2. The Mitigation of Heat Stress |
By Dr. Anthony E. Hall |
2.1 Mitigation of stress by crop management
2.1.1. Management
methods at sowing.
In
subtropical zones, cool-season annuals such as lettuce may be sown in the late
summer to produce a crop during the fall. The soil can be so hot during the
late summer that it reduces the maximum germination that is achieved.
Germination of lettuce seed can be inhibited by temperatures of 250
to 330C occurring during a short period of 7 to 12 hours after the
seed has begun to imbibe water. The incomplete emergence problem can be
overcome by sowing the lettuce seed into dry beds during the day and then
sprinkle irrigating the beds during the late afternoon. Sprinkling cools the
soil in the seed zone by evaporation, and the seeds imbibe water during the
cool conditions of the evening and night enabling most of them to germinate.
Another potential solution to this problem is “seed priming” which involves
placing the seed in an osmotic solution for several days at moderate
temperatures and then drying them. During the priming the seed goes through the
initial temperature-sensitive stages of germination with the osmoticum reducing
water uptake and preventing radical emergence. Primed seed also has some
disadvantages in that it often has a shorter shelf life and is more expensive
than normal seed.
In tropical zones, inadequate plant
emergence and establishment can limit the productivity of several warm-season
annual crops. The soil surface can become very hot. For crops with small seed
that are sown shallow, such as sorghum and pearl millet, seed zone temperatures
can exceed 450C in some cases and substantially reduce emergence
independently of drought effects. Hot soils retard hypocotyl elongation of
cowpea and this can have a detrimental effect on emergence, which is aggravated
by deep sowing of seeds. Consequently, when soils are hot, seed of cowpea must
be sown at a depth that is neither too deep and thus constrain hypocotyl
emergence nor too shallow and be too close to the very hot surface.
2.1.2. Choice of
sowing date.
In
temperate or subtropical climatic zones, which have seasonal variations in
temperature, sowing date can be varied to increase the probability that annual
crop species will escape stressfully high temperatures during subsequent
sensitive stages of development. For example, sowing dates can be chosen so
that reproductive stages that are particularly sensitive to heat do not occur
during periods when stressfully hot weather is most likely to occur. In some
subtropical zones the weather can be chilling in early spring and become
progressively warmer reaching very hot conditions in the middle of the summer.
In these zones warm-season annuals, such as cotton, cowpea and maize that are
sown earlier in the spring tend to flower earlier and have a higher probability
of escaping hot summer weather during heat-sensitive stages of reproductive
development. The earliest dates that sowing should be done depends on the
extent of chilling tolerance during germination and emergence of the species
and cultivar. Genotypic differences in chilling tolerance during emergence have
been detected in cowpea. The chilling tolerance was associated with a dominant
effect due to the presence of a specific dehydrin protein in the seed and an
independent and additive effective associated with slow electrolyte leakage
from seed under chilling conditions (Ismail et al. 1997, 1999). Our subsequent
research demonstrated that it is possible to combine chilling tolerance during
emergence with heat tolerance during reproductive development in cowpea using
conventional hybridization.
2.1.3. Cultivars,
irrigation and other management methods.
Perennial
crop species and cultivars should be chosen that are adapted to the high
temperatures likely to occur in the specific location. For both perennial and
annual crop species, a degree of escape of high leaf temperatures can be
achieved by insuring that maximum transpiration rates are maintained since
evaporative cooling can result in leaf temperatures being up to about 80C
cooler for rapidly transpiring plants compared with slowly transpiring plants.
Plants transpire at maximum rates if their root zones have high levels of soil
water and adequate aeration.
High temperature and intense direct
solar radiation can cause damage to fruit (e.g.
citrus or tomato) and reduce their marketing quality. This can be avoided if
fruit is shaded by foliage. Extent of fruit shading by leaves can be
manipulated by the choice of cultivars, irrigation methods and fertilizer
management methods, and plant training and pruning procedures. Damage to tree
trunk cambium by high temperatures can be avoided by spraying the bark of
exposed trunks and branches with a reflective white coating.
2.2. The Mitigation of Heat Stress by Plant
Resistance
2.2.1. The Nature of Resistance to Heat.
Genetic
resistance to heat is defined as where a genotype is more productive than
another genotype in environments where heat stress occurs. This should be
distinguished from heat tolerance, which is defined as the relative performance
of a plant or plant process under heat compared with performance under optimal
temperature. Resistance to heat is more relevant to the needs of farmers than
heat tolerance, whereas heat tolerance often is of interest to scientists
studying mechanisms of adaptation.
Fischer and Maurer (1978)
partitioned stress effects on yield (Y) into parameters measuring sensitivity
to stress (S) and the extent of the stress (D) and yield potential (Yp
).
Y
= Yp (1 - S x D)
Where D = (1 - X/Xp) and
X and Xp are the mean yields of all cultivars under stressed and
optimal conditions, respectively. Algebraic manipulation shows that:
S
= (1 - Y/Yp)/D = (Yp - Y)/(Yp x D)
Since
D is constant for a particular trial, S is a measure of the yield decrease due
to the stress relative to the potential yield with a low value of S being
desirable. Thus S is the inverse of heat tolerance.
