Journal of Experimental Botany, Vol. 51, No. 350, pp. 1617-1626,
September 2000
© 2000 Oxford University Press
Regulation of leaf and fruit growth in plants growing in drying soil: exploitation of the plants' chemical signalling system and hydraulic architecture to increase the efficiency of water use in agriculture
1 Biological Sciences Department, Institute of Environmental and Natural Sciences, Lancaster University, Bailrigg, Lancaster LA1 4YQ, UK
2 Departmento de Bioloxia Vexetal e Ciencia do Solo, Facultade de Ciencias de Vigo, Universidade de Vigo, Vigo, Spain
Received 31 May 2000; Accepted 9 June 2000
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Abstract |
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 Top Abstract IntroductionWhat are the long-distance...The exploitation of the...Tomato crop production under...Shoot-to-fruit signallingConclusions and future...References |
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In this paper the nature of root-to-shoot signals in plants growing in drying soil is considered in the context of their commercial exploitation in tomato (Lycopersicon esculentum L.) and other crops. Recent findings are presented on the effects of partial root drying (PRD) in the production of a glasshouse tomato crop. These findings show how an understanding of both root-to-shoot signalling mechanisms and fruit hydraulic architecture may explain observed increases in fruit quality, the differential effects of PRD on vegetative and reproductive production and the incidence of blossom end rot. Evidence is provided to support the hypothesis that the success of PRD may lie, at least in part, in the relative chemical and hydraulic isolation of the tomato fruit.
Key words: Root-to-shoot signalling, partial root drying, root hydraulic architecture, tomato, growth regulation, water use efficiency.
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Introduction |
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TopAbstractIntroductionWhat are the long-distance...The exploitation of the...Tomato crop production under...Shoot-to-fruit signallingConclusions and future...References |
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There is now considerable evidence in the literature that shoot growth and plant gas exchange can be limited as a result of both chemical and hydraulic signalling of the effects of soil drying (Davies et al., 1994
). There is little debate over the suggestion that a restriction of water supply from the soil can result in shoot water deficit and that this response will limit shoot growth and functioning (Kramer, 1983). Nevertheless, shoot water deficits do not always result from soil drying and indeed in some circumstances, drought-induced stomatal closure can result in an increase in shoot water potential relative to that of a well-watered plant (Jones et al., 1983). Under these circumstances it is necessary to ask what is limiting the reopening of stomata (and the growth of the shoots)? Some ingenious experimental manipulations have allowed several groups to conclude that chemical signalling between roots and shoots can limit shoot growth and functioning under particular conditions. In some experiments, pneumatic pressure is applied to the roots of plants in drying soil such that the shoot water relations are sustained at values that are comparable to those of well-watered plants. Despite this, stomata can remain partly closed (Gollan et al., 1986) and shoot growth can still be restricted (Passioura, 1988). Gowing et al. have used plants with split roots to demonstrate the effects of root-sourced signals (Gowing et al., 1990). A portion of the root system in contact with dry soil can result in a limitation of leaf growth while removal of this root from the plant is followed rapidly by a recovery of the shoot growth rate to that exhibited by the well-watered plants. The conclusion from this experiment was that roots in contact with drying soil can be the source of inhibitors of shoot growth and functioning and removal of these roots from the plant removes the source of the inhibitor allowing recovery of shoot performance.
Although some studies suggest that hydraulic signalling can dominate in some plants in particular situations (Saliendra et al., 1995) it would be surprising if the control systems for growth and functioning under stress did not have some flexibility to cope with stresses of different kinds. There are many stimuli that will promote stomatal closure, some of which may operate through common signal transduction systems (Webb and Hetherington, 1997). Other transduction systems that are present may be redundant under certain circumstances. It is known, for example, that many genes are responsive to both ABA and to osmotic stress, but will show a complete response to only one of these stresses occurring in isolation. In other circumstances, osmotic stress can apparently enhance the effects of ABA on gene expression (or vice versa) and it is clear that stomatal response to ABA can also be enhanced if the leaf tissue is experiencing a water deficit (Tardieu and Davies, 1992). Some results (Gollan et al., 1986) with the root pressure vessel are consistent with this observation in that quite high doses of ABA are relatively ineffective when the water status is maintained at an artificially high value.
