Plant, Cell and Environment {^995) 18, 605-618

THEORETICAL PAPER

A model of the acclimation of photosynthesis in the leaves ofC3 plants to sun and shade with respect to nitrogen use

K. HIKOSAKA* & I. TERASHIMAf

Department of Bolany, Faculty of Seienee. University of Tokyo, Hongo. Bunkyo-ku, Tokyo 113, Japan

ABSTRACT

A model of leaf photosynthesis of C3 plants has been devel-oped to describe their nitrogen economy. In this model,photosyntbetic proteins are categorized into flve groupsdepending on their functions. The effects of investment ofnitrogen in each of these groups on the maximal rate ofphotosynthesis and/or the initial slope of the light-response curve are described as simple equations. Usingthis model, the optimal pattern of nitrogen partitioningwhich maximizes the daily rate of CO2 exchange is esti-mated for various light environments and leaf nitrogencontents. When the leaf nitrogen content is fixed, theamount of nitrogen allocated to Calvin cycle enzymes andelectron carriers increases with increasing irradiance,while that allocated to chlorophyll-protein complexesincreases with decreasing irradiance. For chlorophyll-proteins of photosystem II, the amount of light-harvestingcomplex II relative to that of the core complex increaseswith decreasing irradiance. At any irradiance, partition-ing into ribulose bisphosphate carboxylase increases withincreasing leaf nitrogen content. Taking the total leafnitrogen content and the daily CO2 exchange rate as 'cost'and 'benefit', respectively, the optimal amount and parti-tioning of nitrogen are examined for various conditions oflight environment and nitrogen availability. The leafnitrogen content that maximizes the rate of daily carbonfixation increases with increasing growth irradiance. It isalso predicted that, at low nitrogen availabilities, low leafnitrogen contents are advantageous in tep-ms of nitrogenuse efficiency. These trends predicted by the presentmodel are largely consistent with those reported for actualplants. The differences in the total amount of leaf nitrogenand in the organization of photosynthetic components thathave been reported for plants from different environ-ments would therefore be of adaptive significance,because such differences can contribute to realization ofefHcient photosynthesis. These results are further dis-cussed in an ecological context.

*Correspondence and present address: K. Hikosaka, BiologicalInstitute, Faculty of Science. Tokohu University. Aoba-yama.Sendai 980-77. Japan.

fPresent address: Institute of Biological Sciences. University ofTokyo, Hongo, Bunkyo-ku, Tokyo 113, Japan.

Key-words: initial slope of light-response curve of photosyn-thesis; leaf nitrogen; model; nitrogen partitioning; nitrogenuse efficiency; photosynthetic components; sun-shade accli-tnation.

INTRODUCTION

The light-saturated rate of photosynthesis expressed on aleaf area basis (Pmax) is very frequently used to character-ize leaf photosynthesis. Many studies have shown strongcorrelations between P^^^^ and amounts or activities ofseveral photosynthetic components such as ribulose bis-phosphate carboxylase (RuBPCase), cytochrome f (cyt f)and coupling factor (CF) (Bjorkman 1968; von Caem-merer & Farquhar 1981; Evans 1987). Since 50 to 80% ofleaf nitrogen is allocated to photosynthetic proteins (Evans1989a; Makino & Osmond 1991), the correlation betweenP,nax and leaf nitrogen content is also fairly strong (Osman& Milthorpe 1971; Mooney, Ferrar & Slatyer 1978; Field& Mooney 1986).

In order to construct a leaf that can assimilate a largeamount of carbon at high irradianees, a large investment ofnitrogen is required. However, under shade conditions, alarge investment of nitrogen in the leaf in order to raise^max would not yield an appropriate return. Since theavailability of nitrogen is often limiting in nature and sincemuch energy is required for the assimilation of nitrate intoprotein, it is essential for plants to use nitrogen efficiently.An investment of nitrogen or protein in a leaf 'appropriate'to its environment must therefore be of adaptive signifi-cance (Mooney & Gulmon 1979). Strong correlations be-tween the leaf nitrogen content and growth irradiance(Field 1983, 1988; DeJong & Doyle 1985; Hirose &Werger 1987; Hikosaka, Terashima & Katoh 1994) sup-port this idea.

However, the relationship between nitrogen and photo-synthesis should not be considered solely in terms of f^axsince the photosynthetic rate at low irradianees is not lim-ited by P„,._,^ but by the availability of photons. The initialslope of the light-response curve of photosynthesis hasbeen taken as an index of the efficiency of light use at lowirradianees (Gabrielsen 1948). The initial slope can be fur-ther analysed into two components: quantum yield on anabsorbed quanta basis and light absorptance of the leaf.While the quantum yield measured under the same condi-

©1995 Blackwell Science Ltd 605

606 K. Hikosaka and I. Terashima

tions is almost identical among healthy C3 plants (Bjork-man & Demmig 1987), the absorptance increases withincreasing leaf chlorophyll (Chi) content (Gabrielsen1948; Adams et al. 1990). Thus, the photosynthetic rate atlow irradiances would be raised by increasing leaf Chicontent. All Chi molecules in leaves are bound to proteins,forming chlorophyll-protein complexes. Since these com-plexes are major nitrogenous components in chloroplasts(Evans & Seemann 1989), the nitrogen cost of Chl-proteincomplexes must also be studied to understand the role ofnitrogen in photosynthetic production.

Many studies have shown that the organization or rela-tive amounts of photosynthetic components differ betweensun and shade leaves (Boardman 1977; Leong & Anderson1984a,b; Anderson 1986; Anderson, Chow & Goodchild1988; Chow & Anderson 1987a,b; Evans 1987, 1993a;Evans & Seemann 1989; De la Torre & Burkey 1990a,b;Terashima & Evans 1988). Since changes in the organiza-tion of various photosynthetic components in response tochanges in growth irradiance are similar in many plantspecies, such changes might be adaptive. However, theeffects of these changes on photosynthetic performancehave not been fully evaluated.

