JXB Advance Access originally published online on September 19, 2005
Journal of Experimental Botany 2006 57(2):401-411; doi:10.1093/jxb/eri280
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RESEARCH PAPER |
Plastic plants and patchy soils
Department of Biology, Area 14, PO Box 373, University of York, York YO10 5YW, UK
* Fax: +44 (0)1904 328564. E-mail: ah29{at}york.ac.uk
Received 11 May 2005; Accepted 4 August 2005
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Abstract |
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 Top Abstract IntroductionWhat is a patch?What are plastic plants?The role of mycorrhizaCompetition for nutrient...Concluding remarksReferences |
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Soil nutrients are distributed in a non-uniform or ‘patchy’ manner. It is well established that the modular nature of root systems allows them to show both morphological and/or physiological plasticity upon encountering nutrient-rich patches. These plastic responses are widely believed to be foraging mechanisms by the plant to enhance nutrient resource capture. Although morphological plasticity has traditionally been viewed as the more expensive option as it requires new root construction, more recent evidence suggests this may not necessarily be the case. Moreover, plants may be able to recapture most of the initial outlay involved in new root construction, again lowering the overall cost to the plant. Under natural conditions the roots of most plant species have an additional nutrient acquisition mechanism namely mycorrhizal symbiosis. However, the impact of these important symbiotic associations upon the host plant's response to nutrient patches has received relatively little attention. The mycorrhizal fungal symbiont should, in theory, be better able to compete directly with the rest of the microbial community for the nutrients in the patch. This could potentially be important to the host plant, as generally, root proliferation responses are more important for interspecific plant, than plant–microbial, competition.
Key words: Mycorrhizal symbiosis, nutrient competition, nitrogen, root physiological and morphological plasticity
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Introduction |
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TopAbstractIntroductionWhat is a patch?What are plastic plants?The role of mycorrhizaCompetition for nutrient...Concluding remarksReferences |
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Soils are unique in that they have a solid, gaseous and liquid phase making them the most complex of environments. This complexity gives rise to a heterogeneous environment at a range of scales from those that affect an individual plant root to that of the entire ecosystem. In this paper, however, comments will be restricted only to the heterogeneity that impacts upon individual plants. This is by no means taking the easy option. Geostatistical analysis has demonstrated that, within the rooting zone of an individual plant, there can be as much variation in nutrient availability as within the entire 120 m2 plot examined (Jackson and Caldwell, 1993a
, b). It is also the level at which most studies have been based.
Roots systems are modular. This allows them to be extremely plastic and therefore to cope with the heterogeneous nature of soil and the patchy distribution of nutrients within the soil. Although enhanced root growth in fertile soil zones was reported in the late 1800s (Nobbe, 1862, and Höveler, 1892, cited in Fitter, 1987), it was the series of studies by Drew and co-workers in the 1970s on barley root systems proliferating in nutrient-rich zones of phosphate, nitrate, and ammonium that is much quoted in this respect (Drew et al., 1973; Drew, 1975; Drew and Saker, 1975, 1978). The stunning images of the root system responding to the local supply of these nutrients published at the same time helped to increase the impact of this work. However, the experimental conditions employed by Drew and co-workers (exposing parts of the root system to a 100 times greater concentration of N or P compared with the rest of the root system) probably demonstrate root proliferation at its maximal. In the soil such proliferation responses may be damped as more than a single nutrient-rich patch is likely to be encountered and nutrient gradients over the entire root may not be as extreme. Moreover, Drew's work was conducted in a sand culture system and so the complex interactions between micro-organisms and roots for nutrient resources were minimized compared with those which occur in soil systems. In addition, in the natural environment most plant roots are in symbiotic associations with mycorrhizal fungi. Thus, the possible contribution of the mycorrhizal fungal symbiont to resource capture and the impact upon the response by the host root should also be considered. Nevertheless, a wealth of literature exists to support the conclusion that roots are physiologically and morphologically plastic in nutrient-rich zones (Jackson et al., 1990; Hutchings and de Kroon, 1994; Hodge, 2004). Rather than repeat the numerous reviews that have recently been published on this topic (Robinson and van Vuuren, 1998; Schenk et al., 1999; Fitter et al., 2000; Hodge, 2004) some of the gaps in our knowledge and areas that still remain to be addressed will be identified here.
