Trees (2006) 20: 334 339 DOI 10.1007/s00468-005-0045-z ORIGINAL ARTICLE Romn Trubt Jordi Cortin Alberto Vilgros Plnt morphology nd root hydrulics re ltered by nutrient deficiency in Pistci lentiscus (L.) Received: 26 April 2005 / Revised: 21 November 2005 / Accepted: 7 December 2005 / Published online: 10 Jnury 2006 C Springer-Verlg 2005 Abstrct The plnts in rid nd semirid res re often limited by wter nd nutrients. Morpho-functionl djustments to improve nutrient cpture my hve importnt implictions on plnt wter blnce, nd on plnt cpcity to withstnd drought. Severl studies hve shown tht N nd P deficiencies my decrese plnt hydrulic conductnce. Surprisingly, studies on the implictions of nutrient limittions on wter use in xerophytes re scrce. We hve evluted the effects of strong reductions in nitrogen nd phosphorus vilbility on morphologicl trits nd hydrulic conductnce in seedlings of common Mediterrnen shrub, Pistci lentiscus L.. Nitrogen deficiency resulted in decrese in boveground biomss ccumultion, but it did not ffect belowground biomss ccumultion or root morphology. Phosphorus-deficient plnts showed decrese in lef re, but no chnges in boveground biomss. Root length, root surfce re, nd specific root length were higher in phosphorus-deficient plnts thn in control plnts. Nitrogen nd phosphorus deficiency reduced both root hydrulic conductnce nd root hydrulic conductnce scled by totl root surfce re. On the other hnd, nutrient limittions did not significntly ffect root conductnce per unit of folir surfce re. Thus, dpttion to low nutrient vilbility did not ffect seedling cpcity for mintining wter supply to leves. The implictions for drought resistnce nd survivl during seedling estblishment in semi-rid environments re discussed. Communicted by H. Cochrd R. Trubt ( ) J. Cortin Depto. de Ecologí, U. de Alicnte, Ap. 99 03080 Alicnte, Spin e-mil: romn.trubt@u.es Tel.: +34-96-5909564 Fx: +34-96-5903625 A. Vilgros Fundcion Centro de Estudios Ambientles del Mediterráneo (CEAM), Prque Tecnologico, C/Chrles Drwin, 46980 Ptern, Spin Keywords Drought. Root hydrulic conductnce. Nutrient deficiency. Pistci lentiscus. Specific root length Introduction There is vst mount of informtion on plnt strtegies to cope with limiting resources. However, in nturl environments, limittion by single resource is uncommon, nd plnts must simultneously optimize the use of multiple resources (Schulze et l. 1991). Xeric environments re chrcterized by excessive rdition, high-evportive demnd, nd low-wter vilbility. Under these conditions, plnts hve evolved morpho-functionl trits to enhnce wter bsorption nd trnsport (Levitt 1980; Lrcher 1995). Species respond to wter deficit by developing voidnce mechnisms bsed on stomtl control, reductions in lef re, lef size nd specific lef re (Wring et l. 1985), nd chnges in root hydrulic conductnce, which cn be considered s complementry mechnisms for regulting trnspirtion (Blnco et l. 2002). In drylnds, soil fertility is frequently low, due to low rtes of nitrogen fixtion, orgnic mtter inputs nd minerlistion rtes, nd high rtes of phosphorus immobiliztion (Henkin et l. 1998; Vllejo et l. 1998). Disturbnces such s recurrent wildfires, nd historicl lnd uses such s low-input griculture nd fiber cropping my hve further decresed soil fertility in these res (Albldejo et l. 1998). Low-moisture levels cn substntilly reduce soil nutrient vilbility by decresing nutrient diffusion nd mss flow (Krmer 1988; Pssiour 1988), nd nitrifiction rte (Killhm 1995), nd by promoting nutrient losses t lef level (Heckthorn et l. 1997; De Luci et l. 1998). Thus, it is not surprising tht drylnd plnts frequently show low nutrient levels (Osonubi et l. 1988) nd my respond to fertiliztion (Hmilton et l. 1998). A negtive reltionship between wter-use efficiency (WUE) nd nutrient use efficiency hs been observed (Ewers et l. 2000), suggesting tht plnts cnnot fully use nutrients for growth when wter is limiting. Incresing N