The problem with using S as a
measure of adaptation to the stress is that there are cases where S has been
positively correlated with Yp in that cultivars whose yield was
affected little by the stress also had very low yield potential. This means
that the cultivars with low S also may have had low stress resistance (Y) and
would not be useful for farmers. The correlation between S and Yp
also indicates that it may not be possible or easy to combine the desirable
features associated with a low S and high yield potential. However, there may
be cases where the desirable features associated with low S can be combined
with high yield potential. I will provide two examples to show where low S in a
genotype may or may not be useful for breeding.
Many landraces of cereals and grain
legumes are competitive and have substantial leaf area and photosynthetic
source capability but produce relatively few seed in all environments. An
example of this is the guineense
sorghums that may be found in
In contrast, consider cases where
heat stress mainly damages reproductive development and particular genotypes
tolerate this stress. The stress-tolerant genotypes would have a low S value
that may be independent of traits conferring yield potential, such that
combining both sets of traits can increase heat resistance. This has been the
case with breeding heat-resistant cowpea cultivars using reproductive-stage
heat tolerance that is described in the next section. Consequently, the heat
sensitivity index S and various heat-tolerance traits must be used with
caution, especially for cases where genotypic values for S are positively
correlated with yield potential and S depends on traits that influence yield
potential.
Greater heat tolerance is defined as
being where a specific plant process is damaged less by high tissue temperature
and can involve constitutive effects or require acclimation. Tolerance to high
soil temperatures during seed germination would appear to require constitutive
genetic effects; although the mother-plant environment during seed development
and maturation also can influence the heat tolerance of seed during
germination. Tolerance to high tissue temperatures during plant emergence and
early seedling growth involves both constitutive and acclimation effects.
Seedlings subjected to moderately high temperatures synthesize a novel set of
proteins that have been called heat-shock proteins, and the plants become more
tolerant, in terms of plant survival, to more extreme temperatures (Vierling
1991). These proteins are thought to enable cells to survive the harmful
effects of heat by two general types of mechanisms: as molecular chaperones,
and by targeting proteins for degradation. As an example of chaperone activity,
it has been shown that a specific small heat-shock protein cooperates with
other heat-shock proteins to reactivate a heat-denatured protein (Lee and
Vierling 2000). Heat-shock proteins do not appear to be the only mechanism
whereby plants differ in heat tolerance. For example, genotypes of cowpea have
been bred that have substantial differences in heat tolerance during
reproductive development but they produced the same set of heat-shock proteins
in their leaves when subjected to moderately high temperatures.
For crops that produce fruit and/or
seed, including cereals and grain legumes, it is useful to examine whether high
temperatures damage the photosynthetic source more than the reproductive sink.
In essence we are asking which of these processes is more limiting under hot
conditions because enhancing the heat tolerance of this process could increase
resistance to heat. Recall that a heat-resistant cultivar is defined as one
that has higher productivity than other cultivars when grown in environments
where heat stress occurs.
Photosynthetic sources and
reproductive sinks, however, may not always be independent factors in adaptation.
For spring wheat growing in hot irrigated environments, cultivar differences in
grain yield have been positively associated with photosynthetic carbon dioxide
fixation rate (Reynolds et al. 1994). Even stronger positive associations were
observed between grain yield and stomatal conductance suggesting that more open
stomata may be responsible for the higher photosynthetic rates through
facilitating the diffusion of carbon dioxide into leaves and reducing leaf
temperature bringing it closer to the optimum for photosynthesis. Also,
cultivar differences in grain yield of spring wheat growing in a hot irrigated
environment have been positively correlated with kernel number per spike
(Shpiler and Blum 1991). Processes that determine kernel number per spike may
be linked to photosynthesis. Fischer (1985) established that wheat cultivar
variation in kernels per m2 was positively correlated with spike dry
weight at anthesis and the ratio of solar radiation to temperature for the
30-day period prior to anthesis. Consequently, heat stress effects on
photosynthesis can reduce both the photosynthetic source and the magnitude of
the reproductive sink making it difficult to determine overall effects on the
ratio of the photosynthetic source to the reproductive sink.
Also, photosynthetic capacity and
stomatal behavior may be influenced by the extent of the reproductive sink for
photosynthate through complex long-term feedback effects. For example, Pima
cotton cultivars with greater boll yields under hot irrigated conditions also
have higher stomatal conductance and greater carbon dioxide assimilation rates
(Cornish et al. 1991, Lu et al. 1994, 1998). Plants that have higher
photosynthetic capacity often have higher maximal stomatal conductance and the
mechanism for this long-term regulation is unknown (Hall 2001). Explanations
for the mechanisms whereby the Pima cottons are heat resistant are complex. The
heat-resistant cotton cultivars were bred by selecting for ability to set more
bolls on lower nodes under hot, irrigated conditions and not for stomatal or
photosynthetic properties (reviewed by Hall 1992). Possible causes for the
higher photosynthetic rates of the heat-resistant cotton cultivars include the
following. More open stomata enhance the diffusion of carbon dioxide into the
leaves. Cooler leaves operate closer to the optimum for photosynthesis. Slower
senescence of leaves could enhance photosynthesis. Positive feedback effects on
stomata or components of leaf photosynthesis may occur due to the stronger sink
strength that results from the increased fruiting.
