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Agriculture, Ecosystems and Environment 108 (2005) 342–349

Atmospheric CO2 concentration effects on N partitioning and

fertilizer N recovery in field grown rice (Oryza sativa L.)

W.M.W. Weerakoon a,*, K.T. Ingram b, D.N. Moss c,�

a Rice Research and Development Institute, Batalagoda, Ibbagamuwa, Sri Lankab Department of Crop and Soil Sciences, The University of Georgia, 1109 Experiment Street, Griffin, GA 30223-1797, USA

c Crop Science Department, Oregon State University, Corvallis, OR 97331, USA

Received 5 September 2003; received in revised form 29 December 2004; accepted 30 December 2004

Abstract

Lowland rice (Oryza sativa L.) responds positively to increased atmospheric CO2 concentration. However, the efficiency of

the canopy depends on the N status of the plant, which could vary with the change in uptake and partitioning of N with increased

atmospheric CO2. A field experiment was conducted at the International Rice Research Institute (IRRI) to determine changes in

N requirement of the rice crop and to propose suitable management strategies to overcome tissue N dilution with increased CO2

concentration. Rice variety IR72 was grown inside open top chambers at ambient (about 350 mmol mol�1) or elevated

(700 mmol mol�1) atmospheric CO2 in combination with three levels of applied N (0, 90, or 200 kg N ha�1). Rooting of rice was

linearly related to tillering, and the relationship did not change with CO2 concentrations, but with age of the crop. When adequate

N was not supplied, rice plants grown at high CO2 became inferior to plants grown at ambient CO2. N uptake and fertilizer N

recovery was higher in plants grown in high CO2 until maximum tillering, but the partitioning of N towards leaves decreased by

9%. Acclimation to high CO2 by rice may, therefore, be dependent on the N uptake. Increased N uptake under high CO2

environment was related to its larger root system, which was due to increased unproductive tillering. This suggests that if

tillering is limited, rice plants at high CO2 may suffer from N limitation due to changes in both uptake and partitioning. It is

concluded that management of the rice crop grown at high atmospheric CO2 should be different to that under current conditions.

# 2005 Elsevier B.V. All rights reserved.

Keywords: Rice; Carbon dioxide; N uptake; N partitioning; Roots; Oryza sativa L.

1. Introduction

About 90% of the world rice crop is grown and

consumed in Asia, where it provides two-thirds of the

* Corresponding author. Tel.: +94 37 2259881.

E-mail address: rice@sltnet.lk (W.M.W. Weerakoon).� Deceased.

167-8809/$ – see front matter # 2005 Elsevier B.V. All rights reserved

oi:10.1016/j.agee.2004.12.014

calories and more than half of the protein for human

diets. Productivity of modern rice cultivars depends

strongly on N availability (Cassman et al., 1994). If N

does not limit growth (Imai and Murata, 1978;

Williams et al., 1981; Wong, 1979; Kim et al.,

2001, 2003), increased atmospheric CO2 concentra-

tion [CO2] increases photosynthesis and growth of

terrestrial plants (Cure and Acock, 1986; Lawlor and

.

W.M.W. Weerakoon et al. / Agriculture, Ecosystems and Environment 108 (2005) 342–349 343

Mitchell, 1991). The benefits of increased atmospheric

[CO2] are greater for C3 species, such as rice than for

C4 species (Lawlor and Mitchell, 1991; Kimball et al.,

2002), even though N fertilizer use efficiency is

relatively low in irrigated rice because of increased

losses from the rhizosphere (Vlek and Byrnes, 1986).

With increased atmospheric [CO2], the capacity of

soils to supply N may not change, but plant N

requirements would increase. Elevated atmospheric

[CO2] leads to increased dry matter accumulation in

rice (Baker et al., 1992), but a decrease in tissue N

concentration could adversely affect late growth

stages and yield of rice (Makino et al., 1997;

Weerakoon et al., 1999).

