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First published online January 21, 2005; 10.1104/pp.104.054759 Plant Physiology 137:638-650 (2005) © 2005 American Society of Plant Biologists
Faster Rubisco Is the Key to Superior Nitrogen-Use Efficiency in NADP-Malic Enzyme Relative to NAD-Malic Enzyme C4 Grasses1Molecular Plant Physiology Group (O.G., T.J.A., S.v.C.), Environmental Biology Group (J.R.E.), and Photobioenergetics Group (W.S.C.), Research School of Biological Sciences, Australian National University, Canberra, Australian Capital Territory 2601, Australia; and Centre for Horticulture and Plant Sciences, University of Western Sydney, Penrith South DC, New South Wales 1797, Australia (J.P.C.)
In 27 C4 grasses grown under adequate or deficient nitrogen (N) supplies, N-use efficiency at the photosynthetic (assimilation rate per unit leaf N) and whole-plant (dry mass per total leaf N) level was greater in NADP-malic enzyme (ME) than NAD-ME species. This was due to lower N content in NADP-ME than NAD-ME leaves because neither assimilation rates nor plant dry mass differed significantly between the two C4 subtypes. Relative to NAD-ME, NADP-ME leaves had greater in vivo (assimilation rate per Rubisco catalytic sites) and in vitro Rubisco turnover rates (kcat; 3.8 versus 5.7 s–1 at 25°C). The two parameters were linearly related. In 2 NAD-ME (Panicum miliaceum and Panicum coloratum) and 2 NADP-ME (Sorghum bicolor and Cenchrus ciliaris) grasses, 30% of leaf N was allocated to thylakoids and 5% to 9% to amino acids and nitrate. Soluble protein represented a smaller fraction of leaf N in NADP-ME (41%) than in NAD-ME (53%) leaves, of which Rubisco accounted for one-seventh. Soluble protein averaged 7 and 10 g (mmol chlorophyll)–1 in NADP-ME and NAD-ME leaves, respectively. The majority (65%) of leaf N and chlorophyll was found in the mesophyll of NADP-ME and bundle sheath of NAD-ME leaves. The mesophyll-bundle sheath distribution of functional thylakoid complexes (photosystems I and II and cytochrome f) varied among species, with a tendency to be mostly located in the mesophyll. In conclusion, superior N-use efficiency of NADP-ME relative to NAD-ME grasses was achieved with less leaf N, soluble protein, and Rubisco having a faster kcat.
C4 photosynthesis involves the close collaboration of two photosynthetic cell types, the mesophyll (M) and bundle sheath (BS). A key characteristic of the C4 syndrome is the operation of a CO2 concentrating mechanism, which serves to raise the CO2 concentration in the BS around Rubisco to levels high enough to suppress photorespiration and almost saturate photosynthesis in air (Hatch, 1987  ). This explains the commonly observed high photosynthetic rates of C4 relative to C3 leaves, when comparisons are made under high light and temperature. C4 plants also have greater photosynthetic rates and accumulate more biomass than C3 plants for less leaf nitrogen (N) and Rubisco (Bolton and Brown, 1978; Brown, 1978; Schmitt and Edwards, 1981; Ghannoum et al., 1997; Ghannoum and Conroy, 1998; Makino et al., 2003). The C4 photosynthetic pathway is divided into three biochemical subtypes following the major C4 acid decarboxylation enzyme (NAD-malic enzyme [ME], NADP-ME, and phosphoenolpyruvate carboxykinase; Hatch, 1987). C4 grasses with different biochemical subtypes have characteristic leaf anatomy (Hattersley, 1992) and different geographic distribution according to rainfall, such as seen in Australia (Hattersley, 1992) and South Africa (Ellis et al., 1980). With increasing rainfall, NADP-ME grasses increase in abundance, whereas NAD-ME grasses become less abundant. The aforementioned observations triggered our interest in the comparative physiology of the C4 subtypes, especially because little is understood about the physiological significance of the biochemical diversification of C4 photosynthesis. Consequently, we undertook a number of studies comparing NAD-ME and NADP-ME grasses because they represent the two most contrasting and floristically abundant subtypes (Hattersley, 1992). Restricting our study to two subtypes also allowed us to include more species in our comparisons. Previously, we showed that water stress enhances water use efficiency to a greater extent in NAD-ME than NADP-ME grasses (Ghannoum et al., 2002). While carrying out these experiments, we observed that NADP-ME grasses tended to have a lower leaf N content and greater whole-plant (NUE) and photosynthetic (PNUE) N-use efficiencies than their NAD-ME counterparts.