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What are the long-distance chemical signals and how do they arise? |
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TopAbstractIntroductionWhat are the long-distance...The exploitation of the...Tomato crop production under...Shoot-to-fruit signallingConclusions and future...References |
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Over the last ten years or so there has been much controversy over the adequacy or otherwise of different chemical signals as an explanation for changes in shoot functioning in response to soil drying (Munns and King, 1988
; Munns and Sharp, 1993; Munns and Cramer, 1996). There is general agreement that these signals move from roots to shoots in the transpiration stream and that at least for plants in drying soil, they may provide shoots with a measure of the access that roots have to soil water (Tardieu et al., 1992). Shoot growth and functioning may then be modified as a function of the intensity of this signal. The chemical signal may be synthesized in the roots (a hormone?) and it seems likely that synthesis will be affected by the water status of the root, but there is no direct evidence of this. Signals may also be chemicals that are taken up from the soil and attention has been given to inorganic ions (Gollan et al., 1992) and to hormones (Hartung et al., 1998). Recent quantification of apoplastic bypasses in roots of some species suggest that interspecific differences in the relative importance of soil-sourced chemical signals in the root-to-shoot signalling process should be expected (Freundl et al., 1998).
Jeschke and colleagues have worked hard to quantify the extent of recirculation of particular chemical species in the plant (Jeschke et al., 1992) and it is clear from experimental work and from modelling that root dehydration can have a significant effect on the amount of ABA arriving in the root in the phloem that is subsequently recirculated to the shoot via the xylem. It has been shown that ABA which leaves chloroplasts in the leaf can be recirculated through the root before it reaches sites of action on the guard cells (Slovik et al., 1995). From all of the above it should be clear that a chemical message arriving in the xylem can be recirculated, a novel root or a soil-sourced message, but is likely to be a combination of all three influences. Jackson has also emphasized the importance of negative messages that may accumulate in leaves as a result of a restriction in export to roots (Jackson, 1993).
There has been much discussion over how to quantify a chemical signal in the xylem. Schurr has discussed the difficulties of sampling xylem sap and estimating concentrations of solutes that might occur in the sap before the xylem was damaged (Schurr, 1997). It is clear that transpiration flux may have a significant effect on solute concentration in the sap and the shortcomings of sampling sap bleeding from cut plant stumps should be obvious. Most commonly, the pressure chamber is used to sample sap from excised leaves and there are several reasons why even this technique may provide an erroneous estimate of solute delivery to the shoot (Else et al., 1995). Jackson and colleagues have argued persuasively that delivery rates of chemical species must be assessed (rather than simple estimates of concentration) if unequivocal statements about root-to-shoot signalling via these species are to be made (Jackson, 1993). They have suggested ways that this variable may be quantified, but this is not an easy thing to do for a plant in the field. The existence of apoplastic bypasses (see above) means that the extent of dilution of the solute by increasing transpiration flux is not always predictable.
There is strong evidence from a number of different studies that ABA plays an important role in the regulation of stomatal behaviour in droughted plants (Mansfield et al., 1990). This hormone may also have a role in the root-to-shoot signalling process (Zhang and Davies, 1990a, b) but there has been controversy over whether there is always enough ABA in the xylem stream to explain the stomatal responses that are generated by soil drying. This is a difficult question to answer, but recent experiments where xylem pH is manipulated (see below) and experiments with transgenics and mutants (Hussain et al., 1999; Mullholland et al., 1999) seem to support the case for a central role for ABA in the regulation of gas exchange of at least some plants. ABA may move through the plant in a complexed form and assessment of concentrations of the free hormone in the xylem may therefore underestimate the role that this chemical species may play in signalling to guard cells (Hartung et al., 1998; Netting, 2000).
