Pugnaire F.I. Valladares F. Functional Plant Ecology

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600 Functional Plant Ecology

Resistance to Air Pollutants:

From Cell to Community

Jeremy Barnes, Alan Davison, Luis Balaguer,

and Esteban Manrique-Reol

CONTENTS

Introduction ....................................................................................................................... 601

Cellular Level ..................................................................................................................... 602

Uptake ............................................................................................................................ 603

Metabolism ..................................................................................................................... 607

Gene Expression ............................................................................................................. 609

Plant Level..........................................................................................................................610

Population Level ................................................................................................................ 613

Community Level............................................................................................................... 617

Conclusions ........................................................................................................................ 620

Acknowledgments .............................................................................................................. 620

References .......................................................................................................................... 621

The race is not to the swift, nor the battle to the strong . . . but time and chance happeneth

to them all.

—Ecclesiastes 9:11

INTRODUCTION

The generation of energy by the burning of fossil fuels, all manner of industrial processes, the

biodegradation of wastes, and some farming operations lead to the release of wide range of

contaminants into the air. Most have little or no discernible effect on the environment,

because the resulting concentrations in the atmosphere are well below levels known to be

toxic or because they are not toxic to biological systems. Others attain levels that are known

to threaten human health and to damage both fauna and flora. The situation is not new

because there have been air pollution problems of one kind or another since fire was first used

and metals were first smelted, but the unbridled expansion of industry in many parts of the

world over the past century has resulted in problems on an unprecedented scale, with impacts

extending from the local or regional to global level.

Although air pollution can take various forms (i.e., dusts, smoke, fumes, aerosols, or

mist), this chapter focuses on resistance and adaptation to the most common gaseous

pollutants. Stringent control measures have resulted in a steady decline in the emissions of

several pollutants in developed regions (e.g., sulfur dioxide [SO

]); however, ground-level

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601

concentrations of some of the most potent gases (e.g., ozone [O

]) continue to increase

(Penkett 1988, Boubel et al. 1994, Stockwell et al. 1997). Locally, ground-level concentrations

of some pollutants may be high enough to result in severe foliar injury under conditions

favoring accumulation in the atmosphere (i.e., periods of high solar radiation, favorable

temperatures, or temperature inversions), whereas potentially damaging concentrations of

others (e.g., O

) maybe generated at a considerable distance from the source (Bell 1984,

Boubel et al. 1994, Krupa 1996). Long distance transport is usually favored by the high levels

of irradiance and stable atmospheric conditions associated with slow-moving high-pressure

systems in the northern hemisphere. Under such conditions, there is poor dispersal of polluted

air masses, and pollutant concentrations, although typically lower than those experienced

near to point sources, may be high enough to result in subtle changes in plant physiology,

growth, and community composition. Such effects are not necessarily associated with the

appearance of typical visible symptoms of injury, but are more common and just as debili-

tating (Wolfenden and Mansfield 1991, Davison and Barnes 1992, 1998).

It would seem that all plants possess the encoded capability for the perception, signaling,

and response to air pollutants; however, differential expression under the influence of genetic

and environmental factors can result in constitutive and inducible differences between the

reaction norms of plants within and between populations to the same air pollution insult. In

this chapter, we discuss aspects related to the ecotoxicology of airborne pollutants. We begin by

reviewing what is known about the mechanisms underlying differential resistance to the most

common gaseous pollutants, and then attempt to scale-up from responses at the cellular level to

those affecting resistance at the plant, population, and community level. A generic model is

used to provide a conceptual framework within which to discuss the mechanisms underlying

differential resistance. Where appropriate, we have elected to focus on plant responses to O

Not only because the authors are more familiar with the literature relating to this pollutant

than any other, but also because O

is now recognized to be one of the most potent and

widespread toxic agents to which vegetation is exposed in the field (Davison and Barnes

1992, Ka

renlampi and Ska

rby 1996, Fuhrer et al. 1997, Davison and Barnes 1998). Moreover,

increasing concentrations of the pollutants pose a growing threat to vegetation in many regions

(Penkett 1988, Stockwell et al. 1997), and exciting advances have recently been made in our

understanding of the mechanisms underlying the genetic basis of resistance to O

(Kangasja

rvi

et al. 1994, Schraudner et al. 1994, Alscher et al. 1997, Pell et al. 1997, Schraudner et al. 1997).

