Plant Cell Physiol. 44(9): 952–956 (2003)
JSPP © 2003
Short Communication
Differences between Maize and Rice in N-use Efficiency for Photosynthesis
and Protein Allocation
Amane Makino 1, Hiroe Sakuma, Emi Sudo and Tadahiko Mae
Department of Applied Plant Science, Graduate School of Agricultural Sciences, Tohoku University, Tsutsumidori-Amamiyamachi, Aoba-ku,
Sendai, 981-8555 Japan
;
mated to be only 5–9% in C4 plants (Schmitt and Edwards
1981, Sage et al. 1987). This means that C4 plants can save
substantial N. However, C4 plants must invest N in the C4 cycle
enzymes. Sage and Pearcy (2000) described that the N cost of
the C4 cycle enzymes is relatively low. For example, in a C4
plant, Amaranthus retroflexus, phosphoenolpyruvate carboxylase (PEPC) accounts for 2–5% of total leaf N, which combined with Rubisco accounts for less than 14% of total leaf N
(Sage et al. 1987). However, there is no available data on the N
cost of other C4 cycle enzymes. Thus, it is not known whether
the N saving because of a lower amount of Rubisco is offset by
the N cost for total C4 cycle enzymes. Moreover, higher rates of
photosynthesis require higher rates of ribulose-1,5-bisphosphate (RuBP) regeneration as well as CO2 assimilation. Nevertheless, it is also not known whether C4 plants have greater
capacity of RuBP regeneration.
In this study, we compared the light-saturated rates of
photosynthesis per unit of leaf-N content in young, expanded
leaves of a C4 plant, maize (Zea mays L. cv. Honeybantam),
and a C3 plant, rice (Oryza sativa L. cv. Notohikari), including
rbcS antisense rice. We also used spinach (Spinacia oleracea
L. cv. Nobel) and bean (Phaseolus vulgaris L. cv. Tendergreen). All plants were grown hydroponically with different N
concentrations. Photosynthetic measurements were made at
ambient normal CO2 and saturating CO2 levels. Since CO2saturated photosynthesis is limited by RuBP regeneration
(Farquhar et al. 1980), we also compared the difference in
RuBP regeneration capacity. In addition, we examined the differences in N allocation to proteins of the photosynthetic apparatus between maize and rice.
The rates of light-saturated photosynthesis measured at
atmospheric partial pressure of CO2 (36 Pa) were linearly correlated with leaf-N content in both maize and several C3 plants
including rice (Fig. 1). At the same N content, although rice
had slightly higher rates of photosynthesis than spinach and
bean, the photosynthetic rate in maize was about two times
higher than that in rice. When the photosynthetic rates were
measured under saturating CO2 conditions (100 Pa CO2), the
rate in maize was still about 1.6-fold higher than that in rice
(Fig. 2). Higher rates of photosynthesis in C4 plants have been
generally considered to be due to the suppression of photores-
The N-use efficiency for photosynthesis was higher in a
C4 plant, maize, than in a C3 plant, rice, including rbcS
antisense rice with optimal ribulose-1,5-bisphosphate carboxylase (Rubisco) content for CO2-saturated photosynthesis, even when photosynthesis was measured under saturating CO2 conditions. The N cost for the C4 cycle enzymes in
maize was not large, and the lower amount of Rubisco
allowed a greater N investment in the thylakoid components. This greater content of the thylakoid components as
well as the CO2 concentrating mechanism may support
higher N-use efficiency for photosynthesis in maize.
Keywords: Gas exchange (leaf) — N-use efficiency — Oryza
sativa L. — Protein allocation — Ribulose-1,5-bisphosphate
carboxylase/oxygenase — Zea mays L.
Abbreviations: CF, coupling factor; LHC, light-harvesting Chl
protein complex; ME, malic enzyme; PEPC, phosphoenolpyruvate carboxylase; PPDK, pyruvate orthophosphate dikinase; PPFD, photosynthetic photon flux density; PS, photosystem; RuBP, ribulose-1,5bisphosphate; Rubisco, RuBP carboxylase/oxygenase.