In some writing it is assumed that a common regulator may be involved in the modulation of both leaf growth and stomatal behaviour of droughted plants. There is no obvious reason why this should be the case and given the very different nature of the control required for these two systems, there is no a priori reason why it should be expected that a single regulator will do the job. There are studies where mild soil drying reduces shoot growth and not stomatal opening (Saab eand Sharp, 1989) and vice versa. There are many reports in the literature which suggest that ABA can act as a shoot growth inhibitor and some which suggest that this hormone will act in the root-to-shoot signalling system to regulate leaf growth. This hypothesis is supported by recent work by Bacon et al. who show that concentrations of ABA comparable to those in well-watered plants will restrict leaf growth (Bacon et al., 1998). This evidence is provided in an experiment where xylem sap pH is manipulated against a background of a low (well-watered) concentration of ABA in the xylem stream. Alkaline pHs limit leaf growth under these conditions. When ABA concentrations are further reduced by the use of a barley mutant (AZ 34) the pH effect on leaf growth disappears. From what is known about the effect of pH upon the distribution of ABA in the different compartments of the leaf (Hartung et al., 1998), these results suggest that very low concentrations of ABA in the apoplast can limit leaf growth and that leaves will grow faster if ABA is removed to the symplast. Whilst providing some insight into the mechanisms by which growth is regulated in plants under stress, these results may only be relevant to situations where the degree of soil drying is very limited (Davies and Gowing, 1999). Very mild stresses can have dramatic effects on plant growth and functioning (Henson et al., 1998) and can also affect plant community structure and productivity. Because of the dramatic effects of a simple compartmental redistribution of ABA (no novel synthesis of hormone is required), it seems possible to argue that ABA has important involvement in the mediation of plant responses to such subtle changes in soil conditions. Nevertheless, many plants experience stress that is much more severe and here, the balance of several hormones may be affected and very high concentrations of hormones can accumulate in certain compartments. One of these is ethylene (Wright, 1977). This hormone will greatly restrict leaf growth and may also promote the development of short fat roots. Recent work suggests that one role of ABA accumulation under conditions where ethylene may potentially accumulate to high concentrations is to offset the effects of this hormone on growth and development (Sharp et al., 2000). Under these conditions, ABA may actually promote leaf growth rate, relative to the rate shown by plants where ABA accumulation is prevented (Hussain et al., 1999; Mullholland et al., 1999). The mechanism by which ABA actually promotes leaf growth remains unidentified.
To unpick these potentially complicated interactions, a very precise definition of the stress that is affecting plants is needed. In addition, the new genetic tools that are increasingly available will allow an increased insight into hormone effects against a background of water and chemical relations that can be carefully controlled. New genetic tools are also needed to help determine whether other hormones such as auxin, cytokinin and gibberellin are involved in the long-distance signalling process. It seems almost certain that they are, but these cases have been difficult to make for hormone responses that are more subtle than the stress-induced accumulation of ABA and ethylene and the stomatal response to a potent hormone like ABA.
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The exploitation of the plants stress signalling system to increase the efficiency of water use in agriculture |
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TopAbstractIntroductionWhat are the long-distance...The exploitation of the...Tomato crop production under...Shoot-to-fruit signallingConclusions and future...References |
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Loveys first suggested that it may be possible to exploit the Gowing split root growing system (above), by drying part of a root system of a vegetatively vigorous plant and thereby restrict shoot growth under circumstances where excessive vigour may be a disadvantage (Loveys, 1991
). One such circumstance is the production of a fruit crop on a plant producing more leaves than are required to supply carbohydrate to developing reproductive plant parts. Many grape vines are pruned to reduce excessive vigour and Loveys and colleagues have successfully used partial root drying (PRD) to reduce the need for pruning in this crop (Dry et al., 1996; Stoll et al., 2000). By watering alternately on the two sides of rows of grapevines, partial root drying can be achieved and much water can be saved. Of particular significance in this work is that fruit yield is not reduced by the PRD treatment while the quality of the fruit produced is greatly increased.
