Annals of Botany 61, 433-449, 1988

433

A Review of Evidence on the Control of Shoot:Root Ratio, in Relation to Models

J. BASTOW WILSON*
Department of Botany and Microbiology, University College of Wales, Aberystwyth, SY23 3DA, UK Accepted: 6 October 1987

ABSTRACT Four basic models exist for the control of shoot: root ratio (S: R): (a) allometric models, proposing a fixed ratio of shoot growth rate to root growth rate; (b) functional equilibrium models, based on the ratio of shoot activity to root activity; (c) the Thornley model, based on carbon and nitrogen uptake and transport, (d) hormone models, generally suggesting the root produces a hormone that controls the shoot and vice versa. Models (a) and (b) are empirical, and therefore provide no test of the processes operating. Ontogenetic changes in S: R for fibrous-rooted herbs could be fitted by a modified Thornley model. Ontogenetic effects must be excluded in judging other effects. Responses of S: R to deficits of water, major inorganic nutrients, light and carbon dioxide, and to defoliation and root pruning, usually conform to Thornley's model. With current knowledge Thornley's model cannot usefully be applied to minor nutrients, nutrient toxicity or temperature differences. S:R changes at reproduction usually conform to Thornley's model if it is assumed that young reproductive structures are a strong sink, but this begs the question of what determines sink strength. There are apparent exceptions to most of these responses, which should be studied further. Phytohormones can influence S:R, but may not be the control operating in the normal, intact plant. Most of the available evidence is compatible with a source-sink model of Thornley's type, and therefore does not demand a hormonal theory of S:R control. There is a need for more critical tests. Key words: Shoot:root ratio, strategy, partitioning, models.

INTRODUCTION

The plant comprises a number of parts which must remain in practicable proportion to one another, Plants that are all root, or all leaf, do not occur, More subtly, the proportions of leaf, stem and root on a plant remain in at least approximate equilibrium. The simplest equilibrium is between the amount of shoot material and the amount of root material - the shoot: root ratio (S: R). Cody (1966) pointed out that it is possible to think of organisms as having a limited amount of energy available for expenditure, and of natural selection as that force which operates in the allocation of this energy in the way that maximizes the contribution of the genotype to following MODELS generations. Harper and Ogden (1970) applied this Models of plant growth can be purely empirical, to plants by examining the proportion of energy fitting equations to the phenomena observed, or allocated to reproductive structures. Much con- they can be mechanistic, attempting to model the sideration has been given to the conditions under processes that comprise plant growth in the hope which particular reproductive strategies should be that if these processes are modelled realistically the Present address for correspondence: Botany Depart- observed phenomena will be exhibited by the ment, University of Otago, P.O. Box 56, Dunedin, New model. Models of shoot:root ratio control have Zealand. included these two types, with intermediates. 0305-7364/88/040433 + 17 $03.00/0 1988 Annals of Botany Company

optimal. This concept of strategy (Jain, 1979) applies not only to the balance between vegetative structures and reproductive structures, but also to that between any other partition of plant growth, for example, partition between shoot and root (Iwasa and Roughgarden, 1984). Given that S:R is controlled, the question remains as to how it is controlled. Models, of various degrees of sophistication, have been proposed for the controlling mechanism, but there had been no overall evaluation of the ability of these models to explain the observed behaviour of plants. This paper attempts to do so.

434

WilsonModels of Shoot: Root Ratio empirical one. It tells us nothing of the mechanism by which assimilate is partitioned 'to maintain a balanced functional economy throughout the plant.' Davidson admitted: 'no attempt is made to define the causal mechanism'. Thornley's model Pearsall (1923) and White (1937) proposed that root growth was determined by the residue of assimilate available after the shoot had used its requirements. Shank (1945) proposed the corresponding mechanism that when any soil factor (nutrient or water) was limiting, a larger proportion was retained in the roots, decreasing the proportion of shoot to root growth. White suggested the C:N ratio in the plant was the controlling factor, and Brouwer (19626) extended this to a model in which growth was controlled by carbohydrates and nitrogen. Under nitrogen deficiency, the greater part of the N taken up was used by the root system for root growth, thus decreasing S: R. Deficiency of other minerals, or of water, would have the same effect. Under carbohydrate deficiency, the opposite mechanism would work. Thornley (1972) put such a model into mathematical form. Thornley's is a mechanistic model, based on the supply, transport and utilization of carbon and nitrogen. There are many simplifying assumptions, such as single pools of labile C and N in the shoot and in the root. The value of models is that they can show us how many aspects of plant behaviour can be predicted from only the most basic of plant processes. The two basic features of the model are the way growth in the shoot and the root (separately) depend on the concentrations of labile carbon (C) and nitrogen (N), and the transport of C and N between shoot and root. Growth is assumed to depend on the concentration of both C and N, in an asymptotic manner. At low levels of C or N, growth is linearly related to the supply, and there is a gradual approach to saturation. Translocation is assumed to depend on the difference in concentration between the shoot and the root, and resistance. Although C and N certainly do not move by diffusion, a roughfitto diffusion formulae seems reasonable. The main area where the model was not intuitive was in the resistance; Thornley found that only a resistance that was inversely proportional to the size of the plant would give steady-state growth. Even one-directional transport is a simplification, for some carbon compounds are certainly translocated from root to shoot, and much of the N translocated from root to shoot is subsequently retranslocated to the root (Lambers et al., 1982).

Allometric models Pearsall (1927) and Troughton (1956) applied the allometric growth formula to the shoot/root balance: , t y = bxc, where y is the dry weight of the root, x is the dry weight of the shoot, and b and k are constants. This formula can also be written: log y = log b + k. log x, which allows a straight-line plot. This model is entirely empirical; it does not attempt to explain growth processes, but it enables the relation between the weights of the shoot and the root to be expressed in a simple manner, and therefore makes it easy to see any departures from a particular relation, for example when the plant starts to flower. Troughton pointed out that the model implied a fixed ratio (log b) between the relative growth rate (RGR) of the shoot and that of the root. Barnes (1979) extended the allometric model to allow for changes in the allometric relation with time.
Functional equilibrium models

Troughton's model fits S: R only under one set of environmental conditions; functional equilibrium models attempt to explain plastic changes in S:R. We can trace such models from Brenchley (1916), who stated 'the plant makes every endeavour to supply itself with adequate nutriment, and as if, when the food supply is low, it strives to make as much root growth as possible'. Brouwer (1963) spoke of the relation between shoot and root being regulated by activities, and later (Brouwer, 1966) of weight/activity ratios. This model was expressed formally by Davidson (1969 a) as root mass. rate of absorption oc leaf mass . rate of photosynthesis. Although Davidson used the leaf mass in his model, he used the shoot mass in displaying his results. Hunt and Burnett (1973) amended the formula, replacing 'leaf mass' with 'shoot mass' and expressing photosynthesis as Unit Shoot Rate. Hunt and Nicholls (1986) expressed the model in terms of environmental stress. Reynolds and Thornley (1982) and Johnson (1985) produced similar models, in which the C:N ratio in the storage pools determines the partition between shoot and root growth by some unspecified means. Gadgil and Gadgil (1979) and Iwasa and Roughgarden (1984) expressed essentially the same model in terms of optimality theory. The functional equilibrium model is again an

WilsonModels of Shoot: Root Ratio Brugge (1985) refined Thornley's model to include rooting at different depths, and root maintenance, senescence, ruboff and exudation. Hole et al. (1984) suggested that a simple sourcesink hypothesis was inadequate, and that anatomical ontogeny might be important. Hormone models Keeble (1931) seems to have been the first to propose that shoot: root integration was dependent on hormones produced by one, stimulating growth of the other. Luckwill (1960) developed this idea, seeing S: R as controlled by the dependence of root growth on factors from the shoot, including the unknown 'rhizocaline', and the dependence of shoot growth on an unknown 'caulocaline'. Others recognized auxin as rhizocaline (Bonner and Galston, 1952) and cytokinins as caulocaline (Russell, 1977). Some workers have considered that their results cannot be explained on a translocation/sink basis (e.g. Benjamin and Wren, 1980). As a result, the suggestion has been made many times that S: R is normally controlled by hormones (e.g. Evenari, 1962; Wilkinson and Ohlrogge, 1964; Buttrose and Mullins, 1968; Vaadia and Itai, 1969; Wareing, 1970; Richards and Rowe, 19776; Russell, 1977; Lambers, 1979; Peterson et al., 1984; Cruz et al., 1986). As will be discussed later, the exogenous application of hormones can affect S: R, and such experiments have also led workers to suggest that hormones are natural regulators of root growth (e.g. Stenlid, 1982). Moreover, when more than two compartments are considered, a third factor limiting growth must be postulated for stable control, which might be a hormone (Thornley, 1976). Goodwin et al. (1978) worked out the possible details of such hormonal control. It is useful in science to nominate a simple or null hypothesis that has logical primacy (Simberloff, 1983). This is the basis of Occam's Razor accepting the simplest hypothesis that fits the facts. In this case there are several reasons for nominating as the null hypothesis that of no hormonal control. It is simpler, in that we have to accept anyway that assimilate supply and mineral nutrients can limit plant growth. Moreover, the mechanism itself is simpler. The idea that growth uses up substrate, and slows when substrate is in short supply, and the idea of a resistance to transport, require little further justification. By contrast, a hormonal explanation requires that the hormone source must detect any shoot:root imbalance before it can send a hormonal message which must then be decoded by the target organ. In using a no-hormone theory as null hypothesis, I do not suggest that hormones cannot affect S: R, ONTOGENY

435

it is clear that they can. Nor do I suggest that some control over S:R in a normal plant may not be hormonally mediated. Rather, I suggest that by identifying which of the known phenomena can be explained without hormones, we can more rigorously test the hypothesis of hormonal control and identify the circumstances in which it is important.

