The Nitrogen Use Efficiency of C3 and C4 PlantsII. LEAF NITROGEN EFFECTS ON THE GAS EXCHANGE CHARACTERISTICS OF CHENOPODIUMALBUM (L.) AND AMARANTHUS RETROFLEXUS (L.)
Received for publication December 29, 1986 and in revised form April 7, 1987
ROWAN F SAGE'* AND ROBERT W. PEARCYDepartment ofBotany, University ofCalifornia, Davis, California 95616
ABSTRACr
The effect of leaf nitrogen (N) on the photosynthetic capacity and thelight and temperature response of photosynthesis was studied in theecologically similar annuals Chenopodium album (C3) and Amaranthusretropxus (C4). Photosynthesis was linearly dependent on leaf N perunit area (N.) in both species. A. retroflexus exhibited a greater depend-ence of photosynthesis on N. than C. albxm and at any given N. it hada greater light saturated photosynthesis rate than C. album. The differ-ence between the species became Lrger as N. increased. These resultsdemonstrate a greater photosynthetic N use efficiency in A. retroJ'exusthan C. album. However, at a given applied N level, C. album allocatedmore N to a unit of leaf area so that photosynthetic rates were similar inthe two species. Leaf conductance to water vapor increased linearly withN. in both species, but at a given photosynthetic rate, leaf conductancewas higher in C. album. Thus, A. retroJiexus had a greater water useefficiency than C. album. Water use efficiency was independent of leafN in C. album, but declined with decreasing N in A. retroflexus.
The photosynthetic rate per unit of N2 is usually higher in C4than C3 plants (4, 18). This is believed to result from the CO2concentrating mechanism of C4 plants leading to CO2 saturationof rubisco. Consequently, less of this enzyme is required for highrates of photosynthesis in C4 than C3 plants (18, 24). C4 grassesgenerally have greater photosynthetic rates per unit ofN than C3grasses and dicots (3, 5, 24, 29) as well as greater growth and leafexpansion rates per unit N (22, 27, 28). However, exceptionshave been noted (5) and the NUE differences ofC3 and C4 dicotshave not been directly compared.The relationship between PNUE and photosynthetic capacity
is unclear. On the one hand, plants with a greater PNUE mayhave similar N. and therefore greater photosynthetic capacitiesthan less efficient plants. However, as photosynthetic capacityincreases, sink capacity and external environmental constraintsmay lead to a reduction of carbon fixation per unit ofN invest-ment (14, 17). Alternatively, more efficient plants may investlessN per unit area, and proportionally moreN to the production
'Present address: Biological Sciences Center, Desert Research Insti-tute, P.O. Box 60220, Reno, NV 89506
2 Abbreviations: N, nitrogen; A, net CO2 assimilation rate; C,, ambientCO2 partial pressure; Cs, intercellular CO2 partial pressure; g, leaf con-ductance to water vapor, N., organic nitrogen per unit area; NUE,nitrogen use efficiency; PFD, photon flux density; PNUE, photosyntheticnitrogen use efficiency; rubisco, RuBP carboxylase/oxygenase (EC4.1.1.39); VPD, leaf-to-air vapor pressure deficit; WUE, water use effi-ciency.
of new leaf area. Leaf area production is often a better predictorof growth than photosynthetic capacity per unit area or netassimilation rate (20). As N is required for both production ofnew leaf area and for increasing photosynthetic capacity, theenhancement ofone under limitingN could come at the expenseof the other.
In this research, we have compared the N response of photo-synthetic nitrogen use efficiency ofthe ecologically similar weedsC. album (C3) and A. retroflexus (C4). LeafN effects on the lightand temperature dependence of photosynthesis, leaf conduct-ance, and water use efficiency of the two species were alsocompared. In an accompanying report (22). we show that whengrown over a range of N nutrition, A. retroflexus had a lowermaximum and minimum leaf N content per unit area than C.album, yet an equivalent or higher growth rate and leaf areapartitioning coefficient. The research reported here was designedto examine in more detail the physiological basis of the differ-ences in the response to N.