Generally, C4 plants show a greater N-use efficiency for
photosynthesis than C3 plants (Brown 1978, Schmitt and
Edwards 1981, Sage and Pearcy 1987, Sage and Pearcy 2000).
This has been considered to be because C4 plants have a mechanism for eliminating photorespiration by increasing the concentration of CO2 around ribulose-1,5-bisphosphate carboxylase (Rubisco). Since the Km values for CO2 and O2 of Rubisco
from higher plants are close to atmospheric CO2 and O2 levels,
respectively, Rubisco in C3 plants fixes CO2 at about 25% of its
potential activity (Farquhar et al. 1980), but operates close to
its potential activity in C4 plants (Usuda 1984, Usuda et al.
1984, Sage et al. 1987). In addition, the specific activity of
Rubisco in C4 plants is about two times higher than that in C3
plants (Seemann et al. 1984, Sage 2002). Thus, a lower amount
of Rubisco may be sufficient to achieve higher rates of photosynthesis in C4 plants. In fact, although the amount of Rubisco
in C3 plants accounts for 20–30% of leaf-N content (Evans and
Seemann 1989, Makino 2003, Kumar et al. 2002), it is esti1
Corresponding author: E-mail, [email protected]; Fax, +81-22-717-8765.
952
Allocation of protein N in maize and rice
953
Fig. 1 Rate of photosynthesis at 36 Pa CO2 versus total leaf N content in young leaves of maize (open squares), rice (closed circles),
spinach (open triangles) and bean (closed triangles). Measurements
were made at a PPFD of 1,800 mmol quanta m–2 s–1, a leaf temperature
of 25°C, and a leaf-to-air vapor pressure difference of 1.0 to 1.2 kPa.
All plants were grown hydroponically with different N levels. Data for
rice were taken from Makino et al. (1997).
Fig. 2 Rate of photosynthesis at 100 Pa CO2 versus total leaf N content in young leaves of maize (open squares), rbcS antisense rice (open
triangles) and wild-type (non-transgenic) rice (closed circles). Measurements were made at a PPFD of 1,800 mmol quanta m–2 s–1, a leaf
temperature of 25°C and a leaf-to-air vapor pressure difference of 1.0
to 1.2 kPa. Data for rice including rbcS antisense rice were taken from
Makino et al. (1997).
piration because of the contribution of the CO2 concentrating
pathway to Rubisco (Brown 1978, Schmitt and Edwards 1981,
Sage et al. 1987). However, CO2-saturated photosynthesis in
rice was not comparable to that in maize. Thus, photosynthetic
N-use efficiency is higher in maize than in rice even under conditions where photorespiration is eliminated. This means that
another factor(s) besides the CO2 concentration mechanism
also contributes to higher N-use efficiency of photosynthesis in
maize.
Since C3 photosynthesis under conditions of saturating
CO2 is strongly limited by RuBP regeneration capacity
determined by electron-transport activity (Von Caemmerer and
Farquhar 1981) or the re-availability of Pi during starch and
sucrose synthesis (Sharkey 1985), the amount of Rubisco in C3
plants is thought to be excessive for CO2-saturated photosynthesis (for a review, see Makino and Mae 1999). Therefore, it is
possible that an excess investment of N in Rubisco led to lower
N-use efficiency of photosynthesis in rice than in maize under
conditions of saturating CO2. Since we previously selected
rbcS antisense rice with 65% wild-type Rubisco as a plant set
with optimal Rubisco content for CO2-saturated photosynthesis (Makino et al. 1997), the data on the photosynthetic rate
obtained with those transgenic plants are included in Fig. 2.
CO2-saturated photosynthesis in maize was still higher than
that in transgenic rice for the same N content. This means that
even if photorespiration is eliminated and if Rubisco content is
optimized for saturating CO2 conditions, the photosynthetic Nuse efficiency is still higher in maize. In addition, since CO2saturated photosynthesis in C3 plants is limited by RuBP-
regeneration capacity, this indicates that RuBP regeneration
capacity is also greater in maize than in rice.
