- Email: [email protected]
Leaf nitrogen distribution to maximize the canopy photosynthesis in rice
Field Crops Research 95 (2006) 291–304 www.elsevier.com/locate/fcr
Leaf nitrogen distribution to maximize the canopy photosynthesis in rice Hiroyuki Shiratsuchi *, Tohru Yamagishi, Ryuichi Ishii 1 Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1 Yayoi, Bunkyoku, Tokyo 113-8657, Japan Received 13 January 2005; received in revised form 1 April 2005
Abstract The optimum distribution of leaf nitrogen (N) in the canopy of rice plants (Oryza sativa L.) for maximum daily canopy photosynthesis (DCP) and the optimization effects on DCP were estimated during the grain filling period. The low- and highdensity canopies (28.3 and 47.5 plants m2) and isolated plants were established at heading using plants in pots grown up at the low density until heading to make the same canopy architecture except plant density and the same leaf N distribution at the start of treatment among the two canopies and the isolated plants. The simulation was conducted under two conditions of the upper limit of leaf N. Under condition 1, upper limit of leaf N content was 1.80 g m2. Under condition 2, upper limits were measured leaf N content in each leaf position at heading. The model indicates that if leaf N content in the upper leaves can be increased with reduction of N in the lower leaves, DCP will increase in any of the plant density, light conditions and under conditions 1 and 2. On a clear day, the estimated increase in DCP was 19–45 and 38–70% in the low- and high-density canopies under condition 1, respectively. Even under condition 2, which is more realistic than condition 1, the increase was up to 21 and 25% in the low- and high-density canopies. These estimates obtained by the present model that incorporates the shading effects of panicles and stems on DCP were higher than the previous reports which did not consider the effects of shading by panicles and stems. In the observed leaf N distribution, the higher the plant density was, the steeper the gradient of the leaf N remained. The gradient in the high-density canopy was closer to that of the predicted optimum leaf N distribution, and likely to contribute to maintaining higher DCP in the canopies. Compared with the hypothetical case in which gradient of leaf N distribution would be more gentle as observed in the isolated plants, the maintained steeper gradient of observed leaf N content in the canopies was estimated to increase DCP by 13 and 5% in the high- and low-density canopy, respectively. # 2005 Elsevier B.V. All rights reserved. Keywords: Canopy photosynthesis; Nitrogen distribution; Optimization; Plant density; Rice
* Corresponding author at: National Agricultural Research Center, National Agriculture and Bio-Oriented Research Organization, Kanto-Tokai Farming System 3-1-1, Tsukuba, Ibaraki 305-8666, Japan. Tel.: +81 29 838 8822; fax: +81 29 838 7038. E-mail address: [email protected] (H. Shiratsuchi). 1 Present address. College of Bioresource Sciences, Nihon University, Fujisawa, Kanagawa 252-8510, Japan.
1. Introduction The light-saturated photosynthetic rate is positively correlated with leaf nitrogen content in many crop species (Yoshida and Coronel, 1976; Uchida et al., 1982; Makino et al., 1988; Peng et al., 1995), and
0378-4290/$ – see front matter # 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.fcr.2005.04.005
292
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
decreases with a decrease of leaf N resulting from remobilization of N to other parts of the plant (Sinclair and de Wit, 1975; Penning de Vries et al., 1988; Sadras et al., 1993; Boote and Tollenaar, 1994). In rice plants, leaf N is remobilized to the grains during the grain filling period along with actively produced photosynthates. That is, there is a compromise between the supply of N and photoasimilates from leaves to the grains during grain filling such that enough N must remain in leaves to allow photosynthesis to continue, yet enough N must be transported to the grains to allow normal grain development and storage of adequate reserves. Studies of leaf N distribution on canopy photosynthesis through the improvement of light use efficiency suggest that there is an optimum distribution for maximizing canopy photosynthesis that could increase net canopy photosynthesis (Field, 1983; Hirose and Werger, 1987b; Pons et al., 1989; Schieving et al., 1992; Evans, 1993; Anten et al., 1995; Connor et al., 1995; Gimenez et al., 1994). Anten et al. (1995) reported that optimization of leaf N distribution in rice plants increases daily canopy photosynthesis (DCP) by 9% during the time before heading. However, there are no reports on the effects of optimized leaf N during the grain filling period in rice, when more than 60% of grain dry matter is usually produced (Thorne, 1966; Cock and Yoshida, 1972; Murata and Matsushima, 1975). During the grain filling period in rice, leaves are shaded by the panicles (Setter et al., 1995) resulting in an increase of the canopy extinction coefficient (Saitoh et al., 1990). Anten et al. (1995) also showed that when the light extinction coefficient is high because of high light intercepting efficiency, the effects of leaf N optimization on daily canopy photosynthesis become large. Therefore, if the shading effects of panicles and stems on DCP are not taken into account, the effects of optimization of leaf N distribution on DCP will be underestimated. The previous studies, which did not consider the shading effects of any parts other than leaves, showed DCP increase by the optimization were only 0–17% (Field, 1983; Hirose and Werger, 1987b; Pons et al., 1989; Schieving et al., 1992; Gimenez et al., 1994; Anten et al., 1995; Connor et al., 1995). The purpose of the present study is to elucidate (1) the effects of optimizing leaf N distribution in the rice plant canopy on DCP during grain filling, when
incident light was absorbed by panicles and stems as well as leaves; (2) response of leaf N distribution to plant density; and (3) the effects of the response on DCP.
2. Materials and methods 2.1. Plant material Seeds of rice plants (Oryza sativa L. cv. Musashikogane) were sown on nursery beds in the field of the Faculty of Agriculture of The University of Tokyo. After 40 days three seedlings each were transplanted to 0.05 m2 pots, which were arranged in a rectangle at a density of 28.3 plants m2. Fertilizer was applied at the rate of 1.2 g pot1 N, 1.8 g pot1 P2O5, and 1.8 g pot1 K2O. At minus 13 days after heading (DAH), two pots were isolated and fertilized with 0.75 g pot1 of N in the form of ammonium sulfate (3 N) to widen the range of leaf N content for determination of the leaf CO2 exchange parameters. The other pots were fertilized with 0.25 g pot1 at the same day (13 DAH). Using these pots, high- and low-density canopies (47.5 and 28.3 plants m2) and isolated plants were established at 0 DAH. The leaf area index (LAI) was 6.7 in the high-density canopy and 4.0 in the low-density canopy at heading. LAI remained essentially constant up to at least 21 DAH. 2.2. Measurement of leaf CO2 exchange rate Light-photosynthesis curves were determined by a gas-exchange measuring system with an infrared gas analyzer (ZAP, Fuji Electric Co. Ltd., Tokyo) on the first, third and fifth leaves counted from the top on main stems, which were illuminated by metal halide lamps (DR400/T (L) Toshiba, Tokyo) at 0, 11 and 21 DAH. For 3 N plants, the measurement was conducted on the first leaf at 10 DAH. All the measurements were done for four replications. 2.3. Measurement of canopy CO2 exchange rate Canopy photosynthesis was measured with a closed measurement system in a low-density canopy to make sure that the model of canopy photosynthesis fits the actual values. Nine plants in three pots were covered
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
293
with an equilateral prism acrylic chamber (0.29 m2 triangular base 1.15 m height) at 0, 1, 5, 7, 19 and 20 DAH.
partial organ area index of organ j in inclination angle ui and layer n, F nji, was obtained by summing the area for each organ and each inclination angle class.
2.4. Nitrogen measurements
2.6. Development of a canopy photosynthesis model
Leaves of the same four plants as leaf CO2 exchange measurement and of the four isolated plants were separated into individual leaves used for CO2 exchange measurement and seven leaf positions, dried at 80 8C at least 3 days, and weighed. The dry leaf samples were ground, and N content was determined by micro Kjeldahl method (Bremner and Mulvaney, 1982).
The model of canopy photosynthesis was developed with two submodels. Submodel 1, expressed by the following equation, gives the light response curve of leaf photosynthesis as a function of leaf N content (Hirose and Werger, 1987b). P¼
2.5. Canopy structure measurements Canopy structure was determined according to the modified tracing method (Ito, 1969). Six plants were selected from each of two different canopies in terms of plant density, at 0, 11–13, and 21–23 DAH. The heights of the tip and base of leaf blades and panicles, and the height of the inflection point, if the leaf is bent, were determined. The lengths and widths of leaf blades, stems, and panicles were measured. Leaf blade width was determined every 10 cm from the base to the tip along the length of the leaf. Each stem was considered to consist of frustums. Each panicle was considered as one or two cylinders, depending on bending. For every leaf blade, stem, and panicle, the area and the inclination angle in each horizontal layer were calculated by the architecture data in 1 cm increments obtained with tracing method. Azimuth angles of the organs were assumed to distribute uniformly. The
QY L þ Pm ððQY L þ Pm Þ2 4C QY L Pm Þ1=2 2C (1)
where P is gross photosynthesis (g m2 h1); C is convexity (0 < C 1); QY is apparent quantum yield (g s h1 mmol1); L is photosynthetic photon flux density (PPFD) (mmol m2 s1); Pm isgross photosynthesis under saturating irradiance (g m2 h1). C was constant at 0.868, determined by the least squares method with the observed Pm and QY. Pm, QY, and respiration (R) were fitted to a linear regression equation of leaf N content, also by the least squares method (Table 1). Submodel 2 is for the determination of irradiance on the leaves from canopy structure and incident light. Incident irradiance was set at 2000, 1000 and 500 mmol m2 h1 on a plane perpendicular to the sun and the proportion of diffuse light in total irradiance was set at 0.400, 0.825 and 0.944, corresponding to a clear, cloudy and overcast day, respectively.
Table 1 Regression analysis of CO2 exchange parameters to leaf N content: Pm, light-saturated gross photosynthesis; QY, apparent quantum yield; R, dark respiration; C, convexity of light-photosynthesis curve fitted to a non-rectangular hyperbola (Eq. (1)) Pm (g m2 h1)
QY (g s h1 mmol1)
R (g m2 h1)
C
a
A Ba r d.f.
3.460 1.111 0.92** 54
0.00478 0.0029 0.50** 54
0.0806 0.039 0.38** 54
0.0044 0.079 (0.868b) 0.04 54
F d.f.
287.8** 1:53
17.7** 1:53
9.4 ** 1:53
a b c
Totalc
362.8** 5:340
A and B are parameters of following regression equation; Y = A (N content (g m2)) + B, where Y is each CO2 exchange parameter. The constant obtained by least squares method with measured Pm and QY for all samples was used for C value. F-test of regression of non-rectangular hyperbola: submodel 1, for which is substituted regression equations of Pm, QY and C (0.868).
294
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
Photosynthesis in each leaf position is calculated by the light-photosynthesis curve (Eq. (1)) in submodel 1 and irradiance distribution on the leaf in submodel 2. Then, the DCP is calculated by the integration of leaf photosynthesis in each position and summation of leaf positions through a day: Z 24 H0 X X X DCP ¼ LFnLC ji PLC j dH p 0 n j i XXX 24 Fn ji R j (2) n
j
i
H0 ¼ arccosðtan a tan bÞ
(3)
where a is latitude, b is declination angle, LFnLCji is partial leaf area index in leaf position j with inclination angle ui and irradiance class on the leaf surface LC in layer n, PLCj is gross photosynthesis of leaf position j in irradiance class LC, Rj is respiration of leaf position j, H is an hour angle and H0 is the hour angle at sunset when H = 0 at noon. The CO2 exchange of stems and panicles was not considered, because it would be independent of leaf N distribution. For further details see Appendix A. Optimum leaf N distribution is defined as the distribution that maximizes DCP and is determined numerically with a fixed total leaf N amount in the model under conditions 1 and 2. Condition 1 is that the upper limit was 1.80 g m2, where the relationship between leaf N content and light-saturated photosynthesis is almost linear (Ishihara et al., 1979; Makino et al., 1988; Peng et al., 1995). Condition 2 is that the upper limits were the measured values in each leaf position at 0 DAH. Condition 2 is more realistic than condition 1. Under both conditions, the lower limit of leaf N content was the measured value of dead leaves (0.18 g m2), because dead leaves were supposed to have remobilized leaf N already and not to remobilize N any more.
3. Results 3.1. Verification of the model The estimated net canopy photosynthesis produced by the model was close to the measured values regardless of light conditions (r = 0.936***, n = 25,
Fig. 1. Observed and estimated net canopy photosynthesis in lowdensity canopies under the clear, cloudy, and overcast days. Estimated photosynthesis = 0.693*** observed ptotosynthesis + 0.583*** and RMSE = 0.2898.
