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IRWIN P. T l N G A N D ROBERT L. HEATH
Stomata1 governing of gaseous uptake can be evaluated using the gas
transfer equations of Penman and Schofield ( 195 1 ) . Simply, the expression
+ R , 4- Rm)
will describe ozone uptake, where Q = ozone uptake in nig cm-2 sec-l;
D = diffusion coefficient for ozone in mg ~ m mbar-l;
Av = ozone pressure
difference between source (atmosphere) and sink (reacting) surface of tissue
in millibars; R, = boundary layer resistance in sec cm-'; R , = leaf or stomatal resistance in sec cm-'; R , = residual resistance to ozone transfer beyond
Ra and R,, also in sec cm-l.
An additional resistance, R,., defined as the resistance to gas transfer
of the nonstomatal surface of the leaf, can usually be ignored since for
water vapor and CO, its value is quite high and constant. We know little
about the R,. for ozone, but Rich et al. (1970) estimated it at 19 sec cm-l
for bean plants. D,the diffusion coefficient for ozone in air is not known,
but would be an exponential function of temperature.
The rate of ozone uptake, therefore, can be increased by a variety of
means including ( a ) temperature increases that directly affect D, ( b )
increases in the amount of ozone in the atmosphere, which would increase
Av, or (c) reductions in any of the resistances, R.
The boundary layer resistance, R,, is a partial function of air movement
as well as the surface characteristics of the leaf and leaf canopy. R,, is
usually in the range of 0.1 to 1.0 sec cm-' and in still air was estimated to
be 0.6 sec cm-' for ozone by Rich et al. (1970). Hill and Littlefield
(1969) reported a severalfold increase in the rate of ozone uptake by
oat leaves with air velocities increased from near 0 to 3.0 miles per hour.
The latter conditions probably operated to reduce R,.
R,, or the stomatal resistance, is most important for our discussion since
it is the variable resistance by which gas transfer is regulated. The study by
Rich et al. (1970) strongly suggests that R , is the major resistance regulating ozone uptake by leaves since resistances for water loss and ozone
uptake are nearly the same. Furthermore, Lee (1965) constructed a curve
showing the expected ozone injury response as a function of stomatal
opening in sensitive bean tissue. This curve is exactly predicted from the
gas transfer equation. At low stomatal apertures, and hence high R,, R ,
becomes the limiting resistance and a near-linear response to gas uptake
and stomatal aperture is seen. At wider stomatal apertures and consequent
lower R , values, other resistances (i.e., the constant R, and Rm)predominate, and further increases in stomatal aperture have minimal effects. This
is why only small correlations may exist between stomatal aperture and
RESPONSES OF PLANTS TO AIR POLLUTANT OXIDANTS
expected responses, such as ozone injury. It is only for low stomatal apertures that R, exerts significant control over gas transfer.
It would be difficult to evaluate R,, without knowing the site or sites of
ozone injury. If the target site was the limiting membrane of the cell, R ,
would be small and probably inconsequential. If, however, other important
sites exist, perhaps, for example, the chloroplast membranes, then R,
could be significant.
BETWEEN INJURYAND R ,
1 . Condition of Stomata
Heggestad and Middleton (1959) demonstrated the importance of R,
in governing the extent of ozone injury in susceptible tissue. The adaxial
leaf surface resistance (R,) of pinto bean leaves is near€y 50% greater than
the abaxial surface. If the adaxial surface of a susceptible leaf is coated
with petroleum jelly, then injury develops as in a control. If, however,
the abaxial surface or both surfaces are coated, ozone injury is prevented
(Evans and Ting, 1974a).
Dean (1972) determined the size and density of adaxial stomata from
two resistant and four susceptible tobacco varieties and found a reduced
stomatal density in the resistant varieties but no difference in stomate size.
2. Water Status, Humidity, and R ,
Water-stressed plants are less prone to ozone injury than those kept on
a favorable moisture regime (Heck, 1968). Seidman et al. (1965) observed that if water was withheld from petunia, bean, and tobacco plants,
fumigation with auto exhaust was not injurious. The artificial drought conditions were correlated with increased leaf resistance to gas transfer. Leone
and Brennan (1969) exposed begonia to high relative humidity and noted
enhanced injury by ozone which they correlated with decreased R,. Otto
and Daines ( 1969) positively correlated leaf permeability index (reciprocally related to R,) determined with a porometer, relative humidity, and
ozone injury, to pinto bean and tobacco leaf. The authors concluded that
humidity affected stomatal aperture.
