Plant Growth Regulation 20: 79-83, 1996. @ 1996 Kluwer Academic Publishers. Printed in the Netherlands.

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Drought and drought tolerance

J.B. Passioura CSIRO, Division of Plant Industry, GPO Box 1600, Canberra, 2601, Australia

Abstract

Drought tolerance is a nebulous term that becomes more nebulous the more closely we look at it, much as a newspaper photograph does when viewed through a magnifying glass. From the vantage point of an ecologist the features that distinguish xerophytic from mesophytic vegetation are clear. We can all tell that a cactus is more drought tolerant than a carnation. But when we look at crop plants, the features that confer drought tolerance are far from clear. The main reason for the contrast is that the traits we associate with xerophytes typically concern survival during drought, whereas with crops we are concerned with production - and insofar as the term “drought tolerance” has any useful meaning in an agricultural context, it must be defined in terms of yield in relation to a limiting water supply.

Further, with the well-developed major crop plants, those of us trying to increase water-limited yield would be pleased to achieve improvements of just a few percent in environments that are highly variable in their water supply. This variability often means that several seasons are required to demonstrate the advantages of an allegedly improved cultivar. Traits that confer drought tolerance in such circumstances are subtle, and may manifest themselves in some types of drought but not in others. Indeed the most influential characters often have no direct connection to plant water relations at all, as I elaborate on below.

I will concentrate on the agricultural rather than the natural environment (although there are no doubt lessons for us still to learn from analysing the behaviour of natural vegetation - see Monneveux, this volume), and will argue that drought tolerance is best viewed at an ontogenetic time scale - i.e. at the time scale of the development of the crop - weeks to months for an annual crop. The timing of the main developmental changes, like floral initiation and flowering, and the rate of development of leaf area in relation to the seasonal water supply, are the most important variables at this time scale. Occasionally though, rapid changes in the environment, such as a sudden large rise in air temperature and humidity deficit, perhaps associated with hot dry winds, make appropriate short-term physiological and biochemical responses essential for the survival of the crop. These short term responses may be amenable to cellular and sub-cellular manipulation, especially if the sudden environmental deterioration occurs at especially sensitive stages in development such as pollen meiosis or anthesis.

Purists insist that “drought” is a meteorological term that refers only substantial to periods in which rainfall fails to keep up with potential evaporation. Within the spirit of this meeting it is appropriate to interpret the term more loosely than this definition, and to define it as circumstances in which plants suffer reduced growth or yield because of insufficient water supply, or because of too large a humidity deficit despite there being seemingly adequate water in the soil.

1. Patterns of drought

Fischer and Turner [6] have provided a good summary of the main climate regions that are prone to drought:

l Savanna. Latitude 0” to 20°, dry winter, wet summer growing season, fairly uniform tempera- tures and evaporative demand throughout the year.

l ‘Ikansition. Latitude 20” to 35”, rain and growth at any time of year.

l Mediterranean. Latitude 30” to 40”, dry summer, wet winter and spring, rapidly rising temperature and evaporate demand during late spring.

l Steppe. Latitude 40’ to 50”, cold winter, spring and summer growing season, water supply may depend on winter snowfall and spring thaw.

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This is a bald climate summary. Overlying it is the problem of variability. False breaks to the wet season and substantial periods of drought within a growing season may be common. Plants that perform well must have their rates of development tuned to the particular combinations of soils and climate, yet at the same time they must be able to cope with major vicissitudes in water supply and evaporative demand within the growing season. Where the soils have a large capacity to store usable water, crops that grow during the dry season may be successful - for example, winter crops sown into full soil profiles at the end of the wet season in a savanna environment.

2. Time scales of environmental and physiological change

Processes in plants that influence drought tolerance span a wide range of time scales. A selection is listed in Table 1. In general, the most important processes match, in time scale, influential environmental changes, also listed in Table 1. For example, by far the most important feature of a drought tolerant crop is its phenology, the timing of its development, in relation to temporal changes in water supply. The matching is most important in environments in which there is rapid change in the main variables as the growing season draws to a close: in a mediterranean climate, yield may fall by several percent for every day that anthesis is delayed past the optimal date [9], as the crop matures into an increasingly hot and water-limiting environ- ment. At the other end of the scale, establishment of seedlings in a savanna environment depends critically on events in both plant and environment that occupy but a few hours; rapid evaporation from the soil surface may soon lead to the surface drying and heating to potentially lethal temperatures exceeding 50” [ 101.

