Journal of Experimental Botany, Vol. 52, No. 90001, pp. 479-485,
March 2001
© 2001 Oxford University Press
Cluster roots: model experimental tools for key biological problems
Department of Biological Sciences, University of Dundee, Dundee DD1 4HN, UK
Received 21 August 2000; Accepted 26 September 2000
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Abstract |
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The cluster root is made up of a number of determinate rootlets tightly grouped along the parent root. Each rootlet grows for a limited time, and then the meristem stops dividing and differentiates. Following cessation of growth, an exudative burst occurs, wherein, over 2–3 d, large amounts of organic acids, as well as phosphatases and phenolics, are exuded from the rootlets. There is a concomitant acidification of the rhizosphere. It is suggested that the temporal and spatial predictability of developmental and functional events in these structures makes them valuable as experimental tools with which to investigate key issues in plant developmental biology, physiology, ecophysiology, evolutionary biology, and biotechnology.
Key words: Cluster roots, plant development, proteoid roots, rhizosphere, root biology, root physiology.
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Introduction |
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The cluster root (or proteoid root, a term stemming from their discovery in the Proteaceae (Purnell, 1960
)) is composed of a number of tightly grouped determinate rootlets that undergo initiation, growth and arrest in a synchronized manner. Most researchers use the term cluster root, or proteoid root, to refer to a single cluster of rootlets (Purnell, 1960; Lamont, 1982; Dinkelaker et al., 1995; Marschner, 1995; Skene, 1998), as this represents a developmental and functional unit, in that physiological and developmental events occur synchronously within any given cluster root (Skene, 2000). However, other workers refer to the entire length of parent root, upon which cluster roots form, as a cluster root (Watt and Evans, 1999). In this paper, the former definition will be used.
In cluster rootlets, meristems differentiate following 2–4 d of growth, depending on the plant species involved. Rootlet hairs are produced at the tips of the rootlets upon determination (Skene et al., 1996, 1998a). Following this, the rootlets undergo an exudative burst, wherein large amounts of organic acids, along with phosphatases and phenolics are released from the rootlets over 2 d (Watt and Evans, 1999). The developmental and functional synchrony within the cluster root leads to a concentrated change in soil chemistry around the cluster root, and is thought to induce the mobilization of phosphate, iron and other elements in the rhizosphere (Dinkelaker et al., 1995). Cluster roots absorb Pi at a faster rate than non-cluster roots on an equal weight basis, with lower values of Km than in non-cluster roots (Jeffrey, 1967; Malajczuk and Bowen, 1974; Gullan, 1975; Siddiqi and Carolin, 1976; Green, 1976; Walters and Jooste, 1980; Vorster and Jooste, 1986). Cluster roots are formed in a wide range of plant families, including the Leguminosae, Proteaceae, Casuarinaceae, Myricaceae, Eleagnaceae, and Betulaceae (Skene, 1998). Physiological, developmental, ecological, and evolutionary aspects of these structures have been reviewed elsewhere (Lamont, 1982; Dinkelaker et al., 1995; Skene, 1998; Watt and Evans, 1999; Neumann et al., 2000; Skene 2000). This paper will outline research areas wherein cluster roots may play a valuable role.
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Root developmental biology |
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Cluster roots appear to provide an excellent model system with which to investigate root initiation, meristem maintenance and the control of the cell cycle. This is because these developmental events occur within a spatially and temporally predictable context. Thus, events can be followed from the beginning, normally an extremely elusive option in root research. Depending on the species, between 35 and 1000 rootlets per cluster root emerge, grow and cease growth within the same time frame in a given cluster root. Therefore, there are large amounts of synchronously produced tissue available for experimental purposes.
