Yinshui LI,Changbing YU,Lihua XIE,Xiaojia HU,Lu QIN,Xiangsheng LIAO,Xing LIAO

Oil Crops Research Institute of the Chinese Academy of Agricultural Sciences,Key Laboratory of Biology&Genetic Improvement of Oil Crops,Ministry of Agriculture,No.2,Xudong 2 Road,Wuhan 430062,China

Rapeseed(Brassica napusL.)is one of the major oilseed crops in China,with the planting area and total yield accounting for 23.5%and 22.6%of world tallies,respectively[1].Since 2000,rapeseed planting area in China has reached 7.0×107hm2,and total yield has increased to more than 1.1×107t,which provides about 4.0×106t of cooking oil each year[2].This crop plays a very significant role in ensuring cooking oil and plant protein supplies for China,and contributes to increasing farmer incomes.To date,rapeseed production has maintained stable and sustainable growth.Yet fundamental issues remain to be addressed in order for these trends to continue.

Chinese rapeseed production has developed rapidly,with improvements being realized not only in cultivation techniques,but,particularly in breeding for high yielding cultivars.Since 1950,there have been three major changes related to rape cultivars grown in China.The first was thatBrassica napusreplacedB.campestrisas the primary species of cultivated rapeseed.The second was that double low cultivars in regard to glucosinolate and erucic acid replaced double high cultivars.The third development was the shift from double low cultivars to primarily utilize hybrid varieties.At present,incorporation of heterosis in Chinese rapeseed breeding efforts has reached the level of advanced agriculture throughout the world,with more than 90%of the double low cultivars now being registered hybrids that account for about 70%of the total area planted in rapeseed[3],which is much higher than the global average of 40%[4].

Heterosis is an important path to increase crop yield[5].Under adequate fertilizer application,hybrid cultivars produce 33%higher yields than openpollinated cultivars[6].As more nutrients are typically required to support higher yields,Mahliet al.[7]suggested that fertilizer rates and other crop management practices need to be revised in order to fully realize yield potentials associated with improved genetic and breeding efforts,especially the need to develop separate management recommendations for open-pollinated versus hybrid rapeseed cultivars.

Rapeseed has a relatively high demand for nitrogen (N),because content of this nutrient in seeds and plant tissues is greater in rape than in most grain crops[8].Therefore,high rates of N fertilizer are commonly applied to maximize yields and quality of rapeseed harvests[9].Previous investigation by Karamanoset al.[6]indicated that N requirements for optimum seed yield are 34 kg/hm2higher for hybrid cultivars than for open-pollinated cultivars.Zhaoet al.[10]also showed that in order to realize peak yields of 2898 and 2870 kg/hm2for the hybrid cultivars"Youyan 599"and"Sanbei 98",the total amounts of N required were 310 and 316 kg/hm2,respectively.This amount of N is significantly higher than the optimum N application rate of 150 kg/hm2in Hubei Province,China[11].In a comparison of hybrid and open-pollinated cultivars,Mahliet al.[7]found that the high yielding hybrid"InVigor 2663"produced more biomass and seed yield than a high yielding open-pollinated cultivar,"Quantum".However,seed yields of two cultivars responded similarly to changes in N application,and the target N fertilizer rates for optimum seed yield were similar for both cultivars when grown in Saskatchewan,Canada.

Rapeseed has a high N uptake efficiency from soil,but a relatively low N utilization efficiency (NUE)[12].Rathkeet al.[13]reported that rapeseed yield responses to increasing N application varies among cultivars and it is affected by environmental variables,including weather,soil type,residual fertility(especially nitrate),and soil moisture.Genotypic differences in rapeseed NUE have been documented by many researchers.Sve cˇnjak and Rengel[8]reported that while significant variation occurs in dry weight,N concentration and N uptake among various rapeseed tissues,no consistent patterns in the variation of N concentration among various tissues could be established for the tested cultivars.In contrast,with 14 genotypes of Indian mustard(Brassica junceaL.),Altafet al.[14]found that N uptake efficiency is positively correlated with plant biomass,leaf area index,and leaf N content,and that N use efficiency is positively correlated with photosynthetic rate and yield.This suggests that genotypes possessing high N uptake efficiencies and high physiological N use efficiencies might require less N fertilization without any penalty to the yield.

