evious chapters have focused on the underlying

processes by which plant roots acquire water and nutrients from the soil (Chapters 1 to 4), leaves harvest light
energy and convert atmospheric CO2 and soil NO- 3 into
stable chemical forms of sucrose, starch, and and amino
acids (Chapters 5, 7, 8, 11) and subsequently unlock
the stored chemical energy through the process of glycolysis and mitochondrial respiration for growth and
development (Chapter 10). By necessity, to elucidate
the biochemical and molecular mechanisms by which
these processes occur, plants are studied under normal
or ideal environmental conditions for growth and development. However, plants often encounter unusual or
extreme conditions: trees and shrubs in the northern
temperate latitudes experience the extreme low temperatures of winter; alpine plants experience cold and drying
winds; and agricultural crops may experience periods of
extended drought as well as high and low temperatures.
Extremes in environmental parameters create stressful conditions for plants, which may have a significant
impact on their physiology, development, and survival.
The study of plant responses to environmental stress
has long been a central theme for plant environmental
physiologists and physiological ecologists. How plants
respond to stress helps to explain their geographic distribution and their performance along environmental
gradients. Because stress invariably leads to reduced
productivity, stress responses are also important to
agricultural scientists. Understanding stress responses is
essential in attempts to breed stress-resistant cultivars
that can withstand drought, and other yield-limiting
conditions. Finally, because stressful conditions cause
perturbations in the way a plant functions, they provide
the plant physiologist with another very useful tool for
the study of basic physiology and biochemistry.
This chapter will examine some of the stresses that
plants encounter in their environment. The principal
topics to be addressed include
• the basic concepts of plant stress, acclimation, and
adaptation,
• the light-dependent inhibition of photosynthesis
through a process called photoinhibition,
• the effects of water deficits on stomatal conductance,
• the effects of high- and low-temperature stress on
plant survival,
• the challenge of freezing stress on plant survival, and
• the responses of plants to biotic stress due to infestations by insects and disease.
13.1 WHAT IS PLANT STRESS?
Because life is an endergonic process, that is G > 0
(Chapter 5), energy is an absolute requirement for the
223
224 Chapter 13 / Responses of Plants to Environmental Stress
maintenance of structural organization over the lifetime
of the organism. The maintenance of such complex
order over time requires a constant through put of
energy. This means that individual organisms are not
closed systems but are open systems relative to their
surrounding environment. This results in a constant
flow of energy through all biological organisms, which
provides the dynamic driving force for the performance
of important maintenance processes such as cellular
biosyntheses and transport to maintain its characteristic
structure and organization as well as the capacity to
replicate and grow. Such energy flow ensures that living
biological organisms are never at equilibrium with their
environment, that is, G is never equal to zero, but
remain in a steady-state condition far from equilibrium
(see Chapter 5). The maintenance of such a steady-state
results in a meta-stable condition called homeostasis.
As a consequence, all life forms may be considered
transient energy storage devices with finite but varying
lifetimes (Figure 13.1).
Any change in the surrounding environment may
disrupt homeostasis. Environmental modulation of
homeostasis may be defined as biological stress. Thus,
it follows that plant stress implies some adverse effect
on the physiology of a plant induced upon a sudden
transition from some optimal environmental condition
where homeostasis is maintained to some suboptimal
condition which disrupts this initial homeostatic state
(Figure 13.2). Thus, plant stress is a relative term since
the experimental design to assess the impact of a stress
always involves the measurement of a physiological
phenomenon in a plant species under a suboptimal,
stress condition compared to the measurement of the
same physiological phenomenon in the same plant
species under optimal conditions. Since the extent of a
stress can be quantified by assessing the difference in
these measurements under optimal versus suboptimal
conditions, the basis of stress physiology is comparative
E
A

