Voi 511996): 261-270. An overview of how rubisco and carbohydrate metabolism may be regulated at elevated atmospheric [COJ and temperature George Bowes Department ofBotany, 220 Bartram Hall, University of Florida, Gainesville, FL 32611, USA, e-mail: bowes@nervm.nerdc.ufl,edu Joseph C.V. Vu USDA-ARS and Agronomy Department, University ofFlorida, USA Mian W. Hussain Department ofBotany, University ofFlorida, USA Arja H. Pennanen Department ofPlant Production, University ofHelsinki, Finland L. Hartwell Allen, Jr. USDA-ARS and Agronomy Department, University ofFlorida, USA Although atmospheric C0 2 concentration ([COJ) has been up to 16-fold higher than at present, the past several million years have seen atypically low values. Thus, modern-day plants are adapted to cope with a low [C0 2]/[02 ] ratio. The present [C02 ] does not saturate C 3 photosynthesis, so its dou- bling produces an “efficiency effect”, but it is not always fully realized. Acclimation to high [C0 2] during growth can down-regulate photosynthesis, presumably to optimize carbon acquisition and utilization. A primary factor in acclimation is a reduction in rubisco. Two crops, rice and soybean, were used to study this phenomenon. Rice photosynthesis and growth peaked at 500 pmol mol~! , whereas soybean responded up to 990 pmol mol"1 . Rubisco concentration declined under C0 2-en- richment and increasing temperatures, more so in rice than soybean. The rubisco k cat of rice was unaffected by growth [C02 ] or temperature, but that from soybean was increased by both. In rice the capacity to handle carbohydrate, as measured by sucrose phosphate synthase activity was up-regulat- ed by C0 2 -enrichment, but not by temperature. Leaf carbohydrates were increased by [C0 2 ], but decreased by higher temperatures, starch more so than sucrose. Even though C 3 species differ in response to [C02 ] and temperature, C0 2 -enrichment can moderate adverse effects of temperature extremes. Key words: acclimation, ribulose bisphosphate carboxylase-oxygenase, rice, soybean, sucrose phos- phate synthase, starch, Q-enzyme © Agricultural and Food Science inFinland Manuscript received February 1996 261 AGRICULTURAL AND FOOD SCIENCE IN FINLAND https://www.c-info.fi/en/info/?token=cIt7lS4tyss4Smdx.k74FBwoW72o6UGv4qilfSA.MsW9d9-0jVD_JC3EyXTUxdHMClYX1sxCCP5M6XFlfnf8QyNWJIMmUtWLJKmOchvHeOhqf_AZAyeY6uo3Yab1Mvnj0lmbPDJ-yNZUoG26WEUB3JQDuwnxD3_UAaomeC-4vF9fwedhzCLTowhJiA0LiD03YSvdZu06162oxGHXT20CVyrqoLdsF8zp06mGRR2ZPT0N4rUGjI-xhfQZChhsiLZTLjno6o_JDFZaMqrjYUZBJVjfh9Ab3bC7UecbPggq7ZTSNIEcID2K7eNJtUEqPPgNM9Ms6cQRlrkcZy2M5jm8qdAYl1tja_ZhquSl6bWzH-qDK_ce8_JzjiQLcBUXzYDK6TbMq-38QycK3HIF Bowes, G. etal: Metabolic regulation under high CO, and temperature Atmospheric [COJ; past, present, and future Predicting the future is an inexact science, but various scenarios forecast an atmospheric C02 concentration ([C02 ]) of between 575 and 900 pmol mol' 1 by the year 2100 (King et al. 1992). The consequences of this rise in atmos- pheric [C0 2 ] will not be distributed equally around the globe. The photosynthetic activity of terrestrial ecosystems in northern latitudes is a major component moderating the rise in atmos- pheric C02 by sequestering a substantial propor- tion of the carbon from anthropogenic sources (Takahashi et al. 1992). Thus, as the [C0 2 ] con- tinues to rise, the responses of northern ecosys- tems and agroecosystems could well have important feedback effects that impact the global rate of increase. Because C02 is a greenhouse gas its increase is expected to cause global warming, and influ- ence climatic patterns. The current Holocene interglacial period is characterized by a stable climate (Thomson 1993). However, climate can oscillate rapidly, and in the previous interglacial period changes on the order of 10°C apparently occurred within a few decades (Dansgaard et al. 1993). Such rapid and extreme temperature fluc- tuations would have more impact on photosyn- thesis and growth, even to the point of species survival, than a doubling in atmospheric CO,. An increase of greenhouse gases equivalent to a doubling of [C02 ] is predicted to lead to a glo- bal mean temperature rise of between 1.5 and 4.5 °C and an