Fig. 1). Only when the measured values were more than 2.5 g m2 h1 on 5 or 7 DAH, did the theoretical values tend to be lower than the measured values. 3.2. Irradiance on leaves Average irradiance on leaves on the clear day decreased steeply from higher to lower leaf positions (Fig. 2A). Irradiance at all leaf positions was higher in the low-density canopy than in the high-density canopy and decreased during grain filling in both canopies. Relative irradiance on the leaves at or lower than the third leaf was always higher in the lowdensity canopy than in the high-density canopy (Fig. 2B), indicating that the gradient of irradiance was less in the low-density canopy than in the highdensity canopy. 3.3. Leaf N distribution Leaf N content was 1.19 g m2 in the first leaf and 0.53 g m2 in the sixth leaf at heading (Fig. 3). Leaf N content decreased with leaf position down the stem, except in the seventh leaf. Leaf N content declined more in the upper leaves than in the lower leaves, especially in the isolated plants after heading. The leaf N content across leaf positions was maintained at a steeper gradient in the higher density canopy than in the lower density canopy (isolated: 0.45–0.64 g m2,
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
Fig. 2. Estimated photosynthetic photon flux density (PPFD) on leaves in each leaf position during daytime under the clear days (A) and relative irradiance to first leaf position (B) in high- and lowdensity canopies.
low density: 0.43–0.80 g m2, high density: 0.48– 0.98 g m2 at 21 DAH). This was because the decline in leaf N content in the upper leaves was slower at the higher density (Fig. 3). 3.4. Optimum leaf N distribution The optimum leaf N distribution on the clear day and under condition 1 resulted in a much larger gradient than the observed one (Fig. 3); leaf N content in the upper position was close to the upper limit (1.80 g m2) and that in the lower position was close to the lower limit (0.18 g m2). The optimum leaf N distribution was not different between low and high plant densities. To attain optimum N distribution, N must be remobilized from the lower leaves and leaf N
295
Fig. 3. Leaf N distribution among different leaf positions in highand low-density canopies and isolated plants under the observed and optimum (condition 1) leaf N distributions. Error bars show the standard deviation of the observed leaf N content.
content in the upper leaf positions must be maintained at a high level throughout the grain filling period. The optimum distribution at heading under condition 1 differed little between the clear and overcast day, although the gradient of leaf N content seemed to be less on the overcast than on the clear day (Fig. 4). The gradient calculated under the overcast day conditions in optimum leaf N distribution was less steep in the low-density canopy than in the high-density canopy. In the optimum distribution under condition 2, leaf N content in the upper position remained at the upper limit (leaf N content at 0 DAH in each leaf position) and decreased to the lower limit from the bottom to the top (data not shown).
296
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
response of leaf N distribution to the gradient of irradiance on DCP. Isolated-type N distribution is defined as a profile of leaf N distribution in the isolated plants (Fig. 3). The function of leaf nitrogen content of leaf position j in the isolated plants at time t in Fig. 3 is defined as NC0iso j ðtÞ. Leaf N content of leaf position j in isolated-type N distribution for any canopy, at time t, NCisoj(t) is as follows: NCiso j ðtÞ ¼ NC0iso j ðt0 Þ Fig. 4. Optimum leaf N distribution under condition 1 in the highand low-density canopies under clear, cloudy, and overcast conditions at heading.
8X XX > NCiso j ðtÞ Fn ji > < n j i XX Nleaf ðtÞ ¼ X > NC0iso j ðt0 Þ Fn ji > : j
3.5. Effects of optimization of leaf N distribution on DCP Optimization of leaf N distribution increased DCP by 19% (from 30.6 to 36.3 g m2 day1) in the lowdensity canopy at heading under the clear day regimen and condition 1 and by 38% (from 28.5 to 39.3 g m2 day1) in the high-density canopy (Table 2). During grain filling, as the leaves aged, DCP in the measured leaf N distribution decreased in both canopies. However, DCP increased by optimization up to 45% in the low-density canopy and 70% in the high-density canopy. Effects of optimization were always smaller in the low-density canopy than in the high-density canopy. Optimization increased DCP regardless of light conditions (clear, cloudy, or overcast), though the increase in DCP was less under the lower irradiance conditions. Optimization increased DCP by 19–21% in the low-density canopy and by 20–25% in the high-density canopy under clear day parameters and condition 2, where the upper limit of leaf N content was set at the values measured at 0 DAH for each leaf position. The increasing rate was always less under condition 2 than under condition 1. 3.6. Effects of the response of leaf N distribution to plant density DCP from the observed N distribution was compared with DCP from the hypothetical isolatedtype N distribution, which is attributed mainly to leaf age gradient and minimally to the gradient of irradiance on leaves, to elucidate the effects of
(4)
n
(5)
i
where t0 is a function of t and makes Eq. (5) true, and, Nleaf(t) is the total amount of leaf N in the objective canopy at time t. Substituting t0 to the right side of Eq. (4), leaf N content in the isolated-type distribution, NCisoj(t) is obtained. On the clear day, DCP under the observed leaf N distribution was 5% higher than under the isolatedtype distribution at 11 and 21 DAH in the low-density canopy, and was 8 and 13% higher at 11 and 21 DAH, respectively, in the high-density canopy (Table 2). DCP under the observed N distribution was higher than under the isolated-type N distribution regardless of light conditions, though there was less of an increase of DCP with a decrease of irradiance.
4. Discussion 4.1. Optimum and observed leaf N distribution The gradient of leaf N content among the leaves under optimum leaf N distribution was larger than under the observed distribution (Fig. 3) as reported previously (Field, 1983; Hirose and Werger, 1987b; Pons et al., 1989; Schieving et al., 1992; Evans, 1993) and particularly in fertilized canopies with a large LAI (Gimenez et al., 1994; Anten et al., 1995). In conditions of optimum leaf N distribution, leaf N content remobilized from the lower leaves during grain filling in both the high- and low-density canopies (Fig. 3). In contrast, in the observed distribution, leaf N content decreased more in the upper leaves than in the lower leaves and, consequently, the gradient of leaf
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
297
Table 2 Daily canopy photosynthesis (DCP) in rice with the different leaf N distribution on the clear, cloudy and overcast days Weather
Clear
Cloudy
Overcast
Density
N distribution
0 DAH
11 DAH
21 DAH
DCP (g m2 d1)
Ratio
DCP (g m2 d1)
Ratio
DCP (g m2 d1)
Ratio
Low
Observed Optimum 1a Optimum 2b Isolated
30.6 36.3 30.6 30.6
1.00 1.19 1.00 1.00
17.3 25.0 20.6 16.4
1.00 1.45 1.19 0.95
15.4 22.1 18.6 14.6
1.00 1.44 1.21 0.95
High
Observed Optimum 1 Optimum 2 Isolated
28.5 39.3 28.5 28.5
1.00 1.38 1.00 1.00
17.3 29.2 20.7 16.0
1.00 1.69 1.20 0.92
12.4 21.1 15.5 11.0
1.00 1.70 1.25 0.89
Low
Observed Optimum 1 Optimum 2 Isolated
23.8 27.4 23.8 23.8
1.00 1.15 1.00 1.00
14.0 18.9 16.1 13.2
1.00 1.35 1.15 0.94
12.9 16.2 14.8 12.1
1.00 1.26 1.15 0.94
High
Observed Optimum 1 Optimum 2 Isolated
19.0 25.8 19.0 19.0
1.00 1.36 1.00 1.00
11.9 19.8 14.1 10.8
1.00 1.66 1.18 0.91
8.7 14.3 10.8 7.6
1.00 1.64 1.24 0.87
Low
Observed Optimum 1 Optimum 2 Isolated
9.6 11.8 9.6 9.6
1.00 1.23 1.00 1.00
5.1 7.7 6.3 4.6
1.00 1.51 1.24 0.90
4.8 6.3 5.8 4.3
1.00 1.31 1.21 0.90
High
Observed Optimum 1 Optimum 2 Isolated
2.9 6.6 2.9 2.9
1.00 2.28 1.00 1.00
0.8 5.1 1.9 0.1
1.00 6.38 2.38 0.13
0.1 2.9 1.1 0.6
– – – –
Optimum 1 is the optimum N distribution under condition 1 in which lower and upper limits of leaf N content are 0.18 and 1.80 g m2. Optimum 2 is the optimum N distribution under condition 2 in which lower limit of leaf N content is 0.18 g m2 and the upper limits in each leaf position are the measured values in the leaf positions at 0 DAH. a
b
N content decreased. A similar decrease in the gradient was reported in sunflower (Sadras et al., 1993; Connor et al., 1995). In contrast, the gradient of leaf N increased during grain filling in rice grown by hydroponics (Hasegawa, 1999). In this hydroponic culture, continuous N application during grain filling could affect the gradient by making nitrogen readily available for uptake to the canopy, whereas N usually diminishes in soil culture. The decrease in the leaf N gradient was affected by plant density (Fig. 3). That is, a steep gradient was maintained in the high-density canopy during grain filling, while the gradient became much shallower in the isolated plants. The optimum leaf N distribution did not differ between light conditions (Fig. 4), as reported previously (Hirose and Werger, 1987b; Pons et al.,
1989). Connor et al. (1995), however, showed that the gradient of leaf N content under optimum distribution conditions increased as incident light decreased. The contradiction between Connor et al. (1995) and the present study apparently results from lower maximum leaf N content (1.8 g m2) in the present study than the highest leaf N content (3.5 g m2) in optimum leaf N profiles for sunflower in Connor et al. (1995). In summary, leaf N distribution was more similar to the optimum distribution in the high-density canopy than in the low-density canopy regardless of light conditions. 4.2. Response of leaf N distribution to irradiance We have shown for the first time under canopy conditions, that a steeper leaf N gradient resulted from
298
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
a steeper gradient of irradiance, by excluding the effects of leaf age (Figs. 2 and 3). The effects of leaf age were excluded by comparing the high- and lowdensity canopies and the isolated plants which consisted of the plants which were grown up in the same canopy until 0 DAH and therefore had the same leaf age distribution and the similar plant architecture. Light distribution in a canopy (DeJong and Doyle, 1985; Hirose et al., 1988; Evans, 1989; Lemaire et al., 1991; Schieving et al., 1992; Pons et al., 1993; Sadras et al., 1993; Anten et al., 1998; Drouet and Bonhomme, 1999) and at least partially leaf age (Mooney et al., 1981; Field, 1983; Hirose et al., 1989; Anten et al., 1998) have been considered as the factors responsible for the gradient of leaf N. However, it has been difficult to distinguish between the effects of the gradient of irradiance and those of leaf age, since a gradient of irradiance is usually accompanied by a gradient of leaf age in the canopy. Hikosaka et al. (1994) has successfully distinguished between these variables by excluding mutual shading and clearly showed that both the irradiance gradient and leaf age can result in a gradient of leaf N. However, there are no similar studies in which canopy effects were considered. 4.3. Factors making the observed gradient of leaf N less than the optimum In the high- and low-density canopies and, especially, isolated plants, leaf N content declined more rapidly in the upper leaves with high N content than the lower leaves with low N content (Fig. 3). It has been proposed that during grain filling in sunflower, a N-priority strategy in which a higher priority for N than C made the upper leaves the source of N rather than of C (Sadras et al., 1993), and a position-dependent mechanism remobilizes more N from leaves close to the grains (Sadras et al., 1993). While not contradicted by the present results, further studies are required to confirm these hypotheses. Growing grains obtain N from leaves during grain filling, causing leaf N content to decline (Sadras et al., 1993). Grain demand also affected leaf senescence in soybean (Noode´n and Guiame´t, 1989). These results suggest that remobilization of leaf N to grains might affect the aging of the leaves and decrease the gradient of leaf N in the present study.
