REGULAR ARTICLE

Plant performance in stressful environments: interpretingnew and established knowledge of the rolesof arbuscular mycorrhizas

Sally E. Smith & Evelina Facelli & Suzanne Pope &

F. Andrew Smith

Received: 19 January 2009 /Accepted: 24 March 2009 /Published online: 19 May 2009# Springer Science + Business Media B.V. 2009

Abstract Arbuscular mycorrhizal (AM) symbiosesare formed by approximately 80% of vascular plantspecies in all major terrestrial biomes. In consequencean understanding of their functions is critical in anystudy of sustainable agricultural or natural ecosys-tems. Here we discuss the implications of recentresults and ideas on AM symbioses that are likely tobe of particular significance for plants dealing withabiotic stresses such as nutrient deficiency andespecially water stress. In order to ensure balancedcoverage, we also include brief consideration of theways in which AM fungi may influence soil structure,carbon deposition in soil and interactions with the soilmicrobial and animal populations, as well as plant-plant competition. These interlinked outcomes ofAM symbioses go well beyond effects in increasingnutrient uptake that are commonly discussed and allrequire to be taken into consideration in future workdesigned to understand the complex and multifaceted

responses of plants to abiotic and biotic stresses inagricultural and natural environments.

Keywords Arbuscular mycorrhizas . Nutrient uptake .

Water relations . Soil structure . Plant competition .

Carbon deposition in soil . Soil microorganisms

Introduction

Terrestrial plants have evolved a range of strategieswhich allow them to access nutrients effectively.These strategies include development of extensiveroot systems, with fine roots and long root hairs, andhighly specialised cluster roots, as well as symbioticinteractions (Lambers et al. 2008a). Although herewe focus on arbuscular mycorrhizal (AM) symbiosesas by far the most prevalent, it is useful to brieflyconsider them in the context of the whole range ofroot and symbiotic strategies that are important insoils containing different types of organic andinorganic nutrients (Table 1). The occurrence, evo-lution and ecological significance of the differentstrategies will of course differ in different plants anddifferent soils (Lambers et al. 2008b). Long, finelybranched root systems and roots with long root hairsare important in increasing effectiveness in acquisi-tion of relatively immobile inorganic nutrients suchas P and Zn (Gahoonia and Nielsen 2004a, b).Where soils are severely impoverished in labileinorganic P, production of exudates containing

Plant Soil (2010) 326:3–20DOI 10.1007/s11104-009-9981-5

Responsible Editor: Peter Christie.

S. E. Smith (*) : E. Facelli : S. Pope : F. Andrew SmithSchool of Earth and Environmental Sciences,University of Adelaide,Adelaide, South Australia 5005, Australiae-mail: sally.smith@adelaide.edu.au

S. PopeSchool of Agriculture, Food and Wine,University of Adelaide,Adelaide, South Australia 5005, Australia

tricarboxylic acid anions, either by simple roots orspecialised cluster roots, can enhance the availabilityof insoluble inorganic P (Lambers et al. 2008a;Lambers and Poot 2003). Such plant adaptations areparticularly prevalent in the Proteaceae, often foundon ancient and highly weathered soils where P and Nare very scarce, but are also produced by somespecies in other families (Lambers and Poot 2003).Similar low-nutrient soils support plants that livesymbiotically with organisms that enhance acquisi-tion of nutrients. The least common are plants thatform N2-fixing symbioses with bacteria and cyano-bacteria (N acquired from the atmosphere), and byfar the most common and widespread are plantsforming mycorrhizal symbioses. These are of fourmain types, which involve approximately 90% ofterrestrial vascular plants and specialised soil-bornefungi (Table 1). The overall significance of differenttypes of mycorrhiza in nutrition of plants is wellestablished (Smith and Read 2008). Arbuscularmycorrhizal (AM) symbioses are the most frequent

symbiotic plant adaptation for plant growth in low-Psoils; they occur in nearly all terrestrial plantecosystems worldwide and involve probably asmany as 80% of vascular plant species, togetherwith a conservative estimate of 150 fungal species(Fitter 2005). The main physiological basis for thissymbiosis is usually considered to be bidirectionaltransfer of nutrients: uptake of inorganic soil P (andalso Zn and N) by AM fungi via their extensiveexternal hyphae, and transfer to the plant, inexchange for organic carbon (C). The fungi areobligate symbionts and cannot survive without thissupply. The end result in experiments using low-Psoil is often (but certainly not always) a largeincrease in plant growth, compared with non-mycorrhizal (NM) control plants, because the activitiesof the fungi in absorbing and transferring soil-derivednutrients result in relief of nutrient deficiencies.However, as will be discussed later, the AM pathwayfor P uptake has also been shown to operate signifi-cantly in plants which do not show an increase in total

Table 1 Diagrammatic representation of plant and symbiotic mycorrhizal strategies involved in acquisition of soil nutrient resources(particularly N, P and Zn) of different availabilities

Plant strategies Symbiotic strategiesStrategy

Resource

Roots and root

hairs

Exudates/clusters AMa ECMb and

ERMc

Soluble

inorganic

all nutrients P P, Zn (N) P & N

Insoluble

inorganic

P (P) P & N

Labile/soluble

organic

all nutrients (P) (P) P & N

Recalcitrant

organic

P & N

Increased intensity of shading indicates increased importance of the adaptation. Modified from Smith and Read (2008)a Arbuscular mycorrhizab Ectomycorrhizac Ericoid mycorrhiza

4 Plant Soil (2010) 326:3–20

P uptake and/or growth. This ‘hidden’ P uptake (whichmay also occur in AM-responsive plants) has importantimplications for interpretation of outcomes of AMsymbiosis at a range of scales from cellular toecological (Smith et al. 2009a).

In soils with a large accumulation of organic matterthe ectomycorrhizal (ECM) and ericoid mycorrhizal(ERM) symbioses come into play, because in these thefungal partners have a strong capacity to mobilise bothP and N from both available and recalcitrant organicforms. Thus ECM trees are often important componentsof both boreal and tropical forests, and ERM shrubs areimportant in heathlands. Both groups of symbiont alsotransfer inorganic P and N to plants, and consequentlyalso occur and play roles in mineral soils, that are low inorganic C, P and N. However, it has to be rememberedthat many types of trees form AM symbioses, whilesome form both AM and ECM symbioses. Further,most plants with N2-fixing symbioses are also AM,though there are exceptions, e.g. lupins, which formcluster-roots (Lambers et al. 2008a; Lambers and Poot2003; Smith and Read 2008). A diversity of outcomesof the symbioses between different plant and AMfungal species or isolates is increasingly recognised,and this will impact on ecological interactions in plantand fungal communities, as well as among the broadersoil microbial community.

