Agriculture, Ecosystems and Environment 209 (2015) 132–137
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Yield and nitrogen accumulation and partitioning in winter wheat under elevated CO2: A 3-year free-air CO2 enrichment experiment Xue Han a,1, Xingyu Hao a,b,1, Shu Kee Lam c, Heran Wang d , Yingchun Li a , Tim Wheeler e, Hui Ju a , Erda Lin a, * a
Key Laboratory of Ministry of Agriculture on Agro-environment and Climate Change, Agro-environment and Sustainable Development Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China College of Agronomy, Shanxi Agricultural University, Taigu 030801, Shanxi, China c Crop and Soil Science Section, Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Victoria 3010, Australia d Institute of Meteorological Sciences of Liaoning Province, Shenyang 110166, China e Walker Institute for Climate Systems Research, School of Agriculture, Policy and Development, University of Reading, RG6 6AR, United Kingdom b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 3 May 2014 Received in revised form 27 March 2015 Accepted 7 April 2015 Available online 1 June 2015
Fossil fuel combustion and deforestation have resulted in a rapid increase in atmospheric [CO2] since the 1950’s, and it will reach about 550 mmol mol1 in 2050. Field experiments were conducted at the Free-air CO2 Enrichment facility in Beijing, China. Winter wheat was grown to maturity under elevated [CO2] (550 17 mmol mol1) and ambient [CO2] (415 16 mmol mol1), with high nitrogen (N) supply (HN, 170 kg N ha1) and low nitrogen supply (LN, 100 kg N ha1) for three growing seasons from 2007 to 2010. Elevated [CO2] increased wheat grain yield by 11.4% across the three years. [CO2]-induced yield enhancements were 10.8% and 11.9% under low N and high N supply, respectively. Nitrogen accumulation under elevated [CO2] was increased by 12.9% and 9.2% at the half-way anthesis and ripening stage across three years, respectively. Winter wheat had higher nitrogen demand under elevated [CO2] than ambient [CO2], and grain yield had a stronger correlation with plant N uptake after anthesis than before anthesis at high [CO2]. Our results suggest that regulating on the N application rate and time, is likely important for sustainable grain production under future CO2 climate. ã2015 Elsevier B.V. All rights reserved.
Keywords: Free-air Carbon dioxide enrichment (FACE) Nitrogen uptake Nitrogen accumulation Winter wheat
1. Introduction The carbon dioxide concentration ([CO2]) in the atmosphere has been increasing since the industrial revolution (from 280 to currently 400 mmol mol1), and is predicted to reach 550 mmol mol1 by 2050 (IPCC, 2007). Increasing [CO2] stimulates photosynthetic processes and often increases crop growth and yield (Drake et al., 1997; Kimball et al., 2002). Nitrogen (N) is essential for plant growth; the biogeochemical N cycle and associated processes will therefore be affected by elevated [CO2] (Hungate et al., 2003; Long et al., 2006; Lam et al., 2012a). Wheat is a staple food crop for almost half the world’s human population. The effects of elevated [CO2] on wheat grain yield and protein have been widely studied; elevated [CO2] generally increases wheat grain yield by 13–37% (Kimball, 1983; Cure and Acock, 1986; Amthor, 2001; Long et al., 2006), but decreases its
* Corresponding author. Tel.: +86 10 82105998. E-mail address:
[email protected] (E. Lin). The first two authors contributed equally to this work.
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http://dx.doi.org/10.1016/j.agee.2015.04.007 0167-8809/ã 2015 Elsevier B.V. All rights reserved.