Root initiation is an important area of research in modern plant biology. Cluster root pattern formation has been reviewed recently (Skene, 2000) and can be seen to consist of three components: the radial, longitudinal and cluster patterns. Within the cluster zone (that is, the part of the parent root where rootlets are produced), rootlets occur opposite every protoxylem pole, yet outwith the cluster zone, rootlets do not occur. Thus, the longitudinal pattern overarches the radial pattern. As reported in their study of lateral root initiation (Beeckman et al., 2000), cells in the pericycle of Arabidopsis, prior to the first lateral emerging, differ regarding their cell division history, depending on the distance from the root tip and the position relative to the vascular tissue. Pericycle cells that give rise to lateral roots (opposite protoxylem poles) are held in G2, whereas pericycle cells opposite protophloem poles, that never give rise to lateral roots, are in G1. Thus it can be seen that the radial pattern can be related to cell cycle stage. Beeckman et al. link the propensity of pericycle cells opposite protoxylem poles to become involved in lateral root initiation (as opposed to those opposite protophloem poles) with the fact that they have completed DNA synthesis and remain at a phase immediately preceding the M phase (Beeckman et al., 2000). They relate this to the ‘primed pericycle model’ of cluster root development (Skene, 2000) (a model proposed to explain cluster rootlet initiation) wherein pericycle cells located opposite protoxylem cells are primed for division (the priming pattern), while only a subset of these cells will be triggered by some longitudinal factor.
If the radial, or priming pattern is recognized as being related to cell cycle state, an inquiry should be made as to why all pericycle cells opposite protoxylem poles are not involved in lateral root initiation. It seems that cluster roots might provide a valuable system with which to identify the triggering factor involved in root initiation. This is because the cluster root is the ultimate example of triggering, wherein all cells opposite protoxylem poles within the cluster root zone become involved in rootlet initiation, whereas none of the cells occupying the same position outwith the cluster produce rootlets (Skene et al., 1998a, b). Furthermore, the system has the advantage that it is possible to predict where the next group of rootlets will be produced before they are initiated (Skene, 2000).
Auxins have been implicated in both lateral root and cluster root initiation (Thimann, 1936; Torrey, 1950; Pecket, 1957; Böttger, 1974; Skene, 1997; Gilbert et al., 1997, 2000; Skene and James, 2000). There is also emerging evidence directly linking auxin with cell cycle processes (Zhang et al., 1996; Tamura et al., 1999; den Boer and Murray, 2000). However, it has been shown that while increasing auxin concentration led to greater numbers of cluster roots, it did not significantly increase the length of each cluster root (i.e. the number of rootlets along the parent root that were initiated, or the longitudinal pattern) (Skene and James, 2000). Thus, auxin alone does not constitute the longitudinal factor.
Recent work on the early developmental events in nodule initiation using Trifolium repens, may shed some light on the longitudinal pattern (Mathesius et al., 1998). These authors reported a temporary, localized inhibition of auxin transport triggered by rhizobia, based on the expression of GH3:gusA, an auxin-responsive reporter construct. High GH3:gusA expression was also noted in pericycle cells opposite protoxylem poles prior to and during lateral root initiation. It is therefore possible that a transient block in auxin transport could explain the large-scale initiation event that occurs within the cluster root zone. Auxin has been shown to play a role in the accumulation of p34cdc2-like proteins that are needed for the activation of mitosis (Zhang et al., 1996). The fact that all species producing cluster roots, with the exception of members of the Proteaceae, also produce nodules containing N2-fixing symbionts, makes this research direction all the more interesting.
Another interesting observation is related to the temporal pattern of cluster root formation in a given plant. Cluster root production occurs in pulses (Watt and Evans, 1999; Neumann et al., 1999; Skene and James, 2000). Watt and Evans suggest that there is a central signalling cascade involved, resulting in a series of signal releases as nutrient deficiency continues (Watt and Evans, 1999). This could result from these experiments being carried out in liquid culture, where exudation by the plant cannot release unavailable nutrients, since none exists in the solution. Thus nutrient stress will continue to increase with time. Analysis of xylem and phloem sap could shed light on putative signal molecules.