Improving NUE is an important target for either increasing yields or reducing fertilizer costs[15].Hybrid cultivars generally produce more biomass and seed yield than conventional cultivars,which provides greater net economic returns under both moist and relatively dry conditions[7].If these gains can be realized without increasing N fertilization,then NUE can be an important component of efforts to improve rapeseed cultivation.The objective of this study is to text the hypothesized that the nitrogen use efficiency of hybrid rapeseed cultivars ZY5628 and ZY7819 are higher than that of conventional cultivar ZS10.A difference in NUE might explain differences observed between these cultivars in seed yield and biomass.Furthermore,a difference in NUE will allow reducing the N fertilization rate for hybrid cultivars ZY5628 and ZY7819 compared to the conventional cultivar ZS10.

Materials and Methods

Experimental site

Field experiments were carried out in 2011 and 2012 at the Yangluo Research Station of the Oil Crop Research Institute (OCRI),Chinese A-cademy of Agricultural Science(CAAS),which is located in Wuhan,Hubei Province,China(114°32′N,30°37′E,16.5 m above sea level).The climate is subtropical,with an average annual rainfall of 1214 mm typically falls mainly from April to July.The mean annual evaporation is 1200 mm,and the annual average temperature is 16.6℃,with a frost-free period of 250 d.Two experiments were arranged in the same field.The previous crop was rice.Soil samples from the yellowbrown soilwere analyzed before planting using previouslypublished methods[16].The cultivated layer(0-20 cm)had a pH of 7.59,organic matter of 1.08%,and available N,phosphorus(P)and potassium (K)concentrations of 43.0,5.7 and 111.5 mg/kg,respectively.

Experiment design

An conventional cultivar cv."Zhongshuang No.10"(ZS 10)and two hybrid cultivars cv."Zhongyouza No.5628"(ZY5628)and"Zhongyouza No.7819"(ZY7819)bred by the Oil Crops Research Institute(OCRI)of the Chinese Academy of Agricultural Sciences(CAAS)were selected for planting in the field site.

In experiment 1,the three cultivars listed above,ZS 10,ZY5628 and ZY7819,were each subjected to 5 N application rates of 0 (N0),75(N75),150 (N150),225 (N225)and 300(N300)kg/hm2.In addition,each plot was amended with 90 kg/hm2phosphorus pentoxide (P2O5)120 kg/hm2,potassium oxide(K2O)and 7.5 kg/hm2boron (11%B).With 3 cultivars,5 N treatments and 3 replications,the experiment consisted of a total of 45 plots.

In experiment 2:the same cultivars were planted with the same fertilizer amendments listed above,except N was applied uniformly at 180 kg/hm2.The design consisted of 3 treatments and 3 replications,for a total of 9 plots.

The sources of N,P and K fertilizers were urea(46%N),superphosphate(12%P2O5)and potassium chloride (60%K2O).All fertilizer was applied once during soil preparation.At each experiment,plots were arranged randomly,and each plot being 20 m2(2 m×10 m).Both experiments were started by direct sowing of rapeseed seeds on September 24,2011,and plots for both experiments were harvested on May 11,2012.Each plot contained 28 rows with a row space of 35.7 cm and a density of 1.5×105plants/hm2.Seedlings were thinned to the planned density twice,once at the three-leaf stage,and again at the fiveleaf stage.Field management followed local practices for rapeseed production.

Samplecollectionandmeasurement

In experiment 1,seed yield was measured at maturity,converted to kg per hectare,and then adjusted to water content of 5.2%of fresh weight.

For experiment 2,plant dry weight was measured at the seedling,bud,blooming and maturity stages at 90,160,180,and 230 days after sowing,respectively.Two rows with an area of 1.43 m2were harvested by cutting plants just above the soil,and separated the shoots into vegetative(stem,leaves,and branches)and reproductive organs (flowers,shells and seeds).Roots were carefully harvested bydigging witha spade,then washed clean with water and stored in 0.5 mm-mesh nylon bags.Samples were put into an electric fan-assisted oven at 105℃for 30 min,followed by a drying oven at 70℃until reaching a constant weight.

