Nutrient Transport Mycorrhizas Structure

8/13/2019 Nutrient Transport Mycorrhizas Structure

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Plant and Soil 159: 103-113, 1994. 1993 Kluwer Academic Publishers. Printed in the Netherlands.

Nutrient transport in mycorrhizas: structure physiology and consequen cesfor efficiency of the symbiosisS.E. SMITH l, V. GIANINAZZI-PEARSON2, R. KOIDE 3 and J.W.G. CAIRNEY ~ZDepartment of Soil Science Waite Institute The University of Adelaide Adelaide SA 5064 Australia2Station d Amelioration des Plantes INRA BV 1540 Dijon 21034 France3Department of Biology Pennsylvania State University University Park PA 16802 USAKey words: interface, mycorrhizas , nutrient acquisition, nutrient transport, nutrient use

AbstractNutrient transport in mycorrhizas occurs across specialized interfaces which are the result ofcoordinated development of the organisms. The structural modifications give rise to large areas ofeither inter- or intra-cellular interface in which wall synthesis is frequently modified and in whichaltered distribution of membrane bound ATPases is important, particularly with respect to mechanismsthat may be involved in bidirectional transfer of nutrients. Except in orchid mycorrhizas, net movementof organic carbon from plant to fungus occurs, complemented by mineral nutrient movement in theopposite direction. The general consensus is that sustained transfer at rates that will maintain thegrowth and development of the organisms requires increases in the rates at which nutrients are lost fromthe organisms; possible mechanisms for this are discussed. The transfer processes are essential indetermining both plant and fungal productivity and an approach to calculating the efficiency of thesymbiosis in terms of the expenditure of carbon or of phosphorus) is discussed.

Introduct ionBidirectional transfer of nutrients between plantand fungus is typical of ecto-, vesicular-a rbuscular VA) and e r icoid mycorrh iza lassociations and is the basis for the prolongedcompat ib le in te rac t ions typica l of thesesymbioses. The transfer occurs across interfaceswhich develop in different ways in the differentmycorrhizas, although the end result in terms ofthe spatial arrangement of membrane and wallcompo nent s varies only in detail . Theeffectiveness of the symbiosis with respect toplant growth and yield is influenced by themagnitude of the flux of phosphat e or othernutrients) to the plant and of carbohydrate to thefungus.

In orchid mycorrh izas the re la t ionshipbetween the symbionts is different; nutrienttransfer is unidirectional, in favour of the plant

and involves both carbohydrate and mineralnutr ients . Never the less , th is symbiosis isimportant in nature and may have horticulturalpotential. It will therefore be considered briefly.

In this review we consider the structure anddevelopment of the interfaces as the sites atwhich transfer occurs, the mechanisms and ratesof transfer and the implications of this for plantproductivity.

Plant fungus interfaces : development andstructure in relation to transportAt the cellular level interfaces in all types ofmycorrhiza are composed of the membranes ofboth partners, separated by an apoplastic region.The various types differ in whether the interfacesare inter- or intr a-cel lular or both), theirdevelopmental and structural complexity and


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104 Smith et alt h e d e g r e e t o w h i c h w a l l a n d m e m b r a n emodificat ions contribute to special izat ion and tol a rg e a rea s o f co n t ac t b e tw een t h e sy m b io n t s(Smith and Smith, 1990). The spectrum rangesfrom simple , in terce l lu lar , wal l -wal l contac t inec tomycorrh iza to specia l ized fungal wal l -p lan tmemb ran e s t ru c tu re i n V A my co r rh i za , b u t i nev e ry ca se t h e fu n g a l p a r tn e r rema in s i n t h eapoplast outside the plant protoplast . Interfacesalso vary ontogenetical ly and the developmentalc h a n g e s m a y b e o f i m p o r t a n c e f o r n u t r i e n ttransport (Duddridge, 1986; Gianinazzi-Pearsonet a l . , 1991; Scannerin i and Bonfante-Fasolo ,1983).

Among endomycorrh iza l associa t ions , o rch ida n d e r i c o i d m y c o r r h i z a l f u n g i h a v e l i t t l eintercel lular growth and hyphal coils or peletonsare formed wi th in the p lan t ce l l s (Gianinazzi -P e a r s o n , 1 9 8 4 ; H a r l e y a n d S m i t h , 1 9 8 3 ) .In t race l l u l a r d ev e lo p men t a f fec t s fu n g a l w a l lstructure, metabolism and physiology, includingt he r e p r e s s i o n o f s u r f a c e a n d e x t r a c e l l u l a renzymes (Gianinazzi-Pearson et al . , 1986; Smith,1974) potentially detrimental to the plant cell.

