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ADVANCES IN DROUGHT TOLERANCE IN PLANTS
similar pollen abortion, thus implicating high ABA levels during dehydrating
conditions. However, the high ABA may have acted by closing stomata and
inhibiting photosynthesis. Increasing CO, pressures around wheat plants overcame some of the reproductive losses (Gifford, 1979), which supports an involvement of photosynthesis. In rice, dehydration of the soil caused especially
severe dehydration of reproductive tissues, and death and bleaching of florets
followed probably because of inadequate cuticular wax (O’Toole et al., 1984).
Therefore, in various crops, there is increasing evidence for metabolic .and
growth regulator effects and some direct dehydration effects that might account
for the susceptibility of early reproduction to water limitation. CO, and ABA
seem to be involved, and photosynthesis also may play a role but each could act
in concert or separately, depending on the crop.
Additional insight may be possible from studies of embryo development in
maize. Westgate and Boyer (1985a) found that the block in embryo development
was correlated with low photosynthetic reserves in the maternal plant. Because
photosynthesis was inhibited during the treatment, the lack of reserves could
have caused embryo starvation. Westgate and Thomson Grant ( 1989) observed
that the sugar content of maize embryos was not significantly different in hydrated and dehydrated plants but concluded that the flux of sugar might differ.
Schussler and Westgate (1991a,b) found that the uptake of sugars was less in
maize ovules isolated from dehydrated plants even though the sugar content was
high, which further confirms that the flux of sugars was more important than the
sugar content of the developing grain. Myers et ul. (1990) showed an inhibition
of endosperm cell division in maize when high ABA levels were present 5 to 10
days after fertilization.
Boyle et a / . (1991a,b) took advantage of the finding of Westgate and Boyer
(1985a; 1986a) that a few days of low water potentials can prevent embryo
growth and developed a system to feed stems a complete medium for embryo
growth during this time. This allowed photosynthetic products and other salts
and metabolites to be supplied to the plants at normal levels without rehydrating
the plants. The controls yielded well, but withholding water for a few days
virtually eliminated grain production because of embryo abortion. Production
was almost fully restored when the plants were infused with the complete medium as low water potentials developed. Infusing the same amount of water alone
showed no restorative activity. Therefore, it was possible to maintain reproduction by feeding substances normally supplied by the parent plant during embryo
development, which indicates that sufficient water was available to the embryos
J. S. BOYER
so that water itself was not the limiting factor, and embryo growth had been
blocked by some other substance(s) that the parent plant failed to supply. Thus,
reproductive loss appears to be a biochemical problem.
Zinselmeier et al. ( I 995a) found that the active ingredient was sucrose, and
ovary sucrose had to be elevated above controls in order for embryo abortion to
be prevented. Because sucrose is the main translocation form of photosynthate in
maize, this finding showed not only that the lack of photosynthate was the basis
of abortion but also that there was a block in the utilization of sucrose by the
ovaries (Zinselmeier et al., 1995b). Abortion was accompanied by a loss of
starch, which is a product of sucrose metabolism in the ovaries, and starch
returned partially toward control levels when sucrose was fed. This suggests that
the block could have been located between the sucrose supply to the ovaries and
starch synthesis in the ovaries, although there is a possibility that starch degradation also was involved.
It is worth noting that little is known about the role of ovary starch. In contrast
to endosperm starch, which is a terminal pool and has received a great deal of
attention, ovary starch is not a terminal pool. It forms before fertilization and,
because it decreases during dehydration and recovers when sucrose is fed to the
stems of dehydrated plants (Zinselmeier et al., 1995a), it appears to be mobilizable. Apparently, under unfavorable conditions for the parent plant, the products
of breakdown are used to support the growth of the ovary tissues. Fader and
Koller (1985) suggested that ovary starch could be important for developing
soybean pods. Important insight may be gained from a fuller understanding of
ovary starch in early reproduction.
Edmeades and his co-workers found that the time between pollen shed and
silking can be changed by genetic means in maize, and they used early silking to
indicate vigorous development of the ear (BolaAos and Edmeades, 1993a,b;
Bolafios ef al., 1993; Edmeades et al., 1992, 1993). Early ear development may
indicate that the plant supplies more of the biochemical requirements for ear
growth and may be a genetic means of accomplishing the same result as feeding
sucrose to the stem (Zinselmeier et al., 1995a). In effect, early ear development
may be a visual signal for enhanced sucrose availability or utilization by the ear.
