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Nitrate influx kinetic parameters of five potato cultivars during vegetative growth

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Information on nitrate uptake kinetic parameters, and their variation among cultivars, is lacking for potato. A growth room solution culture experiment with five potato cultivars (Atlantic, Chieftain, Red Pontiac, Russet Norkotah and Shepody) at
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  Abstract  Information on nitrate uptake kineticparameters, and their variation among cultivars, islacking for potato. Agrowth roomsolution cultureexperiment with five potato cultivars (Atlantic,Chieftain, Red Pontiac, Russet Norkotah andShepody) at three sampling dates [10, 17 and22 days after transplanting (DAT)] and threereplicates was conducted to investigate the varia-tion in nitrate uptake kinetic parameters amongcultivars and with plant age during vegetativegrowth. Potato plantlets from tissue culture weregrown in a re-circulating hydroponic system. Oneach sampling date, depletion of nitrate concen-tration in 3 L of nutrient solution by a single plantwasmeasuredovera360-minperiod.Nitrateinfluxparameters were calculated from depletioncurves.Root length (RL), average diameter and root/shoot ratio were determined and relative growthrate and plant N demand per unit of RL were cal-culated. The maximum influx (  I  max ) ranged from1.30 to 3.65 pmol cm –1 s –1 and was significantlydifferent among cultivars. Russet Norkotah andAtlantic had the highest values of   I  max  at 22 DAT.Values of the Michaelis constant ( K  m ) and mini-mum concentration ( C  min ) were not significantlydifferent among cultivars except for Red Pontiacwhich had the highest values of   K  m  and  C  min . The  I  max ofallcultivarsdecreasedovertime.Therewasastrongnegativecorrelationbetween  I  max andRL.TheplantNdemandperunitofRLexplainedmorethan50%ofvariationin  I  max amongthecultivarsat17 and 22 DAT. The results suggest that  I  max  incombination with root morphology may beimportant in controlling differences in N uptakeefficiency among potato cultivars. Keywords  Maximum influx rate  Æ  Michaelis–Menten  Æ  Nitrogen uptake  Æ  Root  Æ  Solanumtuberosum Abbreviation DMP Dry matter productionPNA Plant N accumulationPNC Plant N concentrationPND Plant N demandRAD Root average diameterRGR Relative growth rateRL Root lengthR/S Root length/shoot weight ratio Introduction Potatoes ( Solanum tuberosum  L.) often receivehigh rates of fertilizer N. These high N inputs,combined with shallow root systems and irrigatedculture on sandy soils, increase the potential for M. Sharifi  Æ  B. J. Zebarth ( & )Potato Research Centre, Agriculture and Agri-FoodCanada, PO Box 20280, E3B 4Z7 Fredericton,NB, Canadae-mail: ZebarthB@agr.gc.caPlant Soil (2006) 288:91–99DOI 10.1007/s11104-006-9092-5  1 3 ORIGINAL PAPER Nitrate influx kinetic parameters of five potato cultivarsduring vegetative growth Mehdi Sharifi   Bernie J. Zebarth Received: 4 April 2006/Accepted: 19 July 2006/Published online: 30 August 2006   Springer Science+Business Media B.V. 2006  nitrate leaching and the resulting contaminationof groundwater (Errebhi et al. 1998). Knowledgeof the N influx characteristics of potato roots isimportant to the understanding of the mecha-nisms controlling potato N uptake efficiency,defined as plant N accumulation per unit of soilN supply, in efforts to improve the efficiencyof fertilizer N use and in developing moreN-efficient cultivars.Nitrate (NO 3– ) uptake kinetics describe therelationship between the influx (  I  n ) of NO 3– andits concentration at the root surface. At con-centrations lower than 2 mM, this relationship isa saturation curve that can be described by amodified Michaelis–Menten function (Nielsenand