MiniReview
Microbial ecology of the arbuscular mycorrhiza
Angela Hodge *
Department of Biology, The University of York, P.O. Box 373, York YO10 5YW, UK
Received 14 January 2000 ; received in revised form 13 March 2000 ; accepted 14 March 2000
Abstract
Arbuscular mycorrhizal (AM) fungi interact with a wide variety of organisms during all stages of their life. Some of these interactions such as grazing of the external mycelium are detrimental, while others including interactions with plant growth promoting rhizobacteria (PG PR) promote mycorrhizal functioning. Following mycorrhizal colonisation the functions of the root become modified, with consequences for the rhizosphere community which is extended into the mycorrhizosphere due to the presence of the AM external mycelium. However, we still know relatively little of the ecology of AM fungi and, in particular, the mycelium network under natural conditions. This area merits attention in the future with emphasis on the fungal partner in the association rather than the plant which has been the focus in the past. ß 2000 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved.
Keywords : Arbuscular mycorrhiza ; Fungal mycelium network ; Soil microbial ecology ; Interaction ; Rhizosphere and mycorrhizosphere
1. Introduction
Mycorrhizal associations between a fungus and a plant root are ubiquitous in the natural environment. The asso-ciations themselves can be further classi¢ed into one of seven di¡erent types (i.e. arbuscular, ectomycorrhiza, ec-tendomycorrhiza, ericoid, arbutoid, orchid and monotro-poid) based on the type of fungus involved and the range of resulting structures produced by the root^fungus com-bination (see [1]). Common to all types of mycorrhizal association, however, is the movement of carbon, gener-ally, but not always, in the direction from plant to fungus. The association may not be obviously mutualistic at all points in time and this together with the range of func-tions thus far identi¢ed for the association (i.e. defence, nutrient uptake, soil aggregation stability, drought resis-tance) has posed problems in producing a clear de¢nition to best describe the association. Currently, the most useful de¢nition is perhaps that of ``a sustainable non-pathogenic biotrophic interaction between a fungus and a root'' as proposed by Fitter and Moyersoen [2], although this does not emphasise the importance of the presence of both intra- and extraradical mycelia in the association.
By far the most common type of association is that of the arbuscular mycorrhiza (AM). The AM association is
the most ancient and probably aided the ¢rst land plants to colonise by scavenging for phosphate [3]. The AM as-sociation is so called because of the formation of highly branched intracellular fungal structures or `arbuscules' which are believed to be the site of phosphate exchange between fungus and plant. Vesicles which contain lipids and are thought to be carbon storage structures may also form in some cases, although this will depend on the fungal symbiont as well as environmental conditions [1].
Approximately two-thirds of all land plants form the AM type of association, in sharp contrast with the rela-tively small numbers of fungi involved, all of which are members of the order Glomales (Zygomycotina) compris-ing only approximately 150 described taxa [1]. Conse-quently, the AM association is generally assumed to have no, or at least very low, speci¢city. More recently however, van der Heijden et al. [4] demonstrated that the biomass of several plant species in microcosms con-taining four native AM fungal taxa was approximately equal to biomass production in treatments that included the single fungal taxa that induced the largest growth re-sponse. This indicated that plants may be able to at least select the AM fungus which may bene¢t them the most. However, the bulk of knowledge of the AM symbiosis derives from microcosm experiments using a small number of plant and fungal taxa, and with little or no attention paid to the other soil biota with which they must interact. The purpose of this review is to focus on the ecology of
0168-6496 / 00 / $20.00 ß 2000 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved. PII : S 0 1 6 8 - 6 4 9 6 ( 0 0 ) 0 0 0 2 3 - 4
* Tel. : +44 (1904) 432878; Fax : +44 (1904) 432860 ; E-mail : ah29@york.ac.uk
the AM association in terms of interactions with other organisms and the implications of these interactions for mycorrhizal development and functioning.
