JXB Advance Access originally published online on September 15, 2006
Journal of Experimental Botany 2007 58(2):119-130; doi:10.1093/jxb/erl118
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RESEARCH PAPER |
Monitoring plant and soil water status: established and novel methods revisited and their relevance to studies of drought tolerance
Division of Applied and Environmental Biology, University of Dundee at SCRI, Invergowrie, Dundee DD2 5DA, UK
* E-mail: h.g.jones{at}dundee.ac.uk
Received 7 May 2006; Accepted 14 July 2006
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Abstract |
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 Top Abstract IntroductionWhy measure water status?General principles and...Choice of water-status measure...Some specific 'case-studies' and...Conclusions and recommendationsReferences |
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In all studies of the effects of water deficits on plant functioning there is a need for an accurate and comprehensive definition of treatments and their effects on plant water status. The various measures of water status used in plant and soil science are reviewed and their appropriateness for different purposes such as for studies of mechanistic effects of water deficits on plants, for breeding of drought-tolerant plants, or for management of irrigation systems are reviewed. An important conclusion is that the frequent emphasis on water potential rather than on cell turgor can be shown to be misleading, as can be measurements in the leaf. The disadvantages of the current trend towards the omission of necessary water-status measurements, especially common in more molecular studies, are outlined, and recommendations made for minimal sets of measurements for specific types of experiments.
Key words: Drought, relative water content, soil water, turgor, water potential, water stress
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Introduction |
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TopAbstractIntroductionWhy measure water status?General principles and...Choice of water-status measure...Some specific 'case-studies' and...Conclusions and recommendationsReferences |
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Precise definition of both the environmental conditions and of the plant responses is a prerequisite for the conduct of repeatable and interpretable experiments. This paper reviews the range of approaches available for monitoring plant and soil water status, includes discussion of both direct and indirect methods, and aims to provide some recommendations as to how to select the most appropriate technique for specific purposes. The discussion builds on the general concepts presented previously (Jones, 1990), with the aim being to compare and contrast the general types of measurement available rather than attempting to evaluate all the specific instruments on the market for measurement of water status. Further details of the necessary instrumentation and its use may be found in appropriate texts (e.g. Slatyer, 1967; Boyer, 1995; Kirkham, 2004).
The choice of measurement technique in any experiment depends critically on the experimental objectives, and also on any pre-existing hypotheses concerning the mechanisms of any response or adaptation to the water deficit. All too often, modern plant physiologists do not incorporate an understanding of the control systems underlying the expected physiological responses into the design of their experiments and their analysis or into their choice of water-status measure. For example, recent improvements in the understanding of mechanisms involved in plant adaptation to drought have only developed through the increasing recognition of the involvement of root–shoot signalling (see review by Davies and Zhang, 1991) in the control of stomatal aperture and growth in some water-stressed plants. Although these advances might have been expected to lead to a shift in the ways in which water status is quantified in drought studies, there has been surprisingly little recognition of these changes in much modern experimental work relating to plant response or adaptation to drought. Where water status is measured (and that is all too rarely) it is too commonly based on measurements of water potential in the leaves, neither of which (water potential or leaves) is usually optimal. In this paper, some of the evidence which indicates a need for a change in the general approach to measurement of water status in modern drought studies, including a need for a shift away from the reliance on leaf water potential, is reassessed. Although these arguments are not new (Jones, 1990) a survey of typical usage (outlined below) highlights the deficiencies in current practice and the need for a more thoughtful approach to the choice of method for monitoring water status in experimental systems.
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Why measure water status? |
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TopAbstractIntroductionWhy measure water status?General principles and...Choice of water-status measure...Some specific 'case-studies' and...Conclusions and recommendationsReferences |
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It is generally accepted that the accurate measurement of plant and/or soil water status is critical in any experiment where one is concerned with understanding the effects of differing water supply. Such measurements are essential to define the conditions of the experiment (both in terms of the treatments applied and in terms of the effects on the plants) and as a first step in facilitating repetition of the experiment (which is an essential part of rigorous scientific method). Precise definition of water status in different parts of the soil–plant system is also required for the formulation and testing of any rigorous mechanistic hypotheses, such as those relating to the mechanisms of drought tolerance or adaptive responses in any plant. It is also essential that the measure of water status chosen is relevant to the physiological process of interest. Reliable measures of water status also provide powerful tools for crop management purposes where there is a need for repeatable control as in irrigation scheduling.