The morphogenesis o f VA mycorrh iza l fungiwi th in host t i ssues i s more complex (Bonfante-F a s o l o , 19 8 4 ; G i a n i n a z z i - P e a r s o n , 1 9 8 4 ) .Colonization of the outermost root cel ls involvesthe sparse formation of simple intracellular coils,w h i l e i n t h e co r t i ca l p a ren ch y ma in fec t i o n i smuch more intense. Num erous highly branchedintracellular arbuscules arise from longitudinallypro l i fer a t ing in te rce l lu lar h yphae , so tha t twos t r u c t u r a l l y d i f f e r e n t t y p e s o f i n t e r f a c e a r epresent (Gianinazzi-Pearson et al . , 1991; Smithand Dickson , 1991) which may have d i fferen tfunctions (see below ). Within the root , hyphaeare thinner compared with external hyphae and,p a r t i cu l a r l y i n a rb u scu l e s , d o n o t d ev e lo p t h em u l t i - l a y e r e d , c r y s t a l l i n e c h i t i n s t r u c t u r e( B o n f a n t e - F a s o l o a nd G r i p p i o lo , 1 9 82 ,Gianinazzi-Pearson, 1986).Host reaction to penetrat ion and proliferat iono f t h e f u n g u s a p p e a r s s i m i l a r i n d i f f e r e n te n d o m y c o r r h i z a s ( s e e f o r e x a m p l e B o n f a n t e -Fasolo , 1984; Bonfante-Fasolo and Gianinazzi -P e a r s o n , 1 9 8 2; G i a n i n a z z i - P e a r s o n , 1 9 8 4 ;Hadley, 1975; Serrigny, 1982) and i t is in thepresence of the in t race l lu lar haustor ia tha t thehost cel l shows the most specific modificat ions.

In al l cases, the interface formed between plantce l l and fungus involves a newly formed p lan tm e m b r a n e e x t e n d i n g f r o m t h e p e r i p h e r a lp lasmamembrane around the fungal haustor iumas the lat ter grow s intra cel lularly. It has beenest imated tha t th i s can cause up to a 20-fo ldincrease in the surface area- to-volume ra t io ofthe host in VA mycorrhiza (e.g. Alexander et al . ,1 9 8 8 ) an d a l t h o u g h i n c reases h av e n o t b eenca l cu l a t ed fo r co i l ed h au s to r i a t h ey mu s t b econsiderab le . Invading hyphae of a ll types ares u r r o u n d e d b y p l a n t - d e r i v e d m a t e r i a l i n t h ea p o p l a s t ( B o n f a n t e - F a s o l o e t a l. , 1 9 91 ;De xheim er et al . , 1979). In orchids , cel l wallmaterial persists around intracellular stages, butin ericoid and VA mycorrhizas i t decreases andc a n b e r e d u c e d t o s c a t t e r e d p r o t e i n a n dp o ly sacch a r id e f i b r i l s (Bo n fan t e -Faso lo e t a l . ,1991; Dexheim er et al ., 1979). The presence ofpectins, cel lulose and glycocalyx consti tuents inthe arbuscular in terface (Gianinazzi -Pearson e tal . , 1990; Bonfante-Fasolo et al . , 1990), togetherwi th neut ra l phosphatase ac t iv i ty (Jeanmaire e ta l . , 1 9 8 5 ) i n d i ca t e s t h a t t h e p l an t p ro to p l a s tretains wall synthesizing act ivi ty. Production ofwall precursors, together with small amounts ofp ec t i n o ly t i c an d ce l l u lo ly t i c en zy mes (G arc i aRomera et al . , 1991; Pearson and Read, 1975 )suggests that the material may represent a carbonso u rce fo r t h e fu n g i ( see H ar l ey an d Smi th ,1 9 8 3 ) . C a r b o h y d r a t e t r a n s f e r i n o r c h i dm y c o r r h i z a s i s f r o m f u n g u s t o p l a n t a n ds y n t h e s i s o f p l a n t w a l l c o m p o n e n t s w i l l n otcont r ibu te to fungal nu t r i t ion in th is case , bu tmay b e o f s i g n i f i can ce in co n t ro l l i n g fu n g a linvasion.A v e ry imp o r t an t mo d i f i ca t i o n i n t e rms o fnutrient t ransport is the ATPase act ivi ty in theh o s t m e m b r a n e f o r m e d a r o u n d c o i l s o ra r b u s c u l e s ( M a r x e t a l ., 1 9 8 2 ; G i a n i n a z z i -Pearson et al. , 1991). In VA mycorrhizas, part ofthis act ivi ty is at tributable to an H-ion ATPasep r e s e n t i n t h e p e r i a r b u s c u l a r m e m b r a n e , b u tcy to ch emica l l y u n d e t ec t ab l e a lo n g o th e r p l an tm e m b r a n e s a d j a c e n t t o h y p h a e ( i n t e r c e l l u l a rhyphae in the cortex , hyphal co i l s e tc . ) o r theplant plasmamembranes adjacent to the walls ofe i ther in fec ted or un infec ted parenchyma ce l l s( G i a n i n a z z i - P e a r s o n e t a l. , 1 9 9 1 ). T h edistribution of act ivi ty around l iving arbuscules


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suggests that the infected root cells haveincreased ability to absorb nutrients, via thesymbiotic fungus, which in non-mycorrhizalroots is restricted to the outer cell layers.