2. Interactions in the mycorrhizosphere
2.1. Soil microbial interactions on AM fungi
Soil micro-organisms in£uence AM fungal development and symbiosis establishment but no clear pattern of re-sponse has been found : positive [5^7], negative [8,9] and neutral [10] interactions have all been reported. Negative impacts upon the AM fungi include a reduction in spore germination and hyphal length in the extramatrical stage, decreased root colonisation and a decline in the metabolic activity of the internal mycelium. Which e¡ect is the more predominant has been found to be in£uenced by the tim-ing of addition of the micro-organisms, the type of AM fungus present and the plant species which the AM fungus has colonised [9,11,12]. These factors together with the complex and dynamic nature of the soil environment mean that it is di¤cult to draw any useful generalisations. Indeed, even the same genus has been shown to have ei-ther a bene¢cial, negative or neutral e¡ect upon AM fungi, as has been reported for bothTrichodermaand Pseudomo-nasspp. [5,8,10,12^14]. Recent advances in both biochem-ical and molecular techniques should provide more useful insights into the nature of the interactions between AM fungi and other soil micro-organisms. For example, although the presence ofTrichoderma harzianumdecreased root colonisation and, when an organic nutrient source was added, external hyphal density of the AM fungus Glomus intraradices, the living AM mycelial biomass (measured as the content of a membrane fatty acid, PFLA16 :1g5) did not decrease nor did AM hyphal trans-port of33P [15].
Positive in£uences on the AM symbiosis after addition of plant growth promoting rhizobacteria (PGPR), which include £uorescent pseudomonads and sporulating bacilli, are frequently reported. For example, dual inoculation of a PGPR (Pseudomonas putida) and an AM fungus induced an additive growth enhancement of subterranean clover when added together rather than singly [5]. Inoculation with the PGPR also increased root colonisation by the AM fungus initially (i.e. measured at 6 weeks) although later (at 12 weeks) colonisation levels were similar regard-less of the presence of the PGPR [5]. Enhanced mycelial growth fromGlomus mosseaespores by a PGPR has also been reported [16]. Thus, PGPR appear sometimes to pro-mote both mycorrhizal development and functioning. In addition, the mycorrhizal and nodulated (i.e.Frankia, Rhi-zobiumand Bradyrhizobium) symbioses are generally syn-ergistic. It is believed that the AM symbiosis relieves P stress for the plant which in turn has bene¢ts for the N2-¢xing nitrogenase system of the other symbiont,
result-ing in enhanced ¢xation levels and consequently improved N status of the plant thus promoting plant growth and functioning which in turn also bene¢ts mycorrhizal devel-opment (reviewed for legumes by [17] ; see [18] for Frank-ia).
2.2. AM in£uences on soil microbial interactions
Once mycorrhizal colonisation has occurred, subsequent exudation release by the root may be modi¢ed both through the mycorrhizal fungus acting as a considerable carbon sink for photoassimilate and through hyphal exu-dation. This may be expected to lead to changes in both the qualitative and quantitative release of exudates into the mycorrhizosphere. AM colonisation generally de-creases root exudation [19] although not always [20] and may be in£uenced by the species of fungus present [21]. In addition, a reduction in sugar and amino acid release has been reported in some studies [19,22] but there is no clear pattern as to the consistency of this phenomenon. Simi-larly the reported impact on the mycorrhizosphere com-munity is equally inconsistent with, for example, £uores-cent pseudomonads showing a decrease, increase or no e¡ect following AM colonisation [10,21,23,24]. Meyer and Linderman [25] observed no alteration in the total number of bacteria or actinomycetes isolated from the rhizosphere of Zea mays and Trifolium subterranean L. colonised by the AM fungus Glomus fasciculatum. How-ever, there was a change in the functional groups of these organisms including more facultative anaerobic bacteria in the rhizosphere of AM colonisedT. subterraneumbut few-er £uorescent pseudomonads and chitinase-producing ac-tinomycetes in the rhizosphere of AM-colonised Z. mays. The total number of bacteria isolated from the rhizoplane of bothT. subterraneumandZ. maysincreased as a result of AM colonisation although total numbers of actinomy-cetes were una¡ected. In addition, leachates fromZ. mays rhizosphere soil reduced production of zoospores and sporangia byPhytophthora cinnamomi when colonised by G. fasciculatumthan non-mycorrhizalZ. maysrhizosphere leachates indicating a potential mechanism by which AM colonisation may aid pathogen resistance [25]. However, the chitinolytic producing actinomycete population may act as general biocontrol agents, thus, the reduction in this population may mean chitin containing pathogens be-come more important. Using three di¡erent AM fungi (Glomus etunicatum, Glomus mosseae or Gigaspora rosea) Schreiner et al. [26] observed di¡erences in bacterial groups (i.e. Gram-negative or Gram-positive) depending on which fungus had colonised the roots of Glycine max L. (soybean). The AM fungus G. mosseae produced the greatest amount of external hyphae (i.e. 8.1 m g31 soil).
