The Temperature Response of C3 and C4 Photosynthesis

The temperature response of C3 and C4 photosynthesisROWAN F. SAGE1 & DAVID S. KUBIEN2

1Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, ON M5S3B2Canada and 2Department of Biology, University of New Brunswick, 10 Bailey Dr., Fredericton, NB, E3B6E1, Canada

ABSTRACTWe review the current understanding of the temperatureresponses of C3 and C4 photosynthesis across thermalranges that do not harm the photosynthetic apparatus.In C3 species, photosynthesis is classically considered tobe limited by the capacities of ribulose 15-bisphosphatecarboxylase/oxygenase (Rubisco), ribulose bisphosphate(RuBP) regeneration or Pi regeneration. Using both theo-retical and empirical evidence, we describe the tempera-ture response of instantaneous net CO2 assimilation rate(A) in terms of these limitations, and evaluate possiblelimitations on A at elevated temperatures arisingfrom heat-induced lability of Rubisco activase. In C3plants, Rubisco capacity is the predominant limitation onA across a wide range of temperatures at low CO2(

been developed to test the possibilities (Farquhar, vonCaemmerer & Berry 1980; von Caemmerer & Furbank1999; von Caemmerer 2000). As a result, we have a goodunderstanding of the limitations over photosynthesis at thethermal optimum in C3 plants (von Caemmerer 2000);however, the biochemical controls over the rate of photo-synthesis at non-optimal temperatures are less clear.Advances in model parameterization and increased experi-mental attention have in recent years improved our under-standing of the mechanisms controlling photosyntheticresponses to both high and low temperatures (Bernacchiet al. 2001, 2002; Medlyn et al. 2002; Bernacchi, Pimentel &Long 2003; Salvucci & Crafts-Brandner 2004a). Theseadvances occur at a time when society is increasinglyconcerned about global climatic change, and we are nowobserving the first wave of responses to climatic change inthe form of range shifts, phenological adjustments andpopulation collapses (Jump,Hunt & Penuelas 2006;Menzelet al. 2006; Mouthon & Daufresne 2006). To be able topredict the effects of climatic change, and to adapt agricul-tural systems and land management to a warmer world, it isimperative to understand how temperature affects photo-synthetic carbon gain. This review will synthesize ourcurrent understanding of temperature effects on the photo-synthetic biochemistry, and how these effects determine thethermal response of whole-leaf photosynthesis in C3 and C4plants.This understanding will then be used to evaluate themechanisms by which plants acclimate to different thermalenvironments.

THEORETICAL CONTROLS ONPHOTOSYNTHETIC CAPACITY IN C3 PLANTSGeneral considerationsThe rate of net CO2 assimilation (A) in the leaves of C3plants is generally characterized as being under the controlof three distinct processes: the capacity of ribulose 15-bisphosphate carboxylase/oxygenase (Rubisco) to consumeribulose bisphosphate (RuBP) (RuBP-saturated photosyn-thesis or Rubisco-limited photosynthesis), the capacity ofthe Calvin cycle and the thylakoid reactions to regenerateRuBP (RuBP regeneration-limited photosynthesis) and thecapacity of starch and sucrose synthesis to consume triosephosphates and regenerate inorganic phosphate for photo-phosphorylation (Pi regeneration-limited photosynthesis ortriose phosphate use-limited photosynthesis) (Harley &Sharkey 1991; von Caemmerer 2000).The Rubisco capacityto consume RuBP is generally the predominant limitationon A at light saturation and CO2 levels below the currentambient partial pressure of 380 mbar. Because of this, theinitial slope of the response of net photosynthesis to inter-cellular CO2 partial pressure (the A/Ci response) is deter-mined by Rubisco capacity (Vcmax) at light saturation(Farquhar & von Caemmerer 1982; Hikosaka et al. 2006).RuBP regeneration capacity (as affected by the rate of lightharvesting) becomes limiting at subsaturating light intensi-ties at all levels of CO2 (Sage, Sharkey & Seemann 1990b).

At saturating light intensities, moderate temperature (2530 C) and elevated CO2, either the capacity of RuBPregeneration or the Pi regeneration capacity limits A(Sharkey 1985a). RuBP regeneration capacity at light satu-ration generally reflects limitations in electron transportcapacity (Jmax), a feature that allows for the estimation ofJmax in vivo using gas exchange measurements at high CO2(von Caemmerer & Farquhar 1981; von Caemmerer 2000;Cen & Sage 2005).Characteristic responses of A to CO2 and O2 variation in

C3 leaves indicate whether A is limited by the RuBP regen-eration capacity versus the Pi regeneration capacity. WhenA is controlled by the RuBP regeneration capacity, it isstimulated by an increase in CO2 or a reduction in O2 supplyunder conditions where photorespiration occurs (von Cae-mmerer & Farquhar 1981; Sharkey 1988). This is normallythe case above 5 C, and below a CO2 level of 500 mbar(cooler temperatures, 35 C) (Ehleringer et al. 1991).Thesensitivity of RuBP regeneration-limited A to CO2 and O2reflects the competition between these gases for RuBP; asCO2 levels increase, oxygenase activity is increasingly inhib-ited and A rises with decreasing slope to a plateau thatbegins at the CO2 level where photorespiration becomesnil. By contrast, when A is limited by the Pi regenerationcapacity, there is little if any stimulation following CO2enrichment or O2 reduction at CO2 levels where photores-piration is present (Sharkey 1985a,b, 1988).This lack of CO2or O2 sensitivity occurs because Pi is used as fast as itbecomes available, a situation that is not altered by reduc-ing photorespiration (Sharkey 1985b). In practice, theeasiest approach to detect a Pi regeneration limitation is tomodel the predicted sensitivity of A to variation in O2 andCO2, and compare this with observed sensitivities (Sharkey1988). O2 sensitivity of A can be defined as (A21 - A2)/A2where A21 is net CO2 uptake at current O2 levels (21% O2)and A2 is A at 2% O2 where photorespiration is nil (Sage &Sharkey 1987). CO2 sensitivity, defined as (Aair - Asat)/Asat,compares A in a lower CO2 atmosphere (Aair) with CO2-saturated A (Sage, Sharkey & Pearcy 1990a). If RuBPregeneration capacity is limiting, the observed O2 or CO2sensitivity will be equivalent to the respective theoreticalsensitivity; if the Pi regeneration capacity is limiting, theratio will be well below the theoretical value, and will oftenbe near zero or negative (Fig. 1) (see also Mawson et al.1986; Sage, Sharkey & Seemann 1989;Cowling & Sage 1998;Sun, Edwards & Okita 1999; Hendrickson, Chow &Furbank 2004b; Kubien & Sage 2004b).

Temperature and the CO2 response ofphotosynthesisA common approach for analyzing environmental effectson photosynthetic limitations in intact leaves has been tomeasure the response of A to intercellular partial pres-sures of CO2 (the A/Ci curve). This is because the threemajor classes of limitation described earlier show charac-teristic responses to CO2 variation that allow for their

Temperature response of C3 and C4 photosynthesis 1087

2007 The AuthorsJournal compilation 2007 Blackwell Publishing Ltd, Plant, Cell and Environment, 30, 10861106

identification and quantification (von Caemmerer & Farqu-har 1981; Hikosaka et al. 2006).The initial slope of the A/Ciresponse at light saturation usually is a direct reflection ofRubisco capacity, while the slope of the A/Ci response atelevated CO2 distinguishes between an RuBP regenerationlimitation (if a positive slope is present) and the Pi regen-eration limitation (if the slope is absent or negative)(Sharkey 1985a; Sage et al. 1990a). Often, at intermediateCO2 levels, there is a region of curvature in the responsewhere it is not obvious which process is limiting. This mayoccur because of colimitation by multiple processes, orbecause the CO2 level corresponds to regions where boththe Rubisco limitation and the RuBP regeneration limita-tion show similar responses to CO2 variation (e.g.Wise et al.2004). To evaluate these possibilities, it is necessary tomodel the A/Ci response using estimated Rubisco Vcmax(from either gas exchange or in vitro assessments), esti-mated Jmax (from either gas exchange, chlorophyll fluores-cence or in vitro assessments) and the Pi regenerationcapacity, which is estimated from the CO2 saturated rate ofA under conditions where photorespiration occurs(Sharkey 1985a,b). Some caution is required, because therecan be substantial variation in the values of kinetic con-stants for Rubisco, mesophyll conductance and light usage(von Caemmerer & Quick 2000; Bernacchi et al. 2002;Yamori et al. 2006b). In addition, it is possible that processesnot parameterized in the classical version of the Farquharet al.model and its derivatives (e.g. Harley & Sharkey 1991;Medlyn, Loustau & Delzon 2002) may become limiting. Forexample, the activation state of Rubisco may become lim-iting in certain circumstances such as low O2 and low CO2,or high temperature (Sage, Cen & Li 2002; Crafts-Brandner

