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1. Heat Stress and its Impact |
By
Dr. Anthony E. Hall |
1.1 The environmental and physiological nature of
heat stress
Heat
stress often is defined as where temperatures are hot enough for sufficient
time that they cause irreversible
damage to plant function or development. In addition, high temperatures can
increase the rate of reproductive development, which shortens the time for
photosynthesis to contribute to fruit or seed production. I also will consider
this as a heat-stress effect even though it may not cause permanent (irreversible) damage to development
because the acceleration does substantially reduce total fruit or grain yield.
The
extent to which heat stress occurs in specific climatic zones is a complex
issue. Plants can be damaged in different ways by either high day or high night
temperatures and by either high air or high soil temperatures. Also, crop
species and cultivars differ in their sensitivity to high temperatures.
Cool-season annual species are more sensitive to hot weather than warm-season
annuals. In Table 1 there are several examples of cool-season and warm-season
annual crop species. I did not include safflower in the table because it is
unusual in that during the vegetative stage it grows well in cool conditions
and during the reproductive stage it grows well in hot conditions.
Table 1. Annual crop species adapted to cool and
warm seasons (Hall 2001).
|
Cool-season
annuals |
Warm-season
annuals |
|
Barley, brassicas,
canola, fava bean, flax, garbanzo bean, Irish potato, lentil, lettuce,
lupine, mustard, oat, pea, radish, rye, spinach, triticale, turnip, vetch,
wheat |
common
bean, cotton, cowpea, cucurbits , finger millet, grain amaranth, lima bean,
maize, mung bean, pearl millet, pepper, pigeon pea, rice sesame, sorghum,
soybean, sunflower, sweet potato, tobacco, tomato |
High
day temperatures can have direct damaging effects associated with hot tissue
temperatures or indirect effects associated with the plant-water-deficits that
can arise due to high evaporative demands. Evaporative demand exhibits near
exponential increases with increases in day-time temperatures and can result in
high transpiration rates and low plant water potentials (Hall 2001). The
effects of drought and plant-water-deficits on crop adaptation are discussed in
the ‘Drought
Stress’ page.
Air
temperatures vary during the day and season. Temperature data from weather
stations for many locations in
The
extent of heat stress that can occur in a specific climatic zone depends on the
probability of high temperatures occurring and their duration during the day or
night. Where global climate change is occurring these probabilities may not be
predicted well based only on historical records for specific locations. Heat
stress is a complex function of intensity (temperature degrees), duration and
rate of increase in temperature. The magnitude of heat stress rapidly increases
as temperature increases above a threshold level and complex acclimation
effects can occur that depend on temperature and other environmental factors.
High
soil temperatures can reduce plant emergence. The maximum threshold
temperatures for germination and emergence are higher for warm-season than for
cool-season annuals. For example, the threshold maximum seed zone temperature
for emergence of cowpea is about 370C compared with 25 to 330C
for lettuce.
During the vegetative stage, high day temperatures can
cause damage to components of leaf photosynthesis, reducing carbon dioxide
assimilation rates compared with environments having more optimal temperatures.
Sensitivity of photosynthesis to heat mainly may be due to damage to components
of photosystem II located in the thylakoid membranes of the chloroplast and
membrane properties (Al-Khatib and Paulsen 1999). Membrane thermostability has been
evaluated by measuring electrolyte leakage from leaf disks subjected to extreme
temperatures (Blum 1988). More stable membranes exhibit slower electrolyte
leakage. Studies comparing responses to heat of contrasting species indicated
that photosystem II of the cool season species, wheat, is more sensitive to
heat than photosystem II of rice and pearl millet, which are warm season
species adapted to much higher temperatures (Al-Khatib and Paulsen 1999).
Extreme
temperatures can cause premature death of plants. Among the cool-season
annuals, pea is very sensitive to high day temperatures with death of the plant
occurring when air temperatures exceed about 350C for sufficient
duration, whereas barley is very heat tolerant, especially during grain
filling. For warm season annuals, cowpea can produce substantial biomass when
growing in one of the hottest crop production environments on earth (maximum
day-time air temperatures in a weather station shelter of about 500C),
although its vegetative development may exhibit abnormalities such as leaf
fasciations. For monocotyledons, including both cool-season and warm-season
annuals, high daytime temperatures can cause leaf firing which involves
necrosis of the leaf tips and this symptom also can be caused by drought.