There have been several attempts to model the relation-ship between photosynthesis and leaf nitrogen. Most (e,g.Field 1983; Hirose & Werger 1987), however, used simplerelationships between photosynthetic performance andleaf nitrogen content, which do not allow analysis of thesignificance of changes in the organization of the photo-synthetic apparatus. As an exception, Evans (1989b,c,1993b) examined the effects of the partitioning of chloro-plast nitrogen into 'thylakoid nitrogen' and 'soluble pro-tein' and suggested that preferential investment in Chimight increase daily carbon gain in a leaf under shade con-ditions. However, this model does not allow a full exami-nation of the effects of changes in amounts of key thyla-koid proteins.

The aim of the present study is to clarify the effects ofchanges in the organization and in the total amount of pho-tosynthetic components on leaf photosynthesis under vari-ous conditions of irradiance and nitrogen availability. Forthis purpose, we employ a more comprehensive model ofleaf photosynthesis, which incorporates quantitative bene-fits and nitrogen costs of the various photosynthetic com-ponents. The study also attempts prediction of the optimalamount and partitioning of nitrogen for various environ-ments in order to consider the ecological significance ofdifferences in the photosynthetic apparatus.

THE MODEL

, Photosynthetic components are categorized into five func-tional groups depending on whether an increment of eachof the components leads to an increase in Pmax or in the ini-tial slope {(j)) of the light-response curve for leaf photosyn-thesis. The dependences of P^ux and/or </) on the amount ofeach of these five groups are expressed as simple equa-tions, based mostly on experimental data obtained with

leaves of Spinacia oleracea L. (Terashima & Evans 1988).By combining these equations, a model of C3 leaf photo-synthesis in air containing 35 Pa CO2 at a leaf temperatureof 25 °C is constructed.

The rate of photosynthesis, and the amounts of nitrogenand photosynthetic components are expressed per unit leafarea. Components in square parentheses (e.g. [cyt f]) rep-resent the amount per unit Ieafarea, A list of abbreviationsis given in Appendix A.

Light-response curve

The dependence of the photosynthetic rate of a leaf onincident photon flux density (PFD) is expressed as a non-rectangular hyperbola (Thornley 1976),

P =[(I)I+P^.^^- {{(j)I + P^^J^ -4<j)I6Pm.^^}^'^]/2d- R, (1)

where P is the net photosynthetic rate, / is the incidentPFD, Pnnax is the light-saturated rate of gross photosynthe-sis, <p is the initial slope of the curve, R is the rate of darkrespiration and 6 is the convexity of the curve. If thechloroplasts in a leaf are not perfectly acclimated to theirrespective light environments within the leaf, 6 of thelight-response curve for the whole leaf may become small(Terashima & Saeki 1985; Terashima 1989; Evans 1989b;Evans, Jakobsen & Ogren 1993). Since the main aim of thepresent study is to estimate the optimal partitioning, 0 isfixed at 0-9.

Photosynthetic components

Co-limitation ofP,,,^^

The amounts or activities of the components of Calvincycle enzymes, electron carriers, CF and the PSII reactioncentre are closely related to Pmax. and each of the reactionsperformed by these components can potentially limit P^ax-However, the efficiency of nitrogen use (carbon gain pernitrogen) is maximized if the amounts of all such compo-nents are balanced so as to co-limit P^^^ (Field & Mooney1986), Thus, it is assumed that Pmax 's co-limited by thereactions carried out by these components. These compo-nents are categorized into three groups (see below).

Group I. RuBPCase. Some recent studies have demon-strated curvilinear relationships between P^ax and theamount or activity of RuBPCase (Evans 1983; Evans &Terashima 1988; Makino, Mae & Ohira 1988). The curvi-linear relationships can be attributed to the decreases inCO2 concentration at the carboxylation site with increas-ing Pmax hecause the resistances to CO2 diffusion from theambient air to the intercellular spaces (Makino et al. 1988)and/or from cell walls to the stroma (Evans 1983; Evans &Terashima 1988; von Caemmerer & Evans 1991) are sub-stantial. In this model, the curvilinear relationship isexpressed as a rectangular hyperbola (Fig. la):

r+ [RuBPCase]), (2)

© 1995 Blackwell Science Ltd, Plant, Cell and Environment, 18,605-618

Modelling of acclimation of photosynthesis 607

oo

3

a.

RuBPCase (gmol

0 1

Cyt f (ijmol

2 0 1

PSII (ymol I

Figure 1. Relationships between P„y„ and the amounts of RuBPCase (a), eytochrome f (b) and PSII (c). Amounts of RuBPCase arecalculated from the activities expressed on a leaf area basis (Evans & Terashima 1988) and the speeifie aetivity of RuBPCase (Evans 1989a).The curve in (a) is fitted to the data of Evans & Terashima (1988), and the lines in (b) and (e) to the data of Terashima & Evans (1988). Therates of O, evolution measured at a saturating CO2 eoncentration (Terashima & Evans 1988) are multiplied by 0-56 (Evans & Seemann 1989)to convert them to the rates of CO2 exchange in normal air.

where a^ and b^ are constants (for the values of a^ and b^,and other a^ and b^, see Table 1).

Group II. Electron transport components, coupling factorand Calvin cycle enzymes (apart from RuBPCase. photo-system I and photosystem II). Linear relationships havebeen reported between P^ax and the amounts or activitiesof the components in this group, such as cyt f (Bjorkman etal. 1972; Evans 1987, Terashima & Evans 1988; Evans &Seemann 1989), CF (Terashima & Evans 1988), and someCalvin cycle enzymes (Makino, Mae & Ohira 1983). Sincereactions carried out by these components would be lessaffected by the decrease in CO2 concentration at the car-boxylation site than RuBP carboxylation/oxygenation byRuBPCase, Pmax is assumed to be proportional to theamount of each of the components in this group (seeMakino, Nakano & Mae 1994). Cyt f is used as a represen-tative of this group and P^ax is expressed as

P =af [cyt f] (3)

(Fig. lb).The molar ratio of the cytochrome b/f complex to plasto-

cyanin to ferredoxin to ferredoxin-NADP'^ oxidoreductaseto the CFQ-CFI complex is assumed to be 1:1:3:1:0-5(Terashima & lnoue 1985; Terashima & Evans 1988;Strotmann & Bickel-Sandkotter 1984). For the molecularmasses of these proteins, see Table BI in Appendix B. Thesum of the molecular masses at the above stoichiometry iscalculated to be 475 g mmoP' cyt f. For Calvin cycleenzymes other than RuBPCase, 359 g mmol ' cyt f isadopted (Evans & Seemann 1989; see Table 2).