EIN EOUT
A
FIGURE 13.1 Biological life forms as energy-storing
devices. A is any biological life form. EIN (thick arrow)
is the energy flowing from the surrounding environment
into the biological organism, A. EOUT (thin arrow) is the
energy flowing out of the biological organism back into
the environment. The thicknesses of the arrows indicate the differences in the relative flux of energy flowing
in and out of a living organism. EA is the steady-state
energy stored or trapped by a living organism. According
to the First Law of thermodynamics (Chapter 5), EIN +
EA + EOUT = 1. Thus, EA = EIN - EOUT.
Rate of a
Physiological Process
Homeostatic
State
Death
Stress
Time
FIGURE 13.2 The effects of environmental stress on plant
homeostasis. Under some optimal environmental condition, a plant is in homeostasis as indicated by a constant
rate of some important physiological process over time.
Upon the imposition of an external stress, the rate of
this physiological process decreases rapidly. It is fatal
for some plants that are unable to adjust to an imposed
stress and can not establish a new homeostatic state. Such
plants are classified as susceptible to the stress.
physiology. However, plant species are highly variable
with respect to their optimum environments and their
susceptibility to extremes of, for example, irradiance,
temperature, and water potential. Is stress a function of
the environment or the organism? For example, are the
extreme environments encountered in deserts or arctic
tundra stressful for plants that normally thrive there?
Are these environments stressful only to some species
but not to others?
13.2 PLANTS RESPOND TO
STRESS IN SEVERAL
DIFFERENT WAYS
Plant stress can be divided into two primary categories.
Abiotic stress is a physical (e.g., light, tempera,-
ture) or chemical insult that the environment may
impose on a plant. Biotic stress is a biological insult,
(e.g., insects, disease) to which a plant may be exposed
during its lifetime (Figure 13.3). Some plants may be
injured by a stress, which means that they exhibit
one or more metabolic dysfunctions. If the stress is
moderate and short term, the injury may be temporary
and the plant may recover when the stress is removed.
If the stress is severe enough, it may prevent flowering,
seed formation, and induce senescence that leads to
plant death. Such plants are considered to be susceptible (Figure 13.3). Some plants escape the stress altogether,
such as ephemeral, or short-lived, desert plants.
13.3 Too Much Light Inhibits Photosynthesis 225