335 investment in leves my not result in significnt increse in photosynthesis when plnts re under strong wter limittion. In contrst, t constnt wter loss, increses in tissue N my increse WUE (Field nd Mooney 1982). Also, t constnt N concentrtion, decreses in stomtl conductnce my increse WUE but decrese overll photosynthesis, nd N use efficiency (Nielsen nd Orcutt 1996). Some plnt strtegies to cope with drought, such s incresed biomss lloction belowground, incresed WUE or chnges in root morphology (Ingestd nd Ågren 1991; Jckson et l. 2000) hve been described for nutrient-limited plnts (Forde nd Lorenzo 2001). However, chnges in root rchitecture in drought-stressed plnts my reduce plnt bility to cpture reltively immobile nutrients such s phosphorus (Fitter et l. 1991; Hung nd Nobel 1994). Deep rooting, commonly reported strtegy to withstnd wter limittion, my lso promote the explortion of soils horizons tht re commonly poor in orgnic mtter nd nutrients (Cndell nd Zedler 1995). The limited N nd P vilbility my ffect the growth rte nd morphology of roots nd root hirs. As P deficiency cn hve profound effect on root system morphology nd rchitecture (Willimson et l. 2001; Búcio et l. 2002), it my lter plnt cpcity for wter trnsport, s observed in intct plnts nd excised roots (Rdin nd Mtthews 1989). Under high-evportive demnd, reductions in the wter trnsport cpcity my promote drought stress bove ground nd increse the risk of hydrulic conductnce loss due to the xylem cvittion (Sperry 2000). In xeric environments plnts hve evolved morphologicl trits to optimize wter bsorption nd trnsport, mximizing trnsport efficiency nd voiding the risk of xylem filure (Mrtínez- Villt et l. 2002). Despite its importnce, little informtion exists on the effects of nutrient limittion on the wter blnce of woody plnts nd, more specificlly, on the cpcity of the root system to trnsport wter. In semi-rid ecosystems seedling survivl is strongly coupled to soil wter vilbility (Cortin et l. 2004). Therefore, chnges in root cpcity for wter trnsport should ffect survivl nd growth under field conditions. The objective of this work is to evlute the effect of nitrogen nd phosphorus deficiency on the morphology, biomss lloction nd root hydrulic conductnce of common Mediterrnen shrub (mstic tree, Pistci lentiscus L.)..P. lentiscus L. is widely distributed sprouting species in the Mediterrnen (Le Houérou 1981; Nveh 1989) nd exhibits high degree of plsticity in response to drought (Vilgros et l. 2003). Previous studies hve shown tht short-term survivl of the Mediterrnen shrubs, such s P. lentiscus L., under semirid field conditions cn be enhnced when N or P is removed from the nutrient solution during the nursery phse (Trubt et l. 2004). Mterils nd methods P. lentiscus L. seeds from locl provennce (E Spin Mountin Rnges) were sown in Mrch 2002 in 305 cm 3 (5 cm 5cm 17 cm) polyethylene plugs with qurtz snd s the culture medium. The plnts were kept in the open ir nd wtered on lternte dys with 40 ml per plnt of modified Hoglnd s solution contining 150 mgl 1 nitrogen (s C(NO 3 ) 2 nd KNO 3 ), 80 mg L 1 phosphorus (s KH 2 PO 4 ) nd 100 mg L 1 potssium (control seedlings, herefter C), or with similr solutions contining either no