Group III. Core complex of photosystem II (PSII core).Core complexes of the photosystems have dual functions:light harvesting and electron transport. Linear relation-ships have been reported between P^^x and the amount ofPSII core, [PSII], although the correlations reported areslightly weaker than those between P^^x and [cyt f] (Evans1987; Terashima & Evans 1988). The relationshipbetween P^^^ and [PSII] is thus expressed as follows:

/'max = «p

Table 1. Constants used in calculations

"Evans & Terashima (1988) and Evans (1989a).'Terashima & Evans (1988)."Evans (1993b).

(4)

Parameter

e

brOf

°p

be

b."n

b.

Unit

-

|xmol m"' s"'nmol m"S-'

S-'

mmol mol"'mol mop'mmol m~^-mol m"-nmol mol"' s"'nmol m" s~'

Value

0 9

44.0"2.27"

19.9b18 2"1-74''00650076^^2.05"00294"8-27"0-779"

Equation

(1)

(2)(2)(3)(4)(5)(7)(7)(9)(9)

(10)(10)

© 1995 Blaekwell Science Ltd, Plant, Cell and Environment, 18, 605-618

608 K. Hikosaka and I. Terashima

(Fig. lc). The PSII core is dealt with separately fromGroup II because of its light-harvesting function. One ofeach of the three minor Chi alb-h'mding proteins, CP29,CP26, and CP24, is included in the PSII core. Althoughthere is no evidence for fixed stoichiometries of thesecomplexes in PSII. many studies suggested 1:1 stoi-chiometries between the PSII reaction centre and each ofthe minor Chi a/b-b'mdmg proteins (see Jansson 1994), Forthe subunit composition of PSII, see Table B2 in AppendixB.

: According to the model proposed by Farquhar, vonCaemmerer & Berry (1980), when the concentration of

• RuBP is saturating and CO2 concentration is low, leaf pho-tosynthesis is limited by the activity of RuBPCase (GroupI), On the other hand, at high CO2, the regeneration ofRuBP through the reactions performed by the componentsin Groups II and III limits the rate of photosynthesis (seevon Caemmerer & Farquhar 1981). Our present assump-tion of co-limitation of P,,,^^ is thus equivalent to RuBPconsumption through carboxylation/oxygenation andRuBP regeneration being balanced. The balance isaffected by the CO2 concentration, and the amounts of thecomponents in Groups II and III relative to [RuBPCase]should increase with increasing CO2 concentration to real-ize the co-limitation (Sage, Sharkey & Seemann 1989).

Group IV. Core complex of photosystem I and light-har-vesting chlorophyll-protein complex I (PSI). The amountof P700 on a Chi basis is virtually constant irrespective ofthe levels of growth irradiance and nutrient conditions(Chow & Anderson 1987b; Evans 1987; Evans & Tera-shima 1987; Anderson et al. 1988; Terashima & Evans1988). Thus

[PSI]=aJChl], (5)

where [PSI] is the amount of PSI and [Chi] is the Chi con-tent on a leaf area basis. Here, stoichiometry between thePSI core and LHCI (light-harvesting Chl-protein complexI), the molecular mass of PSI (core + LHCI) per P700, and

the number of Chi molecules associated with PSI isassumed to be constant (Table 2; for the subunit composi-tion of PSI, see Table B3 in Appendix B), Some changes in[P700]/[Chl] have been reported to occur in response tospectral changes in the growth light environment (Melis &Harvey 1981; Chow et al. 1990) but are not taken intoaccount here.

Group V. Eight-harvesting chlorophyll-protein complex II(LHCII). [LHCII] is estimated on the assumption that Chiis bound either to the PSII core, to PSI (core + LHCI), or toLHCII. The stoichiometry between the PSII core andLHCII is thus not fixed.

[LHCII] =1000 [Chi]-Chips,, [PSII]-Chips,

(6)

where Chips,, Chips,, and ChlLHcii ^re the numbers of Chimolecules bound to one PSI (core + LHCI), the PSII coreand one molecule of LHCII protein, respectively (forvalues, see Table 2). A multiplier, 1000, is needed becausethe units of [Chi] and protein content are different (seeAppendix A),

Relationship between the initial siope and [Chi]

As noted in the Introduction, the initial slope (0, theamount of CO2 fixed per incident quantum) varies with[Chi], (j) is expressed as a rectangular hyperbola (Evans1993b):

(7)

Nitrogen costs of the components

The mass of nitrogen in proteins is assumed to be 16% ofthe mass of proteins. There are four nitrogen atoms in oneChi molecule. The nitrogen cost of each of the groups isshown in Table 2 (see also Tables Bl, B2 and B3 inAppendix B),

Groups

III

IIIIVV

Weight ofprotein(10'g)

550834"(359 + 475)417"465"

25

N cost(1000/iJ(10- mol N)

6-299-53"

5-00"604"0-338

Binding Clil(ChlJ(mol Chi)

00

60184"'

13"

N/binding Chi(mol mol"')

—

83-332-826-0

"Expressed as mol ' cyt f. For electron carriers and CF. see text and Table B1 in AppendixB, The molecular mass of 943g protein moP' Chi for Calvin cycle enzymes other thanRuBPCase is according to Evans & Seemann (1989), This number divided by 2-63 mmol cytf mol"' Chi (Terashima & Evans 1988) is 359g mmol"' cyi f,"Expressed as mol' reactions centre. Sum of all the subunits of PSII and PSI in Tables B2and B3 in Appendix B. respectively,'Evans & Seemann (1989),"Kuhlbrandt era/, (1994),

Table 2. Nitrogen cost of photosyntheticcomponents and the number of chlorophyllmolecules associated with the variousproteins. Group I: RuBPCase; Group 11:electron carriers except for photosystems.coupling factor and Calvin cycle enzymesexcept for RuBPCase; Group HI: PSII core;Group IV: PSI (core + LHCI); Group V:LHCII (see text)

© 1995 Blackwell Science Ltd./>/««/, Celt and Environment, 18.605-618

Modetting of acdimation of photosyrittiesis 609

The molecular masses of the components listed inTables 2 and Appendix B were mostly deduced from DNAsequences. In contrast, the number of Chi molecules asso-ciated with each of the complexes is still uncertain.

