IliolngicaE Journal
the Linncan Suriely (1988), 34: 205-217. With 1 I figures
I
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Stornatal sensing of the environment
C. M. WILLMER
Departmenl o f Biological Science, UniuersiQ o f Stirling, Stirling FK9 4LA, Scotland
'I'lrc cllects of environmental lartors on stornatal behaviour are reviewed and the questions of
whether photosynthesis and transpiration control stomata or whether stomata themselves control
tlrc rates of these processcs is addressed. Light affects stomata directly and indirectly. Light can act
directly as a n energy source resulting in ATP formation within guard cells via
pliotuphusplrorylatirJir, or as a stiniulus as in the case of the blue light effects which cause guard cell
H + extrusion. Light also acts indirectly on stomata by affecting photosynthesis which influences the
iuterccllular leaf CO, conccntration (Ci).Carbon dioxide concentrations in contact with the plasma
membranr of the guard cell or within the guard cell acts directly on cell processes responsible for
stornatal movements. The mcchanism by which CO, exerts its effect is not fully understood but, at
lrast in part, i t is concerned with changing the properties of guard rell plasma membranes which
influcncc ion transport processes. 'l'he C, may remain fairly constant for much of the day for many
spccics which is the rrsult of parallel responscs of stomata and photosynthesis to light. Leaf water
potential also influences stornatal behaviour. Since leaf water potential is a resultant of water
uptake and storage by thr plant and transpirational water loss, any factor which affccts these
processes, such as soil water availability, temperature, atmospheric humidity and air movement,
may indirertly affect stomata. Some of these hctors, such as temperature and possibly humidity,
may allect stomata directly. 'these direct and indirect effects of environmental factors interact to
give a net opening response upon which is superimposed a direct effect of stornatal circadian
rhytliniic activity.
KEY WORDS: - C O Y . environmental sensing - guard cells
and quantity stomata.
-
Icaf water potentials . light quality
-
CON'I'ENTS
. . . . .
Introduction .
Light quality and quantity.
. .
Carbon dioxide concentration .
.
Leaf water potential .
. . .
Atmospheric pollutants
. . .
Mineral nutrition .
. . . .
Circadian rhythmic activity
. .
Interaction of environmental factors in
. . . . . .
References
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the control of stomata
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205
207
208
210
213
214
214
215
216
1NTROI)UC'TION
When plants left their aquatic environment and invaded land they
encountered a number of problems one of which was how to conserve water and
another was how to facilitate efficient transport of gases between the
0024-4066/88/070205
+ 13 $03.00/0
205
(01988 T h e Idinncan Society of London
206
C M WlLLMbR
environment and the innermost parts of the plant. Partly in efforts to solve these
problems, plants developed, at about the same time, a vascular system, a cuticle
and stomata. Such developments probably occurred about 390 million years ago
in the Lower Devonian period.
The first person to publish details on stomata was Malpighi in 1674. Soon
afterwards, Nehemiah Grew presented a series of lectures on plant anatomy,
including details on stomata, to the Royal Society in 1680 when Sir Isaac
Newton was the president. In 1682 his lectures were published (Grew, 1682).
Plant scientists have been fascinated by the subject ever since.
Stomata are situated in the leaf surface where they are best positioned to
control the influx and efflux of gases between the interior of a leaf arid its
environment. Furthermore, guard cells are usually only connected to
neighbouring cells via their dorsal walls, and, at maturity, these walls are
considered not to possess functional plasmodesmata (Willmer & Sexton, 1979).
Thus, because of their relative isolation from the rest of the plant body, stomata
seem ideally suited for sensing environmental factors. T h e classical view,
therefore, is that stomata control, to a large extent, photosynthesis and
transpiration. In recent times, however, a view has emerged that photosynthesis
and transpiration themselves control stomatal movements. This view is
reinforced when it is appreciated that stomatal apertures are affected by several
fhctors which are in part a result of photosynthesis and transpiration. For
example, stomatal aperture is affected by internal leaf CO, levels which are a
function of photosynthetic rates.
