Journal of Experimental Botany, Vol. 53, No. 367, pp. 175-181,
February 1, 2002
© 2002 Oxford University Press
Short Papers |
Long-distance signalling from roots to shoots assessed: the flooding story
IACR-Long Ashton Research Station, Department of Agricultural Sciences, University of Bristol, Long Ashton, Bristol BS25 1PL, UK
Received 20 September 2001; Accepted 1 November 2001
Abstract
Several kinds of signal may be generated when roots are exposed to an environmental stress. Some, but not all, are conveyed to shoots in the transpiration stream. Principles are summarized that may help establish experimentally the presence or intensity of root signals transported by transpiration. In many dryland species, flooding of the soil induces developmental responses in the shoot such as epinastic leaf curvature, stomatal closure and slowing of leaf expansion. These reactions compensate for diminished input of resources from the roots. They lend themselves to the study of root-to-shoot signalling by commencing after a time lag of only a few hours, by persisting for several days and by being highly reproducible. Evidence implicating chemical and hydraulic signals in promoting stomatal closure and epinastic curvature in flooded plants is reviewed. Further progress will depend upon examining a wider range of putative signals, accounting for any interactions between them and improving methods for the evaluation of signal durability in transit, and effectiveness at target sites.
Key words: Abscisic acid, anaerobiosis, environmental stress, ethylene, flooding, long-distance signalling, plant hormones, root-to-shoot communication, xylem sap.
Introduction
The co-ordinated behaviour of roots and shoots (and other organs) of growing plants has intrigued plant biologists for a long time. Stephen Hales’ experiments in the early 18th century (Hales, 1961
) demonstrated that roots support the shoot system with water and other chemicals extracted from the soil. Proposals for more subtle interactions between roots and shoots followed from the idea of du Monceau that movement of sap controlled plant growth (du Monceau, 1758), from Sach's theory of ‘organ forming substances’, and from the development of the hormone concept by animal physiologists in the early 20th century (reviewed in Pincus and Thimann, 1948). Audus has summarized how the idea of the auxin hormone was developed to help explain co-ordinated growth patterns (Audus, 1959). This and similar accounts establish the historical and conceptual underpinning of the study of cell-to-cell and organ-to-organ communication. However, most of these accounts overlook that ethylene, not auxin, was the first chemically and physiologically characterized plant hormone (Crocker et al., 1935). This is important in the context of the present review since ethylene production, entrapment and action are intimately associated with several flooding and submergence responses (Jackson, 1990).
In the late 1930s, FW Went proposed that shoot growth and leaf longevity are dependent upon a hormonal influence from roots that was not auxin and was neither a mineral nutrient nor sugar (Went, 1943). This ‘caulocaline’ hypothesis has since been abandoned in name only and the idea that roots influence shoot growth through chemical signalling remains an active research topic. Much recent work has examined the impact of perturbations to the roots on shoot behaviour (Jackson, 1993). Such treatments are thought to generate signals from the roots that are sensed by target cells of the shoot. The experimental outcome indicates how stressed roots regulate shoot processes such as growth and senescence, and influence shoot water relationships. The outcome may also allow inferences about how unstressed roots regulate shoots. This article re-iterates a simple framework for envisaging the kinds of signals that stressed roots may provide. It also comments on what may or may not be taken as reliable evidence for the existence of signals transported in the transpiration stream, and assesses the contribution such approaches have made to understanding shoot responses to flooding of the soil. Flooding deprives roots of oxygen. It is of major importance in agriculture and strongly affects species-distribution in all but the driest regions.