Leaf nitrogen content

Photosynthetic nitrogen, [Np], is the sum of the nitrogen inall the components:

n, [RuBPCase]+«,, Icytf|+n,,,+ «,v[PSI]+nvtLHCIl], (8)

where «„ is the nitrogen cost of Group n in mol N per |imolof the representative component (for values, see Table 2),

The leaf nitrogen content, [N], is expressed as a functionof [Np], This relationship is derived from the data obtainedin spinach (Terashima & Evans 1988):

[N]=a, [Np] + fc,. (9)

By substituting Eqns 2, 3, 4, 5, 6, 7 and 8 into 9, afterappropriate rearrangements, [N] can be expressed as afunction of two variables, Pmax and (j). Incorporating theChi number of each Chl-protein complex (Table 2), [N] isexpressed as

(10)

13+ b.

Respiration

Positive correlations between the rate of respiration (/?)and [N] have been reported (Hirose & Werger 1987;Terashima & Evans 1988; Makino & Osmond 1991),although there are some reports claiming that R may not beaffected by [N] (Pavlik 1983; Byrd, Sage & Brown 1992),We have used the data obtained by Terashima & Evans(1988), and the respiration rate is assumed to be

(11)

Daily change in photon flux density

The daily course of PFD is assumed to follow a square sinecurve (Terashima & Takenaka 1986),

7=0 (0</<6, 18<f<24), (12)

where t is solar time and /Q is PFD at noon (r= 12), IQ isalso used to express the growth irradiance.

Daily CO2 exchange rate

/? is a function of IN] (Eqn 11) that can be expressed as afunction of Pn.,^,^ and 0 by substituting Eqn 10. Thus, P can

be expressed as a function of P^._,^, 0 and / (see Eqn 1). Pcan also be expressed as a function of f max- [N] and /, bysubstituting Eqn 10 after solving for (j). Integration of P fora day using Eqn 12 gives the daily CER:

24

CER=| Pdt. (13)

In the present study, P is integrated numerically. Weassume a constant temperature of 25 °C throughout a day.

Simuiations

In the present study, daily CER is regarded as the 'benefit'.Thus, the effects of changes in [N] or the 'cost' and innitrogen partitioning on daily CER are the main concern.First, using Eqn I, Pis expressed as a function of P^^^ , [N]and / after 0 and R are substituted by Eqns 10 and 11.Then, for a given combination of P^^^, [N] and ZQ, P isnumerically integrated for a day to obtain daily CER. FromPniax. the amounts of the components in Groups I, II and IIIare calculated using Eqns 2, 3 and 4, respectively. FromPn,ax and [N], (p is obtained using Eqn 10, The amounts ofthe components in Groups IV and V are then calculatedusing Eqns 5 and 7, and Eqns 6 and 7, respectively. Detailsof the calculation methods are given in the figure legends.

RESULTS OF SIMULATIONS

Figure 2 shows the relationships between P^ax and [N]determined for four values of 0. P^^^ increases withincreasing [N] in a saturating manner reflecting the satu-rating nature of the dependence of P^^^ on [RuBPCase]

0.1 0,2Leaf nitrogen content (mol N m~ )

Figure 2. Effects of the initial slope on the relationship betweenPn,;,, and leaf nitrogen content. At 0=0 045, [N] > 0-2 mol m"'causes negative |LHC1I], Eqn 10 is solved forPn,.,,, and [N] and (j)are varied.

i 1995 Blackwell Science Ltd, Ptattt. Cett attd Envirotttnertt, 18, 605-618

610 K. Hikosaka and I. Terashima

^ 2 01en

CM

ECM

oo• 5E3 10

rat

. 0

0

1 0U-

_ „ - — — •

x^-——/ - — • " —

# ^

Z' .n 1 jf^ A

K111 2' #

//f / ^

0

0 1000

PFD (umoi quanta m

Pmax=22,7—

21,820!2~

i7!3~

13,7

13.7^/X/

>^XM7,3y^:>^20,2

>^X21,8^ 2 , 7

, 1 , , I , 1 .

50 10020

Figure 3. Effects of the changes in the partitioning of nitrogeninto photosynthetic components on the light-response curve forleaf photosynthesis. Leaf nitrogen content is fixed at 0-1 mo m"lThus, when ?„„, is 13-7, 17-3, 20-2, 21 -8 and 22 7nmol m""s"',the initial slopes are 0 058, 0 056,0 052, 0 048 and 0-43 mol moP',respectively. These light-response curves yield maximums fordaily CERs at /o= 125, 250, 500, 1000, and 2000nmol m'^s^',respectively (see Fig, 4), 0 and R in Eqn 1 are substituted with Eqn10 after rearrangement for 0, and Eqn 11, respectively, P is thusexpressed as a function of Pn,^,, [N] and /, The light-response curvefor leaf photosynthesis is obtained by changing /,

having a maximum. The leaf nitrogen content that maxi-mizes CER increases with increasing 1Q, Figure 5b showsthe daily nitrogen use efficiency (NUE, daily CER dividedby [N]) calculated from Fig, 5a, For any /Q, there is a max-imal NUE, and the value of [N] maximizing NUE alsoincreases with increasing /Q. However, the differencebetween the [N]s that maximize NUE at /o=125 and/o=2000 is much smaller than the difference between the[N]s that maximize the daily CER at /o= 125 and /o=2000(Fig, 5a), The P^.^^ and 0 that maximize the daily CER atfive /() levels are plotted against [N] in Figs 5c and 5d, Fora given /Q, both Pmax ^nd 0 increases with increasing [N],When compared at a given [N], Pmax increases withincreasing /Q while (j) decreases.