Fischer et al. (1989) selected a population of tropical maize for several physiological attributes likely to improve drought tolerance (low canopy temperature,
low leaf death, early silking relative to pollen shed, days to anthesis) and found
that most of these traits conferred a yield gain, but early silking relative to pollen
shed generally accounted for more of the yield gain than the other traits. After
three cycles of selection, grain yield increased by 320, 420, and 4 10 kg-ha- in
the mild, medium, and severe dehydration treatments but not at the expense of
yield in hydrated conditions. The authors point out that progress was accelerated
by using physiological characters in addition to grain yield in the selection
ADV4NCES IN DROUGHT TOLERANCE IN PLANTS
Tollenaar and Mihajlovic (1991) report that the genetic improvement of maize
yields was associated with improved resistance to the herbicide bromoxynil (4hydroxy-3,5-dibromo-benzonitrile),
which inhibits photosynthetic electron transport at photosystem I1 and probably other aspects of energy metabolism. Tollenaar et d.( I 994) suggest that the mechanism may be related to the production
of oxygen-containing free radicals that may be more rapid during drought or
other unfavorable environments. The production of these agents is destructive to
membrane components, particularly photosynthetic membranes; further, chloroplasts contain high levels of antioxidants (glutathione, hydroquinones, ascorbate,
tocopherols, carotenoids) and the cells possess enzymes (peroxidases, catalases,
superoxide dismutases) that probably are protective. Tollenaar et al. ( 1994)
express the view that modern maize hybrids may have been selected for improved levels of the protective components that would be expressed in protection
against bromoxynil. However, it also seems possible that the selection may have
been toward less penetration of the leaf or greater metabolic degradation of
These experiments offer the promise of identifying components that may protect against losses in early phases of reproductive development when plants are
subjected to moderate dehydration. Selection for genotypes that store significant
amounts of mobilizable photosynthate during early reproduction is one approach.
Avoidance of early leaf senescence, which decreases photosynthetic capacity,
might be another. Regardless of the approaches taken, it is clear that the reproductive fraction of the plant can vary from zero to nearly normal during a
drought, which implies that successful protection of reproductive development
may be possible by genetic and cultural means under otherwise inhibiting
V. DESICCATION TOLERANCE
When seeds mature, it is common for them to dehydrate as part of the maturation process. Barlow et al. (1980) found water potentials as low as -5MPa in
maturing wheat grain. Westgate and Boyer (1986~observed
water potentials of
-7 to -8 MPa or lower in maize grain late in the growing season. These seeds
are exposed somewhat to the atmosphere and are known to desiccate to a large
extent by evaporation to the air. Seeds surrounded by a fleshy fruit show a similar
but less severe desiccation. Welbaum and Bradford (1988) observed that water
potentials of melon seeds (Cucurnis melo L.) decreased to about -2 MPa during
maturation, and the surrounding fleshy fruit decreased similarly in water potential. Bradford (1994) considers high solute concentrations to be present in the
apoplast surrounding embryos and proposes that structures may exist to keep the
J. S. BOYER
solutes localized there, The low osmotic potential of the apoplast solution may
explain how the seeds are dehydrated inside fleshy fruits. Regardless of whether
the seeds air-dry or are dehydrated osmotically inside a fruit, it is clear that
embryos become exceptionally tolerant of desiccation late in maturation despite
their susceptibility to the effects of water limitation when they are young.