CELLULAR LEVEL

The processes controlling differential resistance to pollutants are considered within the frame-

work of a conceptual model (Figure 20.1), discussed first by Ariens et al. (1976) and later by

Tingey et al. (Tingey and Taylor 1981, Hogsett et al. 1988, Tingey and Andersen 1991), where

resistance* is envisaged to be governed by constitutive and inducible differences in a complex

sequence of events that either reduces pollutant penetration to the target (i.e., avoidance

mechanisms) or enhances the ability of plant tissues to withstand the pollutant and its products

once it has penetrated to the target (i.e., tolerance mechanisms). However, various feedbacks

can also influence plant response, especially in relation to pollutant detoxification and the

repair of injury. These processes are initially dependent on the constitutive resources available,

whereas subsequent responses may be governed by the regulation of gene expression, post-

translational modification of enzymes (e.g., phosphorylation=dephosphorylation), and the

synthesis of secondary defense-related metabolites. If these responses are not sufficient

* Herein defined after Roose et al. (1982) as the ‘‘relative ability of a genotype to maintain normal growth and remain

free from injury in a polluted environment. A trait that is quantitative, rather than qualitative, as resistance need not

be complete.’’

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602 Functional Plant Ecology

to prevent damage at the cellular level, then there will be destabilization and injury that will be

reflected in downstream consequences at the level of the individual, population, and commu-

nity. The mechanisms conferring resistance may be independent (i.e., pollutant-specific) or

broadly based (i.e., a number of different pollutants trigger the same coordinated defense

reaction); broadly based responses can result in cross-resistance to several pollutants (and

possibly to a number of other environmental stresses), whereas there is growing evidence that

cross-tolerance may be restricted to pollutants (and other stresses) that provoke similar insult

on the same target (Schraudner et al. 1997, Barnes and Wellburn 1998).

UPTAKE

The dose of a pollutant absorbed by plant tissues plays a key role in determining effects on

metabolism and physiology, and in the description and quantification of dose–response

relationships (Taylor et al. 1998, Runeckles 1992). Uptake is predominantly controlled by

rates of foliar gas exchange, with conventional approaches focusing on the importance of the

cuticle and stomata in controlling the rate at which pollutants diffuse into individual

leaves (Mansfield and Freer-Smith 1984). However, it is important to recognize that factors

operating at different scales of resolution influence the rate of uptake, in addition to those

operating at the level of the individual leaf. At a higher scale of resolution (i.e., scaling-up),

Community

Population

Plant

Cell

Destabilization

Complete repair

Modification of gene expression

Detoxification

Ambient

exposure

Internal

exposure

Internal

interaction

New

metabolic

state

Target

exposure/

Reserve

capacity

Uptake Transport/

metabolism

FIGURE 20.1 Conceptual model showing the processes that govern the sensitivity of plants to gaseous

air pollutants. Pollutant levels that exceed the capacity of avoidance=tolerance mechanisms will result in

cellular destabilization—an effect that underpins changes in the performance of the individual and shifts

in the genetic composition of both populations and communities.

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Resistance to Air Pollutants: From Cell to Community 603

aerodynamic factors influence uptake at the canopy level, whereas at a finer scale of reso-

lution (i.e., scaling-down) physicochemical factors determine uptake at the interface between

the plant and its external surroundings (Figure 20.2).