Therefore, in reviewing the effects of environmental factors on stomata1
behaviour, I will also address myself to the question of to what extent stomata
control rates of photosynthesis and trampiration or to what extent stomata
themselvcs are controlled by these processes. In order to do this, I will compare
the cffects of certain of the environmental factors on stomatal behaviour in
epidermal strips and in intact leaves. The direct effects on stomata can be
ascertained using epidermal strips because thc influence of the Photosynthetic
tissues will be absent. Also, since the epidermal tissue is incubated in a dilutc
buffered medium containing KC1, the water relations of the tissue are kept
constant. With intact leaves the resultant stomatal apertures are due to direct
and indirect effects. Unfortunately, the component of the indirect effect cannot
be obtained by subtracting stomatal apertures in epidermal strips (the direct
effects) from apertures achieved in intact leaves (indirect direct effects)
because the epidermal-strip system is adjusted to optimiLe stomatal aprrture.
Nevertheless, a good impression of the degree of importance of the two sy\tems
in controlling stomata should be realized. Also, wherever possiblc, cornparisoris
will be madc between stomatal behaviour in epidermal strips and intact leavcs
of Cummelina cummuniJ L., because more is known about the use of epidcrmal
strips of this species than possibly any other.
Stomata1 behaviour can be influenced by the following factors; light
quantity and quality, CO, concentration, temperature, atmospheric water
vapour pressure deficit (VPD) or humidity, soil water availability, wind,
mineral nutrition, and atmospheric pollutants. These factors tend to interact so
that stomatal aperture is a resultant of all these factors. Superimposed on the
interaction of these environmental effects are movements brought about by
circadian rhythms.
+
S'IOMATAL SENSING OF THE ENVIRONMEN'I
207
1,IGH'I QIJALITY AND QUANTITY
I n epidermal strips of C. communis maximum stomatal apertures are achieved
at a photon flux density of less than 100 pmol m - * s - ' in COX-freeair or
normal air (Fig. 1 ) . In whole leaves of C. communis, however, maximum stomatal
aperture is obtained at levels approaching 1000 pmol m-' s - ' in normal air
(Fig. 1). It is immediately apparent, therefore, that photon flux density has
direct and indirect effects on stomata, and that in intact leaves the latter effects
are generated via photosynthetic activities of the mcsophyll.
Light quality also has interesting direct effects on stomata. At equal energy
levels light of different wavelengths promotes stornatal opening in epidermal
strips of C. communis in the following order of effectiveness: blue > red > green
(Fig. 2). White light of equivalent energy level to blue light promotes even
wider openings (Fig. 2), suggesting there is some interaction between the
different wavelengths of light.
These direct effects of light can even be observed with guard cell protoplasts
(GCP) of C. communis. I n high energy red light G C P alkalinize the medium in
which they are suspended, probably as a result of CO, fixation. (Calvin cycle
activity is very low or non-existent while phosphoenolpyruvate carboxylase
activity is high in the guard cells of C. communis. However, in wide band red
light ATP will be synthesized via cyclic and noncyclic photophosphorylation
which occurs in guard cell chloroplasts.) If a pulse of low energy blue light is
superimposed on the red light the suspending medium acidifies (Fig. 3 ) . Besides
stimulating H + extrusion by GCP, blue light also causes them to swell with
concomitant K + uptake, a situation analogous to stornatal opening. Thus light
acts directly on guard cells and sets in motion processes which result in stornatal
movements. However, we do not know what the blue light absorbing pigment
is.
W
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O u o n i u m flux d e n s i t y : 4 0 0 - 7 0 0 n m ( p m o l m-'s")
E'igurc 1. Thc t-frcrts ofquantum flux dcnsity on stornatal opening in epidermal strips ( 0 ,0)
(data
from 'I'ravis & Mansfield, 1981) and leaves (A)(data adapted from Morison & Jarvis, 1983) o f
Commelina communis. 0 and 0 , stornatal opcning in CO,-free air and normal air (325 ppm CO )
rcspcctively, in epidermis incubated in 10 mol m - 3 MES buffer, p H 6.15, containing 50 mol m2'
KCl at 25°C. Apertures wcre mcasured aftcr 3 h incubation. Measurements were made with leaves
at 20"C, 320 ppm CO, and a leaf to air water vapour pressure differenre of 0.33 kPa.