of dry soil, than corresponding samples fromG. rosea. Soil from G. etunicatum pots also contained higher counts of Gram-negative bacteria than those counted from G. mos-seae. These results would seem to imply that the hypho-sphere (the volume of soil in£uenced by the external my-celium of the AM fungus) of di¡erent AM fungi may in£uence certain bacterial groups however, it should also be noted that where external mycelium production was greatest (i.e. in the case of G. mosseae) the in£uence on overall counts was less than from G. etunicatum which produced a less extensive mycelium. Indeed, low P status of the soil had a greater e¡ect on total bacterial, and in particular Gram-positive, counts, than did mycorrhizal treatments. Alternatively, the more extensive mycelium could have inhibited bacterial populations as a means of reducing competition for nutrients in the mycorrhizo-sphere [15,24]. Other studies speci¢cally testing the hypho-sphere soil have found no quantitative change in bacterial numbers [27,28]. However, whereas Andrade et al. [27] found variations in bacterial composition which depended on the AM fungus present, Olsson et al. [28] found no such changes in composition or activities of the bacterial community.
Filion et al. [29] examined the release of soluble uniden-ti¢ed substances by the external mycelium ofGlomus intra-radiceson the conidial germination of two fungi and the growth of two bacteria. Conidial germination of Tricho-derma harzianumand growth ofPseudomonas chlororaphis were stimulated whereas growth of Clavibacter michiga-nensis subsp. michiganensis was una¡ected and conidial germination of Fusarium oxysporum f.sp. chrysanthemi was reduced. These observed e¡ects were generally corre-lated with the extract concentration. The authors [29] sug-gested that this was a possible means by which the AM mycelium may alter the microbial environment so that it was detrimental to pathogens. In contrast, Green et al. [15] also examining the interaction betweenG. intraradicesand T. harzianum, observed no e¡ect of the AM external my-celium on the population density of T. harzianum, except in the presence of an organic substrate when population densities and metabolic activity of T. harzianum were ac-tually reduced. The di¡ering results reported on the in£u-ence of AM fungi upon soil micro-organisms therefore are probably not only due to the type of AM fungus present but also the conditions, such as soil nutrient availability, in which the interaction is studied.
2.3. Grazing of AM fungi
AM spores and external mycelium are subject to grazing by larger soil organisms such as collembola (or spring-tails), earthworms and mammals as well as other fungi and actinomycetes (see [30]). For example, although not their preferred food source [31], collembola can graze on the spores and extraradical mycelium of AM hyphae as shown by examination of their gut contents [32,33].
How-ever, the feeding of the collembolaFolsomia candidaon an exclusive diet of the AM fungi Acaulospora spinosa, Scu-tellospora calospora and Gigaspora gigantea actually re-duced the reproductive capacity of this collembola. In contrast, two other AM fungi (G. intraradicesandG. etu-nicatum) although less palatable thanT. harzianumwere as pro¢table in terms of reproductive success [34]. Thus, although active grazing of AM fungal hyphae may not be an important feature under ¢eld conditions, collembola may reduce the e¡ectiveness of the mycorrhizal symbiosis in other ways. For example, although the collembola F. candida did not actively graze on hyphae of the AM fungusG. intraradices, they did bite and sever the external AM hyphae from the root before grazing on their pre-ferred food source (conidial fungal hyphae) present at the same time. This severing of AM hyphal networks was as much as 50% at the highest populations of collem-bola studied [35]. Although under some circumstances grazing by soil organisms such as earthworms, collembola and other organisms will be bene¢cial (e.g. as spores can survive ingestion thus grazing and deposition elsewhere will aid in dispersal) the grazing or cleavage of external hyphae may have more important consequences on the e¡ectiveness of the mycorrhizal symbiosis [33]. The inter-nal colonisation will remain intact and thus represent a carbon drain on the plant, but with reduced bene¢ts due to a reduction in the external hyphal length. Re-establish-ment of the external mycelium will again require more plant carbon to be invested.
