under red light, Fremyella diplosiphon exhibits the characteristic blue-green phenotype due to the fact that PC
most effectively absorbs red light. In contrast, during
growth under green light, Fremyella diplosiphon exhibits
a distinctive red phenotype because PE most effectively absorbs green light. Since this acclimation process
is photoreversible, it appeared to share features that
were common to the red/far red photoreversible, phytochrome response characteristic of terrestrial plants.
However, recently it has been shown that CCA is regulated by both the redox state of the PQ pool as well as
by multiple, as yet unidentified, photoreceptors.
Clearly, CCA is due to changes in the expression of
genes present in the genome of a cyanobacterium to produce the different phenotypes. The reversible changes
in phenotype associated with CCA reflect a remarkable
plasticity of cyanobacteria to respond to changes in ambient light color to maximize absorption of light energy
for photosynthesis and growth. Thus, this phenomenon
should be called complementary chromatic acclimation
rather than complementary chromatic adaptation.
14.3.3 ACCLIMATION TO DROUGHT
AFFECTS SHOOT–ROOT RATIO
AND LEAF AREA
One of the long-term effects of water deficit is a reduction in vegetative growth. Shoot growth, and especially
the growth of leaves, is generally more sensitive than
root growth. In a study in which water was withheld
from maize (Zea mays) plants, for example, there was
a significant reduction of leaf expansion when tissue
water potentials reached -0.45 MPa and growth was
completely inhibited at -1.00 MPa. At the same time,
normal root growth was maintained until the water
potential of the root tissues reached -0.85 MPa and
was not completely inhibited until the water potential
dropped to -1.4 MPa. Reduced leaf expansion is beneficial to a plant under conditions of water stress because
it leads to a smaller leaf area and reduced transpiration.
Traditionally, the effect of low water potential on cell
enlargement has been attributed to a loss of turgor in
the cells in the growing region. Plant cell enlargement
occurs when water moves in to establish full turgor
following stress relaxation in the cell wall (Chapter 16
and 17). It should not be too surprising, then, that an
early consequence of limited water supply would be
reduced growth. Thus, although the cells are able to
maintain turgor, it does not appear to be sufficient to
maintain a full rate of growth based on cell enlargement.
The preceding discussion applies primarily to
shoots and leaves that are actively growing. Many
mature plants, such as cotton (Gossypium hirsutum),
subjected to prolonged water stress will respond by
accelerated senescence and abscission of the older
leaves. In the case of cotton, only the youngest leaves
at the apex of the stem will remain in cases of severe
water stress. This process, sometimes referred to as leaf
area adjustment, is another mechanism for reducing
leaf area and transpiration during times of limited water
availability. So long as the buds remain viable, new
leaves will be produced when the stress is relieved.
As noted above, roots are generally less sensitive
than shoots to water stress. Apparently, osmotic adjustment in roots is sufficient to maintain water uptake
and growth down to much lower water potentials than
is possible in leaves. Relative root growth may actually be enhanced by low water potentials, such that the
254 Chapter 14 / Acclimation to Environmental Stress
root–shoot ratio will change in favor of the proportion of roots. An increase in the root–shoot ratio as
the water supply becomes depleted is clearly advantageous, as it improves the capacity of the root system to
extract more water by exploring larger volumes of soil. A
changing root–shoot ratio is accompanied by a change
in source–sink relationships with the result that a larger
proportion of photosynthate is partitioned to the roots.
Delivery of carbon to the roots can continue, however,
only to the extent that carbon supply can be maintained
by photosynthesis or mobilization of reserves stored in
the leaves. In addition, to changes in leaf area, some
plants respond to growth under water deficit conditions
by reducing stomatal frequency. By reducing the number of stomates per leaf area, a plant can reduce potential
water loss due to transpiration when water is limiting
growth.
An early response to water deficits is closure of
stomates to conserve water. In some plants this may
lead to low internal leaf CO2 concentrations which will
limit photosynthetic capacity. A limited photosynthetic
capacity in the presence of light can result in exposure
of plants to excess light and photoinhibition. Since
leaf O2 levels will remain higher than CO2 when leaf
stomates are closed, O2 will be preferentially consumed
through photorespiration and the action of the enzyme
Rubisco (Equation 14.1). Just as for the reduction of
CO2 (Equation 14.1), the continuous consumption of
O2 by Rubisco (Equation 14.2)
RuBP + CO2 → 2PGA (14.1)
RuBP + O2 → PGA + P-Glycolate (14.2)
requires the continuous regeneration of RuBP by the
Calvin Cycle (Chapter 8). This requires a constant supply of NADPH and ATP generated by photosynthetic
electron transport (see Figure 13.4). The fixation of one
mole of O2 through photorespiration consumes more
energy (5ATP + 3NADPH) than the fixation of one
mole of CO2 (3ATP + 2NADPH). Consequently, the
photorespiratory pathway may play an important role
in maintaining photostasis when CO2 is limiting. Such
a role for photorespiration is supported by the fact
that photorespiratory mutants of Arabidopsis thaliana are
more sensitive to high light under water stress.