With respect to the VA mycorrhizal fungus,H-ion ATPase activity is observed on theplasmamembrane of intercellular hyphae and incoils, but is variable on the arbuscule branches(Gianinazzi-Pearson et al., 1991).

In ectomycorrhizal associat ions, fungalcolonization of host root tissues is entirelyextracellular. A pseudoparenchymatous sheathenvelops the absorbing rootlets and is continuouswith intercel lular hyphae growing betweenepidermal and cortical cells (Hartig net) and theextra-radical network of mycelium. Host/funguscontact results in changes in hyphal morphology.In the Hartig net region hyphae branch profuselyand septa formation becomes irregular orincomplete to give a characteristic labyrinthinesystem (see Harley and Smith, 1983). Surfacefibrils and acid phosphatase activity, present inthe mantle, disappear as hyphae become tightlypressed against host cell walls (Dexheimer et al.,1986; Duddridge, 1986; Lei et al., 1990).Adjacent fungal and host walls becomeindistinguishable from each other, forming ahomogeneous interfacial matrix (Duddridge,1986; Duddridge and Read, 1984; Scannerini andBonfan te-Fasolo, 1983). Structural changes inthe host tissues are small, but in some caseswall ingrowths appear to be induced byfungal infect ion (Ashford and Allaway,1982). These resemble those of transfer cells,increasing the area available for transportbetween the symbionts. ATPase activity isassociated with the plasmamembranes of bothsymbionts when these are active and closelyassociated in the Hartig net region, but itdisappears as plant cells senesce (Lei andDexheimer, 1988).

Ultrastructural information for all types ofmycorrhiza indicates that deposition of wallmaterial in the interface is reduced with possibleconsequences in terms of the permeability of theapoplast. However, extracellular material is alsodeposited around hyphae of endomycorrhizas atpoints of entry to host cells (Scannerini andBonfante-Fasolo, 1983) and accumulates inintercellular spaces of the fungal sheath in

Nutrient transport in mycorrhizas 105ectomycorrhizas of ucalyptus and Pisonia(Ashford et al., 1988, 1989). Such material isimpermeable to fluorescent tracer dyes and, ifalso impermeable to solutes, would restrict thepassage of nutrients to the cortex except via thefungal symplast, prevent loss of solutes from theapoplast to the soil and, along with theexodermis (hypodermis), may permit control ofthe apoplastic nutrient concentrations (Ashford etal., 1989; Smith et al., 1989; Smith and Smith,1990).

ompounds transferred and mechanisms oftransferEvidence (or lack of it) for the nature of thecompounds transferred between the symbiontshas been reviewed previously (Harley and Smith,1983; Martin et al., 1987; Smith and Smith,1990). Sugars are importan t in carboh ydratetransfer, with hydrolysis of sucrose (or trehalosein orchid mycorrhizas), together with synthesisof characteristic non-recyclab le carbohydrates(e.g. mannitol in ectomycorrhizas), as importantsteps in polarizing transport in favour of onesymbion t (see Smith et al., 1969). Hydrolysi scould potentially occur at the host surface, in theapoplast and/or at the fungal wall, but onlyimmunocytochemical methods will confirm theprecise location. Other potential sources ofcarbon include wall precursors, which might alsorequire hydrolysis (see above), and organicanions or organic N compounds, but evidence fortheir involvement is lacking.

The soil-derived nutrients which aretransferred from fungus to plant vary inimportance in the different types of association.Ecto- and ericoid mycorrhizas have a majorinfluence on nitrogen (N) and a lesser effect onphosphorus (P) nutrition. In VA mycorrhiza sthis situation is reversed. N transfer from fungusto plant has been demonstrated in ecto- andericoid mycorrhizas and is also likely in VAassocia tions. Organic N (as amino acids oramides), rather than inorganic NH4+, is probablyinvolved (see Martin et al., 1987). Such transferwill result in movement of organic carbonagainst the general flow of carbohydrate and willaffect the net flux of reduced carbon, providing a


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106 Smith et alpossible route for carbon movement duringinter-plant transfer (see Smith and Smith, 1990).

