Influence of arbuscular mycorrhizal fungi on uptake of Zn and P by two contrasting rice genotypes

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1 Influene of rusulr myorrhizl fungi on uptke of Zn nd P y two ontrsting rie genotypes R. Hjiolnd 1, 3, N. Alisghrzd, R. Brzeghr 1 1 Plnt Siene Deprtment, University of Triz, Triz, Irn Soil Siene Deprtment, University of Triz, Triz, Irn 3 Exellent Center for Biodiversity, University of Triz, Triz, Irn ABSTRACT There is little experimentl evidene out the funtionl signifine of rusulr myorrhizl fungi (AMF) oloniztion in providing nutrients for lowlnd rie. This study ws undertken to exmine whether growth nd nutrient defiienies my ffet plnts enefit from AMF inoultion. Two ontrsting rie (Oryz stiv L.) genotypes nd two AMF speies (Glomus mossee nd G. intrrdies) were used in this experiment. Under P strvtion, P uptke in the genotype tolernt to P defiieny (Fjr), delined signifintly up to 36% (P <.5) in response to AMF inoultion, while it enhned y out 7% (P <.1) in suseptile genotype (Shfgh). Under Zn strvtion, Zn uptke of Zn-effiient genotype (Shfgh) inresed y out fold (P <.1), ut redution of 5% (P <.5) ws oserved in the Zn-ineffiient genotype (Fjr) upon myorrhiztion. Greter genotypi differenes were oserved for plnts. Our results imply tht genotypi differene in responsiveness to inoultion with AMF is ttriutle to different ontriution of mehnisms for inresed nutrient uptke in myorrhizl plnts depending on nutrient, nutritionl sttus nd nutrient effiieny of genotypes. Keywords: rusulr myorrhizl fungi; Glomus mossee; Glomus intrrdies; Oryz stiv; rie genotypes Coloniztion of roots with rusulr myorrhizl fungi (AMF) often improves the phosphorus nutrition of host plnts growing on soils with springly solule P forms (Shenoy nd Klgudi 5). Inresed sorption surfe nd lower threshold onentrtion for P uptke in myorrhizl root systems re ontriuting ftors (Peterson nd Mssiotte 4). Reent evidenes suggest tht AMF n provide the dominnt route for plnt P supply, even when overll growth or P uptke remins unffeted (Smith et l. 3). Improved uptke of other minerl elements y myorrhizl roots hs lso een demonstrted for nitrogen, potssium (George et l. 1995) nd for mironutrients suh s Zn, Cu, Fe nd Mn (Azón et l. 3, Orts nd Akpinr 6). It is well known tht the Zn iovilility is limited y low Zn moility in the soil solution nd then y sptil vilility. Aordingly, sorption re is importnt prmeter influening iovilility of Zn (Hislihoglu nd Kohin 3). Therefore, n inresed sorption surfe s result of rusulr myorrhizl oloniztion my e of prtiulr importne for Zn uptke ompred to other mironutrients. In ontrst to other rop speies, there is little experimentl evidene out the role of myorrhizl oloniztion in lowlnd rie plnts (Solimn nd Hrit 1996, Purkysth nd Chhonkr 1). In previous work, we showed lrge vrition in Zn effiieny mong Irnin lowlnd rie genotypes (Hjiolnd nd Slehi 6). However, there is no informtion on P effiieny trit of these genotypes. In the present study, in ddition of hrteriztion of P effiieny in two seleted genotypes, we investigte whether inoultion of these genotypes with AMF ould further inrese P nd Zn uptke. Here we test if there is vrition in myorrhizl responsiveness etween two ontrsting rie genotypes, nd how this differene is relted to P nd Zn effiieny in the nonmyorrhizl ondition. Moreover, we test the following hypotheses: (i) myorrhizl responsiveness is relted not only to the nutritionl sttus of plnts (e.g. nutrient requirement), ut lso to plnts nutrient effiieny, (ii) high myorrhizl responsiveness sed on plnt growth is not neessrily ssoited with higher myorrhizl responsiveness sed on P or Zn uptke. PLANT SOIL ENVIRON., 55, 9 (3):