Root growth is an inherent necessity for nutrient acquisition because of the depletion of ions with low diffusion coefficients, such as phosphate, around the root. Thus, the maintenance of an active meristem at the root tip plays an important role in nutrient uptake, allowing the plant to explore and exploit the edaphic environment (Skene, 2000). However, not all roots continue to grow. This may be due to physical or chemical changes from the abiotic (e.g. drought) or biotic (e.g. ectomycorrhizas) environment or due to programmed, determinate growth. For example, stem nodule roots in Sesbania rostrata Brem. show a reversible growth arrest in the G0-1 stage of the cell cycle, which is unblocked by hydration (Spencer-Barreto et al., 1995; Parsons et al., 1995). Pea roots, grown under high temperatures, cease growth (Gladish and Rost, 1993) as do sunflower roots grown under drought conditions (Robertson et al., 1990), but in both cases, growth resumes following the return of favourable conditions. Thus, this is not really determinate development. Other roots show growth arrest by programmed abscission of the meristem, including Allium (Berta et al., 1990) and Azolla (Gunning, 1978), while in Opuntia arenaria, root meristems undergo differentiation without abscission (Boke, 1979). Cluster rootlet meristems undergo differentiation at both a local (within a single rootlet) and a global (within a cluster of rootlets) level (Skene, 2000), wherein all the cells of the meristem differentiate in an orderly manner, leading to intact tissue layers at the tip of the rootlets (Skene et al., 1998a, b). Following differentiation, the rootlet tips remain physiologically active. Indeed a new programme of physiological activity ensues.
The determinate nature of cluster root development is of great interest, in terms of meristem maintenance. The global nature of this event (that is, throughout all of the rootlets in a given cluster root) is of particular interest, reflecting some pre-ordained programme, or some common signal from the parent root. Many avenues await exploration. How different is the cluster rootlet meristem from an ‘immortal’ root meristem? What changes occur leading up to determination? What is the spatial link between the temporally synchronous events of meristem differentiation and root hair production at the tip of the rootlet? The signal for root hair initiation appears to be switched on following meristem differentiation, or else some inhibitor is removed at this point. Thus, changes in gene expression relating to root hair initiation during cluster root development can be examined.
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Physiology |
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Physiological studies on cluster roots have focused on the extraordinary temporal aspects of exudation. As already mentioned, upon cessation of rootlet growth, the entire cluster root releases large amounts of organic acids, along with phosphatases and phenolics. The events behind this exudative burst have recently begun to be uncovered.
There have been conflicting reports as to the temporal relationship between organic acid efflux, and the underlying metabolic activity within roots. It has been suggested that citrate efflux is concomitant with an increase in PEPC activity (Johnson et al., 1994, 1996b), whereas a peak in in vitro PEPC activity before the efflux peak in citrate has been reported (Watt and Evans, 1999). These has also been reports of no correlation between PEPC activity and citrate efflux (Keerthisinghe et al., 1998; Neumann et al., 1999). Reduced activity of aconitase, slower root respiration and increases in activities of sucrose synthase, fruktokinase, phosphoglucomutase, and PEPC have been reported in cluster roots compared to non-cluster roots (Neumann et al., 2000). These authors (Neumann et al., 1999, 2000) demonstrated inhibition of citrate exudation when anion channel antagonists were applied to cluster roots and showed that citrate content of rootlets did not differ significantly in citrate-exuding mature rootlets compared to post-burst, non-exuding senescent rootlets. It has been concluded that the exudative burst of citrate is likely to be a product of changes in metabolism (a consequence of the effects of low P upon on metabolism) and of transport processes (Watt and Evans, 1999). It has been suggested that proton extrusion is probably related to maintenance of charge balance, either for the release of citrate (Dinkelaker et al., 1989) or the reduced uptake of nitrate (Neumann et al., 1999) although cation uptake also reduces during the reduced uptake of nitrate (JA Raven, personal communication). The use of cluster roots provides a powerful system in which to investigate control of exudation, again because of this unique temporal and spatial context. This should allow us to address questions such as the following. What controls the release of exudates from roots? Can such controls be manipulated to improve the ability of a plant to acquire nutrients?
