JXB Advance Access originally published online on September 19, 2005
Journal of Experimental Botany 2006 57(2):401-411; doi:10.1093/jxb/eri280
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
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
 |
Abstract |
|---|
 Top Abstract IntroductionWhat is a patch?What are plastic plants?The role of mycorrhizaCompetition for nutrient...Concluding remarksReferences |
|---|
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
|
Introduction |
|---|
|
TopAbstractIntroductionWhat is a patch?What are plastic plants?The role of mycorrhizaCompetition for nutrient...Concluding remarksReferences |
|---|
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.
|
What is a patch? |
|---|
|
TopAbstractIntroductionWhat is a patch?What are plastic plants?The role of mycorrhizaCompetition for nutrient...Concluding remarksReferences |
|---|
‘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).
|
What are plastic plants? |
|---|
|
TopAbstractIntroductionWhat is a patch?What are plastic plants?The role of mycorrhizaCompetition for nutrient...Concluding remarksReferences |
|---|
‘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.
|
The role of mycorrhiza |
|---|
|
TopAbstractIntroductionWhat is a patch?What are plastic plants?The role of mycorrhizaCompetition for nutrient...Concluding remarksReferences |
|---|
‘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.
|
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.
|
Competition for nutrient resources in the soil environment |
|---|
|
TopAbstractIntroductionWhat is a patch?What are plastic plants?The role of mycorrhizaCompetition for nutrient...Concluding remarksReferences |
|---|
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).
|
|
Concluding remarks |
|---|
|
TopAbstractIntroductionWhat is a patch?What are plastic plants?The role of mycorrhizaCompetition for nutrient...Concluding remarksReferences |
|---|
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.
|
Acknowledgements |
|---|
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.
|
References |
|---|
|
TopAbstractIntroductionWhat is a patch?What are plastic plants?The role of mycorrhizaCompetition for nutrient...Concluding remarksReferences |
|---|
Aber JD, Melillo JM, Nadelhoffer KJ, McClaugherty CA, Pastor J. 1985. Fine root turnover in forest ecosystems in relation to quantity and form of nitrogen availability: a comparison of two methods. Oecologia 66, 317–321.[CrossRef][Web of Science]
Abuzinadah RA, Read DJ. 1986. The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. I. Utilization of proteins and peptides by ectomycorrhizal fungi. New Phytologist 103, 481–493.[CrossRef][Web of Science]
Bajwa R, Read DJ. 1985. The biology of mycorrhiza in the Ericaceae. X. The utilization of proteins and the production of proteolytic enzymes by the mycorrhizal endophyte and by mycorrhizal plants. New Phytologist 101, 459–467.[CrossRef][Web of Science]
Bending GD, Read DJ. 1995. The structure and function of the vegetative mycelium of ectomycorrhizal plants. V. The foraging behaviour of ectomycorrhizal mycelium and the translocation of nutrients from exploited organic matter. New Phytologist 130, 401–409.[CrossRef][Web of Science]
Bever JD, Schultz PA, Pringle A, Morton JB. 2001. Arbuscular mycorrhizal fungi: more diverse than meets the eye, and the ecological tale of why. Bioscience 51, 923–931.[CrossRef][Web of Science]
Bilbrough CJ, Caldwell MM. 1995. The effects of shading and N status on root proliferation in nutrient patches by the perennial grass Agropyron desertorum in the field. Oecologia 103, 10–16.[CrossRef][Web of Science]
Bouma TJ, Yanai RD, Elkin AD, Hartmond U, Flores-Alva DE, Eissenstat DM. 2001. Estimating age-dependent costs and benefits of roots with contrasting life span: comparing apples with oranges. New Phytologist 150, 685–695.[CrossRef][Web of Science]
Bradshaw AD. 1965. Evolutionary significance of phenotypic plasticity in plants. Advances in Genetics 13, 115–155.[CrossRef]
Caldwell MM, Manwaring JH, Durham SL. 1996. Species interactions at the level of fine roots in the field: influence of soil nutrient heterogeneity and plant size. Oecologia 106, 440–447.[CrossRef][Web of Science]
Campbell BD, Grime JP, Mackey JML. 1991. A trade-off between scale and precision in resource foraging. Oecologia 87, 532–538.[CrossRef][Web of Science]
Chalot M, Brun A. 1998. Physiology of organic acquisition by ectomycorrhizal fungi and ectomycorrhizas. FEMS Microbiology Reviews 22, 21–44.[CrossRef][Web of Science][Medline]
Charley JL, West NE. 1977. Micro-patterns of nitrogen mineralization activity of soils in some shrub-dominated semi-desert ecosystems of Utah. Soil Biology and Biochemistry 9, 357–365.[CrossRef]
Chiariello N, Hickman JC, Mooney HA. 1982. Endomycorrhizal role for interspecific transfer of phosphorus in a community of annual plants. Science 217, 941–943.
