A possible mechanism of mineral responses to elevated atmospheric CO2 in rice grains

A possible mechanism of mineral responses to elevated atmospheric CO2 in rice grains

Journal of Integrative Agriculture 2015, 14(1): 50–57 Available online at www.sciencedirect.com ScienceDirect RESEARCH ARTICLE A possible mechanism...

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Journal of Integrative Agriculture 2015, 14(1): 50–57 Available online at www.sciencedirect.com

ScienceDirect

RESEARCH ARTICLE

A possible mechanism of mineral responses to elevated atmospheric CO2 in rice grains GUO Jia1, 2, ZHANG Ming-qian2, 3, WANG Xiao-wen1, 4, ZHANG Wei-jian2, 5 1

Institute of Wetland Research, Chinese Academy of Forestry, Beijing 100091, P.R.China Institute of Applied Ecology, Nanjing Agricultural University, Nanjing 210095, P.R.China 3 Technology Center of China Tobacco Fujian Industrial Co., Ltd, Xiamen 361021, P.R.China 4 Chinese Academy of Engineering, Beijing 100088, P.R.China 5 Institute of Crop Sciences, Chinese Academy of Agricultural Sciences/Key Laboratory of Crop Ecology, Physiology & Production, Ministry of Agriculture, Beijing 100081, P.R.China 2

Abstract Increasing attentions have been paid to mineral concentration decrease in milled rice grains caused by CO2 enrichment, but the mechanisms still remain unclear. Therefore, mineral (Ca, Mg, Fe, Zn and Mn) translocation in plant-soil system with a FACE (Free-air CO2 enrichment) experiment were investigated in Eastern China after 4-yr operation. Results mainly showed that: (1) elevated CO2 significantly increased the biomass of stem and panicle by 21.9 and 24.0%, respectively, but did not affect the leaf biomass. (2) Elevated CO2 significantly increased the contents of Ca, Mg, Fe, Zn, and Mn in panicle by 61.2, 28.9, 87.0, 36.7, and 66.0%, respectively, and in stem by 13.2, 21.3, 47.2, 91.8, and 25.2%, respectively, but did not affect them in leaf. (3) Elevated CO2 had positive effects on the weight ratio of mineral/biomass in stem and panicle. Our results suggest that elevated CO2 can favor the translocation of Ca, Mg, Fe, Zn, and Mn from soil to stem and panicle. The CO2-led mineral decline in milled rice grains may mainly attribute to the CO2-led unbalanced stimulations on the translocations of minerals and carbohydrates from vegetative parts (e.g., leaf, stem, branch and husk) to the grains. Keywords: climate change, free-air CO2 enrichment (FACE), hidden hunger, nutritional quality, paddy field, rice

1. Introduction Atmospheric CO2 concentration has exceeded the pre-industrial levels by about 40% (IPCC 2013) and is projected to double during the second half of this century (Solomon

Received 5 March, 2014 Accepted 30 June, 2014 Correspondence ZHANG Wei-jian, Tel/Fax: +86-10-62156856, E-mail: [email protected]; WANG Xiao-wen, Tel: +86-1062824186, Fax: +86-10-62824182, E-mail: [email protected] © 2015, CAAS. All rights reserved. Published by Elsevier Ltd. doi: 10.1016/S2095-3119(14)60846-7

et al. 2007). Attentions have been paid to the impacts of elevated CO2 on food security. Nearly two billion people worldwide are malnourished (Leyva-Guerrero et al. 2012). Atmospheric CO2 enrichment may intensify the problem of nutrient malnutrition (i.e., hidden hunger) (Loladze 2002; Stafford 2007) although it can enhance crop productivity (Long et al. 2006). Therefore, a better understanding of CO2-led impacts on food quality, such as mineral nutrient, will greatly benefit food security and human health in future climate pattern. In long term, elevated atmospheric CO2 can affect plant growth and metabolism indirectly through impacting the interactions among plant, soil and microorganisms in a plant-soil system (de Graaff et al. 2006) although, in short

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paddy field. In our previous reports, significant decrement of mineral (N, K, Ca, Mg, Fe, Zn and Cu) concentrations in milled rice grains occurred under elevated CO2 (Pang et al. 2005; Yang et al. 2007). But the underlying mechanisms need further study. So, after 4-yr operation, we investigated CO2-induced effects on minerals in plant-soil system. Our objectives were to learn (1) the responses of bio-available mineral supply in soil, (2) the responses of mineral translocations in plant, and (3) the possible mechanisms underlying the CO2-led mineral dilution in milled rice grains.