Samples were ground to≤0.5 mm particles for N analysis.Plant N concentration was determined by the micro-Kjeldahl method[17].N efficiency was calculated as following[13]:

Where FNwas the amount of N rates(kg/hm2),and YN(kg/hm2)was the rapeseed yield of the N treatment.

Statistical analysis

Analysis of variance was conducted in DPSv-8.1,along with mean separation using Fisher’s protected least significant difference(LSD)test with aP=0.05 threshold[18].Rapeseed basic yield,plateau yield and N critical rate(Table 3)were determined by regression analysis in SAS[19].

Results

Yield of rapeseed in experiment 1

Nitrogen application had a noticeable impact on rapeseed yield(Table 1).Seed yield for all three cultivars increased significantly with increasing N application from N0 to N225,but not between N225 and N300.N fertilization led to increased seed yields of 65.3%-198.7%in ZS10,75.1%-152.4% inZY5628and80.8%-162.1%in ZY7819 when compared to the N0 treatment.However,the unit production rate of N fertilizer declined with increasing N application for each of the three cultivars(Table 1).

Although the trend of increasing yield with increasing N application was similar among cultivars,there were still significant differences among genotypes in seed yield.Seed yield was significantly higher for either hybrid rapeseed ZY5628 or ZY7819 than for the open-pollinated rapeseed ZS10,at the same N application rates(Table 1).

Optimum N application for rapeseed yield in experiment 1

Table 2 shows the relationship between N application and seed yield for each of the three tested cultivars as determined by regression analysis.It shows that,for ZY5628 and ZY7819,plateau seed yields were 2 872 and 2 908 kg/hm2,which correspond to N applications of urea at 182 and 181 kg/hm2,respectively.Meanwhile,the plateau yield for ZS10 was only 2 420 kg/hm2,with a corresponding urea N application rate of 200 kg/hm2(Table 2).Therefore,compared to ZS10 in equivalent production conditions,the economic yields for ZY5628 and ZY7819 are increased by 18.7%and 20.2%while N fertilization requirements are reduced by 9.5%and 9.6%,respectively.

Dry matter accumulation in experiment 2

Overall,rapeseed dry matter accumulation increased as plants grew,with the trends following typical organ-ism growth curves through several growth stages(Table 3).Close examination reveals differences in growth patterns between aboveground organ biomass (AOB)and root biomass(RB).As Table 3 shows,AOB continued to increase over the entire course of growth,and reached its maximum at maturity with 7 203,8 506 and 8 603 kg/hm2observed for ZS10,ZY5628 and ZY7819,respectively.On the other hand,RB increased rapidly at bud stage and reached maximum values at the blooming stage,from which RB decreased to the values observed at the maturity stage.The highest RB values observed in ZS10,ZY5628 and ZY7819 were 877,1 032 and 1 158 kg/hm2,respectively.

Table 1 Seed yield and N efficiency of three rapeseed cultivars at the same N application rates.

Table 2 Linear plus plateau regression models for rapeseed(Brassica napus L.)yield from three cultivars regressed against N application

Table 3 Dry mater accumulation in three rapeseed cultivars at four growth stages,from a field amended with 180 kg/hm2N,90 kg/hm2P2O5 and 120 kg/hm2K2O

Table 4 N concentration in different organs of three rapeseed cultivars at four growth stages,from a field amended with 180 kg/hm2N,90 kg/hm2P2O5and 120 kg/hm2K2O

Table 5 Yield and components of N acquisition in three rapeseed cultivars at maturity,from a field amended with N of 180 kg/hm2,P2O5of 90 kg/hm2and K2O of 120 kg/hm2

The three cultivars displayed similar trends in dry matter accumulation,but genotypic differences existed between cultivars.Under equivalent experimental conditions,dry matter accumulation was greater in ZY5628 and ZY7819 than in ZS10,particularly for root biomass.These differences were not evident during the seedling and budding vegetative growth stages,after which,at both the blooming and maturity stages RB was greater for both hybrid cultivars,ZY7819 and ZY5628,and AOB was greater for ZY7819 than for ZS10.By maturity,AOB was greater for both hybrid cultivars than for ZS10.Due to its well developed rootsystem during later growth stages,the root-to-shoot ratio of ZY7819 was significantly higher than that of ZS10 at both the blooming and maturity stages.