Environme ntal Stress

Abiotic Biotic

Stress response

Resistance Susceptibility Avoidance

Death
Acclimation
Growth
Survival
Senescence Survival
FIGURE 13.3 The effect of environmental stress on plant
survival.
Ephemeral plants germinate, grow, and flower very
quickly following seasonal rains. They thus complete
their life cycle during a period of adequate moisture
and form dormant seeds before the onset of the dry
season. In a similar manner, many arctic annuals rapidly
complete their life cycle during the short arctic summer
and survive over winter in the form of seeds. Because
ephemeral plants never really experience the stress of
drought or low temperature, these plants survive the
environmental stress by stress avoidance (Figure 13.3).
Avoidance mechanisms reduce the impact of a
stress, even though the stress is present in the environment. Established plants of alfalfa (Medicago sativa), for
example, survive dry habitats as adult plants by sending
down deep root systems that penetrate the water table.
Alfalfa is thereby ensured an adequate water supply
under conditions in which more shallow-rooted plants
would experience drought. Other plants develop fleshy
leaves that store water, thick cuticles or pubescence (leaf
hairs) to help reduce evaporation, or other modifications that help to either conserve water or reduce water
loss. Cacti, with their fleshy photosynthetic stems and
leaves reduced to simple thorns, are another example of
drought avoiders. Most drought avoiders would be
severely injured should they ever actually experience
desiccation.
Many plants have the capacity to tolerate a particular stress and hence are considered to be stress resistant
(Figure 13.3). Stress resistance requires that the organism exhibit the capacity to adjust or to acclimate to the
stress.
Finally, a controversy over terminology is concerned with use of the term strategy. Strategy is often
used to describe the manner in which a plant responds
successfully to a particular stress. Some physiologists
object to use of the term for the reason that strategy implies a conscious plan; that is, it is teleological. 1
However, strategy can validly describe a genetically programmed sequence of responses that enable an
organism
to survive in a particular environment.
13.3 TOO MUCH LIGHT
INHIBITS PHOTOSYNTHESIS
In Chapters 7 and 8, we discussed the conversion of
visible light energy into ATP and NADPH through
photosynthetic electron transport. In addition to forming Triose-P that can be converted to sucrose or starch,
the ATP and NADPH are required to regenerate RuBP
by the Calvin Cycle (Figure 13.4A). The continuous
regeneration of RuBP is an absolute requirement for
the continuous assimilation of CO2 by Rubisco. This
requirement which is satisfied by the light-dependent
biosynthesis of ATP and NADPH is what makes CO2
assimilation light dependent. However, although light
is required for the photosynthetic assimilation of CO2,
too much light can inhibit photosynthesis.
In all plants, the light response curve for photosynthesis exhibits saturation kinetics as illustrated
in Figure 13.4B. At low irradiance, the rate of CO2
assimilation increases linearly with an increase in irradiance. This is to be expected since more absorbed
light means higher rates of electron transport which, in
turn, means increasing levels of ATP and NADPH for
the regeneration of RuBP (Figure 13.4A). Thus, under
low, light-limiting conditions, the rate at which RuBP
is regenerated through the consumption of ATP and
NADPH by the Calvin Cycle limits the rate of photosynthesis measured either as CO 2 assimilation or O2
evolution. The maximum initial slope of the photosynthetic light response curve under low, light-limiting
conditions provides a measure of photosynthetic efficiency measured either as moles of CO2 assimilated per
photon absorbed, or alternatively, moles of O2 evolved
per photon absorbed if photosynthesis is measured as
the rate of O2 evolution (Figure 13.4B).
Upon further increases in irradiance, the rate of
photosynthesis is no longer a linear function of irradiance but rather levels off. At these higher light
intensities, the rate of photosynthesis is said to be
light saturated (Figure 13.4B, red shaded area). This
means that the Calvin Cycle is saturated with ATP and
NADPH which, in turn, means that Rubisco is saturated with one of its substrates, RuBP. The maximum
light saturated rate is a measure of photosynthetic
1Teleology is the doctrine of final causes, assigning purpose
to natural processes. Teleological arguments are considered
inappropriate in natural science.
226 Chapter 13 / Responses of Plants to Environmental Stress
Regenerat
ion
PS II
A.
B.
hv hv
PS I
2PGA RuBP
Triose-P
Rubisco
Calvin
Cycle
CO
2
ATP
NADPH
Rate of CO
2 Assimilation

Rate of O
2 Evolution

Irradiance (mol m2s1)

Light
Limited Photoinhibited
Excess Light
O 2500
Light
saturated
Pit cavity
FIGURE 13.4 A schematic illustration of the response of photosynthesis to increasing
irradiance. (A) A model illustrating the interaction between photosynthetic linear
electron transport and the Calvin Cycle. (B) A schematic light response curve for
photosynthesis measured as either the rate of CO2 assimilation or the rate of O2
evolution. The area above the light response curve represents excess irradiance that
is not used in photosynthesis.
capacity and will have the units of either moles of
CO2 assimilated or moles of O2 evolved per leaf area
per unit time. Thus, under light-saturated conditions,
the rate of regeneration of RuBP no longer limits
the rate of CO2 assimilation but rather it is the rate
at which Rubisco can consume RuBP and CO2 that
limits the rate of photosynthesis. Consequently, under
light-saturated conditions, the rate of photosynthesis
becomes light-independent, that is, the exposure of a
plant to higher irradiance no longer changes the rate of
photosynthesis. Under light-saturated conditions, plants
become exposed to increasing levels of excess light
(Figure 13.4B, yellow shaded area), that is, they become
exposed to more light than the plant can use for photosynthesis. If the plant continues to be exposed to higher
and higher levels of excess light, the rate of photosynthesis begins to decrease (Figure 13.4B). This is called
photoinhibition of photosynthesis and is defined as the
light-dependent decrease in photosynthetic rate that
may occur whenever the irradiance is in excess of that
required either for the photosynthetic evolution of O2
or the photosynthetic assimilation of CO2.
13.3 Too Much Light Inhibits Photosynthesis 227
There is a consensus in the literature that in
most plants, PSII is more sensitive to photoinhibition
than PSI. The effects of exposure to photoinhibition
by shifting plants from low light to high light
can be assessed either by monitoring changes in
photosynthetic efficiency and photosynthetic capacity (Figure 13.5A) or by monitoring chlorophyll
fluorescence (Box 13.1) to assess changes in maximum PSII photochemical efficiency measured as
Fv/Fm (Figure 13.5B). Photoinhibition that results
in a decrease in photosynthetic efficiency as well
as photosynthetic capacity (Figure 13.5A) usually reflects
0 500
 Chronic Photoinhibition
Efficiency