2 MATERIAL AND METHODS Fungl inoulum, plnt mterils, nursery ultivtion nd trnsplnttion. Two myorrhizl fungi speies inluding Glomus mossee (Niol nd Gerd) Gerdemnn nd Trppe or G. intrrdies Shenk nd Smith (Soil Biology Lortory, Fulty of Agriulture, University of Triz) were propgted 4 months on sorghum plnts in greenhouse. Pot ontents, inluding snd, root segments, hyphe nd spores were used s inoulum. Numer of spores in the inoulum ws per g for oth myorrhize speies nd root oloniztion ws 74.8 nd 78.8% for G. mossee nd G. intrrdies, respetively. Surfe sterilized seeds of two genotypes (Fjr, Shfgh) of rie (Oryz stiv L.) (provided y Rie Reserh Center, Guiln, Irn) were germinted in the drk on filter pper soked with sturted CSO 4 solution. In preliminry experiment, Zn defiieny tolerne ws determined in the order of Shfgh > Fjr, nd P defiieny tolerne ws determined in the order of Fjr > Shfgh. Germinted seeds were trnsferred to 5 l nursery ontiners inluding three tretments (without AMF inoultion, inoultion with G. mossee or G. intrrdies) with three independent replitions per tretment. Nursery ontiners were filled with sterilized snd mixed with ~3 mg inoulum, then 3 young seedlings were trnsferred to eh ontiner nd plnts were grown for three weeks. Non-inoulted ontiners reeived the sme mount of sterilized inoulum. Continers were irrigted with distilled wter dily to mintin moisture t field pity nd were fed eh week with hlf strength nutrient solution (Yoshid et l. 197) without P, ut C 3 (PO 4 ) ws dded t 4 g/kg to eh ontiner. At the end of nursery ulture, oloniztion of seedling roots ws tested y rndom smpling (Phillips nd Hymn 197). The used AMF isoltes were isolted from the Triz Plin nd indentified ording to the Shenk nd Perez (1988). Also, the isoltes were onfirmed y Professor J. Morton t the West Virgini University (USA). Tretments nd experimentl design. Five olonized plnts were trnsplnted to the 3 l pots tht were filled with qurtz snd (~1 mm dimeter) fter wshing, steriliztion nd weighing. Roots were refully seprted from rhizosphere soils nd were wshed with distilled wter for removing soil prtiles efore trnsplnting. Three myorrhizl tretments ( AMF, inoultion with G. mossee or G. intrrdies), two levels of Zn (without nd with.5µm Zn) nd P (without nd with.3mm KH PO 4 ) were pplied (Yoshid et l. 197). The plnts were grown under flooded onditions relized y.5 m wter ove the snd. Plnts were grown for two months under ontrolled environmentl onditions with temperture regime of 5 C/18 C dy/night, 14/1 h light/ drk period, reltive humidity of 7/8% nd t photon flux density of out 3 4 µmol/m /s. Plnts were dily irrigted y doule-distilled wter or nutrient solution (Yoshid et l. 197) fter determintion of nutrients depletion y mesuring N nd P onentrtions in the pots. Hrvest nd nlyses. Before hrvest, plnt height ws mesured nd the reltive mount of hlorophyll ws determined with hlorophyll meter (SPAD-5, Minolt). Hrvested plnts were firstly rinsed with tp wter nd then with distilled wter. The myorrhizl oloniztion perentge ws evluted y the grid line interept method (Phillips nd Hymn 197). After determintion of dry weight, oven-dried smples were shed in muffle furne t 55 C for 8 h, then were resuspended in 1% HCl