protein concentration by 10–20% (Jablonski et al., 2002; Taub and Wang, 2008). These consequences for grain yield and quality are associated with the redistribution and availability of N for developing grain. It has been reported that under ambient [CO2] most of the grain N is derived either from N reduced during grain filling or remobilization of N from vegetative parts or from both sources (Donovan and Lee 1978). Different organs contribute at varying capacity to grain filling (Simpson et al., 1983). Will the N partitioning be affected by [CO2]-induced changes in wheat growth and N demand? While the responses to elevated [CO2] of grain yield and N concentration have been shown to be N-dependent (Rogers et al., 1996; Sinclair et al., 2000; Kimball et al., 2002), how will different fertilizer N inputs affect the N uptake and partitioning at various key growth stages of wheat? Free-air CO2 enrichment (FACE) technology is currently regarded as the most realistic and natural CO2 exposure system. FACE experiments on wheat were conducted in the USA, southern China, Australia and Germany (Kimball et al., 2002; Ma et al., 2007; Lam et al., 2012b; Weigel and Manderscheid, 2012). While northern China is a major winter wheat production region, with 60% of the national wheat production (Zhao, 2010), the
X. Han et al. / Agriculture, Ecosystems and Environment 209 (2015) 132–137
association between the responses of wheat grain yield and N accumulation and distribution to elevated [CO2] under field conditions in northern China cropping systems is not well understood. This is particularly important as excessive N fertilization in intensive agricultural areas of China has become a major concern. From 1977 to 2005, total annual grain production in China increased from 283 to 484 million tons (a 71% increase), but synthetic N fertilizer application increased from 7.07 to 26.21 million tons (a 271% increase) over the same period (Ju et al., 2009). A FACE experiment was therefore carried out in Beijing, China to investigate the interactive effects of elevated [CO2] and N supply on winter wheat production and N partitioning. In this higher [CO2] world the sustainability of wheat production may be in jeopardy unless current N management strategies are changed. The objectives of the study were to investigate the response to elevated [CO2] of wheat grain yield in a semi-arid cropping system in northern China, and how the response relates to the effects of elevated [CO2] on N accumulation and distribution in wheat. 2. Materials and methods 2.1. Experimental site The study site is located in an experimental farm in a wheatsoybean rotation in Changping (40 100 N, 116140 E), Beijing, China. The soil (0–0.20 m) is a clay loam with a pH (soil:water ratio of 1:5) of 8.4 and contained 1.06% organic C, 0.11% total N, 6.8 mg ammonium-N kg1, 18.7 mg nitrate-N kg1, 50 mg available phosphorus kg1 (Bray 1) and 140 mg ammonium acetate extractable potassium kg1. The rainfall over the three growing seasons from 2007 to 2010 was 339, 199 and 203 mm, respectively. The corresponding mean temperature was 9.6, 10.0 and 8.0 C, respectively. 2.2. Carbon dioxide concentration The experiment was conducted in the mini-FACE system described in Hao et al. (2012), which consists of 12 octagonal experimental areas, six elevated (three for low N (LN) and three for high N (HN) treatments) and six ambient (three for LN and three for HN treatments), each with a diameter of 4 m. The elevated and ambient atmospheric [CO2]s were measured throughout the season by sensors (Viasala, Finland) at the centre of each octagonal plot and averaged 550 17 and 415 16 mmo mol1, respectively. The plots were separated by at least 14 m to minimize crosscontamination of CO2 between plots. Comparison of the [CO2] of ambient plots with and without the release of CO2 gas to elevated plots showed that cross-contamination was negligible. In the elevated [CO2] plots, carbon dioxide exposure commenced at 6 days after sowing and terminated at harvest time, and [CO2] was maintained at 550 17 mmol mol1 from sunrise to sunset.
