/9780470015902.a0026526

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Stomata
Jingjing He, State Key Laboratory of Hybrid Rice, Department of Plant Sciences,
College of Life Sciences, Wuhan University, Wuhan, China
Yun-Kuan Liang, State Key Laboratory of Hybrid Rice, Department of Plant Sci-
ences, College of Life Sciences, Wuhan University, Wuhan, China
As adjustable pores, each delimited by a pair of
guard cells, stomata are central determinants of
plant photosynthesis, transpirational cooling and
ecological adaptability, which have huge impact
on global water and carbon cycles, plant compet-
itiveness and nutrients in foods. The specialised
guard cell anatomy and membrane ion transport
enable plants to adapt stomatal aperture rapidly to
hormone and environment changes. In contrast to
the highly conserved simple structure across land
plants, the stomatal size, density and distribution
patterns vary substantially among species or geno-
types within a species providing ample genetic
resources on which selection can operate. Study of
the development and function of stomata is crucial
to understand cell fate specification, signal trans-
duction and plant–environment interactions and
inform approaches to breed ‘climate change ready’
crop varieties with improved agricultural capacity
and food nutrients.
Introduction
Plants use and lose a lot of water for growth and transpirational
cooling. Even if they do not live in particularly dry places, most
plants will occasionally encounter water stress for shorter or
longer periods of time. When water availability is limited, one of
the fast responses of plants is to close stomata, the microscopic
pores typically found in the epidermis of leaves and vegetative
stems. Stomata (singular, stoma), sometimes anglicised as sto-
mates, which mean ‘mouths’ in Greek, do resemble tiny mouths
eLS subject area: Plant Science
How to cite:
He, Jingjing and Liang, Yun-Kuan (February 2018) Stomata. In:
eLS. John Wiley & Sons, Ltd: Chichester.
DOI: 10.1002/9780470015902.a0026526
eLS © 2018, John Wiley & Sons, Ltd. www.els.net
Introductory article
Article Contents
• Introduction
• Stomata Structure, Development
and Arrangements
• Stomatal Function and the Mechanistic Basis
• Stomatal Response to Hormone
and Environment Changes
• Concluding Remarks
• Acknowledgement
Online posting date: 16th February 2018
surrounded by swollen lips. The ‘lips’ are actually a pair of guard
cells, which can swell up to open or deflate to close the central
pore through which water as vapour passes into the atmosphere
as a price to pay for the CO2 that diffuses into the leaves for the
photosynthesis. Therefore, plants use stomata to simultaneously
regulate CO2 uptake and water loss and directly influence the
CO2 assimilation and transpiration rates (Raven, 2002; Ruszala
et al., 2011).
Apart from adjusting stomata aperture, plants may exert control
over their gas exchange rates by varying stomatal development
programme. The more stomata per unit area (stomata density), the
more CO2 can be taken up and the more water can be released.
The balance between these two processes depends on stomatal
responses to internal and external stimuli and the synchrony of
stomatal behaviour relative to mesophyll demands for CO2 (Law-
son and Blatt, 2014). Stomatal pores can actively close up to
prevent microbial entry and thus protect plants from pathogen
infection and yield loss (Melotto et al., 2006). Stomata can pro-
foundly impact on global carbon and water cycles as well as plant
competitiveness and the dietary nutrition of crop products that are
likely compounded by the ongoing climate change especially the
increasing atmospheric CO2 (Hetherington and Woodward, 2003;
Myers et al., 2014). See also: Stomatal Patterning
The growing concern over the effects of climate change has
reinvigorated stomatal research, aiming at selecting and using
crop genotypes with less water requirements and enhanced stress
tolerance to produce more food to feed the burgeoning global
population along with the growing pains of water scarcity. This
introductory article gives an overview of our current state of
knowledge with regard to the stomata structure, the evolution
and diversity of stomata traits, continues with consideration of
how plants control stomatal apertures and regulate gas exchange
and ends with a consideration of approaches to develop ‘climate
change ready’ crop varieties with improved ecological adaptation
and agricultural capacity.
Stomata Structure, Development
and Arrangements
Stomata are evolutionarily very ancient and have been found in
fossils dating from more than 400 million years ago. Although
1
