Mycorrhizal phenotypes and the Law of the Minimum

Transcription

1 Rsrh Myorrhizl phnotyps n th Lw o th Minimum ny Collins Johnson, Gil W. T. Wilson, Jqulin A. Wilson, R. Mihl Millr n Mtthw A. Bowkr Shool o Erth Sins n Environmntl Sustinility n Dprtmnt o Biologil Sins, orthrn Arizon Univrsity Flgst, Flgst, AZ 8, USA; turl Rsour Eology & Mngmnt, Oklhom Stt Univrsity, Stillwtr, OK 777, USA; Biosins Division, Argonn tionl Lortory, Argonn, IL 9, USA; Shool o Forstry, orthrn Arizon Univrsity, Flgst, AZ 8, USA Author or orrsponn: ny Collins Johnson Tl: Emil: nny.johnson@nu.u Riv: July Apt: Otor w hytologist () oi:./nph.7 Ky wors: rusulr myorrhizs, ontxt pnny, light, mutulism, nitrogn (), prsitism, phosphorus (), stoihiomtry. Summry Myorrhizl phnotyps ris rom intrtions mong plnt n ungl gnotyps n th nvironmnt. Dirns in th stoihiomtry n uptk pity o ungi n plnts mk rusulr myorrhizl (AM) ungi inhrntly mor nitrogn () limit n lss phosphorus () limit thn thir host plnts. Mutulisti phnotyps r most likly in -limit systms n ommnsl or prsiti phnotyps in -limit systms. Cron (C) limittion is xpt to us phnotyps to shit rom mutulism to ommnslism n vn prsitism. Two xprimnts ompr th inlun o rtilizr n sh on myorrhizs in Anropogon grrii ross thr nturlly -limit or -limit grsslns. A thir xprimnt xmin th intrtiv ts o n nrihmnt n sh on A. grrii myorrhizs. Our xprimnts gnrt th ull sptrum o myorrhizl phnotyps. Ths inings support th hypothsis tht mutulism is likly in -limit systms n ommnslism or prsitism is likly in -limit systms. Furthrmor, sh rs C-ssimiltion n gnrt lss mutulisti myorrhizl phnotyps with ru plnt n ungl iomss. Soil rtility is ky ontrollr o myorrhizl osts n nits n th Lw o th Minimum is usul pritor o myorrhizl phnotyp. In our xprimntl grsslns rusulr myorrhizs n mliort -limittion ut not -limittion. Introution Although myorrhizs r gnrlly mutully niil or oth plnts n ungi, mny tors inlun th symioti outom o rusulr myorrhizl (AM) ssoitions (Hoksm t l., ). Unr rtin onitions AM ungi hv n shown to prss plnt growth (Mojo & Hnrix, 98; ng t l., 99); onsquntly thir untion orms ontinuum rom mutulism to prsitism. Th lotion o prtiulr AM symiosis on this ontinuum n onsir its phnotyp: n mrgnt proprty o intrtions mong plnt n ungl gnotyps n th nvironmnt (Johnson t l., 997). Th trm myorrhizl phnotyp rrs to th itnss outom or oth prtnrs in th symiosis. In AMs, Glomromyot r oligt iotrophs so thr is nvr ngtiv rspons y th ungus; onsquntly, in th ontxt o AM symioss, th trms mutulism (+, +), ommnslism (+, ) n prsitism (+, ) rr to positiv itnss outom or ungi n positiv, nutrl or ngtiv outom or th host plnts. Gnotypi trits rlt to rsour tr n ontrol o th symiosis in th ontxt o lol nvironmntl onitions r importnt trminnts o myorrhizl phnotyps (Johnson t l., 997, ). Th vilility o soil-riv nutrints hs long n rogniz s on o th mor importnt nvironmntl tors ontrolling myorrhizl phnotyp (Moss, 97). Th xtnsiv Ó Th Authors w hytologist Ó w hytologist Trust mylium o AM ungi n ttr ss immoil soil phosphorus () thn plnt roots; n AM symioss otn ilitt plnt growth in -limit soils (Koi, 99). Dspit unquivol vin tht AM ungi n quir n trnsr sustntil mounts o nitrogn () to thir host plnts (.g. Gorg t l., 99; Ligh t l., 8; Fllum t l., ), rports r ontritory rgring th nt ts o AM symioss on plnt growth in -iint soil. Som stuis show tht AM ungi inrs uptk n iomss gin o thir plnt hosts (.g. Tu t l., ) whrs othrs show tht AM symioss hv no nit or mliorting limittion (.g. Rynols t l., ). Ths stuis rprsnt n nigm, i AM ungi n inrs plnt uptk, thn why is thr not onsistnt vin tht AM ungi improv th nt proution o plnts grown in -iint soil? W suggst tht th nswr is tht th rltiv vilility o soil n trmins whthr or not myorrhizl nits outwigh thir osts. This nvironmntl vril (i.. soil nutrint supply) omin with th gntilly trmin pilitis o plnts n ungi to tr ron (C) or r th ky trminnts o myorrhizl phnotyp. Th onomis o tring prtnrships provis usul rmwork or unrstning rsour xhng mong myorrhizl ungi n thir hosts (Koi & Elliott, 989; Mznourt & Shwrtz, ). hotosyntht n minrls r th ommoitis xhng in myorrhizl symioss n th tr w hytologist ()

2 Rsrh w hytologist vlu o ths rsours is st y thir vilility in th nvironmnt. Th Lw o th Minimum stts tht plnt proution my ontroll y singl ssntil rsour tht is in limiting supply (von Liig, 8; vn r log t l., 999). Intiying whih rsours r in limiting supply in th nvironmnt n trmining whthr myorrhizl symioss n nhn ss to ths rsours provis n ologilly n volutionrily soun pproh to priting myorrhizl untion in osystms (R, 99). hotosynthsis provis th C urrny or symioti xhng. As suh, ny onition tht limits th photosynthti pity o host, suh s low light lvls s rsult o shing, my limit th mount o C vill to provision ungl prtnrs (Grhm t l., 98; rson t l., 99). Myorrhizl quisition n tr o C, n r intronnt us th pity o AM ungi to supply n to thir host plnts pns on th synthsis o xtnsiv ntworks o xtrnl hyph. Th mylium o AM ungi my onstitut sizl C n sinks; on squstr into th hyphl wll mtrix ths rsours om unvill or plnt us (Roinson & Fittr, 999). Th onntrtion o in th xtrnl hyph o AM ungi is 7 tims grtr thn tht o plnt shoots n t lst tims grtr thn tht o roots (Hog & Fittr, ). Consquntly, AM ungi must quir lrg mounts o rom th soil or thir own growth, n in -limit systms thy r unlikly to trnsport iologilly mningul mounts o to thir host plnts (ii). Furthrmor, th isprity in C : rtios o plnts n ungi suggst tht limittion is likly to inhiit ungl growth