Cui M, Caldwell MM. 1997. Shading reduces exploitation of soil nitrate and phosphate by Agropyron desertorum and Artemisia tridentata from soils with patchy and uniform nutrient distributions. Oecologia 109, 177–183.[CrossRef][Web of Science]
Cui M, Caldwell MM. 1998. Nitrate and phosphate uptake by Agropyron desertorum and Artemisia tridentata from soil patches with balanced and unbalanced nitrate and phosphate supply. New Phytologist 139, 267–272.[CrossRef][Web of Science]
Dinkelaker B, Römheld V, Marschner H. 1989. Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.). Plant, Cell and Environment 12, 285–292.[CrossRef]
Dowson CG, Springham P, Rayner ADM, Boddy L. 1989. Resource relationships of foraging mycelial systems of Phanerochaete velutina and Hypholoma fasciculare in soil. New Phytologist 111, 501–509.[CrossRef][Web of Science]
Drew MC. 1975. Comparison of the effects of a localized supply of phosphate, nitrate, ammonium, and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytologist 75, 479–490.[CrossRef][Web of Science]
Drew MC, Saker LR. 1975. Nutrient supply and the growth of the seminal root system in barley. II. Localized, compensatory increases in lateral root growth and rates of nitrate uptake when nitrate supply is restricted to only part of the root system. Journal of Experimental Botany 26, 79–90.
Drew MC, Saker LR. 1978. Nutrient supply and the growth of the seminal root system in barley. III. Compensatory increases in growth of lateral roots, and in rates of phosphate uptake in response to a localized supply of phosphate. Journal of Experimental Botany 29, 435–451.
Drew MC, Saker LR, Ashley TW. 1973. Nutrient supply and the growth of the seminal root system in barley. I. The effect of nitrate concentration on the growth of axes and laterals. Journal of Experimental Botany 24, 1189–1202.
Duke SE, Caldwell MM. 2000. Phosphate uptake kinetics of Artemisia tridentata roots exposed to multiple soil enriched-nutrient patches. Flora 195, 154–164.[Web of Science]
Eom AH, Hartnett DC, Wilson GWT. 2000. Host plant species effects on arbuscular mycorrhizal fungal communities in tallgrass prairie. Oecologia 122, 435–444.[CrossRef][Web of Science]
Ettema CH, Wardle DA. 2002. Spatial soil ecology. Trends in Ecology and Evolution 17, 177–183.