nd mde up to volume y doule distilled wter. Conentrtion of P ws determined y the mmonium-vndte-molydte method (Gerike nd Kurmies 195), nd of K y flme photometry. Zn nd Fe were determined y tomi sorption spetrophotometer (AA 63, Shimdzu, Jpn). Nutrient uptke ws lulted for eh pot s the sum of nutrient ontent of shoots nd roots for 5 plnts. P nd Zn effiieny (E) of two tested genotypes were lulted sed on the following formule (Osorne nd Rengel ): E = (Shoot dw t low nutrient supply/shoot dw t dequte nutrient supply) 1. Myorrhizl responsiveness (MR) ws lulted s: MR = [(Plnt dw +AMF Plnt dw AMF )/Plnt dw AMF ] 1 (Hetrik et l. 199). Myorrhizl nutrients responsiveness (MNR) ws lulted similrly: MNR = [(Nutrients uptke +AMF Nutrients uptke AMF )/Nutrients uptke AMF ] 1 (Go et l. 7). Experiments were onduted in rndomized omplete lok design using three independent replitions. Sttistil nlyses of dt were rried out y ANOVA test (Tukey test t P <.5). RESULTS AMF oloniztion ws not oserved in the non-inoulted plnts. The highest oloniztion rte ourred in the sene of oth P nd Zn. 94 PLANT SOIL ENVIRON., 55, 9 (3): 93 1

3 Applition of P lowered oloniztion signifintly from 5 7% to only 13 15% nd ddition of oth Zn nd P to the pots deresed AMF oloniztion from 5 7% to 7 11%. Root oloniztion etween two AMF speies ws signifintly different only in nd tretments. As expeted, P defiieny used redution of growth in oth experiments, however, genotypes differed in the suseptiility to P defiieny. Redution of shoot dw ws 9% in Fjr ut 7% in Shfgh. Clulted P effiieny for Fjr nd Shfgh ws 7 nd 9 respetively, therefore, ler ontrsting response ws oserved etween Fjr nd Shfgh in tolerne to P defiieny. Root nd shoot dw nd plnts height deresed signifintly y low Zn supply. In ddition, genotypi differenes were oserved, Fjr demonstrted high suseptiility with up to 33% redution of shoot dw in tretments, ompred to Shfgh with only 3% redution of shoot dry mtter. Zin effiieny lulted for Fjr nd Shfgh ws 67 nd 97, respetively. Effet of inoultion on hlorophyll ontent nd growth of plnts Shoot nd root dry mtter of non-myorrhizl plnts ws greter thn those of myorrhizl ones. Plnts height nd hlorophyll ontent responded similrly to AMF oloniztion nd were deresed up to 33% (Tle 1). Redution of plnts growth due to AMF inoultion ws similr etween nd plnts. Growth of Zn defiient inoulted plnts (y G. intrrdies) ws deresed up to 73% in shoot nd 77% in roots, while this redution in Zn suffiient plnts ws only 15% in shoot nd 16% in roots. The effet of AMF speies ws different nd the differene etween responses of Zn defiient nd suffiient plnts to inoultion ws greter in plnts inoulted with G. intrrdies thn in those inoulted with G. mossee (Tle 1). In ontrst to Fjr, for Shfgh, signifint growth stimultion ws oserved in inoulted plnts (Tle ). Interestingly, in Shfgh, Zn-effiient genotype, inoultion y AMF stimulted prtiulrly root growth of Zn defiient plnts, while inhiited tht in Zn suffiient ones. Similrly with Fjr, the effet of inoultion with G. intrrdies ws more prominent thn inoultion with G. mossee. However, suh n effet ws less expressed in shoot (Tle ). Nutrients uptke under inoultion nd noninoultion onditions Phosphorus uptke in Fjr delined in response to AMF inoultion in P defiient plnts either signifintly (in plnts inoulted with G. mossee) or in tendeny (in plnts inoulted with Tle 1. Lef hlorophyll ontent, shoot nd root dry weight (mg dw/pot) of rie (Oryz stiv L. v. Fjr) without ( AMF) nd with inoultion y Glomus mossee (G. m.) or Glomus intrrdies (G. in.) t different phosphorus nd zin levels P Zn AMF Root oloniztion (%) Chlorophyll (reltive) Plnt height (m) Shoot dw (mg/pot) Root dw (mg/pot) AMF g 54 ± 9 1 ± ± ± 1 G. m. 5 ±.6 36 ± 14 ± ± 11 d 341 ± 11 d G. in. 7 ± 1 41 ± 6 16 ±.5 84 ± 199 d 33 ± 98 d AMF g 84 ± 5 33 ± ± ± 198 G. m. 19 ±.8 59 ± 1 3 ± ± ± 187 d G. in. ±.6 77 ± 19 3 ± ± ± 98 AMF g 8 ± 13 3 ± ± ± 1 G. m. 13 ± 1 d 59 ± 3 ± ± 158 d 41 ± 78 d G. in. 14 ±.6 d 56 ± 16 ± ± 68 d 41 ± 31 d AMF g 1 ± 1 39 ± ± ± 78 G. m. 8 ± 1 e 8 ± 8 3 ± ± ± 98 G. in. 11 ± 1 f 9 ± 6 36 ± ± ± 11 Dt in eh olumn followed y the sme letter re not different signifintly (P <.5) PLANT SOIL ENVIRON., 55, 9 (3):

4 Tle. Lef hlorophyll ontent, shoot nd root dry weight (mg dw/pot) of rie (Oryz stiv L. v. Shfgh) without ( AMF) nd with inoultion y Glomus mossee (G. m.) or Glomus intrrdies (G. in.) t different phosphorus nd zin levels P Zn AMF Root oloniztion (%) Chlorophyll (reltive) Plnt height (m) Shoot dw (mg/pot) Root dw (mg/pot) AMF i 59 ± 9 4 ± ± 46 de 569 ± 74 f G. m. 5 ±.6 65 ± 1 6 ± ± 63 d 99 ± 91 d G. in. 7 ±.6 58 ± 1 6 ± ± 54 d 718 ± 59 e AMF i 65 ± 1 7 ± ± 74 d 687 ± 68 e G. m. 19 ± 1 d 56 ± 8 6 ± ± 97 d 59 ± 98 e G. in. ± 1 63 ± 7 ± ± 11 e 579 ± 39 e AMF i 86 ± ± ± ± 1 de G. m. 13 ±.6 f 89 ± ± ± ± 116 d G. in. 15 ±.6 e 18 ± ± ± ± 58 AMF i 1 ± 11 4 ± ± ± 59 G. m. 7 ±.8 h 91 ± 1 38 ± ± ± 98 d G. in. 1 ±.6 g 94 ± 9 44 ± ± ± 18 Dt in eh olumn followed y the sme letter re not different signifintly (P <.5) -AMF G. mossee G. intrrdies - AMF G. mossee G. intrrdies P uptke (mg/pot),5.5 1, ,5 P defiient plnts Fjr P sufffiient plnts Fjr P uptke (mg/pot).5, ,5 1.5,5 Shfgh Shfgh Tretments Tretments Figure 1. Uptke of P y rie (Oryz stiv L. v. Fjr nd Shfgh) without ( AMF) nd with inoultion y Glomus mossee or Glomus intrrdies t different phosphorous nutritionl sttus. Columns indited y the sme letter re not different signifintly (P <.5) 96 PLANT SOIL ENVIRON., 55, 9 (3): 93 1

5 G. intrrdies). In this genotype, P suffiient plnts hd lower P uptke under inoultion onditions with oth AMF speies under low ut not dequte Zn supply. In P nd Zn suffiient plnts ( ), signifint improvement of P uptke ws oserved in plnts inoulted with G. intrrdies. In ontrst to Fjr, in Shfgh, AMF inoultion showed positive effet on P uptke either in tendeny or signifint, in oth P defiient nd suffiient plnts with the exeption of plnts inoulted with G. mossee (Figure 1). Zn uptke ws ffeted y AMF inoultion differently depending on genotypes. Inoultion with AMF resulted in redution of Zn uptke in Fjr. In ontrst, AMF inoultion enhned Zn uptke in Shfgh. Phosphorous nutritionl sttus did not ffet the responses of Zn uptke to inoultion, however, P suffiient plnts showed higher Zn uptke thn P defiient ones (Figure ). Potssium uptke tended to derese y inoultion. Although these hnges were minly nonsignifint, the redution ws oviously higher in Fjr thn in Shfgh (Tle 3). Similrly with the effet of AMF inoultion on Zn uptke in Fjr, Fe uptke ws deresed in inoulted plnts in ll tretments. In ontrst, Fe uptke ws inresed signifintly y AMF inoultion in Shfgh prtiulrly in P nd Zn suffiient plnts inoulted with G. intrrdies. However, the effet of AMF inoultion on Fe uptke in oth genotypes ws muh less prominent thn tht of Zn uptke. AMF inoultion inresed Zn uptke up to 4 fold (39%), while this stimultion for Fe uptke ws only 59% for the sme genotype nd tretment ( Shfgh) (Tle 