& Salvucci 2004). In such cases, the models must be adjustedto account for new types of limitation if they are to retainpredictive power. One must also be sure the Vcmax and Jmaxestimates are reasonably correct. Failure to account for thepossibility that Pi regeneration is limiting at the CO2 satu-ration point can lead to serious errors in Jmax estimates, andassumptions that the initial slope of the A/Ci response aredetermined by Vcmax can be in error at low light or extremetemperatures (Sage et al. 1990b; Harley & Sharkey 1991).To demonstrate how temperature theoretically affects

the biochemical limitations on A, we have modelled A/Ciresponses at four temperatures using input parametersfrom tobacco (Fig. 2) (Bernacchi et al. 2001, 2002, 2003). InFig. 2, the predicted A/Ci curve shows a modest responseof the initial slope to temperature variation below 20 C,but little response above 20 C. Photorespiration and mito-chondrial respiration increase with rising temperature(Brooks & Farquhar 1985; Sharkey 1988; Sage et al. 1990a),increasing the CO2 compensation point and shifting theA/Ci curve to higher Ci. The most pronounced effect ofincreasing temperature is on the CO2-saturated plateau,which typically rises with a Q10 near 2 below the thermaloptimum (Sage 2002).This rise in the plateau reflects eithera rise in the electron transport capacity or a rise in the Piregeneration capacity, both of which have a high thermaldependence below the photosynthetic thermal optimum(Sage, Santrucek & Grise 1995; Leegood & Edwards 1996;Yamasaki et al. 2002;Cen & Sage 2005). In the simulation inFig. 2, the Pi regeneration capacity sets a ceiling on A at 10and 20 C, but rises above the RuBP regeneration capacityat 30 C and above. Pi regeneration has a greater thermaldependence than RuBP regeneration because of a high Q10of sucrose and starch synthesis (Pollock & Lloyd 1987; Stitt& Grosse 1988; Leegood & Edwards 1996).As a result, theA/Ci response shifts from being completely CO2 insensitiveabove a Ci of 200400 mbar at 10 and 20 C, respectively,to exhibiting CO2 sensitivity of gradually decreasing slopeabove a Ci of 400 mbar at 30 and 40 C.At 10 C, the ceilingimposed on A by the Pi regeneration capacity lowers theCO2 saturation point below the operational Ci, causingA tobecome CO2 insensitive at current atmospheric CO2 levelsand below.

Models of the temperature response of C3photosynthesisThe theoretical temperature responses of A that corre-spond to the A/Ci responses in Fig. 2 are shown for inter-cellular CO2 partial pressures corresponding to thePleistocene minimum level (180 mbar), current levels ofCO2 (380 mbar) and future CO2 levels (700 mbar) (Fig. 3).Ata Ci of 150 mbar, our model demonstrates how the A/Tcurve is controlled by Rubisco capacity down to 10 C, atwhich point Pi regeneration capacity becomes limiting.Electron transport capacity is non-limiting at 150 mbarexcept above 45 C, where a strong decline in the electrontransport capacity can cause the RuBP regeneration capac-ity to fall below the Rubisco capacity.

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Figure 1. The oxygen sensitivity of photosynthesis inScrophularia desertorum and Populus fremontii growing naturallyin a field near Reno, NV, USA. Oxygen sensitivity is calculated asdescribed in the text. The theoretical oxygen sensitivity assumingan ribulose bisphosphate (RuBP) regeneration limitation on netCO2 assimilation (A) is shown as the thick grey curve. Thedashed line shows where O2 sensitivity is zero, and hence wherephotosynthesis is fully limited by the Pi regeneration capacity(Sage & Sharkey 1987).

1088 R. F. Sage & D. S. Kubien


At all three CO2 levels, the modelled temperatureresponses of Pi regeneration capacity are identical becauseCO2 supply does not affect the triose phosphate use rateestablished by starch and sucrose synthesis (Fig. 3)(Sharkey 1985a,b). By contrast, the rise in CO2 from 150 to300 and 600 mbar stimulates the Rubisco and RuBPregeneration-limited values ofA, such that the limitation bythe Pi regeneration capacity controls A to higher tempera-ture.At a Ci of 300 mbar,A is limited by Pi regeneration upto 18 C, while at a Ci of 600 mbar, Pi regeneration limits Aup to 23 C.As the limitation caused by the Pi regenerationcapacity becomes pronounced, theA/T response develops asteeper thermal response, reflecting a highQ10 of starch andsucrose synthesis.Rubisco capacity limits A at intermediate temperatures

at 300 mbar, forming the broad thermal optimum often seenin the A/T response of C3 plants at current CO2 levels(Ferrar, Slatyer & Vranjic 1989; Hikosaka, Murakami &Hirose 1999; Sage 2002; Atkin et al. 2006). Our simulationshows that Rubisco-limited A gradually declines above thethermal optimum at 300 mbar, until about 40 C, where theelectron transport capacity asserts control. At this point,the drop-off in A with further increases in temperature, ispronounced, following the rapid decline modelled for theelectron transport capacity.Increasing CO2 stimulates Rubisco-limitedA through the

combined effect of the increased substrate availability andthe suppression of photorespiration; rising CO2 enhancesRuBP regeneration-limitedA only by suppressing photores-piration (von Caemmerer 2000). Consequently, Rubisco-limited A increases more with rising CO2 than RuBPregeneration-limitedA.At 600 mbar, the elevated CO2 levelallows Rubisco-limitedA to be in excess at all temperatures,and as a result, the response of A to temperature is

dominated by electron transport capacity above the tem-perature where Pi regeneration capacity is limiting (Fig. 3).The thermal optimum narrows and forms a sharp peak thatoften mirrors the thermal optimum observed for electrontransport in vitro (Mawson & Cummins 1989; Sage et al.1995; Yamasaki et al. 2002; Cen & Sage 2005). The thermaloptimum has also shifted to higher temperature, reflectingthe reduced impact of photorespiration at elevated CO2.

Empirical observationsThemodelled responses presented in Fig. 2 are qualitativelysimilar to A/Ci responses determined on a wide range of C3species, including bean (von Caemmerer & Farquhar 1981);Eucalyptus (Kirschbaum & Farquhar 1984); soybean(Harley,Weber&Gates 1985); chili pepper, tomato,Populusfremontii and Scrophularia desertorum (Sage & Sharkey1987); rice (Makino, Nakano & Mae 1994); alfalfa (Ziska &Bunce 1994); oak (Hikosaka et al. 1999); Abutilon theo-phrastii (Ziska 2001);Chenopodiumalbum (Sage 2002);pine(Medlyn et al. 2002); grape (Hendrickson et al. 2004b); pimacotton (Wise et al. 2004); and sweet potato (Cen & Sage2005). Considerable variation is observed, which generallyreflects species difference and growth regime effects on theabsolute capacities as well as the ratios of the three majorlimitations (Medlyn et al. 2002). In the species where mod-elled analyses were attempted, there is good agreementbetween observed and simulated responses of A (von Cae-mmerer & Farquhar 1981; Kirschbaum & Farquhar 1984;Bernacchi et al. 2001, 2003; Cen & Sage 2005; Hikosakaet al. 2006). As commonly modelled, the initial slope ofthe A/Ci response is moderately stimulated by increasingtemperature below 20 C, with a Q10 between 1.2 and 1.6;above 20 C, the thermal response of the initial slope flattens

Figure 2. Modelled responses of netCO2 assimilation (A) to intercellularpartial pressures of CO2 in leaves oftobacco at (a) 10 C, (b) 20 C, (c) 30 Cand (d) 40 C. The response of A(indicated by the dotted blue curves) isdelineated by the minimum value of theribulose 15-bisphosphatecarboxylase/oxygenase (Rubisco)-limitedA (solid curve), ribulose bisphosphate(RuBP) regeneration-limited A (dashedcurve) and Pi regeneration-limited A(grey line) at any given Ci value.Modelled according to Bernacchi et al.(2001, 2002, 2003) using a Vcmax value of80 mmol m-2 s-1 at 25 C, a Jmax value of150 mmol m-2 s-1 and a triose phosphateuse rate of 10 mmol m-2 s-1 at 25 C. At25 C, we assumed that Vomax was0.25 Vcmax (von Caemmerer 2000).

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and then declines at elevated temperature (Kirschbaum &Farquhar 1984; Ziska 2001; Cen & Sage 2005; Yamori,Noguchi & Terashima 2005). Modest declines in the initialslope at high temperature are predicted from the tempera-ture responses of carboxylation kinetics, mesophyll conduc-tance and respiration (Kirschbaum & Farquhar 1984);however, some species such as oak (Tenhunen et al. 1984)and spinach (Yamori et al. 2005) show larger fractionaldeclines than carboxylation kinetics would predict. Inthese species, there is good evidence that deactivation ofRubisco at elevated temperature causes a limitation on A(Haldimann & Feller 2004; Yamori et al. 2006b). If Rubiscodeactivation does reduce A at low CO2, a model would beunable to predict the initial slope response unless it has beenmodified to incorporate observed changes in the activationstate of Rubisco (Sage et al. 2002; Yamori et al. 2006b).