C. M. WILLMEK
208
-E
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200
Quantum flux density ( p m o l m"s-'
)
Figure 2. EfTcct of red (A),
blue (O),
green (A)
and white ( 0 )light a t diffcrrnt energy levels, and
darkness 011 stomatal o ening in cpidermal strips of Commelina communis. T h e epidermis was
iriruhated in 50 mol "I-' MES buffer, pH 6.15, containing 50 mol m-'i KCI at 25°C; with C 0 , free air bubbling through the medium. Apcrtures were measurrd aftcr 3 h incubation. Data
adapted from Pemadasa (1982).
CARBON DIOXIDE CONCEN'I'RAllON
Changing CO, concentrations also affect stomatal movements, although the
stomata of some species, such as Pinus sylvestris, appear relatively insensitive to
CO, (Morison & Jarvis, 1981). However, atmospheric C O , levels change
little-though
high CO, levels can build up during the night period due to
respiration within dense canopies; this rapidly equilibrates with the bulk-air
CO, levels during early morning. Nevertheless, C O , levels within the leaf airspaces (the intercellular CO, concentration, Ci) do change: Ci values incrcase in
the late afternoon and during the night and decrease during the early morning.
iL
Blue
x
10 min
Figure 3 . Changes of pH of a medium containing guard cell protoplasts of Commelznn communis. In
red light (800 pmol m -' s - I ) the medium alkalinizes before the pH stahilizrs; when a pulsc ( 1 min)
of blue light (50 pmol m - ' s - ' ) is superimposed on thc red light the medium acidifies and then
stabilizes. A second pulse of blue light triggers off another period of acidification of the medium.
(Unpublished data of O m a r Pantoja, Stirling University.)
S'I'OMATAL SENSING OF THE ENVIRONMENT
209
Additionally, in those species which exhibit mid-day closure, Ci values will
change at this time. In CAM plants, also, Ci values vary greatly over 24 h.
However, for most species examined so far, and under most conditions, Ci is kept
well below ambient CO, levels and fairly constant for much of the day (see
Farquhar, Dubbe & Raschke, 1978). T h e relative constancy of Ci is considered
by some investigators to be a consequence of a control system linking
photosynthesis and transpiration to stomatal movements, which ensures that the
maximum amount of CO, is fixed per unit of water transpired (Cowan &
Farquhar, 1977).
Figurc 4 shows that stomata are sensitive to the CO, concentrations by which
they are surrounded. In epidermal strips of C. communis a linear relationship
exists between stomatal aperture and CO, concentration (in the range
0 360 ppm), with increasing apertures as CO, levels decrease. Little is known
about how the guard cells sense the differing C O , concentrations and what the
primary process is which triggers off stomatal opening or closing. However, it is
the plasma membrane and/or thc interior of the guard cell which senses the
changing CO, concentration. In support of the view that the plasma membrane
is a site which senses the C O concentration is the observation that guard cell
membrane permeability to K' increases in C0,-free air (Pantoja, unpublished
data, Stirling University); Edwards & Bowling (1985) also found that high CO,
concentration depolarized guard cell membrane potentials.
I n intact leaves of most species examined, in normal air of about 340 ppm
CO,, Ci is usually maintained at between 200 and 230 ppm CO,, although in
C. communis Morisori & Jarvis (1983) obtained Ci values considerably higher, at
about 290 ppm CO,. However, if Ci is artificially changed then at different light
levels a series of curves are obtained relating stomatal conductance to Ci
(Fig. 5). At the higher light levels stomatal conductance remains steady until Ci
values near to ambient CO, levels are reached and then the stomata begin to
0
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50
100
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200
250
300
350
COZ concentration ( p p m )
Figurc 4. L f r c t of CO, roncxntration on stomatal opening i n epidermal strips of Commelzna
rfJm~nunis.
Epidermis was incubatrd in 10 mol ITl-'' MES huii'er, pH 6.5, containing 'LO mol m - '
KC:I at 26°C and a quantum flux density of 170 pno1 ni-'
Air containing the difkvrcnt CO,
coiiceii~ra[ionswas buhhlrd through the mrdinm at a ratr of 100 ctn" m i n - ' and aprrturrs werc
measured after 2 h incubation.
sC'.