Terashima and Hikosaka (1995) reviewed five reasons that observed leaf N distribution differs from the optimum: limited acclimation to the light environment, an upper limit to photosynthetic components in a leaf, cost of N redistribution, preferential herbivory of leaves of high N content, and neglect of direct sunlight. The first four factors are mainly for vegetative canopies and are not applicable to rice during grain filling in the present study. Direct sunlight is factored into the present study, therefore none of the five previously considered factors can account for the decline of the gradient of leaf N in the present study. The mechanism decreasing the gradient of leaf N during grain filling remains to be elucidated. 4.4. Increase of DCP by the optimization of leaf N distribution We showed for the first time that DCP was 19–45% higher in the low-density canopy and 38–70% higher in the high-density canopy in the optimum leaf N distribution than in the observed distribution on the clear day during grain filling (Table 2). Although essential to crop yield, there has been only one optimization study during grain filling (Connor et al., 1995). DCP increased with the N optimization even under overcast conditions in the present study. In contrast, an increase of N content in the canopy seemed to decrease DCP under overcast conditions, possibly because of increased respiration, while it might increase DCP on clear days (cf. Hirose and Werger, 1987a). DCP increase by the optimization of leaf N distribution was larger in the present study (condition 1, Table 2) than the 0–17% that has previously been reported (Field, 1983; Hirose and Werger, 1987b; Pons et al., 1989; Schieving et al., 1992; Gimenez et al., 1994; Anten et al., 1995; Connor et al., 1995). DCP increases by the optimization of leaf N distribution were larger than in the previous reports for three apparent reasons including, most significantly, the shading effects of panicles and stems. Shading effects of the inflorescence have been reported in rice (Saitoh et al., 1990; Setter et al., 1995) and other crops (Dreccer et al., 1998). The shading effects of plant parts other than leaves increase the apparent extinction coefficient, since the apparent amount of absorbed light by leaves in a leaf layer is the sum of absorbed
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
light by the leaves, panicles, and stems. When the extinction coefficient was large, which increased the gradient of irradiance on the leaves, the effects of optimization of leaf N distribution were large (Anten et al., 1995). A second reason is the relatively large LAI (4.0 and 6.7) compared to previous reports. A large LAI increases the effects of optimization of leaf N distribution on DCP (Hirose and Werger, 1987b; Schieving et al., 1992). Finally, this study was limited to the period of grain filling, rather than pre-senescence, which may accentuate differences in the average leaf N content, which was relatively low (0.61–0.84 g m2) compared to previous reports (1.33 g m2: Hirose and Werger, 1987b; 0.51 g m2: Pons et al., 1989; 0.90– 1.37 g m2: Schieving et al., 1992; 1.15–1.59 g m2 for C3 species: Anten et al., 1995). When canopy leaf N content was low, leaf N distribution had a larger effect on radiation use efficiency than in the high leaf N canopy (Dreccer et al., 1998). The optimization of leaf N distribution greatly increases DCP during grain filling in rice, when the shading effects of panicles and stems are considered. The optimization of leaf N distribution under condition 2 and clear daylight also increased DCP by 19–21% in the low-density canopy and 20–25% in the high-density canopy (Table 2). This result indicates that DCP during grain filling in rice would increase when leaf N is remobilized from the lower leaves in the order of leaf position, since leaf N content decreased in the same way from the lower leaves in the optimum leaf N distribution under condition 2, where the maximum leaf N contents in each leaf position are set to those at heading (data not shown). Therefore, if the remobilization sequence can be changed genetically or chemically, DCP could increase substantially.
299
to the irradiance gradient increased DCP up to 13%. This result indicates that leaf N distribution changes in response to the gradient of irradiance on leaves during grain filling in rice so that DCP increases. Enhancement of this response would make leaf N distribution nearer to the optimum and, consequently, could increase DCP.
5. Conclusion During grain filling in rice, the higher the plant density was, the steeper the gradient of leaf N content across leaf positions remained. As a result of this observed leaf N response to plant density, DCP was estimated to be higher under the observed leaf N distribution than under the isolated-type leaf N distribution by the model in the present study. However, even in the high-density canopy, the gradient was still less than in the optimum distribution. The model showed that DCP would increase by optimization of leaf N distribution, especially in the high-density canopy. The estimated increase in DCP was higher than previously reported, because the shading effects of the panicles and stems were considered in the present study.
Acknowledgements We thank Dr. Kazuhiko Kobayashi for reviewing the manuscript and Dr. Toshihiro Hasegawa for his helpful advice. We are also grateful to Dr. Kouichi Futakuchi for his useful suggestions on experimental design and to Mr. Hirokuni Someya for his assistance.
Appendix A. Details of submodel 2 4.5. Increase of DCP by the effects of the irradiance gradient on leaf N distribution On the clear day, DCP was up to 13% higher under the observed leaf N distribution than under the isolated-type distribution in the high-density canopy, and 5% higher in the low-density canopy (Table 2). The isolated-type N distribution is attributed mainly to the leaf age gradient and minimally to the irradiance gradient. Therefore, the response of leaf N distribution
Submodel 2 determines the irradiance on leaves from a canopy structure and incident light environment. The first step is to calculate the irradiance on the horizon of each layer in the canopy by a modified method by Udagawa et al. (1974). The modifications are: (1) panicles and stems as well as leaves intercept light; (2) diffuse light is assumed as a set of straight lights to any of six inclination angle classes. Sun altitude is calculated according to Loomis and Connor (1992).
300
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
An extinction coefficient of a leaf averaged across azimuth angle a, Kl is obtained according to Monsi and Saeki (1953). An extinction coefficient of a panicle and stem (Kps) averaged across a is as follows: Rp jsinðl; sps Þj da Rp Kps ¼ 0 (A.1) sin f 0 da where (l, sps) is an angle between light direction unit vector l and an organ (panicle or stem) axis unit vector sps and f is the light inclination angle. An averaged extinction coefficient in the layer n, Kn was obtained by a weighted average of Kl and Kps in layer n (cf. Kuroiwa and Monsi, 1963). Irradiance on sunlit and shade areas on the leaf surface is calculated separately (cf. Udagawa et al., 1974). Partial sunlit leaf area index of leaf position j with inclination angle ui in layer n, F snji, is obtained according to Horie (1966). Partial shade leaf area index, F dnji, is obtained as follows: Fdn ji ¼ Fn ji Fsn ji
2. Calculating downward diffuse irradiance on plane n from the uppermost layer to the ground. On the assumption that diffuse irradiance is distributed uniformly over plane n, a downward diffuse irradiance component with inclination angle f without secondary diffuse irradiance scattered in layer n for the first calculation, L0ddn;1 (f), is obtained in the same way for direct sun light: L0ddn;1 ðfÞ ¼ Lddnþ1;1 ðfÞeKn Fn
where Lddn+1,1(f) is the downward diffuse irradiance component with an inclination angle f including secondary diffuse irradiance scattered above layer n for the first calculation. Then, downward diffuse irradiance without secondary diffuse irradiance scattered in layer n for the first calculation, L0ddn;1 , is obtained by integration of L0ddn;1 (f).
(A.2)
Irradiance in a sunlit area is the sum of irradiance of direct sun light, Ls, downward diffuse irradiance, Lddn, and upward diffuse irradiance, Ldun. In a shade area, the irradiance is Lddn + LdunLddn consists of downward diffuse irradiance components with an inclination angle f, Lddn(f). Z p=2 Lddn ¼ 2p cos f sin fLddn ðfÞ df (A.3) 0
(A.6)
L0ddn;1
¼
Z
p=2
2p cos f sin fL0ddn;1 ðfÞ df
0
(A.7)
In the same way, downward diffuse irradiance with secondary diffuse irradiance scattered in layer n + 1 for the first calculation, Lddn+1,1, is obtained. Lddnþ1;1 ¼
Z
p=2
2p cos f sin fLddnþ1;1 ðfÞ df
(A.8)
0
Ldun consists of upward diffuse irradiance components with light angle f, Ldun(f). Z p=2 2p cos f sin fLdun ðfÞ df (A.4) Ldun ¼ 0
Then, absorbed downward diffuse irradiance in layer n, DLddn,1, is calculated as follows: DLddn;1 ¼ Lddnþ1;1 L0ddn;1
(A.9)
Lddn(f) and Ldun(f) are obtained by the following iterative procedure.
Absorbed light in layer n for the first downward and non upward calculation, DLn,1,0 is obtained.
1. Calculating absorption of direct sunlight in the layer n, DLsn, from the uppermost layer to the ground.
DLn;1;0 ¼ DLsn þ DLddn;1
DLsn ¼ Ls ðSs ðn þ 1Þ Ss ðnÞÞ
(A.5)
where Ss(n) is sunlit area proportion on the lower horizon of layer n.
(A.10)
Light transmission and reflection coefficients of the leaves, m, are set at 0.1 (Loomis and Connor, 1992). Both coefficients of the panicles and stems were hypothesized to be the same as leaves. Consequently, a downward diffuse irradiance component with inclination angle f with secondary diffuse irradiance scat-
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
tered in layer n for the first calculation, Lddn,1(f) is calculated as follows: Lddn;1 ðfÞ ¼ Lddn;0 ðfÞ þ R p=2
DLn;1;0 m
2p cos f sin f df (A.11) DLn;1;0 m ¼ Lddn;0 ðfÞ þ p 3. Calculating upward diffuse irradiance from the ground to the uppermost layer. The upward diffuse irradiance component with inclination angle f without secondary diffuse irradiance scattered in layer n for the first calculation, L0dunþ1;1 (f), is obtained in the same way as Eq. (A.6): L0dunþ1;1 ðfÞ ¼ Ldun;1 ðfÞeKn Fn
(A.12)
The upward diffuse irradiance on plane n + 1 without secondary diffuse irradiance scattered in layer n for the first calculation, L0dunþ1;1 , is obtained by integration of L0dunþ1;1 (f). Z p=2 0 2p cos f sin fL0dunþ1;1 ðfÞ df (A.13) Ldunþ1;1 ¼ 0
In the same way, the upward diffuse irradiance on plane n with secondary diffuse irradiance scattered in layer n 1 for the first calculation, Ldun,1, is obtained. Z p=2 2p cos f sin fLdun;1 ðfÞ df (A.14) Ldun;1 ¼ Then, absorbed upward diffuse irradiance in layer n, DLdun,1, is calculated as follows: (A.15)
Absorbed light in layer n for the first downward and first upward calculation, DLn,1,1 is obtained. DLn;1;1 ¼ DLsn þ DLddn;1 þ DLdun;1
(A.100 )
Procedures 2 and 3 are repeated four times in total to obtain convergent results. As a result, downward and upward diffuse irradiance components, Lddn(f) and Ldun(f) are obtained. Lddn ðfÞ ¼ Lddn;4 ðfÞ
(A.18)
Ldun ðfÞ ¼ Ldun;4 ðfÞ
(A.19)
Averaged downward and upward diffuse irradiance in ^ ^ layer n, Lddn (f) and Ldun (f), are an integrated average on the assumption that Lddn+1(f) changes into Lddn(f) exponentially and that Ldun(f) also changes into Ldun+1(f) exponentially. 8Rw ðfÞecz dz > 0 Lddnþ1 > Rw > > > > 0 dz < L ðfÞð1 ecw Þ ^ ddnþ1 (A.20) Lddn ðfÞ ¼ > > cw > > ðL ðfÞ Lddn ðfÞÞ > > : ddnþ1 lnðLddnþ1 ðfÞ=Lddn ðfÞÞ where c¼
lnðLddnþ1 ðfÞ=Lddn ðfÞÞ w
(A.21)
In the same way:
0
DLdun;1 ¼ Ldun;1 L0dunþ1;1
In procedure 2 in the second cycle, DLdun,1 is added to the right side of Eq. (A.10). DLn;2;1 ¼ DLsn þ DLddn;2 þ DLdun;1
0
301
(A.16)
Consequently, an upward diffuse irradiance component with inclination angle f with secondary diffuse irradiance scattered in layer n for the first calculation, Ldun+1,1(f) is calculated as follows: m (A.17) Ldunþ1;1 ðfÞ ¼ L0dunþ1;1 ðfÞ þ DLn;1;1 p 4. Repeating procedures 2 and 3 for three cycles more.
^ Ldun ðfÞ ¼
Ldun ðfÞ Ldunþ1 ðfÞ lnðLdun ðfÞ=Ldunþ1 ðfÞÞ
(A.22)
Direct sunlight on a sunlit leaf surface with inclination angle ui, Lleafsi, was obtained by Kuroiwa (1968). Ls jl sl j sin h sin ui cos a ¼ Ls þcos ui tanh
Lleafsi ¼
(A.23)
where sl is the unit normal vector of the leaf surface and h is sun altitude. In the same way, the diffuse irradiance component, Lleafdni(f), is as follows: Lleafdni ðfÞ ¼
^ ^ ðLddn ðfÞ þ Ldun ðfÞÞjl sl j sin f
(A.24)
302
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
Diffuse irradiance on leaf surface in layer n, Lleafdni, is the integral of Lleafdni(f). Lleafdni ¼
Z
p=2
Z
0
aLCs ¼ arccos
ððLC DLleaf Lleafdni Þ=Ls cos ui Þtanh ; sin ui
0 aLCs p
2p
Lleafdni ðfÞ da df
(A.25)
(A.30)
0
For photosynthesis calculations, irradiance on a leaf’s surface is divided into leaf irradiance classes with a width, DLleaf (50 mmol m2 s1), and partial leaf area index in each leaf irradiance class are summed by leaf positions. Leaf irradiance class LCd of leaf inclination angle ui in the shade in layer n is as follows: Lleafdni LCd ¼ trunc DLleaf
(A.26)
LCs at a = 0, LCs0, and LCs at a = p, LCsp, are defined as follows: ðLs ðsin ui =tanh þ cos ui Þ þ Lleafdni Þ LCs0 ¼ trunc DLleaf (A.31) Ls ðsin ui =tanh cos ui Þ þ Lleafdni LCsp ¼ trunc DLleaf (A.32)
where trunc is a truncating function. Therefore, partial leaf area index of leaf position j with leaf irradiance class LCd in shade, LFdnLCd ji was as follows:
LFsnLCs ji is obtained as follows for all LCs (LCs0 LCs LCsp), because the right side of Eq. (A.29) is monotone decreasing on a:
LFdnLCd ji ¼ Fdn ji
LFsnLCs ji ¼
(A.27)
Irradiance on a sunlit leaf surface, Lleafsni is the sum of direct and diffuse irradiance. Lleafsni ¼ Lleafsi þ Lleafdni
(A.28)
Partial sunlit leaf area index in irradiance class LCs, LFsnLCsji, is obtained as follows. Irradiance on a sunlit leaf is calculated in two cases on sun altitude h and leaf inclination angle ui. 1. h ui When h ui, sin ui cos a/tan h + cos ui Eq. (A.23) on Lleafsi is 0 or more.
in
8 Lleafsi þLleafdni > > trunc > > DLleaf > > < Ls jsin ui cos a=tanhþcos ui jþLleafdni LCs ¼ trunc > DLleaf > > > Ls ðsin ui cos a=tanhþcos ui ÞþLleafdni > > : trunc DLleaf (A.29) Azimuth angle of leaves in irradiance class LCs, aLCs is defined in Eq. (A.30).
