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Asymmetric warming effects on N dynamics andproductivity in rice (Oryza sativa L.)Xiaojin Xiea, Yaohong Zhanga, Renying Lia, Xihua Yangb, Shuanghe Shena, Yunxuan Baoa,Xiaohui Shena & Xiaodong Jianga

a Jiangsu Key Laboratory of Agricultural Meteorology, Nanjing University of InformationScience and Technology, 219 Ningliu Road, Nanjing, 210044, P.R. Chinab New South Wales Office of Environment and Heritage, 10 Valentine Ave, Parramatta, 2150,AustraliaPublished online: 26 Jun 2014.

To cite this article: Xiaojin Xie, Yaohong Zhang, Renying Li, Xihua Yang, Shuanghe Shen, Yunxuan Bao, Xiaohui Shen &Xiaodong Jiang (2014) Asymmetric warming effects on N dynamics and productivity in rice (Oryza sativa L.), Soil Science andPlant Nutrition, 60:4, 530-539, DOI: 10.1080/00380768.2014.907531

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ORIGINAL ARTICLE

Asymmetric warming effects on N dynamics and productivity in rice(Oryza sativa L.)

Xiaojin XIE1, Yaohong ZHANG1, Renying LI1, Xihua YANG2, Shuanghe SHEN1,Yunxuan BAO1, Xiaohui SHEN1 and Xiaodong JIANG1

1Jiangsu Key Laboratory of Agricultural Meteorology, Nanjing University of Information Science and Technology, 219 NingliuRoad, Nanjing, 210044, P.R. China and 2New South Wales Office of Environment and Heritage, 10 Valentine Ave, Parramatta,2150, Australia

Abstract

Climate warming exhibits strong diurnal variations, with higher warming rates being observed at nighttime,which significantly affects rice (Oryza sativa L.) growth and grain yield. The objective of this study was todetermine the effects of asymmetric warming (all-day warming, AW; daytime warming from 07:00 to 19:00,DW; nighttime warming from 19:00 to 07:00, NW, and a control, CK) on rice nitrogen (N) dynamics andproductivity. Two rice bucket warming experiments were performed in Nanjing in Jiangsu Province, China,using the free air temperature increase (FATI) technique. The daily mean temperatures in the rice canopy in theAW, DW and NW plots were 2.0, 1.1 and 1.3ºC higher than those in the rice canopy in the CK plots,respectively. The results indicated that the total N accumulation of rice was 8.27–40.53% higher in thewarming treatment than in the control during the jointing, anthesis and maturity stages. However, therewas no significant difference detected among the three warming treatments. The warming treatment substan-tially decreased N translocation efficiency, leading to the retention of more N in the plant stems during grainfilling. The warming treatment also decreased the N harvest index, N utilization efficiency based on grain yieldand N utilization efficiencies based on biomass in both growing seasons. The warming treatment significantlyincreased the aboveground biomass (9.26–16.18%) in the jointing stage but decreased it (2.75–9.63%) in thematurity stage. Although DW increased the carbon (C) gain by photosynthesis andNW increased the C loss bynight respiration, the daytime higher-temperature treatment affected rice photosynthesis and reduced itsphotosynthetic rate and product. This effect may be one of the primary reasons for the insignificant differencein the aboveground biomass between the DW and NW treatments. In the AW, DW and NW plots, the grainyield was reduced by an average of 10.07, 5.05 and 7.89%, respectively, across both years. The effectivepanicles and grains per spike tended to decrease in the warmed plots, whereas irregular changes in the1000-grain weight were observed. Our results suggest that under the anticipated climate warming, riceproductivity would further decline in the Yangtze River Basin.

Key words: Free air temperature increase (FATI), asymmetric warming, nitrogen, grain yield, Oryza sativa L.

INTRODUCTION

Climate warming is one of the most significant environ-mental problems in the modern world. The global

average temperature has increased by 0.56 to 0.92°Cover the past century, and it is now predicted that theglobal temperature will be 1.4 to 5.8°C warmer by theyear 2100 (IPCC 2007). Indeed, air temperatures havebeen observed to increase rapidly, a process that showsdistinct asymmetry: the increase of the minimum tem-perature at night is nearly twice that of the maximumtemperature in the daytime (Harvey 1995; Easterlinget al. 1997). Such unprecedented changes in the differ-ential increase of the daytime/nighttime temperature

Correspondence: X. XIE, Jiangsu Key Laboratory ofAgricultural Meteorology, Nanjing University of InformationScience and Technology, 219 Ningliu Road, Nanjing, 210044,P.R. China. Email: xxj_200210@sina.comReceived 22 July 2013.Accepted for publication 19 March 2014.