mor svrly thn plnt growth (Ky & Hrt, 997; Johnson, ). In ition, mss low n iusion prosss r usully nough to ring minrl- to th root sur. This is spilly so or soils whr O - is th ominnt orm o minrl-. Ths sm prosss r not nough to prvnt th ormtion o pltion zon roun roots or phospht ions primrily rlt to th low soluility o O - in soil solution. Th growth o xtrnl AM hyph into this pltion zon llows or myorrhizl plnts to hv ss to soil- tht othrwis woul not vill (Millr, 987). Thr is vin tht n vilility ply irnt rols in th trmintion o myorrhizl phnotyp. Exhng o plnt-riv C or ungl-riv hs n shown to nor myorrhizl ooprtion (Hmmr t l., ; Kirs t l., ) n myorrhizl tr is lrly link to iomss gin o plnts n AM ungi growing in -limit soils (Moss, 97). Rnt vin rom root orgn ulturs shows tht C lux rom host plnt to ungus my rgult trnsport (Fllum t l., ); howvr, th outom o this or plnts n ungl iomss gin hs not n monstrt. Stuis using whol plnts init tht tightly link C-or- xhng twn plnts n ungi in -limit systms os not gnrt iltrl ontrol o myorrhizl ooprtion in th sm mnnr tht C-or- xhng nors ooprtion n ontrols plnt n ungl iomss gin in -limit systms (Smith & Smith, ; Corr^ t l., ). Inst, vilility o my inlun myorrhizs inirtly through its ts on oth C supply n C mn. Riulos isphospht roxyls, th rt-limiting nzym in w hytologist () photosynthsis, ounts or s muh s 7% o l (Chpin t l., 987); onsquntly, nutrition ontrols th photosynthti pity o plnts n, in turn, th mount o C tht n tr with myorrhizl ungi. Also, th mn or photosyntht y AM ungi is inlun y vilility us ungl tissus r rih in mino is n polymri inluing hitin n ssoit glyoprotins (Blkwll, 988). In othr wors, soil vilility inluns oth th C sour strngth o th plnt (inrs t high ) n th C sink strngth o th ungus (rs t low ). Mutully niil myorrhizl phnotyps r likly to oun in -limit systms us AM ungi n tivly tr surplus or plnt photosyntht. By ontrst, mutully niil myorrhizl phnotyps r not xpt in -limit systms us AM ungi r unlikly to hv surplus or tr us thy hv highr rquirmnts thn thir host plnts. Both rtiliztion n sh hng th C : : stoihiomtry, n onsquntly, th rltiv osts n nits o myorrhizl symioss. I th mhnism ontrolling myorrhizl untion is simply th ln twn osts n nits o th symioss, thn C limittion us y insuiint light is xpt to hng th thrshol t whih C osts x nits n gnrt ommnslism or vn prsitism. W tst ths hypothss with thr xprimnts tht xmin myorrhizl rsponss to rtiliztion n sh using ig lustm (Anropogon grrii), highly myotrophi C grss rom Cr Crk, Frmi n Konz, thr orth Amrin grsslns with vry irnt soil proprtis. rvious stuis init tht ig lustm gnotyps n thir inignous ommunitis o AM ungi r o-pt to h othr n thir lol soil nvironmnts (Johnson t l., ; Ji t l., ). Consquntly, ll thr xprimnts mintin o-pt systms o plnt gnotyps, soils,- n ungi y growing ig lustm in its lol soil n nturlly o-ourring AM ungi. Expt I xmin myorrhizl rsponss to n nrihmnt t th thr sits, Expt II xmin myorrhizl rspons to shing t th thr sits, n Expt III xmin th intrtiv ts o nutrint nrihmnt n shing t singl sit (Konz). Soils rom Konz n Frmi r rltivly mor -limit thn -limit, whrs soil rom Cr Crk is -rih n -limit (Johnson t l., ). Thus, th Lw o th Minimum prits mutulisti myorrhizs t Konz n Frmi n ommnsl myorrhizs t Cr Crk. I ths pritions r support, thn th Lw o th Minimum my usul gui to mng myorrhizs to inrs rop yil in griultur, rstor osystm untions, n mnipult C-squstrtion in myorrhizl hyph. Mtrils n Mthos Dsign o Expt I: ross-sit nutrint nrihmnt xprimnt Rhizoms o lol otyps o ig lustm (Anropogon grrii Vitmn) wr ollt rom Konz riri Biologil Sttion (Konz), Frmi turl Environmntl Rsrh rk (Frmi), n Cr Crk Eosystm Sin Rsrv (Cr Crk) in Frury whn th grsss wr ormnt. Rhizoms wr Ó Th Authors w hytologist Ó w hytologist Trust

3 w hytologist Rsrh gntly wsh to rmov soil, roots wr trimm to. m n rhizoms wr stor in ol, moist sn. In th spring, ll roots wr rmov rom h rhizom. Rhizom lngths wr msur n 8 rhizoms o similr siz rom h sit wr slt n plnt in thir orrsponing soil. Rhizom siz vri mong sits, rhizoms rom Konz (mn siz. mm 9. mm) wr signiintly smllr thn thos rom Cr Crk (mn siz. mm 9. mm) n Frmi (mn siz.9 mm 9. mm). Soil ws ollt rom h sit, stm-psturiz t 8 C or h, n us to ill 8 plsti pots ( m wi 9 m tll) with kg soil in h pot. Hl o th pots rom h sit wr mintin s nonmyorrhizl (M) trtmnts (psturiz soil) n th rmining hl wr inoult with ommunitis o AM ungi n othr soil orgnisms y pling g o living soil rom thir orrsponing sit irtly low h rhizom uring plnting. All pots wr mn with ml o nonstril soil sivt rom th orrsponing sit prpr y lning soil : wtr in : rtio n pssing th slurry through -lm siv (Johnson t l., ). Four rtilizr trtmnts wr stlish in h o th thr xprimntl systms n h trtmnt ws rplit six tims with or without AM ungi or totl o pots. At Konz n Frmi th trtmnts wr: nrihmnt, nrihmnt, oth n, n no rtilizr. hosphorus ( ml o lgg O : lgg ) ws ppli on t th ginning o th xprimnt. itrogn ( ml o. lgg H O :. lgg ) ws ppli t th ginning o th xprimnt n on vry wk or wk. rvious xprimnts hv shown tht nrihmnt os not inlun AM strutur or untion in -rih Cr Crk soil (Johnson, 99), so in tht systm, w stui n grint inst o n n toril sign. Cr Crk soil ws supplmnt with ml o on o our H O trtmnts:, nonmn ontrol;,. lgg ;,. lgg ;,.9 lgg t th ginning o th xprimnt n vry wk thrtr or wk. Th trtmnt ws quivlnt to il pplition rt o. g m ovr growing sson (i.. th wk o this stuy). At this pplition rt th plnt is xprining n supply rt t lvls typilly nountr in tllgrss