Geographical and plant genotype effects on the formation of arbuscular mycorrhiza in Avena sativa and Avena nuda at different soil depths

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1 Geogrphil nd plnt genotype effets on the formtion of rusulr myorrhiz in Aven stiv nd Aven nud t different soil depths Yng, F. Y., Li, G. Z., Zhng, D. E., Christie, P., Li, X. L., & Gi, J. P. (2010). Geogrphil nd plnt genotype effets on the formtion of rusulr myorrhiz in Aven stiv nd Aven nud t different soil depths. Biology nd Fertility of Soils, 46(5), DOI: /s Pulished in: Biology nd Fertility of Soils Queen's University Belfst - Reserh Portl: Link to pulition reord in Queen's University Belfst Reserh Portl Generl rights Copyright for the pulitions mde essile vi the Queen's University Belfst Reserh Portl is retined y the uthor(s) nd / or other opyright owners nd it is ondition of essing these pulitions tht users reognise nd ide y the legl requirements ssoited with these rights. Tke down poliy The Reserh Portl is Queen's institutionl repository tht provides ess to Queen's reserh output. Every effort hs een mde to ensure tht ontent in the Reserh Portl does not infringe ny person's rights, or pplile UK lws. If you disover ontent in the Reserh Portl tht you elieve rehes opyright or violtes ny lw, plese ontt openess@qu..uk. Downlod dte:15. Fe. 2017

2 Biol Fertil Soils (2010) 46: DOI /s ORIGINAL PAPER Geogrphil nd plnt genotype effets on the formtion of rusulr myorrhiz in Aven stiv nd Aven nud t different soil depths F. Y. Yng & G. Z. Li & D. E. Zhng & P. Christie & X. L. Li & J. P. Gi Reeived: 21 July 2009 /Revised: 3 Ferury 2010 /Aepted: 11 Ferury 2010 /Pulished online: 5 Mrh 2010 # Springer-Verlg 2010 Astrt We hve exmined the influene of host plnt genotype nd geogrphil hrters on the vertil distriution pttern of rusulr myorrhiz ssoited with Aven. The degree of oloniztion of ot roots t different soil depths (0 10, 10 20, 20 30, 30 40, m) ws ompred mong three hitts from lower to higher ltitude nd six different ultivrs in one speifi hitt. Altitude hd no impt on the perentge of root length olonized y myorrhiz. However, ots growing t the higher ltitudes formed more undnt rusules nd vesiles within their roots. Plnt genotype showed signifint influene on the perentge of root length olonized nd undne of rusules nd vesiles, nd F. Y. Yng nd G. Z. Li ontriuted eqully to this work. F. Y. Yng Deprtment of Grsslnd Siene, Chin Agriulturl University, Beijing , Chin G. Z. Li College of Grsslnd nd Environmentl Siene, Xinjing Agriulturl University, Ürümqi, Chin D. E. Zhng College of Prtulture, Gnsu Agriulturl University, Lnzhou, Chin P. Christie Agri-Environment Brnh, Agri-Food nd Biosienes Institute, Newforge Lne, Belfst BT9 5PX, UK P. Christie : X. L. Li : J. P. Gi (*) College of Nturl Resoures nd Environmentl Sienes, Chin Agriulturl University, Beijing , Chin e-mil: gijp@u.edu.n there ws muh greter oloniztion of nked ot thn of husk ot (ommon ot). The vertil distriution pttern of myorrhizl root length ws similr in terms of geogrphil nd genotypi spets, with the most extensive root oloniztion ourring in the topsoil nd deresing with inresing soil depth. However, the perentge of root length olonized y rusulr myorrhizl fungi (AMF) remined t out 20% oloniztion t depth of m. Intrrdil strutures lso showed deresing trend with inresing soil depth. The results suggest tht n AMF gene nk my persist in the susoil, nd this my filitte the eologil restortion of degrded griulturl res. Keywords Arusulr myorrhiz. Ot ultivrs. Vertil distriution. Altitude Introdution Ot (Aven) is