The short-term response to temperature reduction belowthe thermal optimum has been widely linked to limitationsin Pi regeneration, as indicated by (1) O2 and CO2 insensi-tivity of steady-state photosynthesis; (2) oscillations in Afollowing a change in CO2 or O2 in leaves at low tempera-ture; (3) a high ratio of phosphoglycerate (PGA) to triosephosphates, and elevated levels of phosphorylated immedi-ates in the carbon metabolic pathway; (4) high sensitivity ofA to the application of Pi-sequestering agents to the leaf; (5)the Pi optimum for A in isolated chloroplasts increases atlow temperature; and (6) feeding Pi to leaves transferred tolow temperatures enhances A (Leegood & Edwards 1996,and references therein; Strand et al. 1999;Hendrickson et al.2004b). Pi regeneration limitations are associated withdeclines in RuBP pool size; however, deactivation ofRubisco in response to limitations in Pi regeneration canallow metabolite levels to recover to levels observed whenRubisco capacity is limiting (Sage, Sharkey & Seemann1988; Sharkey &Vanderveer 1989). Limitations by Pi regen-eration capacity at low temperature are not universal.Species adapted or acclimated to cool conditions are lesslikely to be limited by the Pi regeneration capacity (Sage &Sharkey 1987; Makino et al. 1994; Strand et al. 1997, 1999;Savitch, Harney & Huner 2000). In winter- and spring-active S. desertorum plants, for example, O2 sensitivity of Ashowed that Pi regeneration limitations were not presentabove 10 C,while in P. fremontii, a deciduous species that isactive in late spring and summer, Pi regeneration was lim-iting below 20 (Fig. 1).The limitation that predominates at suboptimal tempera-

tures when Pi regeneration capacity is excessive is notalways clear. It is probably Rubisco capacity at low CO2levels (

In sweet potato, Cen & Sage (2005) estimated the tem-perature response of Pi regeneration capacity, electrontransport capacity,RubiscoVcmax and the Rubisco activationstate. With these estimates, they were able to effectivelymodel the A/T response from 9 to 41 C (Fig. 4). Rubisco-limited A matched observed A across most of the tempera-ture range at a Ci of 140 mbar, and at the thermal optimumat current levels of CO2. Rising CO2 increased the tempera-ture sensitivity of A in sweet potato, narrowed the breadthof the thermal optimum and raised the thermal optimum, aspredicted by a shift in limitation from Rubisco to electrontransport capacity. A limitation in the Pi regenerationcapacity was more pronounced at elevated CO2 in sweetpotato than that predicted for tobacco in Fig. 3, such that Piregeneration controlled A up to the thermal optimum atelevated CO2, at which point the model predicted electrontransport capacity became limiting.Contrary to the mentioned observations are proposals

that A declines above the thermal optimum because thecapacity of Rubisco activase to maintain Rubisco in anactivated state declines to limiting levels (Salvucci & Crafts-Brandner 2004a, and the references therein). As a result,Rubisco deactivates to a point where its ability to consumeRuBP limits CO2 assimilation. Reductions in the activationstate of Rubisco are well correlated with reductions in Aabove the thermal optimum in spinach, cotton, tobacco,oak, pea, Antarctic hairgrass and Larrea (Salvucci et al.2001; Haldimann & Feller 2004, 2005; Salvucci & Crafts-

Brandner 2004a,b). The issue of Rubisco activase versuselectron transport limitation above the thermal optimum isdiscussed further below.

MECHANISMS CONTROLLING THETEMPERATURE RESPONSE OF THEPHOTOSYNTHETIC BIOCHEMISTRY INC3 PLANTSRubisco capacityThe response of Rubisco-limited photosynthesis to increas-ing temperature has two general explanations: (1) a changein carboxylation capacity caused by thermal effects on theKm and kcat of Rubisco, and an increase in oxygenase activitythat reflects reductions in both the CO2/O2 ratio in solutionand the relative specificity of Rubisco for CO2 versus O2(Jordan &Ogren 1984; von Caemmerer &Quick 2000).Thedecline in the CO2/O2 solubility with rising temperatureaccounts for about a third of the rise in photorespiration,while the remainder is caused by the reduction in relativespecificity.The decline in relative specificity with increasingtemperature is largely driven by a greater increase in theRubiscoKm for CO2 than theKm for O2 (von Caemmerer &Quick 2000).In most higher plants, the Km and kcat of Rubisco have

similar Q10 values (von Caemmerer & Quick 2000; Sage2002). Some species, such asAtriplex glabriuscula (von Cae-mmerer & Quick 2000), rice (Sage 2002) and a wild tomatospecies (Lycopersicon peruvianum) (Brggemann, Klauke& Maas-Kantel 1994) show an increased Q10 below 15 Cthat reflects an increased activation energy in the kcat.WhentheKmand thekcat of an enzymehave identicalQ10 values,theQ10 of the reaction at CO2 levels below the Km is near 1(Berry & Raison 1981). This explains in part the relativelylow thermal response of the initial slope of the A/Ciresponses and of Rubisco-limitedA at low CO2 levels. Someenhancement of the carboxylation potential with rising tem-perature is observed, although mostly at cooler tempera-tures (

to a narrow thermal optimum (Berry & Bjrkman 1980;Mawson & Cummins 1989; Sage et al. 1995; Yamasaki et al.2002; June, Evans & Farquhar 2004; Cen & Sage 2005).Thisrise in the whole chain electron transport rate with increas-ing temperature has been correlated with temperaturestimulation of energy flow through photosystem II (PSII),and electron flow from the quinones to photosystem I (PSI)(Mawson & Cummins 1989 for S. cernua,Makino et al. 1994for rice and Yamasaki et al. 2002 for winter wheat).Electrontransport capacity is closely correlated with cytochrome f(cyt f) content in rice and spinach, implying that this may bea key rate-limiting step (Makino et al. 1994; Yamori et al.2005). If so, the thermal response of electron flow throughcyt f may be a leading controller of the thermal response ofA at high CO2, as indicated by results from pea and winterwheat (Mitchell & Barber 1986; Yamasaki et al. 2002).The mechanism causing the decline in the electron trans-

port rate above the thermal optimum remains uncertain(June et al. 2004).A leading proposal is that cyclic electrontransport is activated at elevated temperature at theexpense of linear electron transport, thereby causing ashortage of NADPH (Bukhov et al. 1999; Sharkey &Schrader 2006). In barley, elevated temperature is proposedto activate cyclic electron flow by diverting electrons fromthe NADPH pool to the plastoquinone pool (Egorova &Bukhov 2002; Egorova et al. 2003; Bukhov, Dzhibladze &Egorova 2005). In pima cotton, enhanced cyclic photophos-phorylation may explain reductions in the stromal oxida-tion state observed above the thermal optimum (Schraderet al. 2004). The rise in cyclic electron flow above thethermal optimum increases the thylakoid pH gradient,thereby activating photoprotective quenching and causing adissociation of the outer light harvesting antennae fromPSII (Sharkey & Schrader 2006). Electron flow throughPSII decreases above the thermal optimum in a patternthat mimics a decline in whole chain electron transport(Yamasaki et al. 2002 for winter wheat); by contrast, elec-tron flow rate through PSI is stable between the thermaloptimum for photosynthesis and 40 C, indicating it hashigh capacity to support enhanced cyclic electron flow atelevated temperature (Berry & Bjrkman 1980; Havaux1993a; Yamasaki et al. 2002). Non-photochemical quench-ing of PSII is widely observed at temperatures where elec-tron transport capacity slows with rising temperature,indicating that the reduction in electron flow through PSIIis a regulatory response to limitations further down theelectron transport chain (Yamasaki et al. 2002; Salvucci &Crafts-Brandner 2004b; Schrader et al. 2004). Consistently,Yamasaki et al. (2002) demonstrated that the capacity forelectron transfer from plastoquinone to P700 declinesabove the thermal optimum, implicating electron flowbetween the photosystems as a possible cause for thedecline in the electron transport rate.Inactivation of the water-spitting complex is also impli-

cated as a cause of heat-induced reductions in electrontransport capacity, particularly at high temperatures (above38 C in potato and above 40 C in spinach) (Havaux 1993a;Enami et al. 1994). At moderately warm temperatures, this

lesion is probably not significant, as leaves can readily alterPSII properties to reduce heat sensitivity of the water-splitting complex (Havaux 1993b). Furthermore, the thyla-koid membrane becomes leaky at higher temperature,potentially uncoupling electron flow from photophosphory-lation (Schrader et al. 2004). This is not thought to be adirect cause of the decline in A at elevated temperature,because ATP levels and the pH gradient remain high dueto the rerouting of electrons from NADPH back to PSI(Sharkey& Schrader 2006).The activation of cyclic electronflow at the expense of linear flow is proposed to protectPSII from damage at high temperature by inducing photo-protective quenching, stabilizing the thylakoid membranethrough enhanced zeaxanthin formation, and reducing thesize of the PSII light-harvesting antennae (Tardy & Havaux1997; Bukhov et al. 1999; Schrader et al. 2006; Sharkey &Schrader 2006).