C. M. WILLMEK
210
0.0
L-L-
I00
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200
300
400
500
lntercellulor C o p concentrotion
C, (ppm)
Figure 5. E f k t of intercellular CO, concentration (Ci) on stomatal ronductanrr in Cumneliiin
communis leaves at different photon flux densities of 950 ( O ) ,490 (A),
240 ( A )and 130 ( 0 )p n o l
m-z
s - l . The dashed line intersects the curves at Ci values equivalent to an ambient CO,
concentration of 320 pprn CO,. Leaf to air vapour pressure difference of 0.33 kPa was maintained
at a leaf temperature of 20°C. From Morison & Jarvis (1983).
close. At lower light levels stomata respond to all Ci values, closing as Ci
increases. The broken line intersects the curves at Ci values that would be
obtained in normal air of about 320 pprn CO, at the various light levels. It is
evident that Ci values are remaining fairly constant for all light levels except the
lowest one. The crucial question is what controls Ci. One view is that
photosynthetic activity of the mesophyll essentially controls Ci which, in turn,
regulates stomata. However, as already indicated, stomata are directly affected
by light and therefore the alternative view is that there are parallel responses of
photosynthesis and stomata to light which, together, result in a constant Ci (see
Morison & Jarvis, 1983).
It must also be acknowledged that this complex situation involving direct and
indirect effects of light and CO, and the interaction between the two factors in
controlling stomata was appreciated, if not quite understood in the detail we
know today, some decades back by Heath and his co-workers (see Heath, 1948;
Heath & Russell, 1954). Unfortunately, this literature seems to have been
overlooked by many modern investigators.
LEAF WAYEK POTENTIAL
Tissue water potential has an important influence on stomatal behaviour also.
Bulk leaf water potential is the resultant of water uptake and storage by the
plant and water loss from the plant via transpiration. Therefore, any factor
which affects these processes such as soil water availability, temperature,
humidity of the atmosphere and wind will tend to perturb leaf water potentials.
Figure 6 shows the relationship of leaf water potential against stomatal
STOMATAL SENSING O F THE ENVIRONMENT
21 I
4
Leaf water potential (MPa)
Figure 6. The effect of changing leaf water potential on stomatal conductance in a number of
species (. . . . ., Sorghum; ---, maize;
, tobacco; - . .-, Phaseolus bean). Leaves were
irradiated at levels greater than 0.6 cal c m - * s - ' . Data from Davies el al (19811, adapted from
Turner (1974).
~
conductance for a number of plant species. Although there are species
differences in stomatal sensitivity to water stress (the C, species are usually less
sensitive), generally stomata begin to close only after a certain level of leaf water
potential has been reached and then close rapidly as the potentials continue to
decrease. (This relationship between bulk leaf water potential and stomatal
conductance is not always observed and in these cases epidermal tissue water
potential may be more closely related to conductance--see Meidner, 1983.) T h e
closing will be the result of a mixture of hydropassive and hydroactive effects.
Hydropassive effects are those that do not involve metabolic activities of the
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Leaf water potential (MPa)
Figure 7. The effect of leaf water potential on absrisic acid levels in excised wheat leaves. From
Wright (1977).
212
C M WILLMEK
guard cells but result from the availability of tissue water to change the turgor
relations of the stomatal complexes. Hydroactive effects are those that influence
stomatal movements via metabolic processes of the guard cells and may occur in
the following manner. A fall in leaf water potential triggers abscisic acid (ABA)
synthesis (more precisely, it is the fall in leaf turgor, closely related to water
& Raschke, 1980) in the
potential, which activates ABA synthesis-Pierce
manner typically described in Fig. 7. Although there is still some controversy, it
appears that ABA synthesis occurs primarily in the cytoplasm of mesophyll cells
(though a little ABA may be synthesized in the guard cells--see Cornish &
Zeevart, 1986) and it is then transportcd apoplastically or symplastically to thc
guard cells where it eff'ects ion transport processes at the plasma membrane to
bring about closure or prevent opening. Figure 8 shows thc potent inhibitory
effects of ABA on stomatal opening in epidermal strips of C. communis. When
ABA is applied to leaves either as a foliar spray or via the transpiration stream,
stomatal opening is also inhibited and closure brought about. These effects must
be considered as indirect ones since ABA is synthesized in the mesophyll as a
result of the fall in turgor potential of the cells. Besides water stress, chilling and
salt stress are known to stimulate ABA synthesis and affect stomata. However,
these stress conditions may act in a common way by decreasing cell turgor
which will result in ABA synthesis. It has also been suggested that low soil water
potentials initiate synthesis of compounds, including possibly ABA, in the roots
which are transported to the leaves where they influence stomatal behaviour.