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What is a patch? |
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TopAbstractIntroductionWhat is a patch?What are plastic plants?The role of mycorrhizaCompetition for nutrient...Concluding remarksReferences |
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‘Heterogeneity (patchiness): variability with a spatial structure, such that spatial distributions are not uniform or random, but aggregated (patchy, clumped)’All soils are heterogeneous not only spatially, as defined by Ettema and Wardle (2002)Ettema and Wardle, 2002
above, but also temporally. Ask any soil scientist and they will tell you the five main factors which determine soil formation are: parent material, organisms present, climate, topography, and time as first proposed by Hans Jenny (1941). Although this explains differences between soils, within each soil itself are finer, but no less important, degrees of nutrient heterogeneity which influence overall soil fertility (reviewed by Stark, 1994).
Although nutrient ions will all diffuse at approximately the same rate in free solution, in soil, due to interactions with charged surfaces such as organic materials and clays, mobility becomes much more restricted. Moreover, different ions are varyingly affected by such interactions. For example, nitrates are relatively unaffected and their diffusion coefficient (D) in soil is c. 10–10 m2 s–1, which is close to that in free solution (c. 10–9 m2 s–1 ). By contrast, the diffusion coefficient (D) for phosphate in soil is much slower (c. 10–13–10–15 m2 s–1 ) because phosphate ions form insoluble complexes with Al3+, Fe3+, and Ca2+ (Tinker and Nye, 2000). As roots can only absorb ions transported via diffusion and mass flow (Tinker and Nye, 2000) the differences in ion mobility in soil impact greatly upon the nutrient status of the plant. Diffusion of these nutrients will obviously be affected by the water status of the soil. In the field, measuring such responses can be difficult as root systems can also show physiological and morphological plasticity to water patches (Huang and Eissenstat, 2000), but increased water content will also enhance ion mobility through the wet patch of soil. By contrast, oxygen diffusion will decrease as soil pores become filled with water rather than air. Thus, which factor the root is responding to (i.e. increased nutrients, water or both) may not always be obvious.
Using geostastical analysis Jackson and Caldwell (1993a) demonstrated concentrations of nitrate and ammonium varied by c. 100–400% within 1 m distances in a sagebrush steppe. Concentrations of extractable phosphate varied at even smaller spatial scales. By removing soil cores, Farley and Fitter (1999a) found differences in soil phosphate, ammonium, and nitrate concentrations at scales greater than 2 m in a woodland soil. Nitrate and ammonium concentrations in the soil solution, however, showed 2–5-fold differences at scales of only 20 cm. Farley and Fitter (1999a) conducted their study over a 2-year period. While they found that there was a degree of seasonality in their data set, the temporal pattern was largely unpredictable. Furthermore, localized peaks of nutrient concentration were short-lived, lasting no more than 4 weeks. These studies demonstrate that, in the field, spatial heterogeneity in the supply of nitrate, ammonium, and phosphate occurs at scales relevant to plant roots and that roots must respond rapidly to acquire temporally available peaks of nutrients in the soil solution.
The solid phase is also important for creating nutrient heterogeneity. Inputs from plants via leaf litter and rhizodeposition have significant effects on nutrient dynamics creating ‘resource islands’ (Reynolds et al., 1990) around the plant that are associated with increased microbial activity resulting in higher mineralization and denitrification rates (Charley and West, 1977; Halvorson et al., 1995; Vinton and Burke, 1995). Protozoa and nematode populations can also increase locally in these resource islands. For example, after the addition of decomposing barley roots to soil, nematode and protozoan populations increased significantly, but this stimulatory effect was localized to less than 1.8 mm from the decomposing roots (Rønn et al., 1996). Previously, there has been much research on the addition of inorganic nutrients mainly in the form of nitrate or phosphate enriched patches to plants in microcosms (Cui and Caldwell, 1998; Linkohr et al., 2002) or in the field (Jackson et al., 1990; Jackson and Caldwell, 1991; Pregitzer et al., 1993; Fitter et al., 2002). In the natural environment, organic inputs of varying complexity are the norm. The microbial decomposition of these patches themselves will be both spatially and temporally variable, depending on the prevailing soil conditions at the time as well as the quality of the substrate being decomposed. Although there is some evidence that plants may be able to take up some simple forms of organic N (such as amino acids) intact, evidence that this is an important N capture mechanism for plants is still lacking (see Jones et al., 2005, for more on this issue). There has been some work to address the root responses to these types of organic patches (Hodge et al., 1999a, b, 2000a), but still comparatively little is known about the responses of roots in the field and the consequences of heterogeneity on plant community structure and function. This is important because, although some areas of the world can receive significant N inputs through rainfall, which will tend to reduce spatial heterogeneity, in most soils solid forms of organic N constitute the dominant form of N present (Stevenson, 1982).