priri osystms ovr growing sson n inlus minrliztion s wll s rom ry position sours (Sstt t l., 99). Th n pplition lvls rprsnt ition rts o n 7. g m, n ouling n tripling o typil supply rts, rsptivly. Dsign o Expt II: ross-sit sh xprimnt Ss rom lol ig lustm otyps rom Cr Crk, Frmi n Konz wr grmint n --ol slings wr trnsplnt into plsti pots ill with kg o psturiz soils rom th thr priris. For Expts II n III, w us slings grmint rom lolly ollt s rthr thn rhizoms to xpit th xprimntl st-up. AM n M pots rom th thr sits wr prpr s in Expt I n soil sivt ws s sri ov. Thr sh trtmnts (%, % n % light rution) wr stlish or h o th thr sits, h trtmnt ws rplit six tims with or without AM ungi or totl o Ó Th Authors w hytologist Ó w hytologist Trust 8 pots. Sh trtmnts wr stlish y hring lk polythyln sh loth (shlothstor.om) to woon rms (. m wi 9. m p 9. m tll). Frms with no sh loth wr inlu s mint ontrols. Dsign o Expt III: Konz nutrint 9 sh xprimnt Ss rom lol ig lustm otyps rom Konz wr grmint n --ol slings wr trnsplnt into pots n ill with kg o psturiz soil rom Konz. AM n M pots rom Konz wr prpr n soil sivt ws s sri ov. Four rtilizr trtmnts ( nrihmnt, nrihmnt, oth n, n no rtilizr) wr stlish s sri in Expt I. Two sh trtmnts (% n % light rution) wr stlish s sri in Expt II. Eh trtmnt ws rplit six tims with or without AM ungi or totl o 9 pots. Glsshous onitions n myorrhizl nlysis All xprimnts wr onut in glsshouss t Knss Stt Univrsity with tmprtur rnging rom to C, n th photosynthtilly tiv rition in mint light rnging rom 8 to 7 lmol m s. lnts wr hrvst tr wk s shoots wr oming snsnt. Thr ws no inition tht plnts wr pot-oun t th trmintion o ths xprimnts. ots wr not nsly ill with root systms n root growth i not ppr to rstrit y lk o vill sp in ny trtmnt. Roots wr wsh r o soil, shoots n roots wr ovn ri or 7 h t C n thn wigh. Susmpls o roots wr stin in trypn lu (Kosk & Gmm, 989) n AM oloniztion ws msur (MGonigl t l., 99). Extrnl AM hyph ws xtrt rom g o soil n quntii y th grilin intrpt mtho (Millr t l., 99). Cron ssimiltion: Expt II hotosynthti rts o intt lvs still tth to th plnt wr msur using LI- portl photosynthsis systm (LI-COR, Linoln, E, USA). On ully xpn l ws msur or ll plnts t wk whn plnts wr tivly growing. All msurmnts wr rri out uring miy (: h to : h ntrl ylight tim (CDT)) unr ull sun onitions. During th msurmnts th ir rltiv humiity ws. 7%, th tmprtur insi th l hmr ws mintin twn n 8 C, n th mint CO onntrtion ws 8 lmol mol. At msurmnt, th portion o th l nlos in th gs xhng uvtt ws smpl or totl l r (l lngth 9 l with). Soil n nutrint nlyss Frshly ollt soil smpls rom h sit wr nlyz or ph, orgni mttr, xtrtl inorgni (H + - n O ) n vill (Bry tst ); inorgni n vill wr lso msur rom th pots t th n o th xprimnts. Soil orgni mttr ws trmin y irt omustion, soil w hytologist ()

4 Rsrh w hytologist ph ws msur rom : (s on wight) soil/wtr pst. Inorgni ws xtrt using M l KCl n nlyz using mium rution/olorimtry. Knss Stt Univrsity Soil Tsting Lortory (Mnhttn, KS, USA) onut ll o th soil nlyss. W us Korslmn & Mulmn (99) thrshols o plnt tissu : rtios s n initor o rltiv n vilility t th thr sits n ssum tht -limit plnts hv tissu : <, -limit plnts hv tissu : >, n plnts with : rtios twn n r ithr not limit y ithr rsour or r o-limit y n. This : initor o nutrint limittion ws nlyz or Expts II n III ut not or Expt I us it ws initit with rhizoms o slightly irnt sizs whih inlun th inl : rtios o th plnts t hrvst. lnt shoots wr ri, groun through -lm msh, n igst with suluri i n hyrogn proxi. hosphorus onntrtion o th igst ws trmin using th molyt-lu mtho (Murphy & Rily, 9), n onntrtion ws trmin y Kjlhl mtho with rpi-low uto-nlyzr. Sttistil nlysis Myorrhizl growth rspons ws lult s simpl rspons rtio s sri in Johnson (): MGR = log (AM/M), whr AM ws th totl ry wight o myorrhizl plnts n M ws mn DW o nonmyorrhizl ontrol trtmnt unr th sm nutrint onitions (n = ). Dt wr nlyz with JM (SAS, ) using AOVA with irnt tors or th irnt xprimntl systms. In Expt I, th Cr Crk systm us two-wy AOVA with myorrhizs n s tors n th Konz n Frmi systms us thr-wy AOVA with myorrhizs, n s tors. Expt II us two-wy AOVA with myorrhizs n sh s tors in ll thr systms. Expt III us our-wy AOVA with myorrhizs, sh, n s tors in th Konz systm. Following AOVA, post ho omprisons o th mns wr lult using Tuky s HSD tst (.). Rsults Assssmnt o soil rtility n nutrint limittion Soil txtur vris ross th thr sits with th orsst (sny) soils t Cr Crk n th inst (lyy) soils t Konz (Tl ). Cr Crk soil ontin signiintly mor vill O, lss minrl (H + O ), lss orgni mttr, n lowr ph ompr to soils rom th othr sits (Tl ). During th ours o Expt II, th minrl onntrtion o Frmi n Cr Crk soil ws ru y > 9% whrs minrl in Konz soil rs y only %. By ontrst, th onntrtion o Konz soil ws ru y 7% whrs in Frmi n Cr Crk soils it ws ru y < 8% (Tl ). Tissu : rtios rom Expt II init tht rgrlss o light trtmnt, M plnts rom Frmi n Konz wr -limit (>> ) whrs M Cr Crk plnts wr -limit (<< ). Furthrmor, myorrhizs limint limittion o Frmi n Konz plnts ut thy i not limint limittion in Cr Crk plnts (Fig. ). Tissu : rtios rom Expt III lso init tht t Konz, unrtiliz M plnts wr strongly -limit n ing myorrhizs limint this limittion (Fig. ). In Expt III, rtiliztion with or with oth n gnrt -limit Konz plnts with : rtios s low s Cr Crk plnts in Expt II (Fig.,). This ourr in oth AM n M plnts n rsult rom highr tissu not us o lowr tissu (Supporting Inormtion Fig. S). Expt I: ross-sit nutrint nrihmnt xprimnt In unrtiliz Cr Crk soil, AM n M plnts wr similr in siz ut nrihmnt us M plnts to lrgr thn AM plnts (Fig., Tl ). In Frmi n Konz soils, Tl Soil proprtis o th thr stuy systms t th onst o Expt II n rom th pots tr ompltion o th xprimnt Soil or Expt II Soil rom pots tr Expt II Sit lotion Soil txtur ph Orgni mttr (%) Initil vill O - (mg kg ) Initil vill H + O (mg kg ) Finl vill O - (mg kg ) Finl vill H + O (mg kg ) Δ % Δ % Cr Crk Eosystm Sin Rsrv, Minnsot Frmi tionl Environmntl Rsrh rk, Illinois Konz riri Biologil Sttion, Knss Sny lom. (.). (.). (.) 