2. Results 2.1. Rice biomass growth The effect of elevated CO2 on rice aboveground biomass growth was presented in Fig. 1. The elevated CO2 significantly increased the stem and panicle biomass (Fig. 1). The biomass of stem in the treatments of FACE with high N application (FH), ambient with high N application (AH), FACE with low N application (FL), and ambient with low N application (AL) were 0.62, 0.52, 0.60, and 0.48 kg m–2, respectively, and the biomass of panicle in FH, AH, FL, and AL were 1.0, 0.8, 1.0 and 0.8 kg m–2, respectively. Averaged across two N levels, the biomass of stem and panicle in the FACE plots were significantly 21.9 and 24.0% higher than in the ambient. The effects of N application level or its interaction with CO2 enrichment were not significant (Table 1).

2.2. Relative changes of bio-available mineral concentration in soil The mineral bioavailability in the soil was enhanced by elevated CO2 (Fig. 2). Under high N application, the elevated CO2 significantly increased the bio-available concentrations of Ca on 40 DAT (days after transplanting) (35.7%), Mg on 40 DAT (16.0%), Fe on 40 DAT (20.2%) and 76 DAT (42.7%),

Biomass (kg m−2)

term, directly through influencing plant photosynthesis (Ainsworth and Long 2005). Studies show elevated CO2 can enhance crop aboveground growth (Kimball et al. 2002), change aboveground metabolism (such as the increment of C/N) (Kimball et al. 2002), improve root and microorganism growth and activities (Hu et al. 2001), change soil physical and chemical properties (Prior et al. 2004; Cheng et al. 2010). So, the effects of elevated atmospheric CO2 on the mineral concentration of milled rice grains might be mainly attributed to three reasons: (1) Soil bio-available mineral supply might not meet crop demand under elevated CO2. Because CO2-led enhancement of crop growth (Kimball et al. 2002; Jablonski et al. 2002) might lead to increment of mineral uptake, the supply of bio-available minerals in the soil might not meet crop demand. (2) Mineral absorption and transport by roots might be restricted under elevated CO2. On one hand, elevated CO2 can stimulate the growth and activities of rhizospheric microorganisms (Hu et al. 2001) and thus accelerate the competition of mineral uptake between roots and microorganisms (Cheng 1999), which might limit mineral absorption by roots. On the other hand, elevated CO2 can alter the tissue composition of plant organs (Booker and Maier 2001), which might affect the mineral transport from roots to aboveground organs. (3) The translocations of minerals and carbohydrates from vegetative parts (e.g., leaf, stem, branch and husk) to the grains might be stimulated unbalancedly under elevated CO2. Elevated CO2 can stimulate the translocations of carbohydrates from vegetative parts to the grains (Jablonski et al. 2002; Kimball et al. 2002). But the mineral translocation from vegetative parts to the grains is relatively difficult compared with the carbohydrate. Therefore, the stimulatory effects of elevated CO2 on mineral accumulation in the grains may be lower than on the carbohydrate, consequently resulting in the dilution of mineral content in the grains. Growing evidence have shown the CO2-led dilution effect (Loladze 2002; Stafford 2007) can decrease mineral concentrations (Ca, Mg, Fe, Zn, Mn, et al.) in milled crop grains (Pang et al. 2005; Yang et al. 2007; Högy and Fangmeier 2008; Pleijel and Danielsson 2009). However, how the elevated atmospheric CO2 results in mineral dilution in milled rice grains needs further study. At present, more than two billion people in the world are afflicted by the hidden hunger, micronutrient deficiencies (Sanchez and Swaminathan 2005). Rice is the staple food for more than 50% population of the world (Sass and Cicerone 2002). The CO2-led dilution of mineral content in rice grains may further aggravate the existing serious micronutrient malnutrition, especially in the developing world (Savithri et al. 1999; Welch and Graham 2004). In order to learn the impacts of elevated CO2 on rice productivity and quality, we set up a Free-air CO2 enrichment (FACE) experiment in