Collectively, these studies demonstrate for the plant root that the distribution of resources can be thought of as ‘patchy’. The distribution of roots within the soil generally follow the pattern of nutrient resource distribution (Fitter, 1994) although not always (Caldwell et al., 1996). In the latter case, roots were extracted from soil cores taken from the field and included roots of varying age, not all of which may have been involved in nutrient acquisition at the time of sampling. Also some potential nutrient patches, such as a dead microbe or a soil animal, perhaps even dead single roots themselves, may be too small to influence root responses. Although there is a wealth of studies upon the response of plant roots to nutrient-rich patches, surprisingly few have considered the characteristics (i.e. duration, concentration, number) of the actual patch itself (Farley and Fitter, 1999b; Hodge et al., 1999a, 2000a, d; Duke and Caldwell, 2000). The minimum size a nutrient-rich ‘patch’ has to be in the soil before a plastic response is evoked by a root is unknown, but will probably ultimately depend upon the nutrient status of the plant at the time, as well as the background soil fertility. In any case, size probably matters less than concentration. If a patch is large but of low concentration it may be insufficiently fertile to evoke any response. If highly concentrated but very small it may not be detected by the root system. Theoretical responses of plant roots, populations, and communities to patches and larger-scale heterogeneity have recently been reviewed (Hutchings et al., 2003; Hodge, 2004).
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What are plastic plants? |
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TopAbstractIntroductionWhat is a patch?What are plastic plants?The role of mycorrhizaCompetition for nutrient...Concluding remarksReferences |
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‘Plasticity is shown by a genotype when its expression is able to be altered by environmental influences.’Roots in nutrient-rich patches can demonstrate both physiological and morphological alterations compared with those roots outside the patch zone. In other words they are plastic in their ability to increase ion uptake and/or deploy new roots. There is also increasing evidence that plants may be able to discriminate between self and non-self roots and that this enables the plant to minimize competition between their own roots (Falik et al., 2003Bradshaw, 1965
; Gruntman and Novoplansky, 2004). For example, the clonal perennial grass Buchloe dactyloides, developed fewer and shorter roots in the presence of other roots of the same individual (Gruntman and Novoplansky, 2004). Moreover, once cuttings that originated from the same node were separated they became progressively alienated from each other. Gruntman and Novoplansky (2004) suggested that this demonstrates that the response is mediated by physiological co-ordination among roots that develop on the same plant rather than allogenetic recognition. The plant can also co-ordinate its root growth in response to environmental conditions such as patchy nutrient supply by investing more root growth in the nutrient-rich patch at the expense of root growth elsewhere (Gersani and Sachs, 1992; Linkohr et al., 2002).
Physiological alterations in ion uptake can be both large and rapid (Jackson et al., 1990; Jackson and Caldwell, 1991; Ivans et al., 2003). However, physiological plasticity should not necessarily be viewed as a less expensive means of exploiting a patch than new root construction. For example, Robinson (2001) estimated that root proliferation might only require an extra 0.2% of the plant's daily carbon gain. This figure compares favourably with other plant sinks involved in nutrient acquisition such as the 4–20% of host plant photosynthate allocated to mycorrhizal symbionts (Paul and Kucey, 1981; Snellgrove et al., 1982; Koch and Johnson, 1984; Jakobsen and Rosendahl, 1990; Fitter, 1991; Rygiewicz and Anderson, 1994) or citrate export into the soil from lupin cluster roots which represented 23% of the plant dry weight (Dinkelaker et al., 1989). However, the balance of ‘benefits’ and ‘cost’ will depend on other factors such as patch size and duration, photosynthetic supply etc.