Soil Science and Plant Nutrition (2014), 60, 530–539 http://dx.doi.org/10.1080/00380768.2014.907531

© 2014 Japanese Society of Soil Science and Plant Nutrition

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could have important effects on crop production (Lobelland Asner 2003; Tao et al. 2008; Fang et al. 2012).Rice (Oryza sativa L.) is the major grain produced in

China, accounting for approximately 40% of the totalgrain output. However, rice production is markedlyaffected by elevated air temperature. Safe rice productionhas aroused an extremely large amount of interest fromthe Chinese government and researchers (Cheng et al.2008; Dong et al. 2011). To date, many studies havebeen conducted to examine the effects of elevated airtemperature on rice growth and yield (Lobell et al.2008; Cheng et al. 2010). For example, Peng et al.(2004) showed that the rice yield decreased by 10%under a 1°C increase in the daily minimum temperature.Sheehy et al. (2006) found that the rice yield declined by13.70% under a 1°C elevation of the daily minimumtemperature by analyzing a crop model. Dong et al.(2011) also observed that nocturnal warming signifi-cantly decreased rice yield and aboveground biomass.These results show that warming treatments shorten therice growth stage, decrease photosynthetic capacityand reduce grain yield. On the other hand, elevatedair temperature could potentially enhance nitrogen (N)soil mineralization and thereby alter the N uptake ofplant roots (Patil et al. 2010). Furthermore, internalnutrient utilization would likely be affected by thedifference in physiological processes as a result of ele-vated temperature (Prieto et al. 2009), which exerts aprofound impact on plant production (Li et al. 2011).Few studies have reported on the effects of elevated airtemperature on N uptake in crops (Jonassona et al.2004; Yang et al. 2010). Hence, experimental data onthe effect of asymmetric warming on rice N dynamicsand productivity are crucial for developing agriculturaladaptation measures to cope with the potential impactsof climate warming on the agro-ecosystem on a regionaland global scale.N uptake is an important plant process that deter-

mines photosynthetic capacity and plant productivity.Numerous studies, mostly conducted in natural ecosys-tems without N fertilization, have shown that warmingtreatments can either increase or decrease the N accumu-lation of the studied plants. For example, An et al.(2005) observed that a 4-year experimental warmingperiod increased grass N accumulation by 5–20% dueto the increases in the aboveground biomass exceedingthe decreases in the leaf N concentration. However,other studies, conducted in growth chambers, havedemonstrated that high temperatures decrease bothaboveground biomass and leaf N concentration (Xuand Zhou 2005), leading to a reduction in plant Naccumulation. Recently, studies conducted with ricecrops in controlled-environment chambers have indi-cated that high nighttime temperatures have no impact

on whole-plant N concentration but significantlyincrease N absorption (Cheng et al. 2010). However,no study has examined the effects of asymmetric warm-ing on N accumulation and translocation in rice.Artificial simulation experiments have recently been

conducted in plant growth chambers or greenhouses,but the temperature increases generated by thesedevices are set in a manner that is inconsistent withactual climate warming. It is notably difficult to simu-late the features of real climate warming (Klein et al.2005; Cheng et al. 2009). Thus, a field experiment wasperformed in Nanjing, China, to investigate the effectsof asymmetric warming on the rice biomass and grainyield and the nutrient utilization dynamics of theHuaidao5 rice cultivar using a free air temperatureincrease (FATI) apparatus. Our principal objectiveswere (1) to determine the effects of asymmetric warm-ing on rice grain yield and yield components and (2) tocharacterize the N dynamics in response to asymmetricwarming.