3. From microcosm to ¢eld
network (CMN). This CMN probably becomes the pri-mary source of inoculum by which plants become colon-ised. However, we know relatively little of the ecology of this network such as the distances to which it can extend, how many plants may be linked, the di¡ering ability of AM fungal taxa to produce such networks and their in-teraction with each other let alone the inin-teractions with the other soil biota. Some data are available, for example the spread of hyphae ofG. fasciculatumthrough unplanted soil has been estimated to occur at a rate of 1.66 mm day31 [37] but again such estimates generally come from
microcosm studies. In a ¢eld study, Chiariello et al. [38] applied32P to the leaves of a donorPlantago erectaplant present in a serpentine annual grassland and detected high levels (i.e. s40% above background counts per min) in the shoots of neighbouring plants at a distance of ca 45 mm after 6^7 days. However, neither the type or size of the neighbouring plants nor the distance between donor and receiver were indicators of the amount of 32P trans-ferred. Thus, there is an urgent need to investigate the ecology of the symbiosis under a range of ¢eld conditions in order to more fully understand the context dependence of the data obtained in relation to mycorrhizal functioning and the nature of the interactions with other soil biota.
For the plant, being linked into the CMN may help to reduce the uncertainty of soil heterogeneity with the fungal mycelium being able to locate, access and exploit the nu-trient-rich zones or patches which occur naturally in all soils due to organic matter inputs (see [39]) more e¡ec-tively than plant roots. It is well established that when roots of some plant species encounter such organic patches they proliferate roots within them [39]. This proliferation is believed to be a foraging response to the heterogeneous nature of the environment. AM fungi can also proliferate hyphae within nutrient-rich organic patches [40,41]. Al-lowing fungal hyphal proliferation instead would be more carbon cost e¤cient for the plant (see [42]). Further-more, because of their size, AM fungal hyphae should be better able to compete with the indigenous soil biota for the microbially released nutrients. The AM fungi may also be able to access organic sources directly (i.e. without the prior need for microbial mineralisation) as has been dem-onstrated for nitrogen under both ¢eld [43] and laboratory conditions [44]. The importance and ubiquity of this up-take of intact organic compounds by AM fungi remains controversial (see [1]) and may depend on the competitive ability of AM fungi in comparison with the other soil biota present. However, the distances over which nutrients can e¡ectively be transported among plants via the net-work may be small (see review by [45]). The reason why we know so little about the CMN is partially the di¤cul-ties associated with studying it particularly under ¢eld conditions. Furthermore, in the past most emphasis in mycorrhizal research has been placed upon the plant rather than the fungus or indeed the symbiotic state. This is particularly true in the AM association probably
due to the essential role the plant plays in ensuring con-tinued growth and functioning of the fungus. However, the fungus should not be out of mind. From the fungal viewpoint, the linking of plants by this CMN makes stra-tegic sense. It allows fungal spread through the soil and maximises carbon capture by active colonisation of roots it encounters ensuring continued growth and activity. Fu-ture research emphasis needs to be placed on the fungal symbiont in the association adopting a more mycocentric approach as suggested by Fitter et al. [46].
Recent development of new techniques such as the sta-ble-isotope probing method [47] and £uorescent in situ hybridization combined with microautoradiography [48] and tracking of labelled substrate uptake [49] now make it possible to directly follow the active populations of bac-teria (rather than just culturable organisms) in soil. In addition, analysis of appropriately selected phospholipid fatty acid (PLFA) pro¢les can indicate the amount of fungal and bacterial biomass present and, when coupled with radio- or stable-isotope analysis, can indicate alter-ations in the activity of this biomass (see [15]). PLFA techniques have recently been used to investigate the in-teraction between AM fungi and other soil micro-organ-isms and have shown considerable promise [15,29]. These new methods in soil microbial ecology together with ad-vances in molecular techniques to identify AM fungi both in colonised roots and the external phase mean that fol-lowing AM fungal ecology and their interaction with the soil biota is now possible. Indeed, molecular methodolo-gies have already shown that spore diversity found in the vicinity of the root is not readily translated into diversity found in the actual colonised root [50]. The combined application of these new techniques in the future should enable valuable insights into the ecological role of inter-acting groups of soil micro-organisms and AM fungi and their subsequent impact upon carbon dynamics and nu-trient translocation under a range of di¡ering soil, and ultimately ¢eld, conditions.