|
Fig.3. Plant production of heat susceptible
lines of cowpea in different fields with contrasting thermal regimes (data
from Ismail and Hall, 1998). |
The sensitivity of photosynthesis
and photosystem II to heat may be due to detrimental effects of high
temperature on chloroplast membranes. Murukami et al. (2000) developed
transgenic tobacco plants with altered chloroplast membranes by silencing the
gene encoding chloroplast omega-3 fatty acid desaturase. The transgenic plants
had less trienoic fatty acids and more dienoic fatty acids in their
chloroplasts than the wild type. The transgenic plants also had greater
photosynthesis and grew better than wild-type plants in hot but highly
artificial environments. The studies are preliminary in that rigorous tests
would include evaluating responses of the transgenic and wild type plants in
more natural hot environments and determining the whole-plant mechanisms of any
effects on photosynthesis and growth. Highly artificial environments can result
in artifacts that do not occur in nature.
Clones of Irish potato have been
bred with differences in resistance to heat, in terms of tuber yield (reviewed
by Hall 1992). Under hot conditions several processes are inhibited that
influence tuber production: the rate of photosynthesis, induction to tuberize
and tuberization. Controlled-environment studies demonstrated that these
processes are influenced differently by root and shoot temperatures (Reynolds
and Ewing 1989). High soil temperature inhibited tuber development and growth
under either hot or more optimal shoot temperatures. In contrast, high shoot
temperatures caused leaf rolling and accelerated leaf senescence and reduced
the induction to tuberize under either hot or more optimal root-zone
temperatures. This example, illustrates the importance of considering both
root-zone and shoot-zone temperatures when developing techniques for screening
for heat tolerance and developing management methods for hot environments.
When plants growing in pots are
subjected to high air temperatures both the shoot and the roots are subjected
to hot conditions. In contrast, when plants growing in the field are subjected
to high air temperatures, the shoot is subjected to more extreme temperatures
than the root system. In field conditions, temperature of the soil below about
10 cm is buffered, and does not heat up as much or cool down as much as the
air. Consequently, using plants in pots when studying effects of heat stress,
can subject roots to unnaturally high temperatures and generate artifacts.
Management practices can influence
soil temperatures. For example, compare the effects of frequent sprinkler
irrigation and frequent drip irrigation on Irish potato grown on beds in hot
environments. Overhead sprinkling will cool the beds more than will drip
irrigation, and cooler beds may enhance tuber development and growth while
effects on plant water status may be similar for the two systems of management.
For cowpea, high temperatures have
greater detrimental effects on reproductive development and grain yield than
they do on biomass production (Fig.3) and presumably photosynthesis.
Consequently, breeding to enhance heat tolerance during reproductive
development could enhance heat resistance. Cowpea genotypes have been
discovered that differ in heat tolerance during reproductive development
(Ehlers and Hall 1996) and genetic studies have elucidated the inheritance of
this complex trait. Heat-tolerance during early floral bud development and ability
to produce flowers was shown to be consistent with the effect of a single
recessive gene and have very high heritability (Hall 1993). In contrast,
heat-tolerance during pod set in cowpea was shown to be consistent with the
effect of a single dominant gene but with strong environmental effects and low
narrow-sense and realized heritabilities of 0.26 (Marfo and Hall 1992). For
some other species, such as tomato, high temperatures may influence several
aspects of reproduction involving both the anther and the stigma and the
inheritance of heat tolerance for fruit set probably is more complex than it is
for cowpea (reviewed by Hall 1992).
Embryo abortion also is a complex
character that is influenced by many stresses, and plant pod-load and age. The
discovery that two cowpea genotypes do not exhibit reductions in number of
seeds per pod under high night temperatures, even with a substantial pod load
(Ehlers and Hall 1998), indicates there may be an opportunity for genetic and
breeding studies of heat tolerance during embryo development. Genetic studies
demonstrated that heat-induced seed coat browning is consistent with the effect
of a single dominant gene that is not linked to the gene conferring heat
tolerance during floral bud development (Patel and Hall 1988).
Heat tolerance during reproductive
development of cowpea is consistent with the presence of a set of genes that
operate in the following developmental sequence. They determine the number of floral
buds that develop and produce flowers, the number of these flowers that produce
pods, the number of embryos that develop and produce seed, and the quality of
the seed that are produced.
Several reproductive processes are
particularly sensitive to high night temperatures but some may be sensitive to
or aggravated by high day temperatures. In addition, for cowpea, there were
greater effects of heat stress on both flower production and pod set under long
days compared with short days. This indicates that heat stress may be more
damaging to cowpea in subtropical than tropical zones and this has been
confirmed in both glasshouse studies (Ehlers and Hall 1998) and field studies.
