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INVITED REVIEW

Plant Respiration and Elevated Atmospheric CO2 Concentration:Cellular Responses and Global Significance

M I Q U E L A . G O N Z A L E Z - M E L E R*, LIN A TA N EV A and R EB EC C A J . TR U EM A N

Department of Biological Sciences, University of Illinois at Chicago, 845 West Taylor St, Chicago, IL 60607, USA

Received: 2 June 2004 Returned for revision: 14 June 2004 Accepted: 6 July 2004 Published electronically: 8 September 2004

BackgroundElevated levels of atmospheric [CO2] are likely to enhance photosynthesis and plant growth, which,in turn, should result in increased specific and whole-plant respiration rates. However, a large body of literaturehas shown that specific respiration rates of plant tissues are often reduced when plants are exposed to, or grown at,high [CO2] due to direct effects on enzymes and indirect effects derived from changes in the plants chemicalcomposition. Scope Although measurement artefacts may have affected some of the previously reported effects of CO2 onrespiration rates, the direction and magnitude for the effects of elevated [CO 2] on plant respiration may largelydepend on the vertical scale (from enzymes to ecosystems) at which measurements are taken. In this review, theeffects of elevated [CO2] from cells to ecosystems are presented within the context of the enzymatic and physio-logical controls of plant respiration, the role(s) of non-phosphorylating pathways, and possible effects associatedwith plant size. Conclusions Contrary to what was previously thought, specific respiration rates are generally not reduced whenplants are grown at elevated [CO2]. However, whole ecosystem studies show that canopy respiration does notincrease proportionally to increases in biomass in response to elevated [CO2], although a larger proportion ofrespiration takes place in the root system. Fundamental information is still lacking on how respiration and theprocesses supported by it are physiologically controlled, thereby preventing sound interpretations of what seem to bespecies-specific responses of respiration to elevated [CO2]. Therefore the role of plant respiration in augmenting thesink capacity of terrestrial ecosystems is still uncertain. 2004 Annals of Botany Company

Key words: Respiration, elevated CO2, cellular processes, ecosystem respiration, oxidation.

I N T R O D U C T I O N

Respiration is essential for growth and maintenance of allplant tissues, and plays an important role in the carbonbalance of individual cells, whole-plants and ecosystems,as well as in the global carbon cycle. Through the processesof respiration, solar energy conserved during photosynthesisand stored as chemical energy in organic molecules isreleased in a regulated manner for the production ofATP, the universal currency of biological energy transfor-mations, and reducing power (e.g. NADH and NADPH). Aquantitatively important by-product of respiration is CO2and, therefore, plant and ecosystem respiration play a majorrole in the global carbon cycle.

Terrestrial ecosystems exchange about 120 Gt of carbon

per year with the atmosphere, through the processes ofphotosynthesis and respiration (Schlesinger, 1997).Roughly, half of the CO2 assimilated annually throughphotosynthesis is released back to the atmosphere byplant respiration (Gifford, 1994; Amthor, 1995). Becauseterrestrial biosphere-atmosphere fluxes of CO2 far outweighanthropogenic inputs of CO2 to the atmosphere, a smallchange in terrestrial respiration could have a significantimpact on the annual increment in atmospheric [CO2](Amthor, 1997). A large body of literature has indicatedthat plant respiration is reduced in plants grown at high[CO2]. For example, it was estimated that the observed

1520 % reduction in plant tissue respiration caused by

doubling current atmospheric [CO2] (Amthor, 1997;Drake et al., 1997; Curtis and Wang, 1998), could increasethe net sink capacity of global ecosystems by 34 Gt ofcarbon per year (Drake et al., 1999), and thus offset anequivalent amount of carbon from anthropogenic CO2 emis-sions. Therefore, not only are gross changes in respirationimportant for large-scale carbon balance issues, changes inspecific rates of respiration can have significant impact onbasic plant biology such as growth, biomass partitioning ornutrient uptake (Amthor, 1991; Wullschleger et al., 1994;Drake et al., 1999).