Falik O, Reides P, Gersani M, Novoplansky A. 2003. Self/non-self discrimination in roots. Journal of Ecology 91, 525–531.[CrossRef]
Farley RA, Fitter AH. 1999a. Temporal and spatial variation in soil resources in a deciduous woodland. Journal of Ecology 87, 688–696.[CrossRef][Web of Science]
Farley RA, Fitter AH. 1999b. The response of seven co-occurring woodland herbaceous perennials to localized nutrient-rich patches. Journal of Ecology 87, 849–859.[CrossRef][Web of Science]
Fitter AH. 1987. An architectural approach to the comparative ecology of plant root systems. New Phytologist 106, Supplement, 61–77.[Web of Science]
Fitter AH. 1991. Costs and benefits of mycorrhizas: implications for functioning under natural conditions. Experientia 47, 350–355.[CrossRef][Web of Science]
Fitter AH. 1994. Architecture and biomass allocation as components of the plastic response of root systems to soil heterogeneity. In: Caldwell MM, Pearcy RW, eds. Exploitation of environmental heterogeneity by plants. San Diego, USA: Academic Press, 305–323.
Fitter AH, Graves JD, Wolfenden J, Self GK, Brown TK, Bogie D, Mansfield TA. 1997. Root production and turnover and carbon budgets of two contrasting grasslands under ambient and elevated atmospheric carbon dioxide concentrations. New Phytologist 137, 247–255.[CrossRef][Web of Science]
Fitter AH, Hodge A, Robinson D. 2000. Plant response to patchy soils. In: Hutchings MJ, John EA, Stewart AJA, eds. The ecological consequences of environmental heterogeneity. Oxford, UK: Blackwell Science Ltd, 71–90.
Fitter AH, Williamson L, Linkohr B, Leyser O. 2002. Root system architecture determines fitness in an Arabidopsis mutant in competition for immobile phosphate ions but not for nitrate ions. Proceedings of the Royal Society of London, Series B 269, 2017–2022.[Medline]
Fransen B, de Kroon H, Berendse F. 1998. Root morphological plasticity and nutrient acquisition of perennial grass species from habitats of different nutrient availability. Oecologia 115, 351–358.[CrossRef][Web of Science]
Gersani M, Sachs T. 1992. Developmental correlations between roots in heterogeneous environments. Plant, Cell and Environment 15, 463–469.[CrossRef]
Gross KL, Peters A, Pregitzer KS. 1993. Fine root growth and demographic responses to nutrient patches in four old-field plant species. Oecologia 95, 61–64.[Web of Science]
Gruntman M, Novoplansky A. 2004. Physiologically mediated self/non-self discrimination in roots. Proceedings of the National Academy of Sciences, USA 101, 3863–3867.
Halvorson JJ, Smith JL, Bolton Jr H, Rossi RE. 1995. Evaluating shrub-associated spatial patterns of soil properties in a shrub–steppe ecosystem using multiple-variable geostatistics. Soil Science Society of America Journal 59, 1476–1487.[Web of Science]
Helgason T, Merryweather JW, Denison J, Wilson P, Young JPW, Fitter AH. 2002. Selectivity and functional diversity in arbuscular mycorrhizas of co-occurring fungi and plants from a temperate deciduous woodland. Journal of Ecology 90, 371–384.[CrossRef]
Hendrick RL, Pregitzer KS. 1992. The demography of fine roots in a northern hardwood forest. Ecology 73, 1094–1104.[CrossRef][Web of Science]
Hendricks JJ, Nadelhoffer KJ, Aber JD. 1993. Assessing the role of fine roots in carbon and nutrient cycling. Trends in Ecology and Evolution 8, 174–178.[CrossRef]
Hodge A. 2001. Arbuscular mycorrhizal fungi influence decomposition of, but not plant nutrient capture from, glycine patches in soil. New Phytologist 151, 725–734.[CrossRef][Web of Science]
Hodge A. 2003. Plant nitrogen capture from organic matter as affected by spatial dispersion, interspecific competition and mycorrhizal colonization. New Phytologist 157, 303–314.[CrossRef][Web of Science]
Hodge A. 2004. The plastic plant: root reponses to heterogeneous supplies of nutrients. New Phytologist 162, 9–24.[CrossRef][Web of Science]
Hodge A, Alexander IJ, Gooday GW. 1995. Chitinolytic enzymes of pathogenic and ectomycorrhizal fungi. Mycological Research 99, 935–941.[CrossRef][Web of Science]
Hodge A, Campbell CD, Fitter AH. 2001. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413, 297–299.[CrossRef][Medline]
Hodge A, Robinson D, Fitter AH. 2000b. An arbuscular mycorrhizal inoculum enhances root proliferation in, but not nitrogen capture from, nutrient-rich patches in soil. New Phytologist 145, 575–584.[CrossRef][Web of Science]
Hodge A, Robinson D, Fitter AH. 2000e. Are microorganisms more effective than plants at competing for nitrogen? Trends in Plant Science 5, 304–308.[CrossRef][Web of Science][Medline]
Hodge A, Robinson D, Griffiths BS, Fitter AH. 1999a. Nitrogen capture by plants grown in N-rich organic patches of contrasting size and strength. Journal of Experimental Botany 50, 1243–1252.