In some cases, plant breeding can be
used to counteract the detrimental heat-induced acceleration of reproductive
development. For indeterminate crops, such as most grain legume cultivars,
cotton and tomato, the length of the reproductive period can be changed by
modifying plant habit and the progression of production of vegetative nodes,
branches and reproductive nodes. For example, once reproductive buds have been
initiated, a few cowpea genotypes have the ability to produce more vegetative
nodes on the main stem alternating with reproductive nodes (Ehlers and Hall
1996). This trait slows down overall reproductive development and may be
advantageous in tropical environments with high night temperature.
For determinate crops, such as rice,
sorghum and wheat, the progression of vegetative and reproductive structures is
not very plastic and the rapid reproductive development caused by high night
temperatures substantially reduces their grain yield potential. Where the
overall reproductive stage is short, the opportunity for the fixation of
photosynthate and its translocation to developing grain also is short. Enhanced
translocation to grain of stored photosynthate fixed prior to anthesis may
provide a heat-tolerance mechanism for determinate crops that are subjected to
heat stress during grain filling. Wheat often experiences heat and drought
stress during grain filling when grown in hotter wheat production zones such as
may be found in
2.2.2. Methods of Breeding for
Resistance to Heat.
The traditional method for breeding
for heat resistance is to grow advanced lines in a hot target production
environment and select those lines that have greater yields than current
cultivars (this provides a direct measure of heat resistance). This approach is
more effective with crop species that can be efficiently yield-tested in small
plots, such as wheat, than crops such as cowpea that require larger plots and
are more difficult to harvest. This direct approach also is more effective in
environments where heat is the only major stress. The presence of other
stresses makes the evaluation of heat resistance very difficult. For example,
insect pests such as lygus bugs and flower thrips can cause damage to
developing flower buds of cowpea that appears similar to the damage caused by
high night temperatures. Some slow progress may have been made in enhancing the
heat resistance of cowpea in
A more efficient approach has been developed for
breeding for heat resistance that involves early generation selection for
specific traits that confer heat tolerance during reproductive development. The
first step in this approach is to discover accessions that have heat-tolerance
traits. When searching for useful accessions, a wide range of materials should
be evaluated including those that evolved or were developed in cool as well as
hot environments. Two cowpea accessions were discovered to have heat tolerance
during reproductive development that came from a hot tropical zone in
|
|
|
Photograph
1. A heat tolerant cowpea 518-2 (right) that is producing many flowers in a
hot field environment where heat sensitive CB65 (left) is producing fewer
flowers. |
Photograph
2. A heat tolerant cowpea line H36 (right) that is abundantly producing pods
in a hot field environment where a heat sensitive line CB5 (left) is
producing few pods. |
Photograph 3. Cowpea lines with similar
genetic background in a hot field environment that either have (right) or do
not have (left) a set of heat tolerant genes. |
For some crop species, methods have
been developed based on selection for heat-tolerance traits in extremely hot
environments that are more effective than selection solely based on yield in hot
target production environments. An example of breeding for resistance to heat
in cowpea is described that has been shown to be very effective. Emphasis was
placed on incorporating heat tolerance during reproductive development. Very
hot field and glasshouse environments were used for screening for
reproductive-stage heat tolerance. The hot field nursery was achieved by sowing
a set of cowpea genotypes that have similar earliness (they initiate floral
buds at the same time) in the Coachella Valley of California during the hot
season. Often sowing was done about the 20th of June and resulted in
an environment where the plants experienced minimum and maximum 24-hour air
temperatures of 230 to 270C and 420 to 500C,
respectively, for the three-week period beginning one week prior to the start
of flowering. In this environment, heat-tolerant day-neutral genotypes begin
flowering about 32 days after sowing. The plants also experience long days
(14.5 hours) and sunny skies, and are subjected to optimal irrigation,
fertilizer application and pest management practices. Plants are selected that
produce many early flowers, and have high pod set producing about four pods per
peduncle on the first five reproductive nodes on the main stem, well-filled
pods and adequate grain quality. In most years many plants can be effectively
screened using this field nursery.
Most parts of the world do not have
field nurseries with the consistently high night temperatures but otherwise
optimal conditions experienced in
Diverse sets of several hundred
early flowering day-neutral cowpea accessions have been screened and three were
detected with ability to produce flowers and set pods under hot conditions in
the field. The heat-tolerant accessions have many undesirable agronomic traits
so it was necessary to cross them with commercial cultivars. We have shown that
heat tolerance during early flower development can be incorporated and virtually
fixed by a single selection for ability to produce flowers in the F2
or a subsequent generation, consistent with it being conferred by a single
recessive gene with high heritability. During the F2 generation, we
select plants that produce many flowers and have high pod set and adequate
numbers of seeds per pod and seed size and no heat-induced seed coat browning
(Photograph 1).
We only can directly screen for heat
tolerance under long days in the summer so we have used the fall and winter
seasons to advance generations once or twice in an optimal-temperature
glasshouse using single-seed or single-plant decent. During the summer we then
screen the F4 or F5 lines for heat tolerance. Most of the
lines that were selected during the F2 generation have heat
tolerance during early flower development in subsequent generations and produce
many flowers. In the advanced generations, we emphasize selecting lines and
then single plants with uniformly high pod set, adequate numbers of seeds per
pod and seed size, and no seed coat browning (Photograph 2).