Different types of root signal
There are at least four kinds of signal by which stressed roots influence shoots (Jackson, 1993). Root stress may increase the output from roots and into the shoot base of some existing signal or generate an entirely new one (positive message). Stressed roots might also reduce the output of an existing signal (negative message). A third, less obvious signal may be formed when stress at the roots reduces their demand for hormones or other compounds originating in the shoot, leading to accumulation at source (accumulation message). A fourth and seldom-considered signal has been termed a ‘debit message’. This could occur where root stress attracts signalling molecules away from the shoot. A rare example is when root infection by parasitic Striga hermonthica raises root demand for assimilates. In reality, two or more types of signalling will coexist in a stressed plant and may interact. Some potentially effective signalling molecules lie outside the five classic hormones (abscisic acid, auxin, cytokinins, ethylene, and gibberellins) and can extend to inorganics such as hydrogen ions, nitrate or calcium, and also to mainstream metabolites such as ethanol (Fulton and Erickson, 1964). They can also include water and solutes originating from outside the root. Quantitative confirmation that putative signals have their suspected effect on shoot behaviour is problematic. Some rules of evidence have been proposed (Jackson, 1993). Convincing tests take care to suppress the signal in some way (e.g. using shoots grafted on to roots of a hormone-deficient mutant; Jackson, 1991) or to reproduce the signal with due attention to duplicating the intensity, location and duration seen in the stressed plant. The concept of the ‘root-sourced’ signal should not be over-interpreted. Obviously, all hydrocarbons have their origin in the shoot and there is also much cycling of solutes between roots and shoots.
Comments on what constitutes a signal carried by the transpiration stream
A problem that continues to beset the study of chemical signalling via the transpiration stream is the widespread use of solute concentration in xylem sap rather than solute flux to assess whether or not there exists a putative positive or negative message generated by stressed roots. This predilection for concentration data can be traced back to FW Went's demonstration that auxin activity was concentration-dependent (Audus, 1959). This viewpoint is perfectly valid when considering events at or near to the site of action (e.g. a guard cell) just as it is in considering deficiency and sufficiency in leaves with respect to inorganic nutrients. However, mineral nutritionists recognize that the flux of nutrients from roots relative to size (and growth rate) of recipient above-ground organs, is a major determinant of mineral concentration at sites of action above-ground and that this is not a simple function of xylem sap concentration alone (Siebrecht and Tischner, 2001). However, this viewpoint is less common amongst those working with hormones. This creates a problem because concentration of substances dissolved in xylem sap can be changed in ways that are not the outcome of greater or smaller output from the roots. One way this can happen is by dilution when changes to the rate of transpiration alters concentration even though solute output from the roots remains much as before. Most stresses affect transpiration rate markedly. Thus, detecting a loss in concentration in the xylem sap of a stressed plant may be wrongly interpreted as a negative message when, in reality, it amounts to little more than extra dilution resulting from an increase in transpiration. Similarly, and more commonly, an increase in concentration may be interpreted wrongly as a positive message when all that may have happened is that slower transpiration gave less dilution of a largely unchanging solute output by the roots. Many stresses, including flooding, slow transpiration by promoting stomatal closure. Clearly, any resulting decrease in solute dilution would create a false positive if the signal were assessed solely on the basis of a rise in concentration. It follows that a transpiration-borne root signal can be demonstrated convincingly only if there is a change in the flux of the solute out of the root and in to the shoot. In whole plant studies, the term ‘delivery rate’ is more appropriate than flux since the exact dimensions needed for a true flux expression are not usually available. Delivery rate is readily calculated by multiplying the rate of transpiration by the concentration in that flow. A change in concentration in the transpiration stream can indicate a genuine signal, but only if the extent of change exceeds that of any alteration in transpiration rate or in stomatal conductance. It is important to note that not all solutes dilute in exactly the same way when transpiration rates rise or fall (Schurr and Schulze, 1995).