Although Robinson (2001) estimated root proliferation to be relatively inexpensive for the plant, shading experiments reveal that plastic responses may be more of a burden if photosynthetic supply is restricted. Although both physiological and morphological plasticity in nutrient-rich patches is reduced when plants are shaded (Jackson and Caldwell, 1992; Bilbrough and Caldwell, 1995; Cui and Caldwell, 1997), which response is restricted the most depends on the plant species (Cui and Caldwell, 1997), the type of patch (Jackson and Caldwell, 1992; Cui and Caldwell, 1997) and, presumably, the nutrient status of the plant. If shading simply reduced nutrient demand by the plant then nutrient capture would be lower irrespective of the spatial placement of nutrients, however, this is not the case. Shaded loblolly pine (Pinus taeda) and sweetgum (Liquidambar styraciflua) both had reduced biomass when grown in a patchy compared with a uniform nutrient environment (Mou et al., 1997). Thus exploiting a patchy nutrient environment via plastic responses must be more expensive, yet this is what plants do. The benefits of being plastic must out-weigh the disadvantages otherwise the response would surely have been lost during evolution. In any case, ‘uniform’ supplies of nutrients are an artefact of scientific experiments rather than nature where heterogeneity is the norm.
Roots are quite remarkable in their ability to make physiological and morphological adjustments to resource heterogeneity. Fine roots can be rapidly deployed into nutrient-rich patches to exploit the resources within the patch, although species may differ widely in their absolute response (Campbell et al., 1991; Wijesinghe et al., 2001). These fine roots also tend to be short-lived compared with coarser roots. Thus, depending on the life span of the patch, high turnover rates may be required to exploit the patch fully. Root turnover in both fertile soils (Aber et al., 1985; Pregitzer et al., 1995) and patches (Gross et al., 1993; Hodge et al., 1999b; but see also Pregitzer et al., 1993 and Hodge et al., 1999a) tends to be higher than in nutrient-poor areas which again may be perceived as a costly outlay for the plant, particularly if the patch is short-lived and the initial construction costs are not repaid. Ultimately, ‘cost’ to the plant will depend on what is actually limiting growth (i.e. nutrient or photosynthetic supply).
Thus, fine roots play a major role in patch exploitation; but what exactly are ‘fine’ roots? In the past, largely for the sake of simplicity, there has been a tendency to group roots together based purely upon size. Generally, roots less than 2.0 mm have been deemed to be ‘fine’ roots (Hendrick and Pregitzer, 1992; Hendricks et al., 1993). There is also evidence that some fine roots in cohorts are longer lived than others, i.e. they go on to become structural, coarse roots (Fitter et al., 1997). What causes some fine roots to die and others to persist is currently unknown. More recently, however, there is mounting evidence that all fine roots are not equal and to group them together based purely upon size, rather than also taking into account position on the root, depth in the soil etc, is inadequate for an understanding of true function or activity. For example, Pregitzer et al. (1998) demonstrated that respiration rates of sugar maple roots <0.5 mm in diameter were 2.4–3.4 times higher than roots of larger diameter. Moreover, roots in nutrient patches actively involved in nutrient uptake had higher respiration rates. Root respiration also varied with depth, being lower at greater depth in the soil. Intriguingly, these finer roots also had the greatest N concentrations, and root respiration costs were related to N concentration rather than carbon content (Pregitzer et al., 1998). Other studies confirm that there is a strong relationship between respiration and N concentrations in fine roots (Reich et al., 1998; Tjoelker et al., 2005).This implies these roots are initially costly for the plant to construct, certainly in terms of N. However, such large costs may only be transient in nature, and the plant may quickly recover its initial outlay. Volder et al. (2005) demonstrated that both nitrate and root respiration rates of fine roots of grape (Vitis rupestrisxV. riparia cv. 3309 C) declined rapidly: within a 24 h period a 50% decline was observed. Root N concentrations also decreased rapidly with 3-d-old roots having half the N concentration of 1-d-old roots. This reduction in N concentration was due to the translocation of N from the roots and thus the plant recovering its initial outlay. Similarly, Tjoelker et al. (2005) found a decline in both respiration rates and N concentration with increased longevity of both leaves and roots, while a rapid decline in root respiration and phosphate uptake in fine roots of both apple and orange has also been reported (Bouma et al., 2001). These findings have led to the suggestion that although fine roots may become less efficient at nutrient uptake the concurrent decline in maintenance costs may result in the actual efficiency of uptake remaining the same or even increasing in the longer term, assuming that nutrient supply does not become limiting (Bouma et al., 2001; Volder et al., 2005). In natural environments such a scenario seems unlikely as patch resources will eventually become exhausted, nevertheless, this work is important as it provides clear evidence that even though roots may persist in the soil for a considerable time they are constantly changing rather than remaining a static mass.