8.7 (.). (.). (.).8 9. Silt lom.9 (.). (.). (.) 9. (.) 9.9 (.). (.) Silty ly lom. (.8).7 (.) 7. (.). (.) 7. (.).7 (.9) 7..8 Δ % n % init th hng rom th ginning to th n o th xprimnt. Dt r mns with SE in prnthss. Vlus within th sm olumn with irnt lttrs ir signiintly rom h othr oring to Tuky HSD tsts. w hytologist () Ó Th Authors w hytologist Ó w hytologist Trust

5 w hytologist Rsrh Tissu : Tissu : () Cr Crk () Frmi Konz Cr Crk Frmi Konz AM plnts wr lwys signiintly lrgr thn M plnts xpt or plnts grown in -rtiliz Konz soil (Fig. ). In Frmi n Konz soils, inrs th iomss o AM plnts ut not M plnts whrs nrihmnt inrs th iomss o M plnts ut not AM plnts (Fig. ). Unrtiliz Cr Crk plnts h signiintly lss AM root oloniztion n lss xtrnl AM hyph ompr to unrtiliz Frmi n Konz plnts (Fig.,). Frtiliztion o Frmi n Konz plnts with ru intrnl root oloniztion n xtrnl hyph, whrs rtiliztion with inrs ths ungl struturs (Fig.,). By ontrst, rtiliztion o Cr Crk soil ru intrnl root oloniztion n h littl inlun on xtrnl AM hyph. Th MGR o Cr Crk plnts ws signiintly lowr thn th MGR o plnts t th othr sits (Fig. ). itrogn rtiliztion ru MGR o Cr Crk plnts n rtiliztion strongly ru MGR o Frmi n Konz plnts (Fig. ). Aross ll trtmnts, th mount o AM ungi insi n outsi plnt roots ws positivly orrlt with MGR o plnts (Fig.,). Expt II: ross-sit sh xprimnt Sh signiintly ru CO ssimiltion t ll thr sits, n inoultion with AM ungi inrs CO ssimiltion t Fig. Tissu nitrogn : phosphorus ( : ) rtios or myorrhizl (opn rs) n nonmyorrhizl (hth rs) plnts in Expt II () n Expt III (). Light trtmnts r init s: sun symol, ull sunlight; lou symol, % rution in light. Frtilizr trtmnts in Expt III r init s:, no rtilizr;, nitrogn lon;, phosphorus lon;, nrihmnt with oth. Horizonl ott lins init thrshol : rtios or limittion (< ) n limittion (> ). Brs rprsnt mns, + SE (n = ). Brs with irnt lttrs ir signiintly rom h othr ( <.). Ó Th Authors w hytologist Ó w hytologist Trust () Extrnl hyph MGR (m g soil ) Root oloniz on(%) Totl plnt mss (g) () () () h h i j Cr Crk Frmi Konz Frmi n Konz ut not t Cr Crk (Fig., Tl ). lnt iomss ws signiintly ru in th % sh trtmnt t ll sits (Fig. ). As in th prvious xprimnt, Cr Crk plnts h signiintly lss myorrhizl oloniztion n orm wr xtrnl hyph ompr to Frmi n Konz plnts (Fig.,). Sh signiintly ru root oloniztion t ll Fig. lnt n ungl rsponss to nutrint nrihmnt in Expt I: totl ry wight o myorrhizl (opn rs) n nonmyorrhizl (hth rs) plnts (); root oloniztion y rusulr myorrhizl (AM) ungi (); nsity o AM ungl hyph in th soil (); n myorrhizl growth rspons (MGR) o plnts (). itrogn trtmnts in th Cr Crk systm (grn rs) r init s:, no supplmntry rtilizr;, n or low, mium n high lvls o, rsptivly. Trtmnts in th Frmi (lu rs) n Konz (orng rs) systms r init s:, no rtilizr;, nitrogn lon;, phosphorus lon;, nrihmnt with oth. Brs rprsnt mns, + SE (n = ). Brs with irnt lttrs ir signiintly rom h othr ( <.). g w hytologist ()

6 Rsrh w hytologist Tl Expt I nlysis o vrin Sit Rspons itrogn hosphorus Myorrhizs 9 9 M 9 M Cr 8 Totl plnt ry mss 9.*** 89.***.*** AM root oloniztion 8.*** Extrnl AM hyph. MGR.*** Frmi 8 Totl plnt ry mss.*** 7.9*** 79.***.9***.8 8.7*** AM root oloniztion.**.8*** 9.** Extrnl AM hyph..**. MGR..***.9 Konz 8 Totl plnt ry mss.*** 7.*** 89.9***..** 8.9*** AM root oloniztion.**.8***. Extrnl AM hyph.7** 87.7***. MGR..9***. F-rtios rom two-wy (Cr Crk) n thr-wy (Frmi n Konz) AOVA or totl plnt mss, rusulr myorrhizl (AM) root oloniztion, xtrnl hyph, n myorrhizl growth rspons (MGR). oninoult plnts wr not inlu in th nlysis o AM ungl rsponss. Signiint min ts n intrtions r init: *,.; **,.; ***,.. () () 8 8 () () MGR MGR () () 8 8 Root oloniz on(%) Extrnl hyph (m g soil ) Fig. Rltionships twn myorrhizl growth rspons (MGR) n rusulr myorrhizl (AM) root oloniztion n xtrnl hyph or Expt I (, ), Expt II (, ) n Expt III (, ). Colors init th irnt sits: Cr Crk (grn), Frmi (lu) n Konz (orng) in Expts I n II. Lttrs init rtilizr trtmnts in Expt I n III:, no rtilizr;, nitrogn lon;, phosphorus lon;, nrihmnt with oth. Soli irls, hl soli, n opn irls rprsnt % sh, % sh, n ull sunlight, rsptivly, in Expt II (, ). Orng lttrs, plnts grown in th ull sun; gry lttrs, plnts grown in th sh Expt III (, ). thr sits; n it tn to ru xtrnl hyph, ut this ws only signiint t Konz. lnt MGR ir signiintly mong sits; it ws highst t Konz n lowst t Cr Crk (Fig. ). Th % sh trtmnt signiintly ru MGR w hytologist () o Konz n Frmi plnts ut it h no inlun on MGR o Cr Crk plnts (Fig. ). Th mount o AM ungi insi n outsi plnt roots ws positivly orrlt with MGR o plnts in th Frmi n Konz systms ut not in th Cr Ó Th Authors w hytologist Ó w hytologist Trust

