Effect of experimental warming on nitrogen uptake by winter wheat under conventional tillage versus no-till systems

Soil & Tillage Research 180 (2018) 116–125

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Effect of experimental warming on nitrogen uptake by winter wheat under conventional tillage versus no-till systems ⁎

Ruixing Houa,b, Xingliang Xua, , Zhu Ouyanga,b,

T

⁎

a

Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China b Yucheng Comprehensive Experiment Station, China Academy of Science, Beijing 100101, China

A R T I C LE I N FO

A B S T R A C T

Keywords: Global warming Inorganic nitrogen Nitrogen uptake pattern Organic nitrogen Winter wheat

Despite the perceived importance of nitrogen (N) to growth and production of wheat, few studies have attempted to examine the effect of warming on wheat N uptake or its preference for NO3−-N vs. NH4+-N, especially under different tillage systems. In the North China Plain, an experimental warming (2 °C increase in soil during the jointing stage) study was conducted using in situ 15N labeling under till and no-till systems. We aimed to investigate the uptake of NO3−-N, NH4+-N, and glycine-N by winter wheat. Warming strongly enhanced wheat biomass (14.7% and 13.2% for till and no-till, respectively) and N content in biomass (11.1 and 7.4 g N m−2 for till and no-till, respectively). Total N uptake rates increased by 47% and 40% under till and no-till treatments, respectively. Warming changed the uptake pattern for the three N forms by significantly increasing the contributions of NO3–N by 16% and glycine-derived N by 5%, while decreasing the contribution of NH4+-N by 20% under the two tillage systems, on average. Collectively, high soil temperatures accelerated N uptake in winter wheat and improved the preferential contribution of NO3−-N and glycine-N due to the increase in soil glycine and NO3− content. Our findings suggest that enhanced N uptake improved growth of wheat and could reduce N losses through increased uptake of NO3− under till and no-till systems in the North China Plain under the warmer conditions that are likely in future.

1. Introduction The challenge to agro-ecosystems in future is two-fold. Securing sufficient food for the world’s estimated 9 billion humans by 2050 requires doubling global agriculture productivity (Foresight, 2011). In addition, global warming, which is projected to increase the global temperature by 3.7 °C by the end of the 21st century (IPCC, 2013), will affect crop growth and yields in varied ways. As the efficiency of nutrient uptake by crops is one of the most important determinants of crop biomass and yield, improving nutrient acquisition and thus crop productivity under climate change conditions can help address the challenge (Garnett et al., 2009; Kraiser et al., 2011; Rimski-Korsakov et al., 2012). As the main limiting nutrient to crop growth and yield, nitrogen (N) uptake by crops is determined by the N availability in the soil, which is strongly affected by tillage practices (Thomsen and Sørensen, 2006). Tilling significantly affects the soil N cycle, N uptake by crops, and microbial activities, which results in different responses of crop yield and soil properties to experimental warming (Hou et al., 2014; Ruisi et al., 2016; Zuber and Villamil, 2016). As a “win-win” measure,

the no-tillage (no-till) agricultural system, which has rapidly spread worldwide during the last two decades, enhances agricultural sustainability concomitant with mitigating global warming (Johan et al., 2004; Powlson et al., 2016). Numerous studies show that the two dominant tillage systems cause differences in soil N availability (Ruisi et al., 2016). Elucidating the relationship between increased temperature and N uptake by crops growing under different tillage systems will improve our understanding of the effect of climate change on agriculture. Wheat growth and yield are very sensitive to temperature (Chowdhury and Wardlaw, 1978; Darwinkel, 1978; Sofield et al., 1977). Previous studies have shown that a higher temperature notably decreases both vegetative growth duration and grain-filling duration (Batts et al., 1997; Porter and Gawith, 1999) and decreases grain weight while decreasing the number of kernel per ear (Sofield et al., 1977; Thorne and Wood, 1987). Studies have reported mixed results regarding the effects of temperature on yield; some have reported declining yield (Lobell et al., 2011; Wheeler et al., 1996), while others have noted increased or unchanged yield (Hatfield et al., 2011). It remains unclear how warming affects plant N uptake in croplands.

⁎ Corresponding authors at: Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China. E-mail addresses: [email protected] (X. Xu), [email protected] (Z. Ouyang).

https://doi.org/10.1016/j.still.2018.03.006 Received 26 June 2017; Received in revised form 28 February 2018; Accepted 4 March 2018 0167-1987/ © 2018 Elsevier B.V. All rights reserved.