Differences in PNUE are mainly brought about by differences in photosynthetic capacity or foliar N allocation either within the photosynthetic apparatus or to nonphotosynthetic pools (e.g. cell walls, nitrate; Field and Mooney, 1986
Leaf A, N, PNUE, and NUE (Experiments 1–3) In three separate experiments, different combinations of 13 NAD-ME and 14 NADP-ME C4 grasses were grown under adequate (experiments 1 and 2) and/or deficient (experiment 3) N supplies (Table I). In each case, average PNUE and NUE were significantly greater in NADP-ME than in NAD-ME grasses (Fig. 1, C and D; Table II). This difference was associated with lower leaf N in NADP-ME grasses, whereas average CO2 assimilation rates (A) were similar for the two subtypes (Fig. 1, A and B; Table II). NADP-ME species accumulated more biomass than NAD-ME counterparts in only one out of three experiments (Table II). Low N supply reduced leaf A and N, biomass accumulation, and tillering, whereas it increased PNUE, NUE, and biomass allocation to roots in all species (Fig. 1; Table II). N deficiency affected measured parameters equally in both subtypes (Tables II and III). Whole-plant N concentration per dry mass was not significantly different between the two subtypes. Lower shoot (leaf and stem) N in NADP-ME relative to NAD-ME grasses was counterbalanced by higher root N (Table II). Of all measured parameters, leaf N and PNUE had the most consistent and significant difference, and species values showed the greatest range separation between the two subtypes (Fig. 1; Table II).
Rubisco Amount and Activity (Experiment 3) N deficiency reduced leaf A, chlorophyll (Chl), N, and Rubisco content in seven NAD-ME and seven NADP-ME C4 grasses, and this effect was not significantly different between the two subtypes (Fig. 2; Table III). Leaf N and A as well as leaf N and Rubisco sites were well correlated (r2 between 0.62–0.74) across species and treatments (Fig. 2, A and B). The slopes of the former (A versus N; Fig. 2A) but not the latter (Rubisco versus N; Fig. 2B) relationships were significantly different between the two subtypes (P < 0.05). In vitro Rubisco catalytic turnover rate (kcat) was assayed at 25°C, for better comparison with the literature, and 10 mM NaHCO3 by measuring Rubisco activity and content of catalytic sites on the same extract of leaves harvested under high light. In vitro kcat, thus measured, was well correlated with calculated in vivo kcat at 30°C (A/Rubisco sites; Fig. 2C). kcat values were significantly greater in NADP-ME than in NAD-ME species (Fig. 3; Table IV).
Leaf N Partitioning in the BS and M (Experiment 4) The two NAD-ME species (Panicum miliaceum and Panicum coloratum) allocated relatively more of their leaf N to Rubisco (8%) and other soluble proteins (45%) compared with the two NADP-ME species (Sorghum bicolor and Cenchrus ciliaris; 5% and 36%, respectively; Fig. 4). In the larger survey of 14 C4 grasses, Rubisco N fraction also tended to be slightly larger in the NAD-ME than NADP-ME grasses (Table III). For the 4 grasses, 30% of leaf N was recovered in the thylakoids, 8% in amino acids, and 5% as nitrate. Up to 4% and 17% of total leaf N were unaccounted for in the NAD-ME and NADP-ME leaves, respectively (Fig. 4). About 60% to 67% of total leaf N and Chl were allocated to the BS tissue of NAD-ME species compared with 33% to 38% for NADP-ME species (Table V). This uneven and opposite N and Chl distribution between BS and M tissues was corroborated by the pattern of Chl a autofluorescence (Fig. 5). Most of the Chl a autofluorescence signal came from the BS of the two NAD-ME species (Fig. 5, A and B), whereas the strongest signal emanated from the surrounding M tissue in the two NADP-ME species (Fig. 5, C and D). The distribution of thylakoid N followed that of Chl. About 48% to 60% and 32% to 37% of total thylakoid N were found in the BS of NAD-ME and NADP-ME leaves, respectively (Table V). About 62% and 55% of soluble protein were found in the BS of NAD-ME and NADP-ME leaves, respectively (Fig. 4; Table V). More than 70% of amino acids were found in the M of all 4 species. Nitrate was evenly distributed between the two tissues except in S. bicolor, in which most of it was in the M (Fig. 4; Table V).