MATERIALS AND METHODSGrowth Conditions. C. album and A. retroflexus plants were
grown in a growth chamber at 27/23C day/night temperaturesand a PFD of 600 umol m 2 s-'. Plants were grown in equalvolumes of sand, vermiculite and perlite. Plants with differentleafN contents were obtained by watering the species with a 0.5or 0.75 mm N Johnson-Hoagland's solution modified to contain12, 8, 6, 4, 3, 2, 1.5, 0.5, or 0.15 mM N in a 7:1 NO3 :NH,'ratio. The concentration of K, P, Ca, and Mg, and the micro-nutrients were identical in all treatment solutions. In the Ndeficient solutions, SO4-2 and Cl- were used to replace NO3-.Gas Exchange Measurements. A, g, and Cs were determined
on fully expanded leaves with no visible signs of senescence onthe main shoot of 2 to 4 week old plants.The gas-exchange apparatus used in these measurements has
been previously described (9) and was modified as follows. Airof known water vapor and CO2 partial pressures was obtainedby mixing air containing 4% CO2 with CO2-free air using twoWostoff precision mixing pumps (models M201 and G-27, Bo-chum, FRG) connected in series. Water vapor pressure enteringthe leaf chamber was controlled by first humidifying the air andthen partially dehumidifying it in a glass condensing columnwhose temperature was controlled by circulating water from athermostated water bath. The leaf chamber was based on thedesign of Pearcy and Calkin (19), but enlarged to 10 cm by 20cm. Air within the chamber was circulated by two Micronel fans(Micronel, Vista, CA). Chamber temperature was controlled bycirculating water from a second thermostated bath through aheat exchange block mounted on the chamber.
In all gas exchange measurements, the leafto air vapor pressuredifference and C02 partial pressure were maintained at 5 to 11mbar and 325 to 345 Abar, respectively. Measurements were
959 www.plantphysiol.orgon July 31, 2020 - Published by Downloaded from
made of (1) the light saturated CO2 assimilation rate at 20, 27,and 34°C (any given leaf was measured at only one of thesetemperatures), (b) the light response of photosynthesis, and (c)the temperature response of photosynthesis. To begin each ex-periment, single leaves were inserted in the chamber and exposedto about 750 ,mol photons m 2 s-'. After 10 to 15 min, the PFDwas increased to a level which saturated photosynthesis (typically1200 to 2000 ,umol m-2 s-', depending upon Na) and after a 30minute equilibration period, light saturated A was recorded. Thelight response of photosynthesis was determined by decreasingthe PFD in steps to darkness. The temperature response wasdetermined by beginning the measurements at 20°C and saturat-ing PFD. Temperatures were first decreased to the lowest values,and then increased in steps to about 40°C.
Following the gas exchange measurements, the leaves weredried at 70°C and weighed. Total N and NO3 were then deter-mined using a micro-Kjeldahl procedure and high-pressure liquidchromotography, respectively (22). The difference between totalleafN and leafNO3 was taken as organic N.
All gas exchange parameters were calculated using the equa-tions presented in Von Caemmerer and Farquhar (26).
RESULTS
Assimilation Rate versus Nitrogen Content. Light saturatedCO2 assimilation increased linearly with Na in both C. albumand A. retroflexus (Fig. 1). Regressions for both species hadsimilar x-intercepts which generally ranged from 46 to 56 mmolm-2, but A increased with increasing Na more strongly in A.retroflexus than C. album at all three measurement temperatures(Table I). Consequently, at equal Na, A. retroflexus generally hada greater A than C. album (Fig. 2) and this difference increasedas A and Na increased. However, C. album achieved a higher Naat a given applied N and therefore had a similar A as that of A.retroflexus at 27°C, the growth temperature.A/Na increased curvilinearly with Na (Fig. 2) since transfor-
mation of the linear equationA = dA/dNa(Na)+b (1)
into the form
A/Na = dA/dNa + b/Na (2)gives a curvilinear function when the x-intercept is positive andb, the y-intercept, is negative. At high Na, the value of A/Naapproaches that of dA/dNa. In general, A/Na was greater in A.retroflexus than C. album, with the differences increasing astemperature increased. However, at 20°C measurement temper-ature and in leaves with low Na, there was little difference in A/Na between the species (Fig. 2).