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was wintering water and the second was applied at the same day with side dressing fertilization to ease drought stress. 2.4. Sample collection and chemical analysis Areas of the crop were destructively sampled at different times over the season. Sampling dates were fixed so as to coincide as much as possible with the stem elongation stage (DC30), half-way anthesis (DC65) and ripening (DC90) of the plants. In 2008, plants were sampled at 19 April, 17 May and 7 June. In 2009, plants were sampled at 18 April, 27 May and 13 June. In 2010, plants were sampled at 9 May, 30 May and 27 June. The samples were separated into leaf, stem and spike (when applicable). All the plant parts were over-dried at 80 C for 72 h, weighed, and ground to fine powder of 0.25 mm for chemical analysis. The N concentrations of all plant parts were determined using a micro-Kjedahl procedure. Grain yield was determined from a 1 m2 patch in each plot. 2.5. Statistical analysis Data were analysed with the statistical package PASW 18.0 and EXCEL 2010. The experimental was designed as a split-plot with the whole plots arranged in randomized complete blocks, the levels of [CO2] (ambient or elevated [CO2]) were the whole-plot treatment and the levels of N (LN and HN) were the split-plot treatment. A general linear model was used to estimate the main effects of year, [CO2] and N levels, as well as their interactions. Statistical analysis of variance (ANOVA) was used to determine differences between treatment means. 3. Results 3.1. Effects of elevated [CO2] on grain yield Across three experimental years and N supply levels, elevated [CO2] increased the grain yield by 11.4% (p < 0.05) (Fig. 1). The [CO2]-induced increase in grain yield was 10.8 and 11.9% at LN and HN treatment, respectively. There was no significant interaction between elevated [CO2] and N supply on grain yield. Grain yield was not influenced by increasing N application. 3.2. Effects of elevated [CO2] on N concentration Irrespective of the experimental year and N input, elevated [CO2] decreased the N concentration of wheat plants by 4.5, 5.6 and 3.3% at the stem elongation, half-way anthesis and ripening stages,
[(Fig._1)TD$IG]
2.3. Wheat cultivation, fertilization and irrigation Winter wheat (Triticumaestivum L. cv. Zhongmai 175) was sown on 7 October 2007, 10 October 2008 and 10 October 2009, respectively, with a seeding rate of 150 kg ha1. Granular urea (N, 46%), diammonium phosphate (N:P2O5 = 13%:44%) and potassium chloride (K2O, 60%) were applied as basal fertilizer, at equal rates of 75 kg N ha1, 72 kg P ha1and 75 kg K ha1. At the stage of stem elongation (decimal code DC30; Zadoks et al., 1974) on 28 April, 2008,14 April, 2009 and 29 April 2010, respectively, granular urea at rates of 25 and 95 kg N ha1 was applied to low N (LN) and high N (HN) plots, respectively. Irrigation (equivalent to 60 mm rainfall) was applied twice during the whole growing seasons. The first one
Fig. 1. Effects of elevated [CO2] on grain yield of wheat at LN and HN levels across three cropping seasons. Values are means of the three replicates in each cropping season, and bars represent standard error for each treatment. a[CO2] and e[CO2] represent ambient [CO2] and elevated [CO2], respectively. ** p < 0.01, ns: not significant.
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[(Fig._2)TD$IG]
Fig. 2. Seasonal changes in N concentration of the plants subjected to ambient [CO2] and elevated [CO2] over three growing seasons. Values are means of the three replicates and bars represent standard error for each treatment.
respectively (Fig. 2). The interaction between CO2 and N input on N concentration was not significant. Regardless of [CO2] levels and experimental years, higher N input increased N concentration of wheat plants by 3.6, 3.6 and 3.9% at the stem elongation, half-way anthesis and ripening stages, respectively (Fig. 2). The year effects were significant (p < 0.05) for plant N concentration at all growth stages, but no significant interactions were observed between any treatment variables.
3.3. Effects of elevated [CO2] on N accumulation Elevated [CO2] increased the whole plant N accumulation by 12.9 (p < 0.05), and 9.2% (p < 0.05) at half-way anthesis and the ripening stage respectively, when averaged across experimental year and N inputs (Table 1). The positive effect of elevated [CO2] on N accumulation reached the maximum at half-way anthesis stage. Across [CO2] levels, the N accumulation was increased by 21.1
Table 1 The effect of elevated [CO2] on N accumulation of the plants. Values are means of the three replicates and standard error for each treatment. *p < 0.05, NS: not significant. Year
2008
N input
LN NN
2009
LN NN
2010
LN NN
Year [CO2] N input a
DC represents decimal code.