Control
Capacity

1000
80
60
40
20
0 10

Dark Control

10
Photoinhibition
Time (h)
Recovery
Time (h)
Fv/Fm
55
0.8
0.6
0.4
0.2
A.
B.
FIGURE 13.5 The effects of chronic photoinhibition on
photosynthesis. (A) Schematic light response curves for
control plants which have not been pre-exposed to high
light and plants that have been pre-exposed to high light
to induce chronic photoinhibition prior to measuring
their light response curve. The maximum initial slope is
a measure of photosynthetic efficiency. The maximum
light saturated rate is a measure of photosynthetic capacity. (B) A schematic representation illustrating the effect
of exposure time to high light to induce chronic photoinhibition on the maximum photochemical efficiency
of PSII measured as Fv/Fm (see Box 13.1). The broken
line illustrates the slow rate of recovery of Fv/Fm when
the chronically photoinhibited plants are shifted back
to low-light conditions. Control plants were kept in the
dark over the course of the experiment.
chronic photoinhibition which is the result of photodamage to PSII. Specifically, the site of damage is the
D1 reaction center polypeptide of PSII which causes
a decrease in the efficiency of PSII charge separation
(Chapter 7). This decrease in the PSII photochemical
efficiency can be measured as Fv/Fm (Figure 13.5B)
(Box 13.1). The decrease in PSII photochemical efficiency is usually paralleled by a decrease in photosynthetic
efficiency of O2 evolution. A characteristic of
chronic photoinhibition is that it is only very slowly
reversible after plants are shifted from excess light to
low light (Figure 13.5B).
13.3.1 THE D1 REPAIR CYCLE
OVERCOMES PHOTODAMAGE
TO PSII
PSII reaction centers exhibit an inherent lifetime. This
was first indicated by the fact that the D1 polypeptide of
PSII reaction centers exhibits the fastest turnover rate
of any plant protein. The D1 polypeptide is degraded
and resynthesized in the time span of approximately
30 minutes. Recently, it has been proposed that PSII
actually exhibits the properties consistent with a photon counter, that is, its lifetime is dependent upon
the number of photons absorbed and not the absolute
time. It has been calculated that, under normal growth
conditions, each PSII reaction center is irreversibly damaged presumably due to photooxidative damage and
spontaneously degraded after the absorption of 105 to
107 photons. Thus, exposure to excess light simply
shortens the lifetime of PSII because these conditions
would enhance the probability of photooxidative damage and shorten the time to absorb the necessary photons
to cause the degradation of D1.
How do plants ensure a constant supply of functional PSII reaction centers? Plants and green algae
exhibit a single chloroplastic gene that encodes the D1
polypeptide called psbA. These organisms have evolved
a D1 repair cycle which repairs photodamage to PSII
(Figure 13.8). When the D1 polypeptide is damaged, it
is marked for degradation by protein phosphorylation.
After phosphorylation of D1, PSII is partially disassembled and the D1 polypeptide is degraded by proteolysis.
Subsequently, the psbA