The size, density, and shape of the canopy all have a pronounced effect on the concen-

tration of a pollutant to which individual leaves are exposed. Relatively few studies have

addressed this issue, but it has been shown that the concentration of O

(and other pollutants)

declines as one passes down through the canopy to soil level (Bennett and Hill 1973). As a

result, leaves within a dense canopy tend to be exposed to lower concentrations than those on

the surface or at the edges. However, because the air movement within a dense canopy is

reduced, concentrations within it tend to be less prone to short-term fluctuations (Runeckles

1992). Other features of the leaves (e.g., leaf thickness, Rubisco content, ratio of mesophyll

cell surface area to projected surface area, etc.) and of the environment (e.g., reduced levels of

irradiance, increased temperature, higher humidity, etc.) also differ within the canopy in

relation to those on the outside. This may strongly influence the uptake and effects of

pollutants one leaves at different positions within the canopy and is an important consider-

ation when attempting to extrapolate to the field from laboratory-based studies, identify the

magnitude of the response of different species in a mixture, and establish the impact of

pollutant at different developmental stages, since certain species or particular growth stages

(e.g., seedlings) may be protected from exposure to potentially damaging pollutant concen-

trations by other elements of the canopy.

At the leaf-level, the flux of the pollutant to the leaf interior (J ) is a function of the

concentration gradient between the atmosphere (i.e., the concentration of the pollutant in

the surrounding air, C

) and the leaf interior (i.e., the concentration of the pollutant in the

intercellular air spaces, C

), and the sum of the physical, chemical, and biological resistances

(SR) to diffusion from source to sink. Mathematically, this is generally expressed in a form

analogous with Ohm’s law, where:

J ¼ (C

 C

)SR:

Plant canopy

Sites of deposition

• Vegetation

• Soil

Sites of deposition

• Substomatal chamber

• Mesophyll tissue

Sites of deposition

• Leaf surface

• Leaf interior

Resistances

• Aerodynamic

• Surface

Resistances

• Cuticular

• Stomatal

Resistances

• Gas-liquid interface

• Residual

Leaf interiorIndividual leaf

FIGURE 20.2 The different scales of resolution that need to be considered in determining rates of

pollutant uptake. (Redrawn from Tanaka, K., Furusawa, I., Kondo, N., and Tanaka, K., J. Plant Cell

Physiol., 29, 743, 1988. With permission.)

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604 Functional Plant Ecology

The various impedances (SR) are generally visualized as a network of resistances to gas

flow (Figure 20.3), using Gaastra’s (1959) fundamental principles governing the tortuous

route taken by effluxing water vapor molecules. The most important resistances at the leaf

level are recognized to be those governing the movement of the pollutant into the leaf interior

(i.e., stomatal resistance, r

, and cuticular resistance, r

), the rate of deposition on the

hydrated surface of mesophyll cells, and the extent of sorption and reaction on the surface

of the cuticle and in the substomatal cavities. These resistances are under genetic and

environmental control, as well as being influenced by the physicochemical characteristics of

the gas in question.

The rate of diffusion of gaseous pollutants through the cuticular membrane is commonly

several orders of magnitude lower than that through the stomata (Lendzian 1984) and may

be considered negligible for some reactive gases, such as O

(Kersteins and Lendzian

1989). Hence, the dose of the pollutant absorbed at the leaf level is predominantly con-

trolled by factors determining stomatal conductance (i.e., stomatal aperture and frequency).

Some plants are known to exhibit intrinsically higher stomatal conductance than others

(Ko

rner 1994), and, in general, these tend to be more susceptible to damage (Reich 1987,

Becker et al. 1989, Darrall 1989). However, the response of stomata to external stimuli

(e.g., irradiance, vapor pressure deficit (VPD), soil moisture content, the presence of

Stoma

Substomatal cavity

Reaction with extracellular antioxidants

Laminar boundary

Air

Epidermis

CuticleCuticle

Epidermis

Cell wall/apoplast

Cytosol

Chloroplast Vacuole

Reaction with

membrane lipids

Reaction with

antioxidants

Reaction with

antioxidants

Reaction with

cytosolic

antioxidants

Reaction with

membrane lipids

reaction with

membrane lipids

reaction with

membrane lipids

Guard cell

FIGURE 20.3 Resistance analog model indicating the network of physical, chemical, and biological

impedances influencing the rate of diffusion of gaseous pollutants from the external atmosphere to

the target.