In measuring water status it is useful to distinguish cause and effect (=‘stress’ and ‘strain’ using the terminology of Levitt, 1972). For example, soil water deficits and the consequently lowered soil water potentials are usually considered as the underlying stresses in the system; the leaf water status is then a result of the soil water deficit. Indeed the actual leaf water status is modulated by plant responses such as stomatal closure or changing xylem hydraulic conductance, so it neither uniquely nor usefully describes the experimental treatment. For some purposes, however, the leaf water status can usefully be regarded as a stress: these are where one is concerned with the direct effects of leaf water status on metabolic or physiological processes within the leaf. The leaf water status can therefore be regarded both as a strain and a stress, with its role at any time being dependent on the adaptive mechanisms that occur in the plant.
Unfortunately there is not necessarily any unique or ‘best’ measure of water status that is applicable in all situations. The choice of the most appropriate method(s) for measuring or describing water status in any situation depends on the purpose of the experimenter and may be very different for (i) those concerned primarily with practical management such as irrigation scheduling or quantification of the benefits of management treatments such as mulching or pruning, (ii) those aiming to understand the mechanisms of water movement, (iii) those aiming to understand the mechanisms involved in water stress effects on growth and physiology and the adaptive plant responses involved, and (iv) those aiming to identify differences in drought tolerance, to isolate the controlling genes, or to breed or test drought-tolerant genotypes.
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General principles and approaches to measurement of water status |
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TopAbstractIntroductionWhy measure water status?General principles and...Choice of water-status measure...Some specific 'case-studies' and...Conclusions and recommendationsReferences |
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Before what should be measured and reported in studies of plant water relations is considered in detail, it is worth reviewing some of the fundamental principles of water-status measurement. The available measures of soil or plant water status can be broadly divided into those based either on (i) the amount of water or on (ii) its energy status. The principles and practice underlying the quantification and measurement of soil and plant water status have been well described in a number of texts and reviews (Slatyer, 1967; Boyer, 1995; Nobel, 1999; Mullins, 2001; Kirkham, 2004) and these should be consulted for more detail and background theory.
Amount of water
Obvious measures of water status for soils or plant tissues are based on water content. Although content can be expressed as an absolute amount this needs normalizing so it is more useful to express it as a fraction of other material in the system on either a volumetric or a mass (or molar) base (e.g. m3 m–3, %, g g–1 fresh mass, etc.).
Soil moisture content measurement:
A basic measurement which can be used for calibration of the other methods available is to measure soil moisture directly using gravimetric measurements. These require extraction of a known volume of soil, which is weighed and then dried and re-weighed. It is normally assumed that organic material is not lost during the drying process. There are a wide range of approaches and instruments for direct and indirect measurement of soil moisture content; these have been extensively reviewed elsewhere (Gardner et al., 2001; Kirkham, 2004) and include neutron probes and a wide range of capacitance or electromagnetic sensors, including time-domain reflectometry, capacitative probes, resistance probes, etc. The majority of these instruments make use of the fact that the dielectric constant of water is very different from that of other components of the soil so the output signal can be directly related to moisture content, while resistance and voltaic probes depend more on the conductive capacity of soil solutions. In addition, there are several indirect approaches for estimation of soil moisture content based on remote sensing using, for example, passive and active microwave or radar techniques (Gardner et al., 2001).
An alternative approach that is widely adopted, especially for agronomic and irrigation purposes, is the indirect estimation of water status on the basis of soil moisture balance calculations. Changes in soil moisture content (
) are estimated from
 | (1) |
A major limitation of water content measurements in soils is that the moisture release curves are quite different for peat soils, fine-grained clays, and coarser soils, so that a given % water content may represent either a sand fully saturated with free water or a rather dry clay (Townend et al., 2001). Slightly more generality may be obtained for soils through a normalization process involving expression of the soil moisture content as a fraction of either the total volume of pore space (giving a relative saturation) or as the related water-holding capacity of the soil (usually defined as the amount of water released in going from field capacity to a tension of 1.5 MPa). Unfortunately, hysteresis and different release curves for different soils mean that these can only be approximate.