Cluster roots also develop under low Fe in Lupinus albus, L. consentinii, Casuarina glauca, Hippophae rhamnoides, and Ficus benjamina. In L. albus grown under –Fe, citrate release, during the exudative burst, was some 10-fold higher than in –P cluster roots, although plants produced many more cluster roots under –P conditions than under –Fe conditions (Hagström et al., 2000). Low iron concentrations lead to a reduction of aconitase activity, because it is an iron–sulphur protein, and requires iron for the spatial orientation of the substrates (Hsu and Miller, 1968; De Vos et al., 1986). This results in a decrease in citrate metabolism (Landsberg, 1981). It has also been reported that, upon iron depletion, citrate synthase, isocitric dehydrogenase and succinate dehydrogenase all decrease in activity, while glycolysis and lactate formation were significantly increased in response to the decreasing ATP production via oxidative phosphorylation, in a human erythroleukemic cell line (Oexle et al., 1999). By comparing the effects of Fe and P deficiency upon gene expression during cluster root formation, it should be possible to dissect shared and unique pathways that lead to such similar structures under two different stresses. Since cluster roots are unlikely to have evolved independently in iron-stressed and phosphate-stressed conditions (based on evidence that the occurrence of cluster roots in lupins was most likely monophyletic: Skene, 2000; and see later section), while both iron and phosphate trigger their occurrence in this genus), common pathways would be expected to be involved.
Recent work has indicated that structural and functional aspects are under two separate controls, with structural characteristics involving auxin level perturbation, while functional characteristics are thought to be related directly to the effects of low P or Fe on metabolism (Gilbert et al., 2000; Neumann et al., 2000; Hagström et al., 2000). Upon addition of NAA to L. albus grown under high P, while classic cluster root morphology was produced, physiological changes, such as increased activity of phosphoenolpyruvate carboxylase (PEPC), did not occur (Gilbert et al., 2000). Thus, the morphological and physiological characteristics of the cluster root would appear not to be part of a single ‘chain reaction’. The developmental events may occur without the physiological events. This is of interest in terms of manipulating cluster root function, and in understanding the evolution of structure and function in any multicellular structure.
By bringing together the results of these experiments, an insight can be gained into how cluster root structure and function are related to phosphate and iron concentrations. In the presence of high phosphate, the addition of auxin substitutes for the conditions created by low internal P or Fe, leading to the morphological characteristics of the cluster root. However, the physiological characteristics require low phosphate or iron conditions, and the addition of auxin does not substitute for the functional implications of low internal phosphate or iron. While changes in synthesis and metabolism of citrate would appear to begin before termination of rootlet growth, the timing of citrate exudation would appear to be linked temporally with meristem differentiation, as is root hair development at the tip.
It is in the interactions of all of these elements that the cluster root has its identity. Low phosphate concentrations in the plant, reflecting low available phosphate concentrations in the environment, have repercussions for rootlet initiation and metabolism. Changes in auxin concentrations are the likely intermediate between development and internal nutrient concentrations. Meanwhile, the intense production of rootlets is likely to lead to a further local deficiency in phosphate and iron, thus acting as a positive feedback. Detailed analysis of gene expression through time will be needed in order to understand the precise sequence of events involved, and the interactions between development and physiology.