3). DISCUSSION Growth stimultion y inoultion with AMF ws not uiquitous for ll tested genotypes nd under ll pplied tretments. The estlishment nd mintenne of myorrhizl symiosis is linked to flow of ron from the host plnt to the fungus (Mrshner 1995). Depression of plnt yield in response to AMF oloniztion in Zn uptke (µg/pot) AMF G. mossee G. intrrdies Zn defiient plnts Fjr AMF G. mossee G. intrrdies Zn sufffiient plnts Fjr Zn uptke (µg/pot) d Shfgh Shfgh Tretments Tretments Figure. Uptke of Zn y rie (Oryz stiv L. v. Fjr nd Shfgh) without ( AMF) nd with inoultion y Glomus mossee or Glomus intrrdies t different Zn nutritionl sttus. Columns indited y the sme letter re not different signifintly (P <.5) PLANT SOIL ENVIRON., 55, 9 (3):

6 Tle 3. Uptke of K nd Fe y rie (Oryz stiv L. v. Fjr nd Shfgh) without ( AMF) nd with inoultion of roots y Glomus mossee (G. m.) or Glomus intrrdies (G. in.) t different phosphorus nd zin levels P Zn AMF Fjr Shfgh K uptke (mg/pot) Fe uptke (µg/pot) K uptke (mg/pot) Fe uptke (µg/pot) AMF 74 ± 1 87 ± ± 6 e 876 ± 15 f G. m. 3 ± ± ± ± 11 e G. in. 7 ± 9 8 ± ± 7 de 93 ± 198 fg AMF 18 ± ± ± 66 d 1649 ± 5 fg G. m. 55 ± ± 9 64 ± ± 59 e G. in. 9 ± ± ± ± 116 e AMF 151 ± ± ± ± 389 d G. m. 6 ± ± ± ± 31 d G. in. 5 ± ± ± ± 395 AMF 188 ± ± ± ± 197 G. m. 118 ± ± ± ± 66 G. in. 166 ± ± ± ± 575 Dt in eh olumn followed y the sme letter re not different signifintly (P <.5) this work might e explined y ompetition of fungus with plnts for photosynthesis produts, likely euse of low photosynthesis rte due to low light intensity in growth hmer (3 4 µmol/m /s) ompred with open field onditions (17 µmol/m /s). It is well estlished tht oloniztion of roots nd estlishment of myorrhize re signifintly redued t high P levels in soil nd plnt (Shenoy nd Klgudi 5). However, there is no experimentl evidene relted to the dependene of root oloniztion on Zn level in soil. In this work, oloniztion of roots ws ffeted not only y P ut lso y Zn supply level, defiieny onditions indued oloniztion in oth genotypes nd AMF speies. Effet of AMF inoultion on nutrient uptke AMF oloniztion hd signifint effet on uptke of P nd Zn. Root oloniztion y AMF improves P (Smith et l. 3) nd Zn (Go et l. 7) uptke per unit of root length due to the enhnement of root surfe re y hyphl growth nd providing n extr route for P uptke s myorrhizl pthwy. In this work, growth response of root to AMF is possily nother importnt use of inresed P nd Zn uptke y inoultion s well s genotypi differenes. Root dry weight ws inresed in Shfgh up to 63% (e.g. in plnts inoulted with G. mossee) whih ws ssoited y 4-fold inrese in P uptke per plnt. Conversely, root length ws inhiited y inoultion in Fjr up to 6% onomitnt with redution of P uptke up to 69%. Redution of Zn uptke in Fjr nd its enhnement in Shfgh in inoulted plnts were lso ssoited with inhiition nd stimultion of root growth, respetively. An ovious genotypi differene in AMF-indued hnges in the root/shoot rtio (dry weight se, dt not shown) of plnts further onfirms this onlusion. This rtio redued from.5 to.37 in Fjr upon myorrhiztion (G. intrrdies), while inresed from.6 to.83 in Shfgh. A generl tendeny in redution of K uptke in Fjr ould e the result of n overll growth redution, prtiulrly root growth nd surfe re in AMF inoulted plnts. Effet of AMF oloniztion in dependene of AMF speies nd of plnt genotype Though similr oloniztion rte, myorrhizl speies were different in their effet on growth nd nutrient uptke. G. intrrdies ffeted positively growth nd nutrient uptke more thn G. mossee. A poor effetivity of G. mossee might e relted to poor development nd tivity of the externl hyphe, low hyphl trnsport rtes, nd poor 98 PLANT SOIL ENVIRON., 55, 9 (3): 93 1