It is of interest to determine why PRD reduces leaf growth of grapevines, but has no influence on fruit growth and development. One hypothesis is that root-sourced chemical signals travel to the shoots in the xylem but that delivery to the fruit is limited. It has long been known that in expanding fruit of many plant species a large proportion of water is transported into the fruit via the phloem. For example, Greenspan et al. demonstrated that in grape the majority of water reaches the fruit via the xylem before veraison but that phloem transport predominated after veraison (Greenspan et al., 1994). This tendency is also particularly extreme in tomato and in the later stages of growth of fruit of this crop considerably more than 90% of water may be transported to the fruit by the phloem (Ho et al., 1987).
In the present study the hypothesis that partial root drying may exert a particularly favourable differential effect on fruit and leaf growth when fruits are relatively isolated from the hydraulics of the rest of the plant has been tested. Tomato has been used as a model species. In addition to a simple test of the PRD system, the transport of growth regulators to the leaves and the fruit of this crop and the extent of the hydraulic connection between the tomato fruit and the vegetative part of the plant has also been investigated.
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Tomato crop production under PRD |
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TopAbstractIntroductionWhat are the long-distance...The exploitation of the...Tomato crop production under...Shoot-to-fruit signallingConclusions and future...References |
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Tomato seeds (Lycopersicon esculentum L. cv. Ailsa Craig) were germinated in a commercial compost and established in a glasshouse until the appearance of the fifth leaf. At this point 80 of the plants were transplanted, with the root system of each plant divided equally between two 5.0 l plastic pots containing the same commercial compost. Both pots were watered daily to drip point for 1 week to allow establishment of the root systems in both pots. A PRD system of watering then commenced. Control plant water use was determined using a Theta probe (Delta-T Devices, Cambridge, UK) with the water used being replenished every 24 h. PRD plants received half the amount of water used by plants in the control treatment via only one of the two pots in which the plants were rooted. The roots in the other pot were allowed to reduce the soil water content to c. 30% (v/v) at which point the watering was reversed; with the previously dry pot being watered and the previously watered pot being allowed to dry. One cycle of the PRD regime initially took between 10–14 d. The frequency with which the treatment was alternated increased as the crop developed. A mature fruiting plant with seven set trusses took c. 6 d to reduce the soil water content of the drying pot to 30% (v/v). The amount of water used to irrigate the well-watered plants was increased as water use increased, until a mature fruiting plant with seven set trusses, receive 2.0 l of water every 24 h, equally between both pots. In order to minimize variation due to differences in the glasshouse environment, plants were arranged in four rows with alternately placed control and PRD irrigated plants within each row. A piece of black plastic was inserted between and under the two pots of each plant to prevent water from a watered pot entering the pot containing roots which were drying the soil. All plants were fed with a commercial tomato feed three times per week after the first truss had set. PRD-watered plants received the same amount of feed as controls.
Measurements on young plants with no fruit load
From the onset of the PRD regime, stomatal conductances and chlorophyll fluorescence were determined every 3 d in the youngest fully expanded leaf of the same 15 plants in each treatment, together with a measurement of plant height (Table 1). A weekly assessment of the number of flowers per truss and trusses per plant was also made. Twenty-two days after the onset of the PRD regime, the leaf area of 7 plants per treatment was determined together with the dry weight of the roots, stems and leaves Table 1). At the same time, the first two side-shoots were removed from all plants and their dry weight determined (Table 1).