Hodge A, Robinson D, Griffiths BS, Fitter AH. 1999c. Why plants bother: root proliferation results in increased nitrogen capture from an organic patch when two grasses compete. Plant, Cell and Environment 22, 811–820.[CrossRef]
Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH. 1998. Root proliferation, soil fauna and plant nitrogen capture from nutrient-rich patches in soil. New Phytologist 139, 479–494.[CrossRef][Web of Science]
Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH. 1999b. Plant, soil fauna and microbial responses to N-rich organic patches of contrasting temporal availability. Soil Biology and Biochemistry 31, 1517–1530.[CrossRef]
Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH. 2000c. Spatial and physical heterogeneity of N supply from soil does not influence N capture by two grass species. Functional Ecology 14, 645–653.[CrossRef][Web of Science]
Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH. 2000a. Competition between roots and soil micro-organisms for nutrients from nitrogen-rich patches of varying complexity. Journal of Ecology 88, 150–164.[CrossRef]
Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH. 2000d. Plant N capture and microfaunal dynamics from decomping grass and earthworm residues in soil. Soil Biology and Biochemistry 32, 1763–1772.[CrossRef]
Huang B, Eissenstat DM. 2000. Root plasticity in exploiting water and nutrient heterogeneity. In: Wilkinson RE, ed. Plant–environment interactions, 2nd edn. New York, USA: Marcel Dekker, Inc. 111–132.
Huante P, Rincón E, Chapin III FS. 1998. Foraging for nutrients, responses to changes in light, and competition in tropical deciduous tree seedlings. Oecologia 117, 209–216.[CrossRef][Web of Science]
Huber-Sannwald E, Pyke DA, Caldwell MM. 1996. Morphological plasticity following species–species recognition and competition in two perennial grasses. American Journal of Botany 83, 919–931.[CrossRef][Web of Science]
Huber-Sannwald E, Pyke DA, Caldwell MM. 1997. Perception of neighbouring plants by rhizomes and roots: morphological manifestations of a clonal plant. Canadian Journal of Botany 75, 2146–2157.[Web of Science]
Hutchings MJ, de Kroon H. 1994. Foraging in plants: the role of morphological plasticity in resource acquistion. Advances in Ecological Research 25, 159–238.[CrossRef][Web of Science]
Hutchings MJ, John EA, Wijesinghe DK. 2003. Toward understanding the consequences of soil heterogeneity for plant populations and communities. Ecology 84, 2322–2334.[CrossRef][Web of Science]
Ivans CY, Leffler AJ, Spaulding U, Stark JM, Ryel RJ, Caldwell MM. 2003. Root responses and nitrogen acquisition by Artemisia tridentata and Agropyron desertorum following small summer rainfall events. Oecologia 134, 317–324.[CrossRef][Web of Science][Medline]
Jackson RB, Caldwell MM. 1991. Kinetic responses of Pseudoroegneria roots to localized soil enrichment. Plant and Soil 138, 231–238.[CrossRef][Web of Science]
Jackson RB, Caldwell MM. 1992. Shading and the capture of localized soil nutrients: nutrient contents, carbohydrates, and root uptake kinetics of a perennial tussock grass. Oecologia 91, 457–462.[CrossRef][Web of Science]
Jackson RB, Caldwell MM. 1993a. Geostatistical patterns of soil heterogeneity around individual perennial plants. Journal of Ecology 81, 683–692.[CrossRef][Web of Science]
Jackson RB, Caldwell MM. 1993b. The scale of nutrient heterogeneity around individual plants and its quantification with geostatistics. Ecology 74, 612–614.[CrossRef][Web of Science]
Jackson RB, Manwaring JH, Caldwell MM. 1990. Rapid physiological adjustment of roots to localized soil enrichment. Nature 344, 58–60.[CrossRef][Medline]
Jakobsen I, Rosendahl L. 1990. Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytologist 115, 77–83.[CrossRef][Web of Science]
Jenny H. 1941. Factors of soil formation. New York, USA: McGraw-Hill.