MATERIALS AND METHODS

Experimental designTwo experiments (Experiment 1 in 2011 and Experiment2 in 2012) were conducted at the agro-meteorologicalexperimental station (32°07’N, 118°50’E) of NanjingUniversity of Information Science and Technology inJiangsu Province, China, during the rice-growing seasonfrom mid-May to October. This region has a warm,semi-humid monsoon climate. The average yearly preci-pitation is 1100 mm. The average air temperature from2000 to 2010 was 16.6°C, which is 1.4 and 0.7°Cwarmer than that in the 1980s and 1990s, respectively.The average sunshine period is over 1900 h, and thefrost-free period is 237 d.The rice cultivar used in this study was Huaidao5 (con-

ventional Japonica rice), which is widely cultivated inNanjing, China. In both study years, sowing was carriedout on May 18. One seedling was transplanted in eachplastic bucket (25 cm inside diameter, 28 cm height) filledwith 8.0 kg Hapli-stagnic gleysol on June 20. The soil wascollected from the plow layer (~15 cm of the top layer) of arice field in Pukou, Nanjing, China, that contained9.28 g kg−1 organic carbon (C), 1.06 g kg−1 total N,6.89 mg kg−1 available phosphorus (P) and 125 mg kg−1

exchangeable potassium (K). A total of 0.68 g N perbucket [CO(NH2)2] carbamide was split-applied: 50%applied at transplanting, 25% at jointing and 25% atbooting. P and K were applied after planting as calciumsuperphosphate and potassium chloride at a rate of 0.15 gP per bucket and 0.37 g K per bucket, respectively. Handweeding was conducted before sowing to control weeds.

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Pesticides (imidacloprid) and fungicides (tebuconazole)were sprayed to control pests and diseases as needed.

Experimental design and warming treatmentFollowing the FATI apparatus design developed by Nijset al. (1996), Kimball (2005) and Dong et al. (2011), wedesigned an experimental warming apparatus with two1-kW far-infrared heating tubes (1.5 m long, 60 cm apart)made by Shanghai Halo Infrared Technology Co. Ltd.,China. They were placed 0.5 m (transplanting stage) to1.7 m (flowering stage) apart on steel column pipe sup-ports and surrounded by a resin film that allowed for 98%light transmittance and was open on the top. The experi-ment involved four treatments (all-day warming, AW;daytime warming from 07:00 to 19:00, DW; nighttimewarming from 19:00 to 07:00, NW, and a control, CK)and covered the time from transplanting to maturation.Each treatment included three replicate plots, which wereplaced in a randomized block design. Twenty-four buck-ets of rice (four buckets of rice were placed in width, sixbuckets of rice were placed in length) were grown in oneplot (1.2 m width × 2.0 m length). Also, all buckets’

positions were not changed during the growth period.The apparatus had a 4-m2 heating area and was able toinduce remarkable increases in temperature (Dong et al.2011). The daily mean temperatures of the crop canopy inthe AW, DW and NW plots were 2.0, 1.1 and 1.3°Chigher than those in the CK plots (Experiment 1), respec-tively, and 2.0, 0.9 and 1.2°C higher than those in the CKplots (Experiment 2), respectively. The canopy tempera-ture data were obtained using a temperature recorderinstrument (Hangzhou Zeda Instrument Co. Ltd.,China), which could automatically record the instanta-neous value every 30 min.Taking Experiment 2 as an example, Fig. 1a displays

the trends of canopy temperature variation during theflowering stage. It was observed that the changes in thecanopy temperature under the three warming treatmentswere similar to those in the CK plots, which showed thatthe warming systems did not change the diurnal varia-tion of the field temperature. The relative canopy tem-peratures under various scenarios were AW > NW > DW> CK, and the temperature variation trends for theremaining development stages were similar to those forthe flowering stage. The daily mean temperatures of the

Figure 1 Trends of diurnal mean temperature variation during (a) the flowering stage and (b) all growing stages of the rice (Oryzasativa L.) canopy under different warming treatments in 2012.

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crop canopy throughout the entire growth stage in theAW, DW and NW plots were 2.0, 1.0 and 1.3°C higherthan those in the CK plots, respectively (Fig. 1b).

Sampling and analytical proceduresSampling and measurements were performed at the joint-ing, anthesis and maturation stages. Three buckets ofrice for each treatment (one bucket of rice was selectedfrom one plot) were cut at ground level and separatedinto leaves and stems at jointing, leaves, stems and spikeat anthesis, and leaves, stems, chaff and grain at matur-ity. All plant parts were oven-dried at 80°C to constantweight for dry weight determination. The plant sampleswere analyzed for N (micro-Kjeldahl) concentration, andN accumulation was calculated by multiplying the Nconcentration by the dry weight. The yield and yieldcomponents in each plot were determined by harvesting16 buckets of rice after maturity. These plants werefurther air-dried for 3 weeks to a constant weight, afterwhich the number of panicles was counted and theplants were carefully threshed. The 1000-grain weightwas determined by randomly weighing 1000 grains. Theactual yield was determined by weighing all grain forthree replications. Afterwards, the grain was soaked intap water, and the numbers of sunken and floating grainswere counted to determine the grain-filling rate.The following parameters related to N accumulation

and remobilization within the rice plants during grainfilling were calculated (Zhang et al. 2013):

(1) Post-anthesis N accumulation = N content of theaboveground biomass at harvest- N content of theaboveground biomass at anthesis.