Changes in the optimal partitioning of nitrogen amongphotosynthetic components with changes in [N] are shownfor three /Q levels (Fig, 6). In this figure, the components inGroup II are further divided into Calvin cycle enzymesother than RuBPCase and thylakoid components otherthan Chl-protein complexes. At /o= 2000, relative levels ofCalvin cycle enzymes and RuBPCase are high. In particu-lar, more than half of the photosynthetic nitrogen is parti-tioned into RuBPCase when [N]>015molm"^ (Fig. 6a).By contrast, nitrogen partitioned into Chl-protein com-plexes increases with decreasing /Q (Figs 6b & c). At/o=125, nitrogen partitioned into Chl-protein complexesincreases with increasing [N], while it is almost constant at/o=500 and 2000.

0,8

(Fig, la). If [N] is fixed, an increase in P^.^^ is accompa-nied by a decrease in (p. Since the relationship between (j)and [Chi] is expressed as a saturating function (Eqn 7), 0plotted against [N], for a fixed Pmax. results in a saturatingcurve (data not shown).

Effects of changes in P^ax and 0 on photosynthetic per-formances are shown in Figs 3 and 4, Since [N] is fixed at0-1 molm"^, Pn,ax and (j) change in different directions inboth figures (see Eqn 10), In Fig. 3, the effects on theinstantaneous light-response curve of leaf photosynthesisare shown. The instantaneous rate of photosynthesis athigh PFD (>600Aimolm"^s^') increases with increasingPmax while the rate of photosynthesis decreases withincreasing P^ax at low PFD. In Fig. 4, effects of thechanges in Pmax and (j) on daily CER are evaluated for five/Q levels. Daily CER dramatically changes with Pmax eventhough [N] is fixed. It is evident that, with increasing /,,,Pmax for the maximal daily CER increases at the expenseof 0, while high values of <j) are favoured at lower /(, levels.

In Fig, 5a, daily CER as maximized by the optimal parti-tioning of nitrogen is plotted against [N], Partitioning dif-fers depending on [N] (see also Fig, 6), The dependence ofdally CER on [N] at any /(> is expressed as a convex curve

0,08

Initial slope lo=2OOO -

10 20

SCO3

0,04

o"o

0 ^

CO2

Figure 4. Effects of P^^^ on the daily carbon exchange rate atvarious levels of/„ (solid lines). Leaf nitrogen content is fixed at0-1 mol m" . Changes in the initial slope are shown (broken line).The solid circles indicate the maximal daily CERs for respective/oS (see Fig, 3), P expressed as a function of P,,,i,x, [N] and / (seelegend of Fig, 3) is numerically integrated for a day to obtain dailyCER, Changes in / follow Eqn 12, Each curve is obtained byvarying P,,,^^ for a given /„, 0 is calculated using Eqn 10 from P,,,^^and [NI.

© 1995 Blackwell Science Ltd, PUmt, Cell and Envinmment. 18,605-618

Modetting of acdimation of photosynthesis 611

1

T3NJ1

CJ

3 0.5

(mol

CER

Dai

ly

0

. (a)

I

/ ^

—!-=•

^ 250-'— " • — —

" •

1 1 . .

lo=2OOO—0-

1000

500• * — — - _

~ ^ - _

1 1 1 . . .

0.1 0.2Leaf nitrogen content (mol N

T-a:zi1

oECJ

OO"o

LU

>,(0Q

o

4

2

0

(b)

/ // /

// // // /

/7\ r1

0

^^0-^0=2000

^OOOOO \ v

\ . \ .

^0^500 ^ - ^ ^ ^ ^

<-, 250 ^^^~..,.,^

^ ^ - • ^ ^ ^ - - ^

125 ^ ^ - ^ ^ ^ ^ ^ ^O » ^ ^

1 , , ,

0.1 0.2Leaf nitrogen content (mol N

0,1 0,2Leaf nitrogen content (mol N

0.1 0.2Leaf nitrogen content (mol N

Figure 5. Daily CER (a), daily NUE (b), P^..,^ (c) and ^ (d) versus leaf nitrogen content when daily CER is maximized at each combinationof/o and [N], The closed and open circles indicate the points that correspond to the maximal daily CER and NUE at each /Q, respectively. Themaximal daily CER for given [N] and /„ is obtained in the same way as that used to produce Fig, 4, The daily NUE is the ratio of the dailyCER to [N], From the P^ax that maximizes daily CER and [N], <p is calculated using Eqn 10,

Changes in the Chi alb ratio and in [Chi] with [N] whennitrogen partitioning is optimized are shown for five /„ lev-els in Fig. 7. The Chi alb ratio increases with increasing /Q.It also changes with changes in [N]. Since the increase inthe Chi alb ratio reflects the relative increase in the ratio of[PSII] to [LHCII], the ratio of the amount of PSII reactioncentre to the amount of PSI reaction centre also increaseswith increasing /Q (data not shown). Relationships between[Chi] and [N] are shown in Fig. 7b. [Chi] increases with

increasing [N], When [N] is fixed, [Chi] increases withdecreasing /„.