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temperature of 13.1 °C and mean precipitation of 561 mm during the past 32 years (from 1985–2016). Approximately 70% of the annual precipitation occurs between June and September. The soil is classified as Calcaric Fluvisol according to the World References Base for soil resources (WRB, 2014). Soil surface texture is silty loam (sand, 12%; silt, 66%; clay, 22%) and uniform in our experimental area, with a pH of 7.1. Winter wheat (Triticum aestivum L.) and summer maize (Zea mays L.) were double cropped according to a common practice in the NCP. For tillage treatment, standing crop stubble of each treatment was cut to approximately 10 cm and all other residues were removed after the harvest of the maize crop. A rotary tiller was used with a tillage depth of about 10–15 cm, which fully incorporated standing stubble into the soil before winter wheat planting. For the no-till treatment, maize residues were chopped into pieces (about 5 cm length) by hand and retained on the soil surface. The residue mass retained for no-till was about 10 Mg ha−1 yr−1 with 4 Mg ha−1 yr−1 of wheat and 6 Mg ha−1 yr−1 of maize. According to the experiential application rate of fertilization in the study region (Ju et al., 2007; Zhen et al., 2006; Zheng et al., 2017), the total N application rate for no-till and till treatments was 285 kg N ha−1 yr−1 for wheat. The base fertilizer, along with phosphorus (P) and potassium (K), was applied as a compound inorganic chemical fertilizer containing N (as urea), P (as P2O5), and K (as K2O) at a ratio of 12:19:13 and with application rates of 116 kg ha−1 of N, 178 kg ha−1 of P, and 122 kg ha−1 of K as the base fertilizer for the crop in both tillage systems each year. Considering residue N (50 kg ha−1 of N), the inorganic N input was 66 kg ha−1 of N for no-till. For topdressed N, during the re-greening stage, the remaining 169 kg ha−1 yr−1 of N was applied as urea for both till and no-till systems. The base fertilizer application of all treatments was the same as for topdressing: October 6 and March 3. There was a one-time irrigation on April 1, 2014, and the amount of irrigation was about 30 mm. All other management procedures were identical for the two systems with spraying of herbicide (2,4-D butylate) and insecticide (40% dimethoate) in May.

Warming often results in a decline of plant N use efficiency (NUE), because higher temperatures increase plant-microbial competition for N and lead to more N becoming immobilized in microorganisms (Kuzyakov and Xu, 2013; Rütting et al., 2010). This in turn leads to a reduction of N utilization by crops and depresses yields (Rathke et al., 2006). Higher temperatures can also increase the risk of N losses by increasing N2O efflux (Kallio et al., 1997; Rankinen et al., 2013) and decreasing NUE and crop biomass (Cai et al., 2016; Liu et al., 2013). In contrast, numerous studies have demonstrated that warming may accelerate N delivery to the root surface by improving transpiration in well-irrigated croplands (Pregitzer and King, 2005). Further, warming may enhance N uptake by plants by increasing the availability of soil N (Bai et al., 2013; Rustad et al., 2001). Numerous studies have suggested that higher temperature increases crop biomass and yield. (Hou et al., 2012b; Tian et al., 2012). Warming could thus improve crop N uptake by increasing N mineralization (Rustad et al., 2001). Because of the variable influence of warming on plant N uptake, crops may show different preferences for different N forms under warming conditions. Inorganic forms of N (NO3−-N and NH4+-N) have long been recognized as the dominant forms of N available to plants, especially in croplands (Chapman et al., 2012; Wang et al., 2015). Higher temperatures can significantly change the availability of these forms of N in the soil by increasing nitrification and by drying the soil (Bai et al., 2013; Carrillo et al., 2012). As a result, crops may need to alter their intake of the two dominant N forms during growth. Several studies have shown that crops are able to uptake organic N in the form of amino acids in cropland (Ge et al., 2009; Reeve et al., 2009; Xu et al., 2008). The availability of soil organic N may increase with more intensive soil organic matter (SOM) decomposition (Carrillo et al., 2012; Rustad et al., 2001) in croplands. As a result, the contribution of organic N to crop N uptake could be increased under warming. A better understanding of the effects of warming on the three forms of N is important to estimate the growth and yield of winter wheat under increased temperatures. Long-term no-till agriculture is known to change the properties and biological functions of soil and therefore affects soil carbon (C) and N cycling, especially in the upper layer of the soil (Bayer et al., 2015; Gregorich et al., 2006). Between no-till and till systems, N mineralization from the soil and plant residues and the status of mineral N are affected by soil temperature and water changes (Sainju et al., 2009, 2012) via changing microbial activity (Bremer and Kessel, 1992). Our previous study showed that warming-induced changes to soil temperature or water content fluctuate less under no-till than under conventional tilling (Hou et al., 2014). In addition, an increase in the extracellular enzyme activities and their sensitivity has been reported with increased temperature in no-till systems alone (Hou et al., 2016). This effect may threaten N uptake by roots by increasing competition for N (Kuzyakov and Xu, 2013). To clarify how warming affects N uptake by winter wheat under the two types of tillage systems, the uptake of three forms of N (NH4+, NO3−, and glycine-N) was examined using in situ 15N labeling under warm conditions in fields that have followed till and no-till systems since 2003 in the North China Plain. We aimed to test two hypotheses: 1) warming could increase N uptake by wheat, especially for organic N, and 2) under warm conditions, no-till, in contrast to till, could decrease the total N uptake by wheat due to stronger microbial competition.