The shoot: root ratio usually changes as the plant grows. Since size and time differences during vegetative growth are usually equivalent (Troughton, 1956), many time differences are probably just a reflection of size, even though Brouwer (1966) suggested that it was a case of 'differentiation'. As a general rule, S:R of herbaceous plants increases with age/size (e.g. Troughton, 1956; Bray, 1963; Ryle, Arnott and Powell, 1981; Bourdot, Saville and Field, 1984). It is interesting that Thornley rejected a hydraulic analogy model in which resistance was proportional to the length divided by the cross-sectional area of the stem, apparently because conductance did not keep pace with the growth in plant volume, resulting in a steadily increasing S:R. Perhaps resistance is proportional to the length divided by the cross-section, and this is the cause of changes in S:R during growth. The main exception for herbaceous plants is that root crops are often reported to have a decreasing S:R (Ford and Thorne, 1967). Currah and Barnes (1979) analysed this very carefully for carrot; they found that it was an age effect, not a size effect; they also found that early in development S:R increases, but beyond a certain age it starts to decrease. It is easy to see this as a result of natural or artificial selection for a large root at the end of the season, but this does not explain the mechanism. It could be that conductance rises more rapidly than plant volume, due to plant morphology or anatomy (Hole et al., 1984), though Barnes (1979) discounted such an explanation. It could also be seen as the effect of the tap root as a strong sink, though that begs the question of what makes it act in this way. With woody species, the most common situation is a continuous decrease in S:R (Wareing, 1950; Ledig, Bormann and Wenger, 1970). In other cases S: R has been shown to decrease at first and then increase later (Balagopalan and Alexander, 1981; Walters and Freeman, 1983), or the reverse (Mullin, 1963), but it is difficult to distinguish between ontogenetic and seasonal changes in this work. Bray (1963) found no ontogenetic change. Ledig et al. (1970) saw the usual trend as adaptive-storage and anchoring structure in woody perennials. Almost all the work has been

436

WilsonModels of Shoot .Root Ratio

with seedlings; realistic root recovery from adult tissues. When nitrogen is not limiting, and so long as toxic levels are not reached, the difference in trees is difficult. Thus, ontogenetic changes for herbs are pre- concentration should produce no differential dicted by an earlier version of Thornley's model, growth between the shoot and the root. When though not by his final one. Root crops are nitrogen levels are lower and limiting they will still problematical in interpretation, and woody plants be lower in the shoot than in the root; McDonald, in both data and interpretation. Indirect effects of Lohammar and Ericsson (1986) showed that in environmental factors on S: R, via their effects on the days after nitrogen availability was decreased growth and hence on ontogeny, should be excluded it was the leaf nitrogen that was most affected. Therefore, the growth of the shoot will be reduced in considering the effects of those factors (Ledig more than that of the root, as observed. Thornley's et al., 1970). model would predict a build-up in carbohydrate OSCILLATIONS levels under nutrient deficiency, and this has been Season is the main determinant of phenology, and observed (e.g. McDonald et al, 1986). it is well known that one aspect of phenology Thornley's model was defined with carbon and affected by season is the relative amounts of shoot nitrogen controlling growth. However, nitrogen growth and root growth (e.g. Parsons and Robson, could equally be replaced with any other nutrient 1981). Some woody plants seem to show fluctua- that behaves in the same way in plants, i.e. is taken tions in the ratio of shoot growth to root growth up mainly through the roots, is translocated to the (e.g. Reich et al., 1980). shoot against resistance, is taken up faster at higher Drew and Ledig (1980) and Drew (1982) have concentrations, and affects shoot and root functionclaimed to find episodic fluctuations in the ratio of ing according to similar equations. The exact shoot growth to root growth. They see this as a relation between nutrient concentration and root mechanism that maintains an 'adaptive' shoot: and shoot functioning should not affect the root ratio. Borchert (1973) modelled the process. qualitative behaviour of the model. However, the episodes Drew and Ledig (1980) and Some workers have found no change in S:R Drew (1982) found were in adjacent harvest intervals. Apparently the same set of plants was when nutrient levels are varied, but this has usually used for the final weight in one harvest-interval been accompanied by the absence of an effect on and the initial weight in the next. This means that growth, indicating that the nutrient was not any random fluctuations in S:R of this set of deficient in any of the treatments. Rufty et al. (1984), examining nitrogen deplants will show as opposite deviations in the increment ratio for the two harvest-intervals. It is ficiency, found redistribution of growth occurring therefore possible that the oscillations of these before any drop in overall growth rate; there was workers is an artefact. This does not mean that the therefore an absolute increase in root growth ratio is not controlled as they suggest, but that the during the first two weeks of deficiency. Yeager control may operate more efficiently and oscil- and Wright (1981) also reported an absolutely greater root mass at lower nitrogen supply in one lations are not seen. of two experiments, and there is some evidence for this in Hirose and Kitajima's (1986) experiment. These observations conflict with Thornley's INORGANIC NUTRIENTS model; further investigation would be valuable. Major nutrients Others have reported an absolute increase in root Many records exist of differences in shoot:root length but not in dry weight (e.g. Krigel, 1967). As was discussed above, Thornley's model ratio at different levels of inorganic nutrients in the rooting medium. For major nutrients, they almost involves a large number of simplifications. Many all show a lower S: R when a particular nutrient is are reasonable. Most nutrients are indeed taken up deficient (e.g. Asher and Ozanne, 1967; Loneragan mainly through the roots, though leaves have a and Asher, 1967; Davidson, 1969*; Hunt, 1975; considerable ability to absorb nutrients (e.g. Caloin, Khodre and Atry, 1980; Yeager and Parker and Boswell, 1980). The exact behaviour of Wright, 1981; McCain and Da vies, 1983). It is elements in translocation is little known, though clear by comparing multiple harvests that in at the resistance to K translocation seems to increase least the results of Caloin et al. (1980) and Rufty, as the plant grows (Widders and Lorenz, 1982). Raper and Huber (1984) this is not an ontogenetic One worrying simplification is that the model effect. assumes that the effect of mineral nutrient supply This result is compatible with Thornley's model. will be via the incorporation of assimilate into Because of the transport resistance, nitrogen is structural plant material, leaving the photosynmore available in the root, though this is difficult thetic rate constant. In fact, there is evidence for to demonstrate because of differences between many nutrients of a direct effect on photosynthesis,

WilsonModels of Shoot: Root Ratio and biochemical reason in many cases why this should be so. Such an increase in photosynthesis rate in Thornley's model would tend to produce the opposite effect, of a higher S: R with nutrient deficiency. An increase in mineral nitrogen supply usually increases the rate of photosynthesis (Yeager and Wright, 1981; Frank and Marek, 1983), probably through the contribution of nitrogen to the molecules of enzymes, perhaps especially RuBP carboxylase. However, nitrogen is a structural component of a vast range of important plant compounds, and notably of all proteins. In fact, the response of plants to nitrogen deficiency is almost always in the direction predicted by Thornley's model (e.g. Davidson, 19696; Hunt, 1975; Caloin et al., 1980; Yeager and Wright, 1981). Milford and Watson (1971) saw a increase in the carbohydrate content of nitrogen deficient plants, as predicted by Thornley's model. An increase in phosphate supply usually increases the rate of photosynthesis (Bottrill, Possingham and Kriedemann, 1970). This may be because of the need for phosphate compounds in the photosynthetic machinery (Sawada, Igarashi and Miyachi, 1983), perhaps ATP (Machler, Schnyder and Nosberger, 1984). However, phosphate does not specifically promote photosynthesis, phosphates such as ATP are important intermediates in most aspects of metabolism. (In contrast, Gregory and Richards (1929) found that phosphate deficient plants tended to have a higher photosynthetic rate.) In fact, the response of plants to phosphate deficiency is almost always in the direction predicted by Thornley's model (e.g. Davidson, 1969ft; McCain and Davies, 1983). Potassium supply also limits photosynthesis (Bottrill et al, 1970), and Gregory and Richards (1929) found that potassium deficiency depressed photosynthesis more than deficiencies of nitrogen. It has been suggested that the effect of potassium is indirect, via the effect on stomatal opening and hence on carbon dioxide supply (Madore and Grodzinski, 1984). Apart from its role in stomatal mechanism, the reasons for potassium requirement in plants are remarkably non-specific to any metabolic process let alone to any organ (Clarkson and Hanson, 1980). Potassium can affect S:R in the same direction as other major nutrients. For example, Steen (1984), working with Atriplex, found that potassium increased S:R more than any other nutrient or combination tried. Toxicity Even the major nutrients become toxic beyond a certain concentration, though that concentration depends on other environmental conditions. This

437

is true for nitrogen (MacLeod, 1969; Ingestad and Lund, 1979), phosphate (Asher and Loneragan 1967; Warren and Benzian, 1959) and potassium (MacLeod, 1969). Following the general model of Thornley, though not his formulae, we can predict that the same mechanism that enables root growth to benefit in comparison to shoot growth when nutrients are deficient will suppress root growth more than shoot growth when levels become toxic. Unfortunately, few of the investigators showing toxicity have reported root weights. Ingestad and Lund (1979) found a slight tendency for S:R to increase at toxic levels of nitrogen. In Loneragan and Asher's (1967) work there was only one species that showed phosphate toxicity, and there was no change in S: R associated with it; Ozanne, Keay and Biddiscombe (1969) found no change in S:R associated with phosphate toxicity; Wilson and Haydock (1971) found a slight increase in S:R at toxic levels of N and P; Loustalot and Winters (1948) found no consistent trends. Minor nutrients For these the picture is less clear. Boron affects photosynthesis, possibly via potassium supply (Dugger, 1983). Its general mode of action is hard to pinpoint, but it may be via membrane function (Clarkson and Hanson, 1980; Shkolnik, 1984). Bottrill et al. (1970) and Bouma (1969) found an increased S: R with boron deficiency. Calcium is required for the integrity of the plasmalemma. This is true in the shoot as well as the root, but it is at the soil/root interface that these abilities become especially crucial. Veierskov and Meravy (1985) found an increase in carbohydrate with calcium deficiency, but Bottrill et al. (1970) observed only a small effect of calcium deficiency on S: R. Copper is part of the molecule of plastocyanin of the electron transport chain and therefore affeets photosynthetic rate (Drozdov, 1958; Shkolnik; 1984), but it is also necessary for the action of a number of enzymes. Bottrill et al. (1970) found no effect of copper deficiency on S: R. Iron also has a large effect on photosynthesis (Bottrill et al, 1970), probably because it is required for the synthesis of chlorophyll (Terry, 1978) and it is part of the molecule of ferredoxin. However, it is part of a number of metalloproteins active throughout the plant. Bottrill et al. (1970) showed little effect on S:R. Magnesium is important for photosynthesis as part of chlorophyll molecule (Peaslee and Moss, 1966), but it also promotes the activity of a number of enzymes (Clarkson and Hanson, 1980), and is required for ribosomal integrity. In fact,