Most of the short term responses to the rapid imposition of drought are probably concerned with metabolic “housekeeping” - the molecular equiva- lent of emptying the fridge and putting the biscuits in a mouse-proof container before going on holidays. A plethora of genes are expressed, of still largely unknown function, which are probably concerned mostly with shutting down the normal metabolic activity of cells as their water status falls to life- threatening levels. For example, large amounts of vegetative storage proteins [ 141 or dehydrins [4] may be produced. Blum [l] has used an elegant metaphor for these activities, which he compares to shutting

down a computer: unless we make sure that active files are first saved and closed before we throw the “off” switch, then normal functioning of the computer might not be easily recovered when the power is restored. These activities are certainly important, but they tend to be associated with extreme events that threaten survival of the plant, rather than with events that influ- ence production. I have mentioned establishment of seedlings in a savanna environment as an example of circumstances in which rapid events may be important. Another example is that of roots near the surface of the soil, which may experience a rapid drying of the soil, and which may be able to undergo rapid acclimation as described by Vartanian [ 151.

At the other end of the time scale of responses to drought is the development of leaf area. In a slowly intensifying drought, plants modulate their leaf areas and thereby adjust the loss of water from the canopy to the size of the supply in the soil. It is unclear what processes are involved, but the modulation is presum- ably brought about either by changes in water status of the growing tissue, or by hormonal regulation, for example via abscisic acid, instigated by falling water status elsewhere in the plant (see Mullet, this volume).

One of the main difficulties facing us when we work on short term responses to drought is that, except where clear issues of survival are concerned, it is very difficult to distinguish between responses that might be important for overall drought tolerance, and those that are essentially biochemical and physiological “noise” that is integrated into insignificance at longer times. This notion of “noise” can be illustrated by imagining a car journey. To get to our destination we must, say, proceed for 10 km along a winding road. While driving the car, we make many adjustments of the steering wheel that ensure that we do not run into anything and that we negotiate the bends in the road while keeping in the correct traffic lane. No two journeys along the road would be identical in detail. A car will drift to one side or the other of the lane on many occasions, and the driver will correct the path to bring the car back towards the centre. These many corrections are all essential. The car would otherwise crash. But in relation to getting to the destination, they are simply random deviations (“noise”) from the main route.

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Table 1. Some phenomena occurring at different times scales in plants and their environment that may bear on drought tolerance or other aspects of plant water relations

Time scale In the plant In the environment

Minutes or less Turnover of some proteins, stomatal movement Movement of shadows, rain or irrigation

Hours Production of heat shock proteins or dehydrins, leaf Diurnal evaporative demand, rundown of surface soil movement, wilting, osmotic adjustment, response to water, rewetting of previously dry topsoil ABA

One to two days Cellular “hardening” - induction of housekeeping Weather (cool to hot, dry winds), rundown of water in genes, seedset, floral initiation, flowering the topsoil

Several days to weeks Canopy development, leaf senescence, root system Rundown of soil water throughout the profile development

Weeks to months Clocks controlling development (e.g. vemalisation, Seasonal evaporate demand, prevailing rainfall pattern time to flowering), gram filling

3. Drought tolerance defined in terms of resource economics

I have been arguing that drought tolerance, as a universal idea, does not bear close scrutiny. There are no traits that confer global drought tolerance, and in particular, short term responses to water stress at the cellular and sub-cellular level may have no bearing on the yield of water-limited crops. Where drought is not severe to the point of threatening the survival of the plants, their productivity is best analysed from the top down - in terms of resource economics: that is, in terms of what determines the effectiveness with which a crop can use a limited supply of water in producing harvestable yet.

The resource is the crop’s water supply, which is the store of accessible water in the soil plus the rain- fall during the life of the crop, minus any losses from drainage beyond the reach of the roots and direct evap- oration from the surface of the soil.

The most effective use of this resource involves three principal factors:

(a) capturing as much as possible of it; (b) using the captured water as effectively as possible when trading it, at the stomata, for carbon dioxide destined to form photoassimilate: and (c) converting as much of this assimilate as possible into a harvestable form, say, grain.

These factors can be expressed symbolically as:

Y=TxWUExHI (1)

where Y is grain yield; T is the amount of water tran- spired; WUE is the water-use efficiency, the ratio of above-ground dry matter to the amount of transpira-

tion; and HZ is the harvest index, the ratio of grain yield to above-ground dry matter. To a first approxi- mation the components in this identity are independent of each other, so an increase in any one of them is likely to increase yield [7, 11, 121. Conversely, any phenomenon that can not be readily related to any of these components is unlikely to have much bearing on water-limited yield, except in the special circum- stances concerned with survival, that I discussed in the previous section.

Figure 1 illustrates this view of drought tolerance. It shows yield as a function of water supply for a hypothetical water-limited crop (the thick line), and it shows improvements that we might hope to make in drought tolerance, by increasing the effective use of the available water. Recent improvements in water-limited performance of maize [3] and of wheat (Richards, this volume), illustrate changes that mimic the thin line of Figure 1. Another possible pattern of improvement is depicted by the dashed line in the figure. This line crosses the thick line, and thereby illustrates improve- ment where the water supply is very low, but deteri- oration where the water supply is moderate to good. This pattern corresponds to recent improvements in the performance of water-limited barley (Ceccarelli, this volume) which was selected in severely water-limiting mediterranean environments, and to the behaviour of some lines of wheat over a wide range of water supply PI.