2.2. Experimental design Experiments were based on four treatments: Till with, and without warming (TW and TN, respectively), and no-till with, and without warming (NW and NN, respectively). We used split-plot design with tillage system (no-till or till) in the main plots and warming (with or without warming treatment) in subplot. Eight randomly ranged plots were chosen, comprising 4 till treatments and 4 no-till treatments. Each plot is 7.5 m × 40 m (300 m−2). Four subplots were chosen in each plot and each subplot size is only 2 m × 2 m (4 m−2) (Fig. 1). Each treatment was replicated four times. There was a 5 m border between adjacent plots and at least 10 m between treatments. The warmed soil was continuously heated (since February 4, 2010) using an MSR-2420 infrared heater (Kalglo Electronics, Inc., Bethlehem, PA, USA) placed 3 m above ground. The control (without warming) plots were the same shape and size as the warmed ones and included a "dummy" infrared heater suspended 3 m above ground to simulate shading effects of the infrared heater. The heater increased the soil temperature by 2 °C relative to the control treatment. Temperature of the canopy was measured by a thermal imager (Model SC2000 ThermaCAM; Flir Systems, Danderyd, Sweden) at 09:00, 15:00, and 21:00 each day from April 22 to 28, 2014. The wave band of the thermal imager was 8–14 l m. According to the thermal radiation balance equation, the measured radiance includes a reflection term from the environment. Thus, to correct for heater radiation and sky radiation reflected off the crop canopy, we used the methods described specifically in our previous study (Hou et al., 2012b).

2. Materials and methods 2.1. Study site This study was conducted in a long-term (since 2003) conservation tillage experiment located in the North China Plain (NCP, 36°50′N, 116°34′E, elevation: 20 m a.s.l.). The set-up of the field experiment is described in detail in a previous study (Hou et al., 2012a). Briefly, the site is located in a temperate semi-arid climate, with mean annual

2.3.

15

N injection and biomass measurements

To determine uptake of different N forms (NO3−, NH4+ and 117

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Fig. 1. Layout of experimental design, which includes non-warmed and warmed (red) plots. 15N was injected as three forms of N in the subplots. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

nutrient analysis.

glycine) by winter wheat, four 10 × 20 cm subplots were randomly set up in each plot to represent the four 15N labeling treatments (15NO3−, 15 NH4+, glycine-15N and the control without 15N). There was at least 1 m between two subplots. Totally, there were 64 subplots. The 15N tracers were used for 15NH4+ as 15NH4NO3 (98.4 atom% 15N), for 15 NO3− as NH415NO3 (98.2 atom% 15N), or for 15N-glycine as C2H515NO2 (98.0 atom% 15N). To ensure 15N uniform distribution in each subplot, each 10 × 20 cm subplot was divided into eight 5 × 5 cm quadrats. An amount of 2.5 ml 15N tracer solution was injected into the soil at a depth of 7 cm at the center of each quadrat, corresponding to 10 μg 15N per gram of dry weight of soil. The untreated subplots in each replication that were not injected with 15N tracer were supplied with equivalent amounts of water and were taken as control (Fig. 1). To avoid diffusion of 15N-labeled solution, each plot was isolated by steel plates up to 15 cm depth because most of roots were concentrated in this depth (unpublished data). To reduce the effects of warming-induced advancing of phenology on the biomass and N uptake, 15N was injected depending on the phenology of each treatment. In warmed plots, the jointing stage (more than 50% wheat in the plots were in the jointing stage) was observed 9 days earlier than that in non-warmed plots; hence, 15N injection, and shoot, root, and soil collection were performed 9 days earlier in warmed plots. Thus, 15N was injected on April 15, 2014 in the warmed plots and on April 24, 2014 in the non-warmed plots. Before 15N injection, we removed the residue on the soil surface for no-till to minimize an influence on the application of labeled N into the soil profile. The two sampling days have similar PAR (Photosynthetically Active Radiation) values, which were 39.66 and 38.79 for April 15 and April 24, respectively. The PAR values were measured by a nearby weather station that is about 100 m from our study field. All plants in each subplot were harvested 3 h after the tracer was injected considering fast turnover of free amino acids in soils (Jones and Murphy, 2007). The four replicate subplots received each of the three 15 N form. Wheat was harvested and separated as roots and shoots. The roots were placed in 0.5 M CaCl2 solution for 30 min and then rinsed with distilled water. After then, roots and shoots were oven-dried at 105 °C for 30 min and then dried at 80 °C for 48 h to estimate biomass. Dried roots and shoots were ground to a fine powder using a ball mill (MM200, Retsch, Germany) for the measurements of N content and 15 N/14N ratios. Fresh soil in the top 15 cm depth was collected for

