AOBPreview originally published online on September 8, 2004
Annals of Botany 2004 94(5):647-656; doi:10.1093/aob/mch189
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Annals of Botany 94/5, © Annals of Botany Company 2004; all rights reserved
INVITED REVIEW |
Plant Respiration and Elevated Atmospheric CO2 Concentration: Cellular Responses and Global Significance
Department of Biological Sciences, University of Illinois at Chicago, 845 West Taylor St, Chicago, IL 60607, USA
* For correspondence. E-mail mmeler{at}uic.edu
Received: 2 June 2004 Returned for revision: 14 June 2004 Accepted: 6 July 2004 Published electronically: 8 September 2004
| ABSTRACT |
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Background Elevated 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 literature has 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 plant's chemical composition.
Scope Although measurement artefacts may have affected some of the previously reported effects of CO2 on respiration rates, the direction and magnitude for the effects of elevated [CO2] on plant respiration may largely depend on the vertical scale (from enzymes to ecosystems) at which measurements are taken. In this review, the effects of elevated [CO2] from cells to ecosystems are presented within the context of the enzymatic and physiological controls of plant respiration, the role(s) of non-phosphorylating pathways, and possible effects associated with plant size.
Conclusions Contrary to what was previously thought, specific respiration rates are generally not reduced when plants are grown at elevated [CO2]. However, whole ecosystem studies show that canopy respiration does not increase proportionally to increases in biomass in response to elevated [CO2], although a larger proportion of respiration takes place in the root system. Fundamental information is still lacking on how respiration and the processes supported by it are physiologically controlled, thereby preventing sound interpretations of what seem to be species-specific responses of respiration to elevated [CO2]. Therefore the role of plant respiration in augmenting the sink capacity of terrestrial ecosystems is still uncertain.
Key words: Respiration, elevated CO2, cellular processes, ecosystem respiration, oxidation
| INTRODUCTION |
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Respiration is essential for growth and maintenance of all plant tissues, and plays an important role in the carbon balance of individual cells, whole-plants and ecosystems, as well as in the global carbon cycle. Through the processes of respiration, solar energy conserved during photosynthesis and stored as chemical energy in organic molecules is released in a regulated manner for the production of ATP, the universal currency of biological energy transformations, and reducing power (e.g. NADH and NADPH). A quantitatively important by-product of respiration is CO2 and, therefore, plant and ecosystem respiration play a major role in the global carbon cycle.
Terrestrial ecosystems exchange about 120 Gt of carbon per year with the atmosphere, through the processes of photosynthesis and respiration (Schlesinger, 1997
). Roughly, half of the CO2 assimilated annually through photosynthesis is released back to the atmosphere by plant respiration (Gifford, 1994
; Amthor, 1995
). Because terrestrial biosphere-atmosphere fluxes of CO2 far outweigh anthropogenic inputs of CO2 to the atmosphere, a small change in terrestrial respiration could have a significant impact on the annual increment in atmospheric [CO2] (Amthor, 1997
). A large body of literature has indicated that 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 increase the net sink capacity of global ecosystems by 3·4 Gt of carbon per year (Drake et al., 1999
), and thus offset an equivalent amount of carbon from anthropogenic CO2 emissions. Therefore, not only are gross changes in respiration important for large-scale carbon balance issues, changes in specific rates of respiration can have significant impact on basic plant biology such as growth, biomass partitioning or nutrient uptake (Amthor, 1991
; Wullschleger et al., 1994
; Drake et al., 1999
).
Scaling the effects of an increase in atmospheric [CO2] on plant respiration at the biochemical level to the whole ecosystem is difficult for at least two important reasons: (1) the fine and coarse control points of respiratory pathways in tissues and whole plants are not well known; and (2) it is unclear how respiration rates actively or passively adjust to the effects that elevated [CO2] may have both upstream (e.g. on substrate availability) and downstream (e.g. on energy demand) of the carbon oxidation pathways. In addition, accurate measurements of respiratory rates as CO2 evolution have been proven difficult with current techniques (Gonzalez-Meler and Siedow, 1999
; Hamilton et al., 2001
; Jahnke, 2001
), presenting yet another limitation to scaling up process-based measurements of respiration rates to organism, ecosystem or global levels. In this document, we re-evaluate the theory on respiration responses to elevated [CO2] in view of recent studies that have provided new insights on the effects of a short- and long-term change in atmospheric [CO2] on plant respiration.