438

WilsonModels of Shoot: Root Ratio by a resistance, but this is the normal model (Newman, 1969). As with mineral nutrients, there remains the problem of a direct effect of water deficit reducing photosynthetic rate. This does occur (Finn and Brun, 1980; Singh and Sasahara, 1981). It can be attributed to stomatal closing (Hanson and Hitz, 1982), greater mesophyll resistance to CO 2 diffusion (Vapaavuori, Korpilahti and Nurmi, 1984), dehydration and hence loss of efficiency by carbon dioxide-absorbing surfaces (Singh and Sasahara, 1981), cytoplasmic water stress reducing enzyme activities, and changes in RNA and protein content and character (Shah and Loomis, 1965). However, water deficiency will affect not only the photosynthetic enzymes but all enzymes, in fact almost all aspects of a plant's physiology (Todd, 1972). It will therefore affect the rate at which assimilate is converted into plant structure. It is not clear whether water stress will have a greater effect on photosynthesis or growth. One could argue that photosynthesis is affected not only enzymatically but also via carbon dioxide supply, and would therefore be affected more. This would lead to a decrease in carbohydrate concentrations in the water-deficient plant, before growth decreased. In fact, most reports are of an increase in carbohydrate concentrations during water stress (e.g. Zholkevich and Koretskaya, 1959; Munns, Brady and Barlow, 1979; Kigel and Dotan, 1982), though Thakur and Rai (1980) found that mannitol-induced water stress led to a general decrease in starch and reducing-sugar content, and Woodhams and Kozlowski (1954) found a slight decrease in all types of carbohydrate after 8 d water stress. The usual response suggests that the net effect of water stress is to limit growth more than photosynthesis, making water analogous to mineral nutrients in Thornley's model. The usual responses of shoot:root ratio to changes in the soil water availability parallel those for nitrogen: when water is in short supply assimilate is directed more towards the root (Finn and Brun, 1980; Chung and Trlica, 1980) and S:R is lower (e.g. Troughton, 1960; Davidson, 1969ft; Baser, Jaggiand and Sinha, 1981; Schwintzer and Lancelle, 1983), irrespective of ontogenetic changes (Troughton, 1960). In contrast, Cruz et al. (1986) found a lower S:R in irrigated rice, which they attributed to mechanical impedance in dry soil. Baser et al. (1981) found that when the water table was close to the surface, reducing growth in comparison with optimal water supply presumably because of waterlogging, S:R decreased again. Thornley's model would not explain an absolute increase of root mass under water deficiency, but I

magnesium deficiency sometimes decreases S:R (Bottrill et al., 1970) and sometimes increases it. Manganese deficiency showed an effect on photosynthesis in spinach second only to that of nitrogen in Bottrill et a/.'s (1970) experiments. It seems to be required in the reactions of Photosystem II (Bishop, 1971). Whilst it may be involved in other enzymatic reactions, Shkolnik (1984) suggests its principal effect is on photosynthesis. Bottrill et al. (1970) found a higher S:R with manganese deficiency, but Ohki (1984) found little effect. Molybdenum is part of nitrate reductase, but also has other roles (Shkolnik, 1984). Bottrill et al. (1970) found a small increase in S:R with molybdenum deficiency. Sulphur seems to affect photosynthesis in a number of ways, via the chlorophyll content, via CO 2 assimilation, via the photoreduction of ferrocyanide (Terry, 1976). It is a structural component of a number of enzymes. Deficiency of it can have rather little effect on S:R (Bottrill et al., 1970). Zinc also affects the rate of photosynthesis (Bottrill et al., 1970; Ohki and Young, 1979), perhaps because of some involvement of the zinccontaining carbonic anhydrase, but more than 20 enzymes in the plant are zinc-dependent. Bottrill et al. (1970) showed only a slight decrease in S:R with zinc deficiency. Thus, there is some evidence that no S:R response is seen with deficiencies of those minor nutrients that are important in photosynthesis. Conclusion Thornley's model explains most observed plant responses to major nutrients. The rare exceptions would be worth further investigation. There is too little evidence from toxicity to draw conclusions. Minor nutrients often display effects in the opposite direction. It is usually possible to explain this by suggesting that the particular nutrient has more effect on photosynthesis than on growth, but this is no test of the model. The best that can be said is that minor nutrients provide no evidence validating or contradicting the model.

WATER Water, like inorganic nutrients, is absorbed primarily by the roots, some is translocated to the shoot, and an adequate supply is necessary for growth of shoots and roots. Therefore water should behave in the same way as nitrogen in Thornley's model. Not only can the translocation of it from shoot to root be thought of as controlled

WilsonModels of Shoot: Root Ratio can find no case of this in the literature. Reports of an absolute increase in root length are common (e.g. Huck et al., 1986), and represent plastic response of unknown cause. Therefore it is quite possible to fit the observed response to water deficit to Thornley's model, but this provides little positive support for the model since, with the assumption of a greater effect of water deficit on photosynthesis, it would have been possible to fit an opposite response.

439

seems premature to suggest the existence of a ' light factor' on such evidence. Thus, the evidence on response of S: R to shade is entirely compatible with Thornley's model. CARBON DIOXIDE LEVEL Many species respond to concentrations of carbon dioxide above normal ambient levels with faster growth. Thornley's model can be applied directly, as with light, since if CO 2 increases growth it is almost certainly via an increase in photosynthetic rate. The predicted decrease in shoot: root ratio at higher CO 2 has generally been found (e.g. Ford and Thorne, 1967; Hurd, 1968; Sionit et al., 198 la, b; Scheidegger and Nosberger, 1984; Whipps, 1985; Potvin and Strain, 1985). In the case of fibrous-rooted herbs there is no confusion with ontogeny, since CO2-induced growth would raise S:R, and CO 2 tends to decrease it, and all the examples just given show the effect with fibrousrooted herbs. Excluding experiments where CO2 level was non-limiting, there is little exception. However, Sionit, Hellmers and Strain (1982) found no clear S: R response in maize, MacDowall (1972) found no clear effect at low light levels, and Oberbauer, Strain and Fetcher (1985) found a response opposite to the usual one, though not significantly so. In Thornley's model there would be an increase in carbohydrate pools, and this has been observed (Scheidegger and Nosberger, 1984). Thus, the usual response of S: R to CO 2 is that predicted by Thornley's model. TEMPERATURE Several authors have reported effects of temperatures, uniform or differentially applied to shoot and root, on shoot:root ratio. Differential temperatures are the most interesting, since we can assume effects on shoot and root activities independently. Brouwer (1964), Nielsen et al. (1960), Tow (1967), Cooper and Thornley (1976), GanmoreNeumann and Kafkafi (1983), Kleinendorst and Veen (1983), Szaniawski (1983), Hogue and Neilsen (1986) and Clarkson, Hopper and Jones (1986) found that as root temperature was increased, keeping shoot temperature constant, S: R increased. Davidson (1969 a) showed that whilst this was true for a number of species, it applied only up to their optimum temperature for growth; above optimum temperature, S:R fell again in some species. In many cases the change in S:R may be simply an ontogenetic effect. However, McAdam and Hayes (1981) found such a decrease

LIGHT Thornley's model can be applied directly to light, since if light increases growth it is almost certainly via an increase in photosynthetic rate. This would decrease the shoot: root ratio in Thornley's model, as has generally been found (e.g. Troughton, 1960; Hughes and Cockshull, 1971; MacDowall, 1972; Raper et al., 1978; Crapo and Ketellapper, 1981; Bourdot et al, 1984; Caloin and Yu, 1984). In the case of fibrous-rooted herbs there is no confusion with ontogeny since increased growth would raise S:R, and all the examples just given are with fibrous-rooted herbs. MacDowall's (1972) low light treatments show ontogenetic trends in the same direction as light effects, but the intercepts are different. Confusion with ontogenetic changes does arise for tap-rooted herbs and for woody seedlings. Although Ekwebalam and Reid (1984) claimed an effect of light on S:R of pine seedlings, a plot of their figures shows, as with Ledig et al. (1970) in another species of pine, that all the differences in S:R can be explained as indirect effect of size. Legid and Perry (1965) suggested that S:R is less plastic in woody plants. Lambers, Kuiper and Van der Toorn (1985) showed S:R to be more plastic in a hayfield population of plantains than in a meadow population. This can be seen as evidence that S: R control has evolved as an adaptation, that is it not simply a by-product of growth processes. By Thornley's model, the effect of higher light on S:R should be accompanied by an increase in carbohydrate pools, especially in the root. Atkinson (1984) and Setter, McDavid and Lopez (1984) found such an increase; it was greater in the leaf than in the root. Lambers and Posthumus (1980), finding an increase in S:R in shade, did not find any differences in carbohydrate. They therefore suggested the existence of a 'light factor', distinct from carbohydrate supply, affecting S:R. However, changes in carbohydrate supply may be partially hidden by consequential changes in carbohydrate utilization. We do not know what size of change to expect in the net concentration. It