This review will highlight activities of arbuscularmycorrhizas, which are important for both natural andagro-ecosystems, including most major crops. Inparticular, we will provide an update on new and lesswidely appreciated aspects of the symbioses. Recentresearch has revealed subtleties in the way AM fungiinfluence plant nutrition, and has implications for thediversity of plant responses ranging from highlypositive to negative, in terms of P uptake and growth.We will also focus on aspects of the symbioses thatare only indirectly related to plant nutrition, includingroles of the external mycelium in stabilising soilstructure and delivering organic C to soil, effects onwater relations of plants and interactions with someother soil organisms. Low soil water content isstrongly linked to low nutrient availability and topoor soil structure, so that mycorrhiza-developmentmay play significant roles in alleviation of both waterand nutrient deficiency. These features of arbuscularmycorrhizas may have special significance in aridenvironments or in fragile or compacted soils, whichwere a particular focus of the International Workshop

in Shihezi, China, and provided the original rationalefor writing this paper. Our intention is to extenddiscussion of the diversity of outcomes of symbiosesinvolving different plant-fungus combinations(Newsham et al. 1995b) and to highlight aspectswhich are likely to have significant ecologicalimplications in a range of different environments.

Arbuscular mycorrhizas and plant nutrientuptake: new research shows that the two uptakepathways do not act additively

It is well established that AM plants have two pathwaysby which nutrients (particularly P) can be absorbed: thedirect uptake pathway through epidermis and root hairs,and an AM pathway, in which P absorbed by externalfungal mycelium is translocated to structures inside theroot and thence across the symbiotic interface to plantcortical cells (Fig. 1). Recent work, both physiologicaland molecular, has provided new insights into theintegration of these two uptake pathways and howthey influence plant nutrient acquisition (Bucher 2006;Javot et al. 2007; Smith and Read 2008). As indicatedabove, a large number of field and glasshouse inves-tigations have shown that the outcome of establish-ment of AM symbioses in low-P soil is a markedincrease in plant growth and P uptake, compared withNM control plants of the same species, which ofcourse do not usually exist in nature. The traditionalexplanation of these effects is that direct uptake of P(and probably other nutrients such as Zn and N) issupplemented by uptake via the AM pathway. Reliefof P stress in the plant is considered to be the basisfor increased growth (i.e. the two pathways actadditively). This simple view is now being questioned(Smith et al. 2009a, b).

In an increasingly well recognised number of cases,AM colonisation does not result in any increases ingrowth or in total plant P, and sometimes the AM plantsare smaller than the NM controls (Johnson et al. 1997;Smith et al. 2009a). There is therefore a continuum ofresponses from strongly positive to negative, indicatingconsiderable ‘functional diversity’ in AM symbioses(Jakobsen et al. 2002). The AM-responsiveness interms of plant growth is determined by properties of 1)the plant genome: e.g. development of extensive rootsystems and long root-hairs that enhance P uptake bythe plant when it is NM; 2) the AM fungal genome:

Plant Soil (2010) 326:3–20 5

e.g. inherent extensiveness of external hyphae andother features, as yet not clearly identified; and 3)plant-fungus genomic interactions: e.g. speed and extentof plant colonisation and upregulation of orthophos-phate transporter genes in colonised root cortical cells(see Jakobsen et al. 2002; Smith et al. 2009a; Smith andRead 2008, and references therein). It is crucial torecognise that for a single plant species responsivenessvaries considerably with the identity of the fungalsymbiont. This has important consequences for dis-cussions of whether AM fungi which do not promote apositive growth response can be viewed as parasitic,‘cheating’ their plant partners by receiving C, butdelivering little or no P (Johnson et al. 1997; Jones andSmith 2004; Smith et al. 2009a).

It is now clear that the AM pathway plays animportant role in P uptake by plants that are colonisedby AM fungi, but do not respond in terms of increased Pcontent. Experiments with compartmented pots, inwhich radioactive P (32P or 33P) is available only tothe external mycelium, have repeatedly shown deliveryof P via the AM pathway to plants, not only inpositively responsive plant-fungus combinations, butalso when the plants show no benefit in terms ofincreased growth or P uptake (e.g. Hetrick et al. 1996;Ravnskov and Jakobsen 1995; Smith et al. 2003; 2004;Zhu et al. 2003). The operation of the AM P uptake

pathway is accompanied by expression of genes forindividual transporters for orthophosphate (Pi) in rootcortical cells that are strongly upregulated in AMplants, regardless of the plant responsiveness (Bucher2006; Poulsen et al. 2005). Where growth responsesare positive it is still possible to suggest that the directand AM uptake pathways act additively, but whenresponses are neutral or negative this cannot be true.Measurement of the contributions of the two pathwayshas now shown unequivocally that in many cases ofnon-responsive symbioses (as well as responsive ones)most of the plant P enters via the AM pathway. Thecorollary must be that the direct uptake pathway makesa reduced or negligible contribution (Li et al. 2006;Poulsen et al. 2005; Smith et al. 2003, 2004). There arethree possible explanations (not mutually exclusive)for the loss of activity of the direct pathway. The firstis that the concentration of P in the soil solutionadjacent to the root becomes depleted to the point thatno further uptake of P can occur, regardless of theactivity of the direct P transport system. Depletion atthe epidermal uptake surface (i.e. in the rhizosphere) isparticularly important for immobile nutrients such as P(Silberbush and Barber 1983; Tinker and Nye 2000),and is worse in dry soil (see below). The secondexplanation is that the orthophosphate transporters inthe direct pathway have reduced expression (measured

root growth

plant high-affinity P transporters

(P-responsive)

P

P

P depletionzone

Arb

CCfungal high-affinity P

transporters

plant high-affinity Ptransporters

(AM-inducible)Direct pathway

AM pathway

Fig. 1 Diagrammatic representation of the integration of thedirect and AM pathways of uptake of P as orthophosphate in aroot growing through soil. The direct pathway involvesexpression of plant orthophosphate transporters in root hairsand epidermis, resulting in progressive depletion of P close tothe root surface. The AM pathway involves the expression offungal high affinity transporters in external mycelium and plant

transporters in the interface between fungus and plant. In thisdiagram the intracellular fungus is depicted as an arbuscule(Arb) inside a cortical cell (CC), but other structures such asintracellular coils may also be important. Diagram drawn byEmily Grace and reproduced from Smith et al. (2009b), withpermission of the ATSE Crawford Fund, Australia