| DIRECT AND INDIRECT EFFECTS OF [CO2] ON PLANT-SPECIFIC RESPIRATION RATES |
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Amthor (1991)
Direct effects
Previously, a rapid short-term doubling of current atmospheric CO2 levels was reported to inhibit respiration of mitochondria and plant tissues by 1520 % (Amthor, 1997
; Drake et al., 1997
; Curtis and Wang, 1998
). Although direct effects of [CO2] on respiratory enzymes have been reported, the magnitude of the direct inhibition of intact tissue respiration by elevated [CO2] has now been shown to be explained by measurement artefacts (i.e. Gonzalez-Meler and Siedow, 1999
; Jahnke, 2001
), diminishing the impact that such reductions in respiration rate may have on plant 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 to inhibit the oxygen uptake of isolated mitochondria and the activity of mitochondrial enzymes under some conditions (Reuveni et al., 1995
; Gonzàlez-Meler et al., 1996a
, b
). Twice current atmospheric [CO2] reduces the activity of cytochrome c oxidase and succinate dehydrogenase in isolated mitochondria from cotyledon and roots of Glycine max (Gonzàlez-Meler et al., 1996b
). Mitochondrial oxygen uptake may show either no response or up to 15 % inhibition by a rapid increase in [CO2], depending on the electron donor used in the assay (Gonzàlez-Meler et al., 1996b
; see also Fig. 1), indicating that the response of mitochondrial enzymes to high [CO2] depends on the cell's metabolism (Gonzalez-Meler and Siedow, 1999
; Affourtit et al., 2001
).
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In scaling the direct effects of high [CO2] on respiratory 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
Direct effects on intact tissues
Recent evidence indicates that, in studying direct effects of CO2 on respiratory CO2 efflux of intact tissues, investigators should first be concerned about measurement artefacts. Amthor (1997)
and Gonzalez-Meler and Siedow (1999)
showed that gas CO2 exchange measurement errors could augment and explain the magnitude of the direct effect. New studies made in this context have shown that respiration rates are little or not at all 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 leakage in CO2-exchange systems could be as large as the previously reported direct inhibitory effects. They also found that leaks through the aerial spaces of homobaric leaves showed a significant apparent inhibition of CO2 efflux that was not due to an inhibition of respiration by elevated [CO2]. Therefore, considerations of the impact direct effects of [CO2] on plant respiration rates may have on the global carbon cycle were overstated (Gonzalez-Meler et al., 1996a
; Drake et al., 1999
). Corrections for instrument leaks can be applied in most cases (Bunce, 2001
; Jahnke, 2001
; Pons and Welschen, 2002
). Applying some corrections for gas exchange leaks, Bunce (2001)
reported a significant reduction in respiration after a rapid increase in [CO2]. Moreover, simultaneously switching the air isotopic composition from 12CO2 to pure 13CO2 when the [CO2] was changed, showed that the efflux of 12CO2 (which represents net respiratory CO2 evolution originating from respiratory substrates minus the CO2 being re-fixed by carboxylases, see below) was reduced in leaves of C3 plants, but not C4, when the [CO2] increased (Pinelli and Loreto, 2003
). These recent results illustrate that not all reports of direct inhibition of respiration by elevated [CO2] have yet been reconciled with each other, but they do not show a clear proof that the direct effect, as defined by Amthor (1991)
exits either.
An alternate explanation for the apparent reduction in respiration rates upon an increase in [CO2] (Bunce, 2001
; Pinelli and Loreto, 2003
) is an increase in dark CO2 fixation catalysed by phosphoenolpyruvate carboxylase (PEPC), resulting in an apparent reduction of CO2 efflux (Amthor, 1997
; Drake et al., 1999
). However, in Rumex and Glycine leaves, 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 the same leaves, indicating at most a small effect of elevated [CO2] on PEPC activity or respiration rates. Similar results were found for a variety of species, involving 600 measurements, in which [CO2] increases did not alter the CO2 and O2 leaf exchanges in the dark (Davey et al., 2004
).
It seems that direct effects of [CO2] on mitochondrial enzymes may have no consequence on the specific respiratory rate of whole tissues. Because mitochondrial respiratory enzymes are generally in excess to the levels required to support normal tissue respiratory activity under most growth 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 direct effects of CO2 on mitochondrial enzyme activity, as it has been seen in leaves of some plants grown at high [CO2] (i.e. Griffin et al., 2001
).