Barber 1978; Rao et al. 1997). The param- eters of Michaelis–Menten kinetics are maxi-mum influx,  I  max , Michaelis constant,  K  m , andminimum concentration,  C  min  (Claassen andSteingrobe 1999).A high value of   I  max  for NO 3– can be beneficialto the plant, but only if the rate of NO 3– transportin soil to the root surface is also high. If thistransport is non-limiting, plants can take upnutrients at a maximum rate, in which case  I  max  isthe main parameter controlling net uptake. TheNO 3– concentration in soil solution will not limitthe rate of N uptake unless it is below a very lowcritical value,  ~ 0.02 mM (Robinson et al. 1991;Steingrobe and Schenk 1991). A concentration of  £  20 mM nitrate was reported in the root zonearea of high yielding potato crop (Asfary et al.1983). Therefore, plants can take up NO 3– at orclose to a maximum rate until the soil solution isnearly depleted of NO 3– . Hence,  I  max  is the pri-mary factor influencing net influx of NO 3– (Steingrobe and Schenk 1993; Claassen andSteingrobe 1999). The importance of   I  max  ininfluencing NO 3– uptake was also confirmed byBarber (1995) based on a sensitivity analysis of the Barber–Cushman mechanistic uptake model(Barber and Cushman 1981).The value of   I  max  is not constant, but varieswith plant species, cultivar (Rodgers and Barneix1988), age (Wild and Breeze 1981), growing conditions (Hallmark and Huffaker 1978), nutri-ent status of the plant (Heins and Schenk 1986)and root morphology (Barber 1995). ‘  I  max ’ istherefore not the absolute maximum uptakecapacity of a unit of root length (RL), but ratherthe maximum net influx under a given set of conditions and plant age. For example, the nitrate  I  max  of corn plants was highest in 18–24-day-oldplants and then decreased exponentially as plantage increased to 58 days (Edwards and Barber1976). In a field experiment Mengel and Barber(1974) showed that mean uptake rates for allnutrients decreased rapidly with increased plantage. They stated that reduction in  I  max  with plantage is not just a reduction in plant demand perunit of root; it also reflects a reduction in the rateat which roots can adsorb nutrients. Baligar andBarber (1979) compared the kinetic parametersof six Florida and six Indiana corn genotypes andshowed that  I  max  for the Florida genotypes was6.3 and 2.7 times higher compared with Indianagenotypes for Ca and P, respectively. Similar re-sults were reported for potassium  I  max  values of three rice cultivars (Teo et al. 1992).Estimates of NO 3– kinetic uptake parametersfor several crops have been reported includingcorn, kohlrabi, lettuce, ryegrass, soybean andspinach (Jungk and Barber 1975; Jungk et al.1990; Steingrobe and Schenk 1991, 1994; Barber 1995). The reported NO 3– influx parameter valuesfor plants between 10 and 30 days old were in therange of 0.2–6.0 pmol cm –1 s –1 for  I  max , 10–30  l Mfor  K  m  and 1–6  l M for  C  min . Abenavoli et al.(2005) reported that potato haploid populationshave a high variability in net NO 3– uptake rate andaccumulation and suggested the selection of cul-tivars with improved capacity for NO 3– uptake.However, there are no published estimates of NO 3– kinetic uptake parameters for potato or onthe degree of variation in NO 3– influx kineticparameters among potato cultivars. The objectiveof this study was to determine the NO 3– influxkinetic parameters for five potato cultivars atthree sampling dates during vegetative growth. Materials and methods Nutrient depletion studies were conducted at thePotato Research Centre, Fredericton, NB,Canada in 2003. The experiments were conductedin a growth room with a 16-h day temperature of 23.5  C with light exposure of approximately 92 Plant Soil (2006) 288:91–99  1 3  210  l mol m –2 s –1 and an 8-h night