Acknowledgements
I am very grateful to Alastair Fitter for detailed com-ments and suggestions on earlier drafts. A.H. is funded by a BBSRC David Phillips Fellowship.
References
[1] Smith, S.E. and Read, D.J. (1997) Mycorrhizal Symbiosis. Academic Press, London.
[2] Fitter, A.H. and Moyersoen, B. (1996) Evolutionary trends in root-microbes symbioses. Phil. Trans. R. Soc. Lond. B 351, 1367^1375. [3] Simon, L., Bousquet, J., Levesque, R.C. and Lalonde, M. (1993)
Origin and diversi¢cation of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363, 67^69.
P., Streitwolf-Engel, P., Boller, T., Wiemken, A. and Sanders, I.R. (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 69^72. [5] Meyer, J.R. and Linderman, R.G. (1986) Response of subterranean
clover to dual-inoculation with vesicular-arbuscular mycorrhizal fun-gi and a plant growth-promoting bacterium, Pseudomonas putida. Soil Biol. Biochem. 18, 185^190.
[6] Bagyaraj, D.J. and Menge, J.A. (1978) Interactions with VA mycor-rhiza andAzotobacterand their e¡ects on rhizosphere micro£ora and plant growth. New Phytol. 80, 567^573.
[7] Gryndler, M., Hrselova¨, H. and Chva¨talova¨, I. (1996) E¡ect of free-soil-inhabiting or root-associated microfungi on the development of arbuscular mycorrhizae and on proliferation of intraradical mycor-rhizae hyphae. Folia Microbiol. 41, 193^196.
[8] Wyss, P., Boller, T.H. and Wiemken, A. (1992) Testing the e¡ect of biological control agents on the formation of vesicular arbuscular mycorrhiza. Plant Soil 147, 159^162.
[9] McAllister, C.B., Garc|¨a-Romera, I., Martin, J., Godeas, A. and Ocampo, J.A. (1995) Interaction betweenAspergillus nigervan Tiegh. and Glomus mosseae (Nicol. and Gerd.) Gerd. and Trappe. New Phytol. 129, 309^316.
[10] Edwards, S.G., Young, J.P.W. and Fitter, A.H. (1998) Interactions betweenPseudomonas £uorescensbiocontrol agents andGlomus mos-seae, an arbuscular mycorrhizal fungus, within the rhizosphere. FEMS Microbiol. Lett. 166, 297^303.
[11] Tylka, G.L., Hussey, R.S. and Roncadori, R.W. (1991) Axenic ger-mination of vesicular-arbuscular mycorrhizal fungi - e¡ects of se-lectedStreptomycetesspecies. Phytopathology 81, 754^759. [12] McAllister, C.B., Garc|¨a-Romera, I., Godeas, A. and Ocampo, J.A.
(1994) Interactions between Trichoderma koningii, Fusarium solani andGlomus mosseae: e¡ects on plant growth, arbuscular mycorrhizas and the saprophyte inoculants. Soil Biol. Biochem. 26, 1363^1367. [13] Calvet, C., Barea, J.M. and Pera, J. (1992) In vitro interactions
be-tween the vesicular-arbuscular mycorrhizal fungus Glomus mosseae and some saprophytic fungi isolated from organic substrates. Soil Biol. Biochem. 24, 775^780.
[14] Dhillion, S.S. (1992) Dual inoculation of pretransplant stageOryyza sativaL. plants with indigenous vesicular-arbuscular mycorrhizal fun-gi and £uorescentPseudomonasspp. Biol. Fertil. Soils 13, 147^151. [15] Green, H., Larsen, J., Olsson, P.A., Jensen, D.F. and Jakobsen, I.