N (Nitrogen-deficient seedlings, herefter N )or no P (phosphorus-deficient, herefter P ). In N nd P seedlings, osmolrity of the nutrient solution ws djusted with KCl (Rdin 1984). Ech tretment ws replicted 20 times. After 6 months, five rndomly selected seedlings per tretment were removed from the field in the night before they were to be mesured in the lbortory. There, fter the stems were then cut 5 cm bove the root collr nd the root plugs were plced in pressure bomb (Scholnder et l. 1965) with the excised stems protruding from the chmber, hydrulic conductnce ws mesured s described in Nrdini et l. (1998). The pressure in the chmber ws incresed t rte of bout 0.07 0.69 MP min 1. The flow ws then mesured t this pressure fter 30 min of equilibrtion. Flow mesurements were mde every 2 min over period of 10 min (n=5 mesures per pressure level) by plcing plstic cpsule with sponge in contct with the sectioned stem nd determining the increse in weight on digitl blnce. The pressure ws then decresed in steps of 0.17 MP, t rte of 0.07 MP min 1, nd the sme procedure ws followed to mesure sp flow t ech pressure level tested (i.e., 0.69, 0.52, 0.34, nd 0.17 MP). Flow ws plotted ginst pressure, nd root hydrulic conductnce (K R ) ws estimted s the slope of the liner regression between both vribles (Fiscus 1975). Hydrulic conductnce of the whole root system is minly function of the root surfce re (A) in contct with the soil (Nrdini et l. 1998), nd thus we estimted root specific hydrulic conductnce (K RR ) s the rtio between root hydrulic conductnce (K R ) nd root surfce re, nd lef specific hydrulic conductnce (K RL ) s the rtio between root hydrulic conductnce (K r ) nd lef re, ccording to Nrdini et l. (2000). Morphologicl trits were mesured on 20 seedlings per tretment. Root length (cm) nd root surfce re (cm 2 ) were mesured fter wshing out the snd, spreding the root system on A4 size try to minimize overlps, scnning (on professionl scnner with trnsprency dpter; 8-bit gryscle imge, resolution 300 dpi), nd nlyzing the imge by mens of specific imge nlysis softwre (WinRhizo, Régent Instruments Inc., Quebec Cnd). Lef re (cm 2 ) ws mesured by the sme procedure. Finlly, ll biomss frctions were dried t 65 C to constnt weight. Biomss lloction belowground ws evluted by clculting the root weight rtio (RWR, g g 1 ) s the rtio between root dry weight nd totl dry weight (Hunt 1978). We clculted the specific root length (SRL, cm g 1 )s the rtio between root length nd root dry weight. The specific lef re (SLA, cm 2 g 1 ) ws clculted s the rtio between lef re nd folir dry weight. We estimted root tissue density (RTD, g cm 3 ) s the rtio between root dry weight nd root volume.
336 Tble 1 Folir nutrient concentrtion in P. lentiscus L. seedlings receiving complete nutrient solution, nutrient solution with no N (N )orno P(P ) Control N P F P N(mgg 1 ) 27.1±1.70 15.6±0.90 b 22.5±1.40 1.67 <0.001 P(mgg 1 ) 5.1±1.10 5.9±0.14 0.8±0.20 b 10.83 0.002 K(mgg 1 ) 12.9±1.20 20.6±0.9 b 10.4±0.50 29.66 <0.001 Dt re mens ± S.E. (n=5 plnts). Mens followed by the sme letter re not significntly different t P<0.05 The dried leves were ground in ring mill nd digested in heting block t 250 C with mixture of H 2 SO 4 nd H 2 O 2 (1:1, v/v). We determined totl N concentrtion by using semi-micro Kjeldhl distilltion (Tector Kjeltec Auto 1030 Anlyzer, Hogn, Sweden), nd P, nd K concentrtion by ICP spectrometry (Perkin Elmer Optim 3000, Perkin Elmer Corp., Norwlk, CT, USA). We evluted the effect of N nd P deficiency on seedling morphology nd root hydrulic conductnce by one-wy nlysis of vrince