2.4. Measurements Soil NH4+ and NO3− were determined by extraction with 2 mol L−1 KCl. Ten gram of fresh soils (< 24 h after sampling) were added with 100 ml mol L−1 KCl (10:1), shaken for 1 h, and filtered with Whatman No. 42 Paper. Following filtration, all KCl extracts were immediately acidified with several drops of 6 mol L−1 HCl to prevent microbial growth and refrigerated at 4 °C until analysis. Soil NH4+ and NO3− were determined in the KCl extracts using a flow-injected auto-analyser. Soil glycine concentrations were measured by high performance liquid chromatography (Waters 515, Waters Inc., USA) in the same extracts (Näsholm et al. 1987). Aliquots of ground plant materials (2 mg) were weighted into tin capsules for analyzing total N, C and 15N/14N ratios using isotope ratio mass spectrometry (IRMS, MAT 253, Finnigan MAT, Germany), with a Flash EA1112 interfaced by ConFlo III to the IRMS. Soil temperature (T) at 5 cm depth and volumetric soil moisture (θ) at 0–10 cm depth were monitored by PT100 thermocouples and FDS100 soil moisture sensors (Unism Technologies Incorporated, Beijing), respectively. Soil temperature and water content data from January 1 to June 15, 2014 are shown (Table 1 and Fig. 2). Canopy temperature was measured at the end of April 2014 for the two tillage systems. 2.5. Nitrogen uptake calculation Atom% excess for 15N (APE) was calculated as the difference between the atom% for 15N in plants that were treated with 15N and those from the control. 15N uptake by plants was estimated by calculating APE of shoots and roots, separately, using the formula, (biomass × N %/100) × (APE/100). The values for shoots and roots were then summed, and divided by the root biomass and time, expressed as μg g−1 h−1. Uptake of the available forms of N corresponding to the 15N treatment was calculated (Xu et al., 2011) as follows: APE(%) = At%labeled − At%control 15

Nuptake = total biomass × Ncontent × APE

(1) (2) −2

where, total biomass is the sum of root and shoot biomass (g m ), Ncontent is the N content in wheat (%), At%labeled refers to the atomic 118

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Table 1 Average soil temperature (Tavg), water content (θavg) during growing season and sampling time (Ts and θs) under four treatments. The warming treatment resulted in an increase of mean daytime (TCDI) and nighttime canopy temperature (TCNI). Index

TN

Tavg (°C) θavg (V/V) Ts (°C) θs (V/V) TCDI (°C) TCNI(°C)

10.32 16.52 17.38 17.02 1.01 (0.15) 1.70 (0.13)

TW (0.26)c (0.87)a (0.44)b (1.27)a

NN

12.10 14.02 19.34 15.01

(0.43)a (0.98)b (0.54)a (1.58)a

9.84 17.74 16.64 17.88

NW (0.17)d (1.04)a (0.37)b (1.24)a

11.17 16.11 19.12 14.92

(0.27)b (0.88)a (0.46)a (1.88)a

Different letters indicate significant (p < 0.05) differences among same index. Values are means with the standard deviation in parentheses (n = 4); values within a row followed by different lowercase letters are significantly different (p < 0.05). TN, till with no warming; TW, till with warming; NN, no-till with no warming; NW, no-till with warming.

Where, MN is the amount of native NO3− or NH4+ in soil, and 15Nadded is the amount of added 15NO3− or 15NH4+ (McKane et al., 2002; Xu et al., 2011). 2.6. Statistical analysis The effects of warming and tillage on soil temperature, moisture, root, shoot, and total biomass, N content in root and shoot, three forms N content in soil, uptake rates of three forms of N, and total N were analyzed using split-plot ANOVA with a General Linear Model in SPSS, followed by post hoc comparisons using least significant different test. Tillage was considered as the main-plot factor and warming as the subplot factor. In other words, warming was nested into tillage treatment. Pearson linear correlations between the parameters were also performed with SPSS. All significant differences were considered at p < 0.05 level. All statistical analyses were conducted with SPSS software (SPSS for Windows, version 11.5, SPSS Inc., Champaign, IL). 3. Results 3.1. Effects of warming on soil temperature, moisture, and canopy temperature Warming significantly affected soil temperature and moisture (Fig. 2 and Table 1). Soil temperatures were increased from March to July by 1.8 and 1.4 °C for till and no-till, respectively. Warming decreased soil moisture by 2.5% and 1.6% (v/v) for till and no-till, respectively. It also affected soil temperature and moisture in similar ways (Table 1). Wheat canopy temperatures increased under warming by 1.01 and 1.7 °C during the daytime and nighttime, respectively (Table 1). Fig. 2. Soil moisture (above) and soil temperature (below) for the four treatments from January 2014 to June 2014. Red and blue arrows indicate the sampling time for warmed and non-warmed plots, respectively. TN, till with no warming; TW, till with warming; NN, no-till with no warming; NW, no-till with warming. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

3.2. Effects of warming and tillage on wheat shoot and root biomass Warming significantly increased total wheat biomass by 14.7% and 13.2% for till and no-till, respectively (Fig. 3). Shoot biomass increased with warming notably in both treatments, by 14.4% under tillage and 13.6% under no-till. Higher root biomass was observed in the warmed plots than in the non-warmed plots for both tillage systems (Fig. 3). Between the two tillage systems, there was little difference in biomass (of both shoots and roots), in the warmed and non-warmed plots. No interactive effect between warming and tillage on shoot biomass was found (p = 0.618, Table 2). A similar result was found for root biomass (p = 0.624, Table 2). By multiplying the biomass (including roots and shoots) and the N concentrations, it was observed that warming significantly increased the total N content by 11.1 and 7.4 g N m−2 for till and no-till, respectively (Fig. 3).

percent of 15N in the 15N-labeled wheat, At%control refers to the atomic percent of 15N in the wheat in the control. 15 N uptake rate by plants (15Nuptakerate, μg N g−1 root h−1) was calculated by dividing 15Nuptakeby root biomass (g m−2) and 15N labeling time (3 h in present study) (McKane et al., 2002; Xu et al., 2008) following the below equation: 15