Of these components by far the most important is harvest index, which in turn depends critically on how well the phenology of the crop is suited to the environ- ment. Figure 2, adapted from [7], illustrates this point further. Fischer [7] discussed the performance of wheat in mediterranean environments, in which the evapora-

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1 Improved General / /

5- Drought Tolerance

4-

of Severe Drought

0 100 200 300 400 500

WATER SUPPLY (mm)

Figure 1. Yield as a function of water supply illustrating possible improvements in drought tolerance over current performance.

tive demand on the crop rises rapidly from about the time of ear emergence onwards, but the principles he discussed apply widely. The most important point is that a large harvest index can arise only if sufficient water is available in the soil at anthesis for the crop to set and fill a large number of grains. If there is too much growth before anthesis, either because anthesis is too late, or because the plants have been too vigorous in their vegetative growth and have consequently tran- spired so much water that little remains stored in the soil at anthesis, then harvest index will be low. Studies on a range of lines of wheat in mediterranean envi- ronments show that yield may fall by several percent for every day that anthesis is delayed [9, 131. Delays in anthesis not only reduce the amount of water avail- able for the crop during grain-filling, but also expose it to greater evaporate demands, with a consequent fall in the effectiveness with which the crops can use the water while fixing carbon dioxide.

If antbesis is too early in relation to the pattern of water use, yield, although typically not harvest index, is reduced because the crop fails to establish a sufficiently large reproductive sink and photosynthetic factory to capitalise on the substantial water supply during grain filling. This point bears on the next most important determinant of water-limited yield, namely, the development of leaf area through time. Watson [ 161 pointed out that a crop’s modulation of its leaf area may be rather more influential on yield than its modula- tion of net assimilation rate. His concern was with the capture of light, but his argument applies equally well

L 3 Too little growth

:: before anthesis

9

Too little water available after

anthesis

Proportion of water supply used by anthesis

Figure 2. Schematic relations between gram yield (solid line) or harvest index (dashed line) and proportional water use. (Adapted from Fischer, 1979).

to the efficient use of water. There are several influ- ences of leaf area development on yield that are worth noting. First, it largely determines the amount of dry matter produced by anthesis, which in turn strongly influences the potential yield of the crop (that is, the yield if conditions are excellent during grain-filling) [7]; the plants set a large number of seeds. Second, it influences the harvest index through its effect on the balance of water use before and after anthesis even when the phenological development is right, that is, when the crops flower at the right time in the given environment. Third, it may influence the amount of water transpired if the soil surface is wet for much of the season - for a high leaf area index will ensure that water that would otherwise be evaporated directly from a wet soil surface is used by the plant.

The modulation of leaf area in relation to the amount and pattern of the water supply depends partly on the intrinsic vigour of the plants (Richards, this volume), and partly on a range of environmental influ- ences: temperature, soil water content, disease, soil compaction, and nutrition - especially nitrogen nutri- tion. Low temperatures have a profound effect on leaf development, and especially in mediterranean envi- ronments can inhibit the development of leaves during the winter when the plants could most effectively trade water for carbon dioxide because of the low evapo- rative demands at that time. In these circumstances the ability of a crop to grow at low temperature could considerably improve its “drought tolerance” as defined in the discussion surrounding Figure 1;

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yet such a trait is not directly related to plant water relations in any way. The effect of soil conditions on the leaf development can be substantial, not only through the supply of the water and nutrients that are needed for the development of the shoot, but also through inhibitory signals that may be gener- ated by roots growing in less than ideal soil [5]. Perhaps the most important interaction between soil conditions and performance during drought is that involving nitrogen nutrition. In soil that is too well supplied with available nitrogen, plants may develop leaf area so fast when water is available, that they deplete the soil profile too fast during periods with- out rain. They may also be particularly susceptible to sudden hot weather during grain filling that can result in shrivelled grain - a response known as hay curing or haying off [S].

4. Discussion

The most important aspect of drought tolerance in an agricultural context is that the pattern of development of the crop must match the pattern of the water supply in relation to the evaporative demand. The traits controlling this development may often have no direct connection with plant water relations, but insights into what is important in the pattern can help focus both breeding and scientific objectives. Breeders have succeeded in matching the phenology of the crops to the environment, but it is not yet clear that the devel- opment of leaf area, which depends both on the geno- type and agronomic management, is well matched. There may be substantial scope for improvement in this respect. Short term responses of plants to changes in water status include may physiological, biochemical and molecular biological changes. Such changes are not necessarily adaptive in the sense that they contri- bute to productive processes that lessen the impact of drought on yield. Many of these changes are house- keeping activities that prepare the plant for entering survival mode when the water supply runs out. How to decide which of these changes are important, and which may be treated as little more than “noise”, is very difficult.

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