Altcrnatively, Blackman & Davies (1985) have suggcsted that soil water stress
inhibits synthesis of kinetins in the roots which would normally be transported
to leaves to influence stomata. This emphasizes the point that control ofstomata
is not influenced just from an input of 'messages' to the guard cells from
processes occurring in the leaves but from 'messages' from all parts of the plant.
Other plant hormones influence stomata (we Willmer, 1983a), and there may
also be an interaction between the different hormones present within the
vicinity of'the guard cells, resulting in a particular stomatal behaviour. As well
as environmental factors determining, to some extent, the levels and mixturrs of
Controi-I0
-9
-8
-7
-6
-5
-4
A B A (log,,M)
Figure 8. 'l'he rfyect of abscisic acid in 10 mol niC3 sodium citrate buffer, pH 5.5, containing
10 mol m - ' KCI, on stomatal opening in epidermal strips of C ' o r n r n e h cornrnunir incubatcd at 30°C'
in light (500 W i n - 2 ) .Air was bubbled through the medium and apertures wrrr mcasurrd aficr 2 ti
incuhation. From Willmrr et nl. (1978).
SI‘OMATAL SENSING OF ‘IHE ENVIRONMENT
213
different hormones within leaves, the developmental changes within a plant can
also change their levels and complement. For example, the development of fruit
in some species is paralleled with wider stomatal openings and with changes in the
levels of ABA, cytokinins and gibberellins in leaves. Additionally, the previous
growth conditions of a plant can influence hormone levels in leaves which, in
turn, may affect stomatal behaviour.
Atmospheric humidity can also affect stomatal movements, essentially by
changing the water relations of leaves, just as soil water availability can affect
leaf water potentials. Figure 9 shows the effects of VPD on stomatal behaviour
in Viciafaba leaves. As the VPD increases (the air becomes drier) stomata close
until certain values of VPD are reached when no more closing occurs. Not all
species are affected by humidity changes in this manner, however.
I n general, humidity effects on stomata will be indirect since the water
vapour release into the atmosphere is from tissues other than the guard cells.
However, if water is lost directly from the guard cells as appears to be the case
in at least some species (e.g. P. .yhertris--Ng, 1978; also see Meidner, 1975),
then the humidity effects can be considered direct ones: under such
circumstances the water potential of the guard cells will be directly affected and,
in turn, this could influence cell metabolism related to the control of stomatal
movements.
ATMOSPHERIC POI,I,1JTANTS
Atmospheric pollutants can also affect stomata in a variety of ways (see
Unsworth & Black, 1981). Figure 9 shows the effects of SO, on stomatal
behaviour in V . f a b a leaves as a function of VPD: 35 ppb SO, in the atmosphere
results in wider conductances than in control leaves except at higher VPD
0.9
-
=\
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Y)
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0.7 -
4
0)
U
C
0
c
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3
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0.5-
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E
+
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0.3
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-
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1.2
I .4
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1.6
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1.8
Vopour pressure deficit
Figure 9. The effcct of water vapour pressure dcficit on stomatal conductancr in Vicia Jaba plants
exposed to charr-oal-filtcrcd air (0)
or air containing 35 ppb SO,
From Unsworth 6t B h c k
(a).
( 198 1).
214
C M WILLMER
values when a sudden drop in conductance occurs. Depending on the particular
pollutant, the mixes of pollutants and their concentrations, on the prevailing
environmental conditions and on the species, stomata may respond in a variety
of ways. The resultant stomata aperture may be due to direct effects of the
pollutants on guard cells but the indirect effects are likely to be more dominant
due to effects of pollutants on photosynthetic processes of the mesophyll and the
water relations of the leaf.
h I I N E R 4 L NUTRI'I ION
;n general, anything that aficcts photosynthesis or leaf water potentials will
indirectly affect stornatal responses to some degree. 'Thus, if a mineral deficimcy
lowers the photosynthetic capacity of a leaf then stomata will tend to close to
keep Ci constant. Hence, as Fig. 10 shows, when plants are grown deficient in N
or P, stornatal conductances are lower than in control plants grown sufficient in
the minerals at all levels of leaf water potential (cxcept at the higher values in
the P treatment). I t is also possible, of course, that the metabolism of guard cells
themselves is directly affected by mineral deficiency. Indeed, since K is the
major osmoticum accumulated by guard cells during stomatal opening then it is
most likely that there will be a direct effect of K deficiency on stornatal
functioning.