Light and Temperature Dependence of Photosynthesis. In bothspecies, the light response curves measured at 27°C were essen-tially identical in leaves with equivalent photosynthetic capacities
60
E 50 200C 270CE / 0 00/00
40-. A ~
30E ~0030 9££0 0/9
0 to0 o0 ~ ~ 1 00
E 0~~~~~~~~~~N io-otii
(Fig. 3). However, C. album required about 40% more Na inorder to accomplish this. The light required for saturation in-creased with increasing Na in both species. At a given Na, A.retroflexus had a higher light saturation point than C. album.When measured at 540 ,mol photons m-2 s-', which was
equivalent to the PFD in the growth chamber, A still increasedlinearly with increasing Na in both species (Fig. 4). However, theslope was much lower than at light saturation. Linearity ofA onNa was maintained because the decrease in photosynthesis fromlight saturation to 540 Mmol m-2 S-2 was proportional to Na.The temperature dependence ofphotosynthesis in both species
was more pronounced in high as compared to low N plants (Fig.5). The optimum temperature of photosynthesis was higher inA. retroflexus than in C. album but was little affected by Na.Because of the differences in the temperature dependence ofassimilation in the two species, A/Na changed only slightly withtemperature in C. album while it increased substantially withincreased temperature in A. retroflexus (Fig. 2). The maximumA/N values at the respective temperature optima for each specieswere 0.21 ,umol CO2 s-' mmol-' N in C. album and 0.40 Mmols-' mmol-' in A. retroflexus. However, at measurement temper-atures below 20aC, A/Na was greater in C. album than A. retro-flexus.
Leaf Conductance. Leaf conductance to water vapor (g) waspositively correlated with A in both species (Fig. 6). Temperaturehad little effect on the slope of this relationship, especially in A.retroflexus. At the highest Na, g was 2 to 2.5 times greater in C.album than A. retroflexus while at the lowest Na, g was similarin the two species. Because the relationship between A and Naand g and A were linear, g versus Na was also linear in bothspecies (data not shown).The ratio of intracellular to ambient CO2 partial pressure (Ci/
Ca) was independent of Na in C. album, but inversely related toNa in A. retroflexus (Fig. 7). Consequently, at low Na both specieshad similar Ci/Ca values. Since at a given VPD, the WUE of aleaf is inversely related to Ci/Ca (13), WUE ofA. retroflexus wasdependent on Na, ranging from a high of about 12 ,umol CO2mmol-' H20 at high Na to a low of about 3 umol mmol-' at lowNa (Fig. 8). In contrast, WUE was independent of Na in C.album, averaging 4.3 rmol mmol'.
DISCUSSIONAt identical Na, the photosynthetic capacity of A. retroflexus
was greater than that of C. album. However, for a given appliedN level, C. album had a greater Na than A. retroflexus so that theactual light saturated assimilation capacities were similar in thetwo species. A comparison of Na and photosynthesis of A.retroflexus and C. album in fields near Davis, California yieldedsimilar results (21). These results show that C4 photosynthesisdoes not automatically enable C4 plants to have a greater pho-tosynthetic capacity than found in C3 plants, because differencesin the amount of N allocated to leaves can offset advantages
&
34°C lA
£ 0
- * /R ° ° °/ FIG. 1. The relationship between.d0 light saturated photosynthetic rate of
I/O - single leaves and organic leaf nitrogen£ 0/0 in C. album (dashed line, 0) and A.
- * OO - retroflexus (solid line, A). See Table I/ov00o for the regression equations. All re-
FIG. 2. The relationship between photosynthesis per unit nitrogenand organic leaf nitrogen in C. album (dotted, dashed lines) and A.retroflexus (solid lines). The relationships were obtained by transformingthe linear regression equations of A versus Na in Table I into the formA/N = dA/dN. + b/Na.