Thylakoid N Partitioning in the BS and M (Experiment 4) The content of functional PSII, PSI, and cytochrome (Cyt) f complexes approached 1 µmol m–2 in all 4 C4 grasses, except for a significantly higher PSII content in S. bicolor (Table V). Although thylakoids accounted for a similar fraction of leaf N (approximately 30%) in the four species (P > 0.05), vast differences were found in thylakoid composition between the BS and M (Fig. 6). Relative to M, BS tissues of NAD-ME species had lower functional PSI and PSII reaction centers and Cyt f, all expressed per unit Chl (Fig. 6). Per unit Chl, functional PSI did not differ between M and BS in NADP-ME species, whereas both PSII and Cyt f were lower in the BS (Fig. 6). Diminished PSII activity in BS of NADP-ME leaves resulted in reduced photochemical efficiency (Fv/Fm; Table V). Thylakoid N can be divided into N pools associated either with pigment-protein complexes or with ATP synthesis and electron transport complexes. When expressed on a Chl basis, measured thylakoid N increased linearly with Cyt f content (Fig. 7). Values measured on the C4 grasses here scattered around those reported for C3 leaves. Calculated values were generally less than measured values for the BS tissues (Fig. 7).
N-Use Efficiency and Rubisco in NAD-ME and NADP-ME C4 Grasses
This study was sparked by our observation that C4 grasses belonging to the NADP-ME subtype have higher NUE and PNUE and lower leaf N content than NAD-ME grasses. Since then, we consolidated this finding in 3 separate experiments using various combinations of 27 NAD-ME and NADP-ME grasses grown under adequate and deficient soil N supplies (Fig. 1; Table II). Along the same line, Bowman (1991)
Using four C4 grasses, we found that NAD-ME species invest a greater proportion of leaf N in soluble protein and Rubisco relative to NADP-ME species. In a larger survey, NADP-ME grasses achieved the same photosynthetic rates as NAD-ME counterparts with less leaf N and Rubisco contents. Greater A per Rubisco sites (in vivo kcat) in NADP-ME than in NAD-ME species suggests, among other things, that there is an intrinsic difference in Rubisco kcat between the two subtypes. This was confirmed by in vitro kcat measurements. Under the high light and temperature conditions used during our gas exchange measurements, C4 photosynthesis operates near maximal Rubisco activity. Therefore, the close correlation between Rubisco's in vivo and in vitro kcat indicates that most variations in photosynthetic efficiency per Rubisco and, hence, per leaf N between grasses of the NAD-ME and NADP-ME subtypes are related to differences in Rubisco kcat (Fig. 2C). In accordance with our results, Seemann et al. (1984)
When grown under high light, C3 leaves typically allocate 22% of leaf N to thylakoids and 60% to soluble protein, one-third of which is Rubisco (Evans and Poorter, 2001
The pattern of Chl distribution found in our study agrees with what has been reported for C4 species (Mayne et al., 1975
This discrepancy may be reconciled by recent evidence suggesting that BS thylakoids of NADP-ME species (e.g. maize and S. bicolor) contain incomplete and inactive PSII centers, devoid of the oxygen evolving complex (Meierhoff and Westhoff, 1993
The uneven PSII distribution necessitates a substantial 3-phosphoglycerate/triose phosphate (PGA/TP) shuttle service between the M and BS of NADP-ME and NAD-ME leaves. This is possible because the enzymes for PGA reduction are present in both cell types and subtypes (Hatch and Osmond, 1976
The close match between measured and calculated thylakoid N contents (Fig. 7) suggests that N costs derived from C3 plants are appropriate for C4 plants. This is surprising given the differences in energetic requirements between the M and BS and the C3 and C4 cycles. The N cost of 8.85 mol N (mol Cyt f)–1 suggested by Evans and Seemann (1989)
In summary, NADP-ME grasses achieved similar photosynthetic capacity to NAD-ME counterparts with less leaf N and Rubisco having higher kcat. Compared to NADP-ME, NAD-ME leaves allocate a greater fraction of leaf N to soluble protein and a similar fraction to thylakoids. Although the majority of leaf Chl and N were found in the BS of NAD-ME and M of NADP-ME grasses, the distribution of thylakoid complexes was species specific.