Nuptake rate = 15Nuptake/(root biomass × time) −1

(3) −1

N uptake rate from soil by wheat (μg N g root h ) was calculated by multiplying the rate of uptake of 15N with the corresponding N pool (i.e., NO3− or NH4+) in the soil, and dividing by the total amount of 15 N added: N uptake rate =

15

15

Nuptake rate × MN/ Nadded

3.3. Effects of warming and tillage on plant N and on the available N in the soil

(4)

Warming significantly increased N concentration in the roots and 119

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uptake of the three forms of N by roots, the patterns of uptake of these N forms also changed dramatically. At 3 h after the tracer was injected, wheat root preferentially absorbed 15NO3−, the uptake of which increased from 55.7% to 71.2% under till, and from 57.0% to 72.2% under no-till treatments, under warming (Fig. 8). The contribution of 15 NH4+ to the total N uptake decreased from 41.0% to 21.5% under till and from 40.4% to 19.2% under no-till. The contribution of glycinederived N was also increased by warming from 3% to 8% under both tillage systems (Fig. 8). The total N uptake by roots was strongly affected by warming (p < 0.001, Table 2) under both tillage systems (Till: 40.0% h−1; No-till: 47.1% h−1, Fig. 9). At same time, the total N uptake was 12.8% higher under no-till than under till with no warming. 4. Discussion 4.1. Wheat biomass under warming Wheat biomass was increased significantly by warming (Fig. 3 and Table 1), consistent with our previous findings at the same site (Hou et al., 2012b). Generally, plants benefit from a relatively small increase in environmental temperature (Jaggard et al., 2010). A previous study reported that wheat biomass began to decrease when the environmental temperature exceeded 13.3 °C in a field warming experiment that utilized 12 planting dates over 2.5 years (Ottman et al., 2012). Similarly, warming induced a significant decline in aboveground biomass of wheat in the Tai Lake plain, where the yearly mean temperature is 15.6 °C (Cai et al., 2016). In the present study region, the yearly mean temperature was 13.1 °C, which is relatively low. In addition, warming improves soil N availability, which directly contributes to higher plant biomass production (Bai et al., 2013; Zhou et al., 2016). A recent metaanalysis found that net N mineralization and net nitrification are increased by 52.2% and 32.2% on average by experimental warming, which leads to more soil N availability and an increase in net primary production (Bai et al., 2013). Furthermore, warming is reported to highly increase photosynthesis by enhancing leaf respiration during the night (Ryan, 1991; Wan et al., 2009). Wan et al. (2009) found that nighttime warming leads to a 17.5% daily net C accumulation by stimulating carbohydrate depletion during the night and plant photosynthesis during the following day. A warming-induced decline in soil moisture adversely affects wheat biomass production. Liu et al. (2013) attributed the decrease in wheat biomass to a warming-induced decline in soil moisture by 5.9–9.1 vol%. In the present study, the soil moisture decline was only 1.3–1.8 vol% (Fig. 2 and Table 1) under routine irrigation, indicating that warminginduced soil drying may contribute a limited negative effect on wheat growth and biomass production.

Fig. 3. Root and shoot biomass under four treatments. TN, till with no warming; TW, till with warming; NN, no-till with no warming; NW, no-till with warming. Different lowercase letters indicate significant difference in shoot biomass or root biomass among four treatments (one-way ANOVA, p < 0.05). Different uppercase letters indicate significant difference in total biomass (including shoot and root biomass) among four treatments.

shoots in both till and no-till systems. In roots, the N concentration increased by 35.7% and 29.6% under till and no-till, respectively (Fig. 5), while in shoots, it increased by 27.3% and 11.5% under till and no-till, respectively (Fig. 5). The N concentration in shoots was twice that in the roots in all four treatments. There were strong interactive effects between warming and tillage on N concentration in both shoots and roots (p < 0.001, Table 2). Warming significantly increased the NO3− content in the soil by 15.4% under the no-till system, but increased the NO3− content under the till system by only 4.3%. Warming decreased the NH4+ content by 14.8% and 21.2% under the till and no-till systems, respectively (Fig. 6). Glycine-N significantly increase by approximately 2.5 times (p = 0.014, Table 2) under both tillage systems (Fig. 6). 3.4. Effects of warming and tillage on N uptake and the contribution of the three forms of N

4.2. Uptake of three forms of N in soil and their contribution to warming

The uptake of the three forms of N by roots was significantly affected by warming (Fig. 7). Warming significantly increased the uptake of NO3− by 87.4% and 74.8% for till and no-till systems, respectively. The uptake of glycine was also highly increased by 2.5 and 3.1 times under till and no-till systems, respectively. However, the uptake of NH4+ declined by 18.5% for till and 20.3% for no-till, respectively (Fig. 7). As a consequence of the notable effects of warming on the

The different forms of N present under till (all inorganic N from fertilizer) and no-till (part of the total N input was from corn residue as the base fertilizer, and the remaining N input was inorganic N from fertilizer) may result in different N uptake rates. We believe that differences due to the different forms of N applied were slight for two reasons. First, the proportion of residue-derived N was only 16% of the total input N. Second, residue-derived N and compound chemical

Table 2 Results of Split-Plot ANOVA on the effects of warming (W), tillage system (T), and their interactions on selected parameters.