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After only 22 d of growth under a PRD watering regime, several significant effects were detected (Table 1
). The water use efficiency (WUE) expressed on a dry weight basis increased by 48% in plants grown under PRD conditions. This increase would appear to have been due the significant restriction in stomatal conductance, as whole plant biomass production actually decreased (c. 16%) during this period. The degree to which PRD caused a reduction in biomass accumulation differed when the individual parts of the plant were examined (7–40%, Table 1), with the most marked reduction occurring in the side shoots (40%).
Analysis of yield and fruit quality
When individual tomatoes reached a predetermined level of ripeness they were removed from the plant, weighed, sized, and visually assessed for damage, uniformity of ripeness and presence of blossom end rot (Table 2). Three weeks after the beginning of fruit harvest, 32 fruit from each treatment were selected over a period of 1 week and used to determine fruit dry weight, total soluble solid (TSS) content and juice pH (Table 2).
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Although PRD caused a significant reduction in vegetative biomass accumulation, this effect was not as marked in the fruit. On a dry weight basis, the mean yield of plants grown under control or PRD conditions did not differ significantly. In some way the carbohydrate supply to the fruit was maintained, either directly by some active mechanism or indirectly via a relative increase in the sink strength of the fruit. An increase in relative strength is likely when the dramatic reduction in side-shoot vigour is considered (Table 1
). Developing side shoots are the major competing sink alongside the developing fruit. The authors therefore speculate, as have others (Dry et al., 1996), that the reduction in the strength of this non-harvestable sink results in a relative increase in the sink strength of the fruit, such that carbohydrate previously partitioned towards the side shoots is redirected towards the fruit. The maintenance of fruit biomass accumulation and significant restriction in transpiration caused by PRD resulted in a 93% increase in the WUE by which fruit biomass was produced during this period.
Although biomass accumulation (DW yield per plant) was sustained in PRD plants compared to controls, it was accompanied by a significant reduction in the size and fresh weight of the fruit. The maintenance of biomass accumulation into relatively smaller fruit however, is reflected in the 21% increase in total soluble solid (TSS) concentration, represented in terms of Brix values, determined via reflectrometry (Table 2). Using measured volume/mass relationships (not shown) it would appear that this decrease in fruit size and maintenance in biomass accumulation can explain only 16% of this increase in TSS. The PRD regime was responsible for a c. 6% increase in TSS content of fruit, independent of the effect on fruit size. This fact, coupled with the maintenance in relative water content, may suggest why a commercial taste test panel (Campdon & Chorleywood Food Association, UK) expressed a marginal preference for PRD-grown tomatoes. Eleven out of 24 assessors correctly identified a difference between control and PRD-grown fruit, with additional descriptors such as ‘sweeter’, ‘riper taste’, ‘more tangy’, and ‘less bitter’ when comparing the flavour of PRD-grown fruit to that of the controls.
The supply of water via half of the root system would appear to maintain an adequate supply of water to the fruit as has been shown elsewhere (Gowing et al., 1990). Our understanding of the signalling mechanisms discussed earlier leads to the suggestion that growth-retarding, root-borne signals emanating from those roots in contact with the drying soil may be responsible for the observed reduction in vegetative vigour and fruit size. Comparing the reductions in size between the vegetative and reproductive parts of plants grown under PRD (Tables 1, 2) it is apparent, however, that the relative effect of any such growth-retarding signals is markedly reduced in the fruit. The ability of such root-borne signals to restrict growth in the fruit to such an extent as seen in the rest of the plant will depend on a number of factors, one of which will be their capacity to penetrate to a site of action in the fruit. It is clearly relevant therefore that the well-developed tomato fruit receives a largely phloem-derived water supply. Xylem-borne signals may reach the fruit early in development but may not be able to penetrate so readily later on, potentially explaining the reduced effect on fruit size and yield, relative to the vegetative parts of the plant. Developmental changes in the hydraulic and consequent chemical connection between the shoot and fruit are poorly understood. Recently, however, the hydraulic architecture at this site has begun to be elucidated and the ideas of root-to-shoot signalling are being extended to a consideration of ‘shoot-to-fruit’ signalling mechanisms.