[CO2]
N accumulation (g m2) Stem elongation (DCa 30)
Half-way anthesis (DC 65)
Ripening (DC 90)
Ambient [CO2] Elevated [CO2] Ambient [CO2] Elevated [CO2]
13.3 2.9 13.6 1.6 19.2 1.5 17.3 1.1
17.1 0.5 19.5 0.7 18.7 1.5 20.3 0.7
19.8 1.3 21.2 1.1 18.6 2.2 20.5 0.9
Ambient [CO2] Elevated [CO2] Ambient [CO2] Elevated [CO2]
9.7 1.0 8.8 1.2 10.1 0.5 11.0 1.4
14.5 0.8 15.7 1.1 16.4 0.9 19.1 1.3
17.1 1.1 17.6 1.3 19.6 0.4 20.3 0.9
Ambient [CO2] Elevated [CO2] Ambient [CO2] Elevated [CO2]
9.0 0.9 10.1 2.1 9.5 0.1 11.1 0.8
17.9 2.3 21.8 2.5 18.7 2.1 20.2 2.8
14.6 2.1 18.6 0.7 18.5 1.5 20.1 0.5
* NS *
* * NS
0.09 * 0.06
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(p < 0.05), 6.4 (p > 0.05), and 8.0% (p = 0.06) under higher N input at the stem elongation, half-way anthesis and ripening stage, respectively. The interaction between [CO2] and N application on N accumulation was not significant. 3.4. Effects of elevated [CO2] on N distribution At the stem elongation stage (DC30), leaf accounted for 62.1– 64.0% of the aboveground plant N, while the remaining 36.0–37.9% was detected in stem (Fig. 3a). Neither elevated [CO2] nor N input had significant effect on the N allocation in different organs of wheat plants at this stage. At the half-way anthesis stage (DC65), the proportion of leaf in N dropped to 32.0–35.3%, while stem accounted for the majority of aboveground N at 37.5–40.5% (Fig. 3b). The remaining N was accumulated in spike, accounting for 26.3–27.7% (Fig. 3b). Averaged over all N levels and seasons, elevated [CO2] significantly decreased N fractions in leaves by 6.5% (p < 0.05), but increased N fractions in stem by 5.0% (p < 0.05) and spike by 1.5% (p > 0.05) (Fig. 3b). N fertilizer did not affect N distribution among different organs of plants at this stage. At the ripening stage (DC90), N distribution in leaf and stem was decreased to 5.3–6.0% and 9.8–11.8%, respectively (Fig. 3c). The majority of N (82.2–84.8%) was contained in spike (Fig. 3c). Across [CO2] levels and experiment years, N fractions in stems tended to increase (p = 0.08), while N fractions in spikes tended to decrease with increasing N supply (p = 0.09). However, elevated [CO2] had no significant effect on N allocation among different parts of wheat plants at the ripening stage. 4. Discussion Our study showed that the grain yield of winter wheat was enhanced by 11.4% under elevated [CO2]. The magnitude of yield enhancementwas similar tothe results in another 2-year FACE study on wheat (by 8.4%, Kimball et al., 1995). But Ma et al. (2007) in southern China wheat FACE experiment observed a stronger stimulation of final above ground biomass of 26.8% under high N (250 kg N ha1) and 13.5% under low N (125 kg N ha1) supply. In this study, the yield stimulation by elevated [CO2] is similar under low N and high N supply. Some studies showed that N deficiency may decrease the relative response to elevated [CO2] (Ainsworth and Long, 2005; Ziska and Bunce, 2007). For example, this has been shown for wheat (Wolf, 1996), barley (Kleemola et al., 1994) in Chamber studies and rice (Kim et al., 2003) in FACE experiment.
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However, some other studies with rice under FACE conditions and different N fertilizer input reported similar yield enhancement by elevated [CO2] under low N and sufficient N supply (Liu et al., 2008; Yang et al., 2009). It is well documented that the response of higher plants to elevated [CO2] often results in a decline in shoot N concentration (Rogers et al., 1996; Bloom et al., 2010; Yang et al., 2007b). In the present study, the plant N concentration was decreased by 1.8, 12.9 and 7.4% under elevated [CO2] at DC30, DC65 and DC90, respectively. This was comparable to the reduction N concentration observed in the other two FACE studies on wheat (5.6 to 17%) (Yang et al., 2007b; Weigel and Manderscheid, 2012). Some studies suggest the decline in plant N status is more obvious when the N supply is low than when the N supply is adequate (Rogers et al., 1996; Daepp et al., 2001; Kimball et al., 2002; Ainsworth and Long, 2005; Yang et al., 2007b). However, the [CO2]-induced decrease in N concentration in our study was not responsive to N supply. It indicates that there was plenty of available N in the soil in the present study site. We found that elevated [CO2] increased N accumulation in wheat plants by 7.4–12.9% over the growing seasons, except for the stem elongation stage. [CO2]-induced increases in N accumulation were also observed for wheat plants at a rice–wheat rotation FACE system in southern China (7–25%) (Yang et al., 2007b) and another semi-arid wheat production region in Australia (18–44%) (Lam et al., 2012b). Some