Plant water content measurement:
Analogous measures of water content are available for plant tissues where the water content may be expressed per unit fresh weight or per unit dry weight (or even in terms of unit leaf area). Unfortunately, as with soils, these raw water contents are not very useful for comparisons between species with different morphologies as the degree of succulence, for instance, influences the value obtained, even for fully turgid leaves. A very powerful method of normalization of such data is the use of relative water content (RWC) which is defined as
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Energy status
A major problem with measures of water content, even the relative measures described above, is that such measures do not necessarily relate to the ease with which that water can be extracted or to its effect on plant functioning. It was recognized many years ago that measures of water status based on the energy status of water in the system have advantages over purely volumetric measures. For soils, the concept of capillary potential (equivalent to the modern matric potential) was introduced by Buckingham (1907), while for plants Ursprung and Blum (1916) introduced the term ‘suction pressure deficit’ as the basis for describing plant water relations. These concepts were re-expressed on a sound thermodynamic basis and brought into line with modern physico-chemical usage by Slatyer and Taylor (1960) who introduced the term ‘water potential’ (
), as a measure of Gibbs free energy. Dainty (1963) and Slatyer (1967) then expressed water potential in pressure units which were familiar to plant physiologists and soil scientists by defining it in terms of the chemical potential of water (µ) and dividing by the partial molal volume of water
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 | (4) |
is the osmotic potential due to dissolved solutes, P is pressure potential (equal to the hydrostatic pressure; often simply given the symbol P), g is the gravitational potential reflecting elevation differences between the site of interest and the reference level, and 
is the matric potential. In practice, the conventions used in soil science (Marshall et al., 1996; Mullins, 2001), where is defined as a component of P, appear more logical than the separation of matric and pressure terms often adopted somewhat misleadingly by plant physiologists. The alternative of combining the osmotic and matric effects into one (osmotic) term is also well based physically (Passioura, 1988). Where the gravitational potential comes into play, as in water transport in tall trees, it is probably most convenient to use differences in what is often called hydraulic potential (= g+P). Notwithstanding the controversies relating to the correct formulation for water potential and its units (see, for example, Passioura, 1988; Roderick, 2001, 2005) it is felt that for compatibility with much current usage it is reasonable to stick with the use of water potential as outlined above, even though it has only restricted relevance to plant physiologists, as will be seen below. In retaining water potential terminology it is important to remember some of the assumptions involved. For example, the standard derivation assumes that the system is in equilibrium and isothermal, which clearly is not true in most plant systems. It is also necessary to understand and recognize the relevant components for water movement in any specific system, with, for example, the osmotic component only being relevant for systems with semi-permeable membranes as modified by the appropriate reflection coefficient when that is not unity (Dainty, 1963).
Soil water potential and its measurement:
By contrast to the measurement of the amount of water in the soil, methods which measure the energy status are of greater value for providing a rigorous indication of the water ‘availability’ to plants, with values that allow comparisons between any growing substrate. Unfortunately even the use of water potential as a measure of availability is somewhat oversimplified as this strictly refers only to the equilibrium situation; the capacity of a soil to give up water also depends on the hydraulic conductivity of the soil (which itself is a function of both soil type and its water potential). Nevertheless, the water potential gradients do determine whether water can be absorbed at all, even if by themselves they do not determine the rate of uptake. Again there is a substantial amount of literature on this subject (Mullins, 2001; Kirkham, 2004) which will not be repeated here. The most common instruments for the measurement of the energy status of soil water are tensiometers (for fairly low suctions) and soil psychrometers (Mullins, 2001), or else one can calibrate volumetric sensors (neutron probes and capacitance sensors) using the moisture release isotherm as derived from, for example, pressure plate calibrations (Townend et al., 2001). Many other indirect sensors of soil moisture tension, such as gypsum blocks depend on the water release characteristics of porous materials (Mullins, 2001).
Plant water potential and its measurement:
Measurements of plant water potential are primarily by means of either psychrometric methods (involving tissue equilibration with air in an enclosed chamber and the estimation of the vapour pressure using wet and dry thermocouples) or by means of the pressure chamber. For psychrometry, can in principle be derived from the vapour pressure using equation 3, but in practice is more usually obtained using a calibration curve for known concentrations of salt solutions. The cell pressure probe (reviewed by Tomos and Leigh, 1999), which measures turgor pressure in cells, can be used in combination with estimates of osmotic potential to derive water potentials according to equation 4, while the xylem pressure probe (Balling and Zimmerman, 1990) can be used to estimate mild xylem tensions, although its use for more extreme tensions is controversial (Angeles et al., 2004). The cell pressure probe is a particularly valuable tool for the study of important cell hydraulic properties such as cell wall elasticity and cell membrane permeabilities. Details of these and other methods are well described elsewhere (Jones, 1992; Boyer, 1995; Kirkham, 2004) so will not be reviewed in more detail here.
Indirect measures of water status
In addition to the various methods for the direct measurement of either water content or energy status of plant or soil water, there are a number of widely used indirect indicators of water status based on the analysis of plant growth or physiological responses known to be indicative of water deficits (Jones, 2004b). These range from visible expression of increasing plant water deficits such as wilting (Jones, 1972), through morphometric changes such as stem, leaf, or fruit shrinkage (Jones, 1973b; Huguet et al., 1992; Fereres and Goldhamer, 2003; Naor and Cohen, 2003) and the well-known reductions in cell expansion and growth rate that are associated with water deficits, to physiological responses such as stomatal closure and reductions in photosynthesis rate. A particularly widely used method for detecting water stress-induced stomatal closure as a guide to irrigation scheduling is the use of infra-red thermometry (Idso et al., 1981) or thermography (Jones, 2004a, b).