6 Plant Soil (2010) 326:3–20

as RNA accumulation) and hence activity; this hasbeen observed in some, but by no means all, experi-ments (Burleigh et al. 2002; Glassop et al. 2005; Liu etal. 1998; Paszkowski et al. 2002). The third explana-tion is that there is downstream regulation of trans-porter synthesis and activity. The last two explanationsassume that transporter activity is important in con-trolling the rate of Pi uptake, although there are somedoubts about this (Rae et al. 2004). Elucidation ofmechanisms underlying reduced contributions of thedirect uptake pathway will be a worthwhile area forfuture research. Clearly plants need to maintain theoption of utilising the direct pathway, because veryyoung seedlings and root apices may not be mycor-rhizal, due to delays in colonisation. Some soils (e.g.following disturbance or burning) have low mycorrhi-zal infectivity, so that plants may not become colonisedat all. Furthermore, only one investigation of the relativecontributions of direct and AM uptake has, as far as weare aware, involved a wild plant species (Hetrick et al.1994) and again extension of our knowledge will beimportant in understanding roles of AM symbioses inplant interactions and competition.

Mycorrhiza-induced growth depressions

The obligately symbiotic AM fungi are of coursecompletely dependent on plants for organic C.Explanations of the outcomes of symbiosis for theplant are often given simply in terms of the balancebetween net costs (C loss to the fungus) and netbenefits (additional P supply via the fungus). Wherenet costs exceed net benefits, and plant growthdepressions follow, it is then conventionally assumedthat the fungus is a parasite that ‘cheats’ or ‘exploits’its host by obtaining C but providing little or no soilP. This conventional explanation is tenable when thefungi colonise the roots extensively. However, recentdata and review of previous results show that largegrowth depressions are not necessarily associatedwith high AM fungal colonisation, but also occurwhen there is very low internal root colonisation, andin some cases also low external mycelium in soil(Grace et al. 2009a, b; Li et al. 2008a; Smith et al.2009a, b). Furthermore, the explanation is very plant-oriented, and ignores questions that are important incontexts of fungus-plant physiological and molecularinteractions, ecology and evolution. Importantly, our

increased understanding of the pathways of P uptakein AM plants are beginning to show that simpleexplanations for growth depressions based on exces-sive C drain are almost certainly incomplete (Grace etal. 2009b; Li et al. 2008a; Smith et al. 2009a). It ispossible that growth depressions in the absence of highfungal biomass are the result of P deficiency, inducedby reduced activity of the direct P uptake pathway andinadequate contribution of the AM pathway because ofthe low root colonisation or hyphal development in soil(Li et al. 2008a; Smith et al. 2009a). The regulatoryinterplay between AM P uptake and direct uptakethrough epidermis and root hairs has yet to be fullyrevealed. Understanding the controlling factors hasthe potential to inform plant breeding strategies toeliminate growth depressions where this might proveadvantageous to crop production (Grace et al. 2009b;Li et al. 2008a; Smith et al. 2009b).

The existence of growth depressions has longperplexed those interested in the evolution of AMsymbioses, because it has been assumed that larger sizeis a selective advantage. Hence, it was hard to com-prehend the evolutionary persistence of a symbiosisthat did not confer a positive growth benefit. A numberof explanations have been brought forward which maypartially explain the conundrum. Some researchershave drawn on the (undoubted) artificiality of potexperiments to suggest that growth depressions areartefacts, most probably caused by low light and hencelow photosynthesis and limiting C supply (Koide andSchreiner 1992). However, this explanation is unlikelyto be correct where depressions are associated withlow colonisation and hence minimal C drain. In anyevent, it is hard to show that depressions do not occurin nature, because of the extreme difficulty of pro-ducing (again artifactual) NM controls under fieldsituations (Plenchette et al. 1983a, b). Other expla-nations for the evolutionary persistence of AMsymbioses in non-responsive plants suggest benefitsof AM symbioses that are not directly related to plantgrowth, such as tolerance to pathogens or drought andeffects on soil structure. These are certainly importantin some circumstances (Miller and Jastrow 2002;Newsham et al. 1995a, b; Tisdall and Oades 1982).However, now that it is known that the AM P uptakepathway operates in virtually all AM plants, whetherresponsive or not in terms of P uptake and growth,additional explanations based on AM P uptakebecome feasible, including effects on plant competi-

Plant Soil (2010) 326:3–20 7

tion. Furthermore, the effects that the external AMfungal mycelium has on soil structure cannot beignored, given that the latter plays a critical role inplant water relations and maintenance of soil fertility.

Exploration of soil by external myceliumand interactions with soil structure

In all types of mycorrhiza the fungi produce largeamounts of mycelium in soil. Hyphal length densityassociated with an AM root can vary considerably,from as low as <1 to 111 m/g; most reported valuesare in the lower range, up to 40 m/g (Miller et al.1995; Smith et al. 2004). The spread of myceliumresults in deposition of considerable amounts oforganic C well beyond the zone normally consideredto be under the influence of roots (the rhizosphere—see Table 2) and hence influences the activities ofnon-symbiotic soil organisms. Hyphae also playhighly important roles in stabilising soil structure, byenmeshing soil particles and stabilising aggregates,particularly in the size range 20–200 µm diameter(Miller and Jastrow 2002; Tisdall and Oades 1982;Hallet et al. 2009). Effects of AM hyphae on soilstructural stability can persist even in the absence ofgrowing plants, and NM plants can gain benefits in‘mycorrhizal soil’ which supported AM plants in aprevious growth cycle, but very little is known aboutmechanisms underlying this effect (Augé et al. 2001,2004). Well developed soil structural stability isvital for maintenance of soil porosity and hence thewater-filled pores from which plants and their AMsymbionts access nutrients and water (Oades 1984).In arid environments and as soil dries out these factorswill play increasingly significant roles in plant survival.