FH

1.5

0.0

FL

AL a

1.0 0.5

AH a

a a a Le af

a

b a b Ste m

b

a

b

Panicle

Fig. 1 Rice aboveground biomass weight at maturity. FH, AH, FL, and AL stand for Free-air CO2 enrichment (FACE) with high N (HN) application, ambient air CO2 concentration (ambient) with HN application, FACE with low N (LN) application, and ambient with LN application, respectively. Values are means±SE and significantly different (P<0.05) within each parameter when followed by a different letter. The same as below.

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Table 1 The split-plot ANOVA design results of leaf, stem and panicle biomass CO2 N CO2×N

Leaf ns ns ns

Stem

Panicle

*

*

ns ns

ns ns

60 40

*

0

, significant at the level of P=0.05; ns, not significant at the level of P=0.05. The same as below.

30 20

2.3. Mineral concentration in rice plant

LN

20

*

40

59

76

59

76

Mg *

*

10 0 Relative CO2 effect (%)

and Mn on 76 DAT (25.1%). And under low N levels, the elevated CO2 significantly increased the bio-available concentrations of Mg on 40 DAT (16.7%), Fe on 40 DAT (21.8%) and 76 DAT (29.8%), and Zn on 40 DAT (188.3%). Over all sampling dates, the mean bio-available concentrations of Ca, Mg, Fe, Zn, and Mn in the FACE plots were respectively 24.9, 12.2, 26.6, 101.6, and 18.7% higher than in the ambient under high N application, and 6.2, 6.8, 20.1, 174.8, and 15.2% higher under low N application. Averaged across two N levels and sampling dates, CO2 enrichment increased the concentrations of bio-available Ca, Mg, Fe, Zn, and Mn in the surface soil (0–15 cm) by 15.6, 9.5, 23.4, 138.2, and 16.9%, respectively.

HN

Ca

−10 60

40 Fe

*

40 20 0 300

* *

*

40 Zn

59

76

59

76

*

200 100 0 60

40 Mn

40

Overall, the mineral concentrations in rice shoot components were stimulated by elevated CO2 (Fig. 3). The concentrations of Ca in the leaf in the treatments of FH, AH, FL, and AL were 8.4, 7.0, 8.9, and 8.6 mg g–1, respectively. Averaged over two N levels, the concentrations of Ca in the leaf were 11.1% higher in the FACE plots than in the ambient. In the stem, the concentrations of Fe in the treatments of FH, AH, FL and AL were 0.25, 0.16, 0.24, and 0.21 mg g–1, respectively, and the concentrations of Zn were 0.037, 0.023, 0.040, and 0.027 mg g–1, respectively, and the concentrations of Mn were 0.33, 0.31, 0.26, and 0.26 mg g–1, respectively. Averaged across two N levels, CO2 enrichment increased the concentrations of Mg, Fe, Zn, and Mn by 5.0, 33.3, 53.5, and 3.3% with no significant effect on Ca content. For the panicle, in the treatments of FH, AH, FL, and AL, the concentrations of Ca were 0.42, 0.28, 0.40, and 0.35 mg g–1, respectively, the concentrations of Mg were 1.1, 1.0, 1.1, and 1.0 mg g–1, respectively, and concentrations of Fe were 0.10, 0.078, 0.11, and 0.073 mg g–1, respectively, the concentrations of Zn were 0.024, 0.022, 0.024, and 0.022 mg g–1, respectively, and the concentrations of Mn were 0.068, 0.046, 0.058, and 0.048 mg g-1, respectively. Averaged over two N levels, the concentrations of Ca, Mg, Fe, Zn, and Mn in the FACE plots were respectively 30.3, 3.9, 42.2, 8.9, and 33.8% higher than in the ambient. There was no clear trend of N-induced effect or its interaction with CO2 on the mineral concentrations (Table 2).

*

20 0

40

59

76

Days after transplanting (d)

Fig. 2 Relative CO2 effects on the bio-available contents of Ca, Mg, Fe, Zn, and Mn in the 0–15 cm soil. Asterisk means the CO2 effects were significant at P<0.05. HN and LN stand for high N application and low N application, respectively.