Plants lower in the evolutionary scale than seed plants sometimes show a
similar tolerance to desiccation. Some fungi, algae from the intertidal zone, and
a few mosses and lycopods can be desiccated to the air-dry state without losing
viability (Bewley, 1979). There also are some specialized seed plants (Craterostigma species, Myrothamnus jiubellifoliu (Welw.), Xerophyta species) that
can tolerate desiccation (Gaff, 197I , 1977; Gaff and Churchill, 1976). However,
desiccation tolerance is virtually nonexistent in most agricultural species except
for the seeds and pollen. It is curious that most seed plants, which are descendants of plants that crossed the intertidal zone, should have lost the ability to
tolerate the desiccation that is so prevalent in that zone. In land plants, desiccation tolerance often evolved as part of the seed habit because an aqueous medium
generally was absent and the pollen and ultimately the embryo were exposed to
drying conditions during dispersal. In agriculture, this property makes it possible
to store seeds and allows uniform planting times. However, after germination, the
plant generally loses its desiccation tolerance and remains sensitive for the rest of
the life cycle until pollen is produced. Pollen can desiccate to a remarkable
degree in species such as maize without losing viability (Westgate and Boyer,
An important aspect of severe desiccation is that water contents can become so
low in the cells that enzyme activities can be directly inhibited by the lack of
water, as described by Vertucci and Leopold (1987a,b). Enzymes are affected
directly when sufficient water is lost to remove the hydration shells next to the
protein. The activities begin to decrease when the monolayer of water next to the
peptide surface is all that remains. When the monolayer begins to be lost, activity
decreases and disappears when water covers only a few polar sidegroups in the
peptide backbone (Rupley et al., 1983). Substrates probably are unable to reach
the active site of the enzyme because the aqueous medium is no longer continuous (Skujins and McLaren, 1967). Cells and tissues begin to show these effects
when they are desiccated in atmospheric humidities around 60-70% (water
activities of 0.6-0.7) and below (Skujins and McLaren, 1967). Thus, seeds
desiccated to the air-dry state are likely to be affected by these phenomena. Most
can return to activity when they are rehydrated, provided water contents have not
ADVANCES IN DROUGHT TOLERANCE IN PLANTS
become so low that the tightly bound water required for viability is lost (Vertucci
and Leopold, 1987a,b).
On the other hand, leaves generally are susceptible to desiccation damage at
much higher water activities. When dehydrated to the air-dry state, leaves of
most crop species show a breakdown of compartmentation that releases cell
constituents to the apoplast (Leopold et al., 1981), and the plasmalemma and
tonoplast show breakage followed by a loss of organelle structure starting at
water activities of about 0.98 (Fellows and Boyer, 1978). In leaves of tolerant
species, the membranes and organelles remain intact at low activities although
they often are distorted (Hallam and Gaff, 1978a,b). Therefore, an important
distinction between tolerance and sensitivity to severe desiccation appears to be
the maintenance of membrane structure and an ability of enzyme activity to
return upon rehydration.
It has been proposed from work beginning with desiccation-tolerant animals
that a possible mechanism to account for preservation of enzymes and cell
structure might be an accumulation of specific sugars such as trehalose or sucrose
whose structure resembles water in certain respects (Crowe and Crowe, 1986).
Sugars having the appropriate stereostructure might form hydrogen bonds with
cell membranes where water would ordinarily bind. Because the sugars would
remain as water is removed, the bonding would be stable and membrane structure might be maintained where otherwise it would become disorganized.
Evidence that the sugar replacement hypothesis may have merit is the accumulation of sugars such as sucrose and raffinose in developing seeds (Caffrey et
al., 1988; Koster and Leopold, 1988). Species such as maize have seeds that can
tolerate desiccation to the air-dry state, and their sugar concentration, while not
high for the seed as a whole, becomes high in the remaining residual water of the
drying seed and could have a stabilizing influence at local sites. As germination
proceeds, the stabilizing sugars are metabolized to nonstabilizing ones such as
glucose and fructose, and desiccation tolerance is lost (Koster and Leopold,
1988). A related hypothesis is that certain sugars may be converted to the glassy
state during dehydration (Williams and Leopold, 1989). The glassy state is
common in sugars such as sucrose used to make candy, and evidence for the
existence of glassy sugars is accumulating for embryos of dehydrated seeds
(Williams and Leopold, 1989).
A similar role has been proposed for certain proteins in seeds (Crowe and
Crowe, 1986; Dure el a l . , 1989). The developing seeds of a range of crops
accumulate hydrophilic proteins in the embryo as normal desiccation begins
(Dure et a l . , 1989). The proteins have been variously called dehydrins, embryo
maturation (Em) proteins, or late embryogenesis abundant (LEA) proteins (Dure
et a l . , 1989). Common to all of them is a high content of hydrophilic amino acids
so that the proteins as a whole are highly water soluble. In some of them, an
J. S. BOYER
alpha-helix is present that could remain structurally stable during desiccation and
it has been proposed that this portion of the protein could act like a membranestabilizing sugar (Crowe and Crowe, 1986).