In contrast to effects on soil structural stability, theimportance of the ability of AM hyphae attached toliving plants to access pores of small diameters thatare inaccessible to roots has not received a great dealof attention. Average diameters of hyphae of AM

fungi are in the range 2–20 µm and thus one or twoorders of magnitude narrower than roots (Table 2;Fig. 2; Friese and Allen 1991; Drew et al. 2003, andsee Smith and Read 2008 for additional references).This size difference has important implications foraccess to water-filled pores, because hyphae will beable to penetrate a much higher proportion of poreswith narrow diameters than roots are able to do.Furthermore, hyphae appear to have the ability toadjust hyphal diameter, depending on the soil poresize (Drew et al. 2003), and in consequence AMplants are able to obtain nutrients via the AM nutrientuptake pathway from increasingly narrow, tortuouspores which, as soil dries or becomes compacted,hold an increasing proportion of the soil solution. AMplants can therefore potentially access nutrients fromdrier or more compacted soils (i.e. smaller pores) thancan NM equivalents (Nadian et al. 1998; Tobar et al.1994). Operation of the AM nutrient uptake pathwaywill therefore persist at lower (more negative) soilwater potentials than direct uptake via root epidermis

Parameter Roots Hyphae

Diameter > 300 µma 2–20 µm

Length density in soil <0.10 m/g 2–40 m/g

Influence away from roota 0.3 cm 25.0 cm

Inter-root or inter-hyphal distance 2.0 cm 0.13 cm

Table 2 Estimated dimen-sions of roots and hyphaegrowing in soil

a Not including root hairs,which have a diameter ofapprox 10 µm

Fig. 2 Hyphae of AM fungi have very much smaller diametersthan many soil pores. Scanning electron micrograph of a hyphaof the AM fungus Glomus intraradices (arrowhead) growingthrough a sand matrix with most common pore diameter of38 µm. Bar=20 µM. Photo courtesy Elizabeth Drew (Drew2002)

8 Plant Soil (2010) 326:3–20

and root hairs. Roles of AM symbioses in plant waterrelations are therefore potentially highly complex,involving hyphal interactions with soil structure aswell as more direct influences on the symbiotic plantsthemselves.

Arbuscular mycorrhizas and plant water relations

Many studies have demonstrated that AM symbiosesalter plant water relations, but the reported effectshave not been consistent between different investiga-tions, and mechanisms are certainly not clear. Never-theless, an extensive review by Augé (2001) coveringhundreds of studies, highlights a number of trends inAM compared to NM plants growing under waterrestrictions in pot experiments. These include increaseddrought tolerance, greater depletion of soil water,higher stomatal conductance and transpiration, bettersupply of diffusion-limited nutrients in dry soil, andlower drought stress (assessed as reduced concentra-tions of xylem abscisic acid (ABA) in AM plants). Suchdifferences suggest that AM plants are under less stressin dry conditions than NM controls (Duan et al. 1996),but the mechanisms underlying the effects remainelusive and deserve ongoing investigation.

Some studies indicate that improved nutrition ofAM compared with NM plants may be the main basisfor improved drought tolerance. In brief, about 80%of the studies assessed by Augé (2001) found thatAM plants grew better under drought stress than NMplants. In some cases the drought-stressed AM plantswere shown to absorb more P even when the NMplants had adequate P nutrition. Neumann and George(2004) used a compartmented pot system to separateeffects of drought on AM function from effects ofplant water stress per se. They demonstrated clearlythat AM roots were able to absorb P more effectivelyfrom dry soil than NM roots, regardless of plant waterstatus. This effect could be explained by the increasedcontribution of the AM uptake pathway as soil dries.Under these conditions continuity between water-filled pores decreases, the tortuosity of the soil to rootpath increases (Tinker and Nye 2000), and soilhydraulic conductivity is reduced. As a result, therate of diffusion and mass flow of nutrients decreaseswith decreasing soil moisture, and nutrients effec-tively become less available (Viets 1972). A sharp Pdepletion zone has been shown to develop close to

the root in a dry soil, but depletion is more gradualand extends further from the root in a moist soil(Gahoonia et al. 1994). In addition, the rate of rootextension is lower in dry soil because of reducedturgor and increased soil strength, as well as reducednutrient availability (Viets 1972). AM colonisationand effective development of external mycelium willbe especially important for nutrient uptake in thesesituations, so that beneficial effects of operation of the‘hidden’ AM pathway in dry soil will exist even inplants which do not respond in terms of growth.Validation of this suggestion will require determinationof the relative contributions of the two pathways to Puptake under well-watered and drought conditions.

It has been known for some time that hydraulicconductivity of intact roots and root cortical cells islower under P deficiency (Andersen et al. 1988; Radinand Eidenbock 1984; Radin and Matthews 1989;Reinbott and Blevins 1999), so that maintenance ofP supply by AM colonisation may play a role inensuring high hydraulic conductivity, and hence wateruptake. In experiments with non-colonised plants,resupply of P to deficient plants restored root perme-ability within 24 h (Carvajal et al. 1996; Reinbott andBlevins 1999). The rapidity of these changes can bestbe understood in the light of new knowledge ofmembrane water channels (aquaporins). Transcriptionof genes encoding aquaporins is adjusted in responseto environmental factors such as light, temperature andnutrient and water supply (Luu and Maurel 2005). Inaddition, the pores of existing water channels can beopened or closed, for example in response to HgCl2(Tyerman et al. 1999). When applied to roots wellsupplied with P, HgCl2 reduced hydraulic conduc-tivity to a level as low as that of P-deficient plants; thelatter were not affected by HgCl2 (Carvajal et al.1996). This result suggests that aquaporins areexpressed or activated to a much lower level in P-deficient plants, contributing to the observed decreasein root hydraulic conductivity with P-deficiency. Itmight therefore be expected that plant aquaporinswould be more strongly expressed in P-sufficient AMplants than in P-deficient NM ones. However, no AM-specific or AM-inducible aquaporin genes, equivalentto the Pi transporter genes in the AM P uptakepathway, have been identified in microarray studiesdirected towards identification of symbiosis-relatedgenes. Increased expression of plasma membraneaquaporin (PIP) genes (PIP1 or PIP2) has, however,

Plant Soil (2010) 326:3–20 9

been observed in Medicago truncatula colonised byGlomus mosseae or Glomus intraradices, but notsubjected to water stress (Journet et al. 2002; Uehleinet al. 2007). Two studies directly investigated the roleof PIPs in the response of AM plants to water stress(Aroca et al. 2007; Porcel et al. 2006). In both casesNM control plants were given additional P in anattempt to obtain plants of similar size and nutrientstatus to the AM plants, but no information wasreported regarding biomass and nutrient status. Therewere no consistent patterns of change in expression ofPIP genes in AM and NM plants, whether water-stressed or not, so it proved difficult to relate increasedhydration or root conductivity in AM plants toaquaporin gene expression (Aroca et al. 2007; Porcelet al. 2006). Furthermore, in contrast to mRNAaccumulation, the level of PIP2 protein decreased inNM bean plants under water stress, but did not changein AM plants. Because root conductivity followed thesame pattern, the authors suggest that PIP2 proteinwas involved in increasing water uptake from a dryingsoil in AM beans (Aroca et al. 2007). However, muchmore extensive studies are needed to substantiate thissuggestion, particularly the use of P-supplementedNM controls to eliminate any AM-mediated effects onaquaporin production via nutritional changes. Otherapproaches could include the use of non-responsiveplant-fungal combinations and non-mycorrhizal mu-tant plants as surrogate non-mycorrhizal hosts. How-ever, again great care would have to be taken to ensurethat results were not confounded by differences intissue P concentrations.