extensively plnted s fodder rop on the vst rnges of northern nd northwestern Chin, espeilly in the lpine regions of the Qinghi Tietn Plteu (M nd Hn 2000) s its resistne to old nd rid onditions, nd its short growth periods re suited to lpine nd rid regions. Most of the ots re used for livestok feed. Ot eomes n importnt supplementry feed for grzing livestok when the nimls suffer from indequte nutrition during the long, hrsh winter seson under trditionl frming prties. The potentilly symioti reltionship etween host plnt roots nd rusulr myorrhizl fungi (AMF) n ontriute signifintly to plnt nutrition nd growth nd hs een shown to inrese the produtivity of vriety of gronomi rops (Smith nd Red 2008). Most studies hve

3 436 Biol Fertil Soils (2010) 46: shown positive effets of AMF on host plnt growth nd development under onditions of low soil fertility (Jeffries nd Rhodes 1987). Severl studies hve lso indited tht AMF n help plnts survive freezing nd drought onditions (Klironomos et l. 2001; Liu et l. 2007; Boomsm nd Vyn 2008). Therefore, AMF my mke n importnt ontriution to the produtivity of ots grown in Qinghi provine where the limte is hrterized y low tempertures nd rid onditions. However, informtion is lking on the myorrhizl sttus of ots in this region. It hs een well estlished tht the extent of oloniztion of plnt roots y AMF is influened y oth environmentl ftors (Smith nd Red 2008; vn der Heijden nd Snders 2002) nd host plnt genetis (Brker et l. 2002; Lindermn nd Dvis 2004). Plnt genotypes hve een shown to differ oth in their ility to form myorrhizs nd in the reltive enefit tht they derive from myorrhizl oloniztion (Smith nd Red 2008; Brker et l. 2002; Twry 2003). By ffeting temperture nd preipittion, ltitudinl grdients re importnt drivers of plnt miroe ssoitions (Väre et l. 1997; Ruotslinen et l. 2004; Zuek et l. 2009). However, few studies hve exmined simultneously host plnt genetis nd environment to determine their reltive influene on myorrhizl oloniztion (Gehring et l. 2006). To understnd the role of AMF in ot produtivity, it is importnt to understnd how AMF differ in their response to different environmentl onditions nd plnt genotypes. Some AMF quire nutrients djent to roots, while others forge further wy nd explore different soil volumes (Smith et l. 2000). This n led to inresed produtivity through the omplementry use of resoures. A similr phenomenon hs een oserved in plnts with different rooting depths. Host preferene nd host rnge re two funtionl trits tht re potentilly very importnt. However, most studies on myorrhizl oloniztion nd ommunity struture re generlly restrited to the min rooting zone (10 30 m soil depth) (Klironomos et l. 1997; Rillig et l. 2000; Oehl et l. 2005), nd few studies hve inluded the susoil (Kir et l. 1998; Neville et l. 2002; Rillig nd Field 2003). It follows tht we hve only very limited understnding of how rusulr myorrhizs respond s funtion of soil depth to different plnt ultivrs nd environmentl onditions. The present study ws onduted to exmine the level of AMF oloniztion of ot in three different hitts rnging from lower to higher ltitude. AMF oloniztion of six ot ultivrs ws lso surveyed t one speifi ltitude. Myorrhizl sttus (perentge of root length olonized, presene of rusules nd vesiles, spore density, nd AMF speies) were ssessed down the 0 50 m soil depth grdient. We hve lso ompred the oloniztion of roots s ffeted y ot genotype. Mterils nd methods Study sites nd host plnts The sites were seleted to provide trnset from lower to higher ltitude (1,600 to 3,100 m sl) nd re loted in Minhe, Hungzhong, nd Hiei