Once a signal has been shown to emerge from the root system, a question remains concerning its fate en route for target tissue in the shoot. Signal intensity can be modified as sap flows between the roots and target organ in the shoot. In Ricinus communis, the delivery rate of ABA out of drying roots in the transpiration stream was halved by the time it reached a young leaf some distance away (Jokhan et al., 1999). Similarly, delivery of osmolality and calcium was found to be halved in transit between basal and apical leaves of flooded tomato plants (Tiekstra et al., 2000). The reverse situation is also known, arising as a consequence of xylem sap being enriched with solutes as it moves in to a leaf. In the case of ABA (Loveys and Robinson, 1987), the effect can be exacerbated by partitioning effects derived from alkalization of xylem sap (Bacon et al., 1998). Thus, if xylem sap samples are taken from stems or leaves high in the canopy (a common practice) their solute content may not closely reflect output from the roots. Obviously, such an analysis may not be a sound guide to what actually emerged from the roots. Ideally, the original root signal should be sought close to the root–shoot junction and its fate thereafter followed to the presumed site of action (e.g. stomatal guard cell). Only there does concentration data take on meaning, as it becomes the physiologically relevant outcome of (a) the initial delivery rate from of the roots and (b) gains or losses during transport in the shoot vasculature and cell walls. Thus, it is entirely possible that changes in the concentration of putative signalling molecules in xylem sap that are measured close to responsive sites in the shoot are not always the outcome of changes in delivery out of the roots.
Methods of sampling the transpiration stream
If a change in delivery rate defines a root signal, the underpinning requirements for its calculation are concentration and flow rate of the xylem sap being analysed. Xylem sap can be obtained in several ways, each with advantages and drawbacks. One approach is to excise a section of shoot and withdraw xylem sap by force, believing the expressed liquid to be genuine transpiration fluid. A second is to decapitate the plant and collect osmotically generated sap as it exudes from the cut stump. The flow rate of this sap is much slower than transpiration and thus solute concentrations will be unnaturally high. But, if in planta dilution is approximately proportional to flow, multiplying the unnaturally high concentration with the abnormally slow flow should give a reasonable estimate of the delivery out of roots in the fast-moving transpiration stream of an intact plant. However, when dilution is considerably less than proportional to change in flow rate (e.g. for ABA in flooded plants; Jackson et al., 1996), the resulting calculation will over-estimate true delivery. In the laboratory, this problem can be overcome by applying sufficient pneumatic pressure to the roots of decapitated plants to induce sap to flow at rates close to those of whole plant transpiration (Else et al., 1994). However, identifying the actual pressure needed to achieve this presents a considerable procedural difficulty, especially when stress changes root hydraulic conductance over time. Tiekstra et al. showed that when leaf water potential (approximating the driving force for xylem sap flow in a transpiring plant) is used as a guide to selecting the correct pressure, the resulting sap flows are much too fast (Tiekstra et al., 2000). An alternative approach is to pressurize roots of whole plants until xylem water potentials are atmospheric (Passioura and Munns, 1984) and then remove a small portion of a leaf, thereby inducing a minor diversion of the transpiration stream out from the cut surface. The technique gives similar estimates of concentration obtained by applying the correct pressure to roots of decapitated plants (Tiekstra et al., 2000), and has the advantage of allowing sap to be sampled at various positions through the canopy. When solute delivery rates are to be compared using subsamples of whole plant transpiration flow (as in the Passioura and Munns approach) it is important to correct for the different leaf areas into which the sap sample would have been drawn by transpiration prior to removing leaf material. In some species, precautions are needed to avoid overestimating deliveries as a result of contamination by wounding at cut surfaces (Else et al., 1994; Jokhan et al., 1999). For some species, an exotic alternative to these highly mechanical methods is to employ insects that feed on xylem sap (Malone et al., 1999).
The flooding story
This account is not comprehensive and concentrates on the regulation of leaf epinastic curvature and stomatal closure in tomato (Lycopersicon esculentum) and Ricinus communis.