440

WilsonModels of Shoot: Root Ratio can be complete (Parker and Sampson, 1930), and can happen within hours (Crider, 1945; Evans, 1971; Hodgkinson and Becking, 1977). It has been called 'root growth stoppage'. Not only growth is stopped, Oswalt, Bertrand and Teel (1959) found a complete stoppage in phosphate uptake. Effects are not always as fast and dramatic as this, and there are differences between species (Hodgkinson and Becking, 1977), but such a response seems almost always to occur. Effects of defoliation have been seen also in increased root mortality, and decreased root branching (Hodgkinson and Becking, 1977). Brouwer (1966) saw root growth stoppage as being caused by a reduction in the assimilatory surface, and a consequential reduction in carbohydrate supply. King, Lamb and McGregor (1978) observed which parts of the plant were most affected by various degrees of defoliation, and saw in the results evidence for the effect being caused by acropetal movement of assimilates. Ryle and Powell (1975) found direct evidence using a radioactive tracer-in the first four days after defoliation, assimilate that would normally have gone to the roots was retained in the shoot. These effects are directly compatible with Thornley's model. Defoliation will reduce the photosynthesizing tissue. In most plants, leaves have a disproportionate amount of photosynthesizing tissue, therefore defoliation will reduce the photosynthesizing tissue more than it reduces the sink for assimilate. This will reduce the availability of assimilate in the plant, and therefore act on S: R in the same way as does low light. Some workers have found mobilization of storage carbohydrate (e.g. Bokhari, 1977). This is not incompatible with Thornley's model. It is possible that such an effect would be evident in a decreased concentration of carbohydrates, especially in the root, and Sullivan and Sprague (1943), Nishikawa (1964) and Evans (1972) found this. Moreover, glucose in the root medium partly restored the root growth of defoliated plants. Evans' work provides excellent, though circumstantial, evidence for root growth stoppage being caused by carbohydrate deficiency. With growth reduced, but nutrient uptake not directly affected, a build-up in nutrients might occur in the roots, though Whitehead (1983) found the opposite. There have also been reports of defoliation causing increased photosynthetic rate in the remaining leaves (Myers and Ferree, 1983; Nowak and Caldwell, 1984), perhaps due to a delay in senescence. Sweet and Wareing (1966) attributed this to 'root factors', which implies hormonally mediated shoot:root control, but Hansen (1978)

in maize well below the optimum root temperature for growth, as did Cumbus and Nye (1985) in rape, and in general Kummerow and Ellis (1984) in two sedges. Discrepancies between reports may be because of interactions with other factors; Nielsen el al. (1961) and Nielsen and Cunningham (1964) found the direction of the temperature response to depend on the mineral nutrient supply. If an increase in S: R occurs because nutrient uptake is faster, internal nutrient levels should increase, and by Thornley's model more so in the shoot than in the root. Clarkson et al. (1986) found this. The usual response is the teleological' adaptive' one: at higher temperatures the root works faster, so there does not need to be as much of it. Davidson's hypothesis of a constant ratio between the activity of the shoot and that of the root puts the same in more acceptable language, but does not explain how the control is achieved. The response is compatible with Thornley's model if we assume that the only effect of root temperature is to increase the activity of the root in absorbing nutrient, which is what Davidson's model assumes. It was this assumption that enabled Cooper and Thornley (1976) to fit Thornley's model. If we consider that temperature might increase the rate of conversion of carbon and nutrient into root structure, the model with that effect alone would predict a lower S: R at higher root temperature. Perhaps this is the cause of the results of McAdam and Hayes (1981), Cumbus and Nye (1985) and Kummerow and Ellis (1984). Increasing shoot temperature, by the same argument, should decrease S:R as Kummerow and Ellis (1984) found in general, though Kleinendorst and Veen (1983), McAdam and Hayes (1981) and Cumbus and Nye (1985) found the opposite, at least in McAdam and Hayes' case apparently independent of ontogenetic effects. There are also reports of the effects of overall (shoot and root) differences in temperature. Raper et al. (1978), found that at higher temperatures, S: R was increased. To fit this with either Davidson's or Thornley's models, we would need to assume that the Q lo of nutrient uptake is greater than that of photosynthesis. There seems inadequate evidence at present to conclude this. Thus, the application of Thornley's model to temperature effects demands that we know more about the way temperature affects growth than we do; no critical test is possible. DEFOLIATION It is a very common observation in the literature that defoliation or shoot removal causes a reduction in root growth (e.g. Kny, 1894). This reduction

WilsonModels of Shoot: Root Ratio and others have suggested a release from feedback inhibition of photosynthesis by assimilate accumulation. An absolute increase in shoot growth on defoliation/pruning would conflict with the Thornley model. Myers and Ferree (1983) reported such an effect, but only in shoot length, leaf area, etc.; they did not estimate dry weight growth. A similar report for dry weight would be very interesting. Thus, the evidence on defoliation does not conflict with Thornley's model. The effect of sink demand on photosynthetic rate may be operating; it is unclear whether this is due to assimilate feedback or to hormonal control.

441

ROOT PRUNING If pruning of the shoot leads to a redirection of growth towards the shoot, thus tending to restore the shoot:root ratio, it is natural to ask whether pruning of the root leads to an analogous redirection of growth towards the root, again tending to restore the ratio. Brouwer (1963), REPRODUCTION asserted that root pruning reduces leaf growth and accelerates root growth. Elegant as such a con- Developing sexual reproductive structures, part of clusion is, the evidence for it is less than clear-cut. the shoot, are strong sinks for assimilates (Rook There is much less evidence available than for and Sweet, 1970). It is therefore not surprising to shoot removal, no doubt partly because of the find reports that the onset of reproduction leads to difficulty of manipulating roots. There is also the an increase in the shoot: root ratio (e.g. Troughton, intrinsic difficulty in removing a representative 1956; 1960; Schuurman and de Boer, 1970; fraction of the root system in tap-rooted plants. Parsons and Robson, 1981; Barraclough, 1984; Humphries (1958) showed that root pruning of Josefusova, Opatra and Pavlova, 1985). Chung tomato plants affected the growth of the shoots and Trlica (1980) observed the same effect in much more than the growth of the roots, so that carbon translocation. The change is usually quite the ratio of shoot increment to root increment was sharp, and in Troughton's work occurred in those decreased - assimilate was indeed directed towards species/cultivars that flowered and generally not the roots. Similar results have been obtained for in those that remained vegetative. other species by Maggs (1964), Buttrose and In Schuurman and de Boer's work the change in Mullins (1968), Benjamin and Wren (1980), S:R occurred just before the first inflorescence Crossett, Campbell and Stewart (1975), Richards appeared, but in the work of Troughton, Barraand Rowe (1977 a), Biddington and Dearman clough and Josefusova et al. the change in (1984), Wiedenroth and Erdmann (1985) and shoot:root partitioning occurred well before the Carmi (1986). floral organs appeared, but quite possibly after the In contrast, Alexander and Maggs (1971) with floral initials had been produced. Even so, this sweet orange seedlings, and Geisler and Ritz implies for a Thornley-type model that floral (1981) with wheat, found that root pruning organs are a strong sink for assimilate when still increased the ratio of shoot increment to root very small. Perhaps so, but perhaps we are coming increment. Detling et al. (1980) followed the to the limit of a Thornley model. Josefusova et al. response to root pruning, and found that for the (1985) suggested, from rather oblique evidence, first week after pruning, less assimilate was that the suppression of root growth in flowering allocated to the roots than in the controls, but that was controlled separately from flowering itself, perhaps by high IAA levels. after three weeks a greater proportion was. However, the majority of experiments menThe issue is seen most starkly with Troughton's tioned above imply a redirection of assimilates to- (1960) experiment with vernalized seed. Here wards the root. Ghobrial (1983) showed this di- plants that had been florally induced by seed rectly, though not particularly clearly, using 14CO2. vernalization showed an increased S: R compared

Buttrose and Mullins (1968) explained such results on the basis of reduced production of rootproduced hormones that stimulated shoot growth. If that is the mechanism, removing the root tips should have a similar effect to removing whole roots, since cytokinins and gibberellins are produced mainly in the tips (Russell, 1977); yet James and Hutto (1972) found this treatment to stimulate growth. If a Thornley-type mechanism is operating when root pruning redirects assimilate towards the root, it would be via a relative deficiency of mineral nutrients in the shoot. Anderson (1980) found such an effect for the potassium concentration, but not for nitrogen, phosphate, calcium or magnesium. This could be because these elements were limiting to growth. There might also tend to be some build-up of assimilates, and Benjamin and Wren (1980) found this for insoluble carbohydrates but not for soluble carbohydrates. Thus, the usual response to root pruning is compatible with Thornley's model, though some results stand out as incompatible.

442

WilsonModels of Shoot: Root Ratio of GA reduce it (Brouwer and Kleinendorst, 1968; Thomas, Currah and Salter 1973; Carmi and Koller, 1977; Currah and Thomas, 1979; Thomas et al., 1983; Wright et al., 1983). There may be a link with reproduction, since GA causes the production of a culm and flowering in many rosette biennials such as the carrot. It might be part of the action of GA, in promoting flowering, to change the partition of assimilate, making more available to the shoot and thus allowing the development of the culm. On the other hand, GA might have caused the apex to become reproductive, a reproductive apex might be a stronger sink, and it might be this stronger sink that is causing more assimilate to be retained in the shoot. Richards and Rowe (19776) found that cytokinin-like BA increased S:R of peach. Such an effect could be via the ability of cytokinins to inhibit root growth (Stenlid, 1982), or via a redirection of assimilate transport (Gersani, Lips and Sachs, 1980). However, the latter story is complicated; the response to BA applied to the shoot was the opposite of that when it was applied to the root. These experiments do not exclude the primary control's being by mineral nutrient supply, since cytokinins can affect nitrogen translocation (Simpson, Lambers and Dalling, 1982). Wittwer and Dedolph (1963) found that in tomato, kinetin in the rooting medium reduced S:R. Auxins can also affect assimilate transport (Gersani et al., 1980), and inhibit root growth (Scott, 1972; Dubucq, Hofinger and Gaspar, 1978) or promote it (Carmi and Koller, 1977). Watts et al. (1981) found that the effect of water stress on S:R could be mimicked by ABA. Since water stress normally causes an increase in endogenous ABA, it is possible that the water-stress response is normally mediated by ABA. This evidence is circumstantial. Carmi and Heuer (1981) investigated the role of growth regulators in a system where bean plants were grown in very small pots. Compared to plants in larger pots, growth was reduced but S:R was increased. Carmi and Heuer concluded that this growth reduction was not due to the supply of water or inorganic nutrients, not only because they were supplied in large amounts, but also because the water potential and nutrient concentrations were actually higher in the dwarfed plants. Carmi and Shalhevet (1983) showed very similar effects in cotton. Carmi and Heuer found that the exogenous application of GA and BA together to plants in small pots increased growth almost to that seen in larger pots. They therefore concluded that the effect of pot size was caused by reduction in the supply of growth regulators, GA and cytokinins, from the root to the shoot. Krizek et al. (1985)