Transfer of P from fungus to plant is welldocumented in ecto-, VA, ericoid, monotropoidand orchid mycorrhizas. In ectomycor rhizasthere is evidence that inorganic orthophosphate isthe major form in which phosphorus istransferred (Harley and Loughman, 1963) butdirect evidence for endomycorrhizas is lacking,largely because of technical difficulties. Giventhat the pH of the interracial apoplast is probablyacid due to the polarized activity of H-ionATP ases , HzPO 4- are li kel y to be thepredominan t ionic species involved. Othernutrients (S, Zn, Cu, Ca and Na) have beenshown by experiments with radio-tracers to betransferred between symbionts in various typesof mycorrhizas and it is likely that these crossthe interface as free ions in solution.Transfer of nutrients must be bidirectional inthe symbiosis as a whole. Carbohydra temovement from plant to fungus and mineralnutrient movement from fungus to plant certainlyoccurs at the whole plant level. However,whether this transfer occurs bidirectionally a t t h es a m e i n t e r f a c e (as has been generally assumed)is open to question (see Smith and Smith, 1990).At a single interface, transfer between symbiontsin either direction depends on export through themembrane of one, movement through theinterracial apoplast and import by the other.Distribution of ATPase activity has given somenew insights with respect to the processesinvolved, but we still have very limitedinformation on the magnitude of the fluxes ofnutrients in either direction or on the conditionsthat may affect these fluxes.Assuming that bidirectional nutrient transferoccurs at a single interface, both symbionts mustpossess functional plasmamembranes capable ofuptake of nutri ents from the apoplast. Inectomycorrhizas the coexistence of ATPaseactivity on plant and fungal plasmamembranes atthe Hartig net interface suggests that the twosystems work cooperatively in bidirectionalnutrient exchange. This is the scenario that hasbeen assumed for all types of mycorrhiza, but wecannot entirely discount the possibility that twospatially separate interfaces such as arbusculeand intercellular hypha in VA mycorrhizas (see

diagram in Smith and Smith, 1990) may beinvolved and this is explored below using P as anexample.Models of P transfer across a single interface

generally invoke passive efflux of Pi from thefungus and active absorption across the plantplasmamembrane (Smith and Smith, 1986, 1989,1990; Woolhouse, 1975). Net loss of Pi fromfree living fungi is normally regarded as slight,with membrane transport processes favouringabsorption (Beever and Burns, 1980), so thatconditions promoting efflux are likely to beimportant at the fungus/root interface. Perhapsthe simplest mechanism for this is where loss ofPi across the fungal plasmamembrane to theinterfacial apoplast is unmodified, butreabsorption from the apoplast by the fungus isreduced. This would result in an increase in neteffiux from the fungus. There is good evidencethat intracellular Pi concentrations in both fungi(Beever and Burns, 1980; Clipson et al., 1987)and plants (Clarkson and Scattergood, 1982; Lee,1982) affec t P~ transpo rt. High intr acel lula rconcentrations result in reduced P uptake relativeto mycelium with a lower Pi status in ecto-(Cairney and Smith, 1992a), ericoid (Straker andMitchell, 1987) and VA (Thomson et al., 1990)mycorrhizal fungi. High P concentrations inhyphae at the interface (Clarkson, 1985) and alow interfacial Pi concentration would, alongwith reduced reabsorption, maximize loss fromthe fungus. Lower Pi status of the root relative tothe fungus (maintained by metabolism and/ortranslocation within the plant) and theconcomitant increase in Pi transporting activity atthe plant plasmamembrane, would permit netmovement of P~ into the plant. Pi transfer to hosttissue in excised beech ectomycorrhizas wasaround 10-20 of Pi absorbed by the sheathhyphae (Harley and Brierley, 1955; see Strullu etal., 1986) and in mycelium of P i s o l i t h u st i n c t o r i u s net efflux of i o v e r an 8 h period wasalso about 10 of P~ abso rbed du ring thepreceding 16 h (Cairney and Smith, 1992b;unpublished results). This implies that effluxacross the unmodified fungal membrane might besufficient to account for transfer in theectomycorrh iza. Prelimin ary estimates in therange 1.4-4.6 10 8 mol.m-2.s 1 can be calculatedfrom data for efflux from P t i n c t o r i u s (see


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Nutrient transport in mycorrhizas 107Cairney and Smith, 1993) which suggestrelatively high efflux from the cultured fungalmycelium. These data require confirmation butit is certainly an approach that merits furtherinvestigation.As with the fungus, membrane transportprocesses in roots normally promote netabsorption from the apoplast rather than efflux(see Patrick, 1989). While coupled sugar-phosphate transporters have been proposed forroot cortical cell membranes at the interface(Schwab et ai., 1991; Woolhouse, 1975), thereremains no evidence for their existence. Indeedthe lack of demonstrable stoichiometry betweensugar and P transfer and the need for transfer ofother nutrients and regulation of pH and chargebalance across the interface suggests independenttransfer of the two (see Smith and Smith, 1990).Furthermore, the general assumption thatbidirectional nutrient transfer occurs at the sameinterface in all mycorrhizas is now beingquestioned. It is conceivable, however, that lossof carbohydrate from the root, like loss ofphosphate from the fungus could be explainedsimply in terms of decreased rates ofreabsorption into the plant cells. This might bebrought about by a reduction in activity of theplant hexose/proton cotransporter, resulting fromfungal infect ion. Hydrolysis of sucrose tohexoses by invertase in the apoplast (Patrick,1989) would allow a net sugar transport to thefungus. This would be supported by rapidconversion of hexoses to fungal metabolites(trehalose and mannitol in ectomycorrhizas)which, not being readily utilized by the plant,would maintain the flux of carbohydrate infavour of the fungus (Smith et al., 1969). Thefact that individual ecto- (Bevege et al., 1975;Cairney et al., 1989) and VA (Bevege et al.,1975) mycorrhizal roots act as greater sinks forphotosy nthet ica l l y-f ixed carbon than non-mycorrhizal roots strongly suggests greaterconcentration at the interface and the probabilityof increased loss from the root cells.