Concentration and accumulation of Nin experiment 2

Table 4 illustrates changes in N concentrations within different organs of three rapeseed cultivars sampled four times from the seedling stage to maturity.During vegetative growth,leaf N concentrations were higher than in stems,branches or roots.Leaf N concentrations also peaked during vegetative growth and decreased during reproductive growth.In reproductive stages,the highest concentrations of N by significant margins were found in flowers and the seeds.N concentrations in roots were lower than in leaves and decreased through all developmental stages.Thus,at maturity,N concentrations in roots had dropped to 0.53%,0.51%and 0.48%,which represented declines of 81.9%,83.4%and 85.4%from the seedling stage for ZS10,ZY5628 and ZY7819,respectively.

During vegetative growth,the only significant difference found in N concentration among the three cultivars was observed at the bud stage between roots of the hybrid cultivars and those of the open-pollinated cultivar.In the blooming stage,the N concentration was higher in leaves of the openpollinated cultivar ZS10 than in leaves of the hybrid cultivar ZY5628,while it was lower in flowers of ZS10 than in flowers of ZY5628.At maturity,N concentrations stems,branches,and roots were all significantly lower in ZY7819 than in ZS10.

N accumulation increased sharply for each cultivar from the seedling stage to the blooming stage,after which,a slight decline was observed at maturity (Fig.1). The maximum amounts of accumulated N observed were 109.7,122.1 and 130.6 kg/hm2during the blooming stage,with 47.3%,56.1%and 58.9%of this N located in leaves and flowers of ZS10,ZY5628 and ZY7819,respectively.At maturity,the total N accumulation reduced to 101.1,115.8 and 116.6 kg/hm2,with 68.2%,68.5%and 74.2%of this N localized in seeds of ZS10,ZY5628 and ZY7819,respectively.

Total N accumulation varied significantly among the tested rapeseed cultivars.The N accumulation in ZY5628 and ZY7819 was significantly higher than in ZS10 at each growth stage,except the seedling stage.

N utilization efficiency in experiment 2

Table 5 shows N use efficiency varied significantly among the tested rapeseed cultivars.At the tested N application rate of 180 kg/hm2,both the N uptake efficiency and the N utilization efficiency were significantly greater for the hybrid rapeseed cultivars ZY5628 and ZY7819 than for the open-pollinated cultivar ZS10.The differences in N use efficiency were such that,in order to obtain 100 kg of seed,the required N application rates for ZY5628 and ZY7819 were 8.0%and 14.0%less,respectively,than for ZS10.

Discussion

The present study demonstrated that,at the same levels of N availability,seed yield was greater for two hybrid cultivars,ZY5628 and ZY7819,than for an open-pollinated cultivar,ZS10 (Table 1).Furthermore,less N was required to reach plateau yields were 2 872 and 2 908 kg/hm2for the hybrid cultivars than for the open-pollinated cultivar was 2420 kg/hm2(Table 2).These results suggest that hybrid cultivars ZY5628 and ZY7819 can be economically viable alternatives for increasing yield and reducing N application rates in rapeseed.

Rapeseed yield determined by N availability can be broken down into two components,N uptake efficiency and N utilization efficiency[20].At low N availability,N uptake may be the major determinant of yield,while at higher N availabilities,N utilization efficiency can become more important[21].A complicating factor in this analysis is that yield differences have been found among rapeseed genotypes at both low and high N supplies[22].

Knowledge of expected plant N concentration and biomass or stand density in the field are prerequisites for optimizing N application rates[23].Dry weights of stems,leaves,siliques,and seeds have all been noted to vary among genotypes[24].These biomass differences might occur despite similar total plant N uptake among cultivars due to differences in NUE,which allows more N-efficient cultivars to produce more biomass with lower N concentrations compared with less N-efficient cultivars[8].At high N supply,cultivars with low seed N concentration can be superior in seed yield[21].