to unvernalized plants. Troughton employed the standard technique of a log root vs. log shoot plot, and reports that there was no evidence of a change in this relationship when flowering started. It is hard to see reproductive initials having been present immediately after germination, and impossible to envisage their being a strong sink there without hormonal direction of nutrient transport. However, Troughton argued from a lack of evidence for any departure from the allometric line. It is dangerous to draw conclusions from inability to demonstrate a difference, especially since he presented no plots of the points. In contrast, Brouwer (1962 a) found that removing flowers and young fruits allowed the vegetative S: R distribution to remain unaltered. This suggests that it is the presence of reproductive sinks, not the reproductive switch itself, which affects S:R. Thus, the evidence on reproductive effects is compatible with a Thornley model if one assumes the developing reproductive organs to be a very strong sink. However, what causes the sink? Troughton's vernalization experiment stands out; an attempt to repeat it would be useful. MANIPULATIONS If water is differentially available to parts of the root system, the part with the greater supply grows more (Coutts, 1982). A similar effect is seen with nutrients such as nitrate, ammonium and phosphate (Drew, 1975; Coutts and Philipson, 1977; Drew and Saker, 1978). Robinson and Rorison (1983) found localized changes in morphology. Such effects are not always seen-Drew (1975) found an effect with nitrate and ammonium but not with potassium; Borkert and Barber (1983) found no effect even with phosphate, and Robinson and Rorison (1983) found their localized changes in one species but not in two others. These effects could fit a Thornley-type model if within-root resistances are considered. HORMONES It has been suggested that plant hormones (chemical growth regulators) are involved in the control of shoot:root ratio. One type of evidence is the effect of exogenously applied hormones. Such work has been criticized on the grounds that correlations are no evidence of hormonal control in the normal plant. However, if growth regulators are important in normal control, it seems likely that exogenous application of them would modify S:R. Experiments on carrot have shown that gibberellic acid (GA) increases S: R, and antagonists

WilsonModels of Shoot: Root Ratio showed a similar small container effect and could not attribute it to water stress, though in their experiment the change in S: R was small. Peterson et al. (1984) found reduced growth and increased S: R in small pots; this could not have been due to NPK deficiency in the small pots, since the concentrations of all three were greater. Thus, the application of hormones suggests that it is possible that hormones are normal mediators of S:R control. Watts et al.'s experiment is particularly suggestive of normal hormonal control. Carmi and Heuer's experiments strongly suggest that in their very unusual experimental conditions a hormonal imbalance is responsible for the effects seen. CONCLUSIONS Hormones certainly can have an effect on shoot: root ratios. However, the vast majority of observations on the plastic responses of plants are compatible with a model of Thornley's general type, where S:R is controlled by the supply of assimilates, mineral nutrients and perhaps water. There is a need for more critical tests of the hypothesis. Observations of carbohydrate and nutrient concentrations are valuable, but too open to interpretation to be critical evidence. New predictions need to be made and tested, and previous crucial work repreated, such as Troughton's on vernalization. In the meantime, in so far as a working hypothesis is needed, Occam's Razor indicates that it should be of Thornley's (1972) type.
LITERATURE CITED
ALEXANDER, D. M C E . and MAGGS, D. H., 1971. Growth

443

BALAGOPALAN, M. and ALEXANDER, T. G., 1981. Shoot

and root growth in Eucalyptus tereticornis seedlings. Indian Journal of Forestry 4, 238-9. BARNES, A., 1979. Vegetable plant part relationships. II. A quantitative hypothesis for shoot/storage root development. Annals of Botany 43, 487-99. BARRACLOUGH, P. B., 1984. The growth and activity of winter wheat roots in the field: root growth of highyielding crops in relation to shoot growth. Journal of Agricultural Science 103, 439-42.
BASER, D. K., JAGGI, I. K. and SINHA, S. B., 1981. Root

and shoot growth and transpiration as influenced by various depths of water table. Z. Acker- und Pslanzenbau, 150, 390-9.
BENJAMIN, L. R. and WREN, M. J., 1980. Root develop-

ment and source-sink relations in carrot, Daucus carota L. Journal of Experimental Botany 31, 1139-46.
BIDDINGTON, N. L. and DEARMAN, A. S., 1984. Shoot

and root growth of lettuce seedlings following root pruning. Annals of Botany 53, 663-8. BISHOP, N. I., 1971. Photosynthesis: the electron transport system of green plants. Annual Review of Biochemistry 40, 197-226. BOKHARI, U. G., 1977. Regrowth of western wheatgrass utilizing 14C-labelled assimilates stored in belowground parts. Plant and Soil 48, 115-27.
BONNER, J. and GALSTON, A. W., 1952. Principles of

Plant Physiology, 449 pp. W. H. Freeman, San Francisco.

BORKERT, C. M. and BARBER, S. A., 1983. Effect of

supplying P to a portion of the soybean root system on root growth and P uptake kinetics. Journal of Plant Nutrition 6, 895-910. BORCHERT, R., 1973. Simulation of rhythmic tree growth under constant conditions. Physiologia Plantarum 29, 173-80.
BOTTRILL, D . E., POSSINGHAM, J. V. a n d K.RIEDEMANN,

The response of Achillea millefolium L. (yarrow) to shading. New Phytologist, 97, 653-63. BRAY, J. R., 1963. Root production and the estimation of net productivity. Canadian Journal of Botany 41, ANDREWS, R. E. and NEWMAN, E. I., 1970. Root density 65-72. and competition for nutrients. Oecologia Plantarum BRENCHLEY, W. E., 1916. The effect of the concentration 5, 319-34. ASHER, C. J. and LONERAGAN, J. F., 1967. Response of of the nutrient solution on the growth of barley and plants to phosphate concentration in solution wheat in water cultures. Annals of Botany 30, culture. I. Growth and phosphorus content. So/7 77-90. Science 103, 225-33. BROUWER, R., 1962 a. Distribution of dry matter in the and Ozanne, P. G., 1967. Growth and potassium plant. Netherlands Journal of Agricultural Science content of plants in solution cultures maintained at 10, 361-76. constant potassium concentrations. So/7 Science 19626. Nutritive influences on the distribution of 103, 155-61. dry matter in the plant. Netherlands Journal of ATKINSON, C. J., 1984. Quantum flux density as a factor Agricultural Science 10, 399-408. controlling the rate of growth, carbohydrate par1963. Some aspects of the equilibrium between titioning and wood structure of Betula pubescens overground and underground plant parts. Mededeseedlings. Annals of Botany 54, 397-411. ling 213 van het I.B.S., 31-9.

responses of sweet orange seedlings to shoot and root pruning. Annals of Botany 35, 109-15. ANDERSON, C. A., 1980. Effect of trunk girdling, root pruning, and blight on sweet orange fruit quality and leaf mineral composition. HortScience 15, 395.

P. E., 1970. The effect of nutrient deficiencies on photosynthesis and respiration in spinach. Plant and Soil 32, 424-38. BOUMA, D., 1969. Effects of changes in boron nutrition on growth and development of subterranean clover. Australian Journal of Biological Sciences 22, 52333.
BOURDOT, G. W., SAVILLE, D. J. and FIELD, R. J., 1984.

444

WilsonModels of Shoot: Root Ratio

nutrition on the root development of trees. Journal of Experimental Botany 28, 1071-5.
CRAPO, N. L. and KETELLAPPER, H. J., 1981. Metabolic

1964. Responses of bean plants to root temperatures. I. Root temperatures and growth in the vegetative stage. Mededeling 235 van het I.B.S. 11-22 1966. Root growth of grasses and cereals, pp. 153-166 In The Growth of Cereals and Grasses eds F. L. Milthorpe and J. D. Ivins, 358 pp. Butterworths, London. and Kleinendorst, A., 1968. Responses of bean plants to root temperatures. III. Interactions with hormone treatments. Mededeling 341 van het I.B.S., 11-28. BRUGGE, R., 1985. A mechanistic model of grass root growth and development dependent upon photosynthesis and nitrogen uptake. Journal of Theoretical Biology 116, 443-67.
BUTTROSE, M. S. and MULLINS, M. G., 1968. Propor-

priorities with respect to growth and mineral uptake in roots of Hordeum, Triticum and Lycopersicon. American Journal of Botany 68, 10-16. CRIDER, F. J., 1945. Root growth stoppage. Technical Bulletin of the U.S. Department of Agriculture 1102, 3-23.
CROSSETT, R. N., CAMPBELL, D. J. and Stewart, H. E.,

1975. Compensatory growth in cereal root systems. Plant and Soil 42, 673-83.
CRUZ, R. T., O'TOOLE, J. C, DINGKUHN, M., YAMBAO, E. B., THANGARAJ, M. and D E DATTA, S. K., 1986.