increase in average precipitation. However, at regional levels the magnitude of the changes is uncertain (Carter 1996). These cli- mate changes, in addition to higher [CO,], will also affect photosynthesis, and the situation is further complicated by interactive effects of the environmental parameters. High [CO,] and temperature are not new phe- nomena for the planet. Atmospheric [C0 2 ] has apparently fluctuated by more than 20-fold over geologic time. Mean global temperatures have also fluctuated in some correspondence with changes in [C0 2 ]. When terrestrial plants first appeared atmospheric [C0 2 ] may have been as high as 4000 to 6000 pmol mol' 1, but the past 400 million years has seen an overall decline (Böger 1980,Budyko et al. 1987,Yapp and Poths 1992, Berner 1993). The rise of vascular plants and their attendant photosynthesis was a major factor in this decline. The past several million years have seen atypically low atmospheric [C0 2 ] (Post et al. 1990). As a consequence, many modern-day plants, including crop species, tend to be adapted to a low [C0 2]/[02 ] ratio (Badger 1992), but they now have to cope with an at- mospheric [C0 2 ] that has almost doubled since the last glacial maximum. Plants of the 21 stcen- tury will encounter even higher [C0 2 ], and like- ly higher temperature regimes. Furthermore, in northern latitudes changing climatic patterns could extend the season for photosynthetic ac- tivity. The degree to which temperate species will respond to these potentially positive inputs will partially depend on their ability to acclimate to the shift in resources, especially a rise in the C:N ratio. In the long-term view it will be influenced by the capacity of a species for genotypic adap- tation, or in the case ofcrop plants, human inge- nuity with molecular or classical breeding tech- niques. Acclimation to elevated [COJ The photosynthesis ofsome 95% of species (C 3 ), which includes virtually all crop and forest spe- cies of northern latitudes, is not saturated by the present [C0 2 ]. Thus in short-term experiments a doubling of [C0 2 ] increases the net photosyn- thetic assimilation rate by 50%; reduces pho- torespiration, dark respiration, and stomatal con- ductance; and enhances quantum and water use efficiency, the C:N ratio, and modulates growth (Bowes 1993,Woodrow 1994). Thus CO, enrich- ment has an “efficiency effect”, and in this re- spect it differs from fertilization responses that occur with other nutrients, such as N and P. Table 1 shows the light-saturated, photosyn- thetic rates for leaves of CO,-enriched rice2 262 AGRICULTURAL AND FOOD SCIENCE IN FINLAND Vol. 5 (1996); 261-270. Table I. Photosynthetic rate, rubisco protein concentration, catalytic turnover, and activation in leaves of rice and soybean grown season-long, with natural sunlight and three different day/night temperature and two [C02 ] regimes. Measurements were made when solar photon irradiance exceeded 1200pmol mV. Growth Conditions Photosyn- Rubisco K cai Activation thetic Rate Content Temperature [C0 2] (pmol C02 (mg g“‘ (mol C02 (°C) (pmol mol"') nrV) fresh wt)mmob's 1)" 1) (%) Rice 32/23 330 19.3 16.4 13.0 91 660 31.8 13.0 13.6 80 35/26 330 21.2 15.7 14.2 87 660 32.6 12.3 13.9 85 38/29 330 16.0 12.7 13.2 79 660 26.6 11.5 13.5 68 Soybean 32/22 350 27.5 15.5 15.6 97 700 40.9 14.2 16.8 83 36/26 350 23.5 14.5 16.8 86 700 39.8 13.1 18.1 78 40/30 350 17.1 12.8 19.1 74 700 33.3 11.3 20.1 71 (Oryza saliva L. cv. IR-72) and soybean (Gly- cine max L. Merr. cv. Bragg). The plants were grown season-long in natural sunlight under sim- ilar controlled conditions at near-ambient and twice-ambient atmospheric [C0 2 ], and three dif- ferent day/night temperatures. The rates were measured on attached, fully-expanded leaves with a LI-COR 6200 system at the growth [CO,] and temperature. Measurements were made 90 days after planting for rice and 60 days for soy- bean at the growth [C0 2 ], At a growth tempera- ture of 32°C, rice and soybean leaf photosyn- thetic rates were enhanced 65 and 49%, respec- tively, by doubling the [CO,]. Thus for both spe- cies a positive effect on photosynthesis of the elevated [C0 2 ] was maintained. Previous data for these two