BLE 14.

2 Effects of growth temperature and

growth irradiance on LT50 of winter rye (Secale
cereale L. cv Musketeer). Growth irradiance is in
units of mol photons m-2 s-1).
Growth Growth
Temperature (◦C) Irradiance LT50 (◦C)
20 50 low light -4
20 250 moderate light -6
20 800 high light -8
5 50 low light -8
5 250 moderate light -16
Cold Stress → Growth/Development
→ Cold Acclimation → Freezing Tolerance (14.3)
As indicated in Table 14.2, exposure to low temperature (5 ◦C) is an absolute requirement for the attainment of
maximum freezing tolerance in winter rye
(LT50 = -16◦C). However, low temperature by itself
is not sufficient to induce maximum freezing tolerance since growth at low temperature but low light
reduces LT50 by 50% (Table 14.2). Thus, light is also
an absolute requirement for the attainment of maximum freezing tolerance in winter cereals (Table 14.2).
This light-dependent increase in freezing tolerance at
constant low-growth temperature occurs independently
of either photoperiod or light quality. Thus, the light
dependence of LT50 in herbaceous winter cereals does
not appear to be phytochrome-dependent. Furthermore, increasing the growth irradiance at temperatures
that normally do not induce freezing tolerance (20◦C)
results in a doubling of LT50 from -4 under low light to
-8◦C under high light, which is consistent with the light
dependence of freezing tolerance. However, high light
can not compensate for low temperature for the induction of maximum freezing tolerance in winter cereals.
Thus, the attainment of maximum freezing tolerance
appears to be the result of an additive effect of both
low-growth temperature and growth irradiance.
14.4.1 COLD ACCLIMATED PLANTS
SECRETE ANTIFREEZE
PROTEINS
Overwintering plants can tolerate freezing because of
their ability to control the freezing event itself. As long
as freezing of water is confined to the apoplast, that
is the cell wall and the extracellular space, the plant
will survive. Alternatively, if freezing occurs intracellularly, the plant will die. Cold acclimation in many
plants is associated with the secretion of antifreeze
proteins (AFPs) from the cytoplasm into the apoplast.
AFPs have been reported in ferns, gymnosperms, as
well as mono- and dicotyledonous angiosperms. AFPs
inhibit ice crystal growth by binding to the surface of
a growing ice crystal via hydrogen bonding between
specific hydrophilic amino acids present in the AFP and
water within the crystal lattice of ice. The presence
of AFPs in cold-tolerant plants is not constitutive but
requires exposure to low temperature and they accumulate in virtually all plant tissue including seeds, stems,
leaves, flowers, and roots. When winter rye plants cold
acclimate, the gaseous plant hormone, ethylene, is produced. Ethylene induces the transcription of the family
of genes that encode AFPs. Upon translation, the AFPs
are secreted via the endoplasmic reticulum, Golgi bodies, and vesicles that fuse with the plasma membrane
and are deposited on the surface of the cell wall where
they inhibit ice crystal formation.
Do AFPs alter LT50? The answer is an unequivocal
no. If this is so, what is the role of AFPs? Although AFPs
have a minimal effect on LT50, AFPs have a significant
effect on the rate of ice crystal formation. Thus, AFPs
most likely enhance winter survival by slowing the rate
of extracellular freezing.
14.4.2 NORTH TEMPERATE WOODY
PLANTS SURVIVE FREEZING
STRESS
Boreal deciduous trees, conifers, and shrubs such as
paper birch (Betula papyrifera), trembling aspen (Populus tremuloides), and willow (Salix sp.)—all found as far
north as the arctic circle—survive because they are able
to acclimate to the below-freezing winter temperatures.
During their normal growing season, these plants will
suffer injury or death if exposed to freezing temperatures. Even a light frost during the spring or summer
may be lethal to plants that are actively growing. Yet,
cold-acclimated stems of these species may survive temperatures as low as -196◦C (liquid nitrogen) without
apparent injury.
Acclimation of woody species to freezing stress
is a common phenomenon in nature, but the precise
mechanism by which acclimation is achieved is not
well understood. It is known that acclimation in woody
tissues occurs in two distinct stages (Figure 14.13). It
begins in the autumn when growth and photosynthesis
ceases and the plant enters dormancy. This first stage
of acclimation is induced by short days and is thought
to be under the control of phytochrome. Acclimation at
this stage can be inhibited by long days and early frost.
Thus, in woody species, it is essential that the plant
enter the dormant stage prior to the onset of frost to
prevent freezing damage.
The second stage of acclimation is triggered by
exposure of the overwintering tissue to low temperature, corresponding to the first frost (Figure 14.13). At
this stage, respiratory activity is sufficient to provide the
14.5 Plants Adjust Photosynthetic Capacity in Response to High Temperature 257
Time (month of year)
Tissue temperature (ºC)
–80
–40
0

First
frost
Short-day
photoperiod
response

Lowest
temperature
tested
Sept. Oct. Nov.