It is important to gain more evidence on theoverall fluxes of nutrients (whether plant- orfungus-derived) across the interface as a wholein order to judge whether norm al efflux,associated with reduced reabsorption, would besufficient to account for the flux across the

interface. There is evidence that this may not beso in VA mycorrhizas, where overall fluxes areof similar order to measured rates of P uptake byplant cells (Cox and Tinker, 1976; Morris,Dickson and Smith, unpublished results), makingit likely that some condition enhancing effluxmust exist at the interface.

Efflux could be promoted in a number ofways, including reversal of H-ion co-transportersfor phosphate and sugar, increases in frequencyor rates of operation of transmembrane carriersor by opening of channels (Patrick, 1989; Smithand Smith, 1986, 1989, 1990; Tester et al.,1992). Perhaps the most direct mechanismwould involve localized accumulation ofpa rt ic ul ar ions (e.g. H , K +, Ca 2+) in theinterracial apoplast, which could certainly occur,possibly as a result of the presence of apoplasticbarriers (see above). High extr acell ularconcentrat ions of monovalent cat ions, inpart icul ar K +, have rece ntly been shown tostimulate efflux of P from mycelium of theectomycorrhizal fungus P i s o l i t h u s t i n c t o r i u s(Cairney and Smith, 1992b; unpublished results).Efflux was stimulated at concentrations of 10-20mM, known to cause depolarization oftransmembrane electric potentials in fungalhyphae (Slayman, 1965) and algal cells (Keiferand Lucas, 1982). This could stimulate openingof a number of ion channel s (Tester , 1990),raising the possibility that the monovalentcation-induced efflux of P from P t i nc to r iu s maybe mediated by opening of a channel. Work ofthis nature is still at an early stage. We do notknow how general the effect is and it must bestressed that the involvement of ion channels insuch cat ion-induced efflux is speculat ive.Release of phytohormones at the interface mightalso influence nutrient transport (see Schwab etal., 1991; Smith and Smith, 1990). Auxin (forexample) can increase ATPase activity in planttissue and may have a role in the mycorrhizalsituation (see Gianinazzi-Pearson et al., 1991)and the cytokinin N6-2-isopentyl-adenosine(2iPA) has been shown to influence bothabsorption and loss of ions from mycelium of theec tomycorrhiza l fungus S u i l l u s v a r i e g a t u s(Pohleven, 1989). Alterna tively , changes inosmotic potential in the apoplast or increasedcytoplasmic sugar concentrations in infected


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108 S m i t h e t a lhost cel ls may influence transmembranetransport either directly, by influencing ATPaseactivi ty Wyse et al., 1986), or indi rect lyvia stretching of the plasmamembrane.Stretch-activated channels specific for bothcations and anions are known to exist on higherplant plasmamemb ranes Cosgrove andHedrich, 1991; Hedrich and Scroeder, 1989) andcould be potentially important in controllingfluxes from both symbionts at the mycorrhizalinterface.While nutrient exchange is general lyinterpreted as occurring simultaneously in bothdirections across a single interface, it istheoretically possible that exchange occursacross interfaces which are separated temporallyor spatially. Temporal separation would involvenet movement of nutrients in different directionsat different developmental stages. In VAmycorrhizas for example, absorption of sugarinto young arbuscules and loss of nutrients suchas P from older arbuscules cannot totally be ruledout at present, although it seems unlikely Smithand Smith, 1990). In ectomycorrh izas, whereturnover of the exchange interface is much lessrapid, it becomes even more difficult to envisage.Functional ectomycorrhizas persist for months,during which time they act as sinks for currentphotosynthate and effect P transfer to the plantCairney and Alexander, 1992a, b; Downes et al.,1992). This, together with the distr ibution of