temperature of 18  C. Plantlets obtained from the New BrunswickPlant Propagation Laboratory were grown invermiculite using a modified Hoagland solution(Hammer et al. 1978) for approximately 10 days.Plantlets were then transferred to nutrient solu-tion culture after washing the vermiculite off.A factorial arrangement of treatments in acompletely randomized design with three repli-cations was used. Factors were five potato culti-vars (Atlantic, Chieftain, Red Pontiac, RussetNorkotah and Shepody) and three sampling dates[10, 17 and 22 days after transplanting (DAT) tonutrient solution]. Cultivars were selected fortheir differences in N requirements and similarityin maturity under field and greenhouse conditions(Zebarth et al. 2004; Sharifi et al. 2007). A re-circulating solution culture system wasdesigned using of a series of PVC pipes 15 cm indiameter and 3 m in length. Each pipe had aninlet and an outlet to let the nutrient solutioncirculate continuously. Solution level was main-tained at 2 cm below the top of each pipe. Thenutrient solution was pumped from a 125-L res-ervoir to the inlet of the appropriate pipe using asubmersible pump with a flow rate of about2 L min –1 . The nutrient solution drained from theoutlet of the pipe to the reservoir by gravity.Plants were supported by 7.5 cm diameterneoprene rings fitted to 7.5 cm diameter plasticbaskets. The baskets were placed in 7.5 cmdiameter holes cut in the PVC pipes. Plantletswere spaced 35 cm apart in each pipe.A modified Hoagland solution (Hammeret al. 1978) was used. The 0.5 mM NaCl wasreplaced by 0.25 mM CaCl 2  and twice the con-centration of MoO 4–2 was used. The pH of thesolution was maintained between 6 and 6.4 bydaily adjustments with HCl or KOH. SolutionNO 3– concentration was adjusted to 1 mM,checked continuously using a NO 3– electrodeconnected to a data logger, and the amount of NO 3– removed by uptake was replenished bycontinuous addition of 1.0 mM NO 3– asCa(NO 3 ) 2  using a peristaltic pump.Depletion experiments were then conducted onthe appropriate sampling dates (10, 17 and 22DAT) using three replicates of the five potatocultivars where a replicate consisted of anindividual plant. The nutrient solution was re-placed by the modified Hoagland solution with0.15 mM NO 3– approximately 4 h before the NO 3– depletion rate was measured (Drew et al. 1984).Subsequently, each plant was placed in a 3-L potwith the modified Hoagland solution with0.15 mM NO 3– (Steingrobe and Schenk 1994). Thenutrient solution was aerated continuously to havean oxygen-saturated solution. A 10 mL sample of the nutrient solution was taken continuously overeach 10-min period for 240 min, then over each20-min period for an additional 360 min, using aperistaltic pump. The samples were kept frozen at–20  C until analysis. The solution NO 3– concen-tration was determined colorimetrically using aTechnicon TRAACS 800 auto-analyzer with a1.4  l M NO 3 –N detection limit. The solution vol-ume was not kept constant during depletion toavoid dilution or other disturbance. The actualsolution volume at each sampling time was inter-polated between the volume measured at thebeginning and at the end of the experiment. Thus,losses by sample removal and by transpirationwere accounted for (Steingrobe and Schenk 1994).The uptake kinetic parameters were calcu-lated assuming that when plants are grown in asolution of a certain volume,  V  , the decrease inNO 3– content of the solution measures the netamount of the respective NO 3– absorbed (Claas-sen and Barber 1974). The quantity of NO 3– innutrient solution,  Q , is given by  Q  =  CV   where C   is the NO 3– concentration in solution. A plot of  Q  versus time,  t  , gives a curve showing thedepletion of NO 3– from solution resulting fromplant absorption, hereafter referred to as