N concentration and biomass accumulation can vary among cultivars,as the present study shows.For example,in growth from the seedling stage to the bud stage,root N concentrations werehigherinbothZY5628and ZY7819 than in ZS10.More obviously,dry matter accumulation was greater for both ZY5628 and ZY7819 than for ZS10 at all stages from budding to maturity.Due to greater accumulation of both biomass and N throughout development,the hybrid rapeseed cultivars ZY5628 and ZY7819 have higher N use efficiency than the open-pollinated cultivar ZS10(Table 5).

Roots are indispensible for rapeseed acquisition of water and mineral nutrients[25].Therefore,specific root phenotypes,such as root morphology,root to shoot ratios,root vigor,and root length density can each have effects on plant N acquisition and assimilation[26-27].Hirelet al.[28]found that spring canola differences in NUE were due to differences in the root to shoot ratio and harvest index.Berryet al.[15]showed that the amount of N taken up after flowering was the most important phase of N uptake for determining yield differences between varieties.Consistent with this,a primary strategy for improving N efficiency in rapeseed may be to prolong N uptake during reproductive growth[29].Consistent with this,in the present study,root biomass accumulation in the hybrid rapeseed cultivars ZY5628 and ZY7819 was higher than in the open-pollinated cultivar ZS10during reproductive growth.At seedling stage,total N accumulation did not vary between ZS10 and ZY7819.At later stages,due to the well developed root system of ZY7819,growth was greater in the hybrid cultivar.Moreover,total N accumulation in ZY7819 reached 130.6 kg/hm2at the blooming stage,with 58.9%of this N located in leaves and flowers.This N accumulation was significantly higher than the 109.7 kg/hm2of N accumulating in ZS10,of which 47.3%was located in leaves and flowers.Taken together,these results suggestthat higher efficiency of N use in hybrid rapeseed cultivars ZY5628 and ZY7819 compared to the open-pollinated cultivar ZS10 might be related to the well developed root system in the hybrid cultivars,along with an ability to mobilize more Ninto flowers and seeds during reproductive growth.

Ulaset al.[29]reported that N efficientgenotypes had highergrain yields at N0 than Ninefficient genotypes,which indicates an ability to grow and yield well under low N conditions[14].Hockinget al.[30]study showed that the maximum dry-matter production and seed yields of rapeseed occurred at an application rate of N at 75 kg/hm2to two fields in Australia.Urbaniaket al.[31]indicated that applying N can increase rapeseed yield,but this increase was not significant in Canadian fields when the application rates were over 60-80 kg/hm2.Considering that hybrid varieties might be more efficient scavengers of soil nutrients,Karamanoset al.[6]stated that planting of hybrids might lead toserious ramifications in regards to the fertility available for following crops.In practice,Ninput rates reach 200 kg/hm2in the Yangtze River Valley in China[32].Under the experimental conditions in the current study,total N accumulation in mature rapeseed reached 101.1,115.8 and 116.6 kg/hm2for ZS10,ZY5628andZY7819,respectively.These values all fall far below the optimum N application rate of 180 kg/hm2.Plus,much of the N stored in vegetative organs is not removed from the field[28],because a large quantity of it is lost in early falling leaves before maturity and harvest[33].Furthermore,according to Brennan and Bolland[34],applying more N might decrease the quality of rapeseed,which means that increasing N application rates can not only reduce seed oil concentration and increase seed protein concentration,but it may also decrease the rapeseed concentrations of oleic acid and eicosenoic acid[31].Therefore,development of hybrid rapeseed appears to be practical and profitable in terms of a high rapeseed yields and reduced production costs,while potentially reducing environmental harm caused by excessive N fertilization without jeopardizing nutrient availability for future crops.

Conclusion

Compared with conventional rapeseed (ZS10),hybrid rapeseed(ZY5628andZY7819)hadmore biomass accumulation and N accumulation throughout the growing season,especially during reproductive growth.Therefore,with N application being constant,seed yield and N use efficiency of hybrid rapeseed ZY5628 and ZY7819 are higher than for the conventional rapeseed ZS10.In addition,the plateau yield is significantly higher,with less N application required to reach this plateau,for hybrid rapeseed ZY5628 and ZY7819 than for the conventional rapeseed ZS10.These results suggest that cultivation of hybrid rapeseed ZY5628 and ZY7819 with higher N use efficiency than the conventional rapeseed ZS10 can be profitable through realization of higher seed yields at lower production costs,and indicating that hybrid rapeseed does not need more N fertilizer than conventionalrapeseed to support higher yields.