This study reports on four experiments (Table I). Experiments 1, 2 (related to Ghannoum et al., 2001 , 2002), and 3 were used for NUE and A/N calculations. Experiment 3 was also used for Rubisco activity assays. Experiment 4 was used for N budget analysis.
Soil was supplemented with basal nutrients (excluding N) and added to 5- to 10-L pots (Ghannoum and Conroy, 1998
Seeds for two NAD-ME (Panicum miliaceum and Panicum coloratum) and 2 NADP-ME (Sorghum bicolor and Cenchrus ciliaris) C4 grasses were sown directly in 4-L pots containing sterilized garden soil supplemented with 4 g of a controlled release fertilizer (15/4.8/10.8/1.2 nitrogen/phosphorus/potassium/magnesium plus trace elements [boron, copper, iron, manganese, molybdenum, and zinc]; Osmocot Plus; Scotts, Baulkam Hills, Australia). Plants were grown in controlled environment chambers (Phoenix, Adelaide, Australia) lit for 9 h with metal halide lamps supplying 800 µmol quanta m–2 s–1 followed by 1 h of incandescent lighting. Air temperature and relative humidity were maintained at 28/24°C and 60/80% day/night, respectively. Plants were watered daily and used for analysis 4 weeks after germination.
Plants were harvested 5 to 7 weeks after germination and separated into leaves, stems (including sheaths), and roots. Leaf area was determined by a digital image analyzer (Delta-T, Cambridge, UK). Roots were washed free of soil. Harvested samples were oven-dried at 80°C, weighed, and then ground to powder. Percentage of N was determined on the ground tissues using a flash combustion CNS analyzer (Fison NA1500; Fison Instruments, Milan, Italy). NUE was calculated as the ratio of plant dry mass to total leaf N content at harvest.
Measurements were made on the youngest fully expanded leaves 1 week before harvest using a portable photosynthesis system (LI-6400; LI-COR, Lincoln, NE), at a photosynthetic photon flux density of 1,500 (experiments 1 and 2) and 1,800 (experiments 3 and 4) µmol m–2 s–1 supplied by an in-built red/blue LED light source, a CO2 partial pressure of 380 µbar, leaf temperature of 30°C, and leaf-to-air vapor pressure difference between 1.5 to 2.0 kPa. Dark respiration (Rd) was measured after 30 min of dark adaptation, before the light was turned on. In experiment 2, the response of A to step increases of intercellular CO2 (Ci) was measured. A/Ci curves were fitted using the C4 photosynthesis model of von Caemmerer (2000)
The four grass species (Table I) were chosen based on their ability to produce highly pure BS strands by mechanical blending as checked under a light microscope (Agostino et al., 1989
Leaf sections (1–2 cm2) or BS preparations (100 nmol Chl) were extracted in 1 mL of ice-cold buffer (50 mM EPPS-NaOH, 5 mM DTT, 15 mM NaHCO3, 20 mM MgCl2, 2 mM EDTA, 4% protease inhibitor cocktail [Sigma, St. Louis], 0.1% [w/v] polyvinylpolypyrrolidone, pH 8.0) and with or without 0.05% Triton X-100 using a 2-mL Potter-Elvehjem glass homogenizer kept on ice. Subsamples were taken from the crude homogenate for Chl determination in 80% acetone (Porra et al., 1989
Leaf sections or BS preparations were extracted in a 7-mL Potter-Elvehjem glass homogenizer in ice-cold extraction buffer (50 mM Na-PO4, 0.33 M sorbitol, 2 mM DTT, 5 mM MgCl2, 2 mM EDTA, pH 6.5). Several extractions were carried out and pooled. The extracts were filtered as described above. The filtrate was centrifuged for 1 min at 1,000g and 4°C. The pellet, enriched in tissue debris and starch, was discarded. The supernatant was centrifuged for 4 min at 2,000g. The pellet was gently suspended and centrifuged twice in 40 mL of extraction buffer before being incubated for 5 min on ice in lysis buffer (extraction buffer devoid of sorbitol), then centrifuged. The pellet was finally washed, suspended in extraction buffer, snap frozen in liquid N2, then stored at –80°C until used for PSI, Cyt f, or total N analysis. PSI was calculated as the amount of P700 using the absorbance change at 702 nm induced by flashes of blue-green light, after correcting for fluorescence (Evans, 1987
Functional PSII centers of leaf and BS tissue were quantified by the O2 yield at 1% CO2 and repetitive flashes at 10 Hz, with continuous background far-red light (Chow et al., 1989
Total leaf N was determined on oven-dried, ground leaf sections taken from the same or matching leaves used for various analyses. BS fractions taken after Rubisco determination were oven-dried in preweighed tubes, weighed, then a subsample analyzed for total percentage of N. Similar results were obtained whether fractions were washed in buffer or distilled water before drying. To obtain pure thylakoids for N analysis, crude thylakoid preparations (0.5–1.0 µmol Chl) were layered over a centrifuge tube containing 30% Percol in washing buffer (25 mM Na-PO4, 5 mM MgCl2, pH 6.5) and centrifuged at 2,000g for 4 min and 4°C. The pure thylakoid bands situated about 1 cm from the top were sucked out and washed twice with the same washing buffer, then suspended in distilled water. Subsamples with known Chl content were dried in tin cups at 80°C then analyzed for percentage of N.