7 solute interhnge t the rusule-host root ell interfe (Mrshner 1995). The positive effet of AMF inoultion, whih ws oserved only in Shfgh with onomitnt enhnement in root growth, suggests onsiderle role for response of root in determintion of response of nutrient uptke in AMF plnts. However, the ontriution of root growth in inresed nutrients quisition should not e overestimted. Root length nd sptil vilility re of high importne for nutrients suh s P, Zn nd K (Mrshner 1995), ut Fe uptke does not seem to e relted highly to root growth. In our experiment, eside expeted inresed uptke of nutrients suh s P nd Zn, Fe uptke ws lso ffeted in prllel with root growth response nd unexpetedly, improvement of root growth did not ffet K uptke. Benefit from AMF ws oserved in the genotype (Shfgh) tht showed higher sensitivity to P defiieny simultneously with higher tolerne to Zn defiieny. A signifint improvement of plnt growth under inoultion onditions my e onsidered the min use of positive response of Shfgh to AMF regrding P nd Zn uptke. To test this hypothesis, we lulted myorrhizl responsiveness (MR) nd myorrhizl nutrient responsiveness (MNR) for four tested nutrients s well s orreltion oeffiient etween the two prmeters (Tle 4). Vrition in responsiveness n e prtitioned into dependene nd nondependene omponents, dependene vrition reltes to plnt performne under stress ut nondependene vrition desries differenes in the intertion etween plnt nd fungus (Swers et l. 8). A signifint orreltion etween myorrhizl responsiveness nd myorrhizl P nd Zn responsiveness in Fjr suggests n importnt ontriution of growth response to P nd Zn quisition of myorrhizl plnts in this genotype, i.e. greter mount for dependene omponent of responsiveness. In ontrst, the lk of suh orreltion in Shfgh indites tht mehnisms whih re not diretly relted to the growth response to AMF, e.g. vrition in nutrient quisition properties nd/or delivery into the host plnt, re responsile for higher MNR in this genotype. Chrteriztion of P trnsporters in rie nd study of their expression under AMF nd +AMF onditions suggest tht there is swith from one pttern of gene expression to nother. Thus the geneti determinnts of performne in AMF nd +AMF plnts vry independently (Pszkowski et l. ). Aordingly, greter MNR for P in Shfgh ould e explined y higher expression level of AMF-speifi P trnsporters nd/or their greter effiieny in the P delivery to the host plnt, i.e. greter mount for non-dependene omponent of responsiveness. However, moleulr se nd the use of greter MNR for Zn in this genotype (with greter Zn-effiieny in the sene of AMF), remins unknown. In ontrst to P nd Zn, Fe nd K uptke in Tle 4. Myorrhizl responsiveness (MR) nd myorrhizl nutrients responsiveness (MNR) lulted for P, Zn, Fe nd K nd orreltion oeffiient (R) etween them in rie genotypes (Oryz stiv L. v. Fjr nd Shfgh) inoulted with Glomus mossee (G. m.) or Glomus intrrdies (G. in.) t different P nd Zn levels Fjr Shfgh MNR MR Tretments P Zn Fe K G. m. G. in. G. m. G. in. G. m. G. in. G. m. G. in. G. m. G. in R.66*.81**.11 ns.53 ns R.9 ns.44 ns.79**.71* ** signifint t.1, * signifint t.5, ns not signifint (P <.5) PLANT SOIL ENVIRON., 55, 9 (3):

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