At least two cycles of family
selection are needed to incorporate heat tolerance during pod set, which is
consistent with it having dominant gene inheritance and a low heritability.
Six pairs of lines were developed
(for example Photographs 2 and 3) that either have or do not have a set of
heat-tolerance genes in similar genetic backgrounds. These pairs of lines were
evaluated in eight field environments with average night temperatures ranging
from cool to very hot but otherwise similar near optimal conditions (Ismail and
Hall 1998). The heat-susceptible lines, which included a commercial cultivar,
exhibited a 13.5 % decrease in grain yield per 0C increase in
average minimum night temperature above 16.50C for the three week
period starting one week prior to first flowering (Fig.3). The heat-tolerant
lines had similar grain yields under cooler night temperatures but 50 % greater
grain yield and numbers of pods per peduncle than the heat-susceptible lines
with average minimum night temperatures of 210C (Fig.4).
Minimum night temperatures greater
than 210C occur in several commercial production zones (Nielsen and
Hall 1985a). Advanced lines are then evaluated in multi-location trials
conducted in commercial fields and experiment stations in the target production
environment. Lines are selected that have consistently high yield, adequate
grain quality and other agronomic traits such as resistance to lodging. One of
the heat-tolerant lines from the study of Ismail and Hall (1998) that performed
well in the multi-location trials now has been released as the cowpea cultivar
“California Blackeye 27" (Ehlers et al. 2000). It should be noted that
heat tolerance by itself will not justify release of a new cultivar, the cultivar
must have greater grain yield than current cultivars when grown in the target
production environment (i.e. greater heat resistance is needed). Farmers often
only will accept a new cultivar that has been shown to substantially enhance
yields or profits. “California Blackeye 27" has greater grain yields when
conditions are hot at flowering and it also has greater grain yields in some
fields due to it having greater resistance to specific pests and diseases than
the older cultivars (Ehlers et al. 2000).
When breeding to incorporate heat
tolerance or any other trait it is important to evaluate potential negative
effects of the trait. In hot and also more moderate temperature environments,
the reproductive-stage heat-tolerance genes cause cowpea to be more compact and
dwarfed due to their internodes being shorter. At a minimum night temperature
of 180C, the heat-susceptible cowpea lines had 50 % longer main
stems, and at 220C they had 50 % more vegetative biomass than the heat-tolerant
lines ( Fig.5 and Photographs 1, 2 and 3).
|
|
Fig.4. Relative plant
production of heat-susceptible and heat tolerant pairs of cowpea lines grown
in different fields with contrasting thermal regimes (data from Ismail and
Hall, 1998). |
Fig.5.
Relative plant height and vegetative biomass of heat-tolerant and
heat-susceptible pairs of cowpea lines grown in different fields with
contrasting hermal regimes. |
Heat-tolerant
semidwarf cowpea lines were compared with standard-height cowpea cultivars under
different row spacing (Ismail and Hall 2000). Heat-tolerant semidwarf cowpea
lines were less effective than standard-height cultivars at the wide row
spacing of 102 cm used by some farmers, more effective with the widely used 76
cm row spacing, and even more effective with a narrow row spacing of 51 cm than
standard-height cultivars. Natural selection likely would not favor this type
of heat tolerance in that plants with the compact plant habit are not very
competitive. In tomato, cultivars with heat-tolerance during reproductive
development may tend to be more compact and exhibit less coverage of fruit by
leaves, which can enhance damage to the fruit surface and internal tissues
caused by excessive solar radiation and temperature. The compactness of the
heat-resistant cowpea and tomato cultivars may be due to their greater and
earlier partitioning of carbohydrate to fruits, which thereby restricts their
vegetative growth compared with heat-susceptible cultivars. The heat-tolerance
gene that enhances pod set in cowpea appears to have major effects on plant
development.
Screening for the extent of
flowering and fruit set in hot conditions can be effective with several crop
species, including several grain legumes, tomato and cotton, but some breeders
do not have suitable very hot field environments, and hot glasshouse screening
can be expensive. Consequently, scientists have tried to develop more efficient
indirect screening procedures.
Considerable research effort has
been devoted to using slow electrolyte leakage from leaf disks that have been
subject to high temperatures as an indication of cell membrane thermostability
(MT, or CMS) and heat tolerance (reviewed by Blum 1988 and Hall 1992).
The yield-forming processes that are
linked with MT have not been clearly identified. However, for spring and winter
wheat, MT was associated with heat tolerance during grain filling (Shanahan et
al. 1990, Saadala et al. 1990a, Reynolds et al. 1994) and it may -be possible
to obtain useful data from seedling screens (Saadala et al. 1990b). Seedling
screens can be very effective because many plants can be screened and selected
plants can be crossed.