ATPase activi ty on the membranes see above),strongly implies simultaneous transfer in activeectomycorrhizas.Separation of the components of bidirectionalnutrient transfer in space seems more likely thanseparation in time. Based on differences in H-ion ATPase distribution between arbuscules andintercellular hyphae, Gianinazzi-Pearson et al.1991) have proposed that spatial separationmight occur in VA mycorrh izas. The resultwould be net loss of nutrients such as P fromarbuscule branches associated with uptake by theplant via the highly energized periarbuscularmembrane. Carbohydrat e transfer would occur

via loss from cortical cells to intercellular spacesand uptake by intercellular hyphae, which haveconsistent H-ion ATPase activity. As stressed bythe authors this interpretation is speculative, butit challenges the generally held view of a single

transport interface in these mycorrhiz as. Weclearly need more information on ATPasedistribution using immunological as well ascytochemical techniques), apoplastic pH andsolute concentrations as well as data for fluxes ofdifferent nutrients across the interface.

he imp ortance o f nutr ient transfer to plantproduct iv i tyFrom an agricultural or ecological standpoint,and therefore in the context of this symposium,the interest in nutrient transfer betweenmycorrhizal symbionts is based on the potentialeffects of infection on plant yield, survival orspecies composit ion of plant communit ies.When plant growth and reproduction are limitedby the rate of nutrient acquisition and whenmycorrhiza l infection increases this by uptakeand transfer processes), it is clear that infectionis of importance and that the net result ofbidirectional transfer is a gain in plant biomassor other measur able paramete r. However,mycorrhizal infection does not always increaseplant growth or reproduct ion Fitter, 1985;McGon igle, 1988). Possible reasons includehigh efficiency of P acquisition or low Prequirement Koide, 1991; Smith et al., 1992) ofthe plants. P acquisition can be reduced whenexternal hyphae are destroyed by grazing soilanimals Finlay, 1985; McGonigle and Fitter,1988; Rabatin and Stinner, 1988), soildistur bance see below) or fungi cides Haleand Sanders, 1982) or where incompletephysiological integration of the symbionts resultsin low rates of transfer see below). In these andother situations it is important to be able toanalyse the effectiveness of a symbiosis in termswhich can be related to the quantitative aspectsof the nutrient transfer processes, so thatpredictions can be made of the importance ofmycorrhizal associations in particular plantspecies or in particular agricultural or naturalsyste ms. The outcome of the increas edunderstanding will be potential reductions inapplicat ion of chemical fert i l izers andimprovement of the efficiency with which theyare used. The reasons are both economic andconcerned with environmental quality.


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utrient transport in mycorrhizas 109easurement of the eff iciency of nutrient

acquis i t ionEff ic ient p lants might be de f ined as those which ,e i t h e r w i t h o r w i t h o u t m y c o r r h i z a l i n f e c t i o n ,t h r i ve in nu t r i e n t de f i c i e n t so i ls . The y c an bed e t e c t e d b y tr i a l a n d e r r o r i n n a t u r a le nv i ronme n t s a nd i n s c re e n i ng p rog ra ms , bu t am o r e m e c h a n i s t i c a p p r o a c h i s n e e d e d i n p l a n tb re e d i ng to p roduc e ' e f f i c i e n t ge no t y pe s ' . Th i srequi res a knowle dge of wha t makes a pa r t icula rge no t ype suc c e s s fu l a nd i t ma y t he re fo re ma kesense to speak of a phys io logica l e ff ic ie ncy wi thwhich resources (such as P) a re e i the r acqui redor u t il i zed . These can be de f ined in te rms of thera t e o r a moun t o f nu t r i e n t a bso rbe d pe r un i t o froo t a nd i n t he a moun t o f d ry ma t t e r p roduc e dper uni t of nut r ient absorbed, re spec t ive ly (Baonet a l . , 1992; Smith e t a l . , 1992).