–60
–20
+20
FIGURE 14.13 Acclimation to low temperature in woody
stems. The curve depicts the lowest survival temperature as a function of time of year. Note that significant
decreases in survival temperature correspond to shortening daylength and the time of the first frost.
energy necessary for the numerous metabolic changes
required to attain the maximum cold-acclimated state.
There are increases in the level of organic phosphates
and the conversion of starch to sugars. Glycoproteins accumulate and the protoplasm becomes generally
more resistant to dehydration. Fully acclimated cells
can withstand temperatures far below those normally
experienced in nature.
14.5 PLANTS ADJUST
PHOTOSYNTHETIC
CAPACITY IN RESPONSE
TO HIGH TEMPERATURE
Plants that can acclimate to high temperatures are
called thermotolerant plants. Photosynthetic capacity
measured as the maximum light-saturated rate of CO2
assimilation is sensitive to temperature (Figure 14.14).
The C3 and the C4 plant illustrated in Figure 14.14
exhibit temperature optima for photosynthesis that are
dependent upon the growth condition to which these
plants were exposed. Plants exposed to cool temperatures generally exhibit a lower temperature optimum for
photosynthesis than those exposed to high temperatures.
Such a shift in temperature optima reflects photosynthetic acclimation to temperature which has been shown
10
5432154321
20 30 40 50

Cool
Hot
T. oblongifolia
A

Cool
L. divaricata
Hot
B

0
Rate of CO
2 Assimilation (nmol cm2 s1)
Leaf Temperature (c)
FIGURE 14.14 A schematic graph illustrating the ability
of thermotolerant C3 and C4 plants to adjust photosynthetic capacity. Temperature profiles for light-saturated
photosynthetic rates are plotted as a function of leaf
temperature for a C4 plant, T. oblongifolia (A), and a
C3 plant, L. divaricata (B). (Adapted from Berry, J. A.,
O. Bjorkman. 1980. ¨ Annual Review of Plant Physiology
31:491–543.)
to be reversible and not due to temperature-dependent
stomatal limitations. Rather, such photosynthetic acclimation appears to be due to a combination of changes
in the temperature stability of thylakoid membranes as
well as the enzymes of the PCR cycle such as Rubisco.
Although photosynthetic acclimation of C3 overwintering species such as wheat and rye requires growth
and development at cold temperatures, this is not the
case for all plants. For example, reversible photosynthetic acclimation in the C3 species, Nerium oleander,
is observed in fully expanded, mature leaves exposed
to either high or low temperatures. This may be due,
in part, to the different absolute temperature ranges to
which a particular species can acclimate.
The maximum rate of photosynthesis of the C4
plant, T. oblongifolia, appears to be more sensitive to
leaf temperature than that of L. divaricata, a C3 plant
(Figure 14.14). However, such differential responses do
not reflect a general difference between C3 and C4
species. Rather, such differences have been shown to
be very species dependent within plants that exhibit
either C3 or C4 photosynthesis. Clearly, plants exhibit
extraordinary plasticity to adjust photosynthetically to
changes in temperature.
258 Chapter 14 / Acclimation to Environmental Stress
14.6 OXYGEN MAY PROTECT
DURING ACCLIMATION TO
VARIOUS STRESSES
Although the oxygen evolving complex (OEC) associated with PSII results in the light-dependent evolution
of oxygen (Chapter 7), O2 can also act as alternative
electron acceptor for photosynthetic electron transport.
Thus, photosynthetic electron transport may also consume oxygen. Even under normal conditions, up to
5 percent to 10 percent of the photosynthetic electrons
that are generated by PSI may react with molecular
oxygen rather than with NADP+. This has important
functional consequences for active chloroplasts. The
photoreduction of oxygen by PSI is called the Mehler
reaction and results in the production of another toxic,
reactive oxygen species known as a superoxide radical
(O- 2 ) (a radical is a molecule with an unpaired electron).
To counteract the accumulation of this radical, photosynthetic organisms have evolved mechanisms to protect
themselves from excess light and the potential ravages
of O2. An effective system for the removal of superoxide is the ubiquitous enzyme superoxide dismutase
(SOD). SOD is found in several cellular compartments
FIGURE 14.15 Oxygen as an alternative
electron acceptor in chloroplasts. (A) The
Asada-Halliwell pathway. O2 can be photoreduced by PSI directly to generate
the superoxide free radical, O- 2 (Mehler
reaction). Superoxide dismutase (SOD)
then converts this radical to hydrogen
peroxide (H2O2). Hydrogen peroxide is
also toxic and is reduced via the chloroplastic enzyme, ascorbate peroxidase, to
water and ascorbate is oxidized to monodehydroascorbate (MDHA). Ascorbate
(vitamin C) is regenerated through the
action of the enzyme, dehydroascorbate
reductase, through the consumption of
reduced glutathione (GSH). Oxidized glutathione (GSSH) is, in turn, reduced by the
enzyme glutathione reductase, which uses
NADPH as reductant. (B) Chlororespiratory pathway. NAD(P)H dehydrogenase
(Ndh) present in thylakoid membranes
consumes stromal NAD(P)H and passes
the electrons (e) directly to plastoquinone
(PQ). The plastid terminal oxidase (PTOX)
present in thlylakoid membranes oxidizes
plastoquinol and reduces O2 to water. The
stromal pool represents any metabolic
pathway present in the stroma that generates reducing power (see Chapter 8). Ndh
may also participate in cyclic electron transport around PSI.
Lumen
Ndh PQ Cyt PSI
PC
fd
ee
ee
e
NAD(P)H
PQ
PTOX

Stomal Pool

PSI
b6f
B. Chlororespiratory pathway
A. Asada-Halliwell pathway
SOD
O2– H2O2 PSI
Ascorbate GSSH
MDHA GSH
NADPH
NADP+
O2
O2
H2O
Thylakoid
membra