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Shoot-to-fruit signalling |
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TopAbstractIntroductionWhat are the long-distance...The exploitation of the...Tomato crop production under...Shoot-to-fruit signallingConclusions and future...References |
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Hydraulic signals
It has been argued above that PRD may be particularly successful with grape and tomato because the fruits of these plants can be particularly isolated from the xylem network of the rest of the plant. One manifestation of this may be only restricted shrinking and swelling of fruit when soil or atmosphere water status is manipulated. Greenspan et al. observed that before veraison, grape fruit exhibited pronounced diurnal changes in fruit size, but that this ceased after veraison as phloem transport became more important (Greenspan et al., 1994
). The extent to which tomato fruit are isolated from the xylem stream is the reason for their susceptibility to blossom end rot (BER) and other disorders caused by calcium deficiency (Ehret and Ho, 1986). Calcium is primarily transported into the fruit by the xylem and so almost all tissue calcium enters the fruit very early in development. If this early deposition is insufficient, calcium deficiency arises in later development.
The degree of hydraulic isolation of tomato fruit was tested by applying pressure to the roots of tomato plants (Lycopericon esculentum L. cv. Counter) grown in enclosed ‘sleeves’ which could be inserted into a root pressure vessel (Munns and Passioura, 1985). Plants in open pots were grown from rooted side shoots (Thompson et al., 1998). Plants in enclosed sleeves for use in the root pressure vessel were grown from seed in trays and threaded through the top of the sleeve approximately 21 d after sowing. The fruit used in these experiments were 21–30 d post-anthesis. Additional pressure was applied as an over-pressure of nitrogen. Plant were placed in a purpose-built controlled environment (Thompson et al., 1999) at least 24 h before the first readings. Leaf and fruit turgor pressure, osmotic pressure and water potential were determined using a single cell pressure probe and nanolitre osmometer (Thompson et al., 1998) and fruit growth using position transducers before and after application of pressure to the roots.
When a pressure of approximately 0.092 MPa was applied to the roots of the plant, although leaf turgor pressure increased by 0.092 MPa, the fruit turgor pressure increased by only 0.006 MPa (Fig. 1). Fruit growth was also unaffected by application of pressure to the roots of the plant. As elastic expansion of plant tissues is a highly sensitive method for qualitative detection of changes in turgor pressure this represents powerful confirmation of the pressure probe data. In the experiment shown in Fig. 2, the applied pressure was increased to 0.30 MPa in a series of steps, again with no effect upon fruit growth or fruit turgor pressure.
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)) during application of pressure to the plant's roots. The solid line represents cumulative fruit size and the dotted line the pressure applied to the roots.
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The extremely limited xylem connection suggested by the results in Figs 1
and 2 is not consistent with all observations reported in the literature. For example, Johnson et al. found considerable diurnal variation in tomato fruit growth rate at low light intensities and diurnal fruit contraction at high light intensities (Johnson et al., 1992). The age of their experimental material was not stated but fruit size suggests that the experiments were late in development. It seems extremely unlikely that these diurnal alterations in fruit growth rate can be explained by changes in phloem translocation, and reversed phloem flow leading to fruit contraction is highly implausible. It therefore seems likely that the hydraulic conductivity of the xylem connection to the fruit is variable. Indeed Ho et al. found that increasing the salinity of nutrient solutions in which tomato plants were grown reduced the quantity and proportion of water entering the fruit via the xylem (Ho et al., 1987).