 Stomata
(a)
(b)
Figure 1 The phenotypes and distribution of stomata. (a,c) Dumbbell-shaped stomata of Setaria viridis typical of the grasses. (b,d) The kidney-shaped
stomata typical of other species such as Commelina communis. (e) Stomata in grass are arranged strictly in cell files with the identical orientation. (f) Stomata
distribute scattered and no-isotropic orientation in C. communis.
the stomatal sizes, numbers and arrangement patterns and their
surrounding cells have been diversified, the morphology of the
individual stomatal complex remains largely unchanged, that is
a central pore bordered by a pair of guard cells that originate
from the same parental cell and a substomatal cavity sitting on the
mesophyll cells. Both the aperture and the number of stomata on
the surface of photosynthetic organs are cocontrolled by genetics
and environmental signals for stomata to ‘set’ gas exchange rates
to suit the prevailing environmental conditions (Hetherington
and Woodward, 2003; Assmann and Jegla, 2016). To conserve
water, desert plants as well as pine trees often have their stomata
recessed in stomatal crypts, which are small chambers below the
surface of the leaf or stem.
There are two distinct types of guard cells, dumbbell- and
kidney-shaped, represented by Setaria viridis (Figure 1a, c and
e) and Commelina communis (Figure 1b, d and f), respectively.
Current evidence tends to support a notion that stomata with
dumbbell-shaped guard cells are more advanced in evolutionary
terms and more efficient physiologically because their guard
cells require fewer solutes and less water to achieve a given
unit increase in aperture (Raschke, 1975; Hetherington and
Woodward, 2003). Guard cells are specialised epidermal cells as
they contain chloroplasts, although the role of guard cell photo-
synthesis in stomatal conductance responses is actively debated
in the literature. The guard cells of a few species including the
lady’s slipper orchid are lacking chloroplasts (Outlaw et al.,
1981; Assmann and Zeiger, 1985; Azoulay-Shemer et al., 2015).
Stomata vary widely in distribution, arrangement, size and
frequency among species or genotypes within a species. Stomata
are typically 20–50 μm long and occur at densities between 50
and 300 mm−2 , and can often be found on stems, leaves, flowers
and fruits, but not on roots. In leaves, stomata may occur on
both surfaces (amphistomatous, e.g. in Arabidopsis) or on only
one surface (hypostomatous) as in most woody plants including
2 eLS © 2018, John Wiley & Sons, Ltd. www.els.net
(c) (e)
5 μm
(d) (f)
20 μm
apple and peach trees. However, poplar and willow are exceptions
among woody plants as they are amphistomatous. Stomata are
usually absent altogether from the submerged leaves of aquatic
plants (astomatous). The majority of parasitic plants are often
lacking stomata.
Plants produce stomata in organised patterns. In grasses,
conifers and some dicots, stomata occur in parallel rows, but in
leaves with netted venation they are often ‘randomly’ scattered.
Arabidopsis stomata are produced by a tightly coordinated series
of stereotypical cell divisions and successive cell-state transi-
tions (Figure 2). First, a subset of protodermal cells acquires
the stomatal progenitor cell fate to become meristemoid mother
cells (MMC), although the regulatory mechanism remains to
be fully discovered. Then the MMC divides asymmetrically to
produce a small triangular cell called a meristemoid and a larger
stomatal-lineage ground cell (SLGC). The SLGC can either
differentiate directly into a pavement cell or may reacquire the
MMC fate and undergo spacing divisions to produce a satellite
meristemoid. The meristemoids could differentiate directly into
a guard mother cell (GMC) or undergo several rounds of ampli-
fying divisions (the division of meristemoid that regenerates
meristemoid and increases the number of SLGCs produced by
a single lineage). Finally, a bisection of GMC occurs to yield
two cells, which concurrently proceed through a final cell-state
transition to form mature guard cells (Pillitteri and Torii, 2012).
The genetic toolbox that control stomata development is highly
conserved between Arabidopsis and rice, despite their stomatal
guard cells are of different morphology. However, in contrast
to Arabidopsis, there is no amplifying divisions required for
the formation of rice stomata and rice GMCs need to recruit
their neighbouring cells to subsequently create subsidiary cells
that grow faster than guard cells and eventually together with
guard cells to form the pore (Liu et al., 2009). The spiralling
effect of amplifying divisions renders stomatal orientation in
 Stomata