Calvin cycle capacityCalvin cycle limitations on A have been explored at thethermal optimum,most directly through the use of antisensetransgenics deficient in key enzymes of the pathway (Raines2003).Of the examinedCalvin cycle enzymes,sedoheptulose1,7-bisphosphate (SBPase) exerts the greatest control, withmodest (

the direct thermal sensitivity of the rate-limiting steps inthe pathway, and temperature effects on the sensitivity ofsucrose phosphate synthase (SPS) and FBPase to regula-tory molecules (Leegood & Edwards 1996). In spinach, SPShas a Q10 of 2.4 in the light, and cytosolic FBPase showedhigh thermal sensitivity in its response to effectors; inhibi-tion of FBPase caused by Pi fell threefold, fructose-2,6-bisphosphate inhibition fell fourfold and AMP inhibitiondeclined 30-fold between 8 and 35 C (Stitt & Grosse 1988).More triose-P was also needed to activate FBPase at lowtemperature in spinach (Stitt & Grosse 1988).

Rubisco activaseAt the thermal optimum, the activation state of Rubiscodeclines in response to shading or elevated CO2(Perchorowicz, Raynes & Jensen 1981; Kobza & Seemann1988; Sage et al. 1988; Woodrow & Berry 1988). In bothcases, Rubisco deactivation is considered a regulatoryresponse to a shift in limitation away from Rubisco capacityto either RuBP or Pi regeneration capacity (Mott et al.1984; Sage 1990; von Caemmerer & Quick 2000). The iden-tification of Rubisco activase as the main regulatory proteinfor Rubisco provided a mechanistic explanation for thepatterns of Rubisco deactivation in response to shade orCO2 enrichment (Spreitzer & Salvucci 2002; Portis 2003).Rubisco activase consumes ATP and reducing power in areaction sequence that frees tightly bound phosphorylatedsugars from Rubisco catalytic sites. Removal of the sugarphosphates allows for spontaneous carbamylation, whichthen activates the catalytic site, or frees the carbamylatedcatalytic site of bound inhibitors. ADP is an importantinhibitor of activase, and activase requires ATP and reduc-ing power to exist in its most active configuration. Activeactivase typically occurs in aggregates of 8 to 16 subunits,which are assembled from inactive dimers and monomersusing ATP and reducing power in a thioredoxin-dependentreaction (Zhang & Portis 1999; Zhang et al. 2002).Away from the thermal optimum, the activation state of

Rubisco declines, particularly at elevated temperature. Atsuboptimal temperature, the reduction in the activationstate is inconsistent, and has been linked to an inhibition onA by a Pi regeneration capacity (Hendrickson et al. 2004b;Cen & Sage 2005). The reduction in the activation stateabove the thermal optimum is widely observed and is pro-posed to limit A (Weis 1981b; Kobza & Edwards 1987;Portis 2003; Haldimann & Feller 2004, 2005; Salvucci &Crafts-Brandner 2004a,b,c). Early evidence in support of alimiting role of the Rubisco activation state was a rise inRuBP pools and RuBP/PGA ratios, which indicate a con-striction at the carboxylation step at elevated temperatures(Weis 1981a; Kobza & Edwards 1987). Later studiesshowed Rubisco activase to be heat labile at temperaturescorresponding to those where A and the activationstate of Rubisco decline (Law & Crafts-Brandner 1999;Crafts-Brandner & Salvucci 2000; Salvucci & Crafts-Brandner 2004b; Haldimann & Feller 2005). In addition,observed increases in the heat stability of Rubisco activase

during acclimation or adaptation to high temperaturecorresponded to enhancements in A above the thermaloptimum (Law & Crafts-Brandner 1999; Salvucci & Crafts-Brandner 2004a,b). Modelled simulations of the tempera-ture response of A assuming a Rubisco limitation predictedobserved A if the capacity of deactivated Rubisco was usedin the model; simulations assuming fully activated Rubiscooverestimated observed A (Crafts-Brandner & Salvucci2000; Salvucci & Crafts-Brandner 2004b).Numerous mechanisms are proposed to explain the

reduction in the Rubisco activation state at elevated tem-perature. Firstly, increasing temperature speeds the produc-tion of inhibitors by misprotonation of RuBP duringcatalysis; if activase capacity is limiting, faster misprotona-tion will reduce the number of functional active sites(Crafts-Brandner & Salvucci 2000; Salvucci & Crafts-Brandner 2004a,c; Kim & Portis 2006). Recent work bySchrader et al. (2006) indicates that this may not be a majorcause of deactivation, because the Rubisco catalytic sitesalso release the misprotonated inhibitors more rapidly atelevated temperature. Secondly, active oligomers of acti-vase more readily dissociate into inactive dimers and mono-mers above the thermal optimum, causing a loss of activasecapacity (Crafts-Brandner & Law 2000; Salvucci & Crafts-Brandner 2004a). Finally, in many species at 4245 C,activase subunits irreversibly denature into insoluble com-plexes that lack the ability to hydrolyseATP (Feller, Crafts-Brandner & Salvucci 1998; Salvucci et al. 2001; Salvucci &Crafts-Brandner 2004a,b; Haldimann & Feller 2005);however, this does not occur in oak (Haldimann & Feller2004).The elegance of the activase lability hypothesis led to its

rapid and widespread acceptance, and efforts are nowunderway to improve heat tolerance of photosynthesis byenhancing the thermal tolerance of activase (Spreitzer &Salvucci 2002; Zhu et al. 2005; Wu et al. 2006). We are notconvinced, however, that heat lability of Rubisco activasealways explains the decline in A above the thermaloptimum, largely because no study has demonstratedactivation state limitations using photosynthetic modelsthat have parameterized electron transport capacity andRubisco capacity in its fully active and deactivated condi-tion. In all studies where an activation state limitation hasbeen proposed, only the response of Rubisco-limitedA wasmodelled, if any modelled analysis was conducted at all.Consequently, we cannot rule out an electron transportlimitation on A, with the decline in the Rubisco activationstate occurring as a regulatory response.By contrast, studiesusing models with electron transport algorithms demon-strate the thermal response of measured A at elevated tem-perature is consistent with the thermal response of electrontransport-limited A (Bernacchi et al. 2001, 2003; Wise et al.2004; Cen & Sage 2005; Hikosaka et al. 2006).Proponents of the activase hypothesis claim to have ruled

out the potential for electron transport limitations based ona rise in RuBP : PGA ratios, sustained ATP/ADP pools inleaves, a rise in non-photochemical quenching above thethermal optimum, and the presence of a CO2 stimulation of



A at 10 mbar O2 and high temperature (Woodrow & Berry1988; Law & Crafts-Brandner 1999; Portis 2003; Crafts-Brandner & Salvucci 2004; Salvucci & Crafts-Brandner2004a; Kim & Portis 2005). The RuBP : PGA increase isperhaps the best evidence in support of an activase limita-tion; however, RuBP : PGA can increase when RuBP or Piregeneration capacities are limiting because of deactivationof Rubisco and other Calvin cycle enzymes (Mott et al. 1984;Sage et al. 1988; Schrader et al. 2004). To evaluate the truelimitation, the response of RuBP pools should be followedimmediately after a rapid increase in temperature. The evi-dence here is uncertain,with reports showing both a decline(Schrader et al. 2004) and a rise in RuBP pools (Crafts-Brandner & Salvucci 2004) following a sudden increase intemperature. The evidence for a rise in non-photochemicalquenching is not definitive, because the heat-induced diver-sionofPSI complexes from linear to cyclic electron transportwould maintain high ATP/ADP and a high pH gradient,thereby promoting non-photochemical quenching at PSII(Sharkey & Schrader 2006).The proposal that a CO2 stimulation of A at high tem-

perature and low O2 is evidence of an activase limitationshould be evaluated with theoritical models of photosyn-thesis to rule out other possible limitations.The importanceof a modelled assessment is demonstrated in Fig. 5, whichpresents anA/Ci response measured for cotton at 42 C and10 mbar O2 (table 5 in Crafts-Brandner & Salvucci 2004).Wemodelled theA/Ci response corresponding to these datausing the Rubisco activity reported for cotton by Crafts-Brandner & Salvucci (2004) and a Jmax value estimated fromthe gas exchange curve in Fig. 5.No deactivation of Rubisco

was assumed in our model. Crafts-Brandner & Salvucci(2004) argued that because A in cotton at 42 C and low O2was stimulated by CO2 enrichment, RuBP regenerationcapacity could not be limiting, given that photorespirationwould have been nil. Instead, they reasoned, A had toreflect a limitation in the Rubisco activation state.As shownin Fig. 5, our modelled Rubisco-limited response matchesthe observedA/Ci response below 450 mbar,whereA is CO2sensitive. The modelled RuBP regeneration rate matchesthe observed A above 450 mbar, where A is CO2 insensitive.This analysis demonstrates that at 42 C and 10 mbar O2,cotton is not limited by deactivation of Rubisco.Recently, Cen & Sage (2005) examined limitations on A