with one fixed fctor (nutrients). When nutrients hd significnt effect on ny vrible, we compred the mens by using Tukey s b HSD test. Sttisticl nlyses were performed by using the SPSS 10.6 sttisticl pckge (SPSS Inc., Chicgo, USA). Results The reductions in N nd P vilbility hd strong effect on folir nutrient concentrtions. The bsence of N in the nutrient solution reduced folir N concentrtion from 27.1 to 1.56 mg N g 1 nd incresed folir K concentrtion from 12.9 to 20.6 mg K g 1. P suppression resulted in n 84% decrese in folir P concentrtion (Tble 1). Both the number of leves per plnt nd the lef re were reduced by N deficiency (Tble 2). Specific lef re ws not ffected by this tretment, nd thus boveground biomss ws lower in N plnts. Lef number nd lef re were lso lower in P plnts thn in control plnts. However, specific lef re decresed from 93.4 to 70.4 cm 2 g 1 in the bsence of P, nd boveground biomss ccumultion in P plnts did not differ from tht of Control plnts. Belowground growth ws not ffected by N deficiency. Trends towrd incresing root length, root surfce re, root biomss, nd specific root length were not sttisticlly significnt. Only root tissue density ws higher in N plnts thn in control plnts. In contrst, root surfce re nd, mrginlly, root length in P seedlings incresed s compred to control seedlings. Root biomss ccumultion nd root tissue density did not differ between control nd P seedlings. Thus, similr vlues of root biomss ccumultion in control nd P seedlings resulted from higher specific root length in the ltter. Biomss lloction belowground, s reflected by the RWR, ws not ffected by N or P deficiency. Sp flow incresed linerly with pressure, generting correltion coefficients higher thn 0.97 for ll plnts (Fig. 1). Sp flow ws similr for ll tretments t low pressure (0.2 MP), but it ws substntilly higher in control seedlings thn in N or P seedlings t higher pressure. Accordingly, root hydrulic conductnce (K R ) ws reduced by N nd P deficiency (F=6.84; P<0.01). K RR ws lso lower in N nd P seedlings thn in the control plnts (F=5.93; P<0.016) (Fig. 2). In contrst K RL ws not ffected by N nd P deficiency (Fig. 3). Discussion We found strong effect of N nd P limittion on folir nutrient concentrtions. N concentrtion in N seedlings ws close to levels tht hve been commonly ssocited with N deficiency (Grundon et l. 1997; Connor nd Fereres 2005). Folir P concentrtion ws lso close to criticl levels in P seedlings. Potssium concentrtion strongly incresed in N seedlings, suggesting luxury consumption (Mrschner 1986). Aboveground biomss ccumultion ws reduced by low N vilbility, n effect tht hs been widely described in the literture (Ingestd nd Ågren 1991; Rubio et l. 2003). N deficiency resulted in decrese in the number of leves nd the whole plnt lef re, with no chnges in specific lef weight nd verge lef re. P deficiency lso lowered the number of leves nd whole plnt lef re. But Tble 2 Morphologicl trits of P. lentiscus L. seedlings growing under contrsted nutritionl regimes N nd P plnts received no N or P dditions, respectively, throughout the period of study. Dt re mens ± S.E (n=20). Different letters in ech row indicte significnt differences t P<0.05 Control N P F p Root dry weight (g) 0.19±0.01 0.21±0.03 0.15±0.05 2.89 0.094 Shoot dry weight (g) 0.37±0.008 0.26±0.01 b 0.35±0.01 1.39 0.028 Lef re (cm 2 ) 32.6±2.5 25.6±1.3 b 25.7±3.1 b 4.46 0.007 Root surfce re (cm 2 ) 59.0±4.7 61.1±5.8 83.2±3.1 b 2.55 0.020 Specific root length (cm g 1 ) 2667±508 3062±424 5207±523 b 48.69 <0.001 Specific lef re (cm 2 g 1 ) 93.4±8.4 98.3±5.2 70.4±3.1 b 1.01 0.046 N Leves 16.0±0.9 12.8±0.7 b 13±0.5 b 6.27 0.006 Root tissue density (g c 3 ) 0.016±0.01 0.023±0.01 b 0.019±0.01 b 4.37 0.024 Root length (cm) 512±21.3 635±30.2 785±67.16 b 3.14 0.08 Root weight rtio (g g 1 ) 0.32±0.02 0.30±0.02 0.38±0.02 4.014 0.046