The effect of soil drying upon fruit growth and water relations of tomato plants grown in ordinary open pots has also been examined. In the experiment illustrated in Fig. 3, water was witheld from a plant for a number of days and changes in leaf and fruit water potential measured daily with the micropressure probe. Fruit growth, turgor pressure and water potential were maintained until shortly before the point at which leaf water potential fell below that of the fruit. At this point fruit growth ceased and reversed within an extremely short period of time (less than 3 h). Little or no early inhibition of fruit growth which could be attributed to chemical signals was observed, even though the leaf water potential had fallen to a considerable degree. Fruit transpiration is negligible and shrinkage is therefore probably caused by xylem ‘back flow’. This behaviour indicates that in these plants there was a limited, but effective, xylem connection to the fruit. There was a clear difference between fruit and leaf water potential, irrespective of the direction of the water potential gradient and so xylem conductivity was clearly insufficient to maintain hydraulic equilibrium between the fruit and the remainder of the plant. The rate at which water left the fruit was greater than the initial rate of growth because of the elasticity of the tissue (as elastic contraction would force water out of the fruit as fruit turgor pressure began to fall), but xylem back flow is likely to be greater than it appears because water may continue to enter the fruit via the phloem even during fruit shrinkage.
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); ±s.e.), and leaf mid-rib turgor pressure and water potential (turgor pressure (•), water potential (
); ±s.e.) during a soil drying episode. The line represents cumulative fruit size. The line becomes thin when water was witheld and becomes thick again when the plant was rewatered.The difference between this behaviour and that shown in Fig. 1
appears to result from the root environment (in that growing conditions were otherwise identical). It is worth noting that the plants grown in pressure pot sleeves were highly susceptible to BER (suggesting extremely limited calcium transport) and never exhibited fruit contraction, even after water had been withheld until severe leaf wilting had occurred (Fig. 4) followed by drought-induced abscission. A short episode of soil drying during flower development and very early fruit growth was, however, found to establish some xylem connection to the fruit. Figure 5 shows the effect of application of 0.094 MPa to the roots of a plant which had experienced such a period of soil drying. There was a slight increase in fruit growth rate, and fruit turgor pressure rose by 0.012 MPa. The fruit of these plants also exhibited fruit contraction after water had been witheld for several days. Figure 5 shows the relationship between fruit turgor pressure and pressure applied to the roots in a well-watered plant and a plant which had experienced a period of soil drying during flower development and early fruit growth. Again here, the mild soil drying treatment apparently enhances the hydraulic connection between the fruit and the rest of the plant.
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Blossom end rot (BER) is a good indicator of limitations in calcium transport and therefore provides an indirect method for assessment of the xylem connection to the fruit. Figure 6
shows the proportion of fruit displaying BER throughout fruit development. The plants which had experienced an episode of soil drying exhibited some protection against BER, consistent with the effects of applied pressure upon fruit water relations. This figure also shows that a split root treatment apparently enhanced the extent of hydraulic isolation of the fruit. If a positive root message such as ABA were promoting xylem connection as a result of soil drying, we might expect to see this result in response to drying only part of the root system. The fact that this was not the case raises the possibility that some signal from the wet soil in the RPV limits xylem development. If the root environment were slightly anoxic then this could be an ACC/ethylene message (Else et al., 1995). High concentrations of ethylene are known to inhibit xylem development (Zobel and Roberts, 1978), but auxin is crucial for early xylem differentiation (Sugiyama and Komamine, 1990) and it is perhaps more likely that this effect was due to ethylene inhibition of polar auxin transport (Beyer and Morgan, 1971). Preliminary experiments suggest that fruit contraction during soil drying is reduced by application of ACC to the pedicel and in plants which experienced root waterlogging during flower development and early fruit growth. Water stress can also lead to reduced xylem hydraulic conductivity, apparently as a defence against cavitation (Lovisolo and Schubert, 1998) and it is possible that the catastrophic levels of BER in fruit on the split root plants resulted from the combination of this effect with that of anoxia in early development.