W T W*T

Root Biomass

Shoot Biomass

Root N Conc.

Shoot N Conc.

Total Biomass

NO3−-N Cont.

NH4+-N Cont.

Glycine Cont.

NO3−-N Uptake

NH4+-N Uptake

Gly-derived N Uptake

Total N Uptake

Total N Content

0.430 0.130 0.624

< 0.001 0.010 0.618

< 0.001 < 0.001 < 0.001

< 0.001 0.080 < 0.001

< 0.001 < 0.001 0.496

0.001 0.780 0.060

0.052 0.268 0.421

0.014 0.065 0.735

< 0.001 0.008 0.777

0.004 0.781 0.296

< 0.001 0.016 0.025

< 0.001 0.101 0.576

< 0.001 < 0.001 0.007

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Fig. 4. Wheat total N content in root and shoot under four treatments. TN, till with no warming; TW, till with warming; NN, no-till with no warming; NW, no-till with warming. Different lowercase letters indicate significant difference in wheat total N content among four treatments (one-way ANOVA, p < 0.05).

Fig. 6. Concentrations of ammonium, nitrate, and glycine in soil under four treatments. TN, till with no warming; TW, till with warming; NN, no-till with no warming; NW, no-till with warming. Different lowercase letters indicate significant difference in soil N concentration among four treatments at the same soil layer (one-way ANOVA, p < 0.05).

fertilizer (24% of all N) were applied as base fertilizer on October 6, 2013, and the other 60% of total N was applied as urea topdressing on March 1, 2014. Meanwhile, our 15N injection and sampling were conducted at the middle and end of April. Thus, there was a long lag time between the two fertilizer applications and there was relatively more urea-N present than base fertilizer, which minimized the effects from the different forms of N in the present study. N concentrations in both roots and shoots in warmed plots were higher than those in non-warmed plots (Fig. 4). Thus, warming not only increased wheat biomass but also enhanced the N uptake. Likewise, Cai et al. (2016) found that in southern China, wheat plants showed a significantly greater N uptake, and they had higher biomass during early stages in warmed plots. As all N was taken up from the soil N pool, we aimed to elucidate the effects of warming on the uptake of available soil N. Compared with the significant increase in total N uptake rate, the change in the levels of the three forms of N in the soil as a response to higher temperature was inconsistent. Warmed soils had a slightly greater NO3−-N content than did non-warmed soils (Fig. 6), and there was a strong relationship between NO3−-N content and total biomass (r = 0.581), and between NO3–N and total N content (r = 0.697) (Table 3). These findings indicated that the NO3−-N content in the soil

Fig. 7. Uptake rates of ammonium, nitrate, and glycine under four treatments. TN, till with no warming; TW, till with warming; NN, no-till with no warming; NW, no-till with warming. Different lowercase letters indicate significant difference in N uptake among four treatments at the same soil layer (one-way ANOVA, p < 0.05).

N pool was increased by warming. A previous study also found that soil NO3− increased in semiarid grassland, leading to more NO3−-N absorption by the plants (Carrillo et al., 2012). Two mechanisms can explain this phenomenon. First, higher temperature facilitates faster conversion of NH4+ to NO3−, which increases soil NO3− concentration by enhancing nitrification (Malchair et al., 2010; Wang et al., 2015). The increased temperatures strongly increase the autotrophic nitrification due to the significantly higher abundance of ammonia-oxidizing archaea (Hu et al., 2016). Secondly, the warming-induced increase in evaporation can result in more NO3− delivered to the root surface (Kuzyakov and Xu, 2013) which also improves the NO3- uptake. The warming-induced decline in soil moisture decreases the delivery of NH4+ to the roots, at least partly. Strongly negative correlations were found between NH4+ uptake and root N content (r = −0.816), and NH4+ uptake and total N uptake (r = −0.617) (Table 3), indicating the decline of NH4+ uptake under warming. The lower NH4+ uptake may result from warming-induced low ammonification (Carrillo et al., 2012) and NH4+ adsorption to soil minerals (Congreves et al., 2016). The labeled NH4+ was likely first adsorbed to soil particles rapidly, then up taken by roots. Although NH4+ may be used by wheat later, the measured uptake rate was low within the 3 h between tracer injection and sampling. Traditionally, the contribution of organic N to the total N uptake by

Fig. 5. Root and shoot N concentrations. TN, till with no warming; TW, till with warming; NN, no-till with no warming; NW, no-till with warming. Different lowercase letters indicate significant difference in root N concentration among four treatments. Different uppercase letters indicate significant difference in shoot N among four treatments (oneway ANOVA, p < 0.05).