Leaf photosynthesis may acclimate to long-term

exposure to high [CO2] (Curtis, 1996; Long et al.,

2004). Long-term exposure of rice to high [CO2]

decreased radiation use efficiency with the decrease in

canopy leaf N (Weerakoon et al., 2000). Photosynth-

esis acclimation to high [CO2] could be partly due to

decrease in Rubisco content in the leaf (Drake et al.,

1997). Acclimation to high CO2 in wheat was

dependent on N supply (Farage et al., 1998).

With improved N management under current

environmental conditions, rate of N uptake by lowland

rice could be as high as 12 kg ha�1 d�1 (Peng and

Cassman, 1998). Fertilizer N in the soil remains

available for less than 14 days after application at

maximum tillering and less than 10 days after

application at panicle primordial initiation (PI) (Peng

and Cassman, 1998). With future increases in atmo-

spheric [CO2], potential N uptake would increase,

which would further deplete soil N. Increased

atmospheric [CO2] leads to increased N uptake by

rice until PI stage (Kim et al., 2001). These results,

however, do not allow us to distinguish whether such

reductions in N uptake observed after PI under

elevated atmospheric [CO2] was because soil N was

limiting, or because the rice plants were unable to take

up the fertilizer N. Little work has been focused on the

partitioning of N within the rice plant and the impact

of increased tillering on rooting and N uptake with

long-term exposure to high [CO2]. We hypothesize

that an increase in atmospheric [CO2] will increase

tillering and rooting capacity of rice and higher N

uptake will deplete soil N more quickly, thus leading

to a higher N fertilizer demand. We hypothesize

further that rice plants will need additional N to

compensate for N dilution in the larger canopy,

especially if plants produce more non-productive

tillers under a higher [CO2] atmosphere.

2. Materials and methods

A field experiment was conducted on rice (Oryza

sativa L.) cv IR 72, during the 1994 dry season at the

lowland research field of the International Rice

Research Institute (IRRI), Los Banos, Philippines

(158N, 1218E). Treatments were factorial combinations

of two [CO2], ambient, and elevated to 700 mmol

mol�1, and three rates of fertilizer N: 0 kg N ha�1 (N0),

90 kg N ha�1 (Nmed), and 200 kg N ha�1 (Nhigh). The

experimental unit was an open-top chamber (OTC),

with a ground area of 3.3 m2. There were three

replications for each treatment. Chamber CO2 control

and the data acquisition were described in Jones et al.

(1995). Each OTC was in a bunded 10 m � 10 m plot,

with the same N fertilization treatments outside and

inside the OTC for each plot.

The soil was an Andaqueptic Haplaquoll puddled

to a depth of 15–20 cm. Initial soil nutrient concen-

tration in the upper 0–15 cm layer was 0.18 � 0.02 mg

N kg�1, 12.0 � 3.2 mg P kg�1, and 8.0 � 0.1 mg

K kg�1. Seedlings were raised at the same [CO2]

into which they would be transplanted. Fields were

drained prior to the transplanting of 14-day-old

seedlings (three per hill), with 20 cm � 20 cm spacing

between hills. After transplanting, floodwater depth

was gradually raised to about 5–7 cm and kept at that

depth throughout the study. Plots were weeded by

hand. Pest and diseases were chemically controlled,

using ingredients, and application rates recommended

by IRRI for a low land rice crop.

Fertilizer N during crop growth was applied based

on the crop requirement measured by the SPAD 502

(soil–plant analysis development, Minolta CO.,

Osaka, Japan) following the method of Peng et al.

(1993). Leaf N was estimated every 6–7 days,

beginning at 21 days after transplanting (DAT). A

minimum SPAD value for treatment, Nhigh, was set at

37. We calculated the amount of N fertilizer needed to

maintain the set SPAD value of Nhigh to have optimum

growth for a 14-day period based on the cumulative

degree-days (CUDD) according to a relationship

developed for IR 72 in a typical dry season at IRRI

W.M.W. Weerakoon et al. / Agriculture, Ecosystems and Environment 108 (2005) 342–349344

ig. 1. Difference in tiller number m�2 (closed symbols) and

anicle number (at harvest, 86 DAT, open symbols) of IR 72 between

igh and ambient CO2 treatments, grown with N0 (*), Nmed (&),

nd Nhigh (~). Error bars represent the S.E. for each sampling day.