ounties, respetively, of estern Qinghi provine ( N, E; Tle 1). All three sites hve the sme soil type nd texture, nmely Typi Clixeroll (USDA Soil Txonomy 1998) nd lom, respetively. The mngement of ll the fields exmined ws the sme nd followed onventionl prtie. The fields smpled hve no irrigtion systems nd routinely reeive kg N nd kg P h 1 yer 1 ; they re plowed to depth of up to m. Smple olletion Soil smples were tken t the grin-filling stge of the ots in August We estlished three rndom 30-m 2 smpling plots within n re of 500 m 2 t eh field site. In eh of the three replite plots per field site, five soil ores in digonl line were tken to depth of 50 m. The ores were seprted into the following depth inrements: 0 10, 10 20, 20 30, 30 40, nd m soil depth, nd the setions from the sme depth of the five ores of given plot were pooled nd nlyzed s single omposite smple. The smples were refully ground y hnd, thoroughly mixed, ir-dried, nd nlyzed for their soil ph (1:2.5 soil/wter), soil totl N (Kjeldhl method), ville P (Olsen nd Sommers 1982), nd orgni mtter ontent (Cmrdell et l. 2001) (Tles 2 nd 3). Assessment of AM oloniztion Roots seprted from ores were wshed refully with tp wter nd ut into segments out 1 m long. Aout 0.5 g of root segments were lered in 10% (w/v) KOH t 90 C in wter th for 60 min. After ooling, the root segments were wshed nd stined with 5% (w/v) Trypn lue (MGonigle et l. 1990). Thirty 1-m-long root segments were mounted on slides in polyvinyl lohol lti id glyerol solution (Koske nd Tessier 1983) nd exmined t mgnifition under Nikon YS100 mirosope. The perentge of root length olonized ws lulted ording to the method of Trouvelot et l. (1986). The oloniztion dt for speifi AM strutures re expressed s perentge of root length. Spore ounting nd identifition Spores nd spororps were extrted from 100 g ir-dried susmples of eh soil smple in triplite y wet sieving

4 Biol Fertil Soils (2010) 46: Tle 1 Desription of the three smpling sites in Qinghi provine Site Lotion Elevtion (m sl) Annul verge temperture ( C) Annul preipittion (mm) Soil totl N (%) Minhe N, E 1, Hungzhong N, E 2, Hiei N, E 3, followed y flottion entrifugtion in 50% surose (Dlpé 1993). The finest sieve used ws 38 µm. AM fungl spores were ounted on grid-ptterned dish under inoulr stereomirosope. The isolted spores of AMF were mounted on glss slides in polyvinyl-ltoglyerol (PVLG) or PVLG+Melzer s regent (1:1, v/v) nd then exmined mirosopilly nd identified ording to txonomi riteri (Shenk nd Péréz 1990) nd using informtion from the INVAM We site on the Internet ( nd the we pge of Arthur Shüßler on Glomeromyot phylogeny nd txonomy on the Internet ( shuessler/mphylo/). Dt nlysis Spore density ws expressed s numers of AM fungl spores per grm dried field soil. The dominnt speies were determined y the importne vlue, whih is the verge of speies frequeny nd reltive undne of prtiulr speies. SAS 8.2 softwre ws used to ondut ll sttistil nlyses. Signifine of differenes in myorrhizl oloniztion mong the smples from different soil depths t the three sites ws nlyzed using two-wy nlysis of vrine nd Dunn's multiple rnge test (three sites nd five soil depths) nd mong ultivr trnsets (six ultivrs nd five soil depths). Results There were no signifint differenes in the root AM oloniztion mong the three sites. However, ots growing t the higher ltitude (Hiei) hd signifintly greter undne of rusules nd vesiles (Fig. 1). The intrrdil strutures were most extensive in roots in the topsoil (mostly t 0 10 m nd some t m) nd showed deresing trend with inresing soil depth t ll three sites. However, there