It is frequently possible to derive repeatable calibration curves to allow estimation of water status for a given cultivar, so such methods are often valuable in agronomic practice. The fundamental problem with all such indirect measures of water status, however, is that, although they may be very valuable for detecting the physiological results of water deficits (whether in terms of damage or adaptive responses such as stomatal closure), they are not very useful in mechanistic studies aiming to understand the process of plant adaptation or response to water deficits because they are not rigorously associated with any underlying measures of water status. As a result they can only be used with circumspection when attempting to identify drought-tolerance mechanisms for incorporation in plant breeding programmes. Nevertheless those techniques, such as thermal imaging (Jones, 2004a), which are suitable for screening large numbers of plants, have real value in drought studies as long as their limitations are remembered.
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Choice of water-status measure and its relevance to physiological processes |
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TopAbstractIntroductionWhy measure water status?General principles and...Choice of water-status measure...Some specific 'case-studies' and...Conclusions and recommendationsReferences |
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As has been pointed out previously (Jones, 1990, 1992) the choice of water-status measure for plant physiological studies is not necessarily straightforward, with the most appropriate method being dependent on the uses to which the data are to be put. The following sections review and expand some of these earlier arguments relating to the measures of water status to be preferred in different situations.
What physical measure of water status?
In soils, the total potential, which normally equates to soil moisture tension, appears to be a good indicator of soil moisture status for physiological studies because it is the measure that most closely indicates the potential ability of plants to extract water, although, as indicated above, the actual rate of extraction will also depend on hydraulic conductivity of the soil–plant pathway. The ease of extraction declines as soil moisture content declines and an increasing proportion of the remaining soil moisture becomes tightly bound to soil particles or in capillaries. On the other hand, a researcher or agronomist concerned with irrigation is often only concerned to replace the soil water lost in transpiration as might be calculated using equation 1. Therefore simple volumetric measures of soil moisture content may be adequate, or indeed most appropriate, as long as information is available on the amount of water loss that can be sustained without yield loss.
A general problem with estimation of soil moisture content or potential arises because of the substantial heterogeneity within soils, with single point measurements rarely being representative. This necessitates either substantial replication of soil moisture sensors or, even better, a combination of a wide distribution of soil moisture sensors with an irrigation system capable of targeted variable water application.
In plants, although water potential terminology has been strongly proposed as the most rigorous basis for assessment of plant water status on the grounds that differences in water potential drive water flow in the soil–plant–atmosphere system, one should note that different sub-components are relevant to flow in different situations with, for example, the osmotic component not being relevant in the absence of semi-permeable membranes (e.g. in the case of xylem flow or water movement in soils). Mass flow in such cases is driven by pressure differences or, where height differences are involved, by differences in hydraulic potential (= p+g).
It has also been clear for some time that biochemical systems in plants do not appear to have sensing mechanisms that can detect/respond to (or to water activity) over the small range of water activity changes (at most a few per cent; compare equation 3) as plants lose turgor and the capacity to grow or survive (Sinclair and Ludlow, 1985). For example, this lack of physiological sensitivity for processes such as photosynthesis has been demonstrated clearly in experiments comparing the effects of the addition of non-permeating and permeating osmotica (e.g. ethylene glycol) to leaf slices (Jones, 1973a). Addition of concentrations of the permeating solute ethylene glycol that lowered the water potential by around 1.5 MPa had no significant effect on the photosynthesis rate of leaf slices, while addition of an equivalent concentration of non-permeating osmotica (mannitol or sodium chloride) substantially inhibited photosynthesis (Fig. 1). As the permeating osmotica equilibrate rapidly across the plasma membrane, cell volume (and hence cell turgor) would be expected to change little as water potential was lowered in this case, leading to the conclusion that it must have been the change in either the turgor pressure or the cell volume, rather than the change in water potential per se, that caused the inhibition of photosynthesis. Though it is usually difficult to devise experiments to distinguish volume from turgor effects, studies with isolated protoplasts (Kaiser, 1982) have suggested the importance of cell volume. It is likely therefore that the many documented cases where drought responses have been associated with changes in water potential result from the common, but often coincidental, close association between turgor and total water potential rather than resulting from any true dependence on water potential.