Fsn ji ðaLCs aLCs þ1 Þ p
(A.33)
when aLCs0 þ1 and aLCsp are defined as follows: aLCs0 þ1 ¼ 0;
aLCsp ¼ p
(A.34)
2. 0 < h < ui When 0 < h LCsp Because among 0 < a a0, sin ui cos a/tan h + cos ui in Eq. (A.29) is positive, LFsnLCs ji is calculated by Eq. (A.33).
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
(2) LCsp LCs > LCd Among LCsp LCs > LCd, there are two a corresponding to LCs. a0LCs is defined as the larger a corresponding to LCs. ððLCs DLleaf LleafdniÞ=Ls cos ui Þtanh 0 aLCs ¼ arccos sin ui (A.36) a0LCsp þ1 is defined as follows: a0LCsp þ1 ¼ p
(A.37)
Then Fsn ji ðaLCs aLCs þ1 þ a0LCs þ1 a0LCs Þ p (A.38) (3) LCs = LCd
LFsnLCs ji ¼
When a is a0, LCs is LCd, because Lleafsi is zero (Eqs. (A.23) and (A.35)) and Lleafsni is Lleafdni (Eq. (A.28)). Therefore: 8 F ða aLCd þ1 þ a0LCd þ1 a0 Þ > < sn ji 0 p LFsnLCs ji ¼ 0 > : Fsn ji ðaLCd þ1 aLCd þ1 Þ p (A.39) Considering sunlit and shaded leaves, partial leaf area index with irradiance class LC, LFnLCji, is as follows: LFnLC ji ¼ LFsnLC ji þ LFdnLC ji
(A.40)
Averaged irradiance on leaf surface during daytime, LF ^j , is an integral average during daytime of averaged irradiance on a leaf surface. R H0 P P P P n i LCLFnLC ji = n i LFnLC ji dH ^ 0 LF j ¼ R H0 0 dH (A.41)
References Anten, N.P.R., Schieving, F., Werger, M.J.A., 1995. Patterns of light and N distribution in relation to whole canopy carbon gain in C3 and C4 mono- and dicotyledonous species. Oecologia 101, 504– 513.
303
Anten, N.P.R., Miyazawa, K., Hikosaka, K., Nagashima, H., Hirose, T., 1998. Leaf nitrogen distribution in relation to leaf age and photon flux density in dominant and subordinate plants in dense stands of a dicotyledonous herb. Oecologia 113, 314– 324. Boote, K.J., Tollenaar, M., 1994. Modeling genetic yield potential. In: Boote, K.J., Bennett, J.M., Sinclair, T.R., Paulsen, G.M. (Eds.), Physiology and Determination of Crop Yield. American Society of Agronomy, Crop Science Society of America. Soil Science Society of America, Madison, pp. 533–565. Bremner, J.M., Mulvaney, C.S., 1982. Nitrogen-total. In: Page, A.L., Miller, R.H., Keeney, D.R. (Eds.), Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties. American Society of Agronomy, Madison, pp. 595–624. Cock, J.H., Yoshida, S., 1972. Accumulation of 14C-labelled carbohydrate before flowering and its subsequent redistribution and respiration in the rice plant. Proc. Crop Sci. Soc. Jpn. 41, 226– 234. Connor, D.J., Sadras, V.O., Hall, A.J., 1995. Canopy nitrogen distribution and the photosynthetic performance of sunflower crops during grain filling—a quantitative analysis. Oecologia 101, 274–281. DeJong, T.M., Doyle, J.F., 1985. Seasonal relationships between leaf nitrogen content (photosynthetic capacity) and leaf canopy light exposure in peach (Prunus persica). Plant Cell Environ. 8, 701– 706. Dreccer, M.F., Slafer, G.A., Rabbinge, R., 1998. Optimization of vertical distribution of canopy nitrogen: an alternative trait to increase yield potential in winter cereals. J. Crop Prod. 1, 47– 77. Drouet, J.L., Bonhomme, R., 1999. Do variations in local leaf irradiance explain changes to leaf nitrogen within row maize canopies? Ann. Bot. 84, 61–69. Evans, J.R., 1989. Partitioning of nitrogen between and within leaves grown under different irradiances. Aust. J. Plant Physiol. 16, 533–548. Evans, J.R., 1993. Photosynthetic acclimation and nitrogen partitioning within a lucerne canopy. II Stability through time and comparison with a theoretical optimum. Aust. J. Plant Physiol. 20, 69–82. Field, C., 1983. Allocating leaf nitrogen for the maximization of carbon gain: leaf age as a control on the allocation program. Oecologia 56, 341–347. Gimenez, C., Connor, D.J., Rueda, F., 1994. Canopy development, photosynthesis and radiation-use efficiency in sunflower in response to nitrogen. Field Crops Res. 38, 15–27. Hasegawa, T., 1999. Changes in vertical distribution of leaf nitrogen with the growth stage and the influence on dry matter production in rice. Plant Prod. Sci. 2, 37–46. Hikosaka, K., Terashima, I., Katoh, S., 1994. Effects of leaf age, nitrogen nutrition and photon flux density on the distribution of nitrogen among leaves of a vine (Ipomoea tricolor Cav.) grown horizontally to avoid mutual shading of leaves. Oecologia 97, 451–457. Hirose, T., Werger, M.J.A., 1987a. Nitrogen use efficiency in instantaneous and daily photosynthesis of leaves in the canopy of a Solidago altissima stand. Physiol. Plant. 70, 215–222.
304
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
Hirose, T., Werger, M.J.A., 1987b. Maximizing daily canopy photosynthesis with respect to the leaf nitrogen allocation pattern in the canopy. Oecologia 72, 520–526. Hirose, T., Werger, M.J.A., Pons, T.L., van Rheenen, J.W.A., 1988. Canopy structure and leaf nitrogen distribution in a stand of Lysimachia vulgaris L. as influenced by stand density. Oecologia 77, 145–150. Hirose, T., Werger, M.J.A., van Rheenen, J.W.A., 1989. Canopy development and leaf nitrogen distribution in a stand of Carex acutiformis. Ecology 70, 1610–1618. Horie, T., 1966. Preliminary report of a method for estimating sunlit leaf area within a corn canopy. J. Agric. Meteorol. 2, 45–49 (in Japanese with English summary). Ishihara, K., Kuroda, E., Ishii, R., Ogura, T., 1979. Relationship between nitrogen content in leaf blades and photosynthetic rate in rice plants measured with an infrared gas analyzer and an oxygen electrode. Jpn. J. Crop Sci. 48, 551–556 (in Japanese with English summary). Ito, A., 1969. Geometrical structure of rice canopy and penetration of direct solar radiation. Proc. Crop Sci. Soc. Jpn. 38, 355–363 (in Japanese with English summary). Kuroiwa, S., 1968. Theoretical analysis of light factor and photosynthesis in plant communities. (3) Total photosynthesis of a foliage under parallel light in comparison with that under isotropic light condition. J. Agric. Meteorol. 24, 75–90 (in Japanese with English summary). Kuroiwa, S., Monsi, M., 1963. Theoretical analysis of light factor and photosynthesis in plant communities. (1) Relationships between foliage structure and direct, diffuse and total solar radiations. J. Agric. Meteorol. 18, 143–151 (in Japanese with English summary). Lemaire, G., Onillon, B., Gosse, G., Chartier, M., Allirand, J.M., 1991. Nitrogen distribution within a lucerne canopy during regrowth: relation with light distribution. Ann. Bot. 68, 483– 488. Loomis, R.S., Connor, D.J., 1992. Crop Ecology: Productivity and Management in Agricultural Systems. Cambridge University Press, Cambridge. Makino, A., Mae, T., Ohira, K., 1988. Relationships between nitrogen and the limiting factors for the photosynthetic rate under ambient air conditions in soybean leaves. Comparison with wheat and rice. Jpn. J. Soil Sci. Plant Nutr. 59, 377–381 (in Japanese with English summary). ¨ ber den lichtfaktor in den pflanzenMonsi, M., Saeki, T., 1953. U gesellschaften und seine bedeutung fu¨r die stoffproduktion. Jpn. J. Bot. 14, 22–52. Mooney, H.A., Field, C., Gulmon, S.L., Bazzaz, F.A., 1981. Photosynthetic capacity in relation to leaf position in desert versus oldfield annuals. Oecologia 50, 109–112. Murata, Y., Matsushima, S., 1975. Rice. In: Evans, J.R. (Ed.), Crop Physiology. Cambridge University Press, London, pp. 73–99. Noode´n, L.D., Guiame´t, J.J., 1989. Regulation of assimilation and senescence by the fruit in monocarpic plants. Physiol. Plant. 77, 267–274.
Peng, S., Cassman, K.G., Kropff, M.J., 1995. Relationship between leaf photosynthesis and nitrogen content of field-grown rice in tropics. Crop Sci. 35, 1627–1630. Penning de Vries, F.W.T., van Keulen, H., Alagos, J.C., 1988. Nitrogen redistribution and potential production in rice. In: Proceedings of the International Congress of Plant Physiology, New Delhi, pp. 513–520. Pons, T.L., Schieving, T., Hirose, T., Werger, M.J.A., 1989. Optimization of leaf nitrogen allocation for canopy photosynthesis in Lysimachia vulgaris. In: Lambers, H., Cambridge, M.L., Konings, H., Pons, T.L. (Eds.), Causes and Consequences of Variation in Growth Rate and Productivity of Higher Plants. SPB Academic Publishing, The Hague, pp. 175–186. Pons, T.L., van Rijnberk, H., Scheurwater, I., van der Werf, A., 1993. Importance of the gradient in photosynthetically active radiation in a vegetation stand for leaf nitrogen allocation in two monocotyledons. Oecologia 95, 416–424. Sadras, V.O., Hall, A.J., Connor, D.J., 1993. Light-associated nitrogen distribution profile in flowering canopies of sunflower (Helianthus annuus L.) altered during grain growth. Oecologia 95, 488–494. Saitoh, K., Shimoda, H., Ishihara, K., 1990. Characteristics of dry matter production process in high yielding rice varieties. I. Canopy structure and light intercepting characteristics. Jpn. J. Crop Sci. 59, 130–139 (in Japanese with English abstract). Schieving, F., Pons, T.L., Werger, M.J.A., Hirose, T., 1992. The vertical distribution of nitrogen and photosynthetic activity at different plant densities in Carex acutiformis. Plant Soil 14, 9–17. Setter, T.L., Conocono, E.A., Egdane, J.A., Kropff, M.J., 1995. Possibility of increasing yield potential of rice by reducing panicle height in the canopy. I. Effects of panicles on light interception and canopy photosynthesis. Aust. J. Plant Physiol. 22, 441–451. Sinclair, T.R., de Wit, C.T., 1975. Photosynthate and nitrogen requirements for seed production by various crops. Science 189, 565–567. Terashima, I., Hikosaka, K., 1995. Comparative ecophysiology of leaf and canopy photosynthesis. Plant cell Environ. 18, 1111– 1128. Thorne, G.N., 1966. Physiological aspects of grain yield in cereals. In: Milthorpe, F.L., Ivins, J.D. (Eds.), The Growth of Cereals and Grasses. Butterworths, London, pp. 88–105. Uchida, N., Wada, Y., Murata, Y., 1982. Studies on the changes in the photosynthetic activity of a crop leaf during its development and senescence. II. Effect of nitrogen deficiency on the changes in the senescing leaf of rice. Jpn. J. Crop Sci. 51, 577–583 (in Japanese with English summary). Udagawa, T., Ito, A., Uchijima, Z., 1974. Phytometrical studies of crop canopies. III. Radiation environment in rice canopies. Proc. Crop Sci. Soc. Jpn. 43, 180–195 (in Japanese with English summary). Yoshida, S., Coronel, V., 1976. Nitrogen nutrition, leaf resistance, and leaf photosynthetic rate of the rice plant. Soil Sci. Plant Nutr. 22, 207–211.