2.4. Mineral accumulation in rice plant Similar to the mineral concentrations in the shoot components, mineral accumulation amounts were also enhanced by the elevated CO2 (Fig. 4). In the leaf, the amounts of Ca in the treatments of FH, AH, FL, and AL were 8.4, 7.0, 8.9, and 8.6 g m–2, respectively, and the amounts of Zn were 8.9, 8.6, 7.9, and 7.6 mg m–2. Averaged across two N levels, the amounts of Ca and Zn in the leaf were respectively 4.8 and 4.1% higher in the FACE plots than in the ambient. In the stem, the amounts of Ca in the treatments of FH, AH, FL, and AL were 0.90, 0.85, 0.87, and 0.71 g m–2, respectively, the amounts of Mg were 0.97, 0.72, 0.73, and 0.69 g m–2, respectively, the concentrations of Fe were 157.5, 104.9, 145.2, and 100.8 mg m–2, respectively, the concentrations of Zn were 23.1, 11.7, 24.5, and 13.1 mg m–2, respectively, and the concentrations of Mn were 203.0, 162.4, 159.2, and

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Mn (mg g−1)

Zn (mg g−1)

Fe (mg g−1)

Mg (mg g−1)

Ca (mg g−1)

12 8

a

b

a a

FH

4 0 3 2

a a a

Le af a a a

1 0 0.6 0.4 0.2

a a

a a

a a

0.02 0.00 1.2 0.8

a

Le af a a

a ab b ab

a

b

a

ab

Ste m a a ab b

Ste m

spectively, the amounts of Mg were 1.1, 0.87, 1.1, and 0.86 g m–2, respectively, the concentrations of Fe were 97.4, 63.6, 99.4, and 41.6 mg m–2, respectively, the concentrations of Zn were 24.4, 17.6, 24.3, and 18.0 mg m–2, respectively, and the concentrations of Mn were 69.5, 37.6, 57.7, and 39.0 mg m–2, respectively. Averaged across two N levels, the amounts of Ca, Mg, Fe, Zn, and Mn increased 61.2, 28.9, 87.0, 36.7, and 66.0% in the FACE plots, respectively. No consistent trend in the N-led effect and its interaction with CO2 occurred on the mineral accumulation (Table 2).

AL

a c ab b Panicle a a a a Panicle

3. Discussion

a a a a

With the same rice variety, our previous investigations have evidenced that elevated CO2 had negative effects on Ca, Mg, Fe, Zn, and Mn concentrations in milled rice grains (Pang et al. 2005; Yang et al. 2007), which were also found in other crops (Högy and Fangmeier 2008). The results are mainly attributed to the dilution by carbohydrates under elevated CO2 in most former reports (Högy and Fangmeier 2008; Taub et al. 2008). But the deeper mechanisms need further investigation. In the introduction, we proposed three possible reasons. However, the results of relative changes of bio-available mineral concentration in soil (Fig. 2) showed the elevated CO2 stimulated mineral bioavailability in paddy soil. So the proposed reason one was not true. The results of mineral concentrations (Fig. 3) and accumulations (Fig. 4) in rice plant suggest the mineral uptake and upward transport by roots were also unrestricted. So, the proposed reason two was also not true. Therefore, the proposed reason three may play an important role in the dilution effects. Firstly, instead of decreasing soil mineral bioavailability, CO2 enrichment significantly increased the bio-available

Panicle a a a a

Panicle

a a ab b b

0.4 0.0

a a

Ste m

Le af a a

FL

Ste m

Le af

0.0 0.06 0.04

AH

Le af

Ste m

a b ab b Panicle

Fig. 3 Mineral concentrations in rice leaf, stem and panicle at maturity.

126.9 mg m–2, respectively. Averaged over two N levels, CO2

enrichment also increased the amounts of Ca, Mg, Fe, Zn, and Mn by 13.2, 21.3, 47.2, 91.8, and 25.2%, respectively. In the panicle, the amounts of Ca in the treatments of FH, AH, FL, and AL were 0.43, 0.23, 0.40, and 0.28 g m–2, re-

Table 2 The split-plot ANOVA design results of minerals in soil and plant

Ca

Mg

Fe

Zn

Mn

1)

CO2 N CO2×N CO2 N CO2×N CO2 N CO2×N CO2 N CO2×N CO2 N CO2×N

DAT, day after transplanting.