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Fig. 8. Contribution of ammonium, nitrate, and glycine to total N uptake (as %) under four treatments. Values are means ( ± SE) of 4 replicates.

crops has been very low. Xu et al. (2008) found that glycine-derived N only contributed an estimated 0.5% of the total N uptake to corn, measured 4 h after tracer addition. Another study observed that glycine-N constitutes between 3.9% and 8.1% of the total N uptake by wheat over 24 h (Reeve et al., 2009). In the present study, the contribution of glycine-derived N to the total N uptake increased from 3% (average for till and no-till under no warming) to 8% (average for till and no-till with warming), and the glycine-N concentration in soil was increased by 2.5 times (Fig. 6). Meanwhile, a high correlation was observed between the glycine-N uptake and its content (r = 0.863, Table 3). In soil, free amino acid N (FAA-N) has two main sources: SOM decomposition and root exudates. As SOM decomposition is enhanced under warming, the release of FAA-N is also expected to increase in the soil (Bai et al., 2013; Rustad et al., 2001). Simultaneously, warming may enhance the release of root exudates, which also increases the organic N content in soil (Yin et al., 2013). These factors explain the dramatic increase in glycine-derived N under warming observed in the present study. Therefore, our results support our first hypothesis that warming could increase N uptake by wheat, especially that of organic N. When considering plant responses to climate change, it is important to distinguish between the different forms of N among the sources available to plants and those present within plants (Bloom, 2015). The

Fig. 9. Total N uptake rates under four treatments. TN, till with no warming; TW, till with warming; NN, no-till with no warming; NW, no-till with warming. Different lowercase letters indicate significant differences in total N uptake among four treatments at the same soil layer (one-way ANOVA, p < 0.05).

Table 3 Pearson correlation between selected parameters at 0–15 cm. Root N Conc.

Root N Conc. Shoot N Conc. Root Mass Shoot Mass Total Biomass NO3−-N Cont. NH4+-N Cont. GlyCont. NT Uptake AM Uptake Gly-Derived N Uptake Total N Uptake Total N Cont.

Shoot N Conc.

Root Biomass

Shoot Biomass

Total Biomass

NO3−-N Cont.

1 0.882**

1

0.575 0.820** 0.810*

0.586* 0.758** 0.759**

1 0.720** 0.802**

1 0.992**

1

0.849**

0.661*

0.329

0.605*

0.581*

1

−0.558

−0.419

0.001

−0.108

−0.093

−0.527

NH4+-N Cont.

GlyCont.

NT Uptake

AM Uptake

Glyderived N Uptake

0.863 0.922** −0.685* 0.855**

0.238 0.581* −0.360 0.545

0.582 0.851** −0.569 0.784**

0.544 0.838** −0.556 0.774**

0.767 0.767** −0.615* 0.868**

−0.571 −0.478 .620* −0.613*

1 0.864** −0.725** 0.863**

1 −0.800** 0.948**

1 −0.754**

1

0.961**

0.902**

0.523

0.819**

0.800**

0.814**

−0.420

0.872**

0.955**

−0.617*

0.935**

**

**

**

**

−0.326

**

**

0.927

**

0.953

0.690

*

*

0.918

0.916

**

0.697

*

** Correlation is significant at the 0.001 level (2-tailed). * Correlation is significant at the 0.05 level (2-tailed).

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Total N Cont.

1

0.865 0.980** −0.816** 0.984**

**

Total N Uptake

0.798

0.959

−0.698

*

0.893

**

1 0.927**

1

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aggregates and exposes the protected SOM, enabling microbial decomposition. Previous studies have found higher levels of NO3−-N and NH4+ under conventional tillage than under no-till (Thomsen and Sørensen, 2006). However, in the long-term, no-till reduced N leaching and allowed more N from fertilizers and crop residues to be retained, due to a greater supply generated by microorganisms for crop uptake (Mbuthia et al., 2015; Zhang et al., 2016; Zuber and Villamil, 2016). Likewise, in the present study, significantly higher total N uptake rates were observed under no till than under till with no warming, which resulted in the crops obtaining more N under the previous condition. It is noteworthy that warming significantly diminished the differences between the total N content observed in the two tillage systems (from 26.3% between no till and till, with no warming, to 4.1% between no till and till treatments with warming). As would be expected, warming resulted in a similar decline in the difference in the total N uptake rate between the two tillage systems, from 12.5% to 4.2% (Fig. 7). These results indicated that N uptake was constrained by no-till as compared with till under warming, at least partly. So far, few studies have compared N uptake between the two tillage systems. Here, we determined that the differences in microbial biomass between till and no-till might be a main factor affecting N uptake. In previous studies, significantly higher concentrations of soil organic carbon and microbial biomass carbon were observed in the upper soil layer under no-till than under till (Hou et al., 2012a; Hou et al., 2016). Under warming, the elevated soil temperature would stimulate microorganisms to uptake more N with the increase in root exudation (Yin et al., 2013). In addition, microorganisms showed higher efficiency N uptake than did plant roots (Jones et al., 2013; Kuzyakov and Xu, 2013). In the future, the effects of warming and tilling on the competition for N between roots and microorganisms should be studied.

