eXtra Botany
VIEWPOINT
Drought decision-making
John S. Boyer*
College of Earth, Ocean and Environment (formerly College of
Marine Studies), University of Delaware, 700 Pilottown Road,
Lewes, DE 19958, USA
* To whom correspondence should be addressed. E-mail:
[email protected]
Journal of Experimental Botany, Vol. 61, No. 13, pp. 3493–3497,
2010
doi:10.1093/jxb/erq231
Advance Access publication 28 July, 2010
Decision-making was a central part of a recent conference
in Shanghai entitled Interdrought III. Several papers in this
and the previous issue of the Journal of Experimental
Botany are the products of the conference, and they deal
with what to a casual observer seems to be decision-making
by plants. A person watching a drought sees plants failing
to flower or trees dropping young fruits. The plants
seemingly ‘decide’ which structures will survive and which
ones will not. The plant reaction to the deteriorating
environment leads to the survival of only a few of the
young grains or fruits. The obvious advantage is a more
certain presence in the next season when drought may be
less severe.
Of course, plants do not decide in the usual sense, and
instead respond to a changing physiology imposed by the
environment, with the result that flowers abort, fruit quality
is lower, or grains become smaller. It is increasingly
apparent that the basic cause is starvation for photosynthetic products. Photosynthesis is diminished because stomata close as a water-saving feature and leaf biochemistry is
altered, and the plant is left respiring without a substrate. In
effect, the plant has lost its self-sufficiency and become
animal-like, needing to be fed. That this is so can be
demonstrated by feeding the plant sucrose. In maize, this
photosynthetic product can be fed as a concentrated sugar
solution to a small well in the stems, and the plants go on to
produce near-normal ears (Zinselmeier et al., 1995a). Grain
production is high despite a drought that would otherwise
block nearly all production.
It is worth exploring the consequences of this ‘decisionmaking’. In agriculture, decreasing the number or size of
the young reproductive structures may not be desirable.
Most of our harvested products are reproductive; that is,
floral structures, seeds, nuts, fleshy fruits, and so on, and
plants have no way of predicting the future. To preserve
their presence in the next generation, plants must scale their
reproduction to the environment of the moment without
prospects for future rainfall or irrigation. Grains and fruits
stop developing while the parent plant remains alive with
substantial dry mass. The plant ‘decides’, and the farmer
often harvests less than necessary.
It is becoming apparent that global water shortages are
getting worse, and governments are being forced to
confront the problem. Agriculture, which consumes far
more water than any other activity in civilization, has to
give up some of it. Decisions are needed about when to
apply limited irrigation, or whether to irrigate at all. So it
was exciting to see at the conference how human decisionmaking can delay some of the bleaker prospects of water
shortages (Steduto et al., 2007; Yang and Zhang, 2010).
Also how new methods can manage the crop with less
irrigation (Liu et al., 2008; Zhang et al., 2008; Dodd et al.,
2009), or identify particularly sensitive phases of development when irrigation is critical (Fereres and Soriano, 2006;
Collins et al., 2008).
However, underlying all of the advanced methods of
breeding and managing for less irrigation was the prospect
of dryland agriculture, or doing without irrigation. What
genes control the drought response and how do they work?
How can roots be made to acquire more water? Can crops
be changed to resemble desert plants more closely? The
presentations indicated that vast numbers of genes change
in expression as drought intensifies (Harris et al., 2007;
Rebetzke et al., 2008; Manavalan et al., 2009; Oliver et al.,
2009; Wang et al., 2009), and the affected genes differ at
different stages of development (Manschadi et al., 2008;
Yamaguchi and Sharp, 2009). There are genetic means to
incorporate deeper rooting in some crops, thus increasing
the potential to acquire additional water from soil (Norton
and Price, 2009; Landi et al., 2010). Stomatal behaviour can
be modified with mutants overexpressing abscisic acid
(ABA) (Tung et al., 2008) or altering ABA receptors
(Klingler et al., 2010). Prospects are bright for converting
crops from C3 to C4 photosynthetic behaviour (Nelson
et al., 2005; Muhaidat et al., 2007), if not yet to desert-like
behaviour, and this could lower the amount of water used
for a unit of dry matter produced.
There also was clear evidence of past progress. For
example, failed pollination is a thing of the past in maize
because flowering has become more synchronized than in
the past (Bolaños and Edmeades, 1996). Overexpression of
certain transcription factors appears to allow larger
amounts of grain production in maize in dryland conditions
(Nelson et al., 2007). Also dryland wheat is increasingly
productive as management decisions have become more
sophisticated (Passioura and Angus, 2010). It was also clear
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3494 | Viewpoint
that traditional methods of plant breeding have for many
years delivered consistent, incremental improvements in
dryland performance of our crops (Jensen and Cavalieri,
1983; Foulkes et al., 2006; Luo, 2010).