Leaf nitrogen distribution to maximize the canopy photosynthesis in rice Hiroyuki Shiratsuchi *, Tohru Yamagishi, Ryuichi Ishii 1 Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1 Yayoi, Bunkyoku, Tokyo 113-8657, Japan Received 13 January 2005; received in revised form 1 April 2005
Abstract The optimum distribution of leaf nitrogen (N) in the canopy of rice plants (Oryza sativa L.) for maximum daily canopy photosynthesis (DCP) and the optimization effects on DCP were estimated during the grain filling period. The low- and highdensity canopies (28.3 and 47.5 plants m2) and isolated plants were established at heading using plants in pots grown up at the low density until heading to make the same canopy architecture except plant density and the same leaf N distribution at the start of treatment among the two canopies and the isolated plants. The simulation was conducted under two conditions of the upper limit of leaf N. Under condition 1, upper limit of leaf N content was 1.80 g m2. Under condition 2, upper limits were measured leaf N content in each leaf position at heading. The model indicates that if leaf N content in the upper leaves can be increased with reduction of N in the lower leaves, DCP will increase in any of the plant density, light conditions and under conditions 1 and 2. On a clear day, the estimated increase in DCP was 19–45 and 38–70% in the low- and high-density canopies under condition 1, respectively. Even under condition 2, which is more realistic than condition 1, the increase was up to 21 and 25% in the low- and high-density canopies. These estimates obtained by the present model that incorporates the shading effects of panicles and stems on DCP were higher than the previous reports which did not consider the effects of shading by panicles and stems. In the observed leaf N distribution, the higher the plant density was, the steeper the gradient of the leaf N remained. The gradient in the high-density canopy was closer to that of the predicted optimum leaf N distribution, and likely to contribute to maintaining higher DCP in the canopies. Compared with the hypothetical case in which gradient of leaf N distribution would be more gentle as observed in the isolated plants, the maintained steeper gradient of observed leaf N content in the canopies was estimated to increase DCP by 13 and 5% in the high- and low-density canopy, respectively. # 2005 Elsevier B.V. All rights reserved. Keywords: Canopy photosynthesis; Nitrogen distribution; Optimization; Plant density; Rice
* Corresponding author at: National Agricultural Research Center, National Agriculture and Bio-Oriented Research Organization, Kanto-Tokai Farming System 3-1-1, Tsukuba, Ibaraki 305-8666, Japan. Tel.: +81 29 838 8822; fax: +81 29 838 7038. E-mail address: [email protected] (H. Shiratsuchi). 1 Present address. College of Bioresource Sciences, Nihon University, Fujisawa, Kanagawa 252-8510, Japan.
1. Introduction The light-saturated photosynthetic rate is positively correlated with leaf nitrogen content in many crop species (Yoshida and Coronel, 1976; Uchida et al., 1982; Makino et al., 1988; Peng et al., 1995), and
0378-4290/$ – see front matter # 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.fcr.2005.04.005
292
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
decreases with a decrease of leaf N resulting from remobilization of N to other parts of the plant (Sinclair and de Wit, 1975; Penning de Vries et al., 1988; Sadras et al., 1993; Boote and Tollenaar, 1994). In rice plants, leaf N is remobilized to the grains during the grain filling period along with actively produced photosynthates. That is, there is a compromise between the supply of N and photoasimilates from leaves to the grains during grain filling such that enough N must remain in leaves to allow photosynthesis to continue, yet enough N must be transported to the grains to allow normal grain development and storage of adequate reserves. Studies of leaf N distribution on canopy photosynthesis through the improvement of light use efficiency suggest that there is an optimum distribution for maximizing canopy photosynthesis that could increase net canopy photosynthesis (Field, 1983; Hirose and Werger, 1987b; Pons et al., 1989; Schieving et al., 1992; Evans, 1993; Anten et al., 1995; Connor et al., 1995; Gimenez et al., 1994). Anten et al. (1995) reported that optimization of leaf N distribution in rice plants increases daily canopy photosynthesis (DCP) by 9% during the time before heading. However, there are no reports on the effects of optimized leaf N during the grain filling period in rice, when more than 60% of grain dry matter is usually produced (Thorne, 1966; Cock and Yoshida, 1972; Murata and Matsushima, 1975). During the grain filling period in rice, leaves are shaded by the panicles (Setter et al., 1995) resulting in an increase of the canopy extinction coefficient (Saitoh et al., 1990). Anten et al. (1995) also showed that when the light extinction coefficient is high because of high light intercepting efficiency, the effects of leaf N optimization on daily canopy photosynthesis become large. Therefore, if the shading effects of panicles and stems on DCP are not taken into account, the effects of optimization of leaf N distribution on DCP will be underestimated. The previous studies, which did not consider the shading effects of any parts other than leaves, showed DCP increase by the optimization were only 0–17% (Field, 1983; Hirose and Werger, 1987b; Pons et al., 1989; Schieving et al., 1992; Gimenez et al., 1994; Anten et al., 1995; Connor et al., 1995). The purpose of the present study is to elucidate (1) the effects of optimizing leaf N distribution in the rice plant canopy on DCP during grain filling, when
incident light was absorbed by panicles and stems as well as leaves; (2) response of leaf N distribution to plant density; and (3) the effects of the response on DCP.
2. Materials and methods 2.1. Plant material Seeds of rice plants (Oryza sativa L. cv. Musashikogane) were sown on nursery beds in the field of the Faculty of Agriculture of The University of Tokyo. After 40 days three seedlings each were transplanted to 0.05 m2 pots, which were arranged in a rectangle at a density of 28.3 plants m2. Fertilizer was applied at the rate of 1.2 g pot1 N, 1.8 g pot1 P2O5, and 1.8 g pot1 K2O. At minus 13 days after heading (DAH), two pots were isolated and fertilized with 0.75 g pot1 of N in the form of ammonium sulfate (3 N) to widen the range of leaf N content for determination of the leaf CO2 exchange parameters. The other pots were fertilized with 0.25 g pot1 at the same day (13 DAH). Using these pots, high- and low-density canopies (47.5 and 28.3 plants m2) and isolated plants were established at 0 DAH. The leaf area index (LAI) was 6.7 in the high-density canopy and 4.0 in the low-density canopy at heading. LAI remained essentially constant up to at least 21 DAH. 2.2. Measurement of leaf CO2 exchange rate Light-photosynthesis curves were determined by a gas-exchange measuring system with an infrared gas analyzer (ZAP, Fuji Electric Co. Ltd., Tokyo) on the first, third and fifth leaves counted from the top on main stems, which were illuminated by metal halide lamps (DR400/T (L) Toshiba, Tokyo) at 0, 11 and 21 DAH. For 3 N plants, the measurement was conducted on the first leaf at 10 DAH. All the measurements were done for four replications. 2.3. Measurement of canopy CO2 exchange rate Canopy photosynthesis was measured with a closed measurement system in a low-density canopy to make sure that the model of canopy photosynthesis fits the actual values. Nine plants in three pots were covered
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
293
with an equilateral prism acrylic chamber (0.29 m2 triangular base 1.15 m height) at 0, 1, 5, 7, 19 and 20 DAH.
partial organ area index of organ j in inclination angle ui and layer n, F nji, was obtained by summing the area for each organ and each inclination angle class.
2.4. Nitrogen measurements
2.6. Development of a canopy photosynthesis model
Leaves of the same four plants as leaf CO2 exchange measurement and of the four isolated plants were separated into individual leaves used for CO2 exchange measurement and seven leaf positions, dried at 80 8C at least 3 days, and weighed. The dry leaf samples were ground, and N content was determined by micro Kjeldahl method (Bremner and Mulvaney, 1982).
The model of canopy photosynthesis was developed with two submodels. Submodel 1, expressed by the following equation, gives the light response curve of leaf photosynthesis as a function of leaf N content (Hirose and Werger, 1987b). P¼
2.5. Canopy structure measurements Canopy structure was determined according to the modified tracing method (Ito, 1969). Six plants were selected from each of two different canopies in terms of plant density, at 0, 11–13, and 21–23 DAH. The heights of the tip and base of leaf blades and panicles, and the height of the inflection point, if the leaf is bent, were determined. The lengths and widths of leaf blades, stems, and panicles were measured. Leaf blade width was determined every 10 cm from the base to the tip along the length of the leaf. Each stem was considered to consist of frustums. Each panicle was considered as one or two cylinders, depending on bending. For every leaf blade, stem, and panicle, the area and the inclination angle in each horizontal layer were calculated by the architecture data in 1 cm increments obtained with tracing method. Azimuth angles of the organs were assumed to distribute uniformly. The
QY L þ Pm ððQY L þ Pm Þ2 4C QY L Pm Þ1=2 2C (1)
where P is gross photosynthesis (g m2 h1); C is convexity (0 < C 1); QY is apparent quantum yield (g s h1 mmol1); L is photosynthetic photon flux density (PPFD) (mmol m2 s1); Pm isgross photosynthesis under saturating irradiance (g m2 h1). C was constant at 0.868, determined by the least squares method with the observed Pm and QY. Pm, QY, and respiration (R) were fitted to a linear regression equation of leaf N content, also by the least squares method (Table 1). Submodel 2 is for the determination of irradiance on the leaves from canopy structure and incident light. Incident irradiance was set at 2000, 1000 and 500 mmol m2 h1 on a plane perpendicular to the sun and the proportion of diffuse light in total irradiance was set at 0.400, 0.825 and 0.944, corresponding to a clear, cloudy and overcast day, respectively.
Table 1 Regression analysis of CO2 exchange parameters to leaf N content: Pm, light-saturated gross photosynthesis; QY, apparent quantum yield; R, dark respiration; C, convexity of light-photosynthesis curve fitted to a non-rectangular hyperbola (Eq. (1)) Pm (g m2 h1)
QY (g s h1 mmol1)
R (g m2 h1)
C
a
A Ba r d.f.
3.460 1.111 0.92** 54
0.00478 0.0029 0.50** 54
0.0806 0.039 0.38** 54
0.0044 0.079 (0.868b) 0.04 54
F d.f.
287.8** 1:53
17.7** 1:53
9.4 ** 1:53
a b c
Totalc
362.8** 5:340
A and B are parameters of following regression equation; Y = A (N content (g m2)) + B, where Y is each CO2 exchange parameter. The constant obtained by least squares method with measured Pm and QY for all samples was used for C value. F-test of regression of non-rectangular hyperbola: submodel 1, for which is substituted regression equations of Pm, QY and C (0.868).
294
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
Photosynthesis in each leaf position is calculated by the light-photosynthesis curve (Eq. (1)) in submodel 1 and irradiance distribution on the leaf in submodel 2. Then, the DCP is calculated by the integration of leaf photosynthesis in each position and summation of leaf positions through a day: Z 24 H0 X X X DCP ¼ LFnLC ji PLC j dH p 0 n j i XXX 24 Fn ji R j (2) n
j
i
H0 ¼ arccosðtan a tan bÞ
(3)
where a is latitude, b is declination angle, LFnLCji is partial leaf area index in leaf position j with inclination angle ui and irradiance class on the leaf surface LC in layer n, PLCj is gross photosynthesis of leaf position j in irradiance class LC, Rj is respiration of leaf position j, H is an hour angle and H0 is the hour angle at sunset when H = 0 at noon. The CO2 exchange of stems and panicles was not considered, because it would be independent of leaf N distribution. For further details see Appendix A. Optimum leaf N distribution is defined as the distribution that maximizes DCP and is determined numerically with a fixed total leaf N amount in the model under conditions 1 and 2. Condition 1 is that the upper limit was 1.80 g m2, where the relationship between leaf N content and light-saturated photosynthesis is almost linear (Ishihara et al., 1979; Makino et al., 1988; Peng et al., 1995). Condition 2 is that the upper limits were the measured values in each leaf position at 0 DAH. Condition 2 is more realistic than condition 1. Under both conditions, the lower limit of leaf N content was the measured value of dead leaves (0.18 g m2), because dead leaves were supposed to have remobilized leaf N already and not to remobilize N any more.
3. Results 3.1. Verification of the model The estimated net canopy photosynthesis produced by the model was close to the measured values regardless of light conditions (r = 0.936***, n = 25,
Fig. 1. Observed and estimated net canopy photosynthesis in lowdensity canopies under the clear, cloudy, and overcast days. Estimated photosynthesis = 0.693*** observed ptotosynthesis + 0.583*** and RMSE = 0.2898.