Soil Concentration1) 40 DAT 59 DAT 76 DAT * ns ns ns ns ns ns ns ns * * ns * ns ns ns ns ns * * ns ns ns ns ns ns ns * ns * ns ns ns ns ns ns ns ns ns * ns ns ns ns ns

Plant Leaf *

ns ns ns ns ns ns ns ns ns ns ns ns ns ns

Concentration Stem ns ns ns ns ns ns *

ns ns *

ns ns ns ns ns

Panicle *

ns ns ns ns ns ns ns ns ns ns ns *

ns ns

Accumulation Stem * ns ns ns ns ns * ns ns ns ns ns * ns ns ns ns ns * ns ns ns ns ns * ns ns ns ns ns

Leaf

Panicle *

ns ns *

ns ns *

ns ns *

ns ns *

ns ns

Mg (g m−2) Fe (mg m−2) Zn (mg m−2)

mineral contents in paddy soil (Fig. 2). Similar results were also found in Duke Forest FACE (Andrews and Schlesinger 2001) and our FACE in wheat season (Wang et al. 2008). This means that the supply of bio-available minerals in soil is enough for rice growing under elevated CO2. The CO2-led stimulatory effects on rice aboveground components (Fig. 1; Yang et al. 2006a, b; Ma et al. 2007) can enhance root growth (Yang et al. 2008) and exudation (Ma et al. 2004), as well as soil microbial growth and activity (Cheng et al. 2010). As a result, belowground environmental conditions are changed (e.g., soil acidification (Cheng et al. 2010)). These CO2-led belowground changes, such as soil acidification, will accelerate mineral transformation from bio-inactive reservoirs to the bioactive ones (Guo et al. 2012). Therefore, due to the huge bio-inactive mineral reservoirs in the soil, paddy field may supply enough bio-available minerals for rice growing in a long-term under future atmospheric CO2 enrichment. Secondly, the CO2-led increments in the mineral concentration (Fig. 3) and accumulation (Fig. 4) in rice aboveground biomass indicate that the mineral uptake and upward transport by rice roots was not limited. Although elevated CO2 can intensify mineral competition between rice roots and soil microorganisms (Cheng 1999), there are enough bio-available minerals for their demands due to the CO2-enhanced soil mineral bioavailability (Fig. 2). Actually, the simultaneous increased mineral concentrations in the leaf, stem and panicle (Fig. 3) suggests that (1) the CO2-led stimulatory effects on mineral uptake via roots are higher than the effects on biomass growth, and (2) elevated CO2 promotes upward transport of mineral by roots. Recent research has also reported that elevated CO2 could significantly stimulate mineral uptake and transport by tomato roots even growing in Fe-limited media (Jin et al. 2009). In a word, CO2 enrichment will facilitate mineral uptake and transport via roots through increasing soil mineral bioavailability (Fig. 2) and root growth and activity (Yang et al. 2008). Finally, the adverse responses of mineral concentrations in rice grains (Pang et al. 2005; Yang et al. 2007) and the panicle (Fig. 3) indicate that CO2-led diluting effects may be mostly attributed to the unbalanced translocations of minerals and carbohydrates from vegetative parts (e.g., leaf, stem, branch and husk) to the grains. Elevated CO2 can significantly increase carbohydrate translocation to the grains, resulting in significant accumulation of carbohydrate in the grains (Yang et al. 2006b). However, most mineral translocations from vegetative organs to the grains are relatively difficult and slow compared with the carbohydrates. Consequently, the CO2-stimulated minerals translocation to the grains may not match up the carbohydrate translocation. Therefore, the mineral nutrient accumulations are diluted by the carbohydrates, resulting in the CO2-led

Ca (g m−2)

GUO Jia et al. Journal of Integrative Agriculture 2015, 14(1): 50–57

Mn (mg m−2)