K o i d e a n d E l l i o t t ( 1 9 8 9 ) d e f i n e d b o t h a Pu t i l i z a t i o n e f f i c i e n c y ( A C '~ / A P W) a n d a Pacquis i t ion e ff ic ie ncy (Apw/ACb), wh ere AC ~ i sthe to ta l ca rbon accumula ted in the whole p lantdur ing uni t t ime , AP W s the P accum ula ted in thep l a n t du r i ng t he s a me pe r i od , a nd AC b i s thec a r b o n e x p e n d e d b e l o w - g r o u n d f o r t heacquis i t ion of tha t P . Ca lcula t ing the e ff ic ien cyof P a c qu i s i t i o n a s the r a t i o o f P a c q u i re d t oc a r b o n e x p e n d e d i s a l o g i c a l a p p r o a c h s i n cec a rbon c a n be r e ga rde d a s t he e ne rgy c u r re nc y o ft he p l a n t (Mo one y , 1972). How e ve r , c a rbon i sn o t t h e o n l y p o s s i b l e c u r r e n c y w i t h w h i c h t oexpress the cos t of P acquis i t ion . For example , i fP were the l imi t ing resource , P would a l so be ana p p r o p r i a t e c u r r e n c y . P a c q u i s it i o n e f f i c i e n c yw o u l d t h e n b e : ( A P ' U A P ~ ) , w h e r e P b i s tha ti n c r e m e n t o f P e x p e n d e d b e l o w - g r o u n d i n t h eacqu isi t ion of A P ~. pb i nc l ude s t wo c ompone n t s :tha t which i s los t f rom the root sys tem throughleakage , dea th , exuda t ion , e tc . , and tha t which i sr e t a i n e d i n t he roo t a nd hypha l t i s su e s o f t hebe l ow -g ro und sys t e m. One mi gh t a rgue t ha t Pand ca rbon a re so c lose ly l inked phys io logica l lytha t the P for P approach cont r ibutes noth ing toou r unde r s t a nd i ng be yond t ha t c on t r i bu t e d by t heP f o r c a r b o n a p p r o a c h . I n d e e d , w h e n Pdef ic iency l imi t s p lant growth i t could be a rguedt h a t i t d o e s s o b y l i m i t i n g c a r b o n a c q u i s i t i o n(He l d t e t a l . , 1977 ; s e e S mi t h a nd Gi a n i na z z i -Pearson, 1988). Mo reove r , in the cons t ruc t io n of

roots , in exuda t ion and t i ssue dea th , e tc . , P aswe l l a s c a rbon a re ' e xpe n de d ' . How e ve r , ma nys t ud i e s show t ha t P -de f i c i e n t p l a n ts a c c um ul a t es ta rch in the i r l eaves (e .g . He ldt e t a l . , 1977) ,s u g g e s t i n g t h a t P l i m i t s g r o w t h m o r e d i r e c t l ythan ca rbon when plants are P-def ic ient . Ei the rt he P fo r P o r t he P fo r c a rbon a pp roa c h ma yprove use ful , depending on the objec t ives of ther e s e a r c h , b u t c l e a r l y t h i s t y p e o f m e c h a n i s t i ca p p r o a c h i s r e q u i r e d i f w e a r e t o b e a b l e tounder s tand the bas i s for va r ia t ion am ong plantsin te rms of e ff ic iency.

Natural vs agricultural systemsAl t hough mos t r e s e a rc h on myc or rh i z a ha s be e ncarr ied out on cul t iva ted p lants , the re i s much tob e l e a r n e d f r o m n a t u r a l e c o s y s t e m s a n d t h eapproach jus t out l ined may be use ful in makingc ompa r i sons . Mos t r e s e arc h has be e n c onc e rne dw i t h s h o r t - l i v e d a n n u a l s a n d t h e r e l a t i o n sh i p b e t w e e n t h e s e a n d m y c o r r h i z a l f u n g i m a yd i f f e r f r o m t h at i n l o n g e r - l i v e d p e r e n n i a l s .A n n u a l s m a y b e a b le t o d e f e r s o m e o f t h e i rpa yme n t s ( i n c a rbon) t o myc or rh i z a l fung i un t i la f t e r r e p r o d u c t i o n h a s o c c u r r e d a n d a l a r g ee x p e n d i t u r e o n f u n g a l s p o r u l a t i o n m a y o c c u rd u r i n g s e n e s c e n c e w i t h o u t n e g a t i v ec o n s e q u e n c e s i n t e r m s o f h a r v e s t a b l e y i e l d .P e r e n n i a l s c a n n o t d o t h i s a nd s o m a y f a c ea d d i t i o n a l c a r b o n c o s t s . M o r e o v e r , t here l a t i onsh i ps be t we e n roo t a nd shoo t g rowt h i nt e r m s o f t e m p o r a l c h a n g e s , a l l o m e t r y a n dp l a s t i c i t y o f roo t / shoo t r a t i o , t oge t he r wi t h t heexplora tory s ize of the root sys tem in re la t ion toP sources (Campbe l l e t a l . , 1991; Koide , 1991)a nd t u rnove r o f roo t s ma y be qu i t e d i f f e re n t i nsho r t a nd l ong - l i ve d spe ci e s . The se d i f f e re nc e sa r e l i k e l y t o h a v e a s t r o n g i n f l u e n c e o n t h ec o n t r i b u t i o n o f m y c o r r h i z a s to n u tr i e n ta c q u i s i t i o n , a s w e l l a s t o t h e ' c o s t s ' o fm a i n t a i n i n g t h e s y m b i o s i s in te r m s o f t h eproport ion of to ta l C (or P) used in the process .