Some studies have linked increased water uptakeby AM roots to the effect of hyphae on conductivityof rhizosphere soil. Roots shrink under high transpi-rational demand, creating air gaps between the rootand the soil matrix and hence a large drop in waterpotential adjacent to the roots (Faiz and Weatherley1982). In the course of a drought, root hydraulicconductivity determines water uptake only in theinitial stages, after which the most important factorsare conductivity of the soil-root gap and subsequentlyconductivity of the dry soil (Nobel and Cui 1992).Hyphae of AM fungi bind roots to the soil, which hasbeen suggested to maintain liquid continuity and limitthe loss of hydraulic conductivity caused by air gaps(Augé 2001; Augé et al. 2001; Davies et al. 1992).

Mycorrhizal fungi, as well as roots, have also beensuggested to influence hydraulic redistribution of

water in soil (hydraulic lift). This process is likely tomaintain soil moisture in surface horizons duringdrought and hence increase both availability ofnutrients and the survival of roots and associatedfungal hyphae. An effect of mycorrhizal myceliumhas been most clearly demonstrated in pot and fieldstudies for ectomycorrhizal plants, and evidence forits operation in AM systems is less clear (Allen 2007;Egerton-Warburton et al. 2007; Neumann and George2004; Querejeta et al. 2003a; 2007a; Schoonmaker etal. 2007; Warren et al. 2008).

An additional possibility links drought tolerance inAM plants to growth depressions. Large plants usemore water, so in water-limited environments largeshoot biomass may be disadvantageous as long asreproductive success (and hence yield) is not com-pletely dependent on vegetative biomass. Hence, lackof positive AM growth response (or even a growthdepression) during vegetative stages will reduce wateruse. If at the same time nutrient uptake is maintainedby the ability of the AM fungal mycelium to capturenutrients effectively from dry soil, then consequencesfor yield of crops or fecundity of wild plant speciesmay be positive. In support of this idea, Li et al.(2005) showed that in two wheat cultivars a growthdepression in AM plants occurred at early growthstages but disappeared at maturity in plants that hadreceived additional P. Furthermore, again with addedP, AM plants produced higher grain yields than NMplants. Subsequent work has shown that the AM Puptake pathway was highly likely to have beenoperating in these plants (Li et al. 2006; 2008b).Although water use was not measured accurately inthis experiment, it was observed that the smaller AMplants unsurprisingly required less water to be appliedto the pots (HY Li, personal communication).

Water use efficiency (WUE) of AM and NM plantshas been investigated in the context of the effects ofAM inoculation on drought tolerance and establish-ment of several plant species. The review by Augé(2001) indicates that both increases and decreaseshave been observed, in about equal numbers. Carbonisotope discrimination (δ13C) has been shown to benegatively correlated with WUE and proposed as aparameter to evaluate differences between plantcultivars (Condon et al. 2002; Farquhar et al. 1989).Querejeta et al. (2003b, 2006, 2007b) used δ13Cmeasurements to evaluate effects of inoculation witheither a single AM fungal species or a mixture of

10 Plant Soil (2010) 326:3–20

species on WUE of two woody plant species fromMediterranean environments. They found that in Oleaeuropea WUE was increased by AM inoculation, withdifferent effects of single and multiple inoculation,whereas in Rhamnus lycioides inoculation had noeffect (Querejeta et al. 2006). Differences betweenplant species and effects of differences in compositionof the inoculum highlight the marked ‘functionaldiversity’ in AM symbioses which will need to betaken into account when evaluating outcomes ofexperiments, particularly in the field. In any event,the potential significance of reduced vegetative growthof AM plants in arid environments deserves moreattention in the context of roles of naturally occurringAM colonisation of both crops and wild plant species.The major emphasis of much mycorrhizal research onbig AM (vs little NM) plants may have clouded ourperceptions of possible advantages of small size.

The possibility of direct water transfer to plants viaAM fungal hyphae has been raised repeatedly, but theevidence is not fully persuasive and the idea remainscontroversial. The pathway is assumed to be similar tothe AM P uptake pathway, with water absorbed by theexternal mycelium and delivered to the cortical apoplastat the symbiotic interfaces, where it would join watertaken up via the root apoplastic pathway. It is presumedthat water would be transferred via mass flow of solutionin the hyphae, but how this might occur in apparentlysimple tubular structures, in which bidirectional nutrienttransfers and cytoplasmic streaming occur simultaneous-ly, has not been addressed satisfactorily. It seemsunlikely that AM colonisation itself alters the apoplasticpathway by which roots absorb water, because entry ofhyphae into the roots occurs via epidermal passagecells and therefore does not create new pathways (Shardaand Koide 2008; Smith et al. 1989).

Operation of a hyphal pathway has usually beenproposed because other mechanisms that would in-crease root hydraulic conductivity in AM plants (e.g.improved nutrition, increased root branching) did notprovide a full explanation for increased transpirationalflux. Early studies calculated (rather than measured)potential hyphal transport of water on the basis ofincreased P delivery to (responsive) AM plants,assuming the mechanism of P translocation was alsoby mass flow (Cooper and Tinker 1981; Koide 1993).There are several problems with this approach: theAM and NM plants had to be of different size andnutritional status and the method used to calculate AM

P delivery was flawed, because it was assumed thatdirect P uptake was not influenced by AM colonisa-tion, i.e. that direct and AM uptake were strictlyadditive and there was no ‘hidden’ P transfer. Further-more, there is no evidence that P transfer occurs bymass flow. The contribution of hyphae to water uptakecalculated in this way was very small, compared todaily transpiration losses (Koide 1993).