[1]YIN Y(殷艳),WANG HZ(王汉中).Achievement,problem andscientific policy of rape seed industry development in China(我国油菜产业发展成就、问题与科技对策)[J].Journal of Agricultural Science and Technology(中国农业科技导报),2012,14(4):1-7.

[2]YIN Y(殷艳),WANG HZ(王汉中),LIAO X(廖星).Analysis and strategy for 2009 rape seed industry development in China(2009年我国油菜产业发展形势分析及对策建议)[J].Chinese Journal of Oil Crop Sciences(中国油料作物学报),2009,31(2):259-262.

[3]FU TD,ZHOU YM.Progress and future development of hybrid rapeseed in China[J].Engineering Sciences,2013,11:13-18.

[4]FU TD(傅廷栋).Rape seed variety improvement and mechanization in China(油菜生产品种改良与机械化)[J].Agricultural Equipment&Technology(农业装备技术).2010,36(2):22-25.

[5]WANG J,GAO YN,KONG YQ,et al.Abortive process of a novel rapeseed cytoplasmic male sterility line derived from somatic hybrids betweenBrassica napusandSinapis alba[J].Journal of Integrative Agriculture,2013,13:741-748.

[6]KARAMANOS RE,GOH TB,POISSON DP.Nitrogen,phosphorus,and sulfur fertility of hybrid canola[J].Journal of plant nutrition,2005,28:1145-1161.

[7]MAHLI SS,BRANDT SA,ULRICH D,et al.Comparative nitrogen response and economic evaluation for optimum yield of hybrid and open-pollinated canola[J].Canadian journalofplantscience,2007,87:449-460.

[8]SVE?NJAK Z,RENGEL Z.Canola cultivars differ in nitrogen utilization efficiency at vegetative stage[J].Field Crop Research,2006,97:221-226.

[9]SCHJOERRING JK,BOCK JG,GAMMELVIND H,et al.Nitrogen incorporation and remobilization in different shoot components offield grown winter oilseed rape(Brassica napusL.)as affected by rate of nitrogen application and irrigation[J].Plant and Soil,1995,177:255-264.

[10]ZHAO JX,REN TB,CHENG GP.Effects of nitrogen application amount during various periods on yield of high grade hybrid rape seed[J].Agricultural Science&Technology,2012,13:1292-1297.

[11]LI YS(李银水),LU JW(鲁剑巍),LIAO X(廖星).et al.Effect of nitrogen application rate on yield and nitrogen fertilization efficiency in rape seed(氮肥用量对油菜产量及氮素利用效率的影响)[J].Chinese Journal of Oil Crop Sciences(中国油料作物学报),2011,33:379-383.

[12]ROSSATO L,LAINÉ P,OURRY A.Nitrogen storage and remobilization inBrassica napusL.during the growth cycle:nitrogen fluxes within the plant and changes in soluble protein patterns[J]. Journal of Experimental Botany,2001,52:1655-1663.

[13]RATHKE GW,BEHRENS T,DIEPENBROCK W.Integrated nitrogen management strategies to improve seed yield oil content and nitrogen efficiency of winter oilseed rape(Brassica napusL.):a review[J].Agriculture Ecosystems&Environment,2006,117:80-108.

[14]ALTAF A,KHAN I,ABROL YP,et al.Genotypic variation of nitrogen use efficiency in Indian mustard[J].Environmental Pollution,2008,154:462-466.

[15]BERRY PM,SPINK J,FOULKES MJ,et al.The physiological basis of genotypic differences in nitrogen use efficiency in oilseed rape(Brassica napusL.)[J].Field Crop Research,2010,119:365-373.

[16]BAO SD(鲍士旦).Analysis methods for agricultural chemistry in soil(土壤农化分析)[M].China Agricultural Press(中国农业出版社),Beijing,2000,285-287.