7 w hytologist Rsrh 7 hotosynth rt μmol (CO ) m s () () () Cr Crk Frmi Konz Tl Expt II nlysis o vrin Sit Rspons Light Myorrhizs L 9 M Cr Totl plnt ry mss.8***.. 8 CO Assimiltion rt 7.7**.8. 7 AM root oloniztion.** 8 Extrnl AM hyph.7 8 MGR. Frmi Totl plnt ry mss 7.***.7*** 7.*** 8 CO Assimiltion rt.7** 7.*** 8.9** 8 AM root oloniztion.7** 8 Extrnl AM hyph. 8 MGR.9*** Konz Totl plnt ry mss 8.7*** 8.*** 9.8*** 8 CO Assimiltion rt 9.9** 7.***.** 8 AM root oloniztion 8.8*** 8 Extrnl AM hyph.* 8 MGR 77.*** F-rtios rom two-wy AOVA or totl plnt mss, rusulr myorrhizl (AM) root oloniztion, xtrnl hyph, n myorrhizl growth rspons (MGR). oninoult plnts wr not inlu in th nlysis o AM ungl rsponss. Signiint min ts n intrtions r init: *,.; **,.; ***,.. rgims (Fig. 7,). Both sh n rtilizr ru MGR, n sh in omintion with nrihmnt gnrt myorrhizl inu plnt growth prssion (Fig. 7). Th mount o AM ungi insi n outsi plnt roots ws positivly orrlt with MGR o plnts (Fig. ). lnts with tissu : < (i.. - limit) h MGR <, whrs thos with : > (i.. - limit) h MGR >. (Fig. ). Myorrhizl on-myorrhizl Fig. Cron ssimiltion rt msur in Expt II in -wk-ol plnts growing in () Cr Crk (), Frmi () n Konz () soils with n without myorrhizs. Light trtmnts r init s: sun symol, ull sunlight; split sun/lou, % rution in light; lou symol, % rution in light. Brs rprsnt mns, + SE (n = ). Brs with irnt lttrs ir signiintly rom h othr ( <.). Crk systm (Fig.,). lnts with tissu : < h MGR nr zro, whrs thos with : > h MGR >. (Fig. ). Expt III: Konz nutrint 9 light xprimnt As in th prvious xprimnts, Konz M plnts rly surviv without nrihmnt (Figs,, 7). Sh signiintly ru plnt iomss ross ll th nutrint trtmnts (Fig. 7, Tl ). In ull sun, nrihmnt inrs th iomss o AM plnts n nrihmnt n ul n nrihmnt inrs th iomss o M plnts (Fig. 7). In ull sun, nrihmnt lon inrs root oloniztion, whrs in omintion with sh, rtiliztion i not inlun intrnl AM oloniztion or xtrnl hyph (Fig. 7,). hosphorus rtilizr ru intrnl oloniztion n xtrnl hyph unr oth light Ó Th Authors w hytologist Ó w hytologist Trust Disussion Aoring to th Lw o th Minimum, plnt growth is ontroll y th rsour tht is most limit in supply (von Liig, 8). This lw is lrly n ovrsimpliition o rlity us plnts r gnrlly o-limit y multipl rsours (Hrpol t l., ); singl rsour my most limiting t ny on momnt ut th intity o tht rsour is likly to hng through th growing sson or vn through singl y (Frrior t l., ). vrthlss, th Lw o th Minimum is ntrl tnt o ologil stoihiomtry, whih is usul rmwork or onnting rsour supply n mn to pritions out myorrhizl untioning (Strnr & Elsr, ; Johnson, ). Myorrhizs hv n onsir ntur s rspons to th lw o th minimum us thy nhn plnt ss to limiting lowgroun rsours in pritl wy (R, 99). Arusulr myorrhizs hv long n rogniz or thir importn to plnt nutrition, ut thir rol in plnt nutrition hs n ontrovrsil (Smith & Smith, ). W tst th ilitis o intt myorrhizl systms to rmy nutrint limittion in thr nturl grsslns n show tht AM symiosis n ompltly limint limittion ut thy nnot mliort limittion (Fig. ). Myorrhizl phnotyps r mrgnt proprtis o th gnotyps o prtnring plnts n ungi n thir nvironmnt. Our w hytologist ()

8 8 Rsrh w hytologist () Extrnl hyph MGR (m g soil ) Root oloniz on(%) Totl plnt mss (g) () () () 8 Cr Crk Frmi Konz Fig. lnt n ungl rsponss to sh in Expt II: totl DW o myorrhizl (opn rs) n nonmyorrhizl (hth rs) plnts (); root oloniztion y rusulr myorrhizl (AM) ungi (); nsity o AM ungl hyph in th soil (); n myorrhizl growth rspons (MGR) o plnts (). Light trtmnts r init s: sun symol, ull sunlight; split sun/lou, % rution in light; lou symol, % rution in light. Brs rprsnt mns, + SE (n = ). Brs with irnt lttrs ir signiintly rom h othr ( <.). inings strongly support th hypothsis tht soil rtility is n importnt trminnt o myorrhizl phnotyp n tht mutulism is most likly in -limit soils n ommnslism n prsitism r most likly in -rih soil, spilly whn light is limit. As prit, ig lustm myorrhizs wr mutulisti t Frmi n Konz, th two -limit sits, n ommnsl t Cr Crk, th -rih sit (Figs, ). Furthrmor, rtiliztion o Frmi n Konz soil rmtilly ru MGR o w hytologist () MGR () () 8 8 Tissu : o Myorrhizl lnts Fig. Rltionships twn myorrhizl growth rspons (MGR) n tissu nitrogn: phosphorus ( : ) rtio o myorrhizl plnts or Expt II (), n Expt III (). Soli irls, hl soli n opn irls rprsnt % sh, % sh n ull sunlight, rsptivly (). Frtilizr trtmnts:, no rtilizr;, nitrogn lon;, phosphorus lon;, nrihmnt with oth (). ig lustm (Fig. ). Ths pttrns in MGR orrspon to rsour limittion s trmin y mn tissu : rtios (Fig. ). Mutulism ws osrv in plnts tht wr -limit or o-limit y n whrs ommnslism ws osrv in plnts tht wr strongly -limit (Fig. ). hosphorus rtiliztion gnrt ommnslism or prsitism o Konz plnts n ru tissu : low th thrshol or limittion n to th rng osrv in plnts grown in Cr Crk soil (Fig.,). Rsults o our stuis suggst tht tissu : is usul pritor o myorrhizl phnotyp. In vry s tht MGR ws high (mutulism), tissu : ws > suggsting o-limittion or limittion, n whn MGR ws nr zro or ngtiv (ommnsl or prsiti), tissu : ws <, low th thrshol or limittion (Korslmn & Mulmn, 99; Fig. ). Although tissu : rtio ws usul inx o nutrint limittion in our stuis o -month-ol plnts, ution is nssry whn using tissu : rtios or inrns out plnt n limittion. Th inx is likly to most urt whn stuying rltivly young plnts o uniorm g. Stuis suggst tht : rtios my not urt initors o plnt nutrint sttus in wtr-limit systms or in olr plnts tht hv squstr nutrints in thir tissus (G uswll, ). In suh ss, it is prrl to tt plnt nutrint limittion using rtiliztion xprimnts to rvl plnt iomss rsponss to nrihmnt o irnt nutrints. Ó Th Authors w hytologist Ó w hytologist Trust