' ' ' ' 2225
A*-- A. retroflexusAO C. album 12
'=40tzE
~~~~~~~~~~~~~~161E 25°
IF ~~~~~~~~~~~~~~105
a 101
54
-5 . .I0 500 1000 1500 2000
PFD, MmoI m-2 s-1FIG. 3. The light response of photosynthesis in C. album (open sym-
bols) and A. retroflexus (closed symbols) at 27°C. The values beside eachcurve represent organic leaf nitrogen contents in mmol m-2.
resulting from a higher PNUE. However, the greater N cost ofphotosynthesis in C3 plants may limit allocation of as much Nto other plant processes, such as root or leaf production, as couldbe possible for C4 plants. As discussed elsewhere (22), C4 plantsmay be able to invest more N into new leaf production than C3plants and therefore have a greater whole plant carbon gain andgrowth rate at high N.
,27-C
NE-5
E
:._Cv
0)
3'
2'
0 60 120 180 240 0 60 120Leaf Nitrogen, mmol m 2
180 240
FIG. 4. The relationship between single leaf photosynthesis at a PFDof 540 Mmol m-2 s-' and organic leaf nitrogen in C. album (0) and A.retroflexus (A) at 27'C and 34°C. The regression equations are: y =
0.082x + 4.9 (R2 = 0.81) for C. album at 27°C, y = 0.058x + 4.1 (R2 =0.92) for C. album at 34°C, y = 0.151x - 0.23 (R2 = 0.74) for A.retroflexus at 27°C, and y = 0. 141x + 1.73 (R2 = 0.84) for A. retroflexusat 340C.
m
E
E
C
0
EIn
6
51
41
3
2
0 10 20 30 40 0 10 20 30 40Leaf Temperature,0C
FIG. 5. The temperature of photosynthesis in C. album and A. retro-flexus at light saturation. The values beside each curve represent organicleaf nitrogen content in mmol m-2.
Most workers have used A/N as an index of PNUE (1, 4, 12).With this index, most C4 plants, including A. retroflexus, gener-ally have a greater PNUE than similar C3 plants (3-5, 12, 24,29). However, comparisons of PNUE based on A/N may bedifficult to interpret if the x-intercept ofA versus Na is unknown.As shown by Eq. 2, A/N is dependent on Na, so that comparisonsbetween species with different Na may lead to erroneous assess-ments ofPNUE. This problem can be seen ifA. retroflexus leaveswith low Na are compared with C. album leaves with high Na. Inaddition, A/N at equivalent Na will vary if the x-intercept ofAversus Na differs significantly. This intercept can range from near0 to 60 mmol m-2 for different species (8, 10, 15, 16, 30). Adifferent measure of PNUE is the slope ofA versus Na, dA/dNa,which gives the increase in assimilation capacity per unit increasein N investment. Because dA/dNa is independent of Na when Aversus Na is linear, PNUE comparisons between species withdifferent Na can be facilitated. However, species with different x-intercepts can have identical slopes, in which case the plant withthe lower x-intercept has a greater A/N. Because of these prob-lems, it is probably best to utilize both A/Na and dA/dNa instudies ofPNUE differences.As with A/N, the value of dA/dNa tends to be larger in C4
plants than similar C3 plants. Values of dA/dNa as large as 0.68,gmol s-' mmol' have been measured in C4 plants (21). In C3annuals, dA/dNa typically ranges from 0.2 to 0.3 gmol s-'mmoli' (8, 10, 16, 30). High growth rate annuals show the
FIG. 6. The relationship betweenleaf conductance to water vaporand photosynthesis in single leavesof C. album (dashed lines, 0) andA. retroflexus (solid lines, A). Alltrends are significant at P = 0.01.
0 10 20 30 40 50 60
Assimilation, ,Mmol m 2 s-
a
C.)