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) are shown.These experiments confirm that tomato fruit are hydraulically isolated from the xylem stream to a considerable degree and may therefore be less likely than vegetative tissues to be affected by root-to-shoot signals. However, it appears events that take place very early in the initiation, growth and development of the fruit can affect the degree of hydraulic isolation of the fruit. This may have many consequences that will be seen throughout fruit development, including effects on fruit calcium concentration, susceptibility of the fruit to splitting during water potential increases and effects of water availability upon soluble solid concentrations. It therefore appears that although reproductive tissues in tomato and some other plants can be isolated from root signals in later development, signals during early development and differentiation can affect tissue physiology so that interactions between fruit and the remainder of the plant are affected in later development.
Chemical signalling
Measurement of accumulated ABA in response to a short period of soil drying (5 d) in expanding and mature leaves and well-developed fruit suggests that at this stage of fruit development, such a signal cannot pass to the fruit. This is supported by an experiment in which mature tomato plants (Lycopersicon esculentum L. cv. Counter) with 10 set trusses were allowed to dry the soil to c. 30% (v/v) water content. Samples of expanding and mature leaf tissue were removed from the plant, frozen in liquid nitrogen and freeze-dried for subsequent analysis of bulk ABA concentration using radioimmunoassay (Quarrie et al., 1988). Breaker fruit from truss number 6 were removed and their epidermis separated away from the fruit with a razor blade, frozen in liquid nitrogen and prepared for determination of bulk ABA concentration in the same way as for leaf material. While a marked accumulation of ABA occurred in expanding and mature leaves after only a short period of soil drying, no ABA accumulation was evident in the fruit epidermis (Fig. 7). This preliminary observation would certainly suggest some degree of chemical isolation of the fruit from the plant, to the point that no xylem-borne, root-souced signals may influence fruit development at this stage. A better understanding of the development of hydraulic isolation and consequent isolation from root-borne signals may explain the observed reduction in fruit size seen in the PRD experiment and provide a basis on which to form recommendations for the commercial implementation of PRD.
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Conclusions and future directions |
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TopAbstractIntroductionWhat are the long-distance...The exploitation of the...Tomato crop production under...Shoot-to-fruit signallingConclusions and future...References |
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While there is now a good understanding of how both chemical and hydraulic signalling of the effects of soil drying may work in specific situations, there is still much work to do. It appears that while the modified delivery of ABA may act as a ‘measure’ of soil drying that can be interpreted by the shoot, this may not always occur because the synthesis and long-distance transport of the hormone is perturbed. It is now clear that the modifications in the partitioning of even the ‘well-watered’ flux of ABA can affect delivery to a site of action in the shoot and thus constitute a signal. It has been shown how this can come about as a result of a change in the pH of the xylem sap that may originate in the roots but it is worthy of note that many climatic factors can influence the pH of different compartments within the leaf and may therefore be expected to change the potency of a root signal. Although poorly understood, it is likely that the effects of climatic and edaphic factors on the growth and functioning of the shoot may be integrated through an influence on the pH relations and provide a high degree of regulatory response to the changing environment.
In this paper, we have also emphasized the importance of the structure of the transport pathways through the plant and the influence that these may have on the nature and the potency of root signals arriving in different parts of the shoot. Restricted xylem connections may limit the flux of different chemical signals to particular organs and thus influence the sensitivity of these organs to root signals. If the plant's own chemical signalling system is to be exploited fully for commercial advantage, it will be important to understand more about the signals that are likely to affect growth and functioning of different plant parts, but also to know more about the ways in which these signals move around the plant. This is particularly the case since root signals themselves can be shown to affect the nature of the transport pathway and the fluxes of water and chemical signals to growing and developing organs that are of commercial interest.
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Acknowledgments |
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The European commission for financial support, Ann Keates, Phil Nott and Maureen Harrison, APCCU, Lancaster University.
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Notes |
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3 To whom correspondence should be addressed. E-mail: m.a.bacon{at}lancaster.ac.uk
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References |
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TopAbstractIntroductionWhat are the long-distance...The exploitation of the...Tomato crop production under...Shoot-to-fruit signallingConclusions and future...References |
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