were some differenes in the proportions of rusules nd vesiles t different soil depths mong the sites. For exmple, root length with rusules in the top 10 m represented 80% of those in the entire Minhe soil profile, with orresponding vlues of 37% nd 41% of those t the Hungzhong nd Hiei profiles, respetively. The ot genotypes showed signifint influene on the myorrhizl root length nd undne of rusules nd vesiles. In generl, perentge of myorrhizl root length ws higher in nked thn in husk ot s determined. The Tle 2 Soil hemil properties t different soil depths t the three field sites Site Soil depth (m) Soil ph (in wter) Soil orgni mtter (g kg 1 ) Soil Olsen-P (mg kg 1 ) Men ± SEM Minhe ±22 6.2± ± ±18 8.4± ± ±12 3.2± ± ±21 4.0± ± ±24 5.3± ±0.47 Hungzhong ± ± ± ± ± ± ± ± ± ±0 18.5± ± ± ± ±0.47 Hiei ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±0.87

5 438 Biol Fertil Soils (2010) 46: Tle 3 Seleted soil physiohemil properties t different field depths with six ot ultivrs growing t the Minhe site Ot ultivr Soil depth (m) Soil ph (in wter) Soil orgni mtter (g kg 1 ) Soil Olsen-P (mg kg 1 ) Qingyin No ±22 6.2± ± ±18 8.4± ± ±12 3.2± ± ±21 4.0± ± ±24 5.3± ±0.47 Cnd ultivr ± ± ± ±13 8.2± ± ±07 6.9± ± ±15 1.0± ± ±03 4.9± ±0.45 Qinghi ±63 7.7± ± ±26 8.7± ± ±30 4.2± ± ±15 4.0± ± ±15 1.9± ±0.35 NEON ± ± ± ± ± ± ± ± ± ±24 4.9± ± ±13 6.5± ±0.79 Xun ± ± ± ±15 8.7± ± ±06 6.8± ± ±03 6.2±10 8.8± ±12 5.8±03 7.0±0.78 Xun ± ± ± ±03 8.7± ± ±12 5.9± ± ±03 4.2± ± ±15 3.5± ±0.55 Men ± SEM oloniztion indies of V4 (Aven stiv L. v. Cnd ultivr) were the highest mong the six ultivrs (Fig. 2). A derese in myorrhizl root length with inresing soil depth ws most pronouned etween the surfe lyer (0 10 m) nd the other soil lyers of V1 (A. stiv L. v. Qingyin No. 2) genotype nd the upper four lyers nd the lowest lyer in the se of V2 (A. stiv L. v. Cnd ultivr), V5 (Aven nud L. v. Xun18), nd V6 (A. nud L. v. Xun 4600) genotypes. Intrrdil strutures inluding rusules nd vesiles were most extensive in the topsoil nd deresed with inresing depth in most of the field sites with the exeption of rusules in V3 (A. stiv L. v. Qinghi 444) nd vesiles in V2. The numer of AMF spores deresed with inresing soil depth t different ltitudes nd on different Aven ultivrs. Spore density t different ltitudes showed signifint differenes, with the highest vlues t Hungzhong nd the lowest t Minhe. Compring ultivrs, lrgest spore numers were found in V2 nd the smllest in V1 (Fig. 3). Thirty-six AM fungl speies representing eight gener were deteted in the soil profiles of the fields investigted. Glomus etunitum, Glomus mossee, Glomus intrrdies, nd Glomus geosporum were the dominnt speies (Tle 4). Disussion We found tht the undne of the intrrdil strutures rusules nd vesiles in the 0 50 m soil lyer ws gretly influened y ltitude with no effet on the overll

6 Biol Fertil Soils (2010) 46: Fig. 1 Perentge of root length of ot (A. stiv L. v. Qingyin No. 2) olonized y AMF t different ltitude nd soil depth tegories t the three sites. Different letters ove the olumns indite signifint differene etween mens y Dunn s multiple rnge test t the 5% level. By nlysis of vrine: **P<1, *P<5, NS not signifint, sme s elow Coloniztion rte (%) A A A Minhe Hungzhong Hiei 0-10m 10-20m 20-30m 30-40m 40-50m Signifine of Altitude (A) NS Arusule undne (%) B B A 0-10m 10-20m 20-30m 30-40m 40-50m Signifine of Altitude (A) ** 5.0 Minhe Hungzhong Hiei 14.0 B B A 0-10m m 20-30m Vesiules undne (%) m 40-50m Signifine of Altitude (A) ** Minhe Hungzhong Hiei levels of root oloniztion t the three ltitudes. The higher numer of rusules t