Jones DL, Healey JR, Willett VB, Farrar JF, Hodge A. 2005. Dissolved organic nitrogen uptake by plants: an important N uptake pathway? Soil Biology and Biochemistry 37, 413–423.[CrossRef]
Kaye JP, Hart SC. 1997. Competition for nitrogen between plants and soil micro-organisms. Trends in Ecology and Evolution 12, 139–143.[CrossRef]
Kerley SJ, Read DJ. 1995. The biology of mycorrhiza in the Ericaceae. XVIII. Chitin degradation by Hymenoscyphus ericae and transfer of chitin-nitrogen to the host plant. New Phytologist 131, 369–375.[CrossRef][Web of Science]
Kerley SJ, Read DJ. 1997. The biology of mycorrhiza in the Ericaceae. XIX. Fungal mycelium as a nitrogen source for the ericoid mycorrhizal fungus Hymenoscyphus ericae and its host plants. New Phytologist 136, 691–701.[CrossRef][Web of Science]
King JS, Albaugh TJ, Allen HL, Buford M, Strain BR, Dougherty P. 2002. Below-ground carbon input to soil is controlled by nutrient availability and fine root dynamics in loblolly pine. New Phytologist 154, 389–398.[CrossRef][Web of Science]
Koch KE, Johnson CR. 1984. Photosynthate partitioning in split-root citrus seedlings with mycorrhizal and non-mycorrhizal root systems. Plant Physiology 75, 26–30.
Linkohr BI, Williamson LC, Fitter AH, Leyser HMO. 2002. Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. The Plant Journal 29, 751–760.[CrossRef][Web of Science][Medline]
Mosse B. 1959. Observations on the extramatrical mycelium of a vesicular–arbuscular endophyte. Transactions of the British Mycological Society 42, 439–448.
Mou P, Mitchell RJ, Jones RH. 1997. Root distribution of two tree species under a heterogeneous nutrient environment. Journal of Applied Ecology 34, 645–656.[CrossRef][Web of Science]
Newsham KK, Fitter AH, Watkinson AR. 1995. Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends in Ecology and Evolution 10, 407–411.[CrossRef]
Nicolson TH. 1959. Mycorrhiza in the Gramineae. I. Vesicular-arbuscular endophytes, with special reference to the external phase. Transactions of the British Mycological Society 42, 421–438.
O'Connor PJ, Smith SE, Smith FA. 2002. Arbuscular mycorrhizas influence plant diversity and community structure in a semiarid herbland. New Phytologist 154, 209–218.[CrossRef][Web of Science]
Ozinga WA, Van Andel J, McDonnell-Alexander MP. 1997. Nutritional soil heterogeneity and mycorrhiza as determinants of plant species diversity. Acta Botanica Neerlandica 46, 237–254.[Web of Science]
Paul EA, Kucey RMN. 1981. Carbon flow in plant microbial associations. Science 213, 473–474.