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Resistance to Air Pollutants: From Cell to Community 605

pollutants in the atmosphere, atmospheric CO

concentrations, etc.) can strongly influence

the rate of pollutant uptake through effects on stomatal aperture (Mansfield and Freer-Smith

1984, Darrall 1989, Wolfenden and Mansfield 1991, Wolfenden et al. 1992, Heath and Taylor

1997). Differences in stomatal conductance between sensitive and resistant individuals are

rarely sufficient to result in complete exclusion of the pollutant from the leaf interior;

therefore, it is generally concluded that mechanisms resulting in the avoidance of pollutant

uptake are not the only factors determining resistance to airborne pollutants.

Physical leaf characteristics such as leaf thickness, mesophyll cell surface area, internal air

space volume, cell wall thickness, and the volume of the aqueous matrix of the cell wall

influence the eventual concentration of the pollutant and its dissolution products in the

apoplast. Plants show considerable variation in all of these attributes. Mesophyll cell surface

area: projected leaf area, for example, ranges from typical values of between 10 and 40 for

mesophytes, but may be as high as 70 for some xerophytes (Nobel and Walker 1985, Pfanz

1987). There may also be systematic differences in anatomy along altitudinal gradients, which

can contribute to differential resistance (Ko

rner et al. 1989). In addition, pollutant molecules

in the intercellular space or substomatal cavity are partitioned across the gas-to-liquid

interface at a rate determined by the solubility of the gas in the extracellular fluid (Nobel

1974) and its chemical reactivity in the liquid phase (Heath 1988, Heath and Taylor 1997),

factors influenced by temperature and possibly radiation (Barnes et al. 1996, Cape 1997).

Differences in physicochemical properties between the most common gaseous pollutants

result in substantial differences in their solubility in water and rates of diffusion in air

(Nobel 1974), factors that, independent of other considerations, result in substantial differ-

ences in the rate at which individual gaseous pollutants are taken up (Runeckles 1992, Taylor

et al. 1998). Leaf surface characteristics (such as surface wetness, was composition, micro-

morphology, etc.) can also influence the extent of sorption onto foliar surfaces (Wellburn et al.

1997), whereas reactions with other gases in the boundary layer or in the substomatal cavities

may constitute a significant sink for some pollutants, for example, O

(Hewitt and Terry 1992,

Salter and Hewitt 1992).

In most instances, difficult and time-consuming measurements of physical leaf character-

istics are not undertaken, so it has become common practice to express rates of pollutant

uptake on the basis of the flux to the leaf interior (i.e., that impinging on the mesophyll cell

surface). This represents what is often termed the absorbed or effective dose of the pollutant,

and can be readily estimated using Fickian diffusion principles from knowledge of boundary

layer, stomatal and cuticular conductances, correcting for differences in the diffusivities

between water vapor and the pollutant of interest. Hence, the flux of O

to the leaf interior

) may be described as

¼ g

þ 0:612 g

O

where g

is the turbulent boundary layer conductance, 0.612 is the difference in the binary

diffusivities of water vapor and ozone in air (Nobel 1983), g

represents the stomatal

conductance to water vapor, and O

and O

represent the concentrations of O

in the external

atmosphere and in the intercellular spaces, respectively. No correction needs to be made for

uptake through the cuticle in this case, since the cuticle is considered to represent a virtually

impermeable barrier to O

(Kersteins and Lendzian 1989), whereas measurements of the

intercellular O

concentration (O

) suggest it is close to zero (Laisk et al. 1989). On a

cautionary note, it is important to emphasize two points. First, such calculations represent

the gross flux to the leaf interior—for some gases where the plant may act as a source as well

as a sink (e.g., H

S, NH

NO), correction for effluxing gas molecules is required to enable

estimates of the net flux of the pollutant. Second, fluxes determined in the above manner take

no account of differences in physical leaf characteristics or internal resistances influencing the