part relationships. I. Effects of time and population density on the shoot and storage root weights of carrot (Daucus carota L.). Annals of Botany 43, KHODRE, A. EL, and ATRY, M., 1980. Effect of 475-86. nitrate concentration on the root:shoot ratio in and THOMAS, T. H., 1979. Vegetable plant part Dactylis glomerata L. and on the kinetics of growth relationships. III. Modification of carrot (Daucus in the vegetative phase. Annals of Botany 46,165-73. carota L.) root and shoot weights by gibberellic acid CARMI, A., 1986. Effects of cytokinins and root pruning and daminozide. Annals of Botany 43, 501-11. on photosynthesis and growth. Photosynthetica 20, DAVIDSON, R. L., 1969a. Effect of root/leaf temperature 1-8. differentials on root/shoot ratios in some pasture and HEUER, B., 1981. The role of roots in control of grasses and clover. Annals of Botany 33, 561-9. bean shoot growth. Annals of Botany 48, 519-27. 19696. Effects of soil nutrients and moisture on and KOLLER, D., 1977. Endogenous regulation of root/shoot ratios in Lolium perenne L. and Trifolium photosynthetic rate in primary leaves of bean repens L. Annals of Botany 33, 571-7. (Phaseolus vulgaris L.). Annals of Botany 41, DETLING, J. K., WINN, D. T., PROCTOR-GREGG, C. and 59-67. PAINTER, E. L., 1980. Effects of simulated grazing by and SHALHEVET, J., 1983. Root effects on cotton below-ground herbivores on growth, CO 2 exchange, growth and yield. Crop Science 23, 875-8. and carbon allocation patterns of Bouteloua gracilis. 14 CHUNG, H.-H. and TRLICA, M. J., 1980. C distribution Journal of Applied Ecology 17, 771-8. and utilization in blue grama as affected by DREW, A. P., 1982. Shoot-root plasticity and episodic temperature, water potential and defoliation growth in red pine seedlings. Annals of Botany 49, regimes. Oecologia 47, 190-5. 347-57. CLARKSON, D. T. and HANSON, J. B., 1980. The mineral and LEDIG, F. T., 1980. Episodic growth and nutrition of higher plants. Annual Review of Plant relative shoot: root balance in loblolly pine seedlings. Physiology 31, 239-98. Annals of Botany 45, 143-8. HOPPER, M. J. and JONES, L. H. P., 1986. The effect DREW, M. C , 1975. Comparison of the effects of a of root temperature on the uptake of nitrogen and localised supply of phosphate, nitrate, ammonium the relative size of the root system in Lolium and potassium on the growth of the seminal root perenne. I. Solutions containing both NH^ and system, and the shoot, in barley. New Phytologist NOg. Plant, Cell and Environment 9, 535-45. 75, 479-90. CODY, M. L., 1966. A general theory of clutch size. and SAKER, L. R., 1978. Nutrient supply and the Evolution 20, 174-84. growth of the seminal root system in barley. III. COOPER, A. J. and THORNLEY, J. H. M., 1976. Response Compensatory increases in growth of lateral roots, of dry matter partitioning, growth, and carbon and and in rates of phosphate uptake, in response to a nitrogen levels in the tomato plant to changes in localised supply of phosphate. Journal of Experiroot temperature: experiment and theory. Annals of mental Botany 29, 435-51. Botany 40, 1139-52. DROZDOV, S. N., 1958. The effect of copper on the COUTTS, M. P., 1982. Growth of sitka spruce seedlings photosynthetic rate of spring wheat leaves. Doklady with roots divided between soils of unequal matric Akademii Nauk SSSR (Botanical Sciences Section) potential. New Phytologist 92, 49-61. 121,212-15. and PHILIPSON, J. J., 1977. The influence of mineral DUBUCQ, M., HOFINGER, M. and GASPAR, T., 1978.

tional reduction in shoot growth of grapevines with root systems maintained at constant relative volumes by repeated pruning. Australian Journal of Biological Science 21, 1095-1101. CALOIN, M. and Yu, O., 1984. Analysis of the time course of change in nitrogen content in Daciylis glomerata L. using a model of plant growth. Annals of Botany 54, 69-76.

Shoot and root responses to water deficits in rainfed lowland rice. Australian Journal of Plant Physiology 13, 567-75. CUMBUS, I. P. and NYE, P. H., 1985. Root zone temperature effects on growth and phosphate absorption in rape Brassica napus cv Emerald. Journal of Experimental Botany 36, 219-27.
CURRAH, I. E. and BARNES, A., 1979. Vegetable plant

WilsonModels of Shoot: Root Ratio

Auxin-controlled root growth and ethylene production. Plant, Cell and Environment 1, 151-3. DuGGER, W. M., 1983. Boron in plant metabolism, pp. 626-50 In Encyclopedia of Plant Physiology, New Series, vol. 15B, Inorganic Plant Nutrition, 417 pp. Springer-Verlag, Berlin.
EKWEBALAM, S. A. and REID, C. P., 1984. Nitrogen

445

HANSON,

A. D. and

HITZ,

W. D.,

1982. Metabolic

response of mesophytes to plant water deficits. Annual Review of Plant Physiology 33, 163-203.
HARPER, J. L. and OGDEN, J., 1970. The reproductive

strategy of higher plants. 1. The concept of strategy with special reference to Senecio vulgaris L. Journal of Ecology 58, 681-98.
HIROSE, T. and KITAJIMA, K., 1986. Nitrogen uptake and

fertilization and light effects on growth and photosynthesis of lodgepole pine seedlings. Annals of Applied Biology 105, 117-27. EVANS, P. S., 1971. Root growth of Lolium perenne L. II. Effects of defoliation and shading. New Zealand Journal of Agricultural Research 14, 552-62. 1972. Root growth of Lolium perenne L. III. Investigation of the mechanism of defoliationinduced suppression of elongation. New Zealand Journal of Agricultural Research 15, 347-55. EVENARI, M., 1962. Plant physiology and arid zone research, pp. 175-95 In Problems of the Arid Zone, Proceedings of the Paris Symposium, 481 pp. Unesco, Paris. FINN, G. A. and BRUN, W. A., 1980. Water stress effects on COJJ assimilation, photosynthate partitioning, stomatal resistance, and nodule activity in soybean. Crop Science 20, 4314.
FORD, M. A. and THORNE, G. N., 1967. Effect of CO 2

plant growth. I. Effect of nitrogen removal on growth of Polygonum cuspidatum. Annals of Botany 58, 479-86.
HODGKINSON, K. C. and BECKING, H. G. B., 1977. Effect

of defoliation on root growth of some arid zone perennial plants. Australian Journal of Agricultural Research 29, 31-42.
HOGUE, E. J. and NEILSEN, G. H., 1986. Effect of root

temperature and varying cation ratios on growth and leaf cation concentration of apple seedlings grown in nutrient solution. Canadian Journal of Plant Science 66, 637-45.
HOLE, C. C , THOMAS, T. H., BARNES, A., SCOTT, P. A.

and RANKIN, W. E. F., 1984. Dry matter distribution between shoot and storage root of carrot, parsnip, radish and red beet. Annals of Botany 53, 625-31.
HUCK, M. G., PETERSON, C. M., HOOGENBOOM, G. and

concentration on growth of sugar-beet, barley, kale, and maize. Annals of Botany 31, 629-44.
FRANK, R. and MAREK, M., 1983. The response of net

BUSCH, C. D., 1986. Distribution of dry matter between shoots and roots of irrigated and nonirrigated determinate soybeans. Agronomy Journal 78, 807-13.
HUGHES, A. P. and COCKSHULL, K. E., 1971. The ef-

fects of light intensity and carbon dioxide concentration on the growth of Chrysanthemum morifolium cv. Bright Golden Anne. Annals of Botany 35, GADGIL, M. and GADGIL, S., 1979. Adaptive significance 899-914. of the relation between root and shoot growth. HUMPHRIES, E. C , 1958. Effect of removal of a part of Journal of the Indian Institute of Science 61, the root system on the subsequent growth of the 25-40. root and shoot. Annals of Botany 22, 251-7. GANMORE-NEUMANN, R. and KAFKAFI, U., 1983. The HUNT, R., 1975. Further observations on root-shoot effect of root temperature and N O j / N H J ratio on equilibria in perennial ryegrass (Lolium perenne L.). strawberry plants. I. Growth, flowering and root Annals of Botany 39, 745-55. development. Agronomy Journal 75, 941-7. and BURNETT, J. A., 1973. The effects of light GEISLER, G. and RITZ, J., 1981. Untersuchungen zur Spross-Wurzel-Beziehung bei Weizen. I. Zeitschrift intensity and external potassium level on the root/ fur Acker- und Pftanzenbau 150, 161-172. shoot ratio and rates of potassium uptake in perennial ryegrass (Lolium perenne L.). Annals of GERSANI, M., LIPS, S. H. and SACHS, T., 1980. The Botany 37, 519-37. influence of shoots, roots, and hormones on the and NICHOLLS, A. O., 1986. Stress and the coarse distribution of leucine, phosphate, and benzylcontrol of growth and root-shoot partitioning in adenine. Journal of Experimental Botany 31, 777-82. herbaceous plants. Oikos 47, 149-58. GHOBRIAL, G. I., 1983. Effects of root pruning on translocation of assimilates in Phaseolus vulgaris L. HURD, R. G., 1968. Effects of CO2-enrichment on the Journal of Experimental Botany 34, 20-6. growth of young tomato plants. Annals of Botany GOODWIN, P. B., GOLLNOW, B. I. and LETHAM, D. S., 32, 531-42. 1978. Phytohormones and growth correlations, INGEST AD, T. and LUND, A. B., 1979. Nitrogen stress in pp. 215-249. In Phytohormones and Related Combirch seedlings. I. Growth technique and growth. pounds - A Comprehensive Treatise. II, eds D. S. Physiologia Ptantarum 45, 137-48. Leatham, P. B. Goodwin and T. J. V. Higgins, IWASA, Y. and ROUGHGARDEN, J., 1984. Shoot/root 641 pp. Biomedical Press, Amsterdam. balance of plants: optimal growth of a system with many vegetative organs. Theoretical Population GREGORY, F. G. and RICHARDS, F. J., 1929. Physiological Biology 25, 78-105. studies in plant nutrition. I. The effect of manurial JAMES, D. B. and H u r r o , J. M., 1972. Effects of tiller deficiency on the respiration and assimilation rate in separation and root pruning on the growth of barley. Annals of Botany 43, 119-61. Lolium perenne L. Annals of Botany 36, 485-95. HANSEN, G. K., 1978. Utilization of photosynthates for JAIN, S. K., 1979. Adaptive strategies: polymorphism, growth, respiration and storage in tops and roots of plasticity, and homeostasis, pp. 160-87 In Topics in Lolium mulliflorum. Physiologia Plantarum 42, Plant Population Biology, eds S. K. Jain, G. J. 5-13.

photosynthetic rate to irradiance in barley leaves as influenced by nitrogen supply. Photosynthetica 17, 572-7.

446

WilsonModels of Shoot: Root Ratio

and PERRY, T. O., 1965. Physiological genetics of the shootroot ratio. Proceedings of the Society of American Foresters 19, 3943.
LONERAGAN, J. F. and ASHER, C. J., 1967. Response of

Johnson, and P. H. Raven, 589 pp. Columbia University Press, New York. JOHNSON, I. R., 1985. A model of the partitioning of growth between the shoots and roots of vegetative plants. Annals of Botany 55, 421-31.
JOSEFUSOVA, Z., OPATRA, J. and PAVLOVA, L., 1985.