1.0 I II1 £ - 0 0a
0.8 . S , D%£ £ n£0
U ~~~~~~02
0.6 4 '
0.4-
0.2 C. fbum AretrofiexusA 20C A 20C0 27C * 27C0 34 C 0 34 C
0.0 I.10 60 120 180 240
Leaf nitrogen, mmol m 2
FIG. 7. The ratio of intercellular to ambient CO2 partial pressure (CJ/C.) versus organic leaf nitrogen in C. album and A. retroflexus. Theregression equation for the significant trend (P = 0.01) in A. retroflexuswas y = -0.00233x + 0.872 (R12 = 0.39).
. c.
EE
.3E;
3:J
0 60 120 180 240Leaf nitrogen, mmol m 2
FiG. 8. The relationship between water use efficiency and leaf nitro-gen per unit area in C. album (open symbols) and A. retroflexus (closedsymbols), assuming a VPD of 10 mbar. Symbol legends are the same asin Figure 7. The regression equation for the response in A. retroflexuswas y = 0.0505x + 2.61 (R2 = 0.38; significant at P = 0.01).
greatest response ofA to Na, deciduous trees and shrubs have anintermediate response, and evergreen species have a low response(12). Similarly, in plants-adapted to high nutrient availability, Aresponds strongly to increasing N while in plants adapted to lownutrient availability, A does not respond strongly to increasingN (21). Because of this, it is important that comparisons of C3and C4 plants be made using species with similar growth forms
and ecological requirements. Low growth capacity C4 plants mayhave a lower PNUE than high growth capacity C3 plants. How-ever, low growth capacity C4 plants probably have a greaterPNUE than similar, low growth capacity C3 plants.
It has been reported that A versus Na is curvilinear when a
sufficiently broad range of Na is examined (10). While studieshave reported curvilinearity between A and Na (10, 16), whenthe measurements are conducted on plants ofsimilar age, growthconditions, and variety, and N storage forms such as NO3- andasparagine are accounted for, A versus Na is usually linear acrossthe entire range of Na (8, 15, 21, 30). In C.-album and A.retroflexus, failure to account for stored NO3- would have re-sulted in a curvilinear relationship betweenA and Na. Ultimately,however, at very high N levels, the A to N. relationship shouldbecome curvilinear because of other limitations imposed onphotosynthesis (1 1). Evans (10), presents evidence that a 'wallresistance' to CO2 diffusion may become significant at high N,resulting in curvilinearity between A and Na. In this study, thelinear response may result from our accounting for NO3- accu-mulation as well as a regulation ofthe maximum Na below levelswhere A versus Na becomes curvilinear.According to Mooney and Gulmon (17), an optimal N allo-
cation exists when leaf N is modulated so that the resultingphotosynthetic rate corresponds to the maximum rate which themost limiting environmental resource can support. By this ar-gument, the leaf N of C. album and A. retroflexus should beallocated so that the corresponding light saturation point occursat about the growth PFD of 600 Mmol m-2 s-1. In C. album thiswould mean an A of 18 to 24 Umol m-2 s-' and a maximum Naof 120 to 150 mmol m-2. That A is double this suggests that leafN and photosynthesis capacity is determined by factors otherthan simply instantaneous or average PFD. Data of Chabot (7)and Bunce (6), indicate leafdevelopment responds more to dailyintegrated PFD, rather than a high instantaneous PFD. The dailyPFD in our chamber was 34 mol m2 d-', which is about 70%of the typical daily PFD on a sunny day (2). This level may behigh enough to stimulate leaf development in C. album and A.retroflexus similar to that found in natural, high light environ-ments.While dAidNa is an index to PNUE, the slope ofg versusA is
inversely related to leaf water use efficiency (25). In C4 ascompared to C3 plants dg/dA is smaller while dA/dNa is greater.In plants which are not photosynthetically CO2 saturated, PNUEis inversely related to WUE (13). This is because a change in dg/dA can change C. and therefore A without any change in Na.However, WUE is not necessarily inversely related to PNUE. Ifg adjusts proportionally to A, an increase in dA/dNa can raisephotosynthetic capacity, but C and WUE may be unchanged.This was evident in A. retroflexus, where dA/dNa increasedsubstantially with temperature while dg/dA remained constant.