Another factor to consider is that increases in alternative pathway activity upon inhibition of cytochrome oxidase by a change in [CO2] will result in unaltered dark respiratory rates (as illustrated in Fig. 1). However, an increase in the non-phosphorylating activity of the alternative pathway reduces the efficiency with which energy from oxidized substrates supports growth and maintenance of plants (Gonzalez-Meler and Siedow, 1999
; Gonzalez-Meler and Taneva, 2004
). Some studies have reported that the growth of 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 patterns have been attributed, in part, to effects of [CO2] on plant respiration, including increased activity of the non-phosphorylating alternative pathway. These CO2 effects are considered next.
Are there direct effects of CO2 on whole plants?
In the past, in some studies, plants have been grown at [CO2] elevated only at night-time to assess the long-term consequences of the previously considered direct effects of CO2 on respiration rates. Although most of these studies have found that growth patterns were altered in plants exposed to high night-time [CO2], these effects cannot be attributed to direct effects of [CO2] on respiration for reasons explained above. Bunce (1995)
observed that the biomass and leaf area ratio of Glycine max increased and that photosynthetic rates decreased in plants exposed to high night-time [CO2] relative to plants grown at normal ambient [CO2]. Similarly, Griffin et al. (1999)
found that Glycine max exposed to high night-time [CO2] had lower leaf respiration rates and greater biomass than plants grown at ambient or elevated [CO2]. Reuveni et al. (1997)
speculated that increases in the biomass of Lemna gibba grown at high night-time [CO2] relative to control plants, was due to a reduction in alternative pathway respiration (although the alternative pathway activity was not measured). Reduction in alternative pathway activity might more fully couple respiration rates with growth 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 C4 species studied. In a later study, Bunce (2002)
described that carbohydrate translocation was reduced within 2 d of exposing plants to elevated night-time [CO2] when compared with plants grown at ambient conditions day and night. These results suggest that elevated [CO2] may have other uncharacterized direct effects on plant physiology that can have the consequence of reducing energy demand for carbohydrate translocation, hence reducing the rate of leaf respiration. If so, these new types of effects cannot be catalogued as direct effects of [CO2] on respiration but as indirect effects, making more research in this area necessary.
In summary, even though rapid changes in [CO2] can inhibit the activity of some mitochondrial enzymes directly, previously reported direct effects of [CO2] on tissue respiration are likely to be due to measurement artefacts. Therefore, direct effects of [CO2] on specific respiration rates (although not necessarily on respiration physiology) should be dismissed as having a major impact on the amount of anthropogenic carbon that vegetation could retain. The role of the alternative pathway in direct respiratory responses to elevated [CO2], although unresolved, would have little impact, if any, on the general conclusion that direct effects of [CO2] on plant respiration are not to be considered in plant growth or carbon cycle models. Other effects of long-term elevation of night-time [CO2] can alter plant growth characteristics, and indirectly affect both respiration rates and the relative activity of the cytochrome and alternative pathways. Therefore these effects cannot be referred to as direct effects but rather as indirect effects of [CO2] on respiration rates.
Indirect effects
Indirect CO2 effects represent changes in tissue respiration in response to plant growth at elevated atmospheric [CO2] (Amthor, 1997
), because of changes in tissue composition (Drake et al., 1997
). Other indirect effects of [CO2] on plant respiration include changes in growth or response to environmental stress, as well as changes in the respiratory demand for energy relative to that of plants grown at ambient [CO2] (Bunce, 1994
; Amthor, 2000b
). Such indirect effects of plant growth at elevated [CO2] can be detected as a reduction in CO2 emission (or O2 consumption) from plant tissues when measured at ambient [CO2] (Gonzalez-Meler et al., 1996a
).
Indirect effects on enzymes: is there acclimation of respiration to elevated [CO2]?
Acclimation of respiration to high [CO2] can be defined as the down- or up-regulation of the respiratory machinery (i.e. amount of respiratory enzymes, number of mitochondria) irrespective of changes in specific respiration rates when plants are grown at elevated [CO2] (Drake et al., 1999
). A change in the leaf respiratory machinery of plants grown at high [CO2] can be expected because of (a) increases in carbohydrate content, (b) reduced photorespiratory activity and (c) reductions in leaf protein content (15 % on average), when compared with plants grown at current ambient [CO2] (Drake et al., 1997
). These three processes can have different and sometimes opposite effects on levels of respiratory enzymes and specific rates of respiration.