337 Flow, Kg s -1 x 10-8 50 40 30 20 10 0 Control 0,2 0,4 0,6 0,8 1,0 Pressure pplied, MP Fig. 1 Chnges in wter flow with pressure in root systems of.p. lentiscus L. seedlings subjected to contrsted nutritionl regimes. Brs correspond to stndrd errors of n=5 plnts per tretment. The slopes of the liner reltionships between flow nd pressure were used to estimte hydrulic conductnce K RR 10-4 (Kg m -2 s -1 MP -1 ) 0,18 0,16 0,14 0,12 0,10 0,08 0,06 0,04 0,02 0,00 Control N- P- Fig. 2 Root hydrulic conductnce scled by totl root surfce re (K RR )ofp. lentiscus L. seedlings receiving complete nutrient solution (control) or nutrient solutions with no N (N )ornop(p ). Dt re mens ± S.E (n=5 plnts). Different letters indicte significnt differences t P<0.05, (F=593; P=0.016) K RL 10-4 (Kg m -2 s -1 MP -1 ) 0,25 0,20 0,15 0,10 0,05 0,00 Control N- P- Fig. 3 Root hydrulic conductnce scled by totl lef surfce re (K RL )ofp. lentiscus L. seedlings receiving complete nutrient solutions, or nutrient solutions with no N (N )ornop(p ). Dt re mens ± S.E (n=5 plnts). Different letters indicte significnt differences t P<0.05, (F=1.26; P=0.31) b b N - P - this ws not reflected in decrese in boveground biomss. The reductions in lef re in P-deficient plnts hve been observed elsewhere (Rdin nd Boyer 1982; Ewers et l. 2000; Ytes et l. 2002). The decrese in lef re my result in decrese in the whole plnt trnspirtion rtes, which would enhnce drought-voiding strtegy (Levitt 1980; Nielsen nd Orcutt 1996). Moreover, the proportion of root re versus lef re incresed from 1.8 in control seedlings to 2.4 nd 3.2 in N nd P seedlings, respectively. Thus, nutrient-deficient plnts mintined lower trnspiring surfce per unit of bsorbing surfce, n djustment tht my fvour seedling resistnce to wter stress. Nutrient deficiency promoted strong modifictions in root system morphology, prticulrly in P seedlings. Specific root length nd root surfce re incresed in P deficient seedlings. Severl studies suggest tht P deficiency ffects root elongtion through chnges in H + excretion nd subsequent effects on cell wll loosening (Anurdh nd Nrynn 1991). The observed increse in the root surfce re resulting from longer nd denser fine root my be importnt in the cquisition of immobile phosphorus (Bielenberg et l. 2001). Higher SRL hs been relted to increses in exploittion efficiency (Fitter 1991), which would fvor uptke efficiency (Coms nd Eissenstt 2002). On the other hnd, chnges in SRL my ffect plnt cpcity to cpture nd trnsport wter. It hs been suggested tht higher SRL could fvor higher hydrulic conductnce (Eissenstt 1991). This does not seem to be the cse in P. lentiscus L. seedlings in the present experiment. Other studies on P. lentiscus L. nd other Mediterrnen woody species hve found increses in SRL in response to wter limittion (Fonsec 1999), suggesting tht modifictions in root morphology due to low P vilbility, s observed in the present study, could hve positive net effect on wter use. The wek response of biomss lloction ptterns to nutrient limittion ws somewht unexpected. Mny studies hve reported n increse in biomss lloction belowground under limiting nutrient vilbility (Ingestd nd Ågren 1991). In contrst, our results suggest tht root morphology ws more sensitive thn biomss lloction to P deficiency. Incresed resource lloction belowground