9 w hytologist Rsrh 9 () Extrnl hyph MGR (m g soil ) Root oloniz on(%) Totl plnt mss (g) () () () 8 8 Fig. 7 lnt n ungl rsponss to simultnous rtiliztion n sh in Expt III: totl DW o myorrhizl (opn rs) n nonmyorrhizl (hth rs) plnts (); root oloniztion y rusulr myorrhizl (AM) ungi (); nsity o AM ungl hyph in th soil (); n myorrhizl growth rspons (MGR) o plnts (). Light trtmnts r init s: sun symol, ull sunlight; lou symol, % rution in light. Frtilizr trtmnts:, no rtilizr;, nitrogn lon;, phosphorus lon;, nrihmnt with oth. Brs rprsnt mns, + SE (n = ). Brs with irnt lttrs ir signiintly rom h othr ( <.). Our inings show tht light vilility ws n importnt trminnt o myorrhizl phnotyp in Frmi n Konz soils, ut not in -rih Cr Crk soil (Fig. ). Simultnous sh n rtilizr in th Konz systm (Expt III) gnrt rmrkl rng o myorrhizl phnotyps, rom mutulism to prsitism (Figs, 7). Sh ru th nt CO ssimiltion rt (Fig. ) n oth sh n nrihmnt ru ungl Ó Th Authors w hytologist Ó w hytologist Trust iomss, prsumly us o ru C-or- tr. Both sh n rtilizr ru MGR y shiting th rltiv ln o ommoitis: sh inrs th rltiv ost o C n rtilizr rs th rltiv nit o myorrhizl uptk. Ths rsults r prsimonious with th isovry tht riprol xhng o C n ontrol myorrhizl ooprtion (Hmmr t l., ; Kirs t l., ). In ontrst to, w osrv littl vin to suggst tht C-or- tr irtly nors myorrhizl ooprtion y linking rsour tr to iomss gin y oth plnt n ungl prtnrs. Othr stuis hv rh th sm onlusion (Corr^ t l., ). Whn is in limit supply, AM ungi r unlikly to rls it to thir host plnts until thir own ns hv n mt (Hog & Storr, ). In this rgr, it is likly tht plnts, AM ungi n othr soil miroorgnisms ll ompt or in soils with vry low vilility. In Expt II, % rution o light ru MGR, ut % rution only ru MGR in Konz soil; it tully inrs MGR in Frmi soil. Ths inings suggst tht th photosynthti pity o ig lustm must sustntilly ru to inu limittion o C or symioti tr with AM ungi in limit soils. This grs with stuy o C ugts in lgum myorrhizs (Kshuk t l., 9), n suggsts tht th C ost o AM ungi is sustntilly lowr thn th photosynthti pity o thir host plnts. Cool-sson grsss with C photosynthti pthwy r xpt to inhrntly mor C-limit thn C grsss, suh s ig lustm in our xprimnt, n this physiologil onstrint hlps xplin why C grsss gnrlly hv muh lowr pnny on myorrhizs (Wilson & Hrtntt, 998). With mpl light, ig lustm hs n shown to inrs its photosynthti pity to stisy th C sink strngth o AM ungl symionts (Millr t l., ). But, without suiint light, w hv shown tht myorrhizl tring prtnrships om C limiting n oth ungl iomss n MGR lin. Othrs hv oun vin tht sh rus C supply to AM ungi n rus AM ungl iomss n MGR (Grhm t l., 98; Olsson t l., ; Shi t l., ). Frtiliztion with n ithr rs or inrs th unn o AM ungi n plnt MGR s sn in Expt I (Fig. ) n in il stuis (Johnson t l., ). itrogn nrihmnt o - rih Cr Crk soil ru AM oloniztion n MGR o plnts. By ontrst, nrihmnt inrs th unn o AM ungi n plnt MGR in Frmi n Konz soils. Th Funtionl Equilirium mol hlps xplin this rsult (Johnson t l., ). itrogn nrihmnt o -rih soils my xpt to inu plnts to just thir iomss llotion in vor o shoots n wy rom roots n myorrhizs. On th othr hn, nrihmnt o -limit soils will xrt limittion, inrs th vlu o AM symioss, n inu plnts to inrs llotion lowgroun to roots n AM ungi. This prsptiv my hlp ronil inonsistnis in th litrtur. Rynols t l. () xmin th ts o our irnt AM ungl spis on iv irnt plnt spis ut i not osrv singl s in whih th ungus inrs th nutrition n iomss o thir host plnt. By ontrst, Tu t l. () oun tht AM ungi signiintly inrs th uptk n iomss gin o Avn tu. Soil : stoihiomtry is th ky to ths w hytologist ()

10 Rsrh w hytologist Tl Expt III nlysis o vrin Sour o vrition Rspons itrogn hosphorus Light Myorrhizs 9 9 L 9 L 9 M 9 M L9 M 9 Totl plnt ry mss 8.7** 7.*** 99.***.***..*.. 8.7***.*** 7 AM oloniztion. 7.***.***.*.. 7 Extrnl AM hyph.7.*** 8.***... 7 MGR 8.9** 99*** ***... F-rtios rom our-wy AOVA or totl plnt mss, rusulr myorrhizl (AM) root oloniztion, xtrnl hyph, n myorrhizl growth rspons (MGR) rom plnts grown in th Konz xprimntl systm. oninoult plnts wr not inlu in th nlysis o AM ungl rsponss. Signiint min ts n intrtions r init: *,.; **,.; ***,.. ontritory inings. Rynols t l. () purposly us - rih soil; onsquntly, similr to Cr Crk, nrihmnt gnrt ommnsl or vn prsiti myorrhizl phnotyps. By ontrst, th soil us y Tu t l. () ws o-limit y oth n (C. Tu, prs. omm.); n oringly, nrihmnt inrs th rltiv nit o myorrhizl uptk n inrs MGR, just s w osrv t Frmi n Konz. Th usulnss o th Lw o th Minimum or priting myorrhizl untion osn t only prtin to n. It is wll known tht AM ungi n mliort plnt limittion o othr rsours suh s wtr n zin (Thompson, 99; Ryn & Angus, ; Aug t l., ). Improv wtr rltions oul wll th most importnt untion o myorrhizs in th sny rought-pron soil t Cr Crk, ut our xprimnts woul nvr tt this us our xprimntl plnts wr nvr xpos to rought. Myorrhizs r known to inrs plnt uptk o immoil mironutrints suh s zin, oppr n mngns, n th xtnt to whih thy improv plnt nutrition is inlun y th rltiv unn o n n othr mironutrints (Liu t l., ). Rsrhrs stuying rtiliztion trils shoul wr o th potntil or hin mironutrints to inlun thir rsults (Hjmn t l., 9). For xmpl, molynum, ritil o-tor in nitrogns, is otn limiting tor or -ixing symioss n it is ommon ontminnt o rtilizr (Brron t l., 9). Rsour limittion n powrul rivr o ommunity omposition n gnti pttion within popultions. turl ommunitis o orgnisms r likly to shit in omposition towrs stoihiomtri ln with thir rsour supply (Sh t l., ; Dngr t l., 8). Whn soil rsours r in limit supply, plnt spis tht orm nutritionl symioss r xpt to omint th ommunity, ut