(Cassman et al., 1994). Accordingly, fertilizer N was

applied in the form of urea at 0, 24, 37, 42, and 60 DAT

at the rate of 30,15, 25, 0, and 20 kg N ha�1 for Nmed

and 60, 30, 50,20, and 40 kg N ha�1 for Nhigh; 30 kg of

K2O ha�1 in the form of muriate of potash (KCl) and

60 kg of P2O5 ha�1 in the form of triple super

phosphate was incorporated to the soil at 2 days before

transplanting.

Plants were destructively sampled between

8:00 a.m. and 10:00 a.m. at 22, 42, 55, 67, and 77

DAT. At least four hills were sampled each day. Plants

were pulled carefully in order to recover as much of

the root system as possible. Not all of the root system

was recovered by this procedure. However, this

method allows relative, if not absolute, comparisons

among treatments. To minimize effects of sampling on

remaining plants, the spaces occupied by sampled

plants were refilled immediately with plants of similar

size taken from the plot area outside the OTCs, which

had received the same amount of fertilizer, though

they did not have the same atmospheric conditions. At

each sampling date, tiller number was counted and

leaf blade, sheath, and culm, roots, and panicles were

dried for 72 h at 70 8C before weighing. N concentra-

tion of leaf blade, sheath, and culm, roots, and panicles

were determined by the micro-Kjeldahl method.

Fertilizer N recovery by the rice plants grown at

ambient and high [CO2] was calculated using the

amount of fertilizer added, and the total N taken up by

the plants, subtracting the soil N supply, which is the N

taken up at N0.

Two-way analysis of variance was performed using

STATGRAPHICS. Means were compared using the

LSD at P < 0.05.

3. Results

Tiller number increased with increases in both

[CO2] and fertilizer N. The difference in tiller number

between high and ambient [CO2] increased with

increased N at early stages of growth and decreased

towards flowering (Fig. 1). Tiller degradation was

extremely high for both high and ambient [CO2]. The

difference in panicle number between high and

ambient [CO2] was not significant for the Nmed and

Nhigh treatments. Furthermore, N fertilizer influenced

the ratio of aborted tillers to panicle number, and the

F

p

h

a

percentage change did not differ between ambient and

high [CO2]. The percent aborted tillers that is, the

difference between the largest tiller number at 42 DAT

and panicle numbers at harvest was 48.5% for N0,

61.5% for Nmed, and 68% for Nhigh.

Root dry weights followed similar increases with

increased tiller number at both ambient and high

[CO2]. To understand the rooting behavior, we

computed linear regressions between tiller number,

and root weight of rice grown at both ambient and high

[CO2] for different biomass harvest dates. Tiller

number and root dry weight were significantly

correlated, and the relationships were similar for rice

plants grown in ambient and high [CO2]. However, the

relationship differed among harvest dates (Fig. 2). At

22 DAT, the change in tiller number per unit root dry

weight was higher, about 18 tillers g�1 root, and

decreased towards flowering to about 12 tillers g�1

root, while maintaining a linear relationship.

Plant N uptake increased in proportion to the

amount of fertilizer N applied until 42 DAT. The

aboveground N content was significantly greater with

increased atmospheric [CO2] at 22 DAT, but from 42

DAT onward the difference between ambient and high

[CO2] was significant only in the Nhigh treatment

(Fig. 3), a trend that continued until flowering. When

fertilizer N was not supplied, the N uptake by rice

plants grown at high [CO2] was significantly less than

that taken up by plants grown under ambient [CO2] at

67 DAT (Fig. 3), apparently because there was more

death of leaf tissue under high [CO2] and no applied N.

W.M.W. Weerakoon et al. / Agriculture, Ecosystems and Environment 108 (2005) 342–349 345

Fig. 2. Relationship between tiller number and root dry weight of

IR72 rice grown under ambient (open) and high [CO2] (closed) for

N0, Nmed, and Nhigh levels at 22 (*), 42 (&), and 55 DAT (~).

Linear regressions were drawn at 22DAP (Y(22)) and 42 and 55 DAP

(Y(42 and 55)).