Leaf epinasty in tomato
Oxygen shortage for >4–6 h at the roots promotes cell expansion on the adaxial surface of petioles resulting in downward leaf growth known as epinasty. It is thought to offset partially, the potentially dehydrating influence of decreases in hydraulic conductance that take place in flooded roots (Else et al., 1995b). Experiments with split root systems and root excision tests (Jackson and Campbell, 1975a) demonstrated that a positive message from the roots was responsible. This is transmitted in the xylem and stimulates shoot ethylene production (Jackson and Campbell, 1976). Bradford and Yang showed that the signal responsible is 1-aminocyclopropane-1-carboxylic acid (ACC), the immediate precursor of ethylene (Bradford and Yang, 1980). Rigorous mass spectrometric analyses and sampling methods that account for dilution errors confirmed ACC delivery is indeed sufficient to support the extra ethylene formed in leaves of flooded plants. This work also showed that delivery of ACC from roots of well-drained plants is also adequate to sustain their entire shoot ethylene production (Else and Jackson, 1998). The ACC signal exported by oxygen-deficient roots results from a block to ACC oxidase enzyme activity that suppresses the oxidation of ACC to ethylene, and by an up-regulation of one member of the ACC synthase gene family (LE-ACS7) starting within 1 h (Yin Shiu et al., 1998). This ACC may be supplemented by any ACC present in the soil (Else et al., 1995a). On arrival in shoot tissues, abundant oxygen facilitates ACC conversion to ethylene by the enzyme ACC oxidase, which itself increases in total activity in the leaves soon after flooding starts. The root signal initiating this increase in foliar ACC oxidase activity remains unknown. However, it is an important part of the overall regulating system since when flood-induced increases in ACC oxidase activity were suppressed by transforming tomato plants with an antisense construct to an ACC oxidase gene (LE-ACO1) ethylene production and epinastic curvature were much reduced (English et al., 1995). Unpublished results by English et al. indicate that flooding-increased ACC oxidase activity is mediated by LE-ACS1 transcript accumulation in petioles that is enhanced within 6 h. This points to up-regulation of gene expression in the shoot by a root signal (Fig. 1 summarizes this signalling system). Ethylene derived from the ACC signal may be supplemented by ethylene taken-up from the soil (Jackson and Campbell, 1975b) that is presumably of microbial origin.
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Flooding is also known to depress cytokinin and gibberellin activity in xylem sap (Burrows and Carr, 1969
; Reid and Crozier, 1971; Neuman et al., 1990), an effect sufficiently large to overcome dilution errors arising from unnaturally slow flow rates of the sap analysed. These negative messages may enhance the epinasty response since applying exogenous cytokinins and gibberellins can inhibit epinasty. However, the presence of well-aerated roots (putative sources of endogenous gibberellins and cytokinins) positioned between flooded roots and the leaves did not inhibit epinasty and shoot ethylene production (Jackson and Campbell, 1979) implying the absence of negative message involvement. Recent evidence of cross-talk between ABA and ethylene in regulating growth (Sharp et al., 2000) suggests that the large decrease in ABA delivery that takes place soon after roots are flooded (Else et al., 1995a) could sensitize leaves to the action of ethylene. This might enhance epinastic curvature and also unmask ethylene inhibition of leaf expansion. Decreased leaf growth is a particularly strong and prompt response to flooding (Else et al., 1995b) deserving closer study. Increased ethanol delivery in the transpiration stream (Fulton and Erickson, 1964) generated by vigorous alcoholic fermentation by flooded roots is insufficient to influence epinasty (Jackson and Campbell, 1976) and thus unlikely to be involved in its regulation.
Stomatal closure
Stomatal closure can start within 2 h of the start of soil flooding and is more effective than epinasty in offsetting foliar dehydration. ABA is implicated since closure is frequently accompanied by increased concentrations of foliar ABA (Jackson and Hall, 1987) and because ABA-deficient mutants of pea (Pisum sativum) have impaired stomatal responses to flooding (Jackson and Hall, 1987; Jackson, 1991). However, any extra ABA involved does not have roots as its source since ABA delivery in xylem sap is strongly decreased by flooding (Else et al., 1994). There is circumstantial evidence that some ABA builds up in leaves as an accumulation message (Jackson and Hall, 1987), but the effect is probably too slow and short-lived to make a major contribution (Else et al., 1996). Subtle recompartmentalization of ABA based on upward pH shifts in xylem sap such as those of droughted plants (Bacon et al., 1998) is a possible effector of stomatal closure even though the pH of sap issuing from roots was reported to be little changed after 24 h flooding (Else et al., 1995a). More detailed studies show increases of at least 0.5 pH units in the first few hours of flooding and at the time stomata begin to close (MA Else, personal communication). If these protons originate in the roots, they would constitute a positive message. Preliminary indications of increases in other unidentified substances in sap that close stomata (Else et al., 1996) have not been substantiated in subsequent work (AE Tiekstra, unpublished data).