rtiliztion will limint th nits o ths symioss, n ovr tim, plnt spis tht invst lss in uslss nutritionl symioss will hv omptitiv vntg n om to omint rtiliz ommunitis. W liv tht this phnomnon my riving th shits in th spis omposition o grssln plnts n ssoit AM ungi tht our in long-trm rtiliztion stuis (Johnson, 99; Egrton-Wrurton t l., 7; Johnson t l., 8; Liu t l., ). W hv oun strong vin tht nutrint limittion my lso n volutionry or tht gnrts sit-spii opttion mong plnt gnotyps n AM ungi. A riprol inoultion xprimnt lrly show tht lol otyps o ig w hytologist () lustm r pt to thir lol soil n inignous AM ungl ommunitis suh tht myorrhizl xhng is mximiz or th most limiting rsour ( t Cr Crk n t Frmi n Konz) (Johnson t l., ; Ji t l., ). Myorrhizl phnotyps r shp y omplx intrtions mong mny ioti n ioti tors (wshm t l., 99; Johnson t l., 997). Th importnt insight rom this work is tht th Lw o th Minimum provis hypothsis-gnrting rmwork tht hlps intiy th ritil tors ontrolling myorrhizl untion in irnt systms. Arusulr myorrhizs r oun ross rmrkl ivrsity o osystms. Crtinly, irnt tors shoul xpt to limit thir untion in systms s irnt s srts n tropil rin orsts. Aurt intiition o ths ritil (limiting) tors is irst stp towrs vloping tiv mngmnt strtgis to mximiz AM nits in griultur, hortiultur orstry, n rstortion. For xmpl, knowing th thrshol tissu : rtio or mutulism will hlp intiy th pproprit rtiliztion shms to mximiz myorrhizl nits n minimiz th us o xpnsiv rtilizrs. Also, this knowlg oul hlp mng AM ungi or thir rol in squstring C in th soil. Aition o to -limit soils oul inrs AM ungl iomss n its potntil to inrs lowgroun C sinks, whrs nrihmnt o -rih soils will hv th opposit t n ru AM ungl iomss. Aknowlgmnts This work ws un y th tionl Sin Fountion DEB-, DEB-87, n IB-98 (Konz riri LTER). R.M.M. s prtiiption ws in prt un y th US Dprtmnt o Enrgy, Oi o Biologil n Environmntl Rsrh unr ontrt DE-AC-CH7. Thnks to Frmi L, Cr Crk, n Konz riri or prmission to ollt rom th sits, n Susn Kirt, Troy Milk n Ay Kul or ssistn with olltion o soil n rhizoms. Th us o tr, prout or irm nms is or inormtion purposs n os not onstitut norsmnt y th US Govrnmnt. Rrns Aug RM, Tolr HD, Sxton AM.. Arusulr myorrhizl symiosis ltrs stomtl onutn o host plnts mor unr rought thn unr mply Ó Th Authors w hytologist Ó w hytologist Trust

11 w hytologist Rsrh wtr onitions: mt-nlysis. Myorrhi. oi:.7/ s Brron AR, Wurzurgr, Bllngr J, Wright SJ, Krpil AML, Hin LO. 9. Molynum limittion o symioti nitrogn ixtion in tropil orst soil. tur Gosin :. Blkwll J hysil mthos or trmintion o hitin strutur n onormtion. In: Woo WA, Kllogg TS, s. Mthos in nzymology. w York, Y, USA: Ami rss,. Chpin FSI, Bloom AJ, Fil CB, Wring RH lnt rsponss to multipl nvironmntl tors. BioSin 7: 9 7. Corr^ A, Cruz C, rz-tin J, Frrol.. Shing light onto nutrint rsponss o rusulr myorhil plnts: nutrint intrtions my l to unprit outoms o th symiosis. lnt Sin : 9. Dngr M, Dursn T, Lus F, issr S, Lroix G. 8. Dos Liig s lw o th minimum sl up rom spis to ommunitis? Oikos 7: 7 7. Egrton-Wrurton L, Johnson C, Alln EB. 7. Myorrhizl ommunity ynmis ollowing nitrogn rtiliztion: ross-sit tst in iv grsslns. Eologil Monogrphs 77: 7. Frrior CE, Tilmn D, Dyzinski R, Rih B, Lvin SA, l SW.. Rsour limittion in omptitiv ontxt trmins omplx plnt rsponss to xprimntl rsour itions. Eology 9: 7. Fllum CR, Ghomo EW, Bstty Y, Chouhri S, Strhn GD, r E, Kirs ET, Buking H.. Cron vilility triggrs ungl nitrogn uptk n trnsport in rusulr myorrhizl symiosis. roings o th tionl Amy o Sins, USA 9: 7. Gorg E, Mrshnr H, Jkosn I. 99. Rol o rusulr myorrhizl ungi in uptk o phosphorus n nitrogn rom soil. Critil Rviws in Biothnology : 7 7. Grhm JH, Lonr RT, Mng JA. 98. Intrtion o light intnsity n soil tmprtur with phosphorus inhiition o vsiulr rusulr myorrhiz ormtion. w hytologist 9: 8 9. G uswll S.. : rtios in trrstril plnts: vrition n untionl signiin. w hytologist :. Hmmr EC, llon J, Hkn W, Olsson A.. Tit or tt? A myorrhizl ungus umults phosphorus unr low plnt ron vilility. FEMS Miroiology Eology 7:. Hrpol WS, gi JT, Clln EE, Sloom EW, Borr ET, Brkn MES, Elsr JJ, Grunr DS, Hillrn H, Shurin JB t l.. utrint o-limittion o primry prour ommunitis. Eology Lttrs : 8 8. Hjmn M, Szkov J, Shllrg J, Srk, Tlustos. 9. Th Rngn Grssln Exprimnt: soil ontmintion y tr lmnts tr yrs o C,,, n K rtilisr pplition. utrint Cyling in Agroosystms 8: 9. Hog A, Fittr AH.. Sustntil nitrogn quisition y rusulr myorrhizl ungi rom orgni mtril hs implitions or yling. roings o th tionl Amy o Sins, USA 7: Hog A, Storr K.. Arusulr myorrhizs n nitrogn: implitions or iniviul plnts through osystms. lnt n Soil. oi:.7/ s---. Hoksm JD, Chuhry VB, Ghring CA, Johnson C, Krst J, Koi R, ringl A, Zinski C, Bvr JD, Moor J t l.. A mt-nlysis o ontxt-pnny in plnt rspons to inoultion with myorrhizl ungi. Eology Lttrs : 9 7. Ji B, Ghring CA, Wilson GWT, Millr RM, Johnson C.. ttrns o ivrsity n pttion in ungl root symionts rom thr priri grsslns. Molulr Eology : Johnson C. 99. Cn rtiliztion o soil slt lss mutulisti myorrhiz? Eologil Applitions : Johnson C.. Tnsly Rviw: rsour stoihiomtry luits th strutur n untion o rusulr myorrhizs ross sls. w hytologist 8: 7. Johnson C, Grhm JH, Smith FA Funtioning o myorrhizl ssoitions long th mutulism-prsitism ontinuum. w hytologist : 7 8. Johnson C, Rowln DL, Corkii L, Alln EB. 8. lnt winnrs n losrs uring grssln utrophition ir in iomss llotion n myorrhizs. Eology 89: Johnson C, Rowln DL, Corkii L, Egrton-Wrurton L, Alln EB.. itrogn