Scaling the effects of an increase in atmospheric [CO2] onplant respiration at the biochemical level to the whole eco-system is difficult for at least two important reasons: (1) the

fine and coarse control points of respiratory pathways intissues and whole plants are not well known; and (2) it isunclear how respiration rates actively or passively adjust tothe effects that elevated [CO2] may have both upstream (e.g.on substrate availability) and downstream (e.g. on energydemand) of the carbon oxidation pathways. In addition,accurate measurements of respiratory rates as CO2 evolu-tion have been proven difficult with current techniques(Gonzalez-Meler and Siedow, 1999; Hamilton et al.,2001; Jahnke, 2001), presenting yet another limitation toscaling up process-based measurements of respiration ratesto organism, ecosystem or global levels. In this document,we re-evaluate the theory on respiration responses to

Annals of Botany 94/5, Annals of Botany Company 2004; all rights reserved

* For correspondence. E-mail [email protected]

Annals of Botany 94: 647656, 2004

doi:10.1093/aob/mch189, available online at www.aob.oupjournals.org


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elevated [CO2] in view of recent studies that have providednew insights on the effects of a short- and long-term changein atmospheric [CO2] on plant respiration.

D I R E C T A N D I N D I R E C T E F F E C T S O F [ C O2]

O N P L A N T - S P E C I F I C R E S P I R A T I O N R A T E S

Amthor (1991) described two different effects of [CO2] onplant respiration rates that can be distinguished experimen-tally: a direct effect, in which the rate of respiration ofmitochondria or tissues could be rapidly and reversiblyreduced following a rapid increase in [CO2] (Amthoret al., 1992; Amthor, 2000a), and an indirect effect inwhich high [CO2] changes the rate of respiration in planttissues compared with the rate seen for those plants grown innormal ambient [CO2] when both are tested at a commonbackground [CO2] (Azcon-Bieto et al., 1994). Most of thestudies investigating the effects of a change in [CO2] onrespiration rates have described magnitude (from non-

significant to 60 %) and direction (either stimulation, inhibi-tion or no effect) of these two effects, with little progresson their underlying mechanisms. Confounding measure-ment artefacts are an added complication for establishingthe presence and magnitude of direct and indirect effects of[CO2] on respiration (Gonzalez-Meler and Siedow, 1999;Amthor, 2000a; Jahnke, 2001; Davey et al., 2004).

Direct effects

Previously, a rapid short-term doubling of current atmo-spheric CO2 levels was reported to inhibit respiration ofmitochondria and plant tissues by 1520 % (Amthor,

1997; Drake et al., 1997; Curtis and Wang, 1998). Althoughdirect effects of [CO2] on respiratory enzymes have beenreported, the magnitude of the direct inhibition of intacttissue respiration by elevated [CO2] has now been shownto be explained by measurement artefacts (i.e. Gonzalez-Meler and Siedow, 1999; Jahnke, 2001), diminishing theimpact that such reductions in respiration rate may have onplant growth and the global carbon cycle.

Direct effects on enzymes. Doubling current levels in[CO2] (here we review the effects of only two- or three-fold increases in atmospheric CO2) have been shown toinhibit the oxygen uptake of isolated mitochondria and theactivity of mitochondrial enzymes under some conditions

(Reuveni et al., 1995; Gonzalez-Meler et al., 1996a, b).Twice current atmospheric [CO2] reduces the activity ofcytochrome c oxidase and succinate dehydrogenase in iso-lated mitochondria from cotyledon and roots ofGlycine max(Gonzalez-Meler et al., 1996b). Mitochondrial oxygenuptake may show either no response or up to 15 % inhibitionbyarapidincreasein[CO2], depending on the electron donorused in the assay (Gonzalez-Meler et al., 1996b; see alsoFig. 1), indicating that the response of mitochondrialenzymes to high [CO2] depends on the cells metabolism(Gonzalez-Meler and Siedow, 1999; Affourtit et al., 2001).