Positive associations between MT and
grain yield under heat stress have been reported for two spring wheat
populations (Blum et al. 2001). One population consisted of 98 F8
random recombinant inbred lines (RILs) between a heat-resistant cultivar,
Danbata, and a heat-sensitive cultivar, Nacozari. Grain yield was measured for
plants growing in the summer at Bet Dagan in
There has been some work on MT for
enhancing heat tolerance of other crops (Blum 1988, Hall 1992). For cowpea,
electrolyte leakage of leaf disks was negatively associated with
reproductive-stage heat tolerance (Ismail and Hall 1999). Subsequent genetic
selection experiments by Thiaw and Hall (2004) confirmed that leaf electrolyte
leakage under heat stress was negatively correlated with heat tolerance for pod
set in cowpea. The leaf-electrolyte-leakage (LEL) protocol that he used
consisted of subjecting leaf discs to 46oC for 6 hours in aerated
water and then measuring electrical conductivity of the solution followed by
boiling the leaf discs and then measuring the electrical conductivity of the
solution again. The percentage leakage during heat stress was calculated from
the two measurements. Blum (1988) and others have proposed that plants should
be heat-hardened prior to sampling tissue, and four measurements of electrolyte
leakage are used in calculating MT. Heat-hardening does not appear to be necessary
for cowpea in that Thiaw and Hall (2004) and Ismail and Hall (1999) observed
useful genotypic differences in LEL with plants grown in a range of different
environments. An advantage of the LEL method used by Thiaw (2003) over the MT
method used by Blum et al. (2001) is that samples for the LEL method can be
taken from plants growing in any field nursery or glasshouse, without the need
for acclimating plants. Also, only two measurements of electrolyte leakage are
needed with the LEL method so that more plants can be evaluated than with the
MT method, which requires four measurements.
Thiaw and hall (2004) selected four
populations from the same cross between heat-resistant and heat-susceptible
parents that have similar genetic background: those with slow LEL and those
with fast LEL, and those with high pod set in hot conditions and those with low
pod set in hot conditions. The association between pod set and LEL was strong
in that lines selected for slow LEL had high pod set, and lines selected for
high pod set had slow LEL. The realized heritability when using slow LEL to
indirectly select for heat tolerance during pod set was significantly greater
than zero but small, similar to the realized heritability for direct selection
for pod set of 0.26 observed by Marfo and Hall (1992). The LEL protocol we used
has an advantage over direct selection in that it can be conducted in the off
season with plants grown in moderate temperatures. We now propose an improved
method for breeding heat-resistant cowpeas. This method consists of direct
selection for abundant flowering and pod set in very hot summer field nurseries
or glasshouses, followed by indirect selection using slow LEL in the fall and
winter with plants grown under moderate temperatures in greenhouses.
Heat tolerance in spring wheat and
Pima cotton has been associated with greater stomatal conductance, which can be
rapidly detected in plots by a low canopy temperature compared with air
temperature using an infrared
thermometer (Reynolds et al 1994, Lu et al. 1994 and 1998).
However, key tests have not yet been reported for any species that demonstrate
whether selecting in segregating populations based on canopy temperature
differences confers some heat resistance. Since measurement of canopy
temperature differences requires plots of similar genotypes it could only be
practiced in relatively advanced generations. This is unfortunate because much
progress can be made if selection can be effectively initiated in the first
segregating generation using single plants. Also the genotypic differences in
canopy temperature that have been reported are relatively small in relation to
the errors encountered in these data. This approach probably may not be
effective with grain legumes that exhibit diurnal leaf movements because this
can increase errors due to the sensor detecting the far infrared radiation
emitted from the soil surface. In addition there are theoretical limits to the
extent that stomatal conductance can be increased by selection and enhance crop
performance.
For crops where the limiting effect
of heat stress involves damage to photosynthesis there is some merit in trying
measurements of chlorophyll fluorescence as an indicator of damage
to photosystem II. Equipment is available that permits rapid field measurement
of the Fv/Fm parameter which provides an estimate of the
damage to photosystem II. For this approach, also, key tests have not yet been
reported for any species that demonstrate whether selection based on
chlorophyll fluorescence is effective in enhancing heat resistance. It should
be noted that when determining whether a selection method is effective it also
is necessary to determine the efficiency of the method: the costs of the
selection procedure in relation to the gains that are made compared with other
selection procedures.
In extreme conditions,
heat-resistance may depend upon the ability of plants to survive hot
environments. The maximum emergence of sorghum and pearl millet seedlings can
be substantially reduced by hot soil conditions in tropical
In plant breeding it is necessary to
take a long term view and consider the environmental and socio-economic
conditions likely to be present in future years (Hall and Ziska 2000). Climatic
conditions are changing, such as the progressive increases in atmospheric
carbon dioxide concentration that are occurring everywhere and will tend to
make photosynthesis of C3 plants more effective. Plant
photosynthetic systems may require modifications through plant breeding so that
they can take full advantage of the elevated atmospheric [CO2]. Also,
maintaining a balance between carbohydrate sources and sinks could require
selecting plants with greater reproductive sinks (Hall and Ziska 2000).