Fig. 1). Only when the measured values were more than 2.5 g m2 h1 on 5 or 7 DAH, did the theoretical values tend to be lower than the measured values. 3.2. Irradiance on leaves Average irradiance on leaves on the clear day decreased steeply from higher to lower leaf positions (Fig. 2A). Irradiance at all leaf positions was higher in the low-density canopy than in the high-density canopy and decreased during grain filling in both canopies. Relative irradiance on the leaves at or lower than the third leaf was always higher in the lowdensity canopy than in the high-density canopy (Fig. 2B), indicating that the gradient of irradiance was less in the low-density canopy than in the highdensity canopy. 3.3. Leaf N distribution Leaf N content was 1.19 g m2 in the first leaf and 0.53 g m2 in the sixth leaf at heading (Fig. 3). Leaf N content decreased with leaf position down the stem, except in the seventh leaf. Leaf N content declined more in the upper leaves than in the lower leaves, especially in the isolated plants after heading. The leaf N content across leaf positions was maintained at a steeper gradient in the higher density canopy than in the lower density canopy (isolated: 0.45–0.64 g m2,
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
Fig. 2. Estimated photosynthetic photon flux density (PPFD) on leaves in each leaf position during daytime under the clear days (A) and relative irradiance to first leaf position (B) in high- and lowdensity canopies.
low density: 0.43–0.80 g m2, high density: 0.48– 0.98 g m2 at 21 DAH). This was because the decline in leaf N content in the upper leaves was slower at the higher density (Fig. 3). 3.4. Optimum leaf N distribution The optimum leaf N distribution on the clear day and under condition 1 resulted in a much larger gradient than the observed one (Fig. 3); leaf N content in the upper position was close to the upper limit (1.80 g m2) and that in the lower position was close to the lower limit (0.18 g m2). The optimum leaf N distribution was not different between low and high plant densities. To attain optimum N distribution, N must be remobilized from the lower leaves and leaf N
295
Fig. 3. Leaf N distribution among different leaf positions in highand low-density canopies and isolated plants under the observed and optimum (condition 1) leaf N distributions. Error bars show the standard deviation of the observed leaf N content.
content in the upper leaf positions must be maintained at a high level throughout the grain filling period. The optimum distribution at heading under condition 1 differed little between the clear and overcast day, although the gradient of leaf N content seemed to be less on the overcast than on the clear day (Fig. 4). The gradient calculated under the overcast day conditions in optimum leaf N distribution was less steep in the low-density canopy than in the high-density canopy. In the optimum distribution under condition 2, leaf N content in the upper position remained at the upper limit (leaf N content at 0 DAH in each leaf position) and decreased to the lower limit from the bottom to the top (data not shown).
296
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
response of leaf N distribution to the gradient of irradiance on DCP. Isolated-type N distribution is defined as a profile of leaf N distribution in the isolated plants (Fig. 3). The function of leaf nitrogen content of leaf position j in the isolated plants at time t in Fig. 3 is defined as NC0iso j ðtÞ. Leaf N content of leaf position j in isolated-type N distribution for any canopy, at time t, NCisoj(t) is as follows: NCiso j ðtÞ ¼ NC0iso j ðt0 Þ Fig. 4. Optimum leaf N distribution under condition 1 in the highand low-density canopies under clear, cloudy, and overcast conditions at heading.
8X XX > NCiso j ðtÞ Fn ji > < n j i XX Nleaf ðtÞ ¼ X > NC0iso j ðt0 Þ Fn ji > : j
3.5. Effects of optimization of leaf N distribution on DCP Optimization of leaf N distribution increased DCP by 19% (from 30.6 to 36.3 g m2 day1) in the lowdensity canopy at heading under the clear day regimen and condition 1 and by 38% (from 28.5 to 39.3 g m2 day1) in the high-density canopy (Table 2). During grain filling, as the leaves aged, DCP in the measured leaf N distribution decreased in both canopies. However, DCP increased by optimization up to 45% in the low-density canopy and 70% in the high-density canopy. Effects of optimization were always smaller in the low-density canopy than in the high-density canopy. Optimization increased DCP regardless of light conditions (clear, cloudy, or overcast), though the increase in DCP was less under the lower irradiance conditions. Optimization increased DCP by 19–21% in the low-density canopy and by 20–25% in the high-density canopy under clear day parameters and condition 2, where the upper limit of leaf N content was set at the values measured at 0 DAH for each leaf position. The increasing rate was always less under condition 2 than under condition 1. 3.6. Effects of the response of leaf N distribution to plant density DCP from the observed N distribution was compared with DCP from the hypothetical isolatedtype N distribution, which is attributed mainly to leaf age gradient and minimally to the gradient of irradiance on leaves, to elucidate the effects of
(4)
n
(5)
i
where t0 is a function of t and makes Eq. (5) true, and, Nleaf(t) is the total amount of leaf N in the objective canopy at time t. Substituting t0 to the right side of Eq. (4), leaf N content in the isolated-type distribution, NCisoj(t) is obtained. On the clear day, DCP under the observed leaf N distribution was 5% higher than under the isolatedtype distribution at 11 and 21 DAH in the low-density canopy, and was 8 and 13% higher at 11 and 21 DAH, respectively, in the high-density canopy (Table 2). DCP under the observed N distribution was higher than under the isolated-type N distribution regardless of light conditions, though there was less of an increase of DCP with a decrease of irradiance.
4. Discussion 4.1. Optimum and observed leaf N distribution The gradient of leaf N content among the leaves under optimum leaf N distribution was larger than under the observed distribution (Fig. 3) as reported previously (Field, 1983; Hirose and Werger, 1987b; Pons et al., 1989; Schieving et al., 1992; Evans, 1993) and particularly in fertilized canopies with a large LAI (Gimenez et al., 1994; Anten et al., 1995). In conditions of optimum leaf N distribution, leaf N content remobilized from the lower leaves during grain filling in both the high- and low-density canopies (Fig. 3). In contrast, in the observed distribution, leaf N content decreased more in the upper leaves than in the lower leaves and, consequently, the gradient of leaf
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
297
Table 2 Daily canopy photosynthesis (DCP) in rice with the different leaf N distribution on the clear, cloudy and overcast days Weather
Clear
Cloudy
Overcast
Density
N distribution
0 DAH
11 DAH
21 DAH
DCP (g m2 d1)
Ratio
DCP (g m2 d1)
Ratio
DCP (g m2 d1)
Ratio
Low
Observed Optimum 1a Optimum 2b Isolated
30.6 36.3 30.6 30.6
1.00 1.19 1.00 1.00
17.3 25.0 20.6 16.4
1.00 1.45 1.19 0.95
15.4 22.1 18.6 14.6
1.00 1.44 1.21 0.95
High
Observed Optimum 1 Optimum 2 Isolated
28.5 39.3 28.5 28.5
1.00 1.38 1.00 1.00
17.3 29.2 20.7 16.0
1.00 1.69 1.20 0.92
12.4 21.1 15.5 11.0
1.00 1.70 1.25 0.89
Low
Observed Optimum 1 Optimum 2 Isolated
23.8 27.4 23.8 23.8
1.00 1.15 1.00 1.00
14.0 18.9 16.1 13.2
1.00 1.35 1.15 0.94
12.9 16.2 14.8 12.1
1.00 1.26 1.15 0.94
High
Observed Optimum 1 Optimum 2 Isolated
19.0 25.8 19.0 19.0
1.00 1.36 1.00 1.00
11.9 19.8 14.1 10.8
1.00 1.66 1.18 0.91
8.7 14.3 10.8 7.6
1.00 1.64 1.24 0.87
Low
Observed Optimum 1 Optimum 2 Isolated
9.6 11.8 9.6 9.6
1.00 1.23 1.00 1.00
5.1 7.7 6.3 4.6
1.00 1.51 1.24 0.90
4.8 6.3 5.8 4.3
1.00 1.31 1.21 0.90
High
Observed Optimum 1 Optimum 2 Isolated
2.9 6.6 2.9 2.9
1.00 2.28 1.00 1.00
0.8 5.1 1.9 0.1
1.00 6.38 2.38 0.13
0.1 2.9 1.1 0.6
– – – –
Optimum 1 is the optimum N distribution under condition 1 in which lower and upper limits of leaf N content are 0.18 and 1.80 g m2. Optimum 2 is the optimum N distribution under condition 2 in which lower limit of leaf N content is 0.18 g m2 and the upper limits in each leaf position are the measured values in the leaf positions at 0 DAH. a
b
N content decreased. A similar decrease in the gradient was reported in sunflower (Sadras et al., 1993; Connor et al., 1995). In contrast, the gradient of leaf N increased during grain filling in rice grown by hydroponics (Hasegawa, 1999). In this hydroponic culture, continuous N application during grain filling could affect the gradient by making nitrogen readily available for uptake to the canopy, whereas N usually diminishes in soil culture. The decrease in the leaf N gradient was affected by plant density (Fig. 3). That is, a steep gradient was maintained in the high-density canopy during grain filling, while the gradient became much shallower in the isolated plants. The optimum leaf N distribution did not differ between light conditions (Fig. 4), as reported previously (Hirose and Werger, 1987b; Pons et al.,
1989). Connor et al. (1995), however, showed that the gradient of leaf N content under optimum distribution conditions increased as incident light decreased. The contradiction between Connor et al. (1995) and the present study apparently results from lower maximum leaf N content (1.8 g m2) in the present study than the highest leaf N content (3.5 g m2) in optimum leaf N profiles for sunflower in Connor et al. (1995). In summary, leaf N distribution was more similar to the optimum distribution in the high-density canopy than in the low-density canopy regardless of light conditions. 4.2. Response of leaf N distribution to irradiance We have shown for the first time under canopy conditions, that a steeper leaf N gradient resulted from
298
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
a steeper gradient of irradiance, by excluding the effects of leaf age (Figs. 2 and 3). The effects of leaf age were excluded by comparing the high- and lowdensity canopies and the isolated plants which consisted of the plants which were grown up in the same canopy until 0 DAH and therefore had the same leaf age distribution and the similar plant architecture. Light distribution in a canopy (DeJong and Doyle, 1985; Hirose et al., 1988; Evans, 1989; Lemaire et al., 1991; Schieving et al., 1992; Pons et al., 1993; Sadras et al., 1993; Anten et al., 1998; Drouet and Bonhomme, 1999) and at least partially leaf age (Mooney et al., 1981; Field, 1983; Hirose et al., 1989; Anten et al., 1998) have been considered as the factors responsible for the gradient of leaf N. However, it has been difficult to distinguish between the effects of the gradient of irradiance and those of leaf age, since a gradient of irradiance is usually accompanied by a gradient of leaf age in the canopy. Hikosaka et al. (1994) has successfully distinguished between these variables by excluding mutual shading and clearly showed that both the irradiance gradient and leaf age can result in a gradient of leaf N. However, there are no similar studies in which canopy effects were considered. 4.3. Factors making the observed gradient of leaf N less than the optimum In the high- and low-density canopies and, especially, isolated plants, leaf N content declined more rapidly in the upper leaves with high N content than the lower leaves with low N content (Fig. 3). It has been proposed that during grain filling in sunflower, a N-priority strategy in which a higher priority for N than C made the upper leaves the source of N rather than of C (Sadras et al., 1993), and a position-dependent mechanism remobilizes more N from leaves close to the grains (Sadras et al., 1993). While not contradicted by the present results, further studies are required to confirm these hypotheses. Growing grains obtain N from leaves during grain filling, causing leaf N content to decline (Sadras et al., 1993). Grain demand also affected leaf senescence in soybean (Noode´n and Guiame´t, 1989). These results suggest that remobilization of leaf N to grains might affect the aging of the leaves and decrease the gradient of leaf N in the present study.