962
E
E
EE;0
ca.O-
0
0
0
Si
I ; s , i bun nun
12£
9 £~~~~~~~~~~
3 ou.°.°. . 4. 0g.0 £000O 0
A 0 A lb3 *. OAO£££0£~~0& A co 2. 0 AO
0 0
0 0
n
I I I . . . I I I I I 9I I I I I I Is s EI I I I I I lI
PHOTOSYNTHETIC NITROGEN USE EFFICIENCY OF C3 AND C4 PLANTS
Thus, leaf temperature at a constant VPD had little affect onWUE in A. retroflexus (Fig. 8).
In both C. album and A. retroflexus, biochemical rather thanstomatal limitations account for the decline in photosynthesiswith leaf N, since Ci/Ca either increased or was unaffected by Na.A similar conclusion regarding the importance of biochemicallimitations was reached with studies of other C3 and C4 specieswhere A was changed by limiting nitrogen, leaf age, phosphorus,or growth light level (25).Few studies have addressed the question of how the environ-
ment influences dA/dNa. In the short term, it is clear that changesin the environment which reduce photosynthetic rate also reduced4/dNa. However, in the long term, where changes in photosyn-thetic capacity are involved, it is unclear whether changes in theenvironment can cause a change in d4/dNa, or simply alter theNa while keeping dA/dNa constant. Some evidence indicates thelatter possibility (23). Acclimation responses to light, temperatureand water stress may involve a repartitioning of leaf N amongphotosynthetic components such that the component most lim-ited by the environment will be proportionally increased relativeto less limited components. How these changes in N partitioningwith leaf N will affect the A versus N response is unknown.
Acknowledgments-We thank T. M. DeJong and R. C. Huffaker for their helpfulcomments on this work and the Jastro-Shields foundation for financial assistance.
LITERATURE CITED
1. BARUCH Z, LUDLOW MM, R DAVIS 1985 Photosynthetic responses of nativeand introduced C4 grasses from Venezuelan savannas. Oecologia 67: 388-393
2. BJORKMAN, 0 1981 Responses to different quantum flux densities. In 0 Lange,P Nobel, C Osmond, and H Ziegler, eds. Encyclopedia of Plant Physiology(New Series), Vol 12A. Springer-Verlag, Berlin, pp 57-107
3. BOLTON JK, RH BROWN 1980 Photosynthesis of grass species differing incarbon dioxide fixation pathways. V. Response of Panicum maximum,Panicum milioides and tall fescue (Festuca arundinacea) to nitrogen nutri-tion. Plant Physiol 66: 97-100
4. BROWN RH 1978 A difference in N use efficiency in C3 and C4 plants and itsimplications in adaptation and evolution. Crop Sci 18: 93-98
5. BROWN RH, JR WILSON 1983 Nitrogen response of Panicum species differingin CO2 fixation pathways. II. CO2 exchange characteristics. Crop Sci. 23:1154-1159
6. BUNCE JA 1983 Photosynthesis characteristics of leaves developed at differentirradiances and temperatures: an extension of the current hypothesis. Pho-tosyn Res 4: 87-97
7. CHABOT B 1979 Influence of instantaneous and integrated light-flux densityon leaf anatomy and photosynthesis. Am J Bot 66: 940-945
8. DEJONG TM 1982 Leaf nitrogen content and CO2 assimilation capacity inpeach. J Am Soc Hort Sci 107: 955-959
9. DEJONG TM, BG DRAKE, RW PEARCY 1982 Gas exchange characteristics ofChesapeake Bay tidal marsh species under field and laboratory conditions.Oecologia 52: 5-11
10. EVANS JR 1983 Nitrogen and photosynthesis in the flag leafofwheat (Triticumaestivum L.). Plant Physiol 72: 297-302