54

3 2

ab b

a a

0 1.5

Leaf ab

a b ab Leaf

200 100 0 45

a a

a a

a a a a

0 300

Leaf a a a a

100 0

Leaf

a b a a

b b b

a

a

a a

a

a bc

Stem b bc c

Stem

b

a

c

Panicle

a c

a

Panicle a b b

Panicle

Stem ab

15

AL

Stem

Leaf

30

200

FL

Stem a

1.0

0.0 300

AH

a a a a

1

0.5

FH

b

a

b

Panicle

a

b a b Panicle

Fig. 4 Mineral accumulations in rice leaf, stem and panicle at maturity.

dilution of mineral nutrients in the grains. However, our evidences were not directly related to mineral translocation to or assimilation in the grains. Thus, further efforts still need to be paid on the unbalanced translocations of minerals and carbohydrates to grains under CO2 enrichment. In summary, our research suggests that future agronomic practices on the improvement of mineral translocation to the grains should be taken to enhance food quality. As discussed above, elevated CO2 will increase soil mineral bioavailability to crops in the long term. Meanwhile, CO2 enrichment can also stimulate mineral uptake and transport upward by roots. Therefore, crop variety improvement may be a critical measurement to promote mineral translocations from vegetative parts to the grains. Since our evidences are indirectly related to mineral translocation in rice plant, more efforts should be paid on further understanding of the dissimilar responses of minerals and carbohydrates translocations to the grains under future climate pattern.

4. Conclusion The field-based data in our research showed that elevated CO2 significantly increased the biomass of stem and panicle of rice by 21.9 and 24.0%, and the contents of Ca, Mg, Fe, Zn, and Mn in panicle (including branch and husk) and in

GUO Jia et al. Journal of Integrative Agriculture 2015, 14(1): 50–57

stem by 61.2, 28.9, 87.0, 36.7, 66.0% and 13.2, 21.3, 47.2, 91.8, 25.2%. Although the biomass and mineral accumulation of stem and panicle were both increased, the weight ratio of mineral/biomass in stem and panicle was stimulated by elevated CO2. Meanwhile, the supply of bio-available minerals in 0–15 cm depth soil was also stimulated by elevated CO2. So based on above data, we found that elevated CO2 can favor the translocation of Ca, Mg, Fe, Zn, and Mn from soil to stem and panicle. Together with the results of CO2-led mineral decline in milled rice grains reported by former studies, we proposed elevated CO2 may stimulate unbalanced translocations of minerals and carbohydrates from vegetative parts (e.g., leaf, stem, branch and husk) to the grains. However, further studies need to be carried out to investigate the specific and detailed mechanisms at the molecular level.

5. Materials and methods 5.1. Experiment site description The Free-air CO2 enrichment (FACE) system was set up in June 2004 near Jiangdu City, Jiangsu Province, China (32°35´5´´N, 119°42´0´´E, 5 m a.s.l.) on a calcareous soil (a Mollisol in USA-ST, pH=7.2). The system has been operating for more than 4 yr until the beginning of our experiment. The rice-wheat cropping system prevails in this region for more than 1 000 yr. Relevant soil properties were as follows: clay (<0.002 mm) 13.6%; silt (0.002–0.02 mm) 28.5%; sand (0.02–2 mm) 57.8%; bulk density 1.16 g cm–3; soil organic C 18.4 g kg–1; total N 1.45 g kg–1 and total P 0.63 g kg –1. The climate conditions are subtropical with mean annual precipitation and temperature being 980 mm and 14.9°C, respectively. The annual sunshine time and frostless period are more than 2 100 h and 220 d, respectively.

5.2. FACE system design The FACE system had two target CO2 concentrations randomly located in six replicate octagonal plots (three for elevated CO2 and the others for the ambient). Each plot had a useful area of 80 m2. The CO2 concentration in the elevated plots (hereinafter referred to as FACE) was controlled constantly 200 μmol mol-1 higher than that in the ambient (hereinafter referred to as Ambient). Adjacent plots were buffered more than 90 m to minimize CO2 contamination. Each plot was averagely split into high and low level N subplots (25 and 12.5 g m–2, respectively) and separated with surrounding area by polyvinyl chloride (PVC) board. In each plot, a 30–cm tall PVC board was inserted into soil between high and low level N subplots (10 cm into soil and 20 cm above the soil surface) to prevent the cross-

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over of water and nutrients. So there were four treatments of the experiment, FACE with high N application (FH), ambient with high N application (AH), FACE with low N application (FL) and ambient with low N application (AL). More details of the FACE system such as design, rationale, operation and performance were provided by Liu et al. (2002) and Okada et al. (2001).