[17]OZER H.Sowing date and nitrogen rate effects on growth,yield and yield componentsoftwosummerrape seed cultivars[J].European Journal of Agronomy,2003,19:453-463.

[18]TANG QY,ZHANG CX.Data processing system (DPS)software with experimental design,statistical analysis and data mining developed for use in entomological research[J].Insect Science,2013,20:254-260.

[19]SAS Institute Inc 1999:SAS/STAT user’s guide,Version 8.1,Cary,NC,1999.

[20]SATTELMACHER B,HORST WJ,BECKER HC.Factors that contribute to genetic variation for nutrient efficiency of crop plants[J].Journal of Plant Nutrition and Soil Science,1994,157:215-224.

[21]SCHULTE AUF‘M ERLEY G,BEHRENS T,Ulas,et al.Agronomic traits contributing to nitrogen efficiency of winter oilseed rape cultivars[J].Field Crop Research,2011,124:114-123.

[22]MÖLLERS C,KESSEL B,KAHLMEYER M,et al.Untersuchungen zur genotypischen Variabilität der Stickstoff-Effizienz bei Winterraps, In:Möllers,C. (Ed.),Stickstoffeffizienz landwirtschaftlicher Kulturpflanzen[M].Erich Schmidt,Berlin,2000,30-47.

[23]THOREN D,SCHMIDHALTER U.Nitrogen status and biomass determination of oilseed rape by laser-induced chlorophyll fluorescence[J].European Journal of Agronomy,2009,30:238-242.

[24]BALINT T,RENGEL Z.Nitrogen efficiency of canola genotypes varies between vegetative stage and grain maturity[J].Euphytica,2008,164:421-432.

[25]WHU L,MCGECHAN MB,WATSON CA,et al.Developing existing plant root system architecture models to meet future agricultural challenges[J].Advances in Agronomy,2005,85:181-219.

[26]GARNETT T,CONN V,KAISER BN.Root based approaches to improving nitrogen use efficiency in plants[J].Plant Cell and Environment,2009,32:1272-1283.

[27]PERKONS U,KAUTZ T,UTEAU D,etal.Root-length densities of various annual crops following crops with contrasting root systems[J].Soil Tillage Research,2014,137:50-57.

[28]HIREL B,GOUIS JL,NEY B,et al.The challenge of improving nitrogen use efficiency in crop plants:towards a more central role for genetic variability and quantitative genetics within integrated approaches[J].Journal of Experimental Botany,2007,58:2369-2387.

[29]ULAS A,SCHULTE AUF’M ERLEY G,KAMH M.et al.Root-growth characteristics contributing to genotypic variation in nitrogen efficiency of oilseed rape[J].Journal of Plant Nutrition and Soil Science,2012,175:489-498.

[30]HOCKING PJ,RANDALL PJ,DEMARCO D.The response of dry land canola to nitrogen fertilizer:partitioning and mobilization of dry matter and nitrogen,and nitrogen effects on yield components[J].Field Crop Research,1997,54:201-220.

[31]URBANIAK SD,CALDWELL CD,ZHELJAZKOV VD,et al.The effect of cultivar and applied nitrogen on the performance ofCamelina sativaL.in the Maritime Provinces of Canada[J].Canadian Journal of Plant Science,2008,88:111-119.

[32]LI YS(李银水),YU CB(余常兵),LIAO X(廖星),et al.Investigation of present fertilization on crops by different rapeseed rotation systems in Hubei Province(湖北省不同油菜轮作模式下作物施肥现状调查)[J].Chinese Agricultural Science Bulletin(中国农学通报),2012,28(36):205-211.

[33]MALAGOLI P,LAINE P,ROSSATO L,et al.Dynamics of nitrogen uptake and mobilization in field-grown winter oilseed rape (Brassica napus)from stem extension to harvest[J].Annals of Botany,2005,95:853-861.

[34]BRENNAN RF,BOLLAND MDA.Effect of fertilizer phosphorus and nitrogen on the concentrations of oil and protein in grain and the grain yield of canola (Brassica napusL.)grown in south-western[J].Australian journal of agricultural research,2007,47:984-991.