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More recently, substantial evidence has been accumulating that membrane stretch-sensitive channels (Alexandre and Lassalles, 1991; Cosgrove and Hedrich, 1991; Lew, 1996; Ramahaleo et al., 1996) may be primary sensors of mild water deficits, although redox-state sensing may also be important [see, for example, Kacperska (2004) for a review especially covering the downstream signal transduction]. Since the early findings there have been many studies confirming the general importance of processes related to cell turgor as a key signal of water deficit stress, for which RWC can frequently be used as a good proxy measure, although some conversion factor may be needed to make the most of it. A consequence of the physiological importance of turgor pressure is that the cell wall elasticity takes on a crucial role in determining cell responses to declining water availability (Schulte, 1992).
Notwithstanding all this evidence, many workers still consider measurement of water potential the ‘gold standard’ for physiological studies. It seems to me that it is now time for a fundamental reassessment of this view, as there are few cases where total water potential can be shown to be the causal variate underlying physiological responses and adaptations. The emphasis on water potential seems misleading as the real value of water potential is only as a means of deriving the more ‘important’ variables such as turgor pressure using equation 4. A clear example where it is easy to see that total water potential may be misleading is in the case of osmotic adjustment: this does not directly affect water potential yet may improve the ability of plants to take up water from the soil simply by maintaining positive turgor pressure at lower tissue water potentials than would otherwise be the case. This point is discussed further below.
Also note that different methods of measurement give different answers. The leaf psychrometer attempts to estimate the total leaf water potential (= +P) but the pressure chamber measures the xylem pressure potential (= –xylem–). In most cases the error is small, but the result may be misleading in cases where there are significant apoplastic solutes (James et al., 2006).
Where in the soil–plant system should water status be measured?
The usual (often implied) concept is that water status should be measured ‘at the site of the process of interest’ (Spomer, 1985). For example, those physiologists concerned with the study of leaf processes such as photosynthesis or stomatal opening have frequently concentrated on measurements of leaf water status, while those concerned with growth have concentrated on the water status of the appropriate meristem. The increasing recognition of the importance of within-plant signalling by non-hydraulic means (reviewed by Davies and Zhang, 1991) has cast substantial doubt on the applicability of the above principle. Rather, the existence of root–shoot signalling implies that, in many cases, the water status should be measured at the site of signal generation [e.g. abscisic acid export or re-export in the roots (Hartung et al., 2002), or pH regulation in the xylem (Wilkinson and Davies, 2002)] rather than in the leaf.
Notwithstanding the evidence for the importance of chemical signalling in plants, there is still an important role for conventional hydraulic signalling, which may be more or less important in different plants (Fuchs and Livingston, 1996). For example, cavitation in the stem as water deficits increase can act as a hydraulic signal, substantially lowering leaf (Jones and Sutherland, 1991; Sperry et al., 1998), while some modelling studies suggest that processes such as transpiration in some species are more closely related to leaf water status than to soil water (Lynn and Carlson, 1991). In practice, it is often difficult to determine precisely where in the soil–plant system it is appropriate to measure because of the feedbacks involving control of water status. These feedbacks mean that it is often difficult to disentangle or break the correlations between, for example, soil and leaf that result from conventional hydraulic signalling (Jones, 1997). There are substantial differences between isohydric plants such as cowpea and maize and anisohydric plants such as sunflower (Bates and Hall, 1981; Tardieu and Simonneau, 1998). In the former, stomatal control (as a result of root–shoot signalling) tends to maintain leaf water status, and hence turgor, stable as soil dries. Therefore, in the isohydric case, leaf turgor (or leaf) cannot be used as a measure of stress, while in more anisohydric plants leaf turgor declines in parallel with soil drying so it is difficult to distinguish the causal stress for any physiological response.
Measurements of leaf can be used to infer at other places in the soil–plant system. For example, predawn leaf is thought to equilibrate closely with soil/root , so it is frequently used as an indicator of soil or root that avoids some of the problems associated with direct soil measurement. Indeed it is widely used as a measure of stress in irrigation experiments (Ameglio et al., 1998; de Souza et al., 2003; Remorini and Massai, 2003). Alternative approaches to the estimation of the potentially more relevant root, based on measurements made at more experimentally convenient times, are either pressure chamber measurements of leaf on root suckers pre-equilibrated in the dark to allow equilibration with root (Higgs and Jones, 1991; Simonneau and Habib, 1991) or the calculation of the root appropriate for a transpiring plant based on leaf and stomatal conductance (Jones, 1983).
When should measurements be made?