(1999) Suppression of the biocontrol agentTrichoderma harzianumby mycelium of the arbuscular mycorrhizal fungusGlomus intraradices in root-free soil. Appl. Environ. Microbiol. 65, 1428^1434. [16] Azcon, R. (1987) Germination and hyphal growth ofGlomus mosseae
in vitro: e¡ects of rhizosphere bacteria and cell-free culture media. Soil Biol. Biochem. 19, 417^419.
[17] Bethlenfalvay, G.J. (1992) Vesicular-arbuscular mycorrhizal fungi in nitrogen-¢xing legumes : problems and prospects. Methods Micro-biol. 24, 375^389.
[18] Fraga-Beddiar, A. and Le Tacon, F. (1990) Interactions between VA mycorrhizal fungi andFrankiaassociated with alder (Alnus glutinosa). Symbiosis 9, 247^258.
[19] Graham, J.H., Leonard, R.T. and Menge, J.A. (1981) Membrane mediated decrease in root exudation responsible for phosphorus in-hibition of vesicular-arbuscular mycorrhiza formation. Plant Physiol. 68, 548^552.
[20] Azaizeh, H.A., Marschner, H., Ro«mheld, V. and Wittenmayer, L. (1995) E¡ects of a vesicular-arbuscular mycorrhizal fungus and other soil microorganisms on growth, mineral nutrient acquisition and root exudation of soil-grown maize plants. Mycorrhiza 5, 321^327. [21] Marschner, P., Crowley, D.E. and Higashi, R.M. (1997) Root
exu-dation and physiological status of a root-colonizing £uorescent pseu-domonad in mycorrhizal and non-mycorrhizal pepper (Capsicum annuumL.). Plant Soil 189, 11^20.
[22] Dixon, R.K., Garrett, H.E. and Cox, G.S. (1989) Boron fertilization, vesicular-arbuscular mycorrhizal colonisation and growth of Citrus jambhiriLush. J. Plant Nutr. 12, 687^700.
[23] Klyuchnikov, A.A. and Kozhevin, P.A. (1990) Dynamics of Pseudo-monas £uorescensandAzospirillum brasilensepopulations during the formation of the vesicular-arbuscular mycorrhiza. Microbiology 59, 449^452.
[24] Ames, R.N., Reid, C.P.P. and Ingham, E.R. (1984) Rhizosphere bac-terial population responses to root colonization by a vesicular-arbus-cular mycorrhizal fungus. New Phytol. 96, 555^563.
[25] Meyer, J.R. and Linderman, R.G. (1986) Selective in£uence on pop-ulations of rhizosphere or rhizoplane bacteria and actinomycetes by mycorrhizas formed byGlomus fasciculatum. Soil Biol. Biochem. 18, 191^196.
[26] Schreiner, R.P., Mihara, K.L., McDaniel, H. and Bethlenfalvay, G.J. (1997) Mycorrhizal fungi in£uence plant and soil functions and in-teractions. Plant Soil 188, 199^209.
[27] Andrade, G., Mihara, K.L., Linderman, R.G. and Bethlenfalvay, G.J. (1997) Bacteria from rhizosphere and hyphosphere soils of dif-ferent arbuscular-mycorrhizal fungi. Plant Soil 192, 71^79. [28] Olsson, P.A., Ba®a®th, E., Jakobsen, I. and So«derstro«m, B. (1996) Soil
bacteria respond to presence of roots but not to mycelium of arbus-cular mycorrhizal fungi. Soil Biol. Biochem. 28, 463^470.
[29] Filion, M., St-Arnaud, M. and Fortin, J.A. (1999) Direct interaction between the arbuscular mycorrhizal fungusGlomus intraradicesand di¡erent rhizosphere micro-organisms. New Phytol. 141, 525^533. [30] Fitter, A.H. and Sanders, I.R. (1992) Interactions with the soil fauna.
In : Mycorrhizal Functioning (Allen, M.F., Ed.), pp. 333^354. Chap-man and Hall, New York.
[31] Klironomos, J.N. and Kendrick, W.B. (1996) Palatability of micro-fungi to soil arthropods in relation to the functioning of arbuscular mycorrhizae. Biol. Fertil. Soils 21, 43^52.