11. FARQUHAR GD, MUF KIRSCHBAUM 1985 Environmental constraints on car-bon assimilation. In A. Hawkins, ed, The Regulation of Sources and Sinksin Crop Plants. British Plant Growth Regulator Group Monograph 12, pp87-97
12. FIELD C, HA MOONEY 1986 The photosynthesis-nitrogen relationship in wildplants. In TA Givinish, ed, On the Economy of Plant Form and Function.Cambridge University Press, London, pp 25-55
13. FIELD C, J MERINO, HA MOONEY 1983 Compromises between water-useefficiency and nitrogen-use efficiency in five species of California evergreens.Oecologia 60: 384-389
14. HEROLD A 1980 Regulation of photosynthesis by sink activity- the missinglink. New Phytol 86: 131-144
15. Hunt ER, Jr, JA Weber, DM Gates 1985 Effects of nitrate application onAmaranthus Powellii, Wat. III. Optimal allocation of leaf nitrogen forphotosynthesis and stomatal conductance. Plant Physiol 79: 619-624
16. LUGG DG, TR SINCLAIR 1981 Seasonal changes in photosynthesis of field-grown soybean leaflets. 2. Relation to nitrogen content. Photosynthetica 15:138-144
17. Mooney HA, SL Gulmon 1982 Constraints on leaf structure and function inreference to herbivory. Bioscience 32: 198-206
18. OSMOND CB, K WINTER, H ZIEGLER 1982 Functional significance of differentpathways ofCO2 fixation in photosynthesis. In 0 Lange, P Nobel, C Osmond,H Ziegler, eds, Encyclopedia of Plant Physiology (New Series), Vol 12B.Springer-Verlag, Berlin, pp 479-547
19. PEARCY RW, HW CALKIN 1983 Carbon dioxide exchange of C3 and C4 treespecies in the understory of a Hawaiian forest. Oecologia 58: 26-32
20. POTTER JR, JW JONES 1977 Leaf area partitioning as an important factor ingrowth. Plant Physiol 59: 10-14
21. SAGE RF 1986 Photosynthesis and nitrogen use efficiency of C3 and C4 plants.PhD thesis, University of California, Davis
22. SAGE RF, RW PEARCY 1987 The nitrogen use efficiency of C3 and C4 plants.I. Leaf nitrogen, growth, and biomass partitioning in Chenopodium album(L.) and Amaranthus retroflexus (L.). Plant Physiol 84: 954-958
23. SEEMANN JR, TD SHARKEY, J WANG, CB OSMOND 1987 Environmental effectson photosynthesis, nitrogen-use-efficiency and metabolite pools in leaves ofsun and shade plants. Plant Physiol. 84: 796-802
24. ScHMIrr MR, GE EDWARDS 1981 Photosynthetic capacity and nitrogen useefficiency of maize, wheat, and rice: a comparison between C3 and C4photosynthesis. J Exp Bot 32: 459-466
25. SCHULZE ED, AE HALL 1982 Stomatal responses, water loss and CO2 assimi-lation rates of plants in contrasting environments. In 0 Lange, P Nobel, COsmond, H Ziegler, eds, Encyclopedia of Plant Physiology (New Series), Vol12B. Springer-Verlag, Berlin, pp 181-230
26. VON CAEMMERER S, GD FARQUHAR 1981 Some relationships between thebiochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376-387
27. WILSON JR 1975 Comparative response to nitrogen deficiency of a tropicaland temperate grass in the interrelation between photosynthesis, growth andthe accumulation of non-structural carbohydrate. Neth J Agric Sci 23: 104-112
28. WILSON JR, RH BROWN 1983 Nitrogen response of Panicum species differingin CO2 fixation pathways. I. Growth analysis and carbohydrate accumula-tion. Crop Sci 23: 1148-1153
29. WONG SC 1979 Elevated atmospheric partial pressure ofCO2 and plant growth.I. Interactions of nitrogen nutrition and photosynthetic capacity in C3 andC4 plants. Oecologia 44: 68-74
30. YOSHIDA S, V CORONELL 1976 Nitrogen nutrition, leaf resistance, and leafphotosynthetic rate of the rice plant. Soil Sci Plant Nutr 22: 207-21 1