Pregitzer KS. 2002. Fine roots of trees: a new perspective. New Phytologist 154, 267–270.[CrossRef][Web of Science]
Pregitzer KS. 2003. Woody plants, carbon allocation and fine roots. New Phytologist 158, 421–424.[CrossRef][Web of Science]
Pregitzer KS, Hendrick RL, Fogel R. 1993. The demography of fine roots in response to patches of water and nitrogen. New Phytologist 125, 575–580.[CrossRef][Web of Science]
Pregitzer KS, Laskowski MJ, Burton AJ, Lessard VC, Zak DR. 1998. Variation in sugar maple root respiration with root diameter and soil depth. Tree Physiology 18, 665–670.
Pregitzer KS, Zak DR, Curtis PS, Kubiske ME, Teeri JA, Vogel CS. 1995. Atmospheric CO2, soil nitrogen and turnover of fine roots. New Phytologist 129, 579–585.[CrossRef][Web of Science]
Reich PB, Walters MB, Tjoelker MG, Vanderklein D, Buschena C. 1998. Photosythesis and respiration rates depend on leaf and root morphology and nitrogen concentration in nine boreal tree species differing in relative growth rate. Functional Ecology 12, 395–405.[CrossRef][Web of Science]
Reynolds JF, Virginia RA, Cornelius JM. 1990. Resource island formation associated with the desert shrubs, creosote bush (Larrea tridentate) and mesquite (Prosopis glandulosa) and its role in the stability of desert ecosystems: astimulation analysis. Supplement to Bulletin of the Ecological Society of America 70, 299–300.
Robinson D. 2001. Root proliferation, nitrate inflow and their carbon costs during nitrogen capture by competing plants in patchy soil. Plant and Soil 232, 41–50.[CrossRef][Web of Science]
Robinson D, Fitter A. 1999. The magnitude and control of carbon transfer between plants linked by a common mycorrhizal network. Journal of Experimental Botany 50, 9–13.
Robinson D, Hodge A, Griffiths BS, Fitter AH. 1999. Plant root proliferation in nitrogen-rich patches confers competitive advantage. Proceedings of the Royal Society of London, Series B 265, 431–435.
Robinson D, van Vuuren MMI. 1998. Responses of wild plants to nutrient patches in relation to growth rate and life-form. In: Lambers H, Poorter H, van Vuuren MMI, eds. Variation in plant growth. The Netherlands: Backhuys, 237–257.
Rønn R, Griffiths BS, Ekelund F, Christensen S. 1996. Spatial distributions and sucessional pattern of microbial activity and micro-faunal populations on decomposing barley roots. Journal of Applied Ecology 33, 662–672.[CrossRef][Web of Science]
Ritz K, Millar SM, Crawford JW. 1996. Detailed visualization of hyphal distribution in fungal mycelia growing in heterogeneous nutritional environments. Journal of Microbiological Methods 25, 23–28.
Rygiewicz PT, Andersen CP. 1994. Mycorrhizae alter quality and quantity of carbon allocated below ground. Nature 369, 58–60.[CrossRef]
Schenk HJ, Callaway RM, Mahall BE. 1999. Spatial root segregation: are plants territorial? Advances in Ecological Research 28, 145–180.[CrossRef]
Simard SW, Perry DA, Jones MD, Myrold DD, Durall DM, Molina R. 1997. Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388, 579–582.[CrossRef]
Smith SE, Read DJ. 1997. Mycorrhizal symbiosis. London, UK: Academic Press Ltd.
Snellgrove RC, Splittstoesser WE, Stribly DP, Tinker PB. 1982. The distribution of carbon and the demand of the fungal symbiont in leek plants with vesicular–arbuscular mycorrhizas. New Phytologist 92, 75–87.[CrossRef][Web of Science]
Stark JM. 1994. Causes of soil nutrient heterogeneity at different scales. In: Caldwell MM, Pearcy RW, eds. Exploitation of environmental heterogeneity by plants. San Diego, USA: Academic Press, 255–284.
Stevenson FJ. 1982. Nitrogen in agricultural soils. Madison WI: Soil Science Society of America Inc., Crop Science Society of America Inc., American Society of Agronomy Inc.