As atmospheric [CO2] rises, increased photosynthesis results in higher cellular carbohydrate concentrations (Drake et al., 1997
; Curtis and Wang, 1998
). Increased carbohydrates can stimulate the specific activity of respiration, due to the greater availability of respiratory substrates (Azcón-Bieto and Osmond, 1983
) and higher energy demand for phloem loading of carbohydrates (Bouma et al., 1995
; Körner et al., 1995
; Amthor, 2000b
). Additionally, increased tissue carbohydrate levels (as in the case of plants grown at high [CO2]) could result in an increase of transcript levels of cytochrome oxidase (Felitti and Gonzalez, 1998
; Curi et al., 2003
) and cytochrome pathway activity (Gonzalez-Meler et al., 2001
). In contrast, a reduction in photorespiratory activity in plants grown at high [CO2] will reduce the need for the mitochondrial compartment, which may result in a reduction in mitochondrial proteins and functions (Amthor, 1997
; Drake et al., l999
; Bloom et al., 2002
). Not surprisingly, the available studies show that levels and activity of respiratory machinery can either increase or decrease in leaves of plants grown at high [CO2] with no concomitant effects on respiration rates (Fig. 2).
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For instance, indirect effects of elevated [CO2] on respiration of leaves of Lindera benzoin and stems of Scirpus olneyi were correlated with a reduction in maximum activity of cytochrome oxidase (Azcon-Bieto et al., 1994
Indirect effects of [CO2] on respiration of tissues and whole plants
It has been historically accepted that leaf respiration is reduced as a consequence of plant growth at elevated [CO2] (El Kohen et al., 1991
; Isdo and Kimball, 1992
; Wullschleger et al., 1992a
; Amthor, 1997
; Drake et al., 1997
; Curtis and Wang, 1998
; Norby et al., 1999
). Poorter et al. (1992)
showed that leaf respiration was reduced, on average, by 14 % when expressed on a leaf mass basis, but increased by 16 % on a leaf area basis. Curtis and Wang (1998)
compiled respiratory data for woody plants, and observed that growth at elevated [CO2] resulted in an 18 % inhibition of leaf respiration (mass basis). In this section 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 not altered by growth at elevated [CO2] during most of the plant's growing season (Johnson et al., 1994
; Matamala and Schlesinger, 2000
). Total ecosystem root respiration may increase if root mass and/or turnover increases (Hungate et al., 1997
; Hamilton et al., 2002
; George et al., 2003
; Matamala et al., 2003
).
Many previous reviews and meta-analyses (see above) have compared respiratory rates of plants grown and measured at the [CO2] at which plants were grown. Therefore, these respiration measurements are also susceptible by the gas 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 compared with plants grown at ambient [CO2] (Table 1). Davey et al. (2004)
also showed that the O2 uptake of leaves of plants grown at high [CO2] was slightly increased relative to control plants. Gas exchange leaks (Jahnke, 2001
) should not be a factor in determining the rates of CO2 emission rates when rates are measured and compared at ambient [CO2] for plants grown at ambient and elevated [CO2]. A re-analysis of the literature focused on leaf respiratory responses (on a leaf mass basis) of plants grown at ambient and elevated [CO2] and measured at an ambient [CO2], suggests that specific leaf respiration rates will be unaltered or even increased in plants grown at elevated [CO2] (Table 2). Therefore, the generally accepted onclusion that respiration rates of plants grown at elevated [CO2] is reduced 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 significant variability in the leaf respiratory response to growth at elevated [CO2] when compared with plants grown at ambient conditions, ranging from 40 % inhibition (Azcon-Bieto et al., 1994
) to 50 % stimulation (Williams et al., 1992
). Considerations on the physiological basis by which the acclimation response of respiration to elevated [CO2] varies, is considered next.
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In boreal species, reduction of respiration of plants grown at high [CO2] was related to changes in tissue N and carbohydrate concentration (Tjoelker et al., 1999
The growth component of respiration (Amthor, 2000b
) could also be reduced in plants grown at elevated [CO2] as a result of altered tissue chemistry (Griffin et al., 1993
). Based on the chemical composition of tissues, Poorter et al. (1997)
found that elevated [CO2] could reduce growth construction costs by 1020 %. Griffin et al. (1993
, 1996a)
also observed reductions in construction costs of Pinus taeda seedlings grown at elevated [CO2]. Hamilton et al. (2001)
reported that elevated [CO2] slightly reduced construction costs of leaves of mature trees (including P. taeda) at the top of the canopy, but not at the bottom of the canopy. Such a small reduction can be explained by reductions in tissue [N], as observed in leaves exposed to high [CO2] at the top of the canopy. Changes in construction costs did not result in a decrease in the leaf respiration rates of P. taeda trees exposed to elevated [CO2] (Hamilton et al., 2001
).