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The role of mycorrhiza |
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TopAbstractIntroductionWhat is a patch?What are plastic plants?The role of mycorrhizaCompetition for nutrient...Concluding remarksReferences |
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‘The study of plants without their mycorrhizas is the study of artefacts.’
BEG Committee, 1993; http://www.kent.ac.uk/bio/beg/englishhomepage.htmMost plants in the natural environment form associations with mycorrhizal fungi. In common with the response of plant roots, mycorrhizal fungi of the ectomycorrhizal (Bending and Read, 1995
) and arbuscular mycorrhizal (AM) (Mosse, 1959; Nicolson, 1959; St John et al., 1983a, b; Hodge et al., 2001) associations have also been demonstrated to proliferate hyphae in nutrient zones. Free-living fungi also demonstrate a similar response (Dowson et al., 1989; Ritz et al., 1996). Thus, perhaps rather unsurprisingly, fungi are also plastic in their response to nutrient availability.
It is also well established that mycorrhizal fungi in the ericoid and ectomycorrhizal associations possess saprophytic capabilities which enable N capture from complex organic sources including proteins and chitin, that otherwise the non-mycorrhizal root would not have direct access to (Bajwa and Read, 1985; Abuzinadah and Read, 1986; Hodge et al., 1995; Kerley and Read, 1995, 1997; Chalot and Brun, 1998). However, different fungal species, and even strains of the same fungus, differ widely in their ability to capture nutrients from such complex organic sources (Smith and Read, 1997). Thus, all mycorrhizal fungi are not equal as regards their nutritional benefit to their host. Moreover, had this review been written a few years ago the most widespread of all the mycorrhizal symbiosis associations, namely the arbuscular mycorrhizal (AM) association which can form on around two-thirds of all plant species, would have been dismissed as having no role to play in N capture from complex organic sources in the soil. More recent evidence, however, has meant that this assumption may need to be reconsidered.
Hodge et al. (2001) have demonstrated that an AM fungus, Glomus hoi, both promoted decomposition of, and enhanced N (followed as 15N) capture from, a complex organic material (Lolium perenne shoots) added to soil. A compartmented microcosm unit was used in which each unit had two sides, a control and an experimental. Each side was further divided into three compartments: the organic patch compartment, a plant compartment containing the AMF inoculum, and an uninoculated plant compartment. Meshes divided the compartments from each other. On the experimental side of the unit both meshes were 20 µm in size. This size of mesh allows AM hyphae, but prevents roots from penetrating. On the control side the mesh separating the two planted compartments was also 20 µm in size. The mesh separating the organic patch and the inoculated plant compartment, however, was 0.45 µm in size. This size of mesh (i.e. 0.45 µm) prevents both roots and AM hyphae from penetrating. Thus, the only difference between the experimental and the control sides of the microcosm unit were that on the experimental side the AM hyphae were permitted access to the organic patch whereas on the control side the AM hyphae were denied access to the organic patch compartment. By the end of the experiment (42 d after the organic patch addition) plants on the experimental side of the unit had captured 15% of the N originally added in the patch whereas those on the control side had captured only 5% of the N originally added in the patch. The N from the patch captured by the inoculated plant on the control side must have occurred via the diffusion of decomposition N products across the mesh. The extra N captured by the inoculated plant on the experimental side must have been due to the AM fungus. This was supported by the fact that AM hyphal proliferation within the patch was directly related to 15N capture from the patch by the associated host plant in the inoculated plant compartment (Hodge et al., 2001).