Fig. 3. Plant N uptake under ambient (open) and high CO2 (closed)

with N0 (*), Nmed (&), and Nhigh (~). Fertilizer N was applied at 0,

24,37, 42, and 60 DAT at the rate of 30, 15, 25, 0, 20, and 60, 30, 50,

20, and 40 kg N ha�1 for Nmed and Nhigh, respectively. Error bars

represent the S.E. (CO2 � N) for each sampling day.

Fig. 4. Relationship between total N uptake and N content of leaves

and sheaths + culm for IR 72 at different dates after transplanting.

Each data point represents the level of fertilizer N (N0, Nmed, and

Nhigh) average over three replicates at 22 (*), 42 (&), 55 (~), and

67 DAT (^) with ambient (open) and high (closed) CO2 concen-

trations.

Because the allocation of N among leaves, sheaths,

and culms has great implications with regard to C

assimilation, we analyzed the N partitioned at

different days until flowering. The relationship

between the N content of leaves with total plant N

for plants grown at different N supplying environ-

ments was linear for both ambient and high [CO2]

(Fig. 4). However, the rate of partitioning towards

these component parts changed with age of the plant

and the atmospheric [CO2]. The relationship between

N partitioned to sheaths and culms, which is the

difference between total plant N and leaf + root N,

with total plant N was also linear. The potential to

partition N towards leaves at high [CO2], which is the

slope of the regression, was always lower towards

leaves (Fig. 5a), while it was higher towards sheath

and culm (Fig. 5b). Until 55 DAT, potential to partition

N to leaves averaged 67% in the ambient and 58% in

the high [CO2]. At 67 DAT, the priority for N appeared

Table 1

Effects of atmospheric [CO2] on grain weight and grain N concentration at harvest and leaf N concentration and fertilizer N recovery at flowering

with N0, Nmed, and Nhigh fertilizer treatments

Fertilizer N treatment Grain weight (g/hill) Grain N concentration

(g/100 g)

Leaf N at flowering

(g/100 g)

Fertilizer N recovery

at flowering (%)

Ambient High Ambient High Ambient High Ambient High

N0 6.8 a 7.2 a 1.21 a 0.98 b 1.51 a 1.10 b – –

Nmed 10.4 a 14.0 b 1.30 a 1.07 b 1.94 a 1.62 b 45.2 a 64.8 b

Nhigh 11.4 a 13.8 b 1.36 a 1.49 a 2.40 a 2.17 b 41.4 a 56.5 b

Values for a given fertilizer N treatment between ambient and high followed by a common letter are not statistically significant at P < 0.05.

W.M.W. Weerakoon et al. / Agriculture, Ecosystems and Environment 108 (2005) 342–349346

Fig. 5. (a) Relationship between percentage N partitioned to leaves

per unit N uptake vs. days after transplanting of IR 72 grown at

ambient (&) and high atmospheric CO2 (&) environments. Each

data point represents the slope of the linear regression between the N

partitioned to leaves vs. the total N uptake (refer Fig. 4) for

respective sampling dates. Regression coefficients were highly

significant (r2 > 0.98). (b) Relationship between the percentage

N partitioned to sheath and culm per unit N uptake vs. days after

transplanting of IR 72 grown at ambient (&) and high atmospheric

CO2 (&) environments. Each data point represents the slope of the

linear regression between the N partitioned to sheath and culm vs.

the total N uptake (data not shown) for respective sampling dates.

Regression coefficients were highly significant (r2 > 0.98).

to have shifted to the developing spikelets. Allocation

towards sheath and culm peaked near 42 DAT and

decreased thereafter presumably a result of plants

shedding non-productive tillers (Fig. 5b).

Increased N uptake with increased atmospheric

[CO2] during early growth stages increased the

fertilizer N recovery at flowering; however, the N

concentration of leaf blades at flowering decreased

with increased atmospheric [CO2] with greatest

difference in the N0 treatment (27%), followed by

the Nmed (16%) and Nhigh (12%) treatments (Table 1).