St John TV, Coleman DC, Reid CPP. 1983a. Association of vesicular–arbuscular mycorrhizal hyphae with soil organic particles. Ecology 64, 957–959.[CrossRef][Web of Science]
St John TV, Coleman DC, Reid CPP. 1983b. Growth and spatial distribution of nutrient-absorbing organs: selective exploitation of soil heterogeneity. Plant and Soil 71, 487–493.[CrossRef][Web of Science]
Tinker PB, Nye PH. 2000. Solute movement in the rhizosphere. Oxford, UK: Oxford University Press.
Tjoelker MG, Craine JM, Wedin D, Reich PB, Tilman D. 2005. Linking leaf and root trait syndromes among 39 grassland and savannah species. New Phytologist 167, 915–919.[CrossRef]
Vandenkoornhuyse P, Husband R, Daniell TJ, Watson IJ, Duck JM, Fitter AH, Young JPW. 2002. Arbuscular mycorrhizal community composition associated with two plant species in a grassland ecosystem. Molecular Ecology 11, 1555–1564.[CrossRef][Medline]
van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 69–72.[CrossRef]
van der Heijden MGA, Wiemken A, Sanders IR. 2003. Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plants. New Phytologist 157, 569–578.[CrossRef][Web of Science]
van Vuuren MMI, Robinson D, Griffiths BS. 1996. Nutrient inflow and root proliferation during the exploitation of a temporally and spatially discrete source of nitrogen in soil. Plant and Soil 178, 185–192.[CrossRef][Web of Science]
Vinton MA, Burke IC. 1995. Interactions between individual plant species and soil nutrient status in shortgrass steppe. Ecology 76, 1116–1133.[CrossRef][Web of Science]
Volder A, Smart DR, Bloom AJ, Eissenstat DM. 2005. Rapid decline in nitrate uptake and respiration with age in fine lateral roots of grape: implications for root efficiency and competitive effectiveness. New Phytologist 165, 493–502.[CrossRef][Web of Science][Medline]
Wijesinghe DK, John EA, Beurskens S, Hutchings MJ. 2001. Root system size and precision in nutrient foraging: responses to spatial pattern of nutrient supply in six herbaceous species. Journal of Ecology 89, 972–983.[CrossRef]
Zobel R. 2003. Fine roots: discarding flawed assumptions. New Phytologist 160, 276–279.[CrossRef][Web of Science]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  J. Zhang and E. George Root proliferation of Norway spruce and Scots pine in response to local magnesium supply in soil Tree Physiol, February 1, 2009; 29(2): 199 - 206. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. E. Drenovsky, C. E. Martin, M. R. Falasco, and J. J. James Variation in resource acquisition and utilization traits between native and invasive perennial forbs Am. J. Botany, June 1, 2008; 95(6): 681 - 687. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Vincent and D. Harja Exploring Ecological Significance of Tree Crown Plasticity through Three-dimensional Modelling Ann. Bot., May 1, 2008; 101(8): 1221 - 1231. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. D. Finlay Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium J. Exp. Bot., March 1, 2008; 59(5): 1115 - 1126. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Lucas, C. Godin, C. Jay-Allemand, and L. Laplaze Auxin fluxes in the root apex co-regulate gravitropism and lateral root initiation J. Exp. Bot., January 1, 2008; 59(1): 55 - 66. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Pierret, C. Doussan, Y. Capowiez, F. Bastardie, and L. Pages Root Functional Architecture: A Framework for Modeling the Interplay between Roots and Soil Vadose Zone J., May 17, 2007; 6(2): 269 - 281. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. KUME, N. SEKIYA, and K. YANO Heterogeneity in Spatial P-distribution and Foraging Capability by Zea mays: Effects of Patch Size and Barriers to Restrict Root Proliferation within a Patch Ann. Bot., December 1, 2006; 98(6): 1271 - 1277. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||