In scaling the direct effects of high [CO2] onrespiratory enzymes to intact tissues two factors need to

be considered: (1) cytochrome oxidase exerts up to 50 %of the total respiratory control (for definitions, see Kacser

and Burns, 1979) at the level of the mitochondrial electrontransport chain (reviewed by Gonzalez-Meler and Siedow,1999); and (2) the competitive nature of the cytochrome andalternative pathways of mitochondrial respiration (Affourtitet al., 2001). The activity of the alternative pathway ofrespiration could increase upon doubling of the [CO2],masking a direct CO2 inhibition of the cytochrome pathway(Fig. 1). The oxygen isotope technique (Ribas-Carbo et al.,1995) allows for the distinction of direct effects of [CO2] onoxygen uptake activity by the cytochrome and the alterna-tive oxidases. Figure 1 shows that mitochondrial electrontransport activity is affected when CO2 (a mild inhibitor)restricts the normal electron flow through one of thepathways (Cyt pathway vcyt). Under conditions of low

alternative pathway activity (for details, see Ribas-Carboet al., 1995), inhibition of the cytochrome pathway (18 %)by doubling the ambient [CO2] is compensated for by asimilar increase in alternative pathway activity (valt), result-ing in no significant reduction in overall oxygen uptake ofthe isolated mitochondria. These results show that enhancedactivity of the alternative pathway upon an increase in[CO2] provides a mechanism by which the direct [CO2]inhibition of the cytochrome oxidase may not be seen inthe total oxygen uptake under conditions of high adenylatecontrol (low ADP). Gonzalez-Meler and Siedow (1999)argued that direct effects of CO2 on respiration exceeding>10 % inhibition are likely due to factors other than

Vt vcyt valt

O2uptake(molmg1proteinmin1)

0

10

50

60

70

80Ambient CO2

Ambient CO2 + 360 L L1

Inhibition of O2uptake: 55 %

Inhibition of

cytochrome

pathway: 176%

F I G . 1. Effectof doublingthe concentration ofCO2 onthe oxygenuptake ofmitochondriaisolated from5-d-old soybean cotyledons in state4 conditions(absence of ADP). Oxidation of NADH andpyruvate wasmeasured in intactmitochondria thatwere incubated for10 minwith 0 (open bars) or 0.1(solidbars)mM dissolved inorganiccarbon(DIC) at 25C. Experiments weredoneusing the oxygen isotope techniqueas describedin Ribas-Carbo etal. (1995)to detect the effects of CO2 on the total activity of mitochondrial respiration(Vt), the activity of the cytochrome pathway (vcyt) and the activity of thealternative pathway (valt). Results are average of four replicates and

standard errors.

648 Gonzalez-Meler et al. Effects of High CO2 on Respiration Rates


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inhibition of mitochondrial enzymes. Due to confoundingmeasurement artefacts (Jahnke, 2001), rates of tissuerespiration have been reported to decrease >10 % whenthe atmospheric [CO2] doubles.

Direct effects on intact tissues. Recent evidence indicates

that, in studying direct effects of CO2 on respiratory CO2efflux of intact tissues, investigators should first be con-cerned about measurement artefacts. Amthor (1997) andGonzalez-Meler and Siedow (1999) showed that gas CO2exchange measurement errors could augment and explainthe magnitude of the direct effect. New studies made in thiscontext have shown that respiration rates are little or not atall inhibited by a doubling of atmospheric [CO2] (Amthor,2000a; Amthor et al., 2001; Bunce, 2001; Hamilton et al.,2001; Tjoelker et al., 2001; Bruhn et al., 2002; Davey et al.,2004). Indeed, Jahnke (2001) and Jahnke and Krewitt(2002) confirmed that measurement artefacts due to leakageinCO2-exchange systems could be as large as the previouslyreported direct inhibitory effects. They also found that leaksthrough the aerial spaces of homobaric leaves showed asignificant apparent inhibition of CO2 efflux that was notdue to an inhibition of respiration by elevated [CO2]. There-fore, considerations of the impact direct effects of [CO2] onplant respiration rates may have on the global carbon cyclewere overstated (Gonzalez-Meler et al., 1996a; Drake et al.,1999). Corrections for instrument leaks can be applied inmost cases (Bunce, 2001; Jahnke, 2001; Pons andWelschen, 2002). Applying some corrections for gasexchange leaks, Bunce (2001) reported a significant reduc-tion in respiration after a rapid increase in [CO2]. Moreover,simultaneously switching the air isotopic composition from12CO2 to pure