Freshly hand cut, leaf cross sections were stained with 0.01 mg mL–1 propidium iodide to highlight cell walls, then mounted on a scanning confocal microscope (Leica SP2 LSCM; Leica Microsystems, Wetzlar, Germany). Sections were excited with weak laser beams at 488 nm for autofluorescence and 543 nm for the stain. Emission was collected between 690 to 740 nm and 550 to 620 nm for Chl a autofluorescence and the stain, respectively.
Leaf parameters were measured on area, Chl, and/or Rubisco basis. BS parameters were measured on a Chl and/or Rubisco basis. BS parameters (P) were converted to leaf area basis using the following formula (Rubisco exclusively located in BS):
and Hikosaka and Terashima (1995) from the following equation: T = [PSII] x 83.3 x 0.06 + [PSI] x 32.8 x 0.184 + [LHC] x 26 x 0.013 + [Cyt f] x 8.85, where [LHC] = (1,000 – [PSII] x 60 – [PSI] x 184)/13. [PSII], [PSI], [LHC], and [Cyt f] have the units mmol (mol Chl)–1. The pigment protein complexes have N costs of 83.3, 32.8, and 26 mol N (mol Chl)–1 and bind 60, 184, and 13 mol Chl (mol complex)–1 for PSII, PSI, and LHC, respectively. The N cost associated with Cyt f was 8.85 mol N (mol Cyt f)–1. The subtype effect (experiments 1 and 2) was calculated by two-way ANOVA (nested design, species nested in subtype) using a general linear model. In experiment 3, a three-way, nested ANOVA was used. Species and fraction effects (experiment 4) were analyzed by one-way ANOVA. For data presented in Tables II and V, a posthoc, Tukey HSD test was carried out on the grouped means.
From the Research School of Biological Sciences (Australian National University), we acknowledge the assistance of Sue Lyons with plant culture; Sue Wood with N analysis; Stephanie McCaffery with NO3– and Cyt f assays; and Heather Kane, Spencer Whitney, and Murray Badger for general technical advice. From Plant Industry (CSIRO), thanks are due to Colin Jenkins, Bob Furbank, and Rosemary White for help with BS separation and Chl autofluorescence. Received October 12, 2004; returned for revision November 25, 2004; accepted November 29, 2004.
1 This work was supported by the Australian Research Council (postdoctoral fellowship to O.G., grant no. F00104004).  Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.054759. * Corresponding author; e-mail ghannoum{at}rsbs.anu.edu.au; fax 61–2–6125–5075.
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ABSTRACT
RESULTS
) and significance levels for the subtype effect calculated as described in "Materials and Methods" are shown and are: *, P < 0.05; **, P < 0.01; ***, P < 0.001; and ns, not significant (P 
0.05). HN, High N soil supply; LN, low N soil supply.
) and 7 NADP-ME (
, 
) C4 grasses grown under high (
) or BS (
). Half-filled symbols represent thylakoid N cost calculated from the contents of functional PSII, PSI, and Cyt f for each species and fraction. Open symbols denote thylakoids prepared from C3 leaves (spinach [Terashima and Evans, 1988