above the thermal optimum using sweet potato. Theyhypothesized that if the activation state of Rubisco wereregulated in response to limitations in RuBP regenerationcapacity at elevated temperature, then any perturbation inthe ratio of RuBP regeneration to RuBP consumptioncapacity would alter the activation state of Rubisco in apredictable manner. By contrast, if the heat lability ofRubisco activase were limiting A, then the activation statewould decline regardless of changes in RuBP regeneration/consumption. Lowering CO2 causes a rise in RuBPregeneration/consumption, and eventually allows Rubiscocapacity to become limiting (Fig. 6a). If Rubisco were deac-tivated at high temperature and high CO2 in response to alimitation in electron transport capacity, then CO2 reduc-tion should reactivate Rubisco. In sweet potato, the activa-tion state of Rubisco markedly declined above 30 C at a Ciof 500 mbar, and above 35 C at current CO2 levels (Fig. 6b).Deactivation was also apparent below 15 C at each ofthese CO2 levels.At low CO2 (a Ci of 140 mbar), the activa-tion state recovered to near maximum values at high andlow temperatures, consistent with modelled predictions thatreactivation would occur when RuBP regeneration capacitywas limiting. Lowering CO2 also increases the activationstate of Rubisco in heated cotton leaves (Crafts-Brandner& Salvucci 2000).The slight deactivation that was observedin sweet potato at high temperature in the low CO2 treat-ment corresponded to a predicted limitation in electrontransport capacity in the low CO2 conditions above 40 C(Cen & Sage 2005). Notably, in the low CO2 region whereRubisco capacity was predicted to be limiting (see Fig. 4),Cen & Sage (2005) were able to effectively model theobserved initial slope of A using Vcmax values determinedin vitro. Furthermore, the observed RuBP pool declinedslightly with rising temperature, which is consistent with anRuBP regeneration limitation on A above the thermaloptimum (Cen & Sage 2005).The discrepancies between the results of Cen & Sage

(2005) and prior studies proposing an activase limitation onA at high temperature may simply reflect species variationin the sensitivity of activase to elevated temperature. Sweetpotato is relatively heat tolerant as it is a warm-season crop,and thus may have a heat-stable form of activase. Spinach isnot heat tolerant, and exhibits contrasting responses thatare consistent with an activase limitation. For example,RuBP pools rise with temperature in spinach (Weis 1981a),

Intercellular CO2 (mbar)

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Figure 5. The CO2 response of the net CO2 assimilation rate(A) in cotton measured at 10 mbar O2 and 42 C byCrafts-Brandner & Salvucci (2004; table 5), and the modelledresponse of ribulose 15-bisphosphate carboxylase/oxygenase(Rubisco)-limited A assuming full activation of Rubisco, and theribulose bisphosphate (RuBP) regeneration-limited A. Theresults were modelled according to Bernacchi et al. (2001, 2002,2003) using a Rubisco Vcmax of 66 mmol m-2 s-1 (the mean of threetotal activity assays from table 3 of Crafts-Brandner & Salvucci(2004) and a Jmax value of 123 mmol m-2 s-1 (determined from theA value shown here at 1000 mbar CO2).



and its initial slope of the A/Ci response rapidly declinesabove the thermal optimum of A in concert with a loss ofRubisco activation (Yamori et al. 2006a). Alternatively, theapparent heat lability of activase may reflect a regulatoryresponse to declining electron transport capacity. This pos-sibility is supported by results that show increased heatstability of the active form of activase at high ATP levelsand redox status (Crafts-Brandner, van de Loo & Salvucci1997; Portis 2003). In tobacco extracts, the addition ofATPgS increased the temperature where activase formedinsoluble aggregates from 37 to 45 C (Salvucci et al. 2001).One possibility that has not been fully evaluated is thatRubisco deactivation between the thermal optimum and4042 C may be a regulatory response to a limitation inelectron transport capacity,while above 42 C, denaturationof activase may reduce the activation state of Rubisco tosuch a degree that it directly limits A. Cen & Sage (2005)did not evaluate this possibility because they examinedresponses below 42 C.

ACCLIMATION OF C3 PHOTOSYNTHESIS TOCHANGES IN GROWTH TEMPERATUREGeneral considerationsMost plant species are able to acclimate to changes ingrowth temperature by modifying the photosynthetic appa-ratus in a manner that improves performance in the newgrowth environment. In general, following a change ingrowth conditions by 510 C, the thermal optimum shiftsin the direction of the new growth temperature, and the rateof A increases at the growth temperature while the rate onthe other side of the thermal optimum decreases (Fig. 7)(Regehr & Bazzaz 1976; Berry & Bjrkman 1980; Mawsonet al. 1986; Yamori et al. 2005). Variations are apparentdepending on growth conditions and species. For example,A often declines at all measurement temperatures in C3plants grown at temperatures approaching their high or lowtemperature limit (Kemp & Williams 1980 for Agropyronsmithii grown at 20 versus 35 C days; Kubien & Sage 2004b


10 20 30 40

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Figure 6. The temperature response in sweet potato of (a) the modelled response of the capacity for ribulose bisphosphate (RuBP)regeneration relative to the capacity of RuBP consumption at 140, 250 and 500 mbar CO2, and (b) the ribulose 15-bisphosphatecarboxylase/oxygenase (Rubisco) activation state measured at the indicated intercellular CO2 partial pressures of 140 (solid circle),250 (open square) and 500 (solid triangle) mbar. The ratio of the RuBP regeneration capacity to the RuBP consumption capacity wasmodelled according to Sage (1990) with input parameters as described in Cen & Sage (2005). If the activation state of Rubisco isregulated to balance a limitation in RuBP regeneration capacity (which includes a Pi regeneration limitation in this model), then it ispredicted that the activation state of Rubisco will decline below an RuBP regeneration to consumption ratio of 1.0 (from Cen and Sage,2005 by permission).

Figure 7. A schematic demonstratingthe typical pattern of thermal acclimationobserved in most C3 plants, with asummary of the leading potential driversof the acclimation response.

Current CO2

3. Heat acclimation:

A. Respiratory decline

B. Increased electron transport capacity

C. Synthesis of a heat stable Rubiscoactivase

1. Increased protein content

2. Cool acclimation:

A. Enhanced starch andsucrose synthesis (O2sensitivity returns)

B. Enhanced electron transport capacity(O2 sensitivity unaffected)

C. Enhanced Rubiscocontent (O2 sensitivityunaffected)



for Calamagrostis canadensis grown at 26 versus 14 Cdays). Furthermore, acclimation that shifts the thermaloptimum appears to require shifting growth regimes to non-optimal temperatures. In C. album (Sage et al. 1995) andbean (Cowling & Sage 1998), the thermal optimum wasunaffected between plants grown slightly below (2325 C)and above (3436 C) the thermal optimum of A.Variationin the acclimation response caused by species differencesmay reflect the degree of thermal specialization (Osmond,Bjrkman & Anderson 1980). In the genus Plantago, fast-growing species from lowland environments show greateracclimation than slow-growing species from high elevations,indicating that specialization for extreme environmentsmay restrict the potential for thermal acclimation (Atkinet al. 2006).Often, reducing growth temperature increases photosyn-

thetic capacity per unit area at the thermal optimum.This iscaused in part by temperature effects on leaf development.Cool-grown leaves are often thicker, with larger cells,greater cell volume, higher leaf nitrogen content and anoverall increase in many (but not all) photosyntheticenzymes (Boese & Huner 1990; Huner et al. 1993; Strandet al. 1999; Yamori et al. 2005). In contrast to these benefi-cial responses, when growth temperature is altered enoughto cause thermal stress, there is typically a prolongeddecline in photosynthetic potential at all temperatures thatis associated with photoinhibition and loss of leaf protein(Maruyama, Yatomi & Nakamura 1990; Brggemann,Vanderkooij & Vanhasselt 1992; Brggemann & Linger1994; Byrd, Ort & Ogren 1995; Hewezi et al. 2006).An important component of thermal acclimation is an

alteration in membrane composition to shift the thermalrange where membranes are fluid yet stable towards thegrowth temperature. Between 20 and 40 C, this is accom-plished by altering the ratio of saturated to unsaturatedfatty acids in the lipid matrix (Huner 1988; Mikami &Murata 2003). Saturation of fatty acids increases thenumber of hydrophobic interactions between adjacent fattyacids, thereby increasing the rigidity of the membrane(Hochachka & Somero 2002). For this reason, increasingsaturation of fatty acids is considered an acclimationresponse to higher temperatures and is associated withincreased thermotolerance in a wide range of species(Sharkey & Schrader 2006). The cost of increased satura-tion of fatty acids could be a loss of fluidity at lower tem-peratures, however, with a potential for reduced stabilityand turnover of membrane-bound enzymes (Mitchell &Barber 1986).Acclimation associated with changes in fatty acid compo-

sition is relatively slow, requiring many hours to a few daysto be effective.As such, this mechanism of acclimation is tooslow to response to rapid changes in leaf temperature overthe course of the day, as may occur in response to suddenenhancements in light level or a reduction in wind speed(Wise et al. 2004; Sharkey 2005). Over the short term(minutes to hours), membrane fluidity is stabilized by therapid production of zeaxanthin and small molecules thatincrease membrane hydrophobicity, such as isoprenes

(Sharkey 2005). Zeaxanthin levels are stimulated by thehigh pH gradient associated with induction of cyclicphotophosphorylation by heat (Tardy & Havaux 1997).Zeaxanthin increases the rigidity of the thylakoid mem-brane in addition to serving a photoprotective role, and maythus help maintain membrane integrity and electron trans-port capacity above the thermal optimum (Havaux 1998).The rate of respiration in the light also acclimates to

rising temperature. Respiration rates generally rise withmeasurement temperature; however, day respirationdeclines in many species following growth at elevatedtemperature, and may approach the rate observed at theoriginal growth temperature (Atkin et al. 2005, 2006). Thischange affects the thermal response of A, particularly inplants with thick leaves and low photosynthetic capacities,such as conifers (Way & Sage, unpublished data). In suchcases, the respiration rate must be estimated and factoredout (e.g. by evaluating responses of gross photosynthesis) ifone is to evaluate acclimation of the photosynthetic bio-chemistry. For detailed discussion of the thermal acclima-tion of respiration, see Atkin et al. (2005).