13CO2 when the [CO2] was changed, showed

that the efflux of12

CO2 (which represents net respiratoryCO2 evolution originating from respiratory substrates minusthe CO2 being re-fixed by carboxylases, see below) wasreduced in leaves of C3 plants, but not C4, when the[CO2] increased (Pinelli and Loreto, 2003). These recentresults illustrate that not all reports of direct inhibition ofrespiration by elevated [CO2] have yet been reconciled witheach other, but they do not show a clear proof that the directeffect, as defined by Amthor (1991) exits either.

An alternate explanation for the apparent reduction inrespiration rates upon an increase in [CO2] (Bunce, 2001;Pinelli and Loreto, 2003) is an increase in dark CO2 fixationcatalysed by phosphoenolpyruvate carboxylase (PEPC),resulting in an apparent reduction of CO2 efflux (Amthor,

1997; Drake et al., 1999). However, in Rumex and Glycineleaves, Amthor et al. (2001) found an effect of elevated[CO2] on CO2 efflux in only a minority of experiments,with no effect of elevated [CO2] on the O2 uptake of thesame leaves, indicating at most a small effect of elevated[CO2] on PEPC activity or respiration rates. Similar resultswere found for a variety of species, involving 600 measure-ments, in which [CO2] increases did not alter the CO2 andO2 leaf exchanges in the dark (Davey et al., 2004).

It seems that direct effects of [CO2] on mitochondrialenzymes may have no consequence on the specific respira-tory rate of whole tissues. Because mitochondrial respira-tory enzymes are generally in excess to the levels required

to support normal tissue respiratory activity under mostgrowth conditions (Gonzalez-Meler and Siedow, 1999;Atkin and Tjoelker, 2003; Gonzalez-Meler and Taneva,2004), a minor inhibition of enzymatic activity by [CO2]will not translate to the overall tissue respiration rate.A small increase in enzyme levels in plants exposed to

elevated [CO2] could be enough to compensate for the directeffects of CO2 on mitochondrial enzyme activity, as it hasbeen seen in leaves of some plants grown at high [CO2](i.e. Griffin et al., 2001).

Another factor to consider is that increases in alternativepathway activity upon inhibition of cytochrome oxidase bya change in [CO2] will result in unaltered dark respiratoryrates (as illustrated in Fig. 1). However, an increase in thenon-phosphorylating activity of the alternative pathwayreduces the efficiency with which energy from oxidizedsubstrates supports growth and maintenance of plants(Gonzalez-Meler and Siedow, 1999; Gonzalez-Meler andTaneva, 2004). Some studies have reported that the growthof plants exposed to elevated [CO2] only during the night-time is altered (Bunce, 1995, 2001, 2002; Reuveni et al.,1997; Griffin et al., 1999). Such altered growth patternshave been attributed, in part, to effects of [CO2] on plantrespiration, including increased activity of the non-phosphorylating alternative pathway. These CO2 effectsare considered next.

Are there direct effects of CO2 on whole plants? In thepast, in some studies, plants have been grown at [CO2]elevated only at night-time to assess the long-term conse-quences of the previously considered direct effects of CO2on respiration rates. Although most of these studies havefound that growth patterns were altered in plants exposed to

high night-time [CO2], these effects cannot be attributed todirect effects of [CO2] on respiration for reasons explainedabove. Bunce (1995) observed that the biomass and leaf arearatio ofGlycine max increased and that photosynthetic ratesdecreased in plants exposed to high night-time [CO2] rela-tive to plants grown at normal ambient [CO2]. Similarly,Griffin et al. (1999) found that Glycine max exposed to highnight-time [CO2] had lower leaf respiration rates and greaterbiomass than plants grown at ambient or elevated [CO2].Reuveni et al. (1997) speculated that increases in the bio-mass ofLemna gibba grown at high night-time [CO2] rela-tive to control plants, was due to a reduction in alternativepathway respiration (although the alternative pathway activ-ity was not measured). Reduction in alternative pathway

activity might more fully couple respiration rates withgrowth and maintenance, enhancing growth. In contrast,Ziska and Bunce (1999) showed that elevation of night-time [CO2] reduced biomass only in two of the four C4species studied. In a later study, Bunce (2002) describedthat carbohydrate translocation was reduced within 2 d ofexposing plants to elevated night-time [CO2] when com-pared with plants grown at ambient conditions day andnight. These results suggest that elevated [CO2] mayhave other uncharacterized direct effects on plant physiol-ogy that can have the consequence of reducing energydemand for carbohydrate translocation, hence reducingthe rate of leaf respiration. If so, these new types of effects