At the same time, there was a sense of frustration.
Drought experiments have always seemed deceptively
simple: just withhold water and see what happens. However, drought continually dehydrates the soil, changing the
treatment conditions in the middle of the experiment. Plants
adapt to these changes to varying degrees, altering the
plant. To make matters worse, the shrinking aqueous
environment inside the cells can force metabolism to react
rather than adapt. The reactions among many genes and
enzymes become passive responses having little impact, with
important events scattered among them. In effect, plants
experiencing drought often seem to be on a slippery slope
too multifaceted to alter and too difficult to repeat
experimentally. Plant breeders confront these problems
without concern for the complexities and simply select
better individuals at the end of the season, a recipe that is
proven. But are there ways to shorten the recipe?
Goals for Interdrought
It seems that much progress could be made for future
Interdrought conferences if scientific effort could focus on
two specific sources of frustration: identifying controlling
genes among multigenic responses; and making experiments
more repeatable. Deciding to focus on these goals might
provide smaller numbers of target genes to modify, and
chances to probe genetics and management more deeply
than at present.
Some of the tools may already be in place. For the first
goal, plant breeding and molecular genetics already allow
several traits to be combined or ‘stacked’ in crops. Also, one
method of deciding which traits to stack is to screen all of
them individually for improved drought performance. Such
an approach seems to have worked for Monsanto, where
screens of hundreds of transcription factors identified
previously unsuspected factors conferring improved
drought performance in maize (Nelson et al., 2007).
However, because hundreds of genes had to be screened,
the costs in manpower and capital were enormous and may
be beyond the means of many researchers.
When gene function is adequately known, though, it may
be possible to limit the screens to those genes likely to be
relevant. Such an approach was taken by McCourt and
Huang and their colleagues (Wang et al., 2005) who
enhanced stomatal closure during drought by altering the
activity of a regulatory enzyme known to alter stomatal
sensitivity to ABA. Characteristic of the Monsanto and
McCourt/Huang successes, the initial experiments were in
the lab in Arabidopsis but quickly moved to the field in
crops for testing in realistic conditions.
Another approach to the goal of identifying controlling
genes is to reverse the drought phenotype. Using methods
such as the sucrose feeding described above, the approach
has been termed ‘functional reversion’ and also is less costly
than screening hundreds of genes (Boyer and McLaughlin,
2007). The key is to reverse the drought phenotype while the
drought is in progress. The controlling genes must be
involved in the reversion, and extraneous non-controlling
genes are not. In effect, one may identify the few controlling
genes among the many irrelevant ones, and this narrows the
number of gene targets. However, as with the success of
Wang et al. (2005), knowledge of physiological and biochemical processes is necessary. This was well illustrated by
Dodd et al. (2009) who reported partial reversion of
stomatal behaviour in tomato mutants for ABA grafted to
normal roots. Also, for the sucrose feeding example, it
became clear that inhibited photosynthesis was a key
feature of floral abortion during drought (Westgate and
Boyer, 1985), and feeding the products of photosynthesis
could thus be predicted to reverse the phenotype (Boyle
et al. 1991; Zinselmeier et al., 1995a, 1999).
The biochemical consequences of inhibited photosynthesis are particularly striking around the time of pollination,
probably because the reproductive events occur rapidly
with precise timing. Maize ovaries are normally loaded
with glucose and starch on the day of pollination
(McLaughlin and Boyer, 2004a, b). However, when the
delivery of photosynthetic products is curtailed at low
water potentials during drought, enzymes that convert
sucrose to glucose lose activity and starch is consumed.
Examples of the enzymes are cell wall invertases and
soluble invertases (Zinselmeier et al., 1995b, 1999; for
a review, see Ruan et al., 2010). Without photosynthetic
products, the starch is eventually depleted, and glucose
largely disappears from the ovary and supporting structures. Feeding sucrose to the stems in photosynthetic
quantities restores the supply of glucose and reverses the
enzyme losses, at least partially, which in turn suggests
changes in gene expression. Abortion that would have
been severe is largely prevented.
During this feeding, a sequence of changes in gene
expression starts to appear. As shown in Fig. 1A and B, for
example, invertase genes are down-regulated by the
drought, and sucrose feeding reverses the down-regulation
in cell wall invertase 2 but not cell wall invertase 1. The cell
wall invertase 2 gene is thus sugar responsive and is
monitoring the sugar status of the ovary cells. Cell wall
invertase 1 is not sugar responsive, does not monitor cell
sugar status, and may be the reason for a lack of full
recovery of ovary starch and glucose in the fed plants.