Figure 8 shows the relationships between [RuBPCase]and [N] when nitrogen partitioning is optimized. With anincrease in [N] and/or in /„, [RuBPCase] increasesmarkedly. The changes in the amounts of other compo-nents are not shown, but [cyt f] and [PSII] are proportionalto P,,,ux (Eqns 3 and 4), and [PSI] is proportional to [Chi](Eqn 5),

© 1995 Blackwell Science Ltd, Ptattt, Cett attd Ertvirontnettt, 18, 605-618

612 K. Hikosaka and I. Terashima

qt32 0,5

PSII core,

Electron carriers & CF

'ci'

RuBPCase

0,5

(c)LHCII

.carriers & CFCE

RuBPCase

0,1 0,2Leaf nitrogen content (mol N m" )

Figure 6. Optimal patterns of nitrogen partitioning amongphotosynthetic components versus leaf nitrogen at three irradiancep y p glevels; /„=2000 (a). 500 (b) and 125 (c) Jmol m'"s"', The closedand open triangles indicate the leaf nitrogen contents thatmaximize the daily CER and NUE at each value of/,,, respectively,CE denotes Calvin cycle enzymes except for RuBPCase, Theamounts of the components in Groups 1, II and III are calculatedfrom P„,^^ in Fig, 5c using Eqns 2. 3 and 4. respectively. Theamount of PSI is calculated from (p in Fig, 5d using Eqns 5 and 7,Having found [PSI] and [PSII]. [LHCll] is obtained using Eqn 6,Group 11 is divided into stromal (CE) and thylakoid (electroncarriers and CF) components with the assumption that the ratio ofthe nitrogen costs of these two components is 359:475 (see Table 2),

o

0,1 0.2Leaf nitrogen content (mol N

0,1 0,2Leaf nitrogen content (mol N

Figure 7. The chlorophyll alb ratio (a), and the leaf chlorophyllcontent (b) when nitrogen partitioning is optimized versus leafnitrogen content. The closed and open circles indicate the values onthe curves that maximize daily CER and NUE at each /„.respectively. Leaf Chl content is calculated from (j) in Fig, 5d usingEqn, 7, The Chl alb ratio is calculated with the assumption thatratios of Chl a to h associated with PSI. the PSII core and LHCIIare 8. 1 1 and 11. respectively. The Chl alb ratio in PSI is takenfrom Mukerji & Sauer (1989), It is assumed that five Chl bmolecules are associated with one PSII core (one molecule each ofthe minor Chl alb proteins CP29. CP26 and CP24),

© 1995 Blackwell Science Ltd. Phmt, Cell and Environment, 18. 60.5-618

Modelling of acclimation of photosynthesis 613

15

10-

5-

-

-

.A 125

^ 5 0 0

50

1

lo=2OOO /

/ /

X r 1000o

ooCDC/3CD

oCLDQ

0,1 0.2Leaf nitrogen content (mol N m"^)

Figure 8. RuBPCase versus leaf nitrogen content. Nitrogenpartitioning is optimized at any combination of [N j and /„, Theclosed and open circles indicate the values on the curves thatmaximize daily CER and NUE at each value of/,,, respectively.The amount of RuBPCase is calculated from the P^^M shown inFig, 5c using Eqn 2,

The simulation results are almost insensitive to slightchanges in the assumptions. For example, when the nitro-gen cost of the Chl number of any one of the five groups ischanged by 10%, the change in P^ax that gives the maxi-mal daily CER in Fig. 4 is no greater than 3%. Thus, theresults presented here are stable in a semi-quantitativesense.

DISCUSSION

Changes in the organization of Chl-proteincomplexes in response to changes in growthirradiance

It is well known that the Chl a/b ratio increases withincreasing growth irradiance (Egle 1960). This tendency isreproduced by three assumptions: a linear relationshipbetween P^^^ and [PSII] (Eqn 4), constant stoichiometryof [PSI] relative to [Chl] (Eqn 5), and Chl molecules otherthan those associated with the PSII core and PSI beingassociated with LHCII (Eqn 6). At higher growth irradi-ances, a large amount of PSII core is required to realizehigh P,,n,x because the PSII core contains several electroncarriers. By contrast, at lower irradiances, the relativeamount of LHCII increases (Fig, 6), Since most Chl b isassociated with LHCII, the relative increase in LHCIIamong Chl-protein complexes in shade leave,s causes a

decrease in the Chl a/b ratio. Table 2 compares the nitro-gen cost (n,,), the number of binding Chl molecules (Chl^)and the nitrogen cost per binding Chl, among LHCII, thePSII core and PSI (core + LHCI), The nitrogen cost per Chlfor the PSII core is approximately three times that forLHCII. Therefore, in order to increase the number of Chlin PSII, an increase in the amount of LHCII is more effi-cient in terms of nitrogen economy than an increase in theamount of PSII core (Evans 1987), Thus, a linear relation-ship between P. ^^ and [PSII] (Eqn 4) would indicate thatthe ratio of PSII core to LHCII tends to be maintained atthe minimal level at which the amount of PSII core co-lim-its F,, x with other components. When similar calculationsare made on the published data on [PSI] and [PSII] in sunand shade leaves (Leong & Anderson 1984a,b; Wild etal.1986; Chow & Anderson 1987a,b; Terashima & Evans1988; De la Torre & Burkey 1990a,b) using Eqn 6 and thenumbers in Table 2, the nitrogen cost of Chl-protein com-plexes per leaf Chl in typical shade leaves is 5-20% lowerthan that in sun leaves of the same species. Thus, the dif-ference in the cost of light harvesting is significant, and thechanges in the organization of Chl-protein complexes areof economic importance.

It is unclear whether such drastic changes in the level ofthe PSI core relative to the level of LHCI occur in responseto changes in growth irradiance. Thus, in the present mode,we assume fixed stoichiometry between PSI and LHCI,Since nitrogen cost per Chl in PSI (core-i-LHCI) is low(Table 2), changes in the stoichiometry between the PSIcore and LHCI may be less important from an economicviewpoint.