CIRCADIAN RHYI'HMIC ACTI\'I'I'Y
Another factor which is primed by the environment and which afrects
stomatal behaviour is the circadian rhythm of stomata (scc Martin & Mcidner,
1971). If a plant is maintained in continuous light after being grown in a fixed
day/night cycle stomata will partly close during what would have been the dark
Leaf water potential (bars)
Figure 10. The effect of nitrogrn (A) or phosphorous (B) deficiency in cotton plants on lcal
conductance (normally rquivalent to stornatal rondurtancr) at diffcrcnt lraf' watrr potentials. 0 ,
Phosphorous and nitrogen deficient plants; 0,
phosphorous and nitroxen suficicnt plants. From
Radin (1984) and Radin, Parker Rr Guinn (1982).
S'L'OMA'TAL SENSING OF THE ENVIKONMEN'I'
215
period and open wider during the light period. T h e amplitude of this freerunning rhythm decreases with time and will cventually 'damp' out. T h e
stomata1 rhythm can be phase shifted by exposing plants to periods of darkness
at various stages of the cycle and a complete inversion of the original patterns
can be obtained. I n complete darkness the rhythm is less apparent and only one
to two cycles may occur, Little is known about the 'clock' that controls the
rhythm, but such rhythms are observed in epidermal strips and the 'clock'
probably resides in the guard cells. This is a direct effect on guard cells.
IN'I ERACTIONS OF THE ENVlKONMENTAL FAC 1 ORS I N 7 HE C O N T R O L OF 5 1 OMATA
Figure 11 summarizes the ways in which the different environmental factors
interact to produce their effects on stomata. Two feedback (loops', one involving
CO, and the other involving tissue water potentials, indirectly affect stomata.
Taking the CO, 'loop' first, CO, enters the leaf via stomata where it is
assimilated in the mesophyll ( A ) , The internal CO, concentration, Ci, is a
resultant mainly of photosynthetic activity of the mesophyll cells (indirect
effects) but also of guard cell CO, metabolism (direct effects). Guard cells have
a high respiration rate relative to mesophyll cells (about x 7 higher on a protein
basis-Fitzsimons & Weyers, 1983) and also the ability to fix considerable
amounts of CO, via phophoenolpyruvate carboxylase activity (Willmer, 1983b)
and therefore have the potential for affecting CO, concentrations at the surface
Water supply
Temperature
Humidity
Wind
Light
(INDIRECT EFFECTS)
Light
Temperature
Mineral nutrition
Pollutants
(INDIRECT EFFECTS)
Figure 11. Direct arid indirect effects of environmental [actors, and their interactions, on stomata.
A = Photosynthetic assimilation of CO, by mesophyll cells; Ci = intercellular space C O ,
conrentration; "tissue and Y M =
C leaf water potential and guard cell water potential, rcspectively.
216
C M WILLMOR
or inside guard cells. Light indirectly affects stomata via mesophyll
photosynthesis: if photon flux density increases, C, will decrease and therefore, in
attempts to keep C, constant, the ‘message’ to the guard cells will be for them to
open more; conversely, if photon flux density decreases, Ci will tend to increase
and the message will be for the stomata to close to some extent. Temperature,
mineral nutrition and pollutants can all affect photosynthetic activity and,
therefore, stomata will respond in a way to maintain constant C,.
Turning to the water potential ‘loop’, leaf water potential is a resultant of the
amount of water lost and the availability of water from the other tissues and the
soil. If the leaf water potential falls due to excessive transpiration this situation
will be transmitted to the guard cells via physical (hydropassive) and/or
chemical (hydroactive) processes. If the stomatal responses are hydropassive
they will normally ultimately close when leaf water potentials fall and begin to
open a\ the potentials rise. With hydroactive stomatal responses, ABA will be
synthesized in the mesophyll as water potentials fall and, upon reaching the
guard cells, ABA will bring about closure. As the water stress is relieved, ABA
levels in or at the surface of guard cells will fall and stomata will begin to open
again. VPD, temperature, wind and light (which tends to increase leaf
temperatures) will all affect stomatal aperture due to their influence on
tran5piration which in turn will affect leaf water potentials.