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cannot be catalogued as direct effects of [CO2] on respira-tion but as indirect effects, making more research in thisarea necessary.

In summary, even though rapid changes in [CO2] caninhibit the activity of some mitochondrial enzymes directly,previously reported direct effects of [CO2] on tissue respira-

tion are likely to be due to measurement artefacts. There-fore, direct effects of [CO2] on specific respiration rates(although not necessarily on respiration physiology) shouldbe dismissed as having a major impact on the amount ofanthropogenic carbon that vegetation could retain. The roleof the alternative pathway in direct respiratory responses toelevated [CO2], although unresolved, would have littleimpact, if any, on the general conclusion that direct effectsof [CO2] on plant respiration are not to be considered inplant growth or carbon cycle models. Other effects of long-term elevation of night-time [CO2] can alter plant growthcharacteristics, and indirectly affect both respiration ratesand the relative activity of the cytochrome and alternativepathways. Therefore these effects cannot be referred to asdirect effects but rather as indirect effects of [CO2] onrespiration rates.

Indirect effects

Indirect CO2 effects represent changes in tissue respira-tion in response to plant growth at elevated atmospheric[CO2] (Amthor, 1997), because of changes in tissue com-position (Drake et al., 1997). Other indirect effects of [CO2]on plant respiration include changes in growth or responseto environmental stress, as well as changes in the respiratorydemand for energy relative to that of plants grown at ambi-ent [CO2] (Bunce, 1994; Amthor, 2000b). Such indirect

effects of plant growth at elevated [CO2] can be detectedas a reduction in CO2 emission (or O2 consumption) fromplant tissues when measured at ambient [CO2] (Gonzalez-Meler et al., 1996a).

Indirect effects on enzymes: is there acclimation ofrespiration to elevated [CO2]? Acclimation of respirationto high [CO2] can be defined as the down- or up-regulationof the respiratory machinery (i.e. amount of respiratoryenzymes, number of mitochondria) irrespective of changesin specific respiration rates when plants are grown at ele-vated [CO2] (Drake et al., 1999). A change in the leafrespiratory machinery of plants grown at high [CO2] canbe expected because of (a) increases in carbohydrate con-

tent, (b) reduced photorespiratory activity and (c) reductionsin leaf protein content (15 % on average), when comparedwith plants grown at current ambient [CO2] (Drake et al.,1997). These three processes can have different and some-times opposite effects on levels of respiratory enzymes andspecific rates of respiration.

As atmospheric [CO2] rises, increased photosynthesisresults in higher cellular carbohydrate concentrations(Drake et al., 1997; Curtis and Wang, 1998). Increasedcarbohydrates can stimulate the specific activity of respira-tion, due to the greater availability of respiratory substrates(Azcon-Bieto and Osmond, 1983) and higher energydemand for phloem loading of carbohydrates (Bouma

et al., 1995; Korner et al., 1995; Amthor, 2000b). Addition-ally, increased tissue carbohydrate levels (as in the case ofplants grown at high [CO2]) could result in an increase of

transcript levels of cytochrome oxidase (Felitti andGonzalez, 1998; Curi et al., 2003) and cytochrome pathwayactivity (Gonzalez-Meler et al., 2001). In contrast, a reduc-tion in photorespiratory activity in plants grown at high[CO2] will reduce the need for the mitochondrial compart-ment, which may result in a reduction in mitochondrialproteins and functions (Amthor, 1997; Drake et al., l999;Bloom et al., 2002). Not surprisingly, the availablestudies show that levels and activity of respiratory machin-ery can either increase or decrease in leaves of plants grownat high [CO2] with no concomitant effects on respirationrates (Fig. 2).