Hiei thn in the other two lower sites my suggest requirement for greter nutrient exhnge etween the two symionts t the highest ltitude. Glomeromyot (Shüßler et l. 2001) n derese the environmentl stress on the host plnt (Entry et l. 2002; Mehrg 2003; Bumnn et l. 2005). Our results my imply tht AMF n mke n importnt ontriution to ot produtivity y sustntil oloniztion to enhne plnt nutrition nd dpttion to low tempertures nd rid onditions. The oservtion tht plnt genetis ffeted the level of oloniztion ontrdits the results of Gehring et l. (2006), who found tht environmentl ftors, prtiulrly ltitude, were more importnt thn host plnt genetis in influening root oloniztion of ottonwood y AMF. Perhps the reltive influene of environment nd plnt genetis might differ etween single nd dul olonized plnts. Edphi onditions were not tested in this study euse we seleted sites with the sme soil type nd texturl lss (Tle 1). However, we found tht the highest ltitude site, Hiei, ontined more soil P ross different depths ompred to other sites nd lso hd the mximum AM oloniztion nd AM fungl strutures, espeilly rusules. A possile explntion my e different growth rtes of A. stiv v. Qingyin No. 2 t different ltitudes resulting in vried nutrient demnd. Zhng et l. (2007) investigte the effets of geogrphil lotion on herge dry mtter yield nd nutritive vlue of ot on the Qinghi Tietn Plteu nd found tht plnts growing t the highest ltitude (2,960 m sl) showed the highest dry weight umultion rte. Another influening ftor my e the lter smpling

7 440 Biol Fertil Soils (2010) 46: Fig. 2 Perentge of root length of six Aven ultivrs olonized y AMF t different soil depth tegories t Minhe field site. V1 V3 (husk ot): A. stiv L. v. Qingyin No.2, A. stiv L. v. Cnd ultivr, A. stiv L. v. Qinghi 444; V4-V6 (nked ot): A. nud L. v. NEON, A. nud L. v. Xun18, A. nud L. v. Xun 4600 Coloniztion rte (%) B B AB A AB A 0-10m 10-20m 20-30m 30-40m 40-50m Signifine of Cultivr (C) * C S * 1 V1 V2 V3 V4 V5 V6 Vriety of ots Arusule undne (%) AB C BC A AB AB 0-10m 10-20m 20-30m 30-40m 40-50m V1 V2 V3 V4 V5 V6 Vriety of ots Signifine of Cultivr (C) * Soil depth(s) ** C S * Vesiules undne (%) B B B A B B 0-10m 10-20m 20-30m 30-40m 40-50m V1 V2 V3 V4 V5 V6 Signifine of Cultivr (C) ** C S * Vriety of ots time (grin-filling stge). It hs een found tht the depressive effet of P on oloniztion ws not pprent during periods of extensive produtivity due to the progressive growth of the plnts (Likr et l. 2009; Surmim et l. 2008). AMF oloniztion ws gretly influened y genotype, in terms of oth rusules nd perentge of root length olonized. The oloniztion rte of nked ot ws muh higher thn tht of husk ot. In ontrst to other otproduing ountries, the predominnt type of ots grown in Chin hs een the hulless vriety A. nud, or nked ots, whih requires more fvorle environmentl onditions thn husk ots (Zhou et l. 1999). The more extensive oloniztion y AMF might inrese the survivl pility of nked ots in the old nd rid onditions previling in Qinghi nd thus mke sustntil ontriution to the produtivity of nked ots. The intrrdil strutures nd the spore numers were more extensive in the surfe thn in the deeper soil lyers (Figs. 2 nd 3) thus onfirming the results of Jkosen nd Nielsen (1983) nd Rillig nd Field (2003). Physil nd hemil properties of soil hnge with depth nd influene the distriution of soil orgnisms (Aott nd Roson 1991; Entry et l. 2002). Fungi re espeilly sensitive to low prtil pressures of oxygen whih previl t depth (Brdy nd Weil 1996), nd AMF re generlly sre where roots re sprse (Anderson et l. 1987). The perentge of root length olonized y AMF t soil depth of m verged 20%. Oehl et l. (2005) studied the vertil distriution of spores of AMF in soil profiles of extensively nd intensively mnged griulturl eosystems nd found tht AMF ommunities in deep soil lyers were surprisingly diverse, even in two ontinuously mono-