(2) N translocation (NT) = N content of the above-ground biomass anthesis – N content of the leaves,stems and chaff at maturity.

(3) N translocation efficiency (NTE) (%) = (N translo-cation amount/N content of the abovegroundbiomass at anthesis) × 100%.

(4) Contribution of translocated N to grain (CTN) (%) =(N translocation amount/N content of grains atmaturity) × 100.

(5) N harvest index = (N content of grain/N content ofaerial plant part)

(6) N utilization efficiency based on grain yield = grainyield/N content of aerial plant part

(7) N utilization efficiency based on biomass = above-ground biomass/N content of aerial plant part

Data analysisStatistical analyses were performed using SPSS 12.0(SPSS Inc., Chicago, IL, USA). Statistically significantdifferences were identified via least significant difference

(LSD) calculations at p = 0.05. The standard errors ofthe means were also calculated and are presented in thegraphs as error bars.

RESULTS

N accumulation and translocationThe total N accumulation in the three growth stages ispresented in Fig. 2. In both growing seasons, the threewarming treatments significantly increased the total Naccumulation during the jointing, anthesis and maturitystages (p < 0.05), resulting in the following order of totalN accumulation: DW > NW > AW > CK. In the AW, NWand DW treatments, the total N accumulation in the joint-ing stage increased by 20.56, 23.33 and 26.41% in 2011and by 33.71, 35.80 and 40.53% in 2012, respectively. Inthe maturity stage, the warming treatment significantlyincreased the N concentration and accumulation in stems

Figure 2 Effect of asymmetric warming on the total nitrogen(N) accumulation of rice (Oryza sativa L.) in three growingstages. The vertical bars indicate the standard error (n = 3).Different lowercase letters between the treatments in eachgrowth stage indicate significant differences at p < 0.05.

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in both years (p < 0.05) but had no significant effect on theother biomass fractions (Fig. 3 and 4).In both growing seasons, the warming treatment

increased the amount of N translocation and significantlyenhanced the contribution of translocated N to grain N.However, the N translocation efficiencies were lower inthe warming plots than those in the CK plots. For exam-ple, in the AW, NW and DW treatments, the NTE

decreased by 10.12, 10.72 and 15.35% in 2011 and by14.87, 10.65 and 19.92% in 2012, respectively (Table 1).

Biomass, grain yield and yield componentsThe total aboveground biomass in the jointingstage varied between 27.79 and 30.11 g per bucketin the CK plots and between 31.06 and 34.98 g per

Figure 4 Effects of asymmetric warming on the nitrogen (N)accumulations in different plant organs at maturity. The verti-cal bars indicate the standard error (n = 3). Different lowercaseletters between the treatments in each growth stage indicatesignificant differences at p < 0.05.

Figure 3 Effect of asymmetric warming on the nitrogen (N)concentrations in different plant organs at maturity. The verti-cal bars indicate the standard error (n = 3). Different lowercaseletters treatments in each growth stage indicate significantdifferences at p < 0.05.

Table 1 Effects of asymmetric warming on nitrogen (N) translocation from vegetative organs to grain after anthesis under a free airtemperature increase (FATI) facility

Year TreatmentN translocation(g per bucket)

N translocationefficiency (%)

Contribution of translocated N tograin (%)

2011 CK-Control 0.33b 47.81a 63.73bAW-All-day warming 0.39a 42.68b 78.84aDW-Daytime warming 0.39a 40.47b 78.81aNW-Nighttime warming 0.39a 42.97b 76.96a

2012 CK-Control 0.28b 42.43a 69.28AW-All-day warming 0.35a 37.91b 72.57DW-Daytime warming 0.33a 33.98b 71.68NW-Nighttime warming 0.34a 36.12b 72.32

*Different lowercase letters within a row indicate significant differences between growing seasons at the 5% level.