The mRNAs for these proteins are not readily detected in leaves or roots of
hydrated plants but can be induced by severe desiccation in very young rape
(Brassica napus (L.)) (Harada er a l . , 1989) and maize and barley seedlings
(Close et al., 1989; Close and Chandler, 1990). There was a marked increase in
dehydrin mRNAs when young wheat seedlings were dehydrated soon after germination (Close and Chandler, 1990). The mRNA expression was especially
increased in shoots, which are most exposed to dehydration under natural conditions. This cellular response suggests that the dehydrin-Em-LEA proteins play a
role in the desiccation tolerance of seedlings. Also, the mRNAs can be induced
by treating hydrated seedlings or immature embryos with high abscisic acid
concentrations (Galau et al., 1986; Hong et al., 1988; Mundy and Chua, 1988).
Abscisic acid levels normally increase in plants subjected to dehydration (e.g.,
Beardsell and Cohen, 1975) and they become high in maturing dehydrating seeds
(Ihle and Dure, 1972). The induction of the mRNAs suggests that there is
molecular control that might be manipulated genetically, thus altering the development of desiccation tolerance of young seedlings and embryos.
Land plants appear not to be optimally adapted to water shortages imposed by
the environment and indeed we likely would see large improvements in dehydration performance if this chapter could be written after a few hundred million
years to give additional time for beneficial adaptations to evolve. Certain metabolic changes have developed during the course of evolution that have improved
the ability of plants to withstand limited water supplies, particularly in photosynthesis. The recent evolutionary development of C, photosynthesis and
Crassulacean acid metabolism are clear examples, and there is increased water
use efficiency in those species possessing these adaptations. Methods of plant
breeding and genetic modification can speed the transition to more efficient water
use and considerable success has already been achieved. Water acquisition has
been improved by deep rooting and strong osmotic adjustment, cuticular characters have been modified to conserve water, and earliness in reproduction has been
used to avoid late season droughts. It also appears increasingly possible to
improve water use efficiency by genetic means using new techniques for screening for this trait.
Water is required for biological activity, and studies show that water use
ADVANCES IN DROUGHT TOLERANCE IN PLANTS
efficiency is unchanged by the water supply when the water limitation remains
stable for the entire season. This allows acclimation to occur, and the harvest
index often remains unchanged as well. However, when the water supply is not
stable for the growing season but slowly declines or varies with rainfall, dry
matter is partitioned differently to plant parts depending on the time in the life
cycle. This is particularly true for reproductive structures and can lead to a
variable harvest index, which can be relatively independent of the overall water
use efficiency. Attention to the harvest index may provide a means for maintaining the economically valuable parts of a crop even though the total plant dry mass
The demonstration that reproductive losses usually associated with drought
may have a biochemical origin raises the possibility that metabolic modifications
may be useful for improving the harvest index with limited water, and genetic
approaches are being applied to this problem. Also, the molecular mechanisms
of desiccation tolerance suggest that changes in expression of specific genes are
correlated with decreased lethality of severe desiccation at least during late seed
From these principles, it is possible to distill certain conclusions that may help
in efforts to improve the efficiency of water use and drought tolerance of plants.
The approaches at first appear diverse and the complexity makes it tempting to
take shortcuts such as selecting seedlings for rapid growth only under favorable
conditions or in osmotica, or by using single biochemical tests for performance.
In general, the temptation should be avoided because the results have not carried
over to field situations. The approaches that have given the most rapid progress
in improving drought performance have been: (1) using realistic soil conditions,
(2) testing with adequate water and with limited water, (3) understanding the
sources of crop failure in the proposed growing area, and (4) targeting a limited
number of traits for improvement.
In most examples of improvement, there was an intimate knowledge of the
soil, climate, and physiology, and biology of the crop. Physiological tests sometimes could be employed to increase the rate of progress, and the problem could
be reduced to a few traits to simplify the selection effort. Great progress was
made under conditions of realistic water limitation in soils because droughtadaptive factors were called into play and had an opportunity to express themselves. This avoided the problem of selecting only genotypes yielding well in
favorable environments that "crashed" in water-limited environments, or using
pots that restricted root development and prevented the expression of this important tolerance character. It is now clear that successful improvement of drought
performance can come at no sacrifice to performance under favorable conditions
but this can be determined only if performance is tested under both favorable and
J. S. BOYER
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