The lack of long-term effects of increased [CO2] on specific plant respiration rates could also be due to a lower involvement of the alternative pathway (Gonzalez-Meler and Siedow, 1999
; Griffin et al., 1999
). Respiration through the alternative pathway bypasses two of the three sites of proton translocation; so the free energy released is lost as heat, and is unavailable for the synthesis of ATP. Respiration associated with this pathway will not support growth and maintenance processes of tissues as efficiently as respiration through the cytochrome path. On the other hand, the activity of the alternative pathway of respiration could decrease upon doubling [CO2], masking increases in the activity of the cytochrome pathway and making respiration more efficient, as it was the case in understorey trees grown under elevated [CO2] (Gonzalez-Meler and Taneva, 2004
).
Despite earlier reports, the responses of plant respiration to growth under high [CO2] are variable and perhaps species specific, although the overall trend may be a moderate increase in respiration rates of leaves of plants grown under elevated [CO2] relative to the ambient ones (Tables 1 and 2). Ultimately, altered specific respiration rates of tissues will depend on the net balance between the demand for ATP from maintenance (including phloem loading and unloading) and growth processes and on carbon allocation patterns between sinks and source tissues. The fact that the mitochondrial machinery has been shown to increase in leaves of plants grown at elevated [CO2] suggests, however, a larger participation of mitochondria in functions other than oxidative phosphorylation. Finally, indirect effects of [CO2] on tissue respiration rates can be augmented or offset by changes in plant size and/or changes in carbon allocation between plant parts.
| INTEGRATED EFFECTS OF ELEVATED [CO2] ON PLANT RESPIRATION AT THE ECOSYSTEM LEVEL |
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Terrestrial ecosystems exchange about 120 Gt of carbon per year with the atmosphere, through the processes of photosynthesis (leading to gross primary production, GPP) and ecosystem respiration (Re) (Schlesinger, 1997
Annually, terrestrial plant respiration releases 4060 % of the total carbon fixed during photosynthesis (Gifford, 1994
; Amthor, 1995
) representing about half of the annual input of CO2 to the atmosphere from terrestrial ecosystems (Schlesinger, 1997
). Therefore the magnitude of terrestrial plant respiration and its responses to [CO2] are important factors governing the intrinsic capacity of ecosystems to store carbon. Plant respiration responses to high [CO2] may stem from several mechanisms (in absence of direct effects on respiration rates): (a) indirect effects; (b) changes in total plant biomass; and (c) changes in plant carbon allocation. If it is confirmed that the response of overall terrestrial plant respiration to an increase in atmospheric [CO2] is small (Tables 1 and 2), then changes in global plant respiration should be proportional to changes in biomass. However, experimental evidence suggests otherwise, or that the response of plant respiration at the ecosystem level to elevated [CO2] may be more a function of carbon allocation patterns rather than just of increases in plant size (Drake et al., 1996
; Hamilton et al., 2002
).
Attempts to scale [CO2] effects on mitochondrial or tissue respiration to the ecosystem level are problematic because, unlike photosynthesis, little is known about applicable scaling methods for plant respiration (Gifford, 2003
). Current attempts to build respiratory carbon budgets at the canopy level require knowledge of maintenance and growth respiration (see above), as well as tissue respiratory responses to light, temperature and [CO2] (Amthor, 2000b
; Gifford, 2003
; Turnbull et al., 2003
) or have been based on theoretical respiration-to-photosynthesis ratios (i.e. Norby et al., 2002
). The respiration-to-photosynthesis ratio was not affected by elevated [CO2] in soybean plants (Ziska and Bunce, 1998
) but was reduced in pine forests stands (Hamilton et al., 2002
) when compared with ambient controls. The limited available data on the effects of elevating the [CO2] on intact field ecosystems on plant and total ecosystem respiration are summarized in Tables 3 and 4.