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bucket in the warming plots (Table 2). Significanteffects of the warming treatment were observed onthe aboveground biomass in the jointing and maturitystage in both growing seasons but not in theanthesis stage in 2012. In the AW, DW and NWtreatments, the warming decreased aboveground bio-mass in the maturity stage by 9.63, 4.86 and 2.75% in2011 and by 9.40, 8.58 and 4.31% in 2012,respectively.In the AW, DW and NW treatments, the grain yield of

the Huaidao5 cultivar declined by 9.58, 5.23 and 7.81% in2011 and by 10.55, 4.88 and 7.97% in 2012, respectively(Table 3). Furthermore, the panicle number, grain numberper panicle and grain filling rate decreased in the warmedplots, whereas the 1000-grain weight did not exhibit con-sistent changes. Compared with the CK treatment, theactual yield, panicle number and grain filling rate wereonly significantly different in the AW treatment in bothyears, whereas other yield components exhibited no sig-nificant differences among the four treatments (p < 0.05).

N utilization efficiencyThe warming treatment significantly decreased the Nharvest index and N utilization efficiency based ongrain yield in both growing seasons (p < 0.05) and theN utilization efficiencies based on biomass in 2012

(Table 4). For example, in the AW, DW and NWtreatments, warming decreased N utilization efficiencybased on grain yield by 13.30, 16.07 and 9.32% in2011 and 16.39, 19.44 and 12.37% in 2012,respectively.

DISCUSSION

Effects of asymmetric warming on grain yieldand aboveground biomassThe results of the present study show that the warmingtreatments decreased the actual rice yield from 4.88 to13.05%. Similarly, a previous study demonstrated that ahigh temperature of 36°C significantly decreased ricegrain yield at the heading stage (Zheng 2003).Furthermore, Mohammed and Tarpley (2011) observedthat increasing the nighttime temperature by 5°Cdecreased rice grain yield by 90.00%. However, theelevated carbon dioxide (CO2) associated with climatechange increased rice photosynthetic rate, biomass andgrain yield (Yang et al. 2010). To accurately assess theresponse of rice growth and yield to potential climatechange, a complex impact study on rice growth and yieldfor both elevated CO2 and air temperature is beingconducted.

Table 2 Effects of asymmetric warming on the aboveground biomass of rice (Oryza sativa L.) in three growing stages under a freeair temperature increase (FATI) facility

Aboveground biomass (g per bucket)

Year TreatmentJointingstage

Anthesisstage

Maturitystage

2011 CK-Control 30.11b 59.93b 93.25aAW-All-day warming 34.33a 69.18a 84.27bDW-Daytime warming 34.98a 66.53a 90.69bNW-Nighttime warming 33.56a 68.53a 88.72b

2012 CK-Control 27.79b 64.64 93.20aAW-All-day warming 31.69a 66.50 84.44bDW-Daytime warming 31.06a 66.49 89.18bNW-Nighttime warming 30.37a 65.93 85.20b

*Different lowercase letters within a row indicate significant differences between growing seasons at the 5% level.

Table 3 Effects of asymmetric warming on rice (Oryza sativa L.) grain yield and components at maturity in both years

Year TreatmentPanicle number

(number per bucket)Grain number perpanicle (number)

Grain fillingrate (%)

1000-grainweight (g)

Actual yield(g per bucket)

2011 CK-Control 15.45a 176.00 98.00a 26.67 56.59aAW-All-day warming 13.69b 163.00 87.67b 22.38 51.17bDW-Daytime warming 14.57a 166.00 95.00ab 25.85 52.17aNW-Nighttime warming 14.92a 171.00 97.00ab 23.38 53.63a

2012 CK-Control 15.36a 153.00 97.67a 25.85 50.63aAW-All-day warming 13.20b 141.00 91.00b 23.48 45.42bDW-Daytime warming 14.13a 145.00 93.67ab 24.80 46.73aNW-Nighttime warming 14.38a 149.00 94.67ab 24.03 48.30a

*Different lowercase letters within a row indicate significant differences between growing seasons at the 5% level.