studies showed the average response was greater under a high N application than under a low N application (Kim et al., 2003), but the interaction between [CO2] and N supply was not detected in our study. Except for the difference in crops species and environmental conditions between studies, one possibility for this contrasting finding may be due to the different levels of N supply. The N application rate in this trial was 100– 170 kg N ha1, while it was 40–150 kg N ha1 in the experiments conducted by Kim et al. (2003). In our previous study, the optimum fertilizerapplication rate was estimated to be 132–135 kg N ha1 based on the extra N demand in a CO2-rich world (Lam et al., 2012c). Thus, it indicates that under higher soil N availability, the interactive effect between [CO2] and N inputs is not apparent compared to the [CO2] main effect. Elevated [CO2] not only affected N accumulation, but it also altered N distribution among different organs in our study. The present results showed the proportion of N translocated from the roots to stems at anthesis was greater under elevated [CO2] than ambient [CO2]. But there was no significant difference in N distribution at the ripening stage. Stems were regarded as the
[(Fig._3)TD$IG]
Fig. 3. Effects on elevated [CO2] on N distribution among different organs of wheat crops at (a) stem elongation stage (DC30), (b) half-way anthesis (DC65) and (c) ripening (DC90) across the three growing seasons. Values are means of the three replicates over three cropping seasons for each treatment and bars represent the standard error. a [CO2] and e[CO2] represent ambient [CO2] and elevated [CO2], respectively.
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Table 2 The correlation coefficients between grain yield and nitrogen (N) uptake before and after half-way anthesis under elevated [CO2].
N uptake before half-way anthesis N uptake after half-way anthesis Total plant N uptake Grain yield
N uptake before half-way anthesis
N uptake after half-way anthesis
Total plant N uptake
Grain yield
1
0.666*
0.428NS
-0.153NS
1
0.370NS
0.546*
1
0.463NS 1
major N sink before anthesis. It was reported that N allocation to stems was enhanced by 8.5% under elevated [CO2] at heading, but was decreased for leaves and remain unchanged for panicles (Yang et al., 2007a). However, the N allocation to panicles was increased by 2.9% under elevated [CO2] at maturity, but was decreased for stems and leaves (Yang et al., 2007a) We found that a positive correlation between N uptake after half-way anthesis and grain yield under elevated [CO2] (Table 2). In present study, side dressing of fertilizer was applied at stem elongation stage, suggesting ample soil N supply before anthesis. Taking into consideration variation in plant N demand at different growth stages and yield response to elevated [CO2], fertilizer N strategies (the recommended application rates and time) for winter wheat production in northern China may need to be adjusted. We previously recommended that N application rate for winter wheat should be 132–135 kg N ha1 in this wheat growing region under elevated [CO2] (Lam et al., 2012c). Through this study, we further suggested that the proportion of N applied at stem elongation stage should be increased to match the extra N demand during the anthesis stage, i.e. from a current ratio of 6:4 (basal: stem elongation fertilizer application rate) to 5:5. These N management strategies would be important for sustainable wheat production in a high CO2 world. 5. Conclusions Elevated [CO2] increased the grain yield of wheat and N accumulation, thereby increasing crops demand for N. But the [CO2]-induced increase was not responsive to N supply. This may due to the adequate N supply in our study, the interaction between [CO2] and N supply on grain yield is not apparent compared to the [CO2] main effect. Considering on N uptake before and after anthesis, a positive correlation was detected between grain yield and N uptake after anthesis. This suggests the proportion of N applied after anthesis and timing across the season of the N application need to be changed to maintain N availability after anthesis, thus improve the grain yield under future elevated [CO2] conditions. Acknowledgements This work was supported by The National Basic Research Program of China (973 Program) (No. 2012CB955904), National Key Technology R&D Program in the 12th Five year Plan of China (No. 2013BAD11B03), the UK-China Sustainable Agriculture Innovation Network (SAIN) projects, The Agricultural Science and Technology Innovation Program of CAAS, and Natural Science Fund projects of Shanxi Province (No. 2013011039-3).
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