For instance, indirect effects of elevated [CO2] onrespiration of leaves of Lindera benzoin and stems of

Scirpus olneyi were correlated with a reduction in maximumactivity of cytochrome oxidase (Azcon-Bieto et al., 1994).However, a reduction of respiratory enzyme activity was notseen in rapidly growing tissues exposed to elevated [CO2](Perez-Trejo, 1981; Hrubeck et al., 1985). No acclimationto elevated [CO2] (i.e. reduction in cytochrome oxidase) hasbeen observed in leaves of C4 plants (Azcon-Bieto et al.,1994) or roots of C3 plants (Gonzalez-Meler et al., 1996a).In contrast, the number of mitochondria is consistentlyshown to increase in response to plant growth at elevated[CO2] (Griffin et al., 2001; Wang et al., 2004). Overallchanges associated with increases or decreases in therespiratory machinery in leaves of plants grown at elevated

00 05 10 15 20 25Relativeresponseofleafrespirationrate(E/A)

00

05

10

15

20

Relative response of leaf respiratory machinery* (E/A)

F I G . 2. Relationship between the relative response of leaf respiration andthe leaf respiratory machinery of plants grown at ambient and elevated[CO2]. Data extracted from Azcon-Bieto et al. (1994), George et al.

(1996), Gonzalez-Meler et al. (1996a), Griffin et al. (2001, 2004),Hrubec et al. (1985), Tissue et al. (2002), Wang et al. (2004) and M. A.Gonzalez-Meler (unpubl.res.). *Respiratory machineryrefers to changes ineither number of mitochondria, or soluble or membrane enzyme activity inplant extracts from plants grown at either ambient or elevated [CO2] in fieldandlaboratory experiments. Onlystudies thathave providedboth respirationrates and respiratory machinery from the same tissues or from differenttissues from the same plants are considered. Rates of [CO2] evolutionused are only those measured for plants grown under ambient or elevated

[CO2] at ambient [CO2] conditions.

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[CO2] (i.e. mitochondrial counts, cytochrome oxidase max-imum activity) seem to be independent of responses of therespiration rates to elevated [CO2] (Fig. 2; r

2 =04, n.s.).Therefore, changes in the mitochondrial machinery ofplants grown in high [CO2] are associated with alteredmitochondrial function and biogenesis and are not necessa-

rily related to energy production. Anaplerotic functions ofmitochondrial activity provide reductant and carbon skele-tons for the production of primary and secondary metabo-lites used in growth and maintenance processes, as well asother processes such as nitrogen reduction and assimilation(Gonzalez-Meler et al., 1996a; Amthor, 1997; Bloom et al.,2002; Davey et al., 2004). Vanoosten et al., (1992) reportedincreases in fumarase and malic enzyme activities in leavesof Picea abies grown in high [CO2]. These increases con-trasted with unchanged or decreased activity of PEPC orglycolitic enzymes. Increase in enzyme activity of the tri-carboxylic acid cycle with no increase in respiration ratesmay support the export of carbon skeletons and reducingpower (mainly as malate) from the mitochondria to thecytosol for biosynthesis. This uncoupling between anincrease in mitochondrial numbers and no increase inrespiratory activity of plants grown at high [CO2] (Fig.2) is further illustrated by the study of Tissue et al.(2002) in which a more than two-fold increase in the leafmitochondrial counts did not alter the maximum activity ofcytochrome oxidase in the same tissues. With the exceptionof two studies (i.e. Azcon-Bieto et al., 1994; Tissue et al.,2002), there are no reports on the response of membrane-associated mitochondrial enzymes to elevated [CO2] inleaves or roots of plants. More research is needed inthis area.