A day or two after these events in ovary invertase
genes, other genes coding for senescence enzymes are upregulated (Fig. 1C, D). In the maize ovaries, the expression
of the ribosome inactivating protein 2 gene is massively upregulated, suggesting the beginning of failed ribosome
function. Subsequently, the phospholipase D1 gene is also
up-regulated, and plasma membrane integrity begins to be
lost, indicating the onset of senescence. Feeding sucrose
during the drought largely prevents these changes, indicating that senescence genes are also monitoring the
sugar status of the ovary cells.
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Fig. 1. Functional reversion of gene expression in maize ovaries
when plants are fed sucrose to the stems. (A) Cell wall invertase 1,
(B) cell wall invertase 2, (C) ribosome inactivating protein 2, and (D)
phospholipase D1. Open circles, adequately watered controls;
filled circles, drought-treated plants with low leaf water potentials
of –1.5 MPa on the day of pollination; filled squares, droughttreated plants but with sucrose fed to the stems. The drought
caused irreversible abortion of nearly all ovaries, and the feeding
prevented most of the abortion. Note that the gene in A fails to
respond to sucrose feeding, indicating it is not controlling abortion,
while genes in B–D respond to the feeding. Also, the downregulation of genes in A and B occurs before the up-regulation of
genes for senescence in C and D. The black bar on the abscissa
indicates days that water was withheld while the white bar
indicates days that sucrose was fed. From McLaughlin and Boyer
(2004b).
Thus it seems clear that drought-induced floral abortion
is traceable to certain genes attuned to the arrival of
photosynthetic products in developing structures. When the
products run out, these genes turn on in sequence and
eventually orchestrate cell death. This accounts for the
irreversible nature of abortion and loss in grain number
even if water is re-supplied. Preventing the up-regulation of
senescence genes becomes a likely target for genetic
improvement because it might allow floral structures to be
quiescent rather than aborted. With a return of rainfall,
floral development could resume.
Preliminary results from ongoing work with wheat at
CSIRO in Australia have been encouraging. Wheat requires
water potentials to be lower than in maize to lose the same
amount of photosynthetic activity. However, just as in
maize, starch is depleted in floral structures after the
inhibition occurs (Ji et al., 2010). Preliminary experiments
indicate that feeding sucrose may reverse the losses.
Although more work is needed before the wheat behaviour
is certain, the results so far suggest widely occurring
biochemical responses that may ultimately be traced to
similar genes across crop species.
None of these experiments at the gene level would have
been possible without the ability to rigorously repeat
drought conditions. Specific physiological and biochemical
conditions had to be met to allow hypotheses to be built
and tested in subsequent experiments. This underscores the
need for the second goal for Interdrought; that is, characterizing the drought conditions to make each experiment
repeatable. Having reproducible environmental conditions
is helpful, whether in the field, controlled environment
chamber, or high quality glasshouse. Measurements of plant
water status are also helpful to confirm that field conditions
are repeated in the laboratory, and to allow others to use
the results. In that way, field droughts lasting for months
can be compared with those in controlled environments in
the laboratory, or compared with results of other workers.
Other examples could be given, but the overall message is
that withholding water and waiting to see what happens is
not enough. The rate of water depletion is too variable and
plant responses too complex to be ignored.
Several methods of minimizing this problem are available
(Boyer, 1995). Perhaps the simplest is to measure plant
water potential with a pressure chamber, which is rapid and
robust in the lab and field. Thermocouple psychrometry is
also useful because of its small sample size and easy
measurement of the components of the water potential (e.g.
turgor pressure, osmotic potential). The relative water
content is another alternative because of its simplicity and
frequent use, although it has errors caused by plants
adjusting osmotically to drought (Boyer et al., 2008).
Another method useful for plant breeding in field conditions is the mean genotypic yield. This gives a useful
measure of the environment and plant conditions for the
whole season with and without drought, against which
individual selections can be compared. The central goal is to
characterize the extent of drought so that the experiments
can be repeated.
In contrast, simply comparing controls with drought
treatments in short experiments may not accomplish this
goal. Withholding water for, say, 10 days can cause marked
inhibition in one climate but not another. Including
hydrated controls may help, but they continue to develop
while the drought-treated plants may not, creating difficult
comparisons. Full-season comparisons may not solve the
problem, either, when yields diminish to 90% of the control
and are compared with those at 10% of the control. It seems
these problems could be largely solved if the water status
causing the results were known because a benchmark would
be available for repeating the work regardless of yield.
In conclusion, decision-making increasingly based on the
physiological performance of crops is creating new ways to
save water in agriculture. However, water scarcity is increasing, and deeper insights are needed in crop physiology
and gene action to cope with diminishing irrigation.
Challenges are the inherently multigenic nature of plant
responses to drought, and the difficulty of repeating experiments while the treatment and plant conditions are
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continually changing. Research that focuses on overcoming
these two challenges may accelerate progress in the future.
Acknowledgements
Thanks are given to the organizers of Interdrought III for
financially supporting the author’s participation in the
conference.
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