Effects of size and nutritional differences betweenAM and NM plants have been avoided in someinvestigations by measuring the effects on transpira-tion in AM plants when hyphae were severed orotherwise damaged (Faber et al. 1991; Hardie 1985).Transpirational flux did then decrease, but resultswere variable and differences not significant (Hardie1985). Using a compartmented system, Faber et al.(1991) produced some evidence for depletion of waterin the hyphal compartment (HC), but later work byGeorge et al. (1992) failed to show any differences inwater depletion in the HC, regardless of degree of plantwater stress or whether hyphae were severed. At thisstage it must be said that the involvement of hyphae ofAM fungi in direct water uptake is ‘not proven’.

Carbon deposition in the rhizosphereof mycorrhizal plants

There is no doubt that extensive proliferation of AMfungal mycelium in soil and production of spores,compared with roots alone, will change the distribution,chemical composition and amount of organic inputs intosoil. The amounts of fungal material are considerable,but have almost certainly been underestimated in manyinvestigations, and indeed sometimes ignored. Becauseroots of most plant species are mycorrhizal under fieldsituations, neglect of the fungal component of below-ground inputs may have resulted in serious under-estimates of C deposition. Very little is known withcertainty about the amounts of C deposited in soil frommycorrhizal fungal sources, and even less about rates ofC turnover and persistence (Olsson and Johnson 2005;Zhu and Miller 2003). For arbuscular mycorrhizas theestimates of the proportion of plant photosynthateconsumed by the fungal partner for growth andmaintenance range from about 4–20% (see Jakobsenet al. 2002; Smith and Read 2008). These valuestranslate into considerable quantities of C directed tofungal productivity belowground. However, turnover

Plant Soil (2010) 326:3–20 11

rates are often thought to be quite high (Staddon et al.2003), perhaps unrealistically so (Olsson and Johnson2005; Zhu and Miller 2003), and the amounts ofpartially decomposed C of AM fungal origin retainedin the rapidly decomposing and persistent fractions ofthe soil organic matter (SOM) pool are not wellestablished. As Olsson and Johnson (2005) show, thevery rapid turnover of AM fungal material measuredby Staddon et al. (2003) may be because only externalmycelium was sampled and the evanescent branchedabsorbing structures (BAS) made a disproportionatecontribution to the total. Thus the estimate takes noaccount of more persistent structures such as vesiclesin roots and spores in soil, nor of persistent runnerhyphae in roots and soil. Spores certainly contribute topersistent soil C and in one investigation it wascalculated that AM spores, present at 28 spores/g soil,contributed up to 919 kg/ha, a large proportion ofwhich would have been organic C (Sieverding et al.1989). Notably, Olsson and Johnson (2005) demon-strated that most of the C assimilated by AM fungiremained in the fungal component of the system up to32 days after the host plant (Plantago lanceolata) wasallowed to assimilate CO2 enriched with 13C. Inenvironments where soil microbial activity is limited(e.g. by arid or very cold conditions) residues of AMfungi will persist much longer.

The production of a glycoprotein (glomalin) byAM fungi, has received much attention with respectto its apparently large contribution to SOM and thecorrelation of amounts of glomalin to hyphal lengthdensity in soil and soil structural stability (e.g. Lal2003; Rillig 2004; Rillig et al. 2001). However, theorigin, chemical composition, method of depositionand turnover of the glomalin fractions are not wellcharacterised, and the significance of this group ofcompounds remains elusive. Again it is hard toreconcile data suggesting turnover of external myceli-um of AM fungi in around 5 d (Staddon et al. 2003),with the extensive length densities and growth rates(1–2 mm/day) of extraradical hyphae, which contain ahigh proportion of relatively resistant chitin. Further-more the large amounts of supposedly AM-derivedglomalin in the SOM pool apparently persist fordecades (Rillig et al. 2001). Accurate quantificationof persistent SOM derived from AM fungi willbecome increasingly important, as mechanisms andmanagement practices that potentially maintain orincrease C sequestration in soil are sought in the

context of minimising atmospheric CO2 accumulation(Lal 2003). It is agricultural ecosystems, where cropsare actually or potentially AM, that are likely toprovide the most significant opportunities for manage-ment to maximise production and sequestration of Cderived from AM fungi.

Interactions with non-symbiotic soil organisms

Inputs of mycorrhizal fungal material into soil, almostentirely supported by recent photosynthate from plantpartners, provide important sources of organic sub-strates for assemblages of soil organisms. The chemicalcomposition of the fungi is different to that of roots,with the major carbohydrates being trehalose, mannitoland glycogen and the major structural polymer chitin.There is an increasing amount of research into theimpacts of AM colonisation on populations and activ-ities of the diverse members of the soil food webs.Extensive coverage is beyond the scope of this articleand more information and references will be found inSmith and Read (2008).

Given the alterations in chemical composition ofinputs as a result of AM development, it is not sur-prising, that community composition of bacterialpopulations in rhizospheres is different between mycor-rhizal and NM control roots (Marschner and Baumann2003; Marschner and Crowley 1996; Marschner et al.2001; Marschner and Timonen 2005). Furthermore,availability of surfaces on which bacterial films canproliferate is also altered by the development of hyphaeand rhizomorphs, as shown for ectomycorrhizas(Nurmiaho-Lassila et al. 1997; Sarand et al. 1998).There are likely to be down-stream alterations inassemblages of soil organisms dependent not only onthe AM fungi themselves, but also on those organismswhich are further up the soil food web. The functionalsignificance of such changes for soil properties,nutrient cycling and plant communities again remainsto be fully elucidated (Gange and Brown 2002a).

Research on AM effects on components of the soilmicrofauna has been more revealing from a functionalperspective, although research has frequently beentargeted more towards individual species of soil animals,than towards the food web community as a whole. AMfungal hyphaemay act as food sources for fungal-feedingnematodes (Bakhtiar et al. 2001) and also collembolans(Finlay 1985), especially when other fungi are absent

12 Plant Soil (2010) 326:3–20

(Klironomos et al. 1999). Some of the investigationshave provided evidence that the interactions betweenAM fungi and other soil organisms have significanteffects on nutrient cycling and hence positive influenceson plant growth (Gange 2000; Gange and Brown 1992;2002b). The mechanisms may include maintenance ofessentially young and active mycorrhizal fungal myce-lium as the soil animals ‘prune’ the fungal hyphae, aswell as increased speed of mineralisation of nutrientsfrom decomposing hyphae. Such mechanisms havebeen proposed to explain the effects of presence ofnematodes and other soil animals on nutrient turnover(Coleman et al. 1983; Gange and Brown 2002b),although the position of mycorrhizal fungi in the foodwebs has not always been explicitly discussed.