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606 Functional Plant Ecology

rate at which the pollutant (or its products) is delivered to the eventual target. Potentially

more informative models are available that enable estimates of the extent of penetration to

the plasmalemma and beyond (Chameides 1989, Ramge et al. 1992, Plo

chl et al. 1993), but

these have rarely been used due to the uncertainties surrounding the complex solution

chemistry of certain gases (e.g., O

) and the relative importance of scavenging=transformation

mation in the cell wall region.

METABOLISM

Once the pollutant has penetrated as far as the mesophyll cell surface, it may be metabolized,

sequestered, or excreted. Recent attention has focused on the rate at which pollutants (and

their reactive products, including a variety of free radical species) are immobilized and

detoxified at either the first barrier encountered after entry into the leaf (i.e., in the apoplast)

or subsequently, after penetration into the cell proper. In any consideration of the processes

underlying pollutant detoxification, it is important to recognize that dissolution in the

apoplast can result in different types of stress on cellular constituents. Many gases (e.g.,

HF, NO

, NH

, and SO

) induce acidification of subcellular compartments, whereas others

(e.g., O

, PAN, NO

) result in oxidative stress, and some (e.g., SO

) produce both (Malhotra

and Khan 1984, Hippeli and Elstner 1996, Mudd 1996). The extent of damage resulting

from the former is related to the ability of cells to buffer the increase in acidity or to excrete

protons to the external media (Slovik 1996, Burkhardt and Drechsel 1997), whereas the

influence of the latter is dependent on the efficiency of endogenous antioxidant systems

that scavenge free radical and active oxygen species before they can react with cellular

constituents (Kangasja

rvi et al. 1994, Luwe and Heber 1995, Alscher et al. 1997).

Detoxification systems capable of protecting sensitive targets from the oxidative stress

imposed by pollutants and their derivatives are common in plants, as in animals, and are

subject to strict genetic control. Most attention has focused on those systems located in the

various intracellular compartments (in chloroplasts, mitochondria, cytosol, and peroxi-

somes); however, similar systems are intimately associated with the plasmalemma and the

cell wall (Figure 20.4). In recent years, the latter has attracted increased attention since there

is growing evidence that some pollutants (e.g., O

, SO

, NO

) and their dissolution products

may be scavenged and detoxified=transformed at the mesophyll cell surface (i.e., in the

apoplast). The aqueous matrix of the cell wall is now recognized to contain significant

quantities of ascorbic acid (vitamin C) and polyamines as well as isoforms of Cu=Zn super-

oxide dismutase (SOD), ascorbate peroxidase (APX), and nonspecific peroxidases (GPODs)

(Polle and Rennenberg 1993, Luwe and Heber 1995, Ogawa et al. 1996, Dietz 1996), which

are known to function as antioxidants (Polle and Rennenberg 1993, Kangasja

rvi et al. 1994,

Alscher et al. 1997, Polle 1997). Research is still at an early stage and many questions remain

to be answered, but preliminary model calculations based on the scavenging of O

(rather

than its dissolution products) by apoplastic ascorbic acid indicate that detoxification pro-

cesses operating in the apoplast may be sufficient to provide at least limited protection against

(Chameides 1989, Polle and Rennenberg 1993, Lyons et al. 1999), a finding supported by

several independent lines of evidence (Lyons et al. 1998). Although the relative importance of

scavenging in the cell wall region remains to be established, there is a growing opinion that

factors such as the extracellular concentration of ascorbic acid may play a central role in

determining resistance to O

(Conklin et al. 1996, Lyons et al. 1998), as well as influencing the

impacts of SO

(Dietz 1996) and NO

(Ramge et al. 1992).