species showed that the C02 response for rice photosynthesis, biomass, and yield peaked at about 500 pmol mol ', whereas the soybean responded up to at least 990 pmol mol-1 (Baker et al. 1989, 1990, Campbell et al. 1990) However, “efficiency effects” such as these in rice and soybean are not necessarily retained by all C, species in long-term C02 -enrichment experiments. Acclimation can cause down-reg- ulation in photosynthesis, as measured by chang- es in the response of assimilation rate to inter- cellular [C02 ] (A/C curve). Presumably this optimizes carbon acquisition with its utilization in plants that are more adapted to low [C0 2 ] con- ditions. Acclimation involves various aspects of me- tabolism, but a major site is ribulose bisphos- phate carboxylase-oxygenase (rubisco). This enzyme initiates both the photosynthetic carbon reduction (PCR) cycle, and the photorespiratory carbon oxidation (PCO) cycle, and is a major component regulating C0 2 assimilation in C 3 species. Control analyses show that at high irra- diance the flux control coefficients for rubisco can be as high as 0.8 to 1.0, where 1.0 indicates it alone is the limiting factor (Stitt and Schulze 1994,Woodrow 1994), though under most con- ditions, control is shared with other photosyn- thetic processes. The kinetics of rubisco have been used to model A/C curves (Farquhar et al. 1980, Long et al. 1993, Sage 1994). The initial, linear phase of the A/C curve is a measure of carboxylation 263 AGRICULTURAL AND FOOD SCIENCE IN FINLAND Bowes, G. et ai: Metabolic regulation under high C02 and temperature efficiency, because photosynthesis is limited by the amount of active rubisco. This phase is fol- lowed at higher [CO,] by an inflection above which A rises more gradually, and is limited by the rate at which RuBP can be regenerated by the PCR cycle. Regeneration of RuBP is linked to the rate ofnon-cyclic electron transport, which provides ATP for the PCR cycle, and to PCR cycle enzyme activities which convert triose phosphates to RuBP. In the RuBP-limited phase, an increase in [C0 2 ] may still increase A because photorespiration is reduced, and a greater pro- portion of RuBP is used for carboxylation, in- stead of oxygenation. Under some conditions, RuBP regeneration is limited by inorganic phos- phate (P,), which depends on the rate at which P. in triose phosphates is recycled to the chloro- plast (Sharkey and Vanderveer 1989, Socias et al. 1993). During photosynthesis, C, leaves maintain C at close to the inflection point, such that rubisco and RuBP-regeneration capacity are co-limiting (Stitt 1991,Long et al. 1993, Sage 1994). A dou- bling in [C0 2 ] reduces stomatal limitations be- cause C rises from about 245 to 490 pmol moL 1 CO,. The rise in C causes the initial 50% in- crease in photosynthesis that is often reported, and moves photosynthesis into the RuBP-limit- ed region of the A/C. curve (Stitt 1991,Woodrow 1994). During long-term enrichment (weeks), accli- mation may occur in theA/C curve, with changes in the initial slope and/or RuBP-limited region. The underlying causes of acclimation in the Al C. curve are only partially resolved. Potentially it could be a stress response, indicating physio- logical dysfunction in plants that over millennia have adapted to low [C0 2 ]. Or, it may be an op- timization process as resources change. In some species or conditions, elevated C02 produces substantial carbohydrate accumulation within the leaves. The leaf morphology can be deformed; massive starch granules can distort chloroplasts, and possibly disrupt function by distending the thylakoid membranes and imposing constraints on the diffusion of gases or metabolites (Bowes 1991, Stitt 1991, Sage 1994). In most instances down-regulation of C02 assimilation probably reflects a restricted capac- ity to handle the extra carbon, because other en- vironmental resources are insufficient, or the plant has inherent metabolic limitations. Accord- ing to this view, acclimation is an optimization process thatreallocates resources from non-lim- iting components, such as carbon acquisition, into limiting components such as electron trans- port, and carbohydrate handling (Bowes 1991, Sage 