In contrast, it has been suggested that activities ofsome animals may damage the mycelia, possibly breakconnections in the mycelial network and hence reducethe effects of mycorrhizal fungi on nutrient acquisitionby plants (Klironomos et al. 1999; McGonigle and Fitter1988). In particular, damage caused by fungal-feedingmembers of the soil microfauna was proposed as onereason why increased inflow of P into roots via hyphaeof AM fungi was rarely observed in the field, incontrast to the situation in sterilised soil in pots (Fitterand Sanders 1992; Sanders and Fitter 1992). Thedamage could certainly be real, but the method forcalculating hyphal P inflow via the AM uptake pathwayagain depended on the assumption that direct and AMpathways were additive (i.e. there was no hidden Puptake, see above). In consequence, hyphal inflow inthe field was almost certainly underestimated andpotential damage overestimated. Furthermore, it hasnow been shown that the hyphal networks have powersof regeneration following damage, via the formation ofhyphal anastomoses (Giovannetti et al. 2004; Jakobsen2004; Mikkelsen et al. 2008). The outcomes for plantsof mycorrhizal interactions with soil fauna will dependon whether the hyphal length density and distribution ofthe network in soil is a factor limiting AM P uptake, orwhether increased nutrient mobilisation as a conse-quence of activities of the organisms in the soil foodweb plays a quantitatively more important role.

AM and plant pathogens

It has been suggested that AM fungi have indirectpositive effects on plant fitness through the protection of

the hosts against soil-borne plant pathogens (Newshamet al. 1995a). In support of this, there is evidence ofAM symbiosis increasing resistance of roots toinfection by fungal pathogens and root knot nematodes(see references in Azcón-Aguilar and Barea 1996;Cordier et al. 1998; Graham 2001). How AM sym-biosis protects plants against root pathogens is not wellunderstood, but several mechanisms have been pro-posed (Azcón-Aguilar and Barea 1996; Graham 2001):i) the improved nutritional status of an AM plant maysuffice to increase its tolerance to pathogen attack and/or the operation of the AM nutrient uptake pathwaymay compensate for the loss in function of damagedroots; ii) AM fungi and fungal pathogens andnematodes compete for infection/colonisation sitesand may also compete for resources; iii) changes inroot morphology (e.g. large proportion of higher orderroots) may alleviate the effect of pathogen attacks; iv)the changes induced by AM symbiosis in root exudatesthat alter interactions between components of the soilmicrobial communities may be detrimental for rootpathogens; and v) the accumulation of plant defence-related molecules in root cortical cells induced by AMsymbiosis produces localised and systemic resistance.In any event, effects of arbuscular mycorrhizas inoffsetting reduced fitness consequent on disease hasbeen shown to provide a convincing (although perhapsnow partial) explanation for evolutionary persistenceof AM colonisation in plants that do not displaygrowth benefits (Newsham et al. 1995a, b).WhereasAM symbioses seem to have a clear mitigating effecton soil-borne diseases, damage from foliar diseasesappears to be increased. Delayed senescence accom-panied by changes in the production of pathogenesis-related proteins are proposed mechanisms (Shaulet al. 1999).

AM in plant competition

Complex interactions among plants can be expectedto be strongly influenced by the plant strategies thatincrease nutrient acquisition, including AM symbio-ses. Resource-mediated competition is the interactionbetween individuals (of the same or different species)with a shared requirement for an essential resource inlimited supply; the likely outcome is reduction infitness of one or more of the competitors. Biomass iscommonly used as surrogate for fitness, mainly

Plant Soil (2010) 326:3–20 13

because it is difficult to carry out long term experi-ments in controlled conditions. Intensity of competi-tion (reduction of individual biomass) generallyincreases as the number of interacting individualsincreases (Begon et al. 1990; Silvertown and Lovett-Doust 1993). Thus, competition affects individualgrowth (Harper 1977) and the structure and dynamicsof the populations (Watkinson and Freckleton 1997;Weiner 1990), and contributes to the structuring ofcommunities (Grace 1995).

Changes in plant community structure have beenobserved in response to presence of AM fungi andalterations in the composition of AM fungal communi-ties (van der Heijden et al. 1998a, b). Such changesmight reasonably be expected to be the result of com-petition between plants with different responses to AMfungi (in terms of changes in biomass), including non-host plants (Grime et al. 1987; O’Connor et al. 2002;van der Heijden 2002). However, predictions of theoutcome of plant competition based on the responsesof individual plants to AM colonisation have been onlypartially successful (Zabinski et al. 2002), presumablybecause of our incomplete understanding of theprocesses that lead to variations in responsivenessand the resources that are under competition.

Most predictions have been based on the premisethat at the single plant level the main physiologicaleffect of AM colonisation is increased access tonutrients (particularly P) and consequent increase inbiomass. The larger plants are then expected to besuccessful competitors. The strength of competitionbetween two organisms is measured as the reduction inbiomass caused by the presence of a competitor. Thus ifAM colonisation does not produce any change inbiomass, no effect of the symbiosis on plant competi-tion is detected at this level. However, as we have seenin preceding sections, a significant contribution ofthe AM pathway to uptake of P (and probably othernutrients) may remain hidden unless radioactive tracersare used. Ignoring the contribution of the AM P uptakepathway risks underestimating the roles of AM symbi-osis in plant-plant interactions. As we have seen, thispathway accesses nutrients from regions of soil that (byreason of distance or diameter of soil pores) aregenerally unavailable to roots. Thus AM colonisationprovides differential access to limiting resources whichmay allow a successful competitor to pre-empt thoseresources and hence gain a competitive advantage(Huston and De Angelis 1994).

The variations in responsiveness (see above) andmarked effects of plant density (inevitably introduced asa factor in extrapolating from single plants to commu-nities) on plant responses to AM fungi have frequentlyalso been ignored. It is now clear that positiveresponses, in biomass and/or plant P, decrease as densityincreases (Allsopp and Stock 1992; Bååth and Hayman1984; Facelli et al. 1999; Koide 1991; Schroeder-Moreno and Janos 2008) and negative responses aremitigated (Li et al. 2008a). This complicates predic-tions from individual plant level to population level,which become even more complex when plants withdifferent genotypes and responses to AM fungi areincorporated at the community level (Graham 2008).