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Grain yield is determined by the panicle number, grainnumber per panicle and 1000-grain weight. In the pre-sent study, the warming treatments decreased the paniclenumber, grain number per panicle and 1000-grainweight as well as the grain-filling rate. The results forthe two study years were similar, and the relative reduc-tions followed the order CK > DW > NW > AW.However, the actual yield, panicle number and grainfilling rate were only significantly different for AW andCK in both years (p < 0.05). The grain number perpanicle and 1000-grain weight were not significantlydifferent among the four treatments. Nighttime warmingnot only shortened the growth stage but also increasedrespiration consumption (Fang et al. 2012). The adverseimpacts of nighttime warming were greater than those ofdaytime warming (Peng et al. 2004) but less than thoseof all-day warming. Zhang et al. (2005) observed thatearly- and late-season rice yields would be reduced by3.60 and 2.80%, respectively, in 2100 using a cropmodel. Although the yield reduction trends determinedby analyzing the abovementioned models were similar tothe trend observed in the present study, the extent of thereductions was associated with the significant tempera-ture differences between daytime and nighttime. It wasalso shown that environmental temperature differences,especially daytime and nighttime differences, should beconsidered when applying crop models to reduce theuncertainty in the model predictions.The warming treatment significantly increased the

aboveground biomass by 9.26–16.18% at the jointingstage but decreased it by 2.75–9.63% at the maturitystage in both growing seasons. Similarly, previous stu-dies reported that a night-warming treatment caused an18.00% increase in daily net C accumulation despitestrongly increasing the nighttime plant leaf C releasevia respiration (Wan et al. 2009). This result could beexplained by the stimulatory effects of the warmingtreatment on the photosynthetic capacity of plant leavesduring the vegetative growth stage. The sink-source

hypothesis of plant photosynthesis indicates that warm-ing treatment would stimulate plant photosynthesisthrough an increased drawdown of leaf carbohydrates,resulting in a much greater compensatory enhancementof the photosynthesis rate in subsequent days (Prietoet al. 2009). Another possible reason for this stimulatingeffect is the low temperatures in the jointing stage, whichmay have been below the threshold of the negative tem-perature effect. In both growing seasons, the above-ground biomass at maturity was lower in the warmingplots than in the CK plots, mainly due to a strongreduction in productive spikes. In both growing seasons,higher pre-anthesis dry matter accumulation in thewarming treatment did not translate to higher grainyields compared with the control. Lower grain yields inthe warming treatment may have been associated withlower dry matter accumulation in the period from post-anthesis to maturity. These results are consistent withthose of previous studies regarding rice plants, whichindicated that warming treatments significantlydecreased the percentage of new C assimilated duringthe reproductive stage in the ears but increased it in thestems (Cheng et al. 2010). The decrease in the harvestindex resulted from the high C allocation to the vegeta-tive organs under the high-warming treatment and maypotentially threaten future rice production.

Effects of warming treatment on N accumulationand translocationThis study revealed a clear pattern in which warmingtreatment generally enhanced the N concentrations of ricestems at maturity relative to the CK plots. However, long-term warming experiments, which have mostly been con-ducted in natural ecosystems without N fertilization, haveshown that high nighttime temperatures decrease the Nconcentrations of grass in prairies as a result of the dilutioneffect caused by increased dry matter accumulation.Recently, Cheng et al. (2010) observed that the whole-

Table 4 Effects of asymmetric warming on nitrogen (N) harvest indexes and N utilization efficiencies under a free air temperatureincrease (FATI) facility

Year TreatmentN harvestindex (%)

N utilization efficiency basedon grain yield (g DW g−1 N)

N utilization efficiency based onbiomass (g DW g−1 N)

2011 CK-Control 0.53a 58.35a 86.96AW-All-day warming 0.49b 50.59b 83.33DW-Daytime warming 0.46b 48.97b 82.06NW-Nighttime warming 0.49b 52.91b 83.15

2012 CK-Control 0.48 51.75a 84.56aAW-All-day warming 0.46 43.27b 75.76cDW-Daytime warming 0.42 41.69b 80.00bNW-Nighttime warming 0.44 45.35b 80.00b

*Different lowercase letters within a row indicate significant differences between growing seasons at the 5% level.