adepletion curve. The slope of the depletioncurve at any given time represents the net influxat that time, and can be estimated as –d Q /d t  , thefirst derivative of the depletion curve (Claassenand Barber 1974). Nitrate kinetic parameterswere then estimated by fitting Eq. 1, as modifiedby Nielsen and Barber (1978), to the relationshipbetween net influx and  C  . Equation 1 describesnet influx of a nutrient into plant roots as afunction of external concentrations of thisnutrient:  I  n  ¼  I  max ð C     C  min Þ K  m  þ  C     C  min ð 1 Þ Plant Soil (2006) 288:91–99 93  1 3  where  I  n  is net influx (pmol cm –1 s –1 ),  I  max  ismaximum influx (pmol cm –1 s –1 ),  C   is concentra-tion at the root surface ( l M),  C  min  is minimumconcentration ( l M) at which no net influx occursand  K  m  is Michaelis constant ( l M).Immediately after the depletion experiment,each plant was partitioned into roots and shoots.Roots were optically scanned and RL and averagediameter (RAD) were measured (Sharifi et al.2007) using WinRHIZO Version 2002C PROsoftware (Arsenault et al. 1995). Roots and shootswere dried at 55  C, weighed and the N concentra-tion was determined by combustion (Leco CNS–1000). Relative growth rate (RGR) was calculatedfor the second and third sampling dates asRGR  ¼ ½ð ln  W  t  2    ln  W  t  1 Þ = ð t  2    t  1 Þ  where  W   isplant dry matter (g) and  t  1  and  t  2  are successiveharvest dates(day).Plant nitrogen demand(PND)was calculated as RGR multiplied by plant Nconcentration (PNC).Data were subjected to Analysis of Varianceusing the General Linear Model of SAS (SASInstitute Inc., Cary, NC, USA, Version 8) whichtreated cultivar and time as two factors in a fac-torial experiment. Treatment means were com-pared using Fisher’s Protected Least SignificantDifference (LSD 0.05 ) test. Results and discussion Mean values of   I  max  for the five cultivars overthree sampling dates ranged from 0.79 to7.62 pmol cm –1 s –1 with an average value of 2.44 pmol cm –1 s –1 (Table 1). These values fallwithin the range of   I  max  values reported for her-baceous plants at comparable plant age, forexample 1.3 pmol cm –1 s –1 for peas (Robinson1986), 4–6 pmol cm –1 s –1 for rape (Bhat et al.1979; Robinson 1986), 0.44–1.04 pmol cm –1 s –1 for sugar beet (Strebel and Duynisveld 1989),0.20–2.50 pmol cm –1 s –1 for lettuce (Steingrobeand Schenk 1994) and 0.3 and 0.6 pmol cm –1 s –1 for spinach and kohlrabi, respectively (Steingrobeand Schenk 1991). The average values of   I  max measured in this study are lower than values re-ported for cereals and grasses ( ‡ 3.0 pmol cm –1 s –1 )(Barber 1995; Peuke and Jeschke 1998). The po- tato crop, which has a more limited and shallowroot system (Sharifi et al. 2005) and lower valuesof NO 3–  I  max  compared with cereal crops, wouldtherefore be expected to be less efficient in NO 3– uptake compared with cereal crops. This reducedefficiency of NO 3– uptake, the generally high fer-tilizer N inputs used in potato production, and thelight textured soils preferred in commercialpotato production contribute to the significantNO 3– leaching measured under potato production(Errebhi et al. 1998).The value of   I  max  decreased over time from anaverage of 5.13 pmol cm –1 s –1 at 10 DAT to0.98 pmol cm –1 s –1 at 22 DAT (Tables 1, 2;Fig. 1). Jungk and Barber (1975) measured the P influx kinetic parameters of corn seedlings Table 1  Kinetic (Michaelis–Menten) parameters for NO 3– uptake by five potato cultivars at 10, 17 and 22 days aftertransplanting (DAT)Sampling date (DAT) Parameter Cultivar MeanAtlantic Chieftain Red Pontiac Russet Norkotah Shepody10  I  max  4.25 6.56 2.09 7.62 5.14 5.13 a K  m  13.4 12.9 15.9 13.8 12.8 13.8 a C  min  1.71 1.45 1.14 1.20 1.10 1.32 a 17  I  max  1.03 1.05 0.91 1.27 1.02 1.04 b K  m  