When choosing a sampling/measurement strategy for water status it is also necessary to consider the appropriate time of day for measurement. Historically plant physiologists have concentrated on simultaneous measurement of characters such as leaf function (e.g. photosynthesis) and leaf water status. Many physiological and developmental responses and adaptations to drought, however, occur as a result of the temporally and spatially integrative responses controlled through hormonal signalling and involving substances such as cytokinins and abscisic acid. These themselves may have substantial lags in their expression, so instantaneous comparisons with local water status are only likely to be appropriate for those responses directly dependent on local water status (e.g. stomatal apertures are determined directly by differences in turgor pressure of guard and subsidiary cells) (Munns et al., 2000). Even in the case of stomatal aperture, however, the ion fluxes that determine the relevant turgor pressures are dependent on integrative signalling systems.
Schematic low time resolution-smoothed average trends in leaf water potential over a typical field drying cycle are illustrated in Fig. 2a, with the corresponding higher temporal resolution data shown schematically in Fig. 2b. There are several points to note from these graphs: the first is that the absolute value of leaf (or any related variable such as turgor pressure) varies diurnally over perhaps an order of magnitude; the second is that substantial changes occur even over time scales as short as minutes (Jones, 1990); and thirdly these short-term changes can be substantially larger than treatment differences, even when clear differences in growth rate or other physiological response have been achieved.
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Drought adaptation in the field usually involves developmental responses occurring over periods of days to weeks. There is little definitive information as to whether it is an integrated measure of water status that provides the controlling signal or whether it may be the maximum daily deficit. In any case, it is difficult to see how the rapidly varying and environmentally extremely sensitive
leaf can provide an appropriate long-term signal of stress, especially as it is clear that treatment differences are often smaller than short-term fluctuations in (Fig. 2b; Jones, 1983; Jones et al., 1983), especially in isohydric species. A further difficulty with integration is that, though it is computationally easy to integrate a linear response (e.g. as day-MPa which is analogous to thermal time), physiological responses to water status tend not to be linear (Jones, 1992). An advantage of predawn leaf measurements as a measure of water stress is that they tend to integrate short-term changes in water status. An alternative approach that also smoothes out some of the short-term variation in leaf is to use the stem which is the potential of leaves pre-equilibrated in the dark, giving an estimate of xylem; this can also be better than leaf as an indicator of stress (McCutchan and Shackel, 1992). |
Some specific ‘case-studies’ and water-status measurement in molecular studies |
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TopAbstractIntroductionWhy measure water status?General principles and...Choice of water-status measure...Some specific 'case-studies' and...Conclusions and recommendationsReferences |
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The methods available for measurement of water status relevant to different applications are outlined below and their relative merits summarized in Table 1 for a number of typical experimental situations.
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Practical management and irrigation scheduling
Since natural droughts develop over timescales of days to weeks and the developmental or adaptive responses also occur over similar timescales, the most appropriate measures of stress for agronomic purposes are integrated over time and space. This therefore suggests that more integrative soil moisture measurements would be preferred to instantaneous measures such as midday
leaf (especially where weather conditions are variable). Predawn leaf and, to a lesser extent, stem may be useful surrogates for soil. Similarly, remote-sensing approaches would have particular advantages because of their capacity to integrate over large areas, although again, those methods such as microwaves that can estimate soil water content may be preferable for agronomic purposes to those (e.g. canopy temperature) that give instantaneous values of crop physiological status. A capacity for automation is particularly valuable for irrigation scheduling: for example, methods for estimation of soil moisture status based on measurement of soil dielectric constant (time-domain reflectometry, etc.) are particularly suitable for routine recording but usually provide rather poor spatial replication unless large sensor networks are installed. Plant measurements tend to be more difficult to automate; direct measures of water status such as the pressure bomb have never been successfully automated and, although psychrometers can be automated, they tend to be expensive and somewhat unreliable, only giving good data in expert hands. This has led, for agronomic purposes, to a greater emphasis on indirect methods, in spite of their problems, such as dendrometry/morphometrics, thermal sensing of stomatal closure, etc. (Huguet et al., 1992; Naor and Cohen, 2003; Jones, 2004a).
Studies of water movement
Thermodynamic and water potential terminology come into their own when considering water flow in the soil–plant–atmosphere system, as water flow is directly dependent on differences in the appropriate components of water potential (together with the relevant resistances to flow). Most publications on this subject use fully appropriate measures of water status.