There is yet a large body of evidence to suggest that favorable water
status predisposes plants to ozone injury beyond just stomatal effects
(Heck, 1968). For example, Turner et al. ( 1972) compared four cultivars
of tobacco, which differed markedly in sensitivity to ozone, with respect
to stomatal conductance, the reciprocal of R,. There appeared to be no
significant differences in R, among these cultivars to warrant the conclusion
IRWIN P . TlNG AND ROBERT L. HEATH
that stomates accounted for the differing ozone sensitivities. However, in
a later study (Rich and Turner, 1972) comparing a sensitive tobacco strain
with a tolerant strain, stomatal resistance did appear to account for differential sensitivities. When kept in a dry atmosphere (37% relative humidity), ozonation for 120 minutes at 0.20-0.25 ppm resulted in an increased
R , for the resistant cultivar over the sensitive one (6.2 sec cm-l as compared to 3.5). Yet in a moist atmosphere (73% R H ) the difference between resistant and sensitive varieties was 4.2 and 5.6 sec cm-'. Hence
at high atmospheric moisture, these data do not necessarily support their
In another study (Ting and Dugger, 1971), water relations were
studied in the ozone-sensitive Be1 W-3 tobacco and the resistant cultivar,
Bel-B. When grown in pots, Bel-B had a significantly smaller root system
and lower leaf tissue water potentials. Concomitantly, in the light, R , was
greater for Bel-B than Be1 W-3.
In a study by Hill and Littlefield (1969), on a variety of plants including
oat, barley, wheat, tobacco, pinto bean, lima bean, chard, corn, cauliflower,
sugarbeet, potato, and tomato, ozone always decreased stomatal aperture.
Stomatal closure, estimated by fixing epidermal strips in alcohol followed
by microscopic observation, was correlated with a reduction in transpiration and net photosynthesis. Their experiments were conducted at 50%
relative humidity and 24°C.
Stomatal opening is a turgor response; positive turgor in guard cells relative to adjacent cells is necessary to bring about stomatal opening (Slatyer,
1967). Recently potassium was found to be necessary for stomatal opening, presumably by acting as an osmotic agent and/or counterion for
organic osmotic agents (Humble and Hsiao, 1970). Any substance that
interferes with water permeability, potassium transport or permeability, or
general leaf water relations, is apt to alter stomatal opening and R,. But because of the complex physical relationships between the guard cells and
adjacent cells, changes in water balance and/or membrane permeability
could result in either an increased or decreased R,.
In an early study, Dugger et al. (1962b) showed that pinto bean plants
exposed to 0.7 ppm of ozone for 30 minutes either showed no change
in leaf resistance or a slight decrease indicative of stomatal opening. In
our own study (Evans and Ting, 1974a), if pinto beans were exposed to
0.65 pprn of ozone, the adaxial leaf surface resistance did not change during a 90-minute fumigation period, but extended fumigation caused a reduced leaf resistance. The abaxial leaf resistance at 0.65 ppm of ozone
increased during the first few minutes, decreased, then increased up to 90
minutes. Exposure to 0.8 ppm caused a steady decrease in leaf resistance
RESPONSES O F PLANTS TO AIR POLLUTANT OXIDANTS
of the adaxial surface. The results of Evans and Ting’s study were obtained
with a leaf resistance hygrometer (van Bavel et al., 1965) and could reflect
changes in transpiration independent of R, changes. The same results were
obtained by Dugger et al. (1962b), however, using an air flow type of
porometer described by Heath and Russel ( 1951 ) .
From previous discussion then, it is evident that for significant foliar
ozone injury to occur, stomata must be open and R , must be low, and,
in general, plants subjected to water stress or plants with inherently poor
water balance will be more ozone tolerant. It is reasonable to conclude
that ozone alters stomatal opening by directly affecting water permeability,
potassium leakage (Evans and Ting, 1973), and potassium transport
(Evans and Ting, 1974b). The degree of stomatal opening is a function
of the osmotic properties of the guard cells as governed, at least in part,
by potassium movement (Humble and Hsiao, 1970).
As observed in the above section, providing the tissue is predisposed
to injury by virtue of age or other factors, then the R , value is closely
correlated with the degree of ozone injury. Frequently, however, plants
are not injured despite the fact that we must assume ozone has entered
In Fig. 3, it is shown that the R, of leaves during maximum ozone
susceptibility is not significantly different from the young and old resistant
periods. Since we must assume that the same quantity of ozone entered
the leaf at day 7 as at day 10, then factors other than stomatal aperture
are responsible for the lack of susceptibility, although a slight average increase in R, after day 12 could account for some of the reduced injury.
The convincing observation made by Dugger et al. (1962b) for pinto bean
leaves was that peroxyacetyl nitrate injury occurred in leaves younger than
those injured by ozone. Hence stomatal regulation of gas transfer could
not account for the differential susceptibility between PAN and ozone.
The early study by Glater et al. (1962) showed that only expanding
tobacco leaves were susceptible to ozone injury and that recently matured
cells were injured. They concluded that the injury potential was a function
of “cellular development and maturity.” Their study further showed that
in tobacco, stomata were nonfunctional in young, nonsusceptible leaves.
They concluded that heavy deposits of suberin protected older, nonsusceptible leaves from ozone injury. Tobacco seems to differ markedly from
bean in that there are functional stomata in bean prior to the age of susceptibility (Evans and Ting, 1974a).