Mechanisms of photosynthetic acclimation totemperature variationFollowing transfer to cooler conditions, cold-adapted plantstypically show an increase inA below the thermal optimum,and a reduction in A above the thermal optimum thatresults in a lowering of the peak temperature for photosyn-thesis (Fig. 7) (Berry & Bjrkman 1980; Huner, Migus &Tollenaar 1986; Mawson et al. 1986; Holaday et al. 1992;Savitch et al. 2000; Yamasaki et al. 2002; Yamori et al. 2005;Atkin et al. 2006; Hikosaka et al. 2006).Acclimation to coolconditions is associated with increased O2 and CO2 sensi-tivity at low measurement temperatures, indicating a dis-proportional enhancement of the Pi regeneration capacity(Badger, Bjorkman & Armond 1982; Huner et al. 1986;Mawson et al. 1986; Makino et al. 1994; Hurry et al. 1995a;Savitch et al. 2001; Ziska 2001). As a result, the degree towhich Pi regeneration limits A is reduced if not eliminated(Hurry et al. 1995a; Savitch, Gray & Huner 1997; Strandet al. 1999; Savitch et al. 2001). At current CO2 levels, fewstudies have characterized the limitation that predominatesbelow the thermal optimum following low temperatureacclimation. In oak and Plantago, theoretical analyses indi-cate that it is Rubisco capacity (Hikosaka et al. 1999), whilein wheat and Arabidopsis it may still be Pi regeneration,although to a lesser degree (Savitch et al. 1997, 2001).The enhancement of the Pi regeneration capacity has two

causes, one that operates rapidly (within hours) and onethat is slower and requires protein synthesis. The rapidresponse is associated with an increase in Pi and metabolitelevels within the cytosol and chloroplast, reflecting a releaseof Pi from the vacuole (Leegood & Furbank 1986; Labate &Leegood 1988; Hurry et al. 1995a; Leegood & Edwards1996; Strand et al. 1999). This rise in Pi restores the Pibalance needed for optimal enzyme activity, and theelevated metabolite pools overcome increased substrate



requirements for high enzyme turnover (Hurry et al. 1995a;Leegood & Edwards 1996; Strand et al. 1999).The second response is to increase the expression of the

enzymes of starch and sucrose synthesis. Activities ofenzymes supporting sucrose synthesis [cytosolic fructosebisphosphatase, SPS and/or sucrose synthase] increase incold hardy winter cereals:winter wheat and rye (Hurry et al.1994, 1995a; Savitch et al. 1997, 2000), rice (Makino et al.1994),winter rape (Hurry et al. 1995b), spinach (Guy,Huber& Huber 1992; Holaday et al. 1992; Martindale & Leegood1997a,b), cold-tolerant alfalfa (Antolin, Hekneby &Sanchez-Diaz 2005) and Arabidopsis (Strand et al. 1999,2003). Inmost of these cases, the increase in SPS and FBPaseactivity in low temperature conditions is disproportional tochanges in other leaf proteins such as Rubisco (Strand et al.1999). For example, Makino et al. (1994) demonstrated thatrice plants grownat 18/15 C (day/night) had greater FBPaseandSPSactivities relative toRubisco,leafNand cyt f contentthan rice plants grown at 23/18 and 30/23 C.The cool-grownrice also had a greater increase in CO2-saturated A, indicat-ing a relaxation of aPi regeneration limitation (Makino et al.1994). There is also an increase in sucrose export followinglow temperature acclimation, indicating adjustments inphloem loading that alleviate feedback limitations in thecold (Strand et al. 1997,1999).Paul,Lawlor&Driscoll (1990)observed that an increase in carbon export from rape leaveswas associated with an increase in O2 sensitivity duringacclimation to low temperature.The rise in A during acclimation to low temperature is

rarely associated with just changes in Pi status and sucrosesynthesis capacity, which complicate the understandingof the predominant limitations on A after acclimation(Leegood & Edwards 1996; Strand et al. 1999). A generalrule is that at low temperature, the kcat of enzymes is slowedsubstantially because of a reduced fraction of enzymeshaving sufficient internal energy to meet activation energythresholds for catalysis (Hochachka & Somero 2002). Tocompensate, plants can increase enzyme levels or shiftprotein expression to produce isoforms with improvedperformance at low temperature. The former commonlyoccurs, and there is some evidence that the latter can also beof significance. At lower growth temperature (4/2 C day/night), winter rye expresses an isoform of Rubisco withhigher affinity for CO2 than warm- (25/20 C) grown rye(Huner & Macdowall 1979). In spinach, an isoform ofRubisco expressed in warm growth conditions (30/25 C)has greater specificity at elevated temperature, but a lowerspecificity at cooler temperatures than an isoformexpressed in plants grown at 15/10 C (Yamori et al. 2006b).The warm-grown isoform also exhibits a break in theArrhenius curve at 15 C, indicating that its activationenergy is increased at low temperature. Consistently, CO2compensation points differed between plants expressing thetwo isoforms, being greater at high temperature and lowerat low temperature in the cool-grown plants (Yamori et al.2006b).In addition to the enzymes of sucrose synthesis, Rubisco

activity often increases during acclimation to cooler

temperatures as seen in Arabidopsis (Strand et al. 1997),winter rape (Hurry et al. 1995b), rye (Hurry et al. 1995a),spinach (Holaday et al. 1992; Yamori et al. 2005) and wheat(Hurry et al. 1995b; Savitch et al. 1997). Calvin cycleenzymes (d-glyceraldehyde-3-phosphate dehydrogenase,aldolase, transketolase) also increase during cold acclima-tion in Arabidopsis (Strand et al. 1999).Whether these dif-ferences affect patterns of limitation depend upon whetherthe increase is disproportional, and here the record is lessclear. Recently, Yamori et al. (2005) provided a detailedassessment of thermal acclimation in spinach. In theirplants, the leaf N content was approximately 50% greater inleaves grown at 15/10 C versus those produced at 30/25 C.Associated with this was a near doubling in Rubisco and cytf levels, and a near threefold increase in leaf mass per area.These changes did not correlate with increased Rubiscocapacity in vivo, as the maximum value of the initial slopewas similar in the two growth conditions. Instead, the CO2-saturated rate of A increased in concert with a rise in cyt fcontent, and the electron transport capacity rose relative tothe Rubisco Vmax. In rice, a warm season grass, there was nochange in Rubisco or leaf N content with a shift in growthtemperature from 30/23 to 18/15 C (Makino et al. 1994).Ata given leaf N level, the content of cyt f and the couplingfactor were unchanged between the temperature treat-ments, while the content of light-harvesting complex II(LHCII) and chlorophyll decreased in the cool-grownplants. This indicates a reduction in electron transportcapacity in cool- versus warm-grown rice. With the rise inFBPase and SPS, it appears that cool-grown rice hasreallocated its internal resources to boost Pi regenerationcapacity at low temperature at the expense of the electrontransport capacity.A common (but not universal) acclimation response to

changes in growth temperature is for the electron transportcurve to shift towards the new growth temperature in apattern that is often identical to the shift in A, particularlywhen measured at elevated CO2. In winter wheat, thethermal optimum of CO2-saturatedA of 15 C grown leaveswas 1520 C, as was the rate of whole chain electron trans-port (Yamasaki et al. 2002). At a growth temperature of35 C, the thermal optimum for both A and whole chainelectron transport in winter wheat had shifted to near 35 C.The optimum for electron transport through PSII shiftedin concert with A and whole chain electron transport;however, electron flow through PSI did not show a shift inthe thermal optimum with changing growth temperature(Yamasaki et al. 2002). In the subpolar species S. cernua, areduction in growth temperature from 20 to 10 C caused adecline in the thermal optimum of A from near 20 to 10 C(Mawson et al. 1986).This was accompanied by a reductionin the thermal optimum of whole chain electron flow, andelectron flow through PSII, from near 25 to 10 C (Mawson& Cummins 1989). As observed with wheat, electron flowthrough PSI in S. cernua did not correlate with the changedthermal response of A or whole chain electron transport.Winter rye also shows a large increase in whole chain elec-tron transport at low temperature following a reduction in