Breeding to maintain a balance will be particularly important for environments
and species where stresses, such as high temperatures, cause greater damage to
the reproductive sink than the photosynthetic source. The genes for
reproductive-stage heat tolerance in cowpea enhance sink strength and harvest
index (Ismail and Hall 1998, 2000). Studies in controlled environments indicate
these heat-tolerance genes may also enhance responsiveness to elevated
atmospheric [CO2] under moderate as well as high night temperatures
(Ahmed et al. 1993a).
Advances in biotechnology may make
possible some new approaches for breeding for heat resistance. Apomixis
could provide resistance to stresses, such as heat, that damage reproductive
development, since the seed are produced from maternal tissues and do not require
meiosis or fertilization. A type of apomixis would be needed that does not
require fertilization of polar nuclei for endosperm development. Through
genetic engineering it may be possible to insert the cassette of genes needed
to confer facultative apomixis (
The literature contains relatively
little information on breeding for heat resistance. Some commercial companies
have been active in this area but have not published their results. This is
unfortunate since their experience with breeding for heat resistance could
guide future breeders. Many advanced institutions are located in temperate
zones where resistance to cold is more important than resistance to heat. Also,
the limited research on heat tolerance conducted in these advanced institutions
often has emphasized heat-shock proteins but has not yet led to any methods for
breeding for resistance to heat that is based on this information. Breeding for
resistance to heat deserves a higher priority than it has been given in the
past.
Ahmed, F. E. and A. E. Hall. 1993.
Heat injury during early floral bud development in cowpea. Crop Sci. 33:
764-767.
Ahmed, F. E., A. E. Hall and D. A.
DeMason. 1992. Heat injury during floral development in cowpea (VIGNA
UNGUICULATA, FABACEAE). Amer. J. Bot.
79:784-791.
Ahmed, F. E., A. E. Hall and M. A.
Madore. 1993a. Interactive effects of high temperature and elevated carbon
dioxide concentration on cowpea (Vigna
unguiculata (L.) Walp.). Plant, Cell Environ.
16: 835-842.
Ahmed F. E., R. G. Mutters and A. E.
Hall. 1993b. Interactive effects of high temperature and light quality on
floral bud development in cowpea. Austral.
J. Plant Physiol. 20: 661-667.
Al-Khatib, K. and G. M. Paulsen.
1999. High-temperature effects on photosynthetic processes in temperate and
tropical cereals. Crop Sci. 39: 119-125.
Blum, A. 1988. Plant Breeding for
Stress Environments. CRC Press, Inc.,
Blum, A., N. Klueva and H. T.
Nguyen. 2001. Wheat cellular thermotolerance is related to yield under heat
stress. Euphytica 117: 117-123.
Cornish, K., J. W. Radin, E. L.
Turcotte, Z. Lu and E. Zeiger. 1991. Enhanced photosynthesis and stomatal
conductance of pima cotton (Gossypium barbadense L.) bred for increased yield.
Plant Physiol. 97: 484-489.
Ehlers, J. D. and A. E. Hall. 1996.
Genotypic classification of cowpea based on responses to heat and photoperiod.
Crop Sci. 36: 673-679.
Ehlers, J. D. and A. E. Hall. 1998.
Heat tolerance of contrasting cowpea lines in short and long days. Field Crops
Res. 55: 11-21.
Ehlers, J. D., A. E. Hall, P. N.
Patel, P. A. Roberts and W.C. Matthews. 2000. Registration of ‘
Fischer, R. A. 1985. Number of
kernels in wheat crops and the influence of solar radiation and temperature. J.
Agric. Sci. Camb. 105: 447-461.
Fischer, R. A. and R. Maurer. 1978.
Drought resistance in spring wheat cultivars. I. Grain yield responses. Austr. J. Agric. Res. 29: 897-912.
Hall, A. E. 1992. Breeding for heat
tolerance. Plant Breed. Rev. 10:
129-168.
Hall, A. E. 1993. Physiology and
breeding for heat tolerance in cowpea, and comparison with other crops. Pp.
271-284, in C. G. Kuo (ed.)
Adaptation of Food Crops to Temperature and Water Stress, Publ. No. 93-410,
Asian Vegetable Research and Development Center, Shanhua, Taiwan.
Hall, A. E. 2001. Crop Responses to
Environment. CRC Press LLC,
Hall, A. E. and L. H. Ziska. 2000.
Crop breeding strategies for the 21st century. Pp. 407-423 in K. R. Reddy and H. F. Hodges (eds.)
Climate Change and Global Crop Productivity, CABI Publishing, New York, USA.
Hall, A. E., B. B. Singh and J. D.
Ehlers. 1997. Cowpea breeding. Plant
Breed. Rev. 15: 215-274.
Ismail, A. M. and A. E. Hall. 1998.
Positive and negative effects of heat-tolerance genes in cowpea. Crop Sci. 38: 381-390.
Ismail, A. M. and A. E. Hall. 1999.
Reproductive-stage heat tolerance, leaf membrane thermostability and plant
morphology in cowpea. Crop Sci. 39:
1762-1768.
Ismail, A. M. and A. E. Hall. 2000.
Semidwarf and standard-height cowpea responses to row spacing in different
environments. Crop Sci. 40:
1618-1623.
Ismail, A. M., A. E. Hall and T. J.