A similar trend was observed with grain N concentra-

tion at N0 and Nmed, but atmospheric [CO2] did not

significantly affect grain N content in the Nhigh

treatment. As compared with plants grown under

ambient [CO2], grain weight per hill in the high [CO2]

treatment increased by 5.8% in N0, 14% in Nmed, and

13.8% in Nhigh. Compared with plants grown under

ambient [CO2], high [CO2] significantly increased

fertilizer N recovery in Nmed by 43% and in Nhigh by

36% (Table 1).

4. Discussion

Dry matter accumulation is driven by the inter-

ception of solar radiation and subsequent conversion

of solar energy into biomass, a process that depends on

N supply to the rice crop (Cassman et al., 1994; Kim

et al., 2001; Peng et al., 1999; Weerakoon et al., 2000).

Leaf area does not appear to respond to increase in

atmospheric [CO2] in rice (Ziska and Teramura, 1992;

Ziska et al., 1996)). Therefore, to maximize the

potential production in rice under high [CO2], leaf N

concentration should be increased.

Increased N uptake with increased atmospheric

[CO2] was observed in many species including rice

(Billes et al., 1993; Dijkstra et al., 1999; Kim et al.,

2001). Sheehy et al. (1998) showed that for maximum

yield in an ambient environment, a rice crop should

acquire 14.4 g N m�2 in 35–45 days. Maximum plant

N uptake at 42 DAT in this experiment reached

10.8 � 0.6 g N m�2 in the ambient and 12.0 �0.5 g N m�2 in the high [CO2], which is lower than

that is required for maximum yield. Little additional N

was taken up by the rice plants after 42 DAT even with

higher quantities of fertilizer N. We presume that N

losses from soil through leaching and other means are

similar in both [CO2] environments; thus, soil and

fertilizer N are depleted faster in the high than in the

ambient [CO2]. Therefore, N fertilizer application

frequency or rate or both should be increased for

W.M.W. Weerakoon et al. / Agriculture, Ecosystems and Environment 108 (2005) 342–349 347

plants growing under high atmospheric [CO2] to

maximize the N uptake rate.

When soil N supply diminishes, internal N

recycling could trigger tissue death. In fact, because

of tissue death in the N0 treatment, total plant N under

high [CO2] was less than that of plants under ambient

[CO2]. This suggests that rice plants grown at high

[CO2] are inferior to plants grown under ambient

[CO2], if adequate N is not supplied, as was reflected

by a decrease in canopy assimilation in the N0

treatment near the time of PI (data not shown).

Enhancement of shoot growth in rice, whether

caused by greater atmospheric [CO2] or increased N

supply, is often manifested through formation of more

tillers. The initiation of tillers is independent of [CO2]

or N, but their subsequent growth depends on the

supply of assimilates to growing tillers. With an

increase in supply of assimilates to tillers, tiller number

increased in the high [CO2]. This is consistent with the

other studies by Kim et al. (2001), Imai et al. (1985),

Jitla et al. (1997), and Baker et al. (1996). However, this

large increase in tiller number with increased [CO2] is

not reflected in an increase in panicle numbers

suggesting that many of the tillers are not productive.

Tillers and roots emerge from the same node at the

same time (Yoshida, 1981). The initial increase in tiller

number resulted in a robust root system. The linear

relationship between tiller number and root dry weight

suggest that increased tillering leads to the formation of

new roots; thus, increase root biomass was an indirect

effect of increased atmospheric [CO2]. In other words,

if higher atmospheric [CO2] did not increase tiller

numbers, it would not increase root weight or N uptake.

Therefore, varieties, which are less tillering may be less

sensitive to increased atmospheric [CO2]. This could be

a reason for the intraspecific variability among cultivars

to prolong exposure to high [CO2] (Moya et al., 1998;

Baker, 2004). Thus, non-productive tillers may be

beneficial to rice plants under high [CO2] through

increased N uptake.

From 22 to 42 DAT root mass per tiller increased

suggesting a greater capacity for nutrient absorption,

but N uptake reached a plateau after 42 DAT, despite

repeated application of N fertilizer. Diminished soil N

supply could explain this scenario in the N0 treatment

and to a certain extent in the Nmed but not with Nhigh.