Spacing Amplifying
division division

Protodermal Young Mature

(a) MMC Meristemoid GMC
cell stomata stomata

Protodermal Stomata Young Mature

(b) GMC
cell precursor stomata stomata

Figure 2 The development of stomata. (a) Developmental framework of angiosperm stomata based on Arabidopsis. A subset of protodermal cells
(white) acquires the MMC identity (dark blue) and divides asymmetrically to create a meristemoid (light blue). The meristemoid either differentiates directly
into a GMC (guard mother cell) (red) or undergoes up to three rounds of amplifying divisions. The GMC divides symmetrically into paired young guard
cells (purple), later forming the mature guard cell (dark green). (b) Developmental framework of monocot stomata based on rice. Protodermal cells gain
the stomata precursor fate and divides asymmetrically to form GMCs (grass green). The GMC divides symmetrically to form immature GC (guard cell) pairs
(light green) that differentiate into mature GCs (dark green).

Arabidopsis to appear to be typically ‘random’. Amplifying
divisions are absent from all monocots, including rice whose
stomata is typically oriented parallel to the long axis of the leaf.
It is worth a mention that not all monocots especially those
with broad, petiolate leaves and reticulate venation arrange their
stomata in rows, nor do all monocots have the dumbbell-shaped
guard cells. Amplifying divisions are also absent from most
early-divergent angiosperms, including Amborella. Regarding
the mosses, Physcomitrella patens stomata develop entirely
without amplifying divisions, but more than three amplifying
divisions can occur in Houttuynia cordata. The absence or pres-
ence, and if presence the different times of amplifying divisions
largely contribute to the great variations in stomata patterning,
size and frequency among species (Peterson et al., 2010). During
the past decade, five HLH family members (SPCH, MUTE and
FAMA plus SCRM and SCRM2) and three EPFs (EPF1, EPF2
and EPFL9) have been identified in Arabidopsis as the key play-
ers responsible for stomata development and distribution. The
five HLH family members control cell divisions and cell-state
transitions to promote stomata formation. Those HLH family
members are regulated by the EPFs via a signalling cascade to
enforce stomata spacing, that all the stomata are always sepa-
rated from each other by at least one intervening cell. This is
referred to as one-cell spacing rule (Larkin et al., 1997). Besides,
their corresponding orthologues have been found to function
in a largely conserved way among dicots (e.g. Arabidopsis),
monocots (e.g. rice) and early land plants including P. patens,
although some MUTE and SPCH functions might have diverged
to some extent (Liu et al., 2009; Vatén and Bergmann, 2012;
Hepworth et al., 2018).
As described earlier, rice stomatal complexes contain sub-
sidiary cells that are located adjacent to a guard cell, but
morphologically distinguishable from neighbouring pavement
cells in a mature leaf epidermis. Stomata can be classed either
as anomocytic stomata or as paracytic stomata depending on
the absence or presence of subsidiary cells. It is traditionally
assumed that anomocytic stomata are primitive, relative to
paracytic stomata. When the relations between guard cells and
their neighbouring cells are considered, stomata can be termed
as mesogenous, perigenous and mesoperigenous. Mesogenous
refers to a stomatal complex in which the neighbouring cells
are formed from the same meristemoid as the GMC, following
one or more asymmetric divisions. In a perigenous stomatal
complex, the GMC and all the neighbouring cells are formed
from different protodermal cells, whereas in a mesoperigenous
stomatal complex, both mesogene and perigene neighbouring
cells are present (Rudall et al., 2013).
Stomatal Function and the
Mechanistic Basis
The high CO2 levels of Silurian–Devonian times, when the early
plants started to move up and colonise the land, meant that CO2
was readily available for photosynthesis to occur, whereas the