Terashima and Hikosaka (1995) reviewed five reasons that observed leaf N distribution differs from the optimum: limited acclimation to the light environment, an upper limit to photosynthetic components in a leaf, cost of N redistribution, preferential herbivory of leaves of high N content, and neglect of direct sunlight. The first four factors are mainly for vegetative canopies and are not applicable to rice during grain filling in the present study. Direct sunlight is factored into the present study, therefore none of the five previously considered factors can account for the decline of the gradient of leaf N in the present study. The mechanism decreasing the gradient of leaf N during grain filling remains to be elucidated. 4.4. Increase of DCP by the optimization of leaf N distribution We showed for the first time that DCP was 19–45% higher in the low-density canopy and 38–70% higher in the high-density canopy in the optimum leaf N distribution than in the observed distribution on the clear day during grain filling (Table 2). Although essential to crop yield, there has been only one optimization study during grain filling (Connor et al., 1995). DCP increased with the N optimization even under overcast conditions in the present study. In contrast, an increase of N content in the canopy seemed to decrease DCP under overcast conditions, possibly because of increased respiration, while it might increase DCP on clear days (cf. Hirose and Werger, 1987a). DCP increase by the optimization of leaf N distribution was larger in the present study (condition 1, Table 2) than the 0–17% that has previously been reported (Field, 1983; Hirose and Werger, 1987b; Pons et al., 1989; Schieving et al., 1992; Gimenez et al., 1994; Anten et al., 1995; Connor et al., 1995). DCP increases by the optimization of leaf N distribution were larger than in the previous reports for three apparent reasons including, most significantly, the shading effects of panicles and stems. Shading effects of the inflorescence have been reported in rice (Saitoh et al., 1990; Setter et al., 1995) and other crops (Dreccer et al., 1998). The shading effects of plant parts other than leaves increase the apparent extinction coefficient, since the apparent amount of absorbed light by leaves in a leaf layer is the sum of absorbed
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
light by the leaves, panicles, and stems. When the extinction coefficient was large, which increased the gradient of irradiance on the leaves, the effects of optimization of leaf N distribution were large (Anten et al., 1995). A second reason is the relatively large LAI (4.0 and 6.7) compared to previous reports. A large LAI increases the effects of optimization of leaf N distribution on DCP (Hirose and Werger, 1987b; Schieving et al., 1992). Finally, this study was limited to the period of grain filling, rather than pre-senescence, which may accentuate differences in the average leaf N content, which was relatively low (0.61–0.84 g m2) compared to previous reports (1.33 g m2: Hirose and Werger, 1987b; 0.51 g m2: Pons et al., 1989; 0.90– 1.37 g m2: Schieving et al., 1992; 1.15–1.59 g m2 for C3 species: Anten et al., 1995). When canopy leaf N content was low, leaf N distribution had a larger effect on radiation use efficiency than in the high leaf N canopy (Dreccer et al., 1998). The optimization of leaf N distribution greatly increases DCP during grain filling in rice, when the shading effects of panicles and stems are considered. The optimization of leaf N distribution under condition 2 and clear daylight also increased DCP by 19–21% in the low-density canopy and 20–25% in the high-density canopy (Table 2). This result indicates that DCP during grain filling in rice would increase when leaf N is remobilized from the lower leaves in the order of leaf position, since leaf N content decreased in the same way from the lower leaves in the optimum leaf N distribution under condition 2, where the maximum leaf N contents in each leaf position are set to those at heading (data not shown). Therefore, if the remobilization sequence can be changed genetically or chemically, DCP could increase substantially.
299
to the irradiance gradient increased DCP up to 13%. This result indicates that leaf N distribution changes in response to the gradient of irradiance on leaves during grain filling in rice so that DCP increases. Enhancement of this response would make leaf N distribution nearer to the optimum and, consequently, could increase DCP.
5. Conclusion During grain filling in rice, the higher the plant density was, the steeper the gradient of leaf N content across leaf positions remained. As a result of this observed leaf N response to plant density, DCP was estimated to be higher under the observed leaf N distribution than under the isolated-type leaf N distribution by the model in the present study. However, even in the high-density canopy, the gradient was still less than in the optimum distribution. The model showed that DCP would increase by optimization of leaf N distribution, especially in the high-density canopy. The estimated increase in DCP was higher than previously reported, because the shading effects of the panicles and stems were considered in the present study.
Acknowledgements We thank Dr. Kazuhiko Kobayashi for reviewing the manuscript and Dr. Toshihiro Hasegawa for his helpful advice. We are also grateful to Dr. Kouichi Futakuchi for his useful suggestions on experimental design and to Mr. Hirokuni Someya for his assistance.
Appendix A. Details of submodel 2 4.5. Increase of DCP by the effects of the irradiance gradient on leaf N distribution On the clear day, DCP was up to 13% higher under the observed leaf N distribution than under the isolated-type distribution in the high-density canopy, and 5% higher in the low-density canopy (Table 2). The isolated-type N distribution is attributed mainly to the leaf age gradient and minimally to the irradiance gradient. Therefore, the response of leaf N distribution
Submodel 2 determines the irradiance on leaves from a canopy structure and incident light environment. The first step is to calculate the irradiance on the horizon of each layer in the canopy by a modified method by Udagawa et al. (1974). The modifications are: (1) panicles and stems as well as leaves intercept light; (2) diffuse light is assumed as a set of straight lights to any of six inclination angle classes. Sun altitude is calculated according to Loomis and Connor (1992).
300
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
An extinction coefficient of a leaf averaged across azimuth angle a, Kl is obtained according to Monsi and Saeki (1953). An extinction coefficient of a panicle and stem (Kps) averaged across a is as follows: Rp jsinðl; sps Þj da Rp Kps ¼ 0 (A.1) sin f 0 da where (l, sps) is an angle between light direction unit vector l and an organ (panicle or stem) axis unit vector sps and f is the light inclination angle. An averaged extinction coefficient in the layer n, Kn was obtained by a weighted average of Kl and Kps in layer n (cf. Kuroiwa and Monsi, 1963). Irradiance on sunlit and shade areas on the leaf surface is calculated separately (cf. Udagawa et al., 1974). Partial sunlit leaf area index of leaf position j with inclination angle ui in layer n, F snji, is obtained according to Horie (1966). Partial shade leaf area index, F dnji, is obtained as follows: Fdn ji ¼ Fn ji Fsn ji
2. Calculating downward diffuse irradiance on plane n from the uppermost layer to the ground. On the assumption that diffuse irradiance is distributed uniformly over plane n, a downward diffuse irradiance component with inclination angle f without secondary diffuse irradiance scattered in layer n for the first calculation, L0ddn;1 (f), is obtained in the same way for direct sun light: L0ddn;1 ðfÞ ¼ Lddnþ1;1 ðfÞeKn Fn
where Lddn+1,1(f) is the downward diffuse irradiance component with an inclination angle f including secondary diffuse irradiance scattered above layer n for the first calculation. Then, downward diffuse irradiance without secondary diffuse irradiance scattered in layer n for the first calculation, L0ddn;1 , is obtained by integration of L0ddn;1 (f).
(A.2)
Irradiance in a sunlit area is the sum of irradiance of direct sun light, Ls, downward diffuse irradiance, Lddn, and upward diffuse irradiance, Ldun. In a shade area, the irradiance is Lddn + LdunLddn consists of downward diffuse irradiance components with an inclination angle f, Lddn(f). Z p=2 Lddn ¼ 2p cos f sin fLddn ðfÞ df (A.3) 0
(A.6)
L0ddn;1
¼
Z
p=2
2p cos f sin fL0ddn;1 ðfÞ df
0
(A.7)
In the same way, downward diffuse irradiance with secondary diffuse irradiance scattered in layer n + 1 for the first calculation, Lddn+1,1, is obtained. Lddnþ1;1 ¼
Z
p=2
2p cos f sin fLddnþ1;1 ðfÞ df
(A.8)
0
Ldun consists of upward diffuse irradiance components with light angle f, Ldun(f). Z p=2 2p cos f sin fLdun ðfÞ df (A.4) Ldun ¼ 0
Then, absorbed downward diffuse irradiance in layer n, DLddn,1, is calculated as follows: DLddn;1 ¼ Lddnþ1;1 L0ddn;1
(A.9)
Lddn(f) and Ldun(f) are obtained by the following iterative procedure.
Absorbed light in layer n for the first downward and non upward calculation, DLn,1,0 is obtained.
1. Calculating absorption of direct sunlight in the layer n, DLsn, from the uppermost layer to the ground.
DLn;1;0 ¼ DLsn þ DLddn;1
DLsn ¼ Ls ðSs ðn þ 1Þ Ss ðnÞÞ
(A.5)
where Ss(n) is sunlit area proportion on the lower horizon of layer n.
(A.10)
Light transmission and reflection coefficients of the leaves, m, are set at 0.1 (Loomis and Connor, 1992). Both coefficients of the panicles and stems were hypothesized to be the same as leaves. Consequently, a downward diffuse irradiance component with inclination angle f with secondary diffuse irradiance scat-
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
tered in layer n for the first calculation, Lddn,1(f) is calculated as follows: Lddn;1 ðfÞ ¼ Lddn;0 ðfÞ þ R p=2
DLn;1;0 m
2p cos f sin f df (A.11) DLn;1;0 m ¼ Lddn;0 ðfÞ þ p 3. Calculating upward diffuse irradiance from the ground to the uppermost layer. The upward diffuse irradiance component with inclination angle f without secondary diffuse irradiance scattered in layer n for the first calculation, L0dunþ1;1 (f), is obtained in the same way as Eq. (A.6): L0dunþ1;1 ðfÞ ¼ Ldun;1 ðfÞeKn Fn
(A.12)
The upward diffuse irradiance on plane n + 1 without secondary diffuse irradiance scattered in layer n for the first calculation, L0dunþ1;1 , is obtained by integration of L0dunþ1;1 (f). Z p=2 0 2p cos f sin fL0dunþ1;1 ðfÞ df (A.13) Ldunþ1;1 ¼ 0
In the same way, the upward diffuse irradiance on plane n with secondary diffuse irradiance scattered in layer n 1 for the first calculation, Ldun,1, is obtained. Z p=2 2p cos f sin fLdun;1 ðfÞ df (A.14) Ldun;1 ¼ Then, absorbed upward diffuse irradiance in layer n, DLdun,1, is calculated as follows: (A.15)
Absorbed light in layer n for the first downward and first upward calculation, DLn,1,1 is obtained. DLn;1;1 ¼ DLsn þ DLddn;1 þ DLdun;1
(A.100 )
Procedures 2 and 3 are repeated four times in total to obtain convergent results. As a result, downward and upward diffuse irradiance components, Lddn(f) and Ldun(f) are obtained. Lddn ðfÞ ¼ Lddn;4 ðfÞ
(A.18)
Ldun ðfÞ ¼ Ldun;4 ðfÞ
(A.19)
Averaged downward and upward diffuse irradiance in ^ ^ layer n, Lddn (f) and Ldun (f), are an integrated average on the assumption that Lddn+1(f) changes into Lddn(f) exponentially and that Ldun(f) also changes into Ldun+1(f) exponentially. 8Rw ðfÞecz dz > 0 Lddnþ1 > Rw > > > > 0 dz < L ðfÞð1 ecw Þ ^ ddnþ1 (A.20) Lddn ðfÞ ¼ > > cw > > ðL ðfÞ Lddn ðfÞÞ > > : ddnþ1 lnðLddnþ1 ðfÞ=Lddn ðfÞÞ where c¼
lnðLddnþ1 ðfÞ=Lddn ðfÞÞ w
(A.21)
In the same way:
0
DLdun;1 ¼ Ldun;1 L0dunþ1;1
In procedure 2 in the second cycle, DLdun,1 is added to the right side of Eq. (A.10). DLn;2;1 ¼ DLsn þ DLddn;2 þ DLdun;1
0
301
(A.16)
Consequently, an upward diffuse irradiance component with inclination angle f with secondary diffuse irradiance scattered in layer n for the first calculation, Ldun+1,1(f) is calculated as follows: m (A.17) Ldunþ1;1 ðfÞ ¼ L0dunþ1;1 ðfÞ þ DLn;1;1 p 4. Repeating procedures 2 and 3 for three cycles more.
^ Ldun ðfÞ ¼
Ldun ðfÞ Ldunþ1 ðfÞ lnðLdun ðfÞ=Ldunþ1 ðfÞÞ
(A.22)
Direct sunlight on a sunlit leaf surface with inclination angle ui, Lleafsi, was obtained by Kuroiwa (1968). Ls jl sl j sin h sin ui cos a ¼ Ls þcos ui tanh
Lleafsi ¼
(A.23)
where sl is the unit normal vector of the leaf surface and h is sun altitude. In the same way, the diffuse irradiance component, Lleafdni(f), is as follows: Lleafdni ðfÞ ¼
^ ^ ðLddn ðfÞ þ Ldun ðfÞÞjl sl j sin f
(A.24)
302
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
Diffuse irradiance on leaf surface in layer n, Lleafdni, is the integral of Lleafdni(f). Lleafdni ¼
Z
p=2
Z
0
aLCs ¼ arccos
ððLC DLleaf Lleafdni Þ=Ls cos ui Þtanh ; sin ui
0 aLCs p
2p
Lleafdni ðfÞ da df
(A.25)
(A.30)
0
For photosynthesis calculations, irradiance on a leaf’s surface is divided into leaf irradiance classes with a width, DLleaf (50 mmol m2 s1), and partial leaf area index in each leaf irradiance class are summed by leaf positions. Leaf irradiance class LCd of leaf inclination angle ui in the shade in layer n is as follows: Lleafdni LCd ¼ trunc DLleaf
(A.26)
LCs at a = 0, LCs0, and LCs at a = p, LCsp, are defined as follows: ðLs ðsin ui =tanh þ cos ui Þ þ Lleafdni Þ LCs0 ¼ trunc DLleaf (A.31) Ls ðsin ui =tanh cos ui Þ þ Lleafdni LCsp ¼ trunc DLleaf (A.32)
where trunc is a truncating function. Therefore, partial leaf area index of leaf position j with leaf irradiance class LCd in shade, LFdnLCd ji was as follows:
LFsnLCs ji is obtained as follows for all LCs (LCs0 LCs LCsp), because the right side of Eq. (A.29) is monotone decreasing on a:
LFdnLCd ji ¼ Fdn ji
LFsnLCs ji ¼
(A.27)
Irradiance on a sunlit leaf surface, Lleafsni is the sum of direct and diffuse irradiance. Lleafsni ¼ Lleafsi þ Lleafdni
(A.28)
Partial sunlit leaf area index in irradiance class LCs, LFsnLCsji, is obtained as follows. Irradiance on a sunlit leaf is calculated in two cases on sun altitude h and leaf inclination angle ui. 1. h ui When h ui, sin ui cos a/tan h + cos ui Eq. (A.23) on Lleafsi is 0 or more.
in
8 Lleafsi þLleafdni > > trunc > > DLleaf > > < Ls jsin ui cos a=tanhþcos ui jþLleafdni LCs ¼ trunc > DLleaf > > > Ls ðsin ui cos a=tanhþcos ui ÞþLleafdni > > : trunc DLleaf (A.29) Azimuth angle of leaves in irradiance class LCs, aLCs is defined in Eq. (A.30).