Fig. 3 shows differences in the partitioning of protein-N in
a leaf between maize and rice. The N partitioning into soluble
protein was significantly lower in maize (33%) than in rice
(50%). This was due to a smaller amount of Rubisco in maize
(8.5%). The N costs of PEPC and pyruvate orthophosphate
dikinase (PPDK) were only 2.8 and 1.5%, respectively.
Although the standard error of the ratio of N investment in
PEPC protein was relatively large (2.8±1.2%), this was not due
to scatter of the data. The ratio of PEPC to leaf N strongly
depended on N treatment and increased with increasing leaf-N
content. It was 1.6±0.2% in the 1.0 mM N treatment, 2.2±0.3%
in the 4.0 mM N treatment and 4.1±0.6% in the 12.0 mM N
treatment. A similar response to N treatment has been previously reported by Sugiyama et al. (1984) with maize. However, the ratios of other photosynthetic components to leaf N
were relatively constant irrespective of N treatment (data not
shown). Sage et al. (1987) deduced the N costs of Rubisco and
PEPC in a C4 plant, A. retroflexus, from their measured activities and the mean specific activities, respectively, and reported
that the ratio of N invested in Rubisco ranged from 5 to 9% and
that in PEPC ranged from 2 to 5%. These are close to our values obtained with maize. Although the N costs of other C4
cycle enzymes such as NADP-malic enzyme (NADP-ME),
adenylate kinase and cytosolic carbonic anhydrase are not
known, the fact that the N investment of Rubisco in rice (27%)
was close to that of total soluble protein in maize (33%) suggests that N saving due to the lower amount of Rubisco in C4
plants is not offset by the N cost for the C4 cycle enzymes. In
addition, although it is possible that the N cost for the photorespiratory enzymes is smaller in maize than in rice, the fact that
954
Allocation of protein N in maize and rice
Fig. 3 Allocation of protein-N in young leaves of maize and rice. Rubisco, PEPC and PPDK were determined spectrophotometrically by formamide extraction of Coomassie Brilliant Blue R-250-stained bands on SDS-PAGE. For the CF1/CF0 complex, a and b subunits of CF1 were also
determined by SDS-PAGE and the amount of CF1/CF0 protein complex was estimated by multiplication by 1.65 (Blankenship 2002). For the Cyt
b6/f complex, the Cyt f content was determined spectrophotometrically from the difference between hydroquinone-reduced and the ferricyanideoxidized spectra (Evans and Terashima 1987) and the amount of Cyt b6 /f protein complex was estimated by multiplication by 3.25 (Cramer et al.
1996). The N content of proteins was assumed to be 16% of the mass of proteins. The N contents of PSI, PSII and LHC II complexes were
assumed to be 37, 83.5 and 25.5 mol N mol–1 Chl, respectively (Evans and Seemann 1989). In rice, since the Chl a/b ratio was 2.9±0.1, the ratios
of Chl in PSI, PSII and LHC II were assumed to be 0.308, 0.126 and 0.566, respectively (Leong and Anderson 1984). Ninety percent of Chl b was
assumed to be bound to LHC II complex including its minor proteins. In maize, the amounts of PSI, PSII and LHC II were estimated on the
assumption that the ratio of PSII to LHC II is the same as that in rice. The Chl a/b ratio in maize was 3.3±0.1. Maize was grown with 1.0, 4.0 and
12.0 mM N, and rice was grown with 0.5, 2.0 and 8.0 mM N. The results are the mean and the values in parentheses show standard error (P <0.05,
n = 8–25). The average contents of total leaf N were 90 and 124 mmol N m–2 for maize and rice, respectively.
the investment of N in other soluble proteins did not differ
(20% for maize and 23% for rice) also shows that this is probably not substantial.