The decrease in uptake of N at later stages could result

from tissue death associated with degeneration of

tillers. Tiller degeneration was greater in the high than

ambient [CO2] treatment; thus, loss of N also could be

high. Decay of non-productive tillers increased root

mass per tiller, even if many of these roots had limited

or no nutrient uptake capacity. However, in the

ambient [CO2] atmosphere, plants produced fewer

tillers with less roots than in the high [CO2], which

may have allowed a slower but longer period of N

uptake with slower depletion of soil N. This suggest

that perhaps the magnitude of increase in root dry

weight before PI by IR72 in the high [CO2] of this

experiment was much larger than that is needed for its

maximum efficiency.

Leaves are the strongest sinks for both N and

carbon. As linear regressions were computed using all

N supplying environments, that is, N limited, N

sufficient, and N surplus conditions, the slope of each

regression line represents the potential of rice plants to

allocate N to leaves or sheaths and culms per unit N

taken up at different stages of growth at ambient and

high [CO2]. The linear relationship suggest that

irrespective of the N supply level, partitioning to

leaves during vegetative stage is disturbed only by the

growing atmospheric [CO2], and it is always a

constant fraction of absorbed N. Partitioning potential

of N towards leaves in the high [CO2] atmosphere was

always less (58%) than that under ambient [CO2], i.e.,

67%, suggesting that the priority for N allocation to

leaves decreased with increased [CO2]. This is

consistent with the findings by Makino et al. (1997)

and Nakano et al. (1997). Due to acclimation, rubisco

content in leaves decreased with the prolonged

exposure to high [CO2] (Rowland-Bamford et al.,

1991; Farage et al., 1998). Therefore, the reduction in

N partitioning potential to leaves with prolonged

exposure to high [CO2] may have resulted in reduction

of rubisco content. Since the partitioning of N to

leaves is a function of N uptake, the acclimation to

high [CO2] could be partly dependent on the N uptake

of the rice plant.

The observed change in N allocation pattern with

increased atmospheric [CO2] could simply be a result

of the increase in tiller number before PI, which

increased partitioning towards sheath and culm. If the

rate of tillering were limited under high [CO2] with a

resulting increase in the duration of tillering, the crop

would produce new roots, extend N uptake, and

maintain leaf N and canopy C assimilation capacity.

W.M.W. Weerakoon et al. / Agriculture, Ecosystems and Environment 108 (2005) 342–349348

Thus, cultivars with moderate non-productive tillers

but with a better root system are essential to maximize

canopy efficiency in future high [CO2] environments.

The increase in grain weight with the CO2

fertilization at Nmed and Nhigh but not in N0 could

be due to decrease in canopy C assimilation with

decreased canopy leaf N concentration at high [CO2],

N0 environment. More importantly, in the high [CO2]

even with increased uptake and fertilizer N recovery,

grain N concentration decreased in the N0 and Nmed

treatments. These results suggest that if N fertilizer is

limited, grain N concentration would decrease; thus,

higher dosages of fertilizer N at later growth stages are

needed under high CO2 environments. Therefore,

moderate fertilizer N at vegetative stage and higher

dosage towards reproductive stages may result in

increased grain yield and grain N concentration under

high [CO2] environments.

5. Conclusions

Increased atmospheric [CO2] would change N

uptake pattern and partitioning of N within the rice

plant. The increase in N uptake at elevated [CO2] was

mainly due to the increase in root mass associated with

increased tillering during early stage of crop growth. If

tillering was reduced, the uptake of nutrients would

also decrease in the high [CO2] atmosphere. Thus, the

positive response of rice to increased atmospheric

[CO2] is primarily manifested through increased

tillering. This should be considered in future rice

crop improvement programs, as the tendency in the

breeding programs is to reduce unproductive tillering.

With prolonged exposure to high [CO2], N partition-

ing potential towards leaves decreased by 9%.

However, the difference in N uptake and leaf N

concentrations with the change in soil N supplying

environment suggest that the reduction in partitioning

of N towards leaves, partly due to acclimation of rice

to prolong exposure to high [CO2], could be partly

corrected with proper management of fertilizer N.

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