nrihmnt ltrs myorrhizl llotion t iv msi to smiri grsslns. Eology 8: Johnson C, Wilson GWT, Bowkr MA, Wilson J, Millr RM.. Rsour limittion is rivr o lol pttion in myorrhizl symioss. roings o th tionl Amy o Sins, USA 7: Kshuk G, Kuypr TW, Llr A, Hungri M, Gillr KE. 9. Ar th rts o photosynthsis stimult y th ron sink strngth o rhizoil n rusulr myorrhizl symioss? Soil Biology n Biohmistry :. Ky J, Hrt SC Comptition or nitrogn twn plnts n soil miroorgnisms. Trns in Eology n Evolution : 9. Kirs ET, Duhml M, Bstty Y, Mnsh JA, Frnkn O, Vrruggn E, Fllum CR, Kowlhuk GA, Hrt MM, Bgo A t l.. Riprol rwrs stiliz ooprtion in th myorrhizl symiosis. Sin : Korslmn W, Mulmn AFM. 99. Th vgttion : rtio: nw tool to tt th ntur o nutrint limittion. Journl o Appli Eology :. Koi R, Elliott G Cost, nit n iiny o th vsiulr-rusulr myorrhizl symiosis. Funtionl Eology :. Koi RT. 99. Tnsly Rviw o. 9 utrint supply, nutrint mn n plnt rspons to myorrhizl intion. w hytologist 7: 8. Kosk RE, Gmm J A moii prour or stining roots to tt myorrhizs. Myologil Rsrh 9: Ligh J, Hog A, Fittr AH. 8. Arusulr myorrhizl ungi n trnsr sustntil mounts o nitrogn to thir host plnt rom orgni mtril. w hytologist 8: von Liig JF. 8. Chmistry in its pplition to griultur n physiology. Lonon, UK: Tylor n Wlton. Liu A, Hml C, Hmilton RI, M BL, Smith DL.. Aquisition o Cu, Zn, Mn, n F y myorhizl miz (Z mys L.) grown in soil t irnt n mironutrint lvls. Myorrhiz 9:. Liu Y, Shi GX, Mo L, Chng G, Jing S, M X, An L, Du G, Johnson C, Fng H.. Dirt n inirt inluns o ight yrs o nitrogn n phosphorus rtiliztion on Glomromyot in n lpin mow osystm. w hytologist 9:. Mznourt C, Shwrtz MW.. A rsour rtio thory o ooprtion. Eology Lttrs : 9 9. MGonigl T, Millr MH, Evns DG, Firhil GL, Swn JA. 99. A nw mtho whih givs n ojtiv msur o oloniztion o roots y vsiulr-rusulr myorrhizl ungi. w hytologist : 9. Millr RM Th ology o vsiulr rusulr myorrhiz in grss- n shrulns. In: Sir GR,. Eophysiology o VA myorrhizl plnts. Bo Rton, FL, USA: CRC rss, 7. Millr RM, Millr S, Jstrow JD, Rivtt CB.. Myorrhizl mit ks inlun nt ron gin n nutrint uptk in Anropogon grrii. w hytologist : 9. Millr RM, Rinhrt DR, Jstrow JD. 99. Extrnl hyphl proution o vsiulr rusulr myorrhizl ungi in pstur n tllgrss priri ommunitis. Oologi :7. Mojo HS, Hnrix JW. 98. Th myorrhizl ungus Glomus mrorpum s us o too stunt iss. hytopthology 7: Moss B. 97. Avns in th stuy o vsiulr rusulr myorrhizs. Annul Rviw o hytopthology : 7 9. Murphy J, Rily J. 9. A moii singl solution mtho o th trmintion o phospht in nturl wtrs. Anlyti Chimi At 7:. wshm K, Fittr A, Wtkinson A. 99. Multi-untionlity n ioivrsity in rusulr myorrhizs. Trns in Eology n Evolution : 7. Olsson A, Rhm J, Alisghrz.. Cron ynmis in myorrhizl symioss is link to ron osts n phosphorus nits. FEMS Miroiology Eology 7:. rson J, Smith SE, Smith FA. 99. Et o photon irrin on th vlopmnt n tivity o VA myorrhizl intion in Allium porrum. Myologil Rsrh 9: 7 7. Ó Th Authors w hytologist Ó w hytologist Trust w hytologist ()

12 Rsrh w hytologist ng S, Eissnstt DM, Grhm JH, Willims K, Hog C. 99. Growth prssion in myorrhizl itrus t high-phosphorus supply. lnt hysiology : 7. vn r log RR, Bohm W, Kirkhm MB On th origin o th thory o minrl nutrition o plnts n th lw o th minimum. Soil Sin Soity o Amri Journl :. R DJ. 99. Myorrhizs in osystms ntur s rspons to th lw o th minimum. In: Hwksworth DL,. Frontirs in myology. Kw Surry, UK: CAB Intrntionl,. Rynols HL, Hrtly AE, Voglsng KM, Bvr JD, Shultz A.. Arusulr myorrhizl ungi o not nhn nitrogn quisition n growth o ol-il prnnils unr low nitrogn supply in glsshous ultur. w hytologist 7: Roinson D, Fittr AH Th mgnitu n ontrol o ron trnsr twn plnts link y ommon myorrhizl ntwork. Journl o Exprimntl Botny :9. Ryn MH, Angus JF.. Arusulr myorrhiz in wht n il p rops on low soil: inrs Zn-uptk ut no inrs in -uptk or yil. lnt n Soil : 9. SAS.. JM sttistil isovry sotwr. Cry, C, USA: SAS Institut In. Sh JD, Esplt JF, Klusmir CA, MGroy ME, Thoms SA, Zhng L.. A onptul rmwork or osystm stoihiomtry: lning rsour supply n mn. Oikos 9:. Sstt TR, Briggs JM, Gison DJ. 99. Controls o nitrogn limittion in tllgrss priri. Oologi 87: Shi GX, Liu Y, Johnson C, Olsson A, Mo L, Chng G, Jing S, An L, Du G, Fng H.. Intrtiv inlun o light intnsity n soil rtility on root-ssoit rusulr myorrhizl ungi. lnt n Soil 78: Smith SE, Smith FA.. Rols o rusulr myorrhizs in plnt nutrition n growth: nw prigms rom llulr to osystm sls. Annul Rviw o lnt Biology : 7. Strnr RW, Elsr JJ.. Eologil stoihiomtry: th iology o lmnts rom moluls to th iosphr. rinton, J, USA: Univrsity rss. Thompson J. 99. Inoultion with vsiulr-rusulr myorrhizl ungi rom ropp soil ovroms long-llow isorr o lins (Linum usittissimum L.) y improving n Zn uptk. Soil Biology & Biohmistry :. Tu C, Bookr FL, Wtson DM, Chn X, Ruty TW, Shi W, Hu S.. Myorrhizl mition o plnt quisition n rsiu omposition: impt o minrl inputs. Glol Chng Biology : Wilson GWT, Hrtntt DC Intrspii vrition in plnt rsponss to myorrhizl oloniztion in priri grsss n ors. Amrin Journl o Botny 8: Supporting Inormtion Aitionl supporting inormtion my oun in th onlin vrsion o this rtil. Fig. S rntg tissu n in Expt III (myorrhizl (AM) n nonmyorrhizl (M) plnts grown with light n rtilizr trtmnts). ls not: Wily Blkwll r not rsponsil or th ontnt or untionlity o ny supporting inormtion suppli y th uthors. Any quris (othr thn missing mtril) shoul irt to th w hytologist Cntrl Oi. w hytologist () Ó Th Authors w hytologist Ó w hytologist Trust