Fsn ji ðaLCs aLCs þ1 Þ p
(A.33)
when aLCs0 þ1 and aLCsp are defined as follows: aLCs0 þ1 ¼ 0;
aLCsp ¼ p
(A.34)
2. 0 < h < ui When 0 < h
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
(2) LCsp LCs > LCd Among LCsp LCs > LCd, there are two a corresponding to LCs. a0LCs is defined as the larger a corresponding to LCs. ððLCs DLleaf LleafdniÞ=Ls cos ui Þtanh 0 aLCs ¼ arccos sin ui (A.36) a0LCsp þ1 is defined as follows: a0LCsp þ1 ¼ p
(A.37)
Then Fsn ji ðaLCs aLCs þ1 þ a0LCs þ1 a0LCs Þ p (A.38) (3) LCs = LCd
LFsnLCs ji ¼
When a is a0, LCs is LCd, because Lleafsi is zero (Eqs. (A.23) and (A.35)) and Lleafsni is Lleafdni (Eq. (A.28)). Therefore: 8 F ða aLCd þ1 þ a0LCd þ1 a0 Þ > < sn ji 0 p LFsnLCs ji ¼ 0 > : Fsn ji ðaLCd þ1 aLCd þ1 Þ p (A.39) Considering sunlit and shaded leaves, partial leaf area index with irradiance class LC, LFnLCji, is as follows: LFnLC ji ¼ LFsnLC ji þ LFdnLC ji
(A.40)
Averaged irradiance on leaf surface during daytime, LF ^j , is an integral average during daytime of averaged irradiance on a leaf surface. R H0 P P P P n i LCLFnLC ji = n i LFnLC ji dH ^ 0 LF j ¼ R H0 0 dH (A.41)
References Anten, N.P.R., Schieving, F., Werger, M.J.A., 1995. Patterns of light and N distribution in relation to whole canopy carbon gain in C3 and C4 mono- and dicotyledonous species. Oecologia 101, 504– 513.
303
Anten, N.P.R., Miyazawa, K., Hikosaka, K., Nagashima, H., Hirose, T., 1998. Leaf nitrogen distribution in relation to leaf age and photon flux density in dominant and subordinate plants in dense stands of a dicotyledonous herb. Oecologia 113, 314– 324. Boote, K.J., Tollenaar, M., 1994. Modeling genetic yield potential. In: Boote, K.J., Bennett, J.M., Sinclair, T.R., Paulsen, G.M. (Eds.), Physiology and Determination of Crop Yield. American Society of Agronomy, Crop Science Society of America. Soil Science Society of America, Madison, pp. 533–565. Bremner, J.M., Mulvaney, C.S., 1982. Nitrogen-total. In: Page, A.L., Miller, R.H., Keeney, D.R. (Eds.), Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties. American Society of Agronomy, Madison, pp. 595–624. Cock, J.H., Yoshida, S., 1972. Accumulation of 14C-labelled carbohydrate before flowering and its subsequent redistribution and respiration in the rice plant. Proc. Crop Sci. Soc. Jpn. 41, 226– 234. Connor, D.J., Sadras, V.O., Hall, A.J., 1995. Canopy nitrogen distribution and the photosynthetic performance of sunflower crops during grain filling—a quantitative analysis. Oecologia 101, 274–281. DeJong, T.M., Doyle, J.F., 1985. Seasonal relationships between leaf nitrogen content (photosynthetic capacity) and leaf canopy light exposure in peach (Prunus persica). Plant Cell Environ. 8, 701– 706. Dreccer, M.F., Slafer, G.A., Rabbinge, R., 1998. Optimization of vertical distribution of canopy nitrogen: an alternative trait to increase yield potential in winter cereals. J. Crop Prod. 1, 47– 77. Drouet, J.L., Bonhomme, R., 1999. Do variations in local leaf irradiance explain changes to leaf nitrogen within row maize canopies? Ann. Bot. 84, 61–69. Evans, J.R., 1989. Partitioning of nitrogen between and within leaves grown under different irradiances. Aust. J. Plant Physiol. 16, 533–548. Evans, J.R., 1993. Photosynthetic acclimation and nitrogen partitioning within a lucerne canopy. II Stability through time and comparison with a theoretical optimum. Aust. J. Plant Physiol. 20, 69–82. Field, C., 1983. Allocating leaf nitrogen for the maximization of carbon gain: leaf age as a control on the allocation program. Oecologia 56, 341–347. Gimenez, C., Connor, D.J., Rueda, F., 1994. Canopy development, photosynthesis and radiation-use efficiency in sunflower in response to nitrogen. Field Crops Res. 38, 15–27. Hasegawa, T., 1999. Changes in vertical distribution of leaf nitrogen with the growth stage and the influence on dry matter production in rice. Plant Prod. Sci. 2, 37–46. Hikosaka, K., Terashima, I., Katoh, S., 1994. Effects of leaf age, nitrogen nutrition and photon flux density on the distribution of nitrogen among leaves of a vine (Ipomoea tricolor Cav.) grown horizontally to avoid mutual shading of leaves. Oecologia 97, 451–457. Hirose, T., Werger, M.J.A., 1987a. Nitrogen use efficiency in instantaneous and daily photosynthesis of leaves in the canopy of a Solidago altissima stand. Physiol. Plant. 70, 215–222.
304
H. Shiratsuchi et al. / Field Crops Research 95 (2006) 291–304
Hirose, T., Werger, M.J.A., 1987b. Maximizing daily canopy photosynthesis with respect to the leaf nitrogen allocation pattern in the canopy. Oecologia 72, 520–526. Hirose, T., Werger, M.J.A., Pons, T.L., van Rheenen, J.W.A., 1988. Canopy structure and leaf nitrogen distribution in a stand of Lysimachia vulgaris L. as influenced by stand density. Oecologia 77, 145–150. Hirose, T., Werger, M.J.A., van Rheenen, J.W.A., 1989. Canopy development and leaf nitrogen distribution in a stand of Carex acutiformis. Ecology 70, 1610–1618. Horie, T., 1966. Preliminary report of a method for estimating sunlit leaf area within a corn canopy. J. Agric. Meteorol. 2, 45–49 (in Japanese with English summary). Ishihara, K., Kuroda, E., Ishii, R., Ogura, T., 1979. Relationship between nitrogen content in leaf blades and photosynthetic rate in rice plants measured with an infrared gas analyzer and an oxygen electrode. Jpn. J. Crop Sci. 48, 551–556 (in Japanese with English summary). Ito, A., 1969. Geometrical structure of rice canopy and penetration of direct solar radiation. Proc. Crop Sci. Soc. Jpn. 38, 355–363 (in Japanese with English summary). Kuroiwa, S., 1968. Theoretical analysis of light factor and photosynthesis in plant communities. (3) Total photosynthesis of a foliage under parallel light in comparison with that under isotropic light condition. J. Agric. Meteorol. 24, 75–90 (in Japanese with English summary). Kuroiwa, S., Monsi, M., 1963. Theoretical analysis of light factor and photosynthesis in plant communities. (1) Relationships between foliage structure and direct, diffuse and total solar radiations. J. Agric. Meteorol. 18, 143–151 (in Japanese with English summary). Lemaire, G., Onillon, B., Gosse, G., Chartier, M., Allirand, J.M., 1991. Nitrogen distribution within a lucerne canopy during regrowth: relation with light distribution. Ann. Bot. 68, 483– 488. Loomis, R.S., Connor, D.J., 1992. Crop Ecology: Productivity and Management in Agricultural Systems. Cambridge University Press, Cambridge. Makino, A., Mae, T., Ohira, K., 1988. Relationships between nitrogen and the limiting factors for the photosynthetic rate under ambient air conditions in soybean leaves. Comparison with wheat and rice. Jpn. J. Soil Sci. Plant Nutr. 59, 377–381 (in Japanese with English summary). ¨ ber den lichtfaktor in den pflanzenMonsi, M., Saeki, T., 1953. U gesellschaften und seine bedeutung fu¨r die stoffproduktion. Jpn. J. Bot. 14, 22–52. Mooney, H.A., Field, C., Gulmon, S.L., Bazzaz, F.A., 1981. Photosynthetic capacity in relation to leaf position in desert versus oldfield annuals. Oecologia 50, 109–112. Murata, Y., Matsushima, S., 1975. Rice. In: Evans, J.R. (Ed.), Crop Physiology. Cambridge University Press, London, pp. 73–99. Noode´n, L.D., Guiame´t, J.J., 1989. Regulation of assimilation and senescence by the fruit in monocarpic plants. Physiol. Plant. 77, 267–274.
Peng, S., Cassman, K.G., Kropff, M.J., 1995. Relationship between leaf photosynthesis and nitrogen content of field-grown rice in tropics. Crop Sci. 35, 1627–1630. Penning de Vries, F.W.T., van Keulen, H., Alagos, J.C., 1988. Nitrogen redistribution and potential production in rice. In: Proceedings of the International Congress of Plant Physiology, New Delhi, pp. 513–520. Pons, T.L., Schieving, T., Hirose, T., Werger, M.J.A., 1989. Optimization of leaf nitrogen allocation for canopy photosynthesis in Lysimachia vulgaris. In: Lambers, H., Cambridge, M.L., Konings, H., Pons, T.L. (Eds.), Causes and Consequences of Variation in Growth Rate and Productivity of Higher Plants. SPB Academic Publishing, The Hague, pp. 175–186. Pons, T.L., van Rijnberk, H., Scheurwater, I., van der Werf, A., 1993. Importance of the gradient in photosynthetically active radiation in a vegetation stand for leaf nitrogen allocation in two monocotyledons. Oecologia 95, 416–424. Sadras, V.O., Hall, A.J., Connor, D.J., 1993. Light-associated nitrogen distribution profile in flowering canopies of sunflower (Helianthus annuus L.) altered during grain growth. Oecologia 95, 488–494. Saitoh, K., Shimoda, H., Ishihara, K., 1990. Characteristics of dry matter production process in high yielding rice varieties. I. Canopy structure and light intercepting characteristics. Jpn. J. Crop Sci. 59, 130–139 (in Japanese with English abstract). Schieving, F., Pons, T.L., Werger, M.J.A., Hirose, T., 1992. The vertical distribution of nitrogen and photosynthetic activity at different plant densities in Carex acutiformis. Plant Soil 14, 9–17. Setter, T.L., Conocono, E.A., Egdane, J.A., Kropff, M.J., 1995. Possibility of increasing yield potential of rice by reducing panicle height in the canopy. I. Effects of panicles on light interception and canopy photosynthesis. Aust. J. Plant Physiol. 22, 441–451. Sinclair, T.R., de Wit, C.T., 1975. Photosynthate and nitrogen requirements for seed production by various crops. Science 189, 565–567. Terashima, I., Hikosaka, K., 1995. Comparative ecophysiology of leaf and canopy photosynthesis. Plant cell Environ. 18, 1111– 1128. Thorne, G.N., 1966. Physiological aspects of grain yield in cereals. In: Milthorpe, F.L., Ivins, J.D. (Eds.), The Growth of Cereals and Grasses. Butterworths, London, pp. 88–105. Uchida, N., Wada, Y., Murata, Y., 1982. Studies on the changes in the photosynthetic activity of a crop leaf during its development and senescence. II. Effect of nitrogen deficiency on the changes in the senescing leaf of rice. Jpn. J. Crop Sci. 51, 577–583 (in Japanese with English summary). Udagawa, T., Ito, A., Uchijima, Z., 1974. Phytometrical studies of crop canopies. III. Radiation environment in rice canopies. Proc. Crop Sci. Soc. Jpn. 43, 180–195 (in Japanese with English summary). Yoshida, S., Coronel, V., 1976. Nitrogen nutrition, leaf resistance, and leaf photosynthetic rate of the rice plant. Soil Sci. Plant Nutr. 22, 207–211.