No saprophytic capabilities have been reported for AM fungi, therefore it seems unlikely that the fungus itself was involved directly in the organic matter decomposition. The most likely explanation is that bacteria closely associated with the AM hyphae were able to enhance the decomposition process and the AM fungus then competed well with the other micro-organisms present for the inorganic N subsequently released. AM hyphal proliferation observed in the patch may also have promoted patch decomposition by physically increasing patch break-up and so enhancing the surface area for decomposition to proceed. Growth of the AM fungus was also promoted in the presence of the organic patch, and was higher than growth into the uninoculated plant compartment, indicating that the fungus itself was benefiting in some way from the organic patch or its decomposition products (Fig. 1). These results suggest that AM fungi may play a previously unrecognized role in N capture from patchy nutrient supplies.
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Mycorrhizal hyphal proliferation instead of root proliferation would appear to make more economic sense for the plant. Because of their size, hyphae should be (i) less expensive to construct, (ii) more able to penetrate to the sites of decomposition, (iii) better able to compete with other micro-organisms for the nutrients in the patch, and (iv) more able to respond by proliferation to patches which are of short temporal duration or spatially discrete. In microcosm studies, however, root proliferation has been observed to be more responsive than that of AM fungi when both are experiencing the patch zone (Hodge et al., 2000b
; Hodge, 2001), but as the substrate was a mixture of sieved soil and sand, root growth tended to be favoured in these units. AM fungi may modify the response of the host roots by altering root demography within the patch zone, in addition to altering patch decomposition (Hodge et al., 2000b; Hodge, 2001). Furthermore, the mycorrhizal fungus is an organism in its own right and these fungi should not necessarily be expected to respond in such a manner as to maximize the host plants needs under all circumstances.
Common mycelial networks (CMN)
Under natural conditions mycorrhizal fungi can form an extensive common mycelial network (CMN). There has been much speculation as to the benefits this CMN may confer on host plants. Certainly it should allow rapid colonization of young seedlings rather than relying simply upon spore germination, but little is known about the ecology of this CMN, its extent in the soil, how many plants can be linked and so forth. It has been shown that ectomycorrhizal CMN may transfer carbon from one plant to another through the CMN network (Simard et al., 1997), but the form in which this carbon is transferred (i.e. as carbon or as carbon bound in amino acid form) has yet to be demonstrated (see Robinson and Fitter, 1999, for more on this issue). In terms of heterogeneity of resource supply, it has been suggested that redistribution of nutrients along this network may reduce the uncertainty of patchy nutrients for the plants linked into this network (Ozinga et al., 1997). This is an intriguing idea but there is little experimental evidence so far to support it. In a field study, Chiariello et al. (1982) applied phosphorus (as 32P) to the leaves of ‘donor’ Plantago erecta plants. After 6–7 d phosphorus was only transferred over very short distances (c. 45 mm). Moreover, neither the type nor size of the neighbouring plants or distance between the donor and receiver were indicators of the amount of phosphorus transferred, implying that the AM fungus connected to the donor root system was not similarly connected to all its closest neighbours. To what extent internal colonization of the root system was related to the amount of P transferred is unknown in this study. Thus, although there is potential to move nutrients along the CMN the distance nutrients move may be relatively small.
AMF influence upon plant community structure
More recently, the situation has become even more complex with increasing evidence that plant–AMF combinations may be more restricted than previously believed. It has long been assumed, mainly due to the large number of plant species (perhaps as much as 200 000) and the relatively small number of fungi involved (only c. 150 have thus far been identified), that AMF must lack any degree of specificity. However, it has been demonstrated that the species of AMF recovered can vary with the host plant present (Eom et al., 2000; Bever et al., 2001; Vandenkoornhuyse et al., 2002) and that different AMF have varying effects on different plant species (van der Heijden et al., 1998, 2003; Helgason et al., 2002; O'Connor et al., 2002). The microcosm study of van der Heijden et al. (1998) demonstrated that increasing the diversity of AMF improved plant community productivity. Collectively, the results of these studies imply that plants may at least be able to select the AMF that benefit them the most and/or AMF can demonstrate a host preference. This, together with the evidence that AMF are multifunctional (Newsham et al., 1995), complicates matters as different AMF present in the same root may be performing different functions, some may even be cheating by obtaining carbon from their host plant but with no reciprocal benefit to the plant. Thus, it is necessary to develop more sophisticated techniques to identify the contribution different AMF are making to nutrient capture in the field. Currently, no such techniques exist and therefore our understanding of AMF nutrient dynamics comes largely from model systems conducted under controlled conditions. This, by its very nature, may be misleading, as the AMF that are more readily able to be cultured may be more generalist in nature and, hence, there is the risk of missing those fungi which may have more specialist roles.