Indirect effects of [CO2] on respiration of tissues andwhole plants. It has been historically accepted that leafrespiration is reduced as a consequence of plant growthat elevated [CO2] (El Kohen et al., 1991; Isdo and Kimball,1992; Wullschleger et al., 1992a; Amthor, 1997; Drakeet al., 1997; Curtis and Wang, 1998; Norby et al., 1999).Poorter et al. (1992) showed that leaf respiration wasreduced, on average, by 14 % when expressed on a leafmass basis, but increased by 16 % on a leaf area basis. Curtisand Wang (1998) compiled respiratory data for woodyplants, and observed that growth at elevated [CO2] resultedin an 18 % inhibition of leaf respiration (mass basis). In thissection we will concentrate on the effects of elevated [CO2]on respiration of above-ground tissues. It is worth noting,

however, that root respiration rates in the field are notaltered by growth at elevated [CO2] during most of theplants growing season (Johnson et al., 1994; Matamalaand Schlesinger, 2000). Total ecosystem root respirationmay increase if root mass and/or turnover increases(Hungate et al., 1997; Hamilton et al., 2002; Georgeet al., 2003; Matamala et al., 2003).

Many previous reviews and meta-analyses (see above)have compared respiratory rates of plants grown and mea-sured at the [CO2] at which plants were grown. Therefore,these respiration measurements are also susceptible by thegas exchange artefacts described by Jahnke and co-workers.Respiratory O2 uptake measured in closed systems is not

susceptible to the measurement artefacts described above.The O2 uptake of green tissues of plants grown at high[CO2] could be increased, reduced or unaltered when com-pared with plants grown at ambient [CO2] (Table 1). Davey

et al. (2004) also showed that the O2 uptake of leaves ofplants grown at high [CO2] was slightly increased relative tocontrol plants. Gas exchange leaks (Jahnke, 2001) shouldnot be a factor in determining the rates of CO2 emissionrates when rates are measured and compared at ambient[CO2] for plants grown at ambient and elevated [CO2]. Are-analysis of the literature focused on leaf respiratoryresponses (on a leaf mass basis) of plants grown at ambientand elevated [CO2] and measured at an ambient [CO2],suggests that specific leaf respiration rates will be unalteredor even increased in plants grown at elevated [CO2](Table 2). Therefore, the generally accepted onclusion thatrespiration rates of plants grown at elevated [CO2] isreduced relative to plants grown at ambient [CO2] should

be re-evaluated (Amthor, 2000a; Davey et al., 2004;Gonzalez-Meler and Taneva, 2004). However, there is sig-nificant variability in the leaf respiratory response to growthat elevated [CO2] when compared with plants grown atambient conditions, ranging from 40 % inhibition(Azcon-Bieto et al., 1994) to 50 % stimulation (Williamset al., 1992). Considerations on the physiological basis bywhich the acclimation response of respiration to elevated[CO2] varies, is considered next.

In boreal species, reduction of respiration of plants grownat high [CO2] was related to changes in tissue N and car-bohydrate concentration (Tjoelker et al., 1999). Tissue Nconcentration often decreases in plants grown at elevated

T A B L E 1. Indirect effects of [CO2]onthedarkO2 uptake rates(on a leaf area basis) at 25 C of green tissues from Scirpusolneyi (C3), Spartina patens (C4), Distchilis spicata (C4),Lindera benzoin (C3), Cinna arundinacea (C3), Quercusgeminata (C3), Quercus myrtifolia (C3) and Serenoa repens

(C3) plants grown at either normal ambient (A) or normal

ambient+ 340 mL L1

atmospheric CO2 (E), inside open-topchambers in the field

SpeciesDark O2uptakea

Dry weight perunit areaa

SaltmarshScirpus olneyi 0.79** 1.00Spartina patens 0.94 0.99

Distchilis spicata 1.22* 1.00

Woodland understoreyLindera benzoin 0.77** 0.96Cinna arundinacea 1.13 1.05

Scrub oaksaw palmettoQuercus geminata 1.31* 1.11*

Quercus myrtifolia 0.82** 1.24**Serenoa repens 0.96 1.02

aE/A.Samples were collected at sunrise during the early summer of 1993.Oxygen uptake was measured at ambient conditions in a liquid phaseoxygen electrode as described in Azcon-Bieto et al. (1994).Significant differences (Students t-test) between respiratory rates ofplants grown at ambient and elevated [CO2] at P < 01 (*) and P

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