14.3.4 COLD ACCLIMATION MIMICS
PHOTOACCLIMATION
For more than a century it has been known that the
growth of winter varieties of cold tolerant herbaceous
plant species such as rye (Secale cereale L. cv Musketeer) and wheat (Triticum aestivum L. cv Kharkov)
at low temperatures results in enhanced freezing tolerance measured as LT50, the freezing temperature
at which 50 percent of a population of plants are
killed (Figure 14.12A). The enhanced freezing tolerance is strongly correlated with the expression of
cor genes. However, in addition to enhanced freezing
tolerance, cold acclimated winter varieties of wheat,
rye, barley, spinach as well as Arabidopsis thaliana also
exhibit a decreased sensitivity to photoinhibition even
though the plants were never exposed to high light
(Figure 14.12B). Thus, the decreased sensitivity to photoinhibition exhibited by these cold acclimated plants
mimics photoacclimation to high light. However, in
20
40
60
80
100
0 4 8 10 12 14 16
% Plants killed
Temperature (c)
100
0 10
Fv/Fm (% of control)
Photoinhibition Time (h)
A.
B.
FIGURE 14.12 (A) The schematic graph illustrating the
effect of growth temperature on freezing tolerance measured as LT50. Cold-tolerant plants grown at 25◦C (black
line) exhibit an LT50 of -7◦C whereas the cold-tolerant
plants that are grown at 5◦C (red line) exhibit an LT50
of about -12◦C. Thus, cold-acclimated plants exhibit an
increased freezing tolerance. (B) A schematic graph illustrating the effect of growth temperature on sensitivity to
photoinhibition. The maximal photochemical efficiency
of PSII measured as Fv/Fm of the plants grown at 25◦C
(black line) decreases to a greater extent than that of
plants grown at 5◦C (red line). Thus, cold-acclimated
plants exhibit a decreased sensitivity to photoinhibition
(Adapted from Gray, G. R., L. V. Savitch, A. G. Ivanov,
N. P. A. Huner. 1996. Plant Physiology 110:61–71).
14.4 Freezing Tolerance in Herbaceous Species is a Complex Interaction Between Light and Low Temperature 255
these winter varieties, this is accomplished with minimal
changes in the structure and composition of LHCII.
How is this possible? Growth of cold-tolerant
winter wheat and winter rye at low temperature stimulates photosynthetic capacity with minimal changes
in photosynthetic efficiency or in the ratios of chlorophyll a/chlorophyll b. This stimulation in photosynthetic
capacity is the result of the following. First, cold
acclimation enhances the transcription and translation
of genes encoding major regulatory enzymes of stromal and cytosolic carbon metabolism such as Rubisco,
chloroplastic FBPase, cytosolic FBPase, and sucrose-P
synthase (SPS), as well as increased fructan biosynthesis
in the vacuole (Chapter 9). This results in higher total
enzyme activity and a higher flux of carbon through
the sucrose biosynthetic pathway. Second, this is coupled to higher rates of carbon export from the leaves
in the light due to enhanced sink activity (Chapter 9).
In contrast to short-term exposure to low temperature,
growth at low temperature stimulates rates of respiratory
carbon metabolism. Third, cold acclimation suppresses
photorespiration which also enhances net carbon gain.
Thus, subsequent exposure of these cold-acclimated
plants to increasing irradiance stimulates their photosynthetic capacity even further, which is translated into
increased growth rates and biomass production at low
temperature in addition to the stimulation of NPQ
via the xanthophyll cycle. Thus, these cold-acclimated
plants exhibit a resistance to photoinhibition because
of their enhanced capacity to utilize the absorbed light
for carbon metabolism, biomass production and growth
coupled with the dissipation of any excess absorbed
light through NPQ. It is important to appreciate that,
to exhibit these characteristics, cold-tolerant plants must
grow and develop at low temperatures.
Similar to cold-acclimated winter varieties of
wheat, rye, barley, spinach, as well as Arabidopsis
thaliana, cold-acclimated Chlorella vulgaris also exhibits
a decreased sensitivity to photoinhibition. However, in
contrast with these terrestrial plants, cold-acclimated
Chlorella vulgaris exhibits the same yellow-pale-green
phenotype as high-light grown cells (Figure 14.9,
HL) even though these cold-acclimated cells have
not grown under high light. It has been shown
that cold acclimation of Chlorella vulgaris mimics
photoacclimation because growth at low temperature
induces a comparable energy imbalance or excitation
pressure as growth at high light. Why does this occur?
Unlike wheat, rye, and Arabidopsis, Chlorella vulgaris
is unable to up-regulate photosynthetic capacity
during cold acclimation when measured on a per-cell
basis. Low growth temperature reduces the rate of
intersystem electron transport as well as enzyme activity
involved in carbon metabolism without affecting light
absorption, and energy transfer from LHCII to P680
and its subsequent photooxidation to P680+. Under
these conditions, PQH2 accumulates because PSII
reduces the PQ pool faster than PSI and ultimately
CO2 assimilation can oxidize this pool. Concomitantly,
this chloroplast redox signal represses Lhcb gene
expression by retrograde regulation (Figure 14.10).
The cyanobacterium, Plectonema boryanum, also shows
a similar phenotypic response to growth at either low
temperature or high light as Chlorella vulgaris. However,
the cyanobacterium responds by decreasing the size of
its phycobilisome associated with PSII (Chapter 7).
The discussion above illustrates the remarkable
plasticity with which photoautrophs respond to energy
imbalances as a consequence of growth at either high
light or low temperature. Although low temperature
and high light cause a similar imbalance in cellular
energy budget, the response of photoautrophs to energy
imbalance or excitation pressure is species dependent.
It appears that many terrestrial cold-tolerant plants can
attain photostasis by combining an up-regulation of photosynthetic capacity and increased growth rates to utilize
absorbed light energy with photoprotection through
xanthophyll cycle activity. In contrast, many green algae
attain photostasis by reducing light-harvesting efficiency
by making a smaller light-harvesting complex through
retrograde regulation due to their inability to utilize
the absorbed energy through