Changes in nitrogen partitioning with changes ingrowth irradiance

Figure 4 predicts that, even when [N] is fixed, daily CERchanges drastically depending on the pattern of the nitro-gen partitioning. It has been suggested that optimal invest-ment in [Chl] increases with decreasing /g (Evans1989b,c), For example, at [N] = O-1, [Chl] at /Q = 125 isapproximately five times as high as that at /o==2000 (Fig.7b), Our semi-quantitative examinations also predict thatthe relative proportion of nitrogen in Chl-protein com-plexes markedly increa.ses with decreasing Z,, in spite of theabove-mentioned fact that the nitrogen cost per Chldecreases considerably with decreasing /„ (Fig. 6). Nitro-gen partitioned into Chl-protein complexes representsabout 20% of photosynthetic nitrogen at /o=2000, while itrepresents 50-60% at /(,= 125, Thus, under shade condi-tions, Chl-protein complexes are the most nitrogeneouscomponents in the leaf. These predictions therefore sug-gest that the preferential investment of nitrogen in thecomponents related to P^M or '" those related to (j) is themost important feature in changes in the organization ofphotosynthetic components with changes in growth irradi-ance.

© 1995 Blackwell Science Ltd, Pkmt, Cell and Environment, 18. 605-618

614 K, Hikosaka and I. Terashima

Changes in nitrogen partitioning with changes inleaf nitrogen content under fixed irradianceconditions

At higher /(, levels, the relative amount of nitrogen inRuBPCase increases with increases in [N], while that inGroup II decreases (Fig. 6), This tendency is caused by thenon-linear relationship between Pmax ^fd [RuBPCase],Since this relationship causes a gradual decrease in thegain of F^ax with increases in [RuBPCase] (Fig. la), therelative partitioning into [RuBPCase] increases withincreases in P^.,,^, The results in Fig. 6 agree with those ofEvans (1989a), who demonstrated an increase in theamount of soluble protein relative to thylakoid nitrogenwith increases in [N] (see also Makino et al. 1992). Simi-larly, the relative increase in the levels of Chl-protein com-plexes with increasing [N] at /o= 125 (Fig, 6c) is caused bythe non-linear relationship between 0and [Chi], If the rela-tionships between F^.^^ and [RuBPCase] and between 0and [Chi] were linear, the partitioning pattern at a given /Qwould be almost constant irrespective of [N] levels (datanot shown).

The Chi alb ratio increases with decreases in [N] (Fig.7a). The increase is particularly marked at high /Q levels.Increases in the ratios of [cyt f]/[Chl] and [PSII]/[PSI] withdecreases in [N] are also predicted (data not shown). Sincethe Chi alb ratio reflects the ratio of [PSII] and [LHCII],the simulation results in Fig. 7a imply that there is adecrease in the amount of PSII core relative to the amountof LHCII with increases in [N], This can finally beattributed to the curvilinear relationship between P^^^ and[N], and this relationship is mainly a result of the non-lin-ear relationship between P^ax and [RuBPCase], Thechanges in [cyt f]/[Chl] and [PSII]/[PSI] can also beattributed to the same factor. However, according to thedata of Terashima & Evans (1988), the Chi alb ratio, andthe amounts of P700, atrazine binding site (PSII core) andcyt f per Chi are all constant irrespective of [N] levels.Thompson, Huang & Kriedemann (1992) showed that theChi alb ratio was higher in leaves with high [N] in trees oftropical rainforest species. These observations are obvi-ously inconsistent with the present prediction. On the otherhand, Kitajima & Hogan (1993) observed that the Chi albratio in leaves of a tropical tree, Tabebuia rosea, increasedto 5-9 with decreases in [N] under 30% full sun, butremained relatively constant under 2% full sun. Theirobservations are consistent with our prediction. Furtherstudies on this subject are clearly needed.

CER, NUE and leaf nitrogen

The dependence of daily CER or the net assimilation rate(plant growth rate per leaf area) on [N] is usuallyexpressed as a convex curve (see Fig. 5a). According toHirose (1984) and Hirose & Werger (1987), the photosyn-thesis of a leaf is limited either by carbon or nitrogendepending on the [N] level. When [N] is lower than the

level that maximizes the daily NUE, photosynthesis by theleaf is nitrogen limited. By contrast, when [N] is higherthan that level, photosynthesis is carbon limited. Accord-ing to this idea, the leaf with the [N] value that gives themaximal daily CER (Fig. 5a) is thought to be carbon lim-ited. Leaves having [N] values that are higher than thevalue giving the maximal daily CER are unlikely to existin nature. On the other hand, when nitrogen availability islow, [N] should be reduced. However, leaves having [N]values that are lower than the value that gives the maximalNUE, or nitrogen-limited leaves in the sense of Hirose(1984), are also unlikely to exist in nature. This is sobecause the rate of photosynthetic production per leaf insuch a leaf is lower than the rate in a leaf that has the sameamount of total nitrogen per leaf at the [N] giving the max-imal NUE, in spite of the fact that the latter leaf has asmaller leaf area. Thus, we propose that [N] values inactual leaves are likely to be defined by these two border[N] values which allow the maximal daily CER and NUE,with developing and senescing leaves being exceptions.

The [N] level that maximizes NUE changes onlyslightly with changes in IQ (Fig, 5b), This tendency agreeswith the observation that [N] levels in leaves of spinachgrown under low nitrogen availabilities were around0-08 mol N m" , independent of growth irradiance (Tera-shima & Evans 1988), The results of the present simula-tions also predict that the difference between the [N] val-ues that maximize CER and NUE is very small when /Q islow while the difference increases with increases in /Q(Fig. 5). In spinach leaves, similar trends were observed(Terashima & Evans 1988). From these, it is clear that notonly CER but also NUE should be taken into accountwhen examining the relationship between photosynthesisand nitrogen.