Reproductive
development of many crop species is damaged by heat such that they produce no
flowers or if they produce flowers they may set no fruit or seeds. The reviews
of Hall (1992, 1993) discuss the detrimental effects of heat stress on
reproductive development that has been reported for cowpea, common bean,
tomato, cotton, rice, wheat, maize and sorghum. I will examine the detrimental
effects of heat stress on cowpea because of the comprehensive information
available for this species and the likelihood that many of the same phenomena
occur with other warm-season crop species.
Controlled-environment
studies in which cowpea plants were subjected to separately controlled root and
shoot and day and night temperatures demonstrated that pod set (the proportion
of flowers producing pods) was damaged by moderately high night temperature of
the shoot (Warrag and Hall 1984a,b). It was surprising that night temperature
would have this effect since much hotter day temperatures did not damage pod
set of cowpea. Reciprocal artificial pollinations between plants grown under
high and optimal night temperatures indicated the low pod set was caused by
male sterility and that the pistils did not appear to be damaged by high night
temperature. The detrimental effects of high night temperature on pod set also
were shown to occur in field conditions (Nielsen and Hall 1985b). In these
experiments a unique experimental approach was used in which plots of cowpea
plants were subjected to different increments of higher night temperatures
during early stages of flowering using enclosure systems placed over the plots
only during the night-time (Nielsen and Hall 1985a).
Possible
mechanisms for the sensitivity of pod set to high night temperatures have been
proposed. Mutters and Hall (1992) demonstrated that there is a distinct period
during the 24-hour cycle when pollen development in cowpea is sensitive to high
night temperatures. Plants subjected to high temperature during the last six
hours of the night exhibited substantially decreased pollen viability and pod
set, whereas plants subjected to high temperature during the first six hours of
a twelve-hour night exhibited no damage. Mutters and Hall (1992) hypothesized
that these results could be explained if a heat-sensitive process in pollen
development is under circadian control and only occurs in the late night
period. Note that if a heat-sensitive process is under circadian control and if
genetic variation exists for the time in the 24-hour cycle when this process
occurs, evolution in hot environments would favor plants in which the
heat-sensitive process occurs at the coolest time which is just prior to dawn.
The damaging effect of high night temperature on pod set was greater in long
days than in short days, and red and far red light treatments indicated it is a
phytochrome-mediated response (Mutters et al. 1989b).
Studies
were conducted in which cowpeas were transferred between growth chambers having
high or optimal night temperatures (Warrag and Hall 1984b; Ahmed et al. 1992).
They demonstrated that the stage of floral development most sensitive to high
night temperature occurs 9 to 7 days prior to anthesis, which is after meiosis
and coincides with release of pollen microspores from the tetrads. Damage due
to high night temperature was associated with premature degeneration of the
tapetal layer that provides nutrients to developing pollen, infertile pollen
and in some genotypes anthers did not dehiscence. The transfer of proline from
the tapetal layer to pollen was inhibited (Mutters et al. 1989a).
Comparisons
of heat-sensitive and heat-tolerant cowpeas showed a genotypic association
between sensitivity to heat during pod set and rapid leakage of electrolytes
from leaf discs subjected to heat stress (Ismail and Hall 1999). Possibly, the
damage to pollen development by high night temperatures may be in some way
associated with a heat-induced malfunction in membrane properties.
Floral
bud development also can be damaged by heat such that plants do not produce
flowers. For cowpea, two weeks or more of consecutive or interrupted hot nights
during the first month after germination caused complete suppression of floral
bud development (Ahmed and Hall 1993). In extreme cases the floral buds become
necrotic and die. In field conditions, the damage occurs under long days but
not under short days. However, responses to red and far red light indicated the
effect was only partially consistent with the system being mediated by
phytochrome (Mutter et al. 1989b). The damaging effect of high night temperature
and long days on floral bud development also depended on light quality whereas
the damaging effect on pod set did not depend on light quality (Ahmed et al.
1993b). When growth chambers were used with relatively large amounts of
fluorescent light and little incandescent light, such that the red/far red
ratio was 1.9, floral buds were not suppressed in long-day high night
temperature conditions, but pod set was very low. This artificial light system
provides a useful experimental method for studying the effects of heat stress
on pod set without complications due to heat stress effects on floral bud
development. When growth chambers were used with lighting systems providing a
red/far red ratio of 1.3 to 1.6, floral bud suppression was observed that was similar
to what is obtained under long-day high night temperature conditions in the
field where sunlight has a red/far red ratio of about 1.2.