By contrast, the N partitioning into insoluble fraction was
appreciably greater in maize (53%) than in rice (37%). This
fraction includes mainly thylakoid-membrane proteins associated with light harvesting, electron transport and photophosphorylation. The total amounts of PSI, PSII, LHC II, CF1/CF0
and Cyt b/f accounted for 34% of leaf N in maize and 24% of
leaf N in rice, respectively. Thus, the greater content of the thylakoid components in maize may contribute to higher capacity
of RuBP regeneration. However, some of these components in
C4 plants are responsible for the energy supply of the C4 cycle.
The total energy required to fix one molecule of CO2 into carbohydrate in C4 plants is theoretically estimated to be three
ATP and two NADPH molecules for RuBP regeneration plus at
least an additional two ATP molecules for the C4 cycles, giving
a total of more than five ATP and two NADPH molecules for
fixation of one molecule of CO2 (Kanai and Edwards 1999).
Thus, the ratio of energy cost for the C4 cycle to RuBP regeneration is about 2 : 3. However, since C4 plants do not require
additional reduction power to drive the C4 cycle, the ratio of the
N cost for the thylakoid components between them is not necessarily 2 : 3. In maize, although oxaloacetate is reduced to
malate by NADPH in the mesophyll chloroplasts, NADPH pro-
duced by ME reaction in the C4 cycle is reused for the Calvin
cycle in the bundle sheath chloroplasts. In addition, a significant cyclic electron flow around PSI is suggested to be driven
in the bundle sheath chloroplasts (Asada et al. 1993, Kubicki et
al. 1996), and the shuttle pathway of PGA and triose-phosphate
operates between the mesophyll and bundle sheath chloroplasts (Hatch 1988). Thus, because of the complexity of the C4
photosynthesis, it is very difficult to distinguish the N cost of
the thylakoid components between the C4 cycle and RuBP
regeneration in the Calvin cycle.
In summary, the N saving due to the lower amount of
Rubisco in maize is not offset by the N cost for the C4 cycle
enzymes, and allows a greater N investment in the thylakoid
components. Since C4 plants have the higher specific activity
form of Rubisco associated with a low affinity for CO2
(Seemann et al. 1984, Sage 2002, Yoeh et al. 1980), a lower
amount of Rubisco is sufficient to achieve high rates of photosynthesis. A greater N investment in the thylakoid components
as well as the CO2 concentrating mechanism may support
higher N use efficiency for photosynthesis in C4 plants.
One approach to improving N use efficiency in crops is to
introduce C4 characteristics into C3 crops by genetic manipulation. The recombinant DNA technology to express high levels
of C4 cycle enzymes at the target locations in C3 crops is
becoming well established (for a review, see Matsuoka et al.
Allocation of protein N in maize and rice
2001). For example, the introduction of the intact maize gene
of the C4 enzymes such as PEPC and PPDK led to high level
expression of C4 enzymes in rice leaves, their expression levels
being comparable to those in the C4 plants (Ku et al. 1999,
Fukayama et al. 2001). In addition, maize NADP-ME located
in the bundle sheath cells could be expressed at high levels in
the mesophyll cells in rice under the control of the rice Cab
promoter (Tsuchida et al. 2001). Such results may lead to the
eventual successful introduction of the complete C4 cycle into
the C3 plants. To improve N-use efficiency of photosynthesis in
C3 crops, however, we must create Kranz leaf anatomy to
obtain an efficient CO2 concentrating mechanism and transport
systems between the mesophyll and bundle sheath cells (Kanai
and Edwards 1999). In addition, our results strongly indicate
that we must establish optimal protein allocation as shown in
Fig. 3, including a lower amount of Rubisco of a type different
from that of C3 plants.