original balance between the uptake of the two main inorganic forms of N (NO3− and NH4+) and the total N was strongly affected by warming, resulting in an increased contribution of NO3− (by 16%, on average across both tilled and non-tilled plots) and a decreased contribution of NH4+ (by 21%) (Fig. 8). There were two explanations for this effect. First, the availability of NO3− in soil was twice that of NH4+ (Fig. 6). Warming increased the NO3− content by promoting nitrification by soil microbes that preferred the higher energy NH4+ to NO3− (Bloom, 2015). As a result, roots may delay the uptake of NH4+ and replace it, at least partially, with NO3- -N and glycine-N (Fig. 8). Second, NO3− is more mobile in soil solution than NH4+ (Jones et al., 2004; Tinker and Nye, 2000) and depletion zones around roots could develop. Thus, under warm conditions, NO3− would be delivered to the root surface faster with water than would NH4+. As a consequence of the contrasting responses of the two inorganic forms of N to warming, NH4+-N was negatively correlated with other parameters (Table 3). 4.3. Responses of N uptake to warming The nutrient uptake efficiency by crops is a principal determinant of crop biomass and yield (Tilman et al., 2002). Our results showed that warming notably increased the total N uptake rate and changed the N uptake pattern (Figs. 7 and 9). In addition to increasing wheat biomass, warming significantly enhanced total N uptake rate by 47% and 40% compared with that in non-warmed plots under till and no-till systems, respectively (Fig. 4). Two factors can explain this effect: N availability and soil moisture. First, higher total N availability in soil in the warmed plots improved root N uptake. Numerous studies indicated that warming increases soil N availability and N uptake by plants (Carrillo et al., 2012; Larsen et al., 2011; Melillo et al., 2002; Rustad et al., 2001) by stimulating soil microbial activity to increase soil N mineralization (Bai et al., 2013). Second, water uptake by roots influences their N uptake (Inselsbacher and Näsholm, 2012; Thomsen and Sørensen, 2006). Warming induces higher rates of transpiration, which can accelerate the delivery of nutrients to the surface of roots. Thus, roots can uptake more N under warm conditions when there is little water pressure (Kuzyakov and Xu, 2013). Furthermore, total N uptake rates were highly correlated with the total N content in wheat (r = 0.927, Table 3) and wheat biomass (r = 0.800), indicating that the increase in the available N in the soil, as a result of increased temperature, could directly support wheat growth. This effect explains the higher total biomass observed under warming. The warming-induced changes to the uptake of the three forms of N may contribute to a reduced risk from inorganic N in cropland in the future warmer world. We observed a high correlation between NO3−-N uptake rates and total biomass (r = 0.838), total N uptake (r = 0.955), and wheat total N content (r = 0.959) (Table 3), implying that the role of NO3−-N in wheat biomass production will be enhanced by warming. In combination with the high proportion of NO3−-N within the total N uptake (more than 70%) (Fig. 8), this means that more NO3−-N would be taken up under warm conditions, contributing to higher wheat biomass, but there may be loss of N through leaching. Meanwhile, a warming-induced decline in soil NH4+-N availability (Fig. 6) due to weakened ammonification would imply a potential decline in NH3 emissions (Bai et al., 2013). As a result, less fertilizer N would be lost through leaching or emission. At the same time, wheat would uptake more organic N under warmer conditions, potentially helping to decrease inorganic N input in cropland.

5. Conclusions Our results showed that higher temperature enhances the total N uptake of winter wheat, and the form of N preferentially taken up will shift to NO3−-N under both till and no-till systems. In addition, warming diminishes the advantage of higher N uptake and N content of the crops under no-till compared with till systems, which might be attributed to the more intensive competition by microbes for N under notill. These findings have important implications for our understanding of the mechanisms responsible for N uptake by winter wheat when nutrient enrichment is induced by global warming. These findings can improve our ability to predict the responses of crop growth to climate change. Acknowledgments This study was supported by the National Natural Science Foundation of China (Grant No. 31670485), National key R & D project (2016YFD030080803). References Bai, E., Li, S., Xu, W., Li, W., Dai, W., Jiang, P., 2013. A meta-analysis of experimental warming effects on terrestrial nitrogen pools and dynamics. New Phytol. 199, 431–440. Batts, G.R., Morison, J.K.L., Ellis, R.H., Hadley, P., Wheeler, T.R., 1997. Effects of CO2 and temperature on growth and yield of crops of winter wheat over four seasons. Eur. J. Agron. 25, 43–52. Bayer, C., Gomes, J., Zanatta, J.A., Vieira, F.C.B., Piccolo, M.D.C., Dieckow, J., Six, J., 2015. Soil nitrous oxide emissions as affected by long-term tillage, cropping systems and nitrogen fertilization in Southern Brazil. Soil Till. Res. 146, 213–222. Bloom, A.J., 2015. The increasing importance of distinguishing among plant nitrogen sources. Curr. Opin. Plant Biol. 25, 10–16. Bremer, E., Kessel, C.V., 1992. Plant-available nitrogen from lentil and wheat residues during a subsequent growing season. Soil Sci. Soc. Am. J. 56, 1155–1160. Cai, C., Yin, X., He, S., Jiang, W., Si, C., Struik, P.C., Luo, W., Li, G., Xie, Y., Xiong, Y., 2016. Responses of wheat and rice to factorial combinations of ambient and elevated CO2 and temperature in FACE experiments. Glob. Change Biol. 22, 7625–7638.

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