eLS © 2018, John Wiley & Sons, Ltd. www.els.net 3

 Stomata
lack of water and the coincident high temperature and light inten-
sity placed a great challenge for plants to retain water and avoid
drying out. To this end, plants ingeniously acquired a cuticle layer
to cover their photosynthetic organs. However, the waxy cuticle
prevents the intake of CO2 , the substrate needed for photosyn-
thesis to operate. This dilemma was solved with the advent of
stomata, as the stomatal guard cells can quickly perceive and
integrate environmental signals, leading to the adjustments of
stomatal aperture and even density in long term and therefore
optimise the trade-off between carbon gain and water loss (Raven,
2002; Ruszala et al., 2011).
The most important characteristic of stomata is that they can
open and close, and the change in size of their aperture regulates
gas exchange. Rapid stomatal movement to reset pore aperture
requires two crucial innovations in guard cell behaviour. The
first is the specialised guard cell anatomy. It has long been
observed that the composition of guard cell wall for example the
micellar structure differs significantly to that of epidermal cells,
and the distinctly thickened but quite flexible inner walls of guard
cells were supposed to play an essential role in causing turgid
guard cells to bulge and separate, opening the stomatal pores
(Jones et al., 2003; Doblin et al., 2010; Amsbury et al., 2016).
Distinct from stomata of other plants, stomata in hornworts once
opened cannot be closed. It is likely because guard cell walls
in hornworts are devoid of arabinan that can modify the ability
of guard cell to respond to environmental and hormonal stimuli
(Lucas and Renzaglia, 2002; Jones et al., 2003). The second is
the mechanism that governs the osmotica shuttle between guard
cells and neighbouring cells and the ion transport across the
plasma membrane and tonoplast. When the plants perceive the
water stress, changes in turgor pressure take place when osmosis
and active transport between the guard cells and neighbouring
cells bring about concentration shifts in solutes, mainly potassium
(K+ ), chloride (Cl− ), malate2− and sucrose, resulting in water
leaving and causing the stomata to close. Stomatal opening, an
energy- and cytoskeleton-dependent process, also arises from the
transport, accumulation and release of osmotically active solutes.
A number of H+ -ATPases, outward and inward K+ ion channels
and at least two major types of anion channels, S-type anion
channels and R-type anion channels that mediate the efflux of
Cl− and malate2+ at the same time have been characterised in the
guard cells of many vascular plants (Santelia and Lawson, 2016).
See also: Membrane Transport in Guard Cells
Starch in guard cells has been observed to accumulate at night
and disappear slowly during the day, indicating starch degrada-
tion in guard cells is important for stomatal response to light,
which prompted investigation into the energy source required
for stomatal movement especially during the opening process
(Tallman and Zeiger, 1988; Horrer et al., 2016). Compelling evi-
dence suggests that the ATP (adenosine triphosphate) produced
by the electron transport chains in both mitochondria and chloro-
plast are likely the primary energy currency for the guard cells to
adjust pore size. Recently, Mclachlan and coworkers have shown
that the triacylglycerols stored in lipid droplets in Arabidopsis
guard cells can be mobilised and used as sources of ATP to drive
K+ uptake for light-induced stomatal opening (McLachlan et al.,