[32] McGonigle, T.P. and Fitter, A.H. (1988) Ecological consequences of arthropod grazing on VA mycorrhizal fungi. Proc. Soc. Edinb. 94B, 25^32.
[33] Warnock, A.J., Fitter, A.H. and Usher, M.B. (1982) The in£uence of a springtailFolsomia candida(insecta, collembola) on the mycorrhizal association of leekAllium porrumand the vesicular-arbuscular my-corrhizal endophyte Glomus fasciculatus. New Phytol. 90, 285^ 292.
[34] Klironomos, J.N., Bednarczuk, E.M. and Neville, J. (1999) Repro-ductive signi¢cance of feeding on saprobic and arbuscular mycorrhi-zal fungi by the collembolan,Folsomia candida. Funct. Ecol. 13, 756^ 761.
[35] Klironomos, J.N. and Ursic, M. (1998) Density-dependent grazing on the extraradical hyphal network of the arbuscular mycorrhizal fun-gus,Glomus intraradices, by the collembolan,Folsomia candida. Biol. Fertil. Soils 26, 250^253.
[36] Helgason, T., Daniell, T.J., Husband, R., Fitter, A.H. and Young, J.P.W. (1998) Ploughing up the wood-wide web ? Nature 394, 431. [37] Harinikumar, K.M. and Bagyaraj, D.J. (1995) Spread of
vesicular-arbuscular mycorrhizal fungal hyphae in soil. Microbiol. Res. 150, 77^80.
[38] Chiariello, N., Hickman, J.C. and Mooney, H.A. (1982) Endomycor-rhizal role for interspeci¢c transfer of phosphorus in a community of annual plants. Science 217, 941^943.
[39] Fitter, A.H. (1994) Architecture and biomass allocation as compo-nents of the plastic response of root systems to soil heterogeneity. In: Exploitation of Environmental Heterogeneity by Plants (Caldwell, M.M. and Pearcy, R.W., Eds.), pp. 305^323. Academic Press, New York.
[40] St. John, T.V., Coleman, D.C. and Reid, C.P.P. (1983) Association of vesicular-arbuscular mycorrhizal (VAM) fungi with soil organic matter. Ecology 64, 957^959.
[41] Ravnskov, S., Larsen, J., Olsson, P.A. and Jakobsen, I. (1999) E¡ects of various organic compounds on growth and phosphorus uptake of an arbuscular mycorrhizal fungus. New Phytol. 141, 517^524. [42] Fitter, A.H. (1991) Costs and bene¢ts of mycorrhizas : implications
arbuscular mycorrhizal fungusGlomus fasciculatumon the uptake of amino nitrogen byLolium perenne. New Phytol. 137, 345^349. [44] Na«sholm, T., Ekblad, A., Nordin, A., Giesler, R., Ho«gberg, M. and
Ho«gberg, P. (1998) Boreal forest plants take up organic nitrogen. Nature 392, 914^916.
[45] Newman, E.I. (1988) Mycorrhizal links between plants : their func-tioning and ecological signi¢cance. Adv. Ecol. Res. 18, 243^270. [46] Fitter, A.H., Graves, J.D., Watkins, N.K., Robinson, D. and
Scrim-geour, C. (1998) Carbon transfer between plants and its control in networks of arbuscular mycorrhizas. Funct. Ecol. 12, 406^412. [47] Radajewski, S., Ineson, P., Parekh, N.R. and Murrell, J.C. (2000)
Stable-isotope probing as a tool in microbial ecology. Nature 403, 646^649.
[48] Lee, N., Nielsen, P.H., Andreasen, K.H., Juretschko, S., Nielsen, J.L., Schleifer, K.H. and Wagner, M. (1999) Combined microauto-radiography ^ a new tool for structure-function analysis in microbial ecology. Appl. Environ. Microbiol. 65, 1289^1297.
[49] Ouverney, C.C. and Fuhrman, J.A. (1999) Combined microautora-diography-16S rRNA probe technique for determination of radioiso-tope uptake by speci¢c microbial cell types in situ. Appl. Environ. Microbiol. 65, 1746^1752.