Not surprisingly therefore, the results of experimentsto determine effects of AM colonisation on plant com-petition have been rather variable. On the one hand,several investigations have produced the conceptuallysimple result that AM colonisation can favour an AMresponsive species competing with non-responsivespecies (in comparison with NM controls) (Hall 1978;Hartnett et al. 1993; Hetrick et al. 1994). However, apioneering study (Fitter 1977) did not show an increasein the competitive ability of the more responsivespecies (Holcus lanatus) due to AM colonisation. Inthis case the outcome of competition was related to thenegative effect of mycorrhizas on the less responsivespecies (Lolium perenne). Furthermore, plants thatshow no or negative responses to AM colonisationwhen grown singly, may become positively respon-sive, and hence successful competitors, when incompetition. Thus, a non-responsive weed (Centaureamaculosa) benefited from the presence of AM fungionly when in competition with non-responsive nativegrasses, which themselves remained unaffected(Marler et al. 1999; Zabinski et al. 2002). Further-more, in a simple model system, the outcome ofcompetition between a non-responsive tomato cultivar(AM host) and its corresponding AM defective mutant(surrogate non-host) favoured the host (Cavagnaro etal. 2004). In this case the interpretation was that theAM P uptake pathway allowed the host genotype topreempt soil P supplies, to the detriment of the non-host. Subsequent work with the same tomato geno-types demonstrated that the magnitude of the changein biomass depended on the identity and combinationof the AM fungi present in the inoculum (E Facelli etal. unpublished), underlining the importance of diver-sity of responsiveness, as a consequence of changes in

14 Plant Soil (2010) 326:3–20

fungal symbionts, in determining outcome of compe-tition (Munkvold et al. 2004; Smith et al. 2003, 2004).

In more complex, but still rather artificial commu-nities, outcomes may depend on the responsiveness ofthe dominant species (see Bergelson and Crawley 1988;Urcelay and Diaz 2003). Thus where the dominants ina community show little or no positive response to thepresence of AM fungi, the subordinates may well bereleased from competition and show increased survi-vorship and growth when AM, resulting in increasedplant diversity (Grime et al. 1987; van der Heijden etal. 1998b). In contrast, where the dominants are highlypositively AM-responsive, the presence of AM fungimay result in suppression of the subordinates by thelarger dominants and hence reduced diversity (O’Con-nor et al. 2002). An explanation of increased survi-vorship of subordinates (and hence diversity) based onorganic C transfer from the dominant species to thesubordinates (Grime et al. 1987) appears unlikely(Bergelson and Crawley 1988; Robinson and Fitter1999). However, adult (dominant) plants may provideproportionally more organic C to a common mycelialnetwork involved in supply of soil-derived nutrients toboth seedlings and adults (Horton and van der Heijden2008; van der Heijden 2004). This would have theeffect of reducing C demand on the seedlings, withconsequent benefit in terms of success (Horton andvan der Heijden 2008; Smith and Read 2008).

It should be clear from this brief outline that changesin plant community structure that follow plant-plant andplant-fungus interactions, together with variations in thecomposition of the fungal community (Klironomos2003; van der Heijden et al. 1998a; Vogelsang et al.2006) must be due to the interplay of complex pro-cesses (including competition) involving AM fungiand both host and non-host plants. Careful experimen-tation will be required to identify the significantprocesses and improve our understanding of them ata mechanistic level.

Conclusions

We have highlighted a number of features of AMsymbioses that are likely to be important for symbioticplants growing in environments experiencing seriousstress due to low soil nutrients and especially watercontent. We have shown that the consequences of‘hidden’ P uptake into plants via the AM pathway are

more wide-ranging than a simple demonstration of ahitherto unappreciated aspect of mycorrhizal function(Smith et al. 2009a, b). The fact that the pathway isactive in non-responsive, as well as responsive, plantsmeans that a very much wider range of plants willpotentially benefit from the symbiosis than previouslybelieved. It also means that most symbioses will bemutualistic at the cellular level, where plant organic Cis exchanged for fungus-derived P and other nutrients.Plants that are non-responsive to the symbiosis interms of growth or P content may nevertheless accessnutrients via the AM pathway in dry or compactedsoils, as well as more generally. They may also beexpected to benefit from the symbiosis when in com-petition with other plants, as in intercropping as wellas natural environments. We conclude that the newinsights into mycorrhizal function revealed by thedemonstration of ‘hidden P uptake’ via the AMpathway, and consequent wide-ranging benefits, pro-vide a much extended rationale for evolutionarypersistence of AM symbioses over the full range of‘diversity of function’ demonstrated with differentplant-fungus combinations under different environ-mental conditions. For non-responsive plants thisrationale no longer depends solely on indirect attributessuch as suppression of disease.

Roles of AM fungal mycelium in the developmentand maintenance of soil structural stability are wellestablished. Links with plant nutrition and growth arestill tenuous at the experimental level, but again arelikely to flow through to benefits for all plants growingin a particular area, not just the responsive mycorrhizalones. Although AM plants appear more drought-tolerantthan NM equivalents, the underlying mechanisms arestill obscure; they may include effects on soil structureand improved plant nutrition as an outcome of the abilityof hyphae of AM fungi to access those soil pores of verysmall diameter that retain both water and nutrients as soildries. However, mechanisms based on direct watertransfer in AM fungal hyphae seem unlikely.

There is no doubt that despite very much increasedemphasis in recent years, there is only fragmentaryunderstanding of the deposition of organic C in soilfrom AM fungal structures (including the externalmycelium, spores and fruitbodies) and the consequen-ces of such deposition for other members of the soilfood webs. The interactions will have importantconsequences for nutrient cycling and hence plantnutrition and plant community dynamics.

Plant Soil (2010) 326:3–20 15

Likewise, quality and quantity of organic inputs intosoil must contribute to the activities of soil organisms inC cycling and sequestration, but contributions ofmycorrhizas as conduits for rapid delivery and turnoverof photosynthate to soil are still only partially under-stood. Information on these important and topical areaswill become increasingly relevant as researchers seek tofind ways for agriculture to respond to global change.Indeed, it is essential for research to cross traditionalboundaries and to harness information and approachesfrom physiology, soil and plant ecology and agronomyin order to understand the complex and multifacetedcontributions of mycorrhizal symbioses, which are inte-gral to root function of the majority of terrestrial plants.

Acknowledgements We are grateful to Emily Grace andElizabeth Drew for making Figs. 1 and 2, respectively, availableto us. Our research is funded by the Australian ResearchCouncil. Our attendance (FAS and SES) at the InternationalWorkshop on Soil-Plant Interactions and Sustainable Agriculturein Arid Environments, Shihezi, Xinjiang, China was supportedby the conference organisers, for which we are most grateful.

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