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plant N concentrations of rice plants were unaffected bynighttime warming treatment, whereas the living leaf Nconcentration increased significantly. The N concentrationin plant leaves is generally closely associated with photo-synthetic capacity. In our study, increased N concentrationin living leaves under the warming treatment may haveenhanced the net photosynthetic rate, thereby promotingthe accumulation of carbohydrates, as supported by the9.26–16.18% higher dry matter accumulation in the joint-ing period under the warming treatment compared withthe CK plots.We observed a significant increase in the total N accu-

mulations in the whole plant under the warming treat-ment compared with that under the CK treatment ateach growing stage. The results are consistent with pre-vious studies conducted with rice crops and prairie grass(An et al. 2005; Cheng et al. 2010). The warming treat-ment increases plant N accumulation, likely due to ele-vated soil N mineralization in the warming plots and/orthe increased N uptake ability of plant roots (Tingeyet al. 2003). Although DW increased the C gain byphotosynthesis and NW increased the C loss by nightrespiration, the higher-temperature treatment decreasedthe chlorophyll content of the rice, inhibited its photo-synthesis and reduced its photosynthetic rate and photo-synthetic product (Li 2003; Kanno et al. 2009; Kannoand Makino 2010). The continuous daytime averagetemperature during 3 d, which was over 32°C/5 h,would affect the growth and development of conven-tional rice varieties, and Fig. 1b shows that an averagetemperature above 32°C was commonly observed fromthe middle of July to the end of July in this study. Thiseffect may be a primary cause of the insignificantdifference in above-ground biomass between the DWtreatment and NW treatment. Plant N concentration ismainly affected by the plant’s natural features (such asphysiological characteristics or gene) and environmentalfactors (e.g. temperature), but the former factor isstronger than the latter (Mae 2011). In addition, thetotal N content of the soil used in this experiment was1.06 g kg−1 (corresponding to very poor soil), and theamount of N fertilizer used in our experiment was13.80 g m−2 (relatively low N fertilizer application; theamount of N fertilizer in the Yangtze River Basin wasover 30.00 g m−2, Wang et al. 2003), and the N con-centration of the rice plants was almost the same underthe warming treatment due to the lower soil N content.The plant N accumulation was mainly affected by the Nconcentration and aboveground biomass. However, theimpact of aboveground biomass was higher than that ofN concentration (Zhang et al. 2013). The N accumula-tion of the rice plants did not differ significantly amongthe three warming treatments due to the insignificantdifference in above-ground biomass.

The warming treatment exerted a profound effect onthe seasonal patterns of N uptake processes, with warm-ing increasing pre-anthesis N accumulation by 33.42–49.86% in both growing seasons but decreasing post-anthesis N accumulation by 10.88–26.55%. Generally, ahigher pre-anthesis N accumulation is favorable forobtaining high grain yields because grain N mainly ori-ginates from the remobilization of N stored temporarilyin vegetative plant parts (Masoni et al. 2007; Dordas2009). However, in the present study, the warming treat-ment significantly decreased N translocation efficiencydespite substantially increasing the absolute transloca-tion efficiency. Thus, more N was retained in the vege-tative parts during grain filling, which has also beenreported in rice plants (Cheng et al. 2010). On theother hand, previous studies have shown that post-anthesis N uptake that goes directly to the grain is sig-nificantly correlated with grain yield for both low- andhigh-N conditions (Cox et al. 1985). In our study,reduced post-anthesis N uptake may have contributedto the decrease in grain yield under the warming treat-ment. Therefore, decreased N translocation efficiencytogether with reduced post-anthesis N uptake led to thereduction in the internal N utilization efficiency.

CONCLUSIONS

Warming treatments decreased the rice grain yield andyield components. The results for the two study yearswere similar, the measured properties, except for the1000-grain weight, ranking as follows: CK > DW > NW> AW. The actual yield and effective panicles were onlysignificantly different between the AW and CK plots inboth years, whereas other yield components exhibited nosignificant differences among the four treatments. At thejointing, anthesis and maturity stages, the total N accumu-lation in the whole plant was 8.27to 40.53% higher in thewarming treatment than in the CK plots. The warmingtreatment substantially increased pre-anthesis N accumula-tion and reduced post-anthesis N uptake.

ACKNOWLEDGMENTS

The authors acknowledge experimental help providedby Siqi Qiu, Lu Liu and Chenyu Xie. This study wassupported by the Natural Science Foundation ofChina (Nos. 41205087, 41103039 and 41001190),the University Students Innovation Training Project inJiangsu Province (No. 201310300064Y), the NaturalScience Project of the University in Jiangsu Province(No. 12KJB170009) and the National SpecialResearch Fund for the Non-profit Sector (No.GYHY201206020). We also acknowledge the

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funding support provided by the Priority AcademicDevelopment Program for Jiangsu Higher EducationInstitutions (PAPD) and Jiangsu GovernmentScholarship for Overseas Studies.

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