8 Biol Fertil Soils (2010) 46: Fig. 3 AMF spore density t different soil depth t different ltitudes on different Aven ultivrs Numer of spores g -1 soil Numer of spores g -1 soil d d C Minhe Hungzhong Hiei D A C B B C 0-10m 10-20m 20-30m 30-40m 40-50m d d A B d d d 0-10m 10-20m 20-30m 30-40m 40-50m d e d d V1 V2 V3 V4 V5 V6 Vriety of ots Signifine of Altitude (A) ** A S ** Signifine of Cultivr (C) ** ** C S ropped mize fields. We lso deteted 36 AMF speies in the fields we investigted (Tle 4). Some speies prefer speifi soil lyers, for exmple, G. etunitum, ws isolted more frequently t the lower soil lyers, whih ws in ord with the result of Opik et l. (2006). Additionlly, some dominnt speies suh s G. mossee, G. intrrdies, nd G. etunitum hve een found to hve glol distriution (Opik et l. 2006). This suggests tht n AM fungi gene nk my persist in the susoil, filitting gro-eologil restortion. Some dditionl funtionl trits suh s the integrity nd stility of hyphl networks might e importnt in rid environments where AMF types with stle networks my provide etter reltionship etween plnts nd soil nd Tle 4 Arusulr myorrhizl fungi of Aven stiv in Qinghi provine AMF genus Aulospor Appendiispor Diversispor Entrophospor Gigspor Glomus Pispor Sutellospor AMF speies A. iretiult Rothwell & Trppe; A. delit Wlker, Pfeiff. & Bloss; A. dentiult Sieverd. Toro; A. rehmii Sieverd. & Toro; A. rugos Sieverd. Toro; A. spinos Wlker & Trppe; A. sp Ap. gerdemnnii Spin, Oehl & Sieverd. D. spur (Pfeiff., Wlker & Bloss) Wlker & Shüßler E. infrequens (Hll) Ames & Shneid. Gi. rose Niolson &Shenk; Gi.sp G. ggregtum Shenk & Sm.; G. lidum Wlker & Rhodes; G. rorense MGee; G. ledonium Niolson & Gerd. Trppe & Gerd.; G. lrum Niolson & Shenk; G. desertiol Trppe, Bloss & Menge; G. drummondii Blszk. & Renker; G. eurneum Kenn., Stutz & Morton; *G. etunitum Beker & Gerd. ; G. fsiultum (Thxt.) Gerd. & Trppe emend. Wlker & Koske; G. frgilistrtum Skou & Jkosen.; *G. geosporum (Niolson & Gerd.) Wlker; *G. intrrdies Shenk & Sm.; G. invermium Hll; G. mirorpum Koske, Gemm & Olexi; *G. mossee (Niolson & Gerd.) Gerd. & Trppe; G. tortuosum Shenk & Sm.; G. versiforme (Krst.) Berh; G.wlkeri Blszk. & Renker; G. sp1; G. sp2; G. sp3 P. sintillns Wlker, Vesterg & Shuessler S. lospor (Niolson & Gerd.) Wlker & Snders; S. sp

9 442 Biol Fertil Soils (2010) 46: my protet the vegettion ginst drought (vn der Heijden nd Sheulin 2007). Moreover, vritions in root morphology in different vegettion types nd their reltionship with myorrhizl oloniztion levels were very pronouned (Muthukumr et l. 2003). Thus, the hrteristis of extrrdil hyphl networks nd root morphology of ot ultivrs will e the sujet of future studies. New methods suh s quntittive moleulr tehniques should lso e onsidered for future investigtions on the reltive undne of vrious AMF types nd their impt on eologil proesses. Aknowledgments We thnk the Ntionl Bsi Reserh Progrm of Chin (Projet 2009CB119000), the innovtive group grnt of NSFC (No ), the British Counil, nd the UK Deprtment for Interntionl Development through their Development Prtnerships in Higher Edution progrm (Projet DelPHE 1.64), Xinjing Corps Funds (No. 2009ZJ06), nd the Dotorl Fund of the Chinese Ministry of Edution (Projet ) for finnil support. 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