2016).
4 eLS © 2018, John Wiley & Sons, Ltd. www.els.net
Stomatal Response to Hormone
and Environment Changes
Stomata are often exposed to multiple and frequently conflicting
signals from the environment. Guard cells integrate these sig-
nals and dictate plants in short term to change stomatal aperture,
whereas in long term to adjust stomatal size and density; the over-
all result is the optimisation of gas exchange under the prevailing
environmental conditions. Significant variation in stomatal sensi-
tivity is known to exist among different species, and stomata of a
same genotype behaviour can be completely different when plant
growth conditions are different. In general, stomata is open in
response to photosynthetically active radiation (and there exists
a synergistic effect between red light and blue light in promot-
ing stomatal opening), high temperatures and high air humidity,
while closure is induced by darkness, low air humidity, drought
and plant hormone abscisic acid (ABA). A rapid rise of Ca2+ ,
reactive oxygen species, nitric oxide and cytosolic pH in guard
cells is often associated with stomatal closing, suggesting second
messengers play essential roles in mediating stomatal movement
(Kim et al., 2010; Lawson et al., 2012; Murata et al., 2015).
Ever since its discovery, ABA has been intensively studied
because of its versatile functions in regulating many develop-
mental and adaptive stress processes. The role of ABA in stom-
atal development and function has been well reviewed by Cutler
et al. (2010). See also: Plant Hormones. Interestingly, ABA
can enhance stomatal response to CO2 , which is the chief green-
house gas that is keeping accumulating in the atmosphere largely
because of the heavy use of fossil fuel and deforestation since the
commencement of industrial revolution. Atmosphere [CO2 ] now
stands at approximately 403 parts per million (ppm), surged from
280 ppm in 1750 (Brodribb et al., 2009). To uptake enough CO2
for photosynthesis to continue stomata open widely when [CO2 ]
is low, whereas high [CO2 ] induces reduction in stomatal aper-
ture as plants can afford to partially close their pores to conserve
precious water (Figure 3a). Elevated [CO2 ] depresses stomatal
conductance but enhances photosynthesis, water use efficiency
(WUE) and biomass accumulation in many species (Ainsworth
and Long, 2005) (see also: Water Use Efficiency of Cultivated
Crops). Accumulating evidence suggests that it is the concentra-
tion of CO2 inside the leaf [CO2 ]i , not the atmospheric [CO2 ] that
directly dictates stomatal aperture. ABA application or short peri-
ods of slight drought treatments that induce ABA biosynthesis
can rescue the phenotypic deficiency of roses and other horticul-
tural species when grown in humid greenhouse of being unable to
close stomata when exposed to elevated [CO2 ] and low air humid-
ity as well (Assmann, 1993; Chater et al., 2015; Engineer et al.,
2016). This practice is widely adopted to extend the shelf life of
cut flowers including roses.
Stomatal development is also controlled by [CO2 ], with stom-
atal density typically reduced in plants grown under elevated
[CO2 ] (Figure 3b). Lake and coworkers have recently beautifully
demonstrated it is the mature leaf to sense and transmit the sig-
nals, and then the stomatal density in developing leaves is modi-
fied (Lake et al., 2001). A trend has been observed on a geological
time scale that early evolved plants having lower stomatal densi-
ties also showed a greater mean stomatal size, whereas smaller
 Stomata