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Competition for nutrient resources in the soil environment |
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TopAbstractIntroductionWhat is a patch?What are plastic plants?The role of mycorrhizaCompetition for nutrient...Concluding remarksReferences |
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The importance of root proliferation for N capture from patches must be considered within the context of plant–plant competition. Previously, root proliferation to N-rich patches appeared a paradox because, although root proliferation within N-rich patches could easily be demonstrated, the benefit in terms of N capture from the patch could not (van Vuuren et al., 1996
; Hodge et al., 1998; Fransen et al., 1998). These three earlier studies all used different plant species but in all cases plants were grown as individuals. It has since been demonstrated that when plants are grown in interspecific plant competition for a common complex organic patch then root proliferation does make sense: the species which proliferated the most captured the most N (Hodge et al., 1999c, 2000c; Robinson et al., 1999). The benefit of root proliferation could be demonstrated under these conditions because the complex organic patch contained a mixture of N sources, thus, release of N for plant capture would have occurred both spatially and temporally throughout the patch. Consequently, the species with the most roots in the patch was more likely to be present when the available N was released allowing capture before the weaker proliferator competitor plant. By contrast, when plants are grown as individuals then root proliferation is less important because the plant roots will capture most of the N released from the decomposing patch irrespective of the amount of roots in the patch due to the high mobility of the 
ion. In addition, there is evidence that the plastic response of different plant species respond differently to shading, thus competitive interactions between species may also vary depending on light availability (Mou et al., 1997; Huante et al., 1998). Thus, increased root proliferation does result in an increased benefit when plants are in interspecific plant competition, but does it have any role to play in plant–microbial competition?
At harvest, 49 d after patches of varying physical and chemical complexity had been added to soil–grass sward systems, the plants had captured more N from the patches with a low C:N ratio (urea, algal amino acids, algal cells, and L-lysine) than that estimated to be in the microbial biomass (Fig. 2; Hodge et al., 2000a). By contrast, plant N capture from the most complex patch with the highest C:N ratio was comparable to that captured by the microbial biomass, but this patch still had to be fully decomposed as demonstrated by the amount estimated to be present as unaltered substrate (Fig. 2). Thus, from these data it does appear that plants are effective competitors with micro-organisms for the available patch resources. To test if this was actually the result of direct competition or simply because plant roots represent a slower turnover pool compared with the microbial biomass, dead earthworms or L. perenne shoot material were added as patches of varying C:N ratio (i.e. 4.1:1 earthworm; 12.2:1 L. perenne shoots) and destructively harvested units after 3, 7, 14, and 30 d. In both patches protozoan biomass and nematode numbers peaked at day 7 but then declined. By contrast, plant N capture was less than 2% of the N originally available at day 7, but increased over the next two harvest dates until by day 30 plants had captured 29% and 22% of the N in the earthworm and the L. perenne shoot patches, respectively (Hodge et al., 2000d). Thus, plants are effective competitors with micro-organisms for patch resources but only because they represent a slower turnover pool (Kaye and Hart, 1997; Hodge et al., 2000e).