Pollutants and their reactive products that breach the extracellular defense, or are pro-

duced from the reaction with plasmalemma constituents, must be scavenged by intracellular

detoxification systems if damage is to be averted. There is, for example, strong evidence

linking SO

tolerance with the activity of intracellular enzymes such as catalase (CAT),

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Resistance to Air Pollutants: From Cell to Community 607

superoxide dismutase (SOD), glutathione synthetase (GS), glutathione reductase (GR),

glutathione peroxidase (GPX), and glutathione transferase (GST) (Tanaka et al. 1988, Ranieri

et al. 1992, Lea et al. 1998), as well as with levels of glutathione (GSH) and ascorbic acid (ASC)

(Madamanchi and Alscher 1994). Furthermore, recent work has drawn attention to the

importance of the subcellular localization of these systems in relation to the protection afforded

against different pollutants. For example, SO

tolerance in transgenic plants engineered to

overexpress GR in different cellular compartments indicates that it is the cytoplasmic activity

of this enzyme, rather than that of the plastidic forms, which is important in determining SO

tolerance (Aono et al. 1993, Broadbent 1995, Lea et al. 1998). There is also considerable

evidence linking components of the cellular antioxidant system (ASC, GSH, polyamines,

a-tocopherol, carotenoids, SOD, ascorbate peroxidase [APX], GR, and CAT) with O

toler-

ance (Heath 1988, Kangasja

rvi et al. 1994, Hippeli and Elstner 1996, Mudd 1996, Alscher et al.

1997, Pell et al. 1997, Heath and Taylor 1997). However, the degree of protection afforded by

these intracellular systems in relation to that achieved by scavenging in the cell wall region

(the primary site of O

action) remains poorly understood (Lyons et al. 1998), and it is

interesting to note that transgenic plants overproducing particular antioxidant enzymes in

different intracellular compartments rarely display enhanced O

resistance (Pitcher et al. 1991,

Van Camp et al. 1994, Pitcher and Zilinskas 1996, Torsethaugen et al. 1997).

In addition, toxicity thresholds are influenced by the efficiency of metabolic processes

resulting in the utilization, sequestration, and excretion of pollutants. The plasmalemma, for

example, is known to constitute an important obstacle impeding the penetration of pollutants

(and their products) to their intracellular sites of action (Herschbach et al. 1995). Some

pollutants (e.g., O

) react readily with membrane constituents (Mudd 1996, Heath and Taylor

1997). The uptake of others (i.e., SO

-derived sulfate [SO

2

], sulfite [SO

2

], and bisulfite

[HSO



] is limited by the activity of membrane-bound carriers and transformation processes

Plasma membrane

α-Tocopherol

Chloroplasts

Mitochondria

GSH

SOD

MDHAR

Plasma membrane α-Tocopherol

APX

α-Tocopherol

MDHAR & DHAR

GSH

Carotenoids

SOD

APX

PODs

GSH

MDHAR & DHAR

SOD

Peroxisomes

Cytosol

Vacuole

Nucleus

SOD

CAT

GSH

PODs

Extracellular fluid

AA, APX, PODs, SOD, Polyamines, (GSH?)

FIGURE 20.4 Subcellular localization of the antioxidant systems. AA, ascorbic acid; GSH, glutathione;

APX, ascorbate peroxidase EC. 1.11.1.11; MDHAR, monodehydroascorbate radical reductase EC.

1.1.5.4; DHAR, dehydroascorbate radical reductase EC. 1.8.5.1; GR, glutathione reductase

EC 1.6.4.2; SOD, superoxide dismutase EC. 1.15.1.1; CAT, catalase EC. 1.11.1.6; PODs, nonspecific

peroxidase (sometimes referred to as guaiacol peroxidase) EC. 1.11.1.7.