5.3. Crop management A Oryza japonica cv. Wuxiangjing 14 was tested in the experiment. And it was a major local cultivar for the target area with large panicle (ca. 155 spikelets per panicle) and a high-yielding potential. Standard cultivation practices as commonly performed in the area were followed in all experimental plots. Every year in rice growing season, rice seeds were respectively sown under elevated and ambient CO2 in mid-May. In mid-June, rice seedlings were transplanted manually into their corresponding field plots at a density of three seedlings hill-1 and 24 hills m-2. About 36% of the total N was applied as a basal dressing one day prior to transplanting and 24% as a side dressing at early tillering on 6 days after transplanting (DAT), and the other 40% at panicle initiation on 43 DAT. Typical irrigation regimes of the surrounding areas were conducted. Each plot was submerged with water (about 5 cm in depth) from mid-June to -July, and drained dry several times to the beginning of August, and then flooded with intermittent irrigation until 10 days before harvest.

5.4. Sampling method and measurement At rice maturity in 2008, in order to ensure representativeness of the sampling, the number of stems in 100 hills was counted at different places in each subplot, and then five plants with the mean stem number were selected. The aboveground of the selected plants were taken and then separated into leaves, stems (including leaf and leaf sheaths) and panicles (including milled rice grains, branches and husks). The portions of the plant were oven-dried at 80°C to a constant weight and weighed. Afterwards, they were ground and passed through 0.5 mm mesh sieve. The concentrations of Ca, Mg, Fe, Zn, and Mn in all the plant parts were extracted with HNO3, HF and H2O2 on a microwave digestion system (Berghof MWS-3; Berghof Products, Eningen, Germany) and then determined by an inductively coupled plasma atomic emission spectrometer (Optima 2100DV ICP-AES, PerkinElmer, USA) (Bi et al. 2009). The mineral accumulations in shoot parts were calculated by the biomass dry weight and the mineral concentration within each part. The 0–15 cm soil samples were collected on 40, 59 and

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76 DAT, which were chosen to conform to the key stages of rice growing as far as possible. Soil samples from each subplot were chosen randomly from six spots and avoided repetition with the next time. As soon as the samples were transported to the laboratory on the sampling day, each sample was timely homogenized and picked up all the visible extraneous materials (residues, roots and stones). The samples which were not measured on the sampling day were stored in a 4°C condition prior to analysis and measured as soon as possible. The bio-available Ca, Mg, Fe, Zn and Mn in the soil were extracted with CH3COONH4 (1.0 mol L–1, pH 7.0) and then determined by an inductively coupled plasma atomic emission spectrometer (Optima 2100DV ICP-AES, PerkinElmer, USA) (Bao 2008; Bi et al. 2009). The relative CO2 effect on the minerals (Ca, Mg, Fe, Zn and Mn) was calculated as: Relative effect (%)=[Ca (or Mg, Fe, Zn and Mn) concentration under elevated CO2–Ca (or Mg, Fe, Zn and Mn) concentration under ambient CO2] ⁄ [Ca (or Mg, Fe, Zn and Mn) concentration under ambient CO2]×100

5.5. Statistical analysis Data were analyzed with Excel 2003 for Win and the statistical package SPSS11.5. A split-plot ANOVA design was used with CO2 levels as the main plot factor and N levels as the subplot factor. Multiple comparisons were also performed to permit separating of effect means. Differences were considered significant at P<0.05.

Acknowledgements This work was supported by the National Natural Science Foundation of China (31200369), the Lecture and Study for Outstanding Scholars from Home and Abroad, Chinese Academy of Forestry (CAF), 2014. We are grateful to Dr. Hu Shuijin in Department of Plant Pathology, North Carolina State University for his constructive suggestions to this research, Dr. Zhu Jianguo and Dr. Xie Zhubin in the Institute of Soil Science, Chinese Academy of Sciences, China, for his great comments on this investigation.

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