A n o t h e r i m p o r t a n t d i f f e r e n c e b e t w e e nagricul tura l and na tura l sys tems i s the degree ofd i s t u r b a n c e o f t h e s o i l . T h i s h a s a n e g a t i v ee f f e c t on t h e r a t e an d e x t e n t ot m y c o r r h i z a linfec t ion , and hence on nut r ient acquis i t ion andg r o w t h b e c a u s e o f t h e d i s t u r b a n c e o f t h e


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110 Smith et al.

m y c e l i a l n e t w o r k ( E v a n s a n d M i l l e r , 1 9 8 8 ;F a i r c h i l d a n d M i l l e r , 1 9 8 8 ; J a s p e r e t a l . , 1 9 8 9 a ,b ) . E v e n n o - t i l l a g r i c u l t u r a l s y s t e m s m a y h a v ef a r l e s s d i v e r s e a s s e m b l a g e s o f m y c o r r h i z a ls p e c i e s t ha n n a t u r a l e c o s y s t e m s , b r o u g h t a b o u tb y t h e d e g r e e o f e c o l o g i c a l s p e c i f i c i t y b e t w e e nh o s t p l a n t s a n d m y c o r r h i z a l f u n g i ( e . g .M c G o n i g l e a n d F i t t e r, 1 9 9 0) . T h e c o n s e q u e n c e so f t h is f o r e f f i c i e n c y o f n u t r ie n t u p t a k e a n d u s ea r e p r e s e n t l y u n k n o w n , b u t i ts r e l e v a n c e i s n o wb e i n g a p p r e c i a t e d a n d w o r k i s i n p r o g r e s s t od e t e r m i n e w h a t a t t r i b u t e s o f t h e s y m b i o n t s ( s u c ha s l e n g th o f e x t e r n a l h y p h a e o r n u tr i e n t f l u x e sa c r o s s t h e i n t e r f a c e ) a r e i m p o r t a n t d e t e r m i n a n t so f f u n g al e f f e c t i v e n e s s ( J a k o b s e n an d P e a r s o n ,u n p u b l i s h e d r e s u l t s ; M o r r i s , D i c k s o n a n d S m i t h ,u n p u b l i s h e d r e s u l t s ) .

I n m i x e d c r o p p i n g s y s t e m s ( e c o n o m i c a l l ys i g n i f i c a n t i n s o m e c o u n t r i e s ) m y c o r r h i z a s m a yh a v e i m p o r t a n t e f f e c t s o n y i e l d ( P u g n a a n dJ a n o s , u n p u b l i s h e d r e s u l t s ) , j u s t a s t h e y h a v e o nt h e c o m m u n i t y s t r u c t u r e a n d s p e c i e s c o m p o s i t i o ni n n a t u r a l c o m m u n i t i e s ( A l l e n a n d A l l e n , 1 9 8 4 ;E i s s e n s t a t a n d N e w m a n , 1 9 9 0 ; F i t t e r , 1 97 7 ;G a n g e e t a l. , 1 9 90 ; G r i m e e t a l. , 1 9 8 7 ; K o i d e a n dM o o n e y , 1 9 8 7) . T h e b a s i s f o r t h i s m a y b e f o u n di n t e r m s o f i n t e r p l a n t t r a n s p o r t o f b o t h c a r b o na n d m i n e r a l n u t r i e n ts a n d i t w i l l be n e c e s s a r y t od e t e r m i n e t h e c o m m u n i t y e f f i c i e n c y i n a s i m i l a rw a y a s th a t o u t l i n e d a b o v e f o r i n d i v i d u a l p l a n t s .

onc lus ions

I d e n t i f i c a t i o n o f e f f i c i e n t g e n o t y p e s o f b o t hf u n g u s a n d h o s t a n d u n d e r s t a n d i n g t h e w a y t h e i rf u n c t i o n i s i n t e g r a t e d d e p e n d s , a s w e h a v e s a i db e f o r e ( S m i t h a n d G i a n i n a z z i - P e a r s o n , 1 9 8 8 ) , o nt h e i d e n t i f i c a t i o n a n d q u a n t i f i c a t i o n o f th e k e yp r o c e s s e s i n v o l v e d in n u t ri e n t u p t a k e a n d u s e .M u c h o f th e e m p h a s i s o f m y c o r r h i z a l r e s e a r c h i na n a g r i c u l t u r a l c o n t e x t h a s b e e n o n t h e w a y i nw h i c h m y c o r r h i z a s i n c r e a s e n u t r ie n t u p t a k e v i a t h em y c e l i a l n e t w o r k i n s o il . T h i s i s a c r u c i a l p r o c e s si n e x p l o i t a t i o n o f s o i l r e s o u r c e s , b u t i s u s e l e s su n l e s s w e a l s o h a v e a q u a n t i t a t i v e u n d e r s t a n d i n go f t h e c o m p l e m e n t a r y p r o c e s s e s o f n u t r i e n tt r a n s f e r t o r o o t c e l l s a n d t h e w a y t h e s y m b i o s i s i sm a i n t a i n e d w i t h r e s p e c t t o a l lo c a t i o n o f c a r b o na n d o t h e r n u t r i e n t s b e t w e e n t h e p a r t n e r s .

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