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Ecophysiology |
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The exudative burst in cluster roots not only provides an interesting system with which to study physiological events related to exudation, but it should also facilitate studies of rhizosphere microbial dynamics. The amount of citrate released in cluster roots of Lupinus albus can be between 11% (Gardner et al., 1983
) and 23% (Dinkelaker et al., 1989) of the total plant dry weight. Thus, the rhizosphere of the cluster root undergoes dramatic chemical manipulation, and the microflora within the rhizosphere and rhizoplane experience great change in their environment. The exudative dynamics are well characterized in terms of the physiology (Dinkelaker et al., 1995), developmental biology (Watt and Evans, 1999) and molecular biology (Johnson et al., 1994, 1996a, b). Research has shown that micro-organisms play significant roles in affecting root exudation in many species of plant (Meharg and Killham, 1991, 1995; Grayston et al., 1996). In turn, changing rhizosphere conditions should also influence the rhizobacterial community structure. Following rhizosphere population dynamics before, during and after the exudative burst will give a key insight into microbial response to changing resources. These studies should then allow the determination of the rate of change of size and functional characteristics of this microbial community. In the longer term, it may be possible to predict the consequences of change in the aerial environment (CO2, UV-radiation, temperature) upon the rhizosphere, both in terms of mutualistic and pathogenic considerations. In order to make such predictions, and in order to model bacterial community changes in response to changing climates, detailed data on microbial community structure and its response to change in the microenvironment that is the rhizosphere must first be acquired. |
Ecosystem studies |
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Cluster roots occur in many regions of significant biodiversity world-wide, including south-western Australia and the Fynbos, South Africa (Skene, 1998
). Species with cluster roots are often pioneers in primary or secondary succession, and important in soil stability (Gould, 1998a, b). They play important roles in key communities both in the northern and southern hemispheres (e.g. Myrica gale in north-west Europe and North America (Skene et al., 2000), and Banksia marginata in eastern Australia (Beadle, 1981)). Thus their role in these communities deserves further study. The activity of cluster roots in mobilizing phosphate and other nutrients also impacts on other species. It has been reported that Triticum aestivum, when intercropped with the cluster root-producing L. albus, had significantly higher concentrations of Mn (150 ppm) than when grown alone (90 ppm), while the concentrations of Mn in L. albus intercropped with T. aestivum were lower (6070 ppm) than when grown alone (7370 ppm) (Gardner and Boundy, 1983). Thus, mobilization of nutrients by ‘bucket chemistry’, as seen in the exudative burst, will have consequences for community structure and function. The impact of a neighbour that can significantly alter the availability of nutrients will surely be important in terms of competition and nutrient cycling. This needs further investigation.
In the wallum heathland of Australia, cluster roots of Hakea species, which are mostly concentrated in the litter layer, are able to take up organic nitrogen and ammonium in equal amounts, unlike other non-mycorrhizal or weakly VAM species, which cannot assimilate organic nitrogen, and are akin to to ecto- and ericoid mycorrhizal species, which can (Turnbull et al., 1996). Thus, plants with cluster roots demonstrate niche differentiation in terms of their ability to take up different nitrogen sources compared to non-cluster rooted species (Chapin et al., 1993; Kielland, 1994).
An interesting case study of plants with cluster roots having an effect upon their environment comes from the use of Casuarina in the rehabilitation of a formerly barren fossil coral limestone quarry near Mombasa, Kenya (groundwater pH 7.4) (Wood, 1987). It was reported that Casuarina glauca is only able to grow and nodulate in alkaline conditions if cluster roots are formed (Diem et al., 2000). As a result of the successful growth and resultant litterfall, the Casuarina trees led to an amelioration of conditions at the quarry, allowing other species to grow, and resulting in luxuriant vegetation (Diem et al., 2000). Thus cluster-rooted plants are also important in community development, and show potential in bio-remediation projects.
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Evolutionary studies |
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In terms of the evolution of these structures, their phylogenetic distribution is of interest. Among the Proteaceae, all species so far examined, with the exception of the primitive genus (based on phylogenetic analysis by Johnson and Briggs, 1975
), Persoonia, produce cluster roots (Lamont, 1982). This ancient family is indigenous to South Africa, South America and Australia (Johnson and Briggs, 1975), indicating a Gondwanan distribution of cluster roots. In contrast to this, cluster root evolution in Lupinus is thought to have been much more recent. New phylogenetic evidence points towards a single origin of cluster roots in lupins at around 2.5–3 million years ago, and in only eight of the 600 species (Skene, 2000).