Ability for acclimation

In spinach leaves, ratios of [Chl]/[N] were 3-8, 4-4 and4-4 mmol mol"' for leaves grown under 100, 30 and 15%sunlight, respectively (Terashima & Evans 1988). Thevalue at 100% sunlight, 3-8 mmol mol"', corresponds wellto the optimal ratio estimated for [Chl]/[N] at /o= 500 (Fig,7b). However, the value of 4-4 mmol mol"' is much lowerthan that expected from the optimal partitioning at /()= 125.Since spinach is a typical sun species, the photosyntheticapparatus may be unable to acclimate completely to verylow growth irradiance. The similar ratios of [ChI]/[N] forthe leaves grown under irradiances of 15 and 30% sunlightalso support this possibility. On the other hand, Seemannet al, (1987) showed that ratios of [Chl]/[N] were mar-kedly higher in leaves of a shade species, Alocasia mac-rorrtiiza, than in those of a sun species, Phaseolus vut-garis. This implies that the photosynthetic apparatus ofshade species has the ability to acclimate to the shade.However, its ability to acclimate to full sun may be lim-ited.

© 1995 Blackwell Science Ltd, Plant, Cell and Environment, 18, 605-618

Modelling of acclimation of photosynthesis 615

Concluding remarks

The optimal leaf nitrogen content and the pattern of nitro-gen allocation among photosynthetic components pre-dicted for various /(> and nitrogen conditions are largelyconsistent with previous observations. This agreementstrongly suggests that the differences in [N] and in nitro-gen partitioning among leaves from different environ-ments are of adaptive significance. Although the trends insuch differences are similar in most higher plants, therange of environments to which the plants can adjust theirphotosynthetic apparatus appears to be different depend-ing on species. Such differences may be causes or conse-quences of specialization of the plants to particular ecolog-ical niches. The present model can also be used as a toolwith which to assess the ability of various aspects to accli-mate to a particular range of environments.

ACKNOWLEDGMENTS

The authors thank Professor S. Katoh and Drs W.S, Chow,M. Ikeuchi, T. Hisabori, I, Enami, A, Takenaka, K. Kita-jima, K, Sonoike, K.C, Han and H, Hatanaka and M,Ishibashi for valuable suggestions and discussions. Thiswork was supported in part by a grant from the Ministry ofAgriculture, Forestry and Fishery for Biocosmos Projectand by grants from the Ministry of Education, Culture andSciences, Japan,

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Received 16 June 1993; received in revised form 18 August 1994;accepted for publication 10 October 1994

APPENDIX A: List of abbreviations

a^, b^, regression coefficients (see Table 1)CER, (daily) carbon exchange rate on a leaf area basis (mol

CF, coupling factorChl, chlorophyll[Chl], amount of Chl on a Ieafarea basis (mmol Chl m~~)Chl,, number of Chl associated with Chl-protein complex Xcyt f, cytochrome f[cyt f]. amount of cyt f on a leaf area basis (|lmol f m"^)FNR, ferredoxin-NADP* oxidoreductase/, incident photon flux density (|imol quanta m "s^')/„. incident photon flux density at noon (fimol quanta m""s"')LHC, light-harvesting complex[LHCII], amount of light-harvesting complex of photosystem II

(|imol LHCII m^")MM, molecular mass[N], leaf nitrogen content (mol N m^")«„, nitrogen cost (mol N ^tmol"' protein, cyt f or reaction centre);

see Table 2[Np], amount of nitrogen in all the photosynthetic components (mol

Nm"-)NUE, (daily) nitrogen use efficiency (mol CO2 mol"' N d"')P, rate of net photosynthesis on a leaf area basis ((imol CO2 m"" s"')PFD, photon flux density^max' light-saturated rate of gross photosynthesis on a leaf area

basis (|imol CO2 m"-s"')PSI, core complex and light harvesting complex of photosystem 1[PSI], amount of PSI on a Ieafarea basis ()imol PSI m"~)PSII core, core complex of photosystem II[PSII], amount of core complex of photosystem II (|imol PSII m ")R, rate of dark respiration (|imol CO2 m"s"')RuBPCase, ribulose-1.5-bisphosphate carboxylase[RuBPCase], amount of RuBPCase (|j.mol m ")/, time of day (h)(p, initial slope of the light-response curve of photosynthesis (mol

CO2 mol"' incident quanta)6. convexity of the light-response curve of photosynthesis (no

dimensions)

Rieske De-SIV

V

Plastocyanin"

Ferredoxin"FNR" (54-5)

FNRFNR binding protein

Coupling factor" (562-5)CF,

aP75

IIIIIIIV

20174

10-5

10-5

3717-5

59x356x33717-513

18168x12

20

"According to Anderson (1986), Barber (1987) and Bassi et al.(1990),"Molecular masses of subunits of CF,, andCF, are after Feng &McCarty (1990) and Strotmann & Bickel-Sandkotter (1984),respectively, Stoichiometries are based in Ort & Oxborough(1992),

Table B2. Subunit composition of PSII core

Subunit

Core"CP47 apo proteinCP43 apo proteinDlD2PSII-SPSll-Rbssy-large subunitPSII-H6-1 kDPSII-IPSll-L

subunit

MM(kD)

4-1 kDPSII-KPSII-M

56-251-838-139-52010-29-37-66-14-24-44-34-24-23-73

APPENDIX B: Subunit compositions of variouscomponents

Table B1. Subunit composition of electron carriers and couplingfactor in thylakoid membranes

Component MM (kD)

Cytochrome b(,/f complex" (97-5)cytfcyt b,,

3323-5

Oxygen evolving complex"33 kD24 kD18kD

Minor Chl alb binding proteins"CP29CP26CP24

26-720-216-5

282723

"Ikeuchi (1992a. and personal communication),"Jansson (1994),

© 1995 Blackwell Science Ltd. Phmt, Cell cmd Environment, 18. 605-618

618 K. Hikosaka and I. Terashima

Table B3. Subunit composition of PSI

Subunit MM (kD)

Core"PSI-A 83PSt-B 82PSt-C 8-5PSI-D 18PSI-E 10PSt-F 17PSI-G 10PSt-H 10PSI-I 4PSt-J 4PSI-K 7PSI-L 18PSt-O 9

LHCI"LHCt-I 22x2LHCI-II 23x2LHCt-ttI 25x2LHCI-IV 22x2

"tkeuchi (1992b).''Jansson(1994).

© 1995 Blackwell Science Ltd, Plant. Cell and Environment. 18, 605-618