Short-term changes in stomatal aperture

Auxin ABA
High light Darkness
Blue light SA

Low [CO2] High [CO2]

High humidity Low humidity
(a)

Long-term changes in stomatal number

High Low
atmospheric atmospheric
CO2... CO2...

...indicates low ...indicates high

stomata density stomata density

(b)

Figure 3 Stomatal response to environmental signals and hormones. (a) In the short term, various factors control stomatal movements, such as
blue light, low CO2 , auxin as well as the high humidity that can induce stomatal opening, while darkness, high CO2 , abscisic acid (ABA), salicylic acid (SA)
and low humidity intend to induce stomatal closure. (b) In the long term, stomatal density is modified by time-changing atmosphere carbon dioxide levels.
When the atmosphere CO2 is rich, the stomatal density would be low. In contrast, when the atmosphere CO2 is low, the stomatal density would be high.
(b) Reproduced by kind permission of Web Manager Trish Roque (http://evolution.berkeley.edu/evolibrary/copyright.php) © The University of California Museum
of Paleontology, Berkeley, and the Regents of the University of California.

stomata were found in leaves of recently evolved species with
greater stomatal densities (Hetherington and Woodward, 2003;
Franks and Beerling, 2009), indicating the plasticity and eco-
logical adaptability of stomata development. It was generally
assumed that small stomata alter aperture faster than large stom-
ata. Therefore, high density of small stomata may represent the
best way of achieving maximal gas exchange and preventing CO2
starvation in periods of low atmospheric [CO2 ]. However, the
rapidity of stomata of plants that diversified under low or declin-
ing atmospheric [CO2 ] demonstrated by McElwain and cowork-
ers indicating that atmospheric [CO2 ] is likely a stronger driver of
stomatal closing rate than stomatal size (Elliott-Kingston et al.,
2016). In 2014, Myers and coworkers published an intrigu-
ing finding that the rising levels of atmospheric [CO2 ] caused
dietary deficiencies of zinc, iron and protein in crop plants,
which prompted a new research direction in selecting differences
between cultivars of a single crop and breeding for decreased
sensitivity to atmospheric [CO2 ] to mitigate the adverse effect of
climate change on global health (Myers et al., 2014).
Distinct from most plants whose stomata are open during the
day and closed at night, the stomata of a number of desert plants
are open only at night to absorb and convert CO2 into organic
acid, which are then converted back to CO2 during the day when
photosynthesis occurs. Adopting this so-called crassulacean acid
metabolism (CAM) photosynthesis strategy is useful to conserve
water, but the potential downside is that because plants close their
stomata during the day they do not have the benefits of tran-
spirational cooling (see also: Crassulacean Acid Metabolism).
Apart from taking advantage of the air currents, whether and how
these plants actively manage to avoid heat up and even sunburn
remains largely unknown. Another phenomenon that is notewor-
thy here is the so-called patchy stomatal conductance, that is,
plant leaves frequently exhibit dramatic spatial and temporal het-
erogeneity in stomatal behaviour. We still know very little of the
stomatal patchiness, but it might be a form of emergent property
that is inherently difficult to predict resulting from complex inter-
actions of guard cells and various environment parameters (Mott
and Buckley, 2000).
Concluding Remarks
The innovation of stomata and stomatal control over gas
exchange enabled the successful movement of plants from
aquatic to terrestrial habitats. Current evidence tends to sup-
port a single genetic origin of stomata in the ancestor to all