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Concluding remarks |
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TopAbstractIntroductionWhat is a patch?What are plastic plants?The role of mycorrhizaCompetition for nutrient...Concluding remarksReferences |
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Plants demonstrate both physiological and/or morphological plasticity to exploit the patchy distribution of nutrient resources in the soil environment. Often physiological responses occur first and may act as a signal that the patch is durable and so trigger new root construction (i.e. morphological responses) in the patch zone (Hodge, 2004
). Physiological responses to short-lived patches would make economic sense. Although recent evidence suggests new root construction may not be as costly as previously believed, it may still take considerable time for substantial root proliferation to occur (Hodge et al., 1998, 1999c). There remains much debate as to which plastic response, physiological or morphological, is the more important. However, simply measuring the type and size of the response is insufficient without an understanding of the context in which the response is expressed. Plant root systems may be able to discriminate between self and non-self roots (Falik et al., 2003; Gruntman and Novoplansky, 2004), so the extent of the plastic response in patches will be influenced by the type and density of neighbouring species (Huber-Sannwald et al., 1996, 1997; Hodge et al., 1999c, 2000c; Robinson et al., 1999). Neighbouring species will also influence above-ground competition for light and the extent to which plants experience shading as a result of above-ground competition will affect root plasticity in nutrient patches in addition to other competing sinks for carbon in the plant, such as mycorrhizal symbiosis. Ectomycorrhizal colonization has been shown to increase root longevity (King et al., 2002), while AM colonization has been shown to increase root proliferation specifically within an organic patch zone (Hodge et al., 2000b). Furthermore, AM colonization increased N capture from a complex organic patch, but only when plants were grown in interspecific competition (Hodge, 2003). The role that mycorrhiza may play in nutrient acquisition from patches is only just beginning to be unearthed and more research effort is clearly required.
Most previous research has concentrated upon the addition of inorganic patches of phosphate or nitrate. In natural systems, however, complex organic patches are the norm. The spatial/temporal decomposition, and, hence nutrient release, from these complex patches will be vastly different from simply adding an inorganic patch. Thus, there is a need for more realism in the selection of patch materials to be studied. There is also increasing evidence that the manner in which root systems are sampled needs to be rethought if root function is truly to be understood. More attention needs to be taken upon branching order, the relation of the root compared with others, and the degree of mycorrhizal colonization (Pregitzer, 2002, 2003; Zobel, 2003). The difficulty, of course, is roots are buried underground and simply viewing part of the root system by minirhizotron techniques may be insufficient to obtain the detailed information required. Assessing AM colonization in situ is also difficult as, unlike the ectomycorrhizal symbiosis where a fungal sheath encases the colonized root making visual identification of the degree of colonization of the root system much easier, there are no such external hints as to whether a root is colonized by AMF or not. Thus, sampling strategies need to be more precise. There is evidence that root systems can co-ordinate their growth so that more effort is placed into growing into nutrient-rich zones and reduced into nutrient-poorer areas (Gersani and Sachs, 1992; Linkohr et al., 2002). However, when does an exhausted patch become a nutrient-poor zone, and when can root growth be expected to be reduced in the ‘de-patch’? In the experiments that have been conducted root proliferation has either continued or has been maintained at a high level even when it would be expected that the patch would be exhausted (Hodge et al., 1999a, 2000a; Hodge, 2001). Although the studies have been relatively short-term (i.e. a few months) the simple organic patches such as urea, lysine, and glycine applied would be expected to have been fully utilized within this period (Fig. 2). The turnover of microbial biomass may result in a secondary nutrient-rich patch long after the original patch has been exhausted. Yet few studies have considered the effects upon the microbial community (van Vuuren et al., 1996; Hodge et al., 1999b). Root proliferation itself would also be expected to enhance microbial populations in the patch zone as more roots would result in increased root exudation/secretion processes to fuel the microbial biomass, but again this area has received little research attention. Future studies therefore need to consider the soil–plant system as a whole rather than simply focusing upon the plasticity response of individual plants under relatively contrived experimental growing conditions. The consequences of soil heterogeneity upon plant community structure in the field remains the big unknown.
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Acknowledgements |
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AH is funded by a BBSRC David Phillips Research Fellowship. This paper was one of a series of invited presentations at a session on Plasticity in plants, held as part of the Society for Experimental Biology Plant Frontier Meeting, Sheffield University in March 2005. Funding for the session was provided by the Journal of Experimental Botany, which is gratefully acknowledged. I thank two anonymous referees for their helpful comments that improved the manuscript.
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