Close. 1997. Chilling tolerance during emergence of cowpea associated with a
dehydrin and slow electrolyte leakage. Crop
Sci. 37: 1270-1277.
Ismail, A. M., A. E. Hall and T. J.
Close. 1999. Allelic variation of a dehydrin gene cosegregates with chilling
tolerance during seedling emergence. PNAS
96: 13566-13570.
Jefferson, R. A. 1993. Beyond model
systems - new strategies, methods and mechanisms for agricultural research. Ann.
Lee, G. J. and E. Vierling. 2000. A
small heat shock protein cooperates with heat shock protein 70 systems to
reactivate a heat-denatured protein. Plant
Physiol. 122: 189-197.
Lu, Z., R. G. Pearcy, C. O. Qualset
and E. Zeiger. 1998. Stomatal conductance predicts yields in irrigated Pima
cotton and bread wheat grown at high temperatures. J. Exp. Bot. 49: 453-460.
Lu, Z., J. W. Radin, E. L. Turcotte,
R. Percy and E. Zeiger. 1994. High yields in advanced lines of Pima cotton are
associated with higher stomatal conductance, reduced leaf area and lower leaf
temperature. Physiol. Plant. 92:
266-272.
Marfo, K. O. and A. E. Hall. 1992.
Inheritance of heat tolerance during pod set in cowpea. Crop Sci. 32: 912-918.
Murakami, Y., Tsuyama, M.,
Kobayashi, Y., Kodama, H. and K. Iba. 2000. Trienoic fatty acids and plant
tolerance of high temperature. Science
287: 476-479.
Mutters, R. G. and A. E. Hall. 1992.
Reproductive responses of cowpea to high temperature during different night
periods. Crop Sci. 32: 202-206.
Mutters, R. G., L. G. R. Ferreira
and A. E. Hall. 1989a. Proline content of the anthers and pollen of heat-tolerant
and heat-sensitive cowpea subjected to different temperatures. Crop Sci. 29: 1497-1500.
Mutters, R. G., A. E. Hall and P. N.
Patel. 1989b. Photoperiod and light quality effects on cowpea floral
development at high temperatures. Crop
Sci. 29: 1501-1505.
Nielsen, C. L. and A. E. Hall.
1985a. Responses of cowpea (Vigna
unguiculata [L.] Walp.) in the field to high night temperature during
flowering. I. Thermal regimes of production regions and field experimental
system. Field Crops Res. 10: 167-179.
Nielsen, C. L. and A. E. Hall.
1985b. Responses of cowpea (Vigna
unguiculata [L.] Walp.) in the field to high night temperatures during
flowering. II. Plant responses. Field
Crop Res.10: 181-196.
Patel, P. N. and A. E. Hall. 1988.
Inheritance of heat-induced brown discoloration in seed coats of cowpea. Crop Sci. 28: 929-932.
Reynolds, M. P. and E. E. Ewing.
1989. Effects of high air and soil temperature stress on growth and
tuberization in Solanum tuberosum. Annals Bot. 64: 241-247.
Reynolds, M. P., M. Balota, M. I. B.
Delgado,
Saadala, M. M., J. S. Quick and J.
F. Shanahan. 1990a. Heat tolerance in winter wheat. II. Membrane
thermostability and field performance. Crop
Sci. 30: 1248-1252.
Saadala, M. M., J. F. Shanahan and
J. S. Quick. 1990b. Heat tolerance in winter wheat. I. Hardening and genetic
effects on membrane thermostability. Crop
Sci. 30: 1243-1247.
Shanahan, J. F.,
Shpiler, L. and A.
Blum. 1991. Heat tolerance for yield and its components in different wheat
cultivars. Euphytica 51: 257-263.
Soman, P. and J. M. Peacock. 1985. A
laboratory technique to screen seedling emergence of sorghum and pearl millet
at high soil temperature. Expl. Agric. 21: 335-341.
Thiaw, S. 2003. Association between
slow leaf-electrolyte-leakage under heat stress and heat tolerance during
reproductive development in cowpea. Ph.D. Dissertation,
Thiaw, Samba and Anthony E. Hall.
2004. Comparison of selection for either leaf-electrolyte-leakage or pod set in
enhancing heat tolerance and grain yield of cowpea. Field Crops Res.86:
239-253.
Vierling, E. 1991. The roles of heat
shock proteins in plants. Ann. Rev. Plant Physiology Plant Mol. Biol. 42:
579-620.
Warrag, M. O. A. and A. E. Hall.
1983. Reproductive responses of cowpea to heat stress: genotypic differences in
tolerance to heat at flowering. Crop Sci. 23: 1088-1092.
Warrag, M. O. A. and A. E. Hall.
1984a. Reproductive responses of cowpea [Vigna
unguiculata (L.) Walp.] to heat stress. I. Responses to soil and day air
temperatures. Field Crops Res. 8:
3-16.
Warrag, M. O. A. and A. E. Hall.
1984b. Reproductive responses of cowpea [Vigna
unguiculata (L.) Walp.] to heat stress. II. Responses to night air
temperatures. Field Crops Res. 8:
17-33.