Mechanisms of water stress effects on growth and physiology
There is an enormous current interest in improving the drought tolerance of crops. The ‘rational’ approach is to elucidate existing drought tolerance mechanisms in different plant species or cultivars and to identify the genes involved so that they can be incorporated into improved cultivars. This requires an understanding of the physiological basis of drought tolerance in existing cultivars/wild lines and the variation that exists; in particular, it is necessary to consider the trade-offs between increased survival in dry conditions and the tendency for reduced production. The particular balance between survival and production, and hence the optimal value of specific characters such as stomatal closure or osmotic adjustment, tends to depend critically on the environment in which the plant is to be grown (e.g. terminal drought versus random drought events) as well as on the harvested component of the plant.
As has been pointed out by many authors (Jones et al., 1989; Jones, 1992; Passioura et al., 1993; Kramer and Boyer, 1995; Sinclair and Purcell, 2005) drought tolerance is an emergent property involving a wide range of component processes such as drought escape (e.g. as a result of early maturity), drought avoidance (e.g. through control of water loss or enhanced root uptake), biochemical tolerance of tissue water deficits (favouring survival), and efficiency of water use. Only in rare agricultural situations is survival of drought a key character in agronomic drought tolerance (Sinclair and Purcell, 2005).
In order to understand fully the balance between the different drought-tolerance strategies and their values to plants, it is essential that the experimental protocols include measurements of both environmental stress (e.g. soil moisture and its distribution) and the plant responses (including tissue water status and controls of water uptake and loss such as leaf area and stomatal conductance). Crucially it is also necessary that the drought treatments imposed in experimental systems are similar in intensity to the stresses that occur naturally.
Screening for drought tolerance and plant breeding
In the field:
A common approach to identifying drought-tolerant genotypes is to screen for overall yield under dry conditions. Unfortunately the genotypic rankings and even the location of quantitative trait loci from such screens are very dependent on the range of environments chosen (Hall et al., 2005; Atlin et al., 2006). High-yielding genotypes under a terminal drought scenario, for example, may not perform so well with intermittent drought. For the terminal drought, early maturing genotypes often perform best and therefore may be classified as drought tolerant solely as a result of their phenology, not as a result of any specific ‘drought tolerant’ physiology. A further complication is that, in many agricultural situations, the most drought-tolerant lines are not necessarily those with the highest potential yields, but those with the most stable yields over a range of water availabilities.
Effective interpretation of field screens in terms of the mechanism giving rise to any apparent drought tolerance (including distinguishing phenological differences and drought escape, drought avoidance, and desiccation tolerance mechanisms) requires the measurement of both the dynamics of soil moisture availability in the rooting zone of each specific cultivar and the corresponding tissue water status changes (at least RWC or preferably both P and ). In addition, these data need supplementing with information on the control of water loss (e.g. leaf area and stomatal behaviour). In practice, it may not be feasible to obtain such a full data set for all entries in this type of trial, but interpretation, and subsequent incorporation into a breeding programme, will be greatly facilitated by measurements of tissue water status at key developmental stages.
An alternative approach to the discrimination of tolerance mechanisms is to control the water supply to each genotype on the basis of measurements of tissue water status. This facilitates the separation of drought escape and drought tolerance mechanisms. For example, Yue et al. (2006) adjusted sowing dates in a drought screen of different lines of rice so that key growth stages are synchronized, and based individual plant watering regimes on measurements of tissue water status.
Plant breeders have made some progress by combining specific drought-tolerance characters such as improved water use efficiency (Condon et al., 2004) into commercial lines that perform well under specific drought conditions, with some recent advances in understanding the underlying genetics (Masle et al., 2005). The hope is that further improvements in crop drought tolerance can be facilitated by rational combination of appropriate physiological characters. There is unlikely, however, to be a unique ideal combination for these characters for drought tolerance, as many processes can combine in different ways in different genetic backgrounds and environments.
Molecular studies:
A large proportion of modern molecular research on drought tolerance attempts to identify those genes whose expression contributes to differences in drought tolerance. Although by no means universal, a substantial proportion of such studies lack any rigorous measurement of either the environmental stress imposed or the resulting tissue water status. Table 2 summarizes the broad types of water-status measures that have been reported in a selection of recent papers (between 2003 and July 2005) where the main objectives have included an analysis of molecular responses to drought. Results are separated into those papers published in some more ‘molecular’ journals such as Plant Physiology, Plant Molecular Biology, The Plant Journal, and The Plant Cell and more ‘physiological’ journals such as Journal of Experimental Botany and Plant, Cell and Environment. The summary data in Table 2, where over half the papers in more molecular journals had no measure of water status whatsoever, raise serious concerns.
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Where there is a lack of critical information on water status it follows that the experiments are likely to be both difficult to repeat with any certainty and, more importantly, almost certainly limits the value of the information collected. The problems arising from the limited information are of several types, many of which could be avoided by careful experimental design.