Leaf water potentials can also affect the CO, ‘loop’ since water stress is known
to inhibit photochemical and enzymatic processes of photosynthesis (Keck
& Boyer, 1974; soyer, 1976). Stomata will, therefore, close to maintain a
constant C,.
Light, temperature arid circadian rhythmic activity all can effect stomatal
metabolism directly leading to changes in stomatal aperture. Carbon dioxide
levels generated by the guard cells may also have some influence on stomatal
apertures. In CAM plants, a circadian rhythm of CO, production by the
mesophyll is considered to be a dominant factor controlling stomata. This is an
indirect effect of circadian rhythms on stomata.
’The indirect effects and the direct effects are equivalent to the closed,
negative and positive feedback ‘loops’ and to the open, feedforward ‘loops’,
respectively, terminology used by some of the more recent investigators (see
Raschke, 1975; Cowan, 1977).
In conclusion, it is apparent that there are direct and indirect environmental
effects on stomata but it is not possible to determine what proportion of the
driving force for stomatal opening comes from each of the two systems. Light
has direct and indirect effects which are superimposed on the stomatal response.
The indirect effects are via photosynthesis, which influences Ci; the direct effects
may be particularly important for triggering off stomatal opening and may
dominate in the early morning and late afternoon and in plants growing in
shade environments. Carbon dioxide affects stomatal processes directly, and it is
believed that C, is dominantly controlled by photosynthetic activity of the
mesophyll rather than by guard cell metabolism.
REFERENCES
HLACKMAN, 1’. G. & DAVIES, W. J., 1985. Root to shoot communication in maize plants of thc cffccts of
soil drying. Joiirnnl qf ExfJerirncntal Bofanv, 36: 39-48.
STOMATAL SENSING OF 1'HE ENVIRONMEN'I'
217
SOYLK, J . S., 1976. Photosynthesis a t low water potentials. IJhilosophical Transactions of the Royal Sociely o/
London, Series B, 273: 50 1--5
1 2.
CORNISH, K. & ZEEVAR'I', J . A. D., 1986. Abscisic acid accumulation by in ~ i t uand isolated guard ct4ls of
Pisum satiuum L. and Vzczafaha I,. in relation to watrr stress. Plant Physiology, 81: 1017-1021.
COWAN, I. R., 1977. Stornatal lieliaviour and environment. Advances in Botanical ReJearch, 190: 117-228.
COWAN, 1. R. & PARQUHAR, G . D., 1977. Stornatal function in relation to leaf metabolism and
environment. In Integralion cf Arlivity in thP Higher Plant. Soriety ,for Experimental Biology Symposium, 31:
471-505.
DAVIES, \V. J., WILSON, J. A,, SHARP, R. E. & OSONUBI, O., 1981. Control of stornatal behaviour in
water-stressed plants. I n P. G. Jarvis & T. A. Mansfield (Eds), Stornatal Physiology: 166. Cambridge:
Cambridgr Univc-rsity Press.
EDlVARDS, A. & ROWI,ING, I). J. F., 1985. Evidence for a CO, inhibited proton extrusion pump in the
stornatal cells of Tradesrantin virginiana. Journal of Experimental Botany, .?6: 91-98.
FARQC'HAR, G. D., DUBBE, D. R . & KASCHKE, K., 1978. Gain of thc feedback loop involving carbon
dioxidc and stomata: theory and measiirement. Plant P/ysinloLv,
62: 406-412.
FI'IZSIMONS, P. J. & W'EYERS, J. D. B., 1983. Separation and purification of protoplast types from
Commelinci communis L. leaf epidermis. Journal of Experimental Bulay, 34: 55--66.
GKELY, N., 1682. Anatomy qf Plants. London.
HEA'I'H, 0. V. S., 1948. Control ofstomatal movcmciits by a reduction in the normal carbon dioxidr content
of the air. .Nature, London, Z61; 179-181.