IRWIN P. TING AND ROBERT L. HEATH
I . Genetic
Although there is much documentation for genetically determined oxidant resistance in plants, in few instances is there a sound physiological
or biochemical basis for the resistance. An exception, however, is the work
of Engle and Gabelman (1966), who isolated inbred onion cultivars resistant and sensitive to ozone. They observed that the sensitive inbred SW34
maintained open stomata after ozone exposure whereas stomata of the resistant inbred onion strain closed. They hypothesized that the guard cells
of the resistant plants became leaky after ozone exposure resulting in subsequent closure, after which tl.:y functioned again. Genetic crosses suggested
that resistance was controlled by a dominant genetic system, but it was
not ascertained whether resistance was a single gene trait.
It is now generally known that high CO, results in stomatal closure and
low CO, brings about opening. Hence, Heck and Dunning (1967) exposed
pinto bean and tobacco to 500 ppm of CO, excess and observed a reduced
injury to tobacco by ozone but no change in pinto bean injury. They did
not, however, measure R , responses to CO,.
Abscisic acid (ABA), presumably because of effects on membrane
permeability, tends to close stomata (Addicott and Lyons, 1969). In one
study stomata were closed with 10 ppm of ABA to protect 14-day-old
bean leaves against ozone (Fletcher et al., 1972). Four hours after ABA
treatment, plants were exposed to 0.2-0.4 pprn of O:, for one hour. Before
ozone, the water-treated controls had stomatal apertures of 10.7 pm whereas
the ABA-treated plants had apertures of 4.2 pm. After ozone, the controls
and treated leaves were 4.9 and 2.9 pm, respectively, and the ABA-treated
plants did not show visible injury. Though no R , estimates were made,
stomatal closure was probably sufficient to account for the observed
Certain other chemicals which reduce stomatal aperture such as phosphon D, 8-hydroxyguinoline sulfate, and phenylmercuric acetate tend to
protect against smog injury (Seidman et al., 1965). The feasibility of using
such compounds to prevent oxidant injury has not as yet been pursued
in depth, but may be a promising approach. Unfortunately, plant productivity also declines with these chemicals due to lack of CO,.
RESPONSES OF PLANTS TO AIR POLLUTANT OXIDANTS
In general, the oxidants ozone and peroxyacetyl nitrate cause a variety
of injury symptoms in plant tissues ranging from excessive water loss, impairment of photosynthetic activity, an imbalance of metabolites, a reduction in cell wall biosynthesis, and finally to cellular collapse and visible
necrosis. Visible injury always results in a reduction in growth and, in the
case of valuable crop plants, a reduction in yield and quality. Most of the
symptoms described above are probably of a secondary nature and do not
reflect the primary target sites.
It is our hypothesis that oxidants initially alter the selectivity of limiting
cellular membranes such that solutes and salts leak from or into organelles
and cells. The resulting imbalance of ionic potential anJ water balance
is manifested first by leakage of potassium from the cells followed osmotically by water. This initial loss of membrane differential permeability produces other biochemical effects which ultimately cause necrosis or cellular
collapse and death of the tissue. Just why these oxidants should alter membrane selectivity is not known for certain but could be related to the oxidation of the sulfhydryls or unsaturated fatty acids of the membranes.
Given our present economic and technological status, it is rather unlikely
that increasing air pollution will be little more than slowed in the near
future. In fact, there is no real attempt to eliminate pollution, but simply
to meet air quality standards of a tolerable level and ones that are acceptable with respect to human health alone. Although rather pessimistic, a
reasonable agricultural goal is to develop pollution-resistant crops that can
grow and maintain high yields under a variety of pollution conditions. We
emphasize that the only way to achieve this goal is by the cooperation
of physiologists and geneticists. Further work must be done to allow US
more fully to understand the biochemical and physiological basis of air
pollution injury. The hypothesis we present concerning oxidant alterations
of membrane permeability is merely a beginning. Future physiological and
biochemical information can and should be used by the geneticist in
thoughtful breeding programs.
Both authors wish to acknowledge a major indebtedness to W. M. Dugger, Jr.,
who began much of the work described here and who still is a major contributor
to the thrust of this research. Over the years in our laboratories a number of people
have contributed significantly to our understanding of the mechanism of oxidant
injury to plants; among them are: C. Coulsen, P. Chimiklis, L. E. Evans, P. Frederick, F. Fong, R. Gross, J. Koukel, S. Lackey, S. K. Mukerji, J . Perchorowicz,
IRWIN P. TING AND ROBERT L. HEATH
J. Vereen, and R. Sutton. We also thank our many colleagues including J. B. Mudd,
L. Ordin, R. Palmer, 0. C. Taylor, and W. W. Thomson for many helpful discussions.
Much of our own research was supported by Federal Grants from the following
agencies: NAPCA, USPHS, EPA, and USDA.
We especially thank Ms. Paula Frederick for her editorial efforts during the preparation of this manuscript.
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