growth temperature from 20 to 5 C; this increase corre-sponds to increases in the rate of electron transport throughPSI in the cold-acclimated plants (Huner 1988; Huner et al.1993). In two species from hot, dry climates, Larrea divari-cata (Armond, Schreiber & Bjrkman 1978) and Neriumoleander (Badger et al. 1982), growth temperature (45versus 20 C days) did not affect the thermal optimum ofwhole chain electron transport, while the thermal optimumof A was reduced about 10 C. However, electron transportcapacity was stimulated below 35 C in the cool relative tothe warm-grown plants. In pea, electron transport capacityincreased across the measurement range (420 C) in plantsgrown at 7 C relative to 17 C, apparently because of anincrease in turnover rate at a step between the photosys-tems (Mitchell & Barber 1986). Mitchell & Barber (1986)suggest that changes in membrane fluidity at low growthtemperature accelerate interactions between cyt f and theplastoquinones, allowing for the rise in the electron trans-port capacity in the cold-grown plants.In plants transferred to hot conditions, a different isoform

of Rubisco activase can be produced that confers heat sta-bility. In spinach, a 45 kDa isoform is produced by alterna-tive splicing in hot conditions, while in mild conditions, a41 kDa isoform is the only form synthesized (Crafts-Brandner et al. 1997). The longer isoform is heat stable to45 C, while the shorter isoform is heat stable to about32 C in vitro. In cotton, heat stress promoted the synthesisof a 46 kDa isoform to complement existing 47 and 43 kDaforms (Law, Crafts-Brandner & Salvucci 2001). In wheat,heat acclimation of activase stability was associated with aslight reduction of a 46 kDa isoform, and a large increase ofa 42 and 41 kDa isoform (Law & Crafts-Brandner 2001).Mixtures of the isoforms in these species enhance thermalstability of activase activity in vitro (Portis 2003). In contrastto the species with multiple isoforms differing in heat sen-sitivity, tobacco only produces one isoform (Salvucci et al.2001), while Arabidopsis produces two isoforms of similarthermal sensitivity (Kallis, Ewy & Portis 2000). Given thatspinach has a large acclimation response ofA (Yamori et al.2005, 2006b), it would be interesting to know if the thermalacclimation response of tobacco is constrained by havingonly one isoform of activase.

DIFFUSION LIMITATIONSThe diffusion of CO2 into the leaf and chloroplast is directlydependent on temperature via diffusivity effects, stomatalcontrol, solubilization and membrane permeability. Sto-matal responses to temperature will not be covered indetail here, as they are highly variable and would require alengthy review to provide a cogent synthesis. Dependingupon species and growth conditions, stomata can open withrising temperature (a common response when vapor pres-sure deficit is low), close (often in response to increasingvapor pressure deficit with rising temperature) or remainunaffected (Kemp & Williams 1980; Monson et al. 1982;Tenhunen et al. 1984; Sage & Sharkey 1987; Santrucek &Sage 1996; Cowling & Sage 1998; Yamori et al. 2006a).

It is worth noting that the sensitivity of A to variationin stomatal conductance generally increases at warmertemperatures, because the biochemical controls over A athigh temperature are more sensitive to changes in Ci. If Ais Pi-regeneration limited at cooler temperatures, largechanges in stomatal conductance have little affect on A; bycontrast, a Rubisco limitation onA at elevated temperaturecreates a steep A/Ci response such that substantial changesin A would result from small changes in stomatal conduc-tance. For this reason, stomatal limitations are generallygreater at elevated temperature, regardless of the stomatalresponse (Sage & Sharkey 1987; Hendrickson et al. 2004a).Mesophyll conductance (the conductance ofCO2 from the

stomata to the chloroplast stroma) affects stromalCO2 levelsand as such, potentially contributes to the thermal responseofA.Mesophyll conductance is highly sensitive to tempera-ture, showing aQ10 near 2 below the thermal optimum,and athermal optimum that is similar to the thermal optimumofA(Bernacchi et al. 2002;Warren & Dreyer 2006; Yamori et al.2006a). This high Q10 indicates that the temperatureresponse of mesophyll conductance is largely controlled byproteins (Yamori et al. 2006a). Both aquaporins and car-bonic anhydrase are known to be important facilitators ofCO2 entry into the cell and chloroplast (Evans & Loreto2000; Terashima et al. 2006; Yamori et al. 2006a). Unlike theresponse of mesophyll conductance below the thermaloptimum ofA, above the thermal optimum, there is no clearpattern. Substantial reductions in mesophyll conductance atelevated temperature are reported for tobacco and cool-grown spinach (Bernacchi et al. 2002; Warren and Dreyer2006;Yamori et al. 2006a),but little if any reductions occur inoak andwarm-grown spinachbetween 25 and 35 C (Warren& Dreyer 2006). No study has examined the response ofmesophyll conductance above 40 C, so its contribution inthe thermal range where electron transport or Rubisco acti-vase may assert control is unknown. If mesophyll conduc-tance substantially declines above 40 C, then it could be amajor limitation on A at elevated temperatures.Mesophyll conductance also acclimates to variation in

growth temperature. In rice, plants had a threefold highermesophyll conductance when grown at 32 C relative to25 C (Makino et al. 1994). In spinach, the mesophyll con-ductance increased in warm-grown plants (30/25 C) rela-tive to cool grown (15/10 C), but only at measurementtemperatures above 20 C; plants from both growth condi-tions had the same thermal response of mesophyll conduc-tance below 20 C (Yamori et al. 2006a).

TEMPERATURE RESPONSE OFC4 PHOTOSYNTHESISIn C4 plants, photosynthetic carbon assimilation reflects theactivity of Rubisco in vivo, as it does in C3 plants. However,because Rubisco is enclosed in a sealed compartment whereCO2 is concentrated to near-saturating levels, the dynamicsof photosynthetic limitation differ. At low CO2, A is theo-retically predicted to be limited by the capacity of phos-phoenolpyruvate (PEP) carboxylase (PEPCase) to fix



bicarbonate for movement into the bundle sheath as partof a C4 acid (von Caemmerer 2000). PEPCase activity isindependent of temperature at low CO2 (Laisk & Edwards1997).Hence, the initial slope of the CO2 response ofA in C4plants is largely insensitive to temperature, except in chillingconditions where injury occurs (Fig. 8) (Long &Woolhouse1978;Sage 2002).Here, the initial slopemay decline,possiblyreflecting increases in the activation energy of PEPCase atlow temperature (Pittermann & Sage 2000; Kubien & Sage2004b) or chilling lability of PEPCase in vivo (Krall &Edwards 1993; Matsuba et al. 1997). Oxygenase activity islargely suppressed in C4 plants, and as a result, the CO2compensation point does not rise significantly with tempera-ture as it does in C3 plants. This, in combination with thethermally insensitive response of the initial slope, causes thetemperature response of A at low CO2 to be relatively flatin C4 plants (Sage 2002). This commonly occurs at lowatmospheric CO2 levels corresponding to late-Pleistocene(180 mbar) and pre-Industrial (270 mbar) times. To exhibithigh thermal sensitivity, the photosynthesis rate in C4 plantshas to be above the CO2 saturation point (Sage 2002).AswithC3 plants, theCO2-saturatedplateauof theC4A/Ci

response rises with temperature up to the thermal optimumthat is typically between 38 and 45 C (Fig. 8) (Pittermann&Sage 2000; Sage 2002). This plateau can be determined bynumerous limitations:Rubisco capacity,RuBP regenerationcapacity, PEP regeneration as controlled by pyruvatePidikinase capacity and Pi regeneration capacity (vonCaemmerer & Furbank 1999; von Caemmerer 2000). Atcooler temperatures (3800 m), and in boreal fens where summer chilling isroutine (Long 1999; Sage,Wedin & Li 1999; Kubien & Sage2003).Alpine C4 species are frequently exposed to summerfreezing, without apparent harm (Sage & Sage 2002; Sageunpublished data). The relatively low ceiling imposed on Aby a limitedRubisco capacity in these species does appear tobe an important consideration for their low temperatureperformance, however (Pittermann & Sage 2000, 2001; Sage& Sage 2002). In addition to directly limiting A, the lowceiling predisposes the C4 plants to photoinhibition, whichnecessitates a higher investment in photoprotection than

Figure 8. (a) The CO2 response of netCO2 assimilation (A) in Muhlenbergiamontanum at 13, 23 and 33 C grown at aday/night regimes of 26/16 and 26/4 C ina plant growth chamber. (b) Thecorresponding temperature response ofA measured in intact leaves (circles,at the two growth regimes indicated)and total ribulose 15-bisphosphatecarboxylase/oxygenase (Rubisco) activitymeasured in vitro (triangles) for M.montanum (Pittermann & Sage (2000).