eLS © 2018, John Wiley & Sons, Ltd. www.els.net 5

Stomata
Light CO2
420
Hornworts
Mosses
Liverworts
480
Figure 4 Stomata evolution. Plants acquired the land around 480 million years ago (Mya), the acquisition of stomata approximately in 420 Mya. Mosses
and hornworts of the bryophytes and all of vascular plants have stomata.
stomatous land plants. Figure 4 shows that stomata are found
in the early land plants including hornworts and mosses. But
whether the pores in liverworts should be treated as primitive
stomata or just as gas chambers developed by convergent evolu-
tion is controversial (Rensing et al., 2008; Ruszala et al., 2011)
(see also: Evolution: Convergent and Parallel Evolution).
If they are just gas chambers, then the complete absence of
stomata in liverworts maybe interpreted either as a loss or a
plesiomorphy, depending on whether hornworts or liverworts
are sister to land plants (Villarreal and Renzaglia, 2015). A large
body of evidence shows that in both modern seed plants and
early land plants including mosses stomata possessed a suite of
active aperture control responses to water deficit via ABA and
to changes of atmospheric [CO2 ] (Ruszala et al., 2011; Franks
and Britton-Harper, 2016). However, based on their findings
that ferns lack the necessary signalling components for active
ABA-mediated stomatal closure, Brodribb and McAdam have
recently put forward a gradualistic model for stomatal evolution
suggesting that plants may gain active pathway after the diver-
gence of ferns (Brodribb and McAdam, 2011; McAdam and
Brodribb, 2013). In contrast, Cai et al. (2017) have reported that
genes of ABA reception and signalling components are found in
all stomata-bearing terrestrial plants including ferns, and argued
against the gradualistic model. Nonetheless, the evolution of
stomata and active stomata control over gas exchange merits
further investigation because of its importance for understanding
their influence on the rise of global vegetation.
The phenotypic effects of genetic and environmental factors
such as light, CO2 and water stress cause great variations in
stomatal size, density and distribution pattern among species or
genotypes within a species. The plasticity and ecological adapt-
ability of stomatal development prompted early investigators to
select and develop plant varieties with less water requirement
but improved ecological adaptation and agricultural capacity by
targeting stomata, for example by using ABA, a major player
in mediating plant adaptation to various stresses as a proxy.
The outcome is mixed as in many cases engineering stomata
6 eLS © 2018, John Wiley & Sons, Ltd. www.els.net
Vascular plants
Bryophytes
Land
Sea
Green algae
aperture through manipulating ABA metabolism and signalling
could enhance WUE and drought tolerance but often resulted in
retarded growth even when water supply is not limited.
Increasing or decreasing stomatal numbers would correspond-
ingly increase or decrease stomatal conductance in a given envi-
ronment. Therefore, selecting crop plants with alterations in
stomatal density to reduce plant water use was also explored.
Interestingly, in contrast to the ‘high density but smaller stom-
ata’ approach, the ‘low density but larger stomata’ could con-
fer drought tolerance without yield penalty under various water
stress conditions (Yu et al., 2008; Doheny-Adams et al., 2012;
Hughes et al., 2017). If more tests, particularly the field trials
can further substantiate these findings, genetically reducing stom-
ata numbers is likely a promising route to follow. Genome-wide
association study in combination with deep sequencing could be
used to efficiently mine the great genetic variations of stomatal
density, which somehow has been largely overlooked in modern
crop breeding history that is dominated by pursuing high-yielding
cultivars.
Great progress has been made in the past study of the stomatal
development and function. However, there are still many knowl-
edge gaps to bridge. To name just a few here, for example, the
evolution of stomata and active stomatal control, the mechanis-
tic basis of the distinct function of stomata in cotyledons and of
stomata in true leaves, and why and how plant differentially reg-
ulate stomatal development in the surfaces of leaf and stem? And
how plants control the programmed truncation of plasmodesmata
during stomatal maturation to establish symplastic isolation of
guard cells?
Acknowledgement
The authors acknowledge National Natural Science Foundation
of China (No. 31470360 and No. 31770282) for supporting this
work, and apologise to all colleagues whose work could not be
cited because of space constraints.

Glossary
Active stomatal control Stomatal opening and closure
regulated by non-hydraulic mechanisms stimulated by such as
light, CO2, and ABA, which is achieved via, for example, the
modulation of the light and the ABA signaling pathways to
drive membrane transports for solutes and water uptake or
loss to make stomatal aperture change. It requires metabolic
energy.
Convergent evolution A process whereby organisms including
plants that are not closely related independently acquire
similar traits to adapt to similar environmental constraints.
One-cell spacing rule A stomatal patterning rule for many
dicots, where two stomata are separated by at least one
intervening nonstomatal epidermal cell, which ensure guard
cells (GC) can efficiently exchange ions to regulate the pore
size.
Plant hormone Signal molecules produced within the plant
usually in very low concentrations that often operate in
concert to regulate plant growth, development and physiology.
Spacing divisions An SLGC asymmetric division that is
oriented away from a neighbouring stoma (or GMC) to
enforce stomatal spacing.
Subsidiary cell A cell type often found in grasses that is
neighbouring GC and morphologically distinct from other
epidermal cells.
Water use efficiency The amount of water required to produce
a unit of biomass.
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Further Reading
Lau OS (2017) Stomata. In: eLS. Chichester: John Wiley & Sons,
Ltd. DOI: 10.1002/9780470015902.a0002075.pub3.
Willmer C and Fricker M (1996) Stomata, 2nd edn. London: Chap-
man & Hall.