Root-shoot correlation linked with photoperiodic floral induction in Chenopodium rubrum L. Biologia LOUSTALOT, A. J. and WINTERS, F. R., 1948. The effect of Plantarum 27, 386-91. three factorial levels of nitrogen and phosphorus on KEEBLE, F., 1931. The integration of plant behaviour, the growth and composition of Cinchona ledgeriana. p. 447 only. Report of Proceedings of the fifth Plant Physiology 23, 343-50. International Botanical Congress, 679 pp. Cam- LUCKWILL, L. C , 1960. The physiological relationships bridge University Press, Cambridge. of root and shoot. Scientific Horticulture 14, 22-6.
KIGEL, J. and DOTAN, A., 1982. Effect of different MCADAM, J. H. and HAYES, P., 1981. The effect of shoot-

plants to phosphate concentration in solution culture. II. Rate of phosphate absorption and its relation to growth. So/7 Science 103, 311-18.

durations of water withholding on regrowth potential and non-structural carbohydrate content in Rhodes grass (Chloris gayana Knuth). Australian Journal of Plant Physiology 9, 113-20.
KING, J., LAMB, W. I. C. and MCGREGOR, M. T., 1978.

zone and root-zone temperature on the early growth and development of Zea mays Maris Carmine. Record of Agricultural Research (Department of Agriculture for Northern Ireland) 29, 39-45.
MCCAIN, S. and DA VIES, M. S., 1983. Effects of pretreat-

Effect of partial and complete defoliation of white clover plants. Journal of the British Grassland Society 33, 49-55.
KLEINENDORST, A. and VEEN, B. W., 1983. Responses of

young cucumber plants to root and shoot temperatures. Netherlands Journal of Agricultural Science 31, 47-61. KNY, L. 1894. On correlation in the growth of roots and shoots. Annals of Botany 8, 265-80. KRIGEL, I., 1967. The early requirement for plant nutrients by subterranean clover seedlings (Trifolium subterraneum). Australian Journal of Agricultural Research 18, 879-86.
KRIZEK, D . T., CARMI, A., MIRECKI, R. M., SNYDER,

ment with phosphate in natural populations of Agrostis capillaris L. 1. Influences on the subsequent long term yield of, and accumulation of phosphorus in, plants grown from tillers. New Phytologist 94, 367-79.
MACDONALD, A. J. S., LOHAMMAR, T. and ERICSSON, A.,

F. W. and BUNCE, J. A., 1985. Comparative effects of soil moisture stress and restricted root zone volume on morphogenetic and physiological responses of soybean (Glycine max (L.) Merr.) Journal of Experimental Botany 36, 25-38.
KUMMEROW, J. and ELLIS, B. A., 1984. Temperature

1986. Growth response to step-decrease in nutrient availability in small birch (Betula pendula Roth). Plant, Cell and Environment 9, 427-32. MACDOWALL, F. D. H., 1972. Growth kinetics of Marquis wheat. II. Carbon dioxide dependence. Canadian Journal of Botany 50, 883-9. MACLEOD, L. B., 1969. Effects of N, P and K and their interactions on the yield and kernel weight of barley in hydroponic culture. Agronomy Journal 61, 26-9.
MACHLER, F., SCHNYDER, H. and NOSBERGER, J., 1984.

effect on biomass production and root/shoot biomass ratios of two arctic sedges under controlled MADORE, M. and GRODZINSKI, B., 1984. Simulation of environmental conditions. Canadian Journal of net photosynthesis in cucumber leaf discs: effect of Botany 62, 2150-3. K-glyoxylate and KC1. Journal of Experimental LAMBERS, H., 1979. Efficiency of root respiration in Botany, 35, 941-7. relation to growth rate, morphology and soil MAGGS, D. H., 1964. Growth-rates in relation to assimicomposition. Physiologia Plantarum 46, 194-202. late supply and demand. I. Leaves and roots as and POSTHUMUS, F., 1980. The effect of light limiting regions. Journal of Experimental Botany 15, intensity and relative humidity on growth rate and 574-83. root respiration of Plantago lanceolata and Zea MILFORD, G. F. and WATSON, D. J., 1971. The effect of mays. Journal of Experimental Botany 31, 1621-30. nitrogen on the growth and sugar content of sugarSIMPSON, R. J., BEILHARZ, V. C. and DALLING, beet. Annals of Botany 35, 287-300. M. J., 1982. Growth and translocation of C and N MULLIN, R. E., 1963. Growth of white spruce in the in wheat (Triticum aestivum) grown with a split root nursery. Forest Science 9, 68-72. system. Physiologia Plantarum 56, 421-29. MUNNS, R., BRADY, C. J. and BARLOW, E. W. R., 1979. KUIPER, D. and VAN DER TOORN, J., 1985. Genetic Solute accumulation in the apex and leaves of wheat differentiation for physiological and morphological during water stress. Australian Journal of Plant traits in Plantago lanceolata L. and Plantago Physiology 6, 379-89. major L, pp. 195-218. In Structure and Functioning MYERS, S. C. and FERREE, D. C , 1983. Influence of of Plant Populations, 2, eds J. Haeck and J. W. summer pruning and tree orientation on net photoWoldendorp, 405 pp. North-Holland, Amsterdam. synthesis, transpiration, shoot growth, and dryLEDIG, F. T., BORMANN, F. H. and WENGER, K. F., 1970. weight distribution in young apple trees. Journal of The distribution of dry matter growth between the American Society for Horticultural Science 108, shoot and roots in loblolly pine. Botanical Gazette 4-9. 131, 349-59. NEWMAN, E. I., 1969. Resistance to water flow in soil and

Influence of inorganic phosphate on photosynthesis of wheat chloroplasts. I. Photosynthesis and assimilate export at 5 C and 25 C. Journal of Experimental Botany 35, 481-7.

WilsonModels of Shoot: Root Ratio

plant. I. Soil resistance in relation to amounts of root: theoretical estimates. Journal of Applied Ecology 6, 1-12.
NIELSEN, K. F. and CUNNINGHAM, R. K., 1964. The

447

effects of soil temperature and form and level of nitrogen on growth and chemical composition of Italian ryegrass. Proceedings of the Soil Science Society of America 28, 213-18.
NIELSEN, K. F., HALSTEAD, R. L., MACLEAN, A. J., HOLMES, R. M. and BOURGET, S. J., I960. The

of growing plant organs. Annals of Botany 41, 549-56. PEASLEE, D. E. and Moss, D. N., 1966. Photosynthesis in K- and Mg-deficient maize {Zea mays L.) leaves. Proceedings of the Soil Science Society of America 30, 220-3.
PETERSON, C. M., KLEPPER, B., PUMPHREY, F. V. and

RICKMAN, R. W., 1984. Restricted rooting decreases tillering and growth of winter wheat. Agronomy Journal 76, 861-3.
POTVIN, C. and STRAIN, B. R., 1985. Effects of CO 2

influence of soil temperature on the growth and mineral composition of oats. Canadian Journal of Soil Science 40, 255-63.
NIELSEN, K. F., HALSTEAD, R. L., MACLEAN, A. J., BOURGET, S. J. and HOLMES, R. M., 1961. The

enrichment and temperature on growth in two C4 weeds, Echinochloa crus-galli and Eleusine indica. Canadian Journal of Botany 63, 1495-9.
RAPER, C. D., OSMOND, D. L., WANN, M. and WEEKS,

influence of soil temperature on growth and mineral composition of corn, bromegrass and potatoes. Proceedings of the Soil Science Society of America 25, 369-72. NISHAKAWA, K..-I., 1964. Studies on the physiological nature of alfalfa plants. I. The effects of cutting intervals on the growth, top yield and carbohydrate root reserves in alfalfa. Science Reports of the Hyogo University of Agriculture 6 (Agricultural Science series), 89-96.
NOWAK, R. S. and CALDWELL, M. M., 1984. A test of

W., 1978. Interdependence of root and shoot activities in determining nitrogen uptake of roots. Botanical Gazette 139, 289-94.
REICH, P. B., TESKEY, R. O., JOHNSON, P. S. and

HINCKEY,T. M., 1980.Periodicrootandshootgrowth

in oak. Forest Science 26, 590-8.

REYNOLDS, J. F. and THORNLEY, J. H. M., 1982. A

compensatory photosynthesis in the field: implications for herbivory tolerance. Oecologia 61, 311-18.
OBERBAUER, S. F., STRAIN, B. R. and FETCHER, N.,

1985. Effect of CO2-enrichment on seedling physiology and growth of two tropical tree species. Physiologia Planlarum 65, 352-6. OHKI, K., 1984. Manganese deficiency and toxicity effects on growth, development, and nutrient composition in wheat. Agronomy Journal 76, 213-18.
OHKI, K. and YOUNG, C. T., 1979. Photosynthesis,

shoot: root partitioning model. Annals of Botany 49, 585-97. RICHARDS, D. and ROWE, R. N., 1977a. Effects of root restriction, root pruning and 6-benzylamino purine on the growth of peach seedlings. Annals of Botany 41, 729^0. 1977&. Root-shoot interactions in peach: the functions of the root. Annals of Botany 41, 1211-16.
ROBINSON, D. and RORISON, I. H., 1983. A comparison

of the responses of Lolium perenne L., Holcus lanatus L. and Deschampsia flexuosa (L.) Trin. to a localised supply of nitrogen. New Phytologist 94, 263-73.
ROOK, D. A. and SWEET, G. B., 1970. Photosynthesis

carbonic anhydrase and amino acids related to zinc status in cotton, pp. 161-173. In Photosynthesis and Plant Development, eds R. Marcelle, H. Clysters and M. van Poucke, 376 pp. Junk, The Hague.
OSWALT, D. L., BERTRAND, A. R. and TEEL, M. R., 1959.

and photosynthate distribution in Douglas-fir strobili grafted to young seedlings. Canadian Journal of Botany 49, 13-17.
RUFTY, T. W. JR, RAPER, C. D. JR. and HUBER, S. C ,

Influence of nitrogen fertilization and clipping on grass roots. Proceedings of the Soil Science Society of America 23, 228-30.
OZANNE, P. G., KEAY, J. and BIDDISCOMBE, E. F., 1969.