13C

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Intercellular CO2, mbar

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6026/16C treatment26/4C treatmentRubisco

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1(a) (b)PEPCase limited regionRubisco-limited region



seen inC3 plants (Long 1983,1999;Kubien et al. 2003;Kubien& Sage 2004a; Sage unpublished results). C4 photosynthesisalso becomes less efficient at low temperature because theRubisco limitation causes the bundle sheathCO2 level to riseat low temperature, and a greater proportion of the CO2 inthe bundle sheath leaks out of the leaf (Kubien et al. 2003;Kubien & Sage 2004b).As a result of these additional costs,C4 plants at high elevation and latitude have to escape theconsequences of a cool climate by growing in micrositeswhere solar heating allows for favourable daytime tempera-tures for photosynthesis (Sage & Sage 2002; Kubien & Sage2003).The low frequency of C4 plants in cool climates is notlikely the result of an inherent physiological intolerance atlow temperature, but is instead a combination of lowerquantum yield, a greater probability of high light stress thatin turn increases photoprotection costs, a limited number offavourablemicrosites, and competition fromC3 plants (Sage& Pearcy 2000).

Thermal acclimation of C4 photosynthesisC4 photosynthesis shows three general patterns of thermalacclimation. The first is observed in generalist species suchas found in warm desert Atriplex shrubs that are activeyear-round. Here, the breadth of the thermal response andthe values of A at the thermal optimum change a little withvariation in growth temperature; instead, the thermaloptimum shifts in the direction of the growth temperature(Osmond et al. 1980).The second response has largely beenobserved in C4 species from cool environments [Atriplexconfertifolia, Bouteloua gracilis, Miscanthus, Muhlenbergiaspecies, Paspalum dilatatum (Caldwell et al. 1977; Kemp &Williams 1980; Sage 2002; Cavaco et al. 2003; Naidu et al.2003)], but can occur in summer active weeds [Atriplexrosea (Bjrkman & Pearcy 1971)]. Here, the thermalresponse of A changes little below measurement tempera-tures of 20 C following growth in a cooler environment,while it changes at elevated temperature (see, e.g. Fig. 8). Inthe third type of response, A changes at all measurementtemperatures following thermal acclimation; species withthis type of response often increase A following transfer tocooler conditions that are not stressful [e.g. warm-seasongrasses and Atriplex sabulosa (Osmond et al. 1980; Dwyeret al. 2007)]. In contrast to these acclimation responses,there is also the response of chilling-sensitive C4 plants suchas maize to low growth temperature. These species showa loss in photosynthetic capacity, membrane integrity isimpaired and enzyme activity is reduced at all measurementtemperatures following prolonged chilling (Long 1983,1999; Naidu et al. 2003). These are considered to be stressresponses that lead to a loss of vigour and possibly death.The mechanistic explanation for acclimation in C4

photosynthesis remains unclear, although recent progress inour understanding of the biochemical controls over C4 pho-tosynthesis allows for some partial evaluations. BecauseRubisco imposes a strong limitation on A at low tempera-ture, the most obvious means of thermal acclimation tosuboptimal temperatures would be to enhance Rubisco

content. Studies to date indicate some species do acclimatein this manner, while numerous others do not.Acclimationinvolving a change in Rubisco content occurs in the warm-season grasses Panicum coloratum and Cenchrus ciliaris,and the warm-season dicot Flaveria bidentis grown at 25/20and 35/30 C; plants grown at the cooler temperatures had3040% more Rubisco than plants grown at the warmertemperatures, which was associated with a rise in A below25 C (Dwyer et al. 2007). In C4 Atriplex lentiformis fromDeath Valley grown at 23 C days, Rubisco content wasmore than double the levels measured in plants grown at43 C, and this was associated with a near doubling of mea-suredA at 10 C (Pearcy 1977). In maize grown at 19 versus31 C, Rubisco activity was by 21% greater while PPDKand NADPmalic enzyme activities were 64100% greaterin the 19 C-grown plants (Ward 1987).These responses aredistinct from responses of warm-season C4 grasses in chill-ing conditions (1015 C), where Rubisco and other proteinlevels gradually decline following chilling exposure (Duet al. 1999a; Naidu & Long 2004).In chilling-tolerant, cool-season C4 grasses, there is no

change in Rubisco content nor A below 20 C, indicatingminimal acclimation capacity to cool conditions (Fig. 8)(Pittermann & Sage 2001; Cavaco et al. 2003; Naidu et al.2003;Kubien & Sage 2004a). Instead, acclimation responsesare mostly observed at the thermal optimum. Cool- andwarm-grown plants of the boreal C4 grass Muhlenbergiaglomerata exhibited identical A/T responses below 23 C,while the warm-grown grass had 50% higher A at thethermal optimum and a 5 C higher thermal optimum(Kubien & Sage 2004a). Miscanthus giganteus, a cool-tolerant C4 grass from the mountains of Taiwan, shows thesame A/T response below 20 C in warm- and cool-grownplants, and an enhancement inA at the thermal optimum inthe warm-grown plants (Naidu et al. 2003). Cool-grownPaspalum dilitatum also showed no change in the A/Tresponse and Rubisco content below 20 C compared towarm-grown plants, but had a higher A at the thermaloptimum and less heat tolerance (Cavaco et al. 2003). Thehigher rate at elevated temperature in the cool-grown P.dilitatum was associated with greater total protein in theleaves; however, PEPCase activity was unchanged by thetreatment (Cavaco et al. 2003).The most comprehensive C4 acclimation study is by

Dwyer et al. (2007) with three warm-season C4 species (C.ciliaris, F. bidentis and P. coloratum) grown at 25/20 and35/20 C. In these species, A was reduced at the thermaloptimum, and the thermal optimum forA was about 13 Chigher, in the warmer-grown plants (Dwyer et al. 2007). InP.coloratum and C. ciliaris, A showed a pronounced declineabove 35 C in the plants grown at 25/20 but not 35/30 C. Inthe cooler-grown plants, the increase in A at the thermaloptimum was associated with increased Rubisco capacity, arise in carbonic anhydrase activity, a rise in leaf nitrogencontent and the production of leaves with higher leaf massper area.The two grass species also had greater cyt f contentin the cool-relative to the warm-grown plants, indicatingthat there may have been an increase in electron transport



capacity that supported an increase inA at the thermal opti-mum.In all three species,PEPCase activity,PSII content andchlorophyll content were unchanged.Dwyer et al. (2007) didnot examine Rubisco activation state or activase lability.

GLOBAL CHANGE AND THE TEMPERATURERESPONSE OF PHOTOSYNTHESISWith the rise in atmospheric CO2 and the associatedwarmingof the global climate, it is becoming clear that plantsof the future will face fundamentally different patterns ofcontrol over photosynthetic carbon gain. In the past 400millennia, when CO2 levels ranged between 180 and300 mbar (Sage & Coleman 2001), light-saturated photosyn-thesis would have largely been limited by Rubisco capacityin C3 plants and PEPCase capacity in C4 plants over much ofthe thermal range encountered during the growing season.At higher CO2 in a warmer world, Rubisco will be lesslimiting unless there is a strong,disproportional reduction inRubisco content. If electron transport capacity is the pre-dominant limitation in warm, high CO2 environments of thefuture, natural selection should favour species and geno-types with increased heat stability of membrane and pro-teins.Alternatively, if activase is a strong controller ofA, thenheat-stable forms of activase should be favoured. Throughbreeding and genetic engineering, humans could get a jumpon climatic change by directly selecting for traits that willpreadapt species to warmer,CO2-enriched environments.Todo this effectively, however, we will need to clearly identifythe main limitations on A above the thermal optimum andhow they vary in natural and agricultural populations.Whilemuch of the discussion of climatic change effects on

plants has addressed heat effects, the greater effect willactually occur at the low-temperature end of the growingrange. This is because most of the warming will occur athigher latitudes,duringwinter and at night (IPCC 2001).Themoderation of winter temperatures in temperate to boreallatitudes will allow for longer cool growing seasons in springand even winter, which will favour species adapted for pho-tosynthesis in cooler conditions. In these situations, theability of plants to avoid Pi regeneration limitations will beimportant. Paradoxically, if humans are to best exploit theopportunities and minimize the danger of global climaticchange, it is important to understand the biochemicalresponses controllingA in cool conditions as well as increas-ingly warm conditions.In summary, this review has assessed our understanding

of the mechanisms controlling the temperature response ofphotosynthesis in land plants.While there is a good generalknowledge of the potential limitations, major areas ofuncertainty remain, particularly with respect to limitationsat supraoptimal temperatures. In the immediate future,efforts should be made to clarify the limitations onA abovethe thermal optimum, in particular, the importance of elec-tron transport versus lability of Rubisco activase. Betterunderstanding is also needed of the main limitations on Afollowing thermal acclimation to low temperature in C3plants. Over the longer term, we need to develop a better

understanding of the acclimation and adaptation potentialof photosynthesis in natural populations. For example, thegreatest warming will tend to affect the more thermallystressed environments, where highly specialized specieslive. Do these species generally lack the acclimation poten-tial to allow them to persist in a warmer environment?Withan improved understanding, we will be in a much betterposition to predict andmitigate the effects of global climaticchange.

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The Temperature Response of C3 and C4 Photosynthesis