An additional possibility is that loss of root hydraulic conductance brought about by oxygen deficiency induces ABA production in leaves by the dehydration mechanism operating in plants subjected to soil drying (Qin and Zeevaart, 1999). This would amount to a negative hydraulic message. Evidence of this has been found in R. communis where pneumatic pressure applied to flooded roots to negate the negative hydraulic message delayed stomatal closure (Else et al., 2001). However, in flooded tomato plants, root pressure does not prevent closure (Else et al., 1995b) indicating that some non-hydraulic signal (increased pH?) initiates stomatal closure in this species.
Conclusions and issues for the future
The fast effects on shoots that flooding of the soil brings about make this stress especially suitable for studies of root–shoot signalling. Research with flooded plants provided some of the earliest direct evidence of chemical-based signalling in xylem sap (e.g. ethanol, cytokinins, and gibberellins) and of signals originating from outside the root system (e.g. soil ethylene). It also pioneered the use of divided root systems to explore signalling systems (Jackson, 1956), and provided the first chemically identified example of a positive chemical message from stressed roots invoking developmental change in shoots (ACC). Issues for the future include redressing the present imbalance in hormone coverage by using mass spectrometric methods to quantify changes in delivery of auxins, gibberellins and cytokinins in the transpiration stream. In addition, methods are required that can duplicate delivery rates of these and other putative signals for use in experiments designed to test their efficacy. The durability of signals as they move up the shoot is also worthy of further attention, as is the effect of night-time on signal transmission. Soil stresses such as flooding affect root size, as do mutations such as that causing ABA-deficiency in the notablis tomato (Sharp et al., 2000). Thus, in comparative studies using such plants, estimations of signal strength (delivery rate) in the transpiration stream would benefit from refining to account for the different sizes of the root system generating the signal (Jokhan et al., 1996). Possible interactions between various root signals in regulating epinasty, stomatal closure and leaf expansion require urgent attention. They could be addressed by the judicious use of mutants, particularly in tomato, where ABA-deficient mutants and transgenic lines are available, as are ABA overproducers (Thompson et al., 2000), ethylene-insensitive mutants such as Never ripe (Ciard and Klee, 2001) and ethylene under-producers such as LE-ACO1 antisense plants. It is likely that double or triple mutant analysis and well-thought-out reciprocal grafting experiments that add or delete hormone production or action in the root or shoot will help greatly in the study of ABA/ethylene interactions. Mutational analysis may also extend to studies of how shoots may influence the formation of root signals. Recent studies of shoot branching in mutant families of pea (Beveridge, 2000) point the way here. This approach may, for example, help investigate the involvement of auxin as an accumulation message in flooded plants in such processes as epinasty (Phillips, 1964) and adventitious root formation (Visser et al., 1996) where auxin and ethylene interactions have been implicated.
Acknowledgments
I thank Dr MA Else for helpful comments on a draft of this paper.
Notes
1 Fax: +44 (0)1275 394282. E-mail: mike.jackson{at}bbsrc.ac.uk 
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M. C.H. Cox, F. F. Millenaar, Y. E.M. d. J. van Berkel, A. J.M. Peeters, and L. A.C.J. Voesenek Plant Movement. Submergence-Induced Petiole Elongation in Rumex palustris Depends on Hyponastic Growth Plant Physiology, May 1, 2003; 132(1): 282 - 291. [Abstract] [Full Text] [PDF]
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