, J., 1954. Studies on stornatal behaviour. VI. An investigation of the light
with the attempted elimination of control by the mesophyll. Part 11.
Intrractions with external carbon dioxidc, and general discussion. Journal uf Experimental Botag, 5:
269-292.
KECK, K. W. & BOYER, ,J. S., 1974. Chloroplast response to low leaf water potentials. 111. Differing
inhibition of electron transport arid photophosphorylation. Plant Phyhlogy, 53: 474-479.
MAK'I'IN, E. S. & MEIDNER, M., 197 1. Endogenous stomatal movements in Trade~cantinuirginiana. N r 7 ~
Phyfolo$, 70: 923-928.
MEIDNER, H., 1975. Water supply, evaporation and vapour diffusion i n leavcs. Journal of Experimental
Botany, 26: 666-673.
MEIDNER, H., 1983. Our understanding of plant water relations. @rnal of Experimental Botany, 34:
1606-1618.
MORISON, J. I. L. & JARVIS, P. G., 1981. The control of transpiration and photosynthrsis by the stomata.
In P. G. Jarvis & 'I'. A. Mansfield (Eds), .Stornatal Physi~lo~v.
Cambridge: Camhridgc IJniversity Press.
MORISON, J. I. L. & JARVIS, P. G., 1983. Direct and indirect effects of light on stomata. 11. In Commelina
conimunz.r L. Plant, Cell and Environment, 6: 103--109.
NG, P. A. P., 1978, 'Response of stomata to environmental variables in Pinus syluestriJ L.' Uripublishcd Ph.D.
thesis, University of Edinburgh.
I'EMADASA, M. A,, 1982. Abaxial and adaxial stornatal responses to light of different wavclcngths and to
phcnylacetic acid on isolated epidermis of Commelina communis L. 3ournal of Experimental Botany, .?.?: 92-99.
PIERCE, M . & RASCHKE, K., 1980. Correlation betwrcn loss of turgor and accumulation of abscisic acid in
dctachcd leaves. Planla, 148: 174-182.
RAUIN, J . IV., 1984. Stornatal responses to watcr stress and to abscisic acid in phosphorus-dr~cientcotton
plants. Plant Plyszology, 76: 392-394.
KAI)IN, J. W.,PAKKEK, L. L. & G L I N N , G., 1982. Water relations of cotton plants under rlitrogen
deficiency. V. Environmental control of abscisic. acid accumulation and stornatal sensitivity to abscisic
acid. Plant Physiology, 70: 1066-1070.
RASCHKE, K., 1975. Stomata1 action. Annual Reuirw of Plant PhyJiology, 26: 309-340.
'I'RAVIS, A. J. & MANSFIELD, '1'. A,, 1981. Light saturation of stomatal opening on the adaxial and
abaxial epidermis of Cummelina communis.Journal of Experimental Botalzy, 3: 1169-1 179.
T U R N E R , N. C., 1974. Stornatal respoiisrs to light and water under field conditions. In R . Bieleski (Ed.),
,I.lechani.smc qfKe,qulation of Plant ( h w l h , Bulletin 12. 423-432. Royal Society of New Zealand.
UNSW'ORTH, M. H. & BLACK, V. J., 1981. Stomatal responses to pollutants. In 1'. G . Jarvis & 1'.A.
Mansfield (Eds), Slurnatal Physzolo,~:191. Cambridge: Cambridge University Press.
WILLMER, C. M., 1983a. Stomata. 1,ondon: Longman.
WILLMER, C. M., 1983h. l'hosphornolpyruvatc carhoxylasr activity arid stornatal opcration. Physzologie
vigltale, 21: 943--953.
WILLMER, C:. M., DON, R. PAKKEK, W.,1978. Levels of short-chain fatty acids and of abscisic acid in
watcr-stressed and non-str
d lcavcs and their r l k c t s 011 stomata in epidermal strips and cxcisrd leaves.
Planta, 13.9: 281-287.
\YII,I.MER, C. M . & SEXTON, K., 1979. Stomata and plasmodesmata. Protoplasma, 100: 113-129.
WRIGHL', S. '1'. C., 1977. Ttir relationship tic-tween leaf watcr potential (Yleaq and the level of ah
and ethylene in rxciscd whcat leaves. Planta, 134: 183-189.