nd reductions in lef re re common strtegies to cope with drought (Levitt 1980; Lloret et l. 1999). However, other studies hve found no chnges in either the root weight rtio or the root-to-shoot rtio in.p. lentiscus L. seedlings subjected to mild wter stress (Fonsec 1999; Green et l. 2005). Mediterrnen drought-resistnt species my hve cquired geneticlly determined chrcters tht influence lloction ptterns. In fct, severl studies hve shown tht Mediterrnen species hve low phenotypic plsticity in comprison with species from humid climtes (Vlldres et l. 2000; Vlldres et l. 2002). Severl works hve reported decresed wter-trnsport cpcity in nutrient-deficient plnts (Rdin nd Eidenbock 1986; Syvertsen nd Grhm 1985; Rdin nd Mtthews 1989). In the present study, plnts subjected to N nd P deficiency showed lower K RR thn control plnts. These vlues represented 27% reduction in the wter trnsport
338 cpcity s compred to control plnts on root surfce re bsis. The reduction in the cpcity for trnsporting wter in nutrient-deficient plnts my hve importnt implictions on the wter blnce of plnts (Reinbott nd Blevins 1999; Clerwter nd Meinzer 2001). Reductions in K RR could result either from decresed hydrulic conductnce of the cells in the rdil flow pthwy or from chnges in the hydrulic rchitecture of the whole root system (Ewers et l. 2000). Moreover, reductions in root hydrulic conductnce could be the result of n incresed SRL or decresed conduit dimeter (Linton et l. 1998). The prllel decreses in the lef re nd the root hydrulic conductnce re consistent with the findings of Rdin nd Eidenbock (1984). They noted tht differences in hydrulic conductnce due to low phosphorus supply clerly preceded ny effects on lef re development, nd they concluded tht hydrulic conductnce limited lef expnsion by restricting wter trnsport. A mjor consequence of prllel decreses in root hydrulic conductnce nd lef re ws tht K RL, mesure of root system cpcity for wter supply to leves, ws similr in both nutrient-deficient plnts nd control plnts. Severl works hve nlyzed the reltionship between chnges in plnt hydrulic conductnce, nd stomtl conductnce nd trnspirtion (Nrdini et l. 2000; Sperry et l. 2002). High-hydrulic conductnce my be dvntgeous becuse it fcilittes efficient wter nd nutrient trnsport to leves. However, under moderte wter vilbility, limittions to wter trnsport due to reductions in hydrulic conductnce my enhnce conservtive wter use (Hubbrd et l. 2001; Sperry 2003). In the present work, root hydrulic conductnce scled by lef re (K RL ) showed the sme trnsport cpcity in ll tretments. According to Drcy s lw (Sperry 2000), the grdient of wter potentil from soil to leves should be similr in both control nd nutrient-deficient plnts for given evportive flux, due to similr K RL. The equivlent K RL vlues show clerly tht under given evportive flux, pressure grdients t the root level will be the sme for ll experimentl groups. In conclusion, N deficiency resulted in chnges in boveground biomss ccumultion, but it hd little effect on belowground morphology or biomss lloction. In contrst, P deficiency resulted in chnges in both boveground nd belowground morphology, but not in root nd shoot biomss ccumultion. Both N nd P deficiency strongly reduced hydrulic conductnce nd root specific hydrulic conductnce but showed no significnt effect on lef specific hydrulic conductnce. Survivl of P. lentiscus L. seedlings under semirid field conditions cn be higher in plnts tht hve been grown in nutrient-deficient conditions (Trubt et l. 2004). 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