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The contribution of CO2-induced changes in ecosystem respiration to annual NEP of an intact salt marsh exposed to elevated [CO2] in open-top chambers is shown in Table 3. In this ecosystem, elevation of atmospheric CO2 by 350 µL L1 over ambient levels consistently reduced night-time ecosystem respiration in C3 and C4 community stands (Drake et al., 1996
In forests exposed to elevated [CO2] using free air CO2 enrichment (FACE), GPP was stimulated by 1536 % (Table 4) over ambient stands, resulting in consistent increases in net primary productivity (NPP). Increases in GPP and NPP seemed to be accompanied by variable responses on whole-plant respiration, which could be increased by as much as 20 % (Table 4). For instance, Hamilton et al. (2002)
found that elevated [CO2] increased forest NPP by 27 % without any increase in total plant ecosystem respiration. This result can be explained by a possible decrease in specific respiration rates at high [CO2] accompanied by larger biomass of plants grown at elevated [CO2]. In a Popolus deltoides plantation at Biosphere 2 centre, elevated [CO2] increased stand-level plant respiration by 40 % when compared with ambient (Table 4). The total increase in stand-level plant respiration was larger than the CO2 stimulation of NPP, suggesting that, in this case, specific respiration rates and plant size both contributed to the increase in plant respiration of trees grown in high [CO2] (R. J. Trueman and M. A. Gonzalez-Meler, unpubl. res.).
Some studies suggest that increases in ecosystem-level plant respiration in ecosystems exposed to elevated [CO2] mainly occur in below-ground plant tissues (Hungate et al., 1997
; Lin et al., 2001
; Hamilton et al., 2002
), which in turn may stimulate soil respiration rates (Zak et al., 2000
; Pendall et al., 2003
). This requires a substantial proportion of the additional C assimilated by plants growing at elevated [CO2] to be allocated to roots for growth and turnover (Johnson et al., 1994
; Hungate et al., 1997
; King et al., 2001
; Matamala et al., 2003
). Greater plant C allocation below ground can theoretically increase the contribution of root respiration to total soil respiration because of greater root biomass relative to ambient [CO2]. However, Hamilton et al. (2002)
reported increases in total root respiration in a forest exposed to elevated [CO2], where root mass, turnover (Matamala et al., 2003
) or respiration rates (Matamala and Schlesinger, 2000
; George et al., 2003
) were not affected by the CO2 treatment. The apparent disparity may be due to the different methodologies employed in these studies and in the contribution of rhizosphere activity to soil CO2 efflux, emphasizing the need for more coordinated research in building ecosystem carbon budgets using multiple approaches, especially below ground.
In conclusion and contrary to what was previously thought, specific respiration rates are generally not reduced when plants are grown at elevated [CO2]. This is because direct effects of [CO2] on respiratory enzymes are inconsequential to specific respiration rates of tissues. A re-analysis of the literature comparing respiration of leaves of plants grown at ambient [CO2] with leaves of plants grown at elevated [CO2] when rates are measured at the same [CO2], indicate that leaf respiration on average will not be greatly changed by increasing atmospheric [CO2]. Increases in growth rates appear to be compensated for by changes in tissue chemistry that affect growth and maintenance respiration. If specific rates of respiration are not affected by growth at elevated [CO2], respiration from the terrestrial vegetation in a high-CO2 world should be proportional to changes in plant biomass. However, whole ecosystem studies show that canopy respiration does not increase proportionally to increases in biomass when natural ecosystems are exposed to elevated atmospheric [CO2]. Field studies also suggest that a larger proportion of plant respiration takes place in the root system under elevated [CO2] conditions. Fundamental information is still lacking on how respiration and the processes supported by it are physiologically controlled, thereby preventing sound interpretations of what seem to be species-specific responses of respiration to elevated [CO2]. Therefore the role of plant respiration in augmenting the sink capacity of terrestrial ecosystems is still uncertain.
| ACKNOWLEDGEMENTS |
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This review is part of a lecture given at the International Congress of Plant Mitochondria held in Perth in July 2002, partly sponsored by Annals of Botany. M.A.G.-M. specially thanks Jeff Amthor for his work in this area, his thoughts, discussions and specific comments in parts of this manuscript. Authors also wish to thank Joaquim Azcon-Bieto, Bert Drake, Evan DeLucia, Steve Long, Miquel Ribas-Carbo and Jim Siedow for their discussion on the effects of elevated [CO2] on respiration of organelles, plants and ecosystems over the years. We acknowledge financial support by US Department of Agriculture (M.A.G.-M.), UIC fellowship (L.T.), and Sigma Xi and provost awards to L.T. and R.J.T.
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