11.4 17.3 15.8 14.2 13.4 14.2 a C  min  1.05 1.24 1.92 1.26 1.28 1.37 a 22  I  max  1.11 0.80 0.89 1.28 0.79 0.98 b K  m  11.2 12.7 16.9 13.8 12.1 13.3 a C  min  1.00 0.94 2.01 1.00 1.41 1.27 a Mean  I  max  2.13 c 3.02 b 1.30 d 3.65 a 2.32 c K  m  12.0 b 13.9 b 16.2 a 13.9 b 12.8 b C  min  1.26 b 1.21 b 1.69 a 1.14 b 1.26 b The  I  max , K  m and C  min reportedunitsarepmol cm –1 s –1 , l Mand l M,respectively.Dataaremeansofthreereplications( n  = 3).Means for a given parameter followed by the same letter are not significantly different based on a protected LSD 0.05  test94 Plant Soil (2006) 288:91–99  1 3  from 12 until 80 days after seeding. They reportedthat maximum  I  max  occurred at 28 days anddeclined sharply thereafter. Similar observationswere made by Edwards and Barber (1976) for N,and Elgawhary et al. (1972) for Ca and Sr in corn.The reduction in calculated  I  max  as the plantsmatured may have been due to a reduced uptakerate by older roots (Bar-Yosef and Kafkafi 1971)and/or to a reduced proportion of the root systemactive in uptake (Robinson et al. 1991). However,Kuhlmann and Barraclough (1987) showed thatthe decrease of   I  max  with plant age was not due toa lower uptake capacity of older roots, but ratherto a decreased demand that had to be satisfied perunit RL. The nutrient demand during the lineargrowth phase is nearly constant, but the rootsystem is still growing, resulting in lower demandper unit RL (Barber 1995). In this study,  I  max  andRL were negatively correlated (Fig. 2) whichsuggests that the reduction in  I  max  was likely dueto decreasing demand for nitrate per unit of RL.The reduction of   I  max  with increasing RL wasmuch greater at 10 DAT than at 17 and 22 DAT.This may be related to faster development of roots during early plant growth.Thereweresignificantdifferencesin  I  max amongcultivars (Table 2). In addition, there was a sig-nificant cultivar by time interaction on  I  max . At 10DAT, values for  I  max  were highest for RussetNorkotahandChieftain,intermediateforShepodyand Atlantic and lowest for Red Pontiac (Table 1;Fig. 1).Asimilarpatternwas measuredat17DATexcept that  I  max  values for Chieftain were similarto values for Shepody and Atlantic. At 22 DAT,the  I  max  values were higher for Russet Norkotah AtlanticChieftainRed PontiacRusset NorkotahShepody00.20.40.60.811.2    N   O    3   -   n  e   t   i  n   f   l  u  x   (  p  m  o   l   c  m   -   1    s   -   1    )  a   t   1   7   D   A   T aabb 0 50 100 150 01234567    N   O    3   -    n  e   t   i  n   f   l  u  x   (  p  m  o   l   c  m   -   1    s   -   1    )  a   t   1   0   D   A   T aabbccd 0 50 100 15000.20.40.60.811.20 50 100 150Solution NO 3 - concentration (µM)    N   O    3   -   n  e   t   i  n   f   l  u  x   (  p  m  o   l  c  m   -   1    s   -   1    )  a   t   2   2   D   A   T  aab Fig. 1  The nitrate net influx (  I  n ) of five potato cultivars asa function of solution NO 3– solution concentration ( C  ) atthree sampling dates (10, 17 and 22 days after transplant-ing (DAT)). The  curves  were calculated using theMichaelis–Menten kinetic equations. Calculated maximumvalues for  lines  with the  same letter   are not significantlydifferent based on a protected LSD 0.05  test Table 2  Analysis of variance for NO 3– kinetic uptake(Michaelis–Menten) parameters of potato as affected bycultivar and sampling dateSource of variationMean square df I  max  K  m  C  min Cultivar ( C  ) 4 5.08*** 23.02** 0.401*Sampling date ( T  ) 2 82.45*** 4.27 ns 0.021 ns T   ·  C   8 4.06*** 4.83 ns 0.366**Error 28 0.24 4.25 0.12 CV   (%) 20.1 15.0 26.2ns, ***, ** and * non-significant or significant at  P   £  0.001, P   £  0.01 and  P   £  0.05, respectivelyPlant Soil (2006) 288:91–99 95  1 3
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