1984. Alterations in internal partitioning of carbon in soybean plants in response to nitrogen stress. Canadian Journal of Botany 62, 501-8. RUSSELL, R. S., 1977. Plant Root Systems, 298 pp. McGraw-Hill, Maidenhead.
RYLE, G. J. A. and POWELL, C. E., 1975. Defoliation and

The comparative applied phosphate requirements of eight annual pasture species. Australian Journal of Agricultural Research 20, 809-18.
PARKER, K. W. and SAMPSON, A. W., 1930. Influence of

regrowth in the graminaceous plant: the role of current assimilate. Annals of Botany 39, 297-310.
ARNOTT, R. A. AND POWELL, C. E., 1981. Dis-

leafage removal on anatomical structure of roots of Stipa pulchra and Bromus hordeaceus. Plant Physiology 5, 543-53.
PARKER, M. B. and BOSWELL, F. C , 1980. Foliar injury,

tribution of dry weight between root and shoot in white clover dependent on N 2 fixation or utilizing abundant nitrate nitrogen. Plant and Soil (ft, 29-39.
SAWADA, S., IGARASHI, T. and MIYACHI, S., 1983. Effects

nutrient intake, and yield of soybeans as influenced by foliar fertilization. Agronomy Journal 72,110-13.
PARSONS, A. J. and ROBSON, M.J., 1981. Seasonal

of phosphate nutrition on photosynthesis, starch and total phosphate levels in single rooted leaf of dwarf bean. Photosynthetica 17, 484-90.
SCHWINTZER, C. R. and LANCELLE, S. A., 1983. Effect of

changes in the physiology of S24 perennial ryegrass {Lolium perenne L.). 3. Partition of assimilates between root and shoot during the transition from vegetative to reproductive growth. Annals of Botany 48, 733-44. PEARSALL, W. H., 1923. Studies in growth. IV. Correlations in development. Annals of Botany 37, 261-75. 1927. Growth studies. VI. On the relative sizes

water-table depth on shoot growth, root growth, and nodulation of Myrica gale seedlings. Journal of Ecology 71,489-501.
SCHEIDEGGER, U. C. and NOSBERGER, J., 1984. Influence

of CO 2 concentration on growth, carbohydrate content, translocation and photosynthesis of white clover. Annals of Botany 54, 735-42.

448

WilsonModels of Shoot: Root Ratio

SCHUURMAN, J. J. and DE BOER, J. J. H., 1970. The

developmental pattern of roots and shoots of oats under favourable conditions. Netherlands Journal of Agricultural Science 18, 168-81. SCOTT, T. K., 1972. Auxins and roots. Annual Review of Plant Physiology 23, 235-58.
SETTER, T. L., MCDAVID, C. R. and LOPEZ, F. B., 1984.

THAKUR, P. S. and RAI, V. K., 1980. Water stress effects on maize: Carbohydrate metabolism of resistant and susceptible cultivars of Zea mays L. Biologia Plantarum 22, 50-6.
THOMAS, T. H., CURRAH, I. E. and SALTER, P. J., 1973.

Photosynthate partitioning in pigeonpea in response to defoliation and shading. Crop Science 24,
SHAH, C. B. and LOOMIS, R. S., 1965. Ribonucleic acid

Effect on carrot root yield and size distribution of the growth-retardants chlormequat chloride and aminozide. Annals of Applied Biology 75, 63-70.
BARNES, A., RANKIN, W. E. F. and HOLE, C. C ,

and protein metabolism in sugar beet during drought. Physiologia Plantarum 18, 240-54. SHANK, D. B., 1945. Effect of phosphorus, nitrogen, and soil moisture on top-root ratios of inbred and hybrid maize. Journal of Agricultural Research 70, 365-77. SHKOLNIK, M. YA., 1984. Trace Elements in Plants, 463 pp. Elsevier, Amsterdam. SIMBERLOFF, D., 1983. Competition theory, hypothesistesting, and other community ecological buzzwords. American Naturalist 122, 625-35.
SIMPSON, R. J., LAMBERS, H. and DALLING, M. J., 1982.

Kinetin application to roots and its effect on uptake, translocation and distribution of nitrogen in wheat (Triticum aestivum) grown with a split root system. Physiologia Plantarum 56, 4305.
SINGH, M. K. and SASAHARA, T., 1981. Photosynthesis

and transpiration in rice as influenced by soil moisture and air humidity. Annals of Botany 48, 513-17.
SIONIT, N., MORTENSEN, D. A., STRAIN, B. R. and

1983. Dry matter distribution between the shoot and storage root of carrot (Daucus carota L.). II. Effect of foliar application of gibberellic acid. Annals of Botany 51, 189-99. THORNLEY, J. H. M., 1972. A balanced quantitative model for root:shoot ratios in vegetative plants. Annals of Botany 36, 431-41. 1976. Mathematical Models in Plant Physiology, 318 pp. Academic Press, London. TODD, G. W., 1972. Water deficits and enzymic activity, pp. 177-216. In Water Deficits and Plant Growth, vol. HI, ed. T. T. Kozlowski 368 pp. Academic Press, New York. Tow, P. G., 1967. Controlled climate comparisons of a tropical grass and legume. Netherlands Journal of Agricultural Science 15, 141-54. TROUGHTON, A., 1956. Studies on the growth of young grass plants with special reference to the relationship between the shoot and root systems. Journal of the British Grassland Society 6, 56-65. TROUGHTON, A., 1960. Further studies on the relationship between shoot and root systems of grasses. Journal of the British Grassland Society 15, 41-7.
VAADIA, Y. and ITAI, C , 1969. Interrelationships of

HELLMERS, H., 1981a. Growth response of wheat to CO 2 enrichment and different levels of mineral nutrition. Agronomy Journal 73, 1023-7.
STRAIN, B. R. and HELLMERS, H., 19816. Effects of

growth with reference to the distribution of growth substances, pp. 65-77. In Root Growth, ed. W. J. Whittington, 450 pp. Butterworths, London.

different concentrations of atmospheric CO 2 on VAPAAVUORI, E. M., KORPILAHTI, E. and NURMI, A. H., 1984. Photosynthetic rate in willow leaves during growth and yield components of wheat. Journal of water stress and changes in the chloroplast ultraAgricultural Science, 97, 335-9. structure with special reference to crystal inclusions. HELLMERS, H. and STRAIN, B. R., 1982. Interaction Journal of Experimental Botany 35, 306-21. of atmospheric CO 2 enrichment and irradiance on VEIERSKOV, B. and MERAVY, L., 1985. Changes in plant growth. Agronomy Journal 74, 721-5. carbohydrate composition in wheat and pea seedSTEEN, E., 1984. Root and shoot growth of Atriplex lings induced by calcium deficiency. Plant Physiology littoralis in relation to nitrogen supply. Oikos 42, 79, 315-17. 74-81. STENLID, G., 1982. Cytokinins as inhibitors of root WALTERS, J. P. and FREEMAN, C. E., 1983. Growth rates and root:shoot ratios in seedlings of the desert growth. Physiologia Plantarum 56, 500-506. shrub Larrea tridentata. Southwestern Naturalist SULLIVAN, J. T. and SPRAGUE, V. G., 1943. Composition 28, 357-63. of the roots and stubble of perennial ryegrass following partial defoliation. Plant Physiology 18, WAREING, P. F., 1950. Growth studies in woody species. I. Photoperiodism in first-year seedlings of Pinus 656-70. sylvestris. Physiologia Plantarum 3, 258-76. SWEET, G. B. and WAREING, P. F., 1966. Role of plant 1970. Growth and its co-ordination in trees, pp. growth in regulating photosynthesis. Nature 210, 1-21. In Physiology of Tree Crops, ed. L. C. Luckwill 77-9. and C. V. Cutting, 382 pp. Academic Press, SZANIAWSKI, R. K.., 1983. Adaptation and functional London. balance between shoot and root activity of sunflower plants grown at different root temperatures. Annals WARREN, R. G. and BENZIAN, B., 1959. High levels of phosphorus and die-back in yellow lupins. Nature of Botany 51, 453-9. 184, 1588. TERRY, N., 1976. Effects of sulfur on the photosynthesis of intact leaves and isolated chloroplasts of sugar WATTS, S., RODRIGUEZ, J. L., EVANS, S. E. and DAVTES, W. J., 1981. Root and shoot growth of plants beets. Plant Physiology 57, 477-9. treated with abscisic acid. Annals of Botany 47, 1978. Photosynthesis, growth, and the role of 595-602. chloride. Plant Physiology 60, 69-75.

WilsonModels of Shoot: Root Ratio

449

WHIPPS, J. M., 1985. Effect of CO 2 concentration on WILSON, J. R. and HAYDOCK, K. P., 1971. The comparagrowth, carbon distribution and loss of carbon from tive response of tropical and temperate grasses to the roots of maize. Journal of Experimental Botany varying levels of nitrogen and phosphorus nutrition. 36, 644-51. Australian Journal of Agricultural Research 22, 573-87. WHITE, H. L., 1937. The interaction of factors in the growth of Lemna. XII. The interaction of nitrogen WITTWER, S. H. and DEDOLPH, R. R., 1963. Some and light intensity in relation to root length. Annals effects of kinetin on the growth and flowering of of Botany 1, 649-54. intact green plants. American Journal of Botany 50, 330-6. WHITEHEAD, D. C , 1983. The influence of frequent defoliation and of drought on nitrogen and sulphur WOODHAMS, D. H. and KOZLOWSKI, T. T., 1954. Effects in the roots of perennial ryegrass and white clover. of soil moisture stress on carbohydrate development Annals of Botany 52, 931-4. and growth in plants. American Journal of Botany 41, 316-20. WIDDERS, I. and LORENZ, O. A., 1982. Ontogenetic changes in potassium transport in xylem of tomato. WRIGHT, S. A., JORDAN, W. R., MORGAN, P. W. and Physiologia Planlarum 56, 458-64. MILLER, F. R., 1983. Genetic and hormonal control of shoot and root growth of sorghum. Agronomy WIEDENROTH, E. M. and ERDMANN, B., 1985. MorphoJournal 75, 682-6. logical changes in wheat seedlings (Triticum aestivum L.) following root anaerobiosis and partial pruning YEAGER, T. H. and WRIGHT, R. D., 1981. Influence of of the root system. Annals of Botany 56, 307-16. nitrogen and phosphorus on shoot: root ratio of Ilex WILKINSON, S. R. and OHLROGGE, A. J., 1964. Mechacrenata Thunb. 'Helleri'. HortScience 16, 564-5. nism for nitrogen-increased shoot/root ratios. ZHOLKEVICH, V. N. and KORETSKAVA, T. F., 1959. Nature 204, 902-4. Metabolism of pumpkin roots during soil drought. Soviet Plant Physiology 6, 690-700.