- (i) The first common problem is that, notwithstanding the complexity of drought responses and adaptations outlined above, drought tolerance is frequently equated with survival or the proportion of tissue death (Yamaguchi-Shinozaki and Shinozaki, 1994; Cheong et al., 2003; Sugano et al., 2003; Chini et al., 2004; Chen et al., 2005). The widespread use of this measure of drought tolerance probably arises in part because of the ease of conducting severe ‘all-or-nothing’ experiments, where clear responses are readily detectable, and the perception that, as long as the stress is severe enough, it does not need to be measured.
- (ii) A related point is that assessment of survival requires the desiccation of the tissues to water potentials substantially below those that are commonly observed under typical drought conditions in agriculture and that are known to cause severe yield losses. Although it is rare for any information to be provided on the actual tissue desiccation achieved in experiments, some data are available (Boominathan et al., 2004; Kawaguchi et al., 2004) confirming that the tissue water status achieved (RWC of 49–55%) can be in the range that would normally be expected to lead to severe tissue damage and is much below the normal range in agricultural crops (Barrs, 1968). In both these papers (Boominathan et al., 2004; Kawaguchi et al., 2004) the ‘controls’ were close to 80% RWC, which is a value that already corresponds, for many plants, to severe dehydration and a water potential of around –3 MPa (Jones and Higgs, 1979); this is well below the value where turgor is commonly lost and growth stops. It could be argued therefore that such experiments can only yield information of limited relevance to the key genes involved in the subtle responses to the mild droughts that are agriculturally more relevant (see also Sinclair and Purcell, 2005).
- (iii) A third common problem is that many studies do not take adequate precautions to ensure that the ‘stress’ treatments are truly comparable between test lines. For example, it is common to withhold water for an extended but fixed period, and to compare the response in terms of survival or yellowing of a range of lines, mutants, or transgenics (Cheong et al., 2003; Chini et al., 2004; Chen et al., 2005). Where the lines being compared have differences in leaf size (Chen et al., 2005; De Block et al., 2005) or, less obviously in stomatal conductance, rates of drying may be very different, and thus differences in survival may indicate only differences in water use, not tissue tolerance. In such cases the survivors are unlikely to be particularly productive. Although these differences may be of great interest, it would be of value to have the necessary information to allow dissection of the mechanism(s) involved. A better, more quantifiable, approach could be to apply treatments that ensure comparable tissue water status for the different experimental lines. For example, the use of tissue equilibration at a given water content pioneered by Henson and Quarrie (1981) in their genetic studies of abscisic acid accumulation might be worth further consideration.
- (ii) A related point is that assessment of survival requires the desiccation of the tissues to water potentials substantially below those that are commonly observed under typical drought conditions in agriculture and that are known to cause severe yield losses. Although it is rare for any information to be provided on the actual tissue desiccation achieved in experiments, some data are available (Boominathan et al., 2004; Kawaguchi et al., 2004) confirming that the tissue water status achieved (RWC of 49–55%) can be in the range that would normally be expected to lead to severe tissue damage and is much below the normal range in agricultural crops (Barrs, 1968). In both these papers (Boominathan et al., 2004; Kawaguchi et al., 2004) the ‘controls’ were close to 80% RWC, which is a value that already corresponds, for many plants, to severe dehydration and a water potential of around –3 MPa (Jones and Higgs, 1979); this is well below the value where turgor is commonly lost and growth stops. It could be argued therefore that such experiments can only yield information of limited relevance to the key genes involved in the subtle responses to the mild droughts that are agriculturally more relevant (see also Sinclair and Purcell, 2005).
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Conclusions and recommendations |
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TopAbstractIntroductionWhy measure water status?General principles and...Choice of water-status measure...Some specific 'case-studies' and...Conclusions and recommendationsReferences |
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Although the need for good and appropriate measurements of water status is well recognized for studies of water movement in the soil–plant system and in crop physiology, such measurements are often not made in more molecular studies. An associated problem is that the drought treatments imposed in many molecular studies are often rather unrealistic so that the results may have little relevance to the common objective justification of the work to ‘improve agricultural production’. It would seem that enhanced inputs from environmental plant physiologists could benefit experimental design and enhance the value of the molecular studies for agricultural purposes. In general, although any measure of water status is better than none, a choice of measures including both the environmental stress and the plant water status will substantially enhance the information obtained. What is required for future experiments is a greater use of repeatable protocols that allow researchers to identify specific genes explicitly related to key processes involved in drought tolerance for incorporation into new varieties.
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Acknowledgements |
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Part of the work described here was supported by the UK Department for the Environment, Agriculture and Rural Affairs under project HH3609TX.
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References |
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