All species that produce these structures, with the exception of the Proteaceae, form symbioses with nitrogen-fixing bacteria. They either never form mycorrhizas or they produce cluster roots under conditions where mycorhizal development is precluded by environmental conditions, such as waterlogging or disturbed habitats (Skene, 1998). The association with nodulation may either involve common pathways or else the two adaptations may have evolved separately in response to demanding environments where both N and P are limiting. For example, the eight species of Lupinus that produce cluster roots were thought to have evolved from a narrow genetic base from the late Tertiary (Gladstones, 1998; Skene, 2000). Repeated fluvial events associated with glaciation cycles in the Quaternary would have resulted in soils low in nutrients and organic matter. While all Lupinus species tested fix nitrogen, only these eight species form cluster roots. Among the plants that produce cluster roots, only the Proteaceae do not form nodules. Thus, there is the possibility that this family might make an interesting model in which to attempt to induce nodules, if there is a common link between the two adaptations.
Other interesting questions relate to how this one structure has undergone specialization in order to operate in a number of different niches. For example, how different are cluster roots of plants such as Viminaria juncea or Myrica gale, both of which occupy waterlogged environments, from those of L. albus or Grevillea robusta that are intolerant of waterlogging? Why is Persoonia the only genus of the Proteaceae that does not produce cluster roots? What differences exist between the neighbouring clade of Lupinus, composed of L. angustifolius, L. luteus and L. hispanicus, with that of L. micranthus and L. albus, wherein the latter clade all produce cluster roots, yet the former do not? Both are Old World, smooth-seeded, nitrogen-fixing clades, yet only one produces this significant adaptation. A comparison of L. albus and L. angustifolius may yield an important insight into the key genetic information involved in cluster root formation and function. Techniques are now available to approach these problems. The search for answers to questions relating to development and physiology, posed earlier, will be greatly enlightened by research into these evolutionary issues.
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Biotechnology |
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Four key characteristics of cluster roots have been identified (Skene, 2000
): the clustered nature of rootlets; the synchronous, determinate development of rootlets; the exudative burst; and the enhanced absorption of P per unit area of root. What then are the opportunities of genetic manipulation in order to facilitate cluster root production, or some elements of it, in species within which they are not presently produced? Unlike mycorrhizas and nitrogen-fixing nodules, cluster roots are not dependent on another organism for their development (although microbes enhance cluster root production, possibly through the production of auxins: Skene and James, 2000). The broad phylogenetic diversity of species producing cluster roots, and the conservative developmental and physiological characteristics across all species, would suggest that there may be only a limited number of changes needed at the genetic level in order to lead to the formation of these structures. Also the key characteristics represent extensions of normal root properties, rather than completely new structures. Thus, the task of identifying genes of significance and subsequently engineering other species to produce cluster roots should be much more straightforward than attempting to develop symbiotic relationships where they did not previously exist. Recent work has demonstrated the production of recombinant proteins, using root exudation (Borisjuk et al., 1999; Gleba et al., 1999). The cluster root, with its highly up-regulated rhizo-deposition, would make an excellent system with which to increase the productivity of such an approach. Cluster roots have not been found in monocotyledons, and so efforts should be concentrated upon dicotyledons. The ability to improve phosphate and iron uptake without the addition of fertilizers makes the cluster root a valuable biotechnological target.
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Acknowledgments |
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I am indebted to the Royal Society, the Nuffield Foundation and the University of Dundee for funding. Also I thank two reviewers, and Professor HG Jones for their helpful criticisms.
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Notes |
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1 Fax: +44 1382 344275. mailto\|[colon ]\|k.r.skene{at}dundee.ac.uk
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References |
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