There
are two important conclusions from these studies. First, the use of growth
chambers with lighting systems that mainly depend on fluorescent lights can
result in either serious artifacts or methodological advantages when studying
plant reproductive responses to heat stress. Second that intense shading of
floral buds could reduce the red/far red ratio below 1.2 in field conditions
and intensify the floral bud suppression effect. In densely sown fields of
cowpea, individual plants that are suffering from competition and are tall and
spindly can exhibit floral bud suppression even though night temperatures are
not too hot.
Pods
of different cowpea genotypes produce 9 to 20 ovules with many cultivars having
15 ovules, but pods rarely produce these many seeds per pod. Under optimal
conditions two-thirds of the ovules may produce seed, whereas with high day or
high night temperature (Warrag and Hall 1983) and other stresses, such as
drought, fewer seeds are produced per pod. For most cultivars and stresses it
is the ovules at the blossom end of the pod that suffer embryo abortion and do
not produce seed, resulting in the production of “pinched” pods.
Cowpea
seeds produced under high day temperatures can have asymmetrical twisted
cotyledons (Warrag and Hall 1984a). Germination of the seed is not influenced
and this effect of heat stress may not be a major problem for commercial
production. In contrast, heat-induced brown discoloration of cowpea seed coats
can occur with some cultivars and be a major problem causing consumers to
reject grain. Higher night temperatures resulted in progressively larger
numbers of seed with larger areas of brown discoloration on seed coats (Nielsen
and Hall 1985b).
The
extent to which high-temperature damage to photosynthesis or reproductive
development affect fruit or grain yield probably depends on the extent to which
the photosynthetic source and the reproductive sink are limiting fruit or grain
yield, and this may vary among species and cultivars.
Surface
and internal tissues of tomato and citrus fruit can be damaged by the
combination of high temperatures and intense solar radiation. High tissue
temperatures also can damage cambium layers in exposed trunks and branches.
1.2 Repercussions of heat stress
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Fig.1. Days from anthesis to mature dry pod for cowpeas
grown under nighttime temperatures in the same field (Data from Nielsen and
Hall, 1985b) |
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Fig.
2.
Grain yield and % flowers producing pods for cowpeas grown under different
night-time temperatures in the same field (data from Nielsen and Hall 1985b) |
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Fig.3.
Plant production of heat-susceptible cowpea lines grown in different fields
with contrasting thermal regimes (data from Ismail and Hall 1998) (data from Ismail
and Hall 1998)." |
The
reduction in maximal emergence of annual crops due to hot soils can be so
pronounced that yield of the economic product is reduced substantially. This
can be a major problem for crops, such as lettuce, whose canopies are not very
plastic and cannot compensate for the low emergence. Heat stress at emergence
is a major problem for cool-season crops that are sown in the late summer in
hot subtropical zones with the objective of producing a crop during the cooler
weather in the fall. Warm-season crops also can experience this problem in
those tropical zones and seasons where soil temperature can be extremely hot at
sowing.
The
acceleration of reproductive development by high temperatures may partially
explain why the potential grain yields of warm season crops, such as rice and
cowpea, usually are higher in the subtropics than the tropics. The extent of
the acceleration of development of cowpea has been determined (Fig.1) by
subjecting plants to different night temperatures in field conditions using
temporary enclosures imposed only at night with regulated heating systems
(Nielsen and Hall 1985a). Under the cool night temperatures of subtropical
More
rapid pod development may increase the extent of embryo abortion, and
individual seed usually are smaller in tropical compared with subtropical
conditions for the same cowpea cultivar. Cowpeas subjected to elevated
night-temperature treatments produced smaller seed (Nielsen and Hall 1985b).
The more rapid development of individual fruits also results in the overall
reproductive period of the plant being shorter. Grain yields of cowpea
cultivars grown with optimal management are much less in tropical zones than in
subtropical zones mainly due to the shorter overall reproductive period caused
by the hot nights of tropical zones (Hall et al. 1997). Acceleration of
reproductive development also is a problem for cool season crops, such as
wheat, growing in environments that are hot during reproductive development
(reviewed by Hall 1992, 1993).
Direct
evidence for heat-stress effects on grain yield was provided by the studies of
Nielsen and Hall (1985b) in which cowpea was subjected to different increments
of elevated night temperature under field conditions in a subtropical location
in California (Fig.2). For minimum night temperatures greater than 150C
there were linear reductions in both grain yield and the proportion of flowers
that set pods with 50% reductions occurring at minimum night temperatures of
about 260C.
Evaluating
the same set of cultivars over a range of environments that mainly differ in
temperature provides a more indirect approach for evaluating heat stress
effects on the performance of crops that is of interest to farmers. Six
heat-susceptible cowpea genotypes, including a
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