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608 Functional Plant Ecology

(Pfanz et al. 1990). Indeed, research on the inheritance of SO

resistance in Cucumis sativus L.

suggests that differences in intrinsic membrane properties may contribute to variations in SO

resistance (Bressan et al. 1981). Once inside the cell, the products of some (e.g., SO

2

, NO



and NH

) may be metabolized via the usual channels, sequestered for later use, stored

indefinitely, or volatilized. For example, SO

-derived SO

2

can either be metabolized to

yield elevated levels of water-soluble nonprotein thiols (such as cysteine, g-glutamylcysteine,

and glutathione), which can be degraded at a later date to provide reduced S to support

new growth (De Kok 1990), or it can be sequestered on a semipermanent basis in the vacuole

(presuming there is sufficient available energy and H

ions to facilitate its transport across

the tonoplast) (Cram 1990, Kaiser et al. 1989, Slovik 1996). In contrast, SO



may be

photoreduced and, after volatilization, be reemitted, mainly as H

S. This pathway was

originally considered to form a possible pathway for the detoxification of SO

(Rennenberg

1984), but current opinion suggests that the contribution of such emissions to the detoxifi-

cation of environmentally relevant SO

concentrations may be negligible (Stuhlen and

De Kok 1990).

GENE EXPRESSION

The photoautotrophic habit adopted by plants has resulted in the evolution of a sophisticated

battery of mechanisms that renders them, with exception of all but a few microbes, the most

adaptable of all multicellular organisms on the planet (Smith 1990). This flexibility includes

the capacity to sense and react to the presence of airborne pollutants, as to other environ-

mental stimuli, in a manner directed at sustaining survival to reproduction, a goal that may or

may not be achieved, depending on the extent of metabolic flexibility and the degree of stress

imposed at the cellular level.

Exposure to pollutants and other oxidative stresses induces changes in the expression

of defense-related genes, posttranslational modification of enzymes (e.g., phosphoryla-

tion=dephosphorylation), and the synthesis of secondary metabolites—resulting in increases

in the threshold for damage, that is, acclimation (Kangasja

rvi et al. 1994, Schraudner et al.

1994). Recent work suggests that the pattern of changes induced by some pollutants (e.g., O

)

reflects on orchestrated series of events, triggered by disparate oxidative syndromes, which

resembles the hypersensitive response provoked by pathogen attack (Alscher et al. 1997,

Pell et al. 1997, Schraudner et al. 1997). This raises the question of whether the patterns of

defense-related gene expression triggered by one pollutant are similar to those induced by

another, whether the same signal transduction pathways are involved, and whether the

similarity in response results in enhanced tolerance to a range of pollutants, and possibly

other oxidative stresses. Opinions differ. However, based on the fact that particular geno-

types, specific transformants, and plants treated with specific protectants (e.g., EDU) may be

sensitive to one pollutant but not to another (Barnes and Wellbum 1998 and references

therein), whereas the direction and the extent of the responses of the same species to different

pollutant combinations vary in individual genotypes grown under common conditions

(Bender and Weigel 1992), we take the view that despite the common responses observed at

the level of gene expression, specific mechanisms must underlie tolerance to different air

pollutants (i.e., tolerance to one pollutant is independent of that to another), as the action and

subcellular localization of the stresses imposed by pollutants differ. This conclusion is

supported by observations that differences in stomatal behavior=conductance (i.e., avoidance

mechanisms) commonly govern the similarity in response to different pollutants (Winner et al.

1991). It is also interesting to note that some pollutants (e.g., SO

and NO

) are much less

effective than others (e.g., O

) in eliciting changes in antioxidant gene expression (Schraudner

et al. 1994, Schraudner et al. 1997), whereas other stresses (such as wounding, necrotizing

pathogens, or elevated levels of UV-B radiation), which are known to elicit strong and rapid

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