All plants, excluding spinach, were grown hydroponically
in growth chambers at a day/night temperature of 25/20°C, a
photosynthetic photon flux density (PPFD) of 1,000 mmol
quanta m–2 s–1 and a 14-h photoperiod. Spinach was grown at a
day/night temperature of 19/14°C, a PPFD of 900 mmol quanta
m–2 s–1 and a 9-h photoperiod. The hydroponic solution used
has been previously described by Makino and Osmond (1991)
and was continuously aerated. All measurements were made on
young, expanded leaves of 3- to 10-week-old plants. One to
two weeks before measurements, plants were supplied with a
hydroponic solution containing different N concentrations from
0.5 to 12 mM N as previously described (Makino and Osmond
1991). These nutrient solutions were changed every 5 d for
maize and every 7 d for other plants. For maize, to maintain the
pH of the solution during the 5-day culture, 5 mM MES was
added.
Gas exchange was determined with an open gas-exchange
system using a temperature-controlled chamber equipped with
a fan (Makino et al. 1988). A fresh, young leaf blade was
homogenized with a chilled pestle and mortar in 50 mM Naphosphate buffer (pH 7.0) containing 2 mM iodoacetic acid,
120 mM 2-mercaptoethanol and 5% (v/v) glycerol. Total leaf-N
was determined from part of the homogenate before centrifugation (Makino et al. 1988). Total soluble-N and soluble proteinN were determined from the supernatant of the homogenate
after centrifugation. Soluble protein-N was measured using
trichloroacetic acid precipitate of the supernatant. Insoluble-N
was calculated by subtracting soluble-N from total leaf-N.
Trichloroacetic acid soluble-N was calculated by subtracting
soluble protein-N from soluble-N. N content was determined
with Nessler’s reagent after Kjeldahl digestion. The remaining
homogenate was used for the determinations of Chl, Rubisco,
PEPC, PPDK and CF1. Chl content was determined from part
of the homogenate before centrifugation by the method of
Arnon (1949). Rubisco, PEPC and PPDK contents were determined using the homogenate after the addition of Triton X-100
955
(0.1%, final concentration). After this homogenate was centrifuged at 10,000´g for 3 min, the supernatant was treated with
lithium dodecylsulfate (1.0%, w/v) at 100°C for 90 s and analyzed by SDS-PAGE. Rubisco, PEPC and PPDK were determined spectrophotometrically by formamide extraction of the
respective Coomassie-Brilliant-Blue-R-250-stained bands corresponding to 99 kDa for PEPC (Uedan and Sugiyama 1976),
94 kDa for PPDK (Sugiyama 1973), and 52 and 15 kDa for
Rubisco. Whereas the calibration curve for the Rubisco determination was made with the purified Rubisco, those for PEPC
and PPDK were made with BSA because of a large difference
in dye-efficiency among proteins (Makino et al. 1986,
Fukayama et al. 2001). For the determination of CF1 content, a
portion of this homogenate was filtered through four layers of
cheesecloth and centrifuged. After washing the pellet with
50 mM Tris/HCl buffer (pH 7.2), it was treated with lithium
dodecylsulfate (2.5%, w/v) at 100°C for 90 s and analyzed by
SDS-PAGE. CF1 was determined spectrophotometrically at
595 nm by formamide extraction of the respective dye-stained
bands corresponding to 55 and 52 kDa for the CF1 a- and
b-subunits (Blankenship 2002). Bovine serum albumin was
used as the standard. The Cyt f content was determined from
the difference between the hydroquinone-reduced and the ferricyanide-oxidized spectra of the thylakoid fractions solubilized
with 1% (v/v) Triton X-100 in 50 mM MES-NaOH (pH 6.5),
5 mM MgCl2 and 1 mM EDTA according to the method of
Evans and Terashima (1987). The millimolar extinction coefficient used was 20 mM–1 cm–1.
Acknowledgments
This work was supported by a Grant-in-Aid for Scientific
Research from the Ministry of Education, Science, Sports and Culture
of Japan (Nos. 14360036 to A.M.) and by the Bio-Design-Program of
the Ministry of Agriculture, Forestry and Fisheries of Japan (BDP 031-1 to A.M.)
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(Received April 9, 2003; Accepted July 1, 2003)