1994). The availability of N would be a primary factor, because C02 enrichment increas- es the C:N ratio of plants (Conroy and Hocking 1993, Pettersson and McDonald 1994). Rubisco responses to elevated m Although various biochemical components are involved in acclimation, rubisco has a leading role, due to the fact that this enzyme is both the primary regulatory site for CO, fixation and a major repository of leaf N. There are reports for a number of species of reduced rubisco activity at elevated C02 (Spencer and Bowes 1986,Sage et al. 1989,Besford et al. 1990, Rowland- Barn- ford et al. 1991, Tissue et al. 1993). A decrease in rubisco activity may be caused by a reduction in rubisco protein concentration, which is con- sistent with the hypothesis that N is being real- located. We found the rubisco protein of rice declined linearly with increasing [C0 2 ], drop- ping by as much as 60% (Rowland-Bamford et al, 1991). Rubisco protein may still decline with seemingly adequate N supplies (Sage et al. 1989, Rowland-Bamford et al. 1991, Conroy and Hock- ing 1993), possibly because the C:N ratio dur- ing growth is unbalanced. Some species show little or no decline in rubisco concentration (Campbell et al. 1988, 1990, Sage et al. 1989, Socias et al. 1993, Sage 1994). In this regard, our studies with rice and soybean grown under similar conditions indicate that rice seems more 264 AGRICULTURAL AND FOOD SCIENCE IN FINLAND Vol. 5 (1996): 261-270. susceptible to down-regulation of rubisco pro- tein than soybean, and this is also true for the A/ C. curve (Campbell et al. 1988,Rowland- Barn- ford et al. 1991). In some situations the reduction in rubisco activity is due to a lower activation state (Camp- bell etal. 1988, Sage etal. 1989,Yelleet al. 1989, Rowland-Bamford et al. 1991,Sociaset al. 1993, Tissue et al. 1993). Enrichment does not change the apparent K m(CO,) of rubisco (Bowes 1991, Rowland-Bamford et al. 1991). Table 1 shows several parameters for rubis- co extracted from rice and soybean leaves rap- idly frozen in liquid N 2 around midday, 60 and 53 days after planting, respectively. Rubisco was extracted, and assayed at 30°C, as described pre- viously (Vu et al. 1987); while rubisco protein concentration was measured using the radioim- mune procedure (Vu and Yelenosky 1988). Rice grown at the two lower temperatures showed about a 20% decrease in rubisco protein concentration under the double-C02 treatment (Table 1). Soybean, however, exhibited only about a 10% reduction. The catalytic turnover rate (K ca| ) of rice rubisco was unaffected by the high [CO,] treatment; whereas unexpectedly, that of soybean showed a small but consistent in- crease (Table 1). Both species exhibited lower daytime rubisco activation values when the plants were grown under CO,-enriched condi- tions (Table 1). Measurement ofrubisco activities from dark- sampled leaves of these plants, taken after sun- set or before dawn, indicated that C02-enrich- ment may affect the metabolism of carboxyara- binitol 1- phosphate (CAIP), an endogenous in- hibitor of rubisco which occurs in both rice and soybean. In rice during the transition from day to night, rubisco activity declined more rapidly when the plants were growing in the C0 2-en- riched conditions (data not shown). This suggest- ed that synthesis of CAIP was enhanced by the higher C02 . Growth temperature had little effect on this response. In contrast, with soybean this apparent enhancement of CAIP synthesis was more dependent upon elevated temperature than ICO,]. These experiments with similarly-treated rice and soybean plants, indicate we must expect spe- cies-specific differences in the acclimation and regulation of rubisco among plants exposed to elevated [CO,]. Feedback effects from carbohydrate metabolism The most often cited explanation for acclima- tion and the down-regulation of rubisco is that C0 2 enrichment causes an imbalance in the source-sink capacities, especially insufficient sink capacity for the excess carbohydrate pro- duction (Arp 1991, Farrar and Williams 1991, Stitt 1991, Sheen 1994, Woodrow 1994). The mechanism by which the imbalance is sensed probably involves feedback effects via end-prod- uct accumulation (Stitt 1991, Sheen 1994). This is indicated by a number of sugar-feeding stud- ies which resulted in reduced photosynthesis, rubisco activity and concentration. Similarly, the over-expression of acid invertase in transgenic plants, and the resultant hexose accumulation, decreasedphotosynthesis and PCR cycle enzyme activities (Stitt et al. 1990, Sheen 1994). A molecular model invokes the metabolite regulation ofgene expression, with glucose pro- viding a regulatory signal to repress the tran- scription of photosynthetic genes, including those encoding the small and large subunits of rubisco (Stitt 1991, Krapp et al. 1993, Sheen 1994). Nuclear genes encoding chloroplast pro- teins are reported to be more sensitive than chlo- roplastic genes when plants are exposed to ele- vated [C0 2 ] or sugar supply (Van Oosten et al. 1994). In addition, genes involved directly with carbohydrate metabolism can be positively, or negatively, regulated by sugars (Sheen 1994). This could be a means to up-regulate enzymes that process carbohydrate, and thereby assist in balancing the sink capacity with the source. This concept is consistent with our findings 265 AGRICULTURAL AND FOOD SCIENCE IN FINLAND Bowes, G. et ai: Metabolic regulation under high C02 and temperature Table 2. Sucrose phosphate synthase (SPS) activity, sucrose and starch contents in rice grown for 48 days with natural sunlight and five different day/night temperatures and two [C0 2 ] regimes. The SPS activity was measured at 30°C under saturating substrate conditions using leaves frozen in liquid N 2 at midday. Sucrose and starch contents repre- sent peak daytime values sampled late in the afternoon. Growth Conditions SPS Sucrose Starch Activity Content Content Temperature [C02 ] (nmol mg ' (mg g-1 (°C) (pmol mol ') protein lr') dry wt) 25/18 660 1488 61.8 55.4 28/21 330 1440 52.2 42.4 660 1638 65.6 62.5 31/24 660 1728 60,5 34,2 34/27 660 1806 58,9 30.6 37/27 660 1620 50.6 21.3 for C0 2 -enriched rice. While rubisco concentra- tion and activation were down-regulated (Row- land-Bamford et al. 1991), the activity of sucrose phosphate synthase (SPS) was increased by about 20% at 600 vpm as compared to 330 vpm C02 (Table 2). This enzyme is a key regulatory point in carbohydrate synthesis, especially for species which accumulate sucrose. The data shown in Table 2 are for SPS activity measured under saturating substrate and activator condi- tions as described by Stitt et al. (1988), using theresorcinol method to determine sucrose phos- phate formation. Along with SPS activity, both sucrose and starch were increased by C02-en- richment (Table 2). Rice clearly accumulates sucrose, as under all growth conditions the su- crose content of the leaves was equal to or high- er than that of starch. In this it differs from soy- bean, which mainly accumulates starch. A similar situation occurred in the sink-lim- ited regions of transgenic tobacco leaves which had invertase over-expressed in the cell walls; rubisco and fructose bisphosphatase activities declined, but SPS increased (Stitt et al. 1990). More work is required to determine how C02 enrichment influences the enzymes and alloca- tion of carbohydrates in plants that are predomi- nantly starch- or sucrose-accumulators. It is pos- sible that plants exemplified by soybean have inherent capacity to handle the additional car- bohydrate, and thus show less propensity for down-regulation of rubisco. Although soybean accumulates substantially more starch under C02 - enriched conditions, we have not observed any major up-regulation of ADP-glucose pyro- phosphorylase comparable to that of SPS activ- ity in rice. C0 2 enrichment and temperature effects Environmental conditions have a marked influ- ence on the stimulation of photosynthesis and growth by C02 -enrichment. Because of the effi- ciency effect, C02 -enrichment can improve re- source use, even when parameters such as tem- perature are exerting stress (Gifford 1992,Bowes 1993). Higher global temperatures are an impor- tant consideration in the rising CO, debate be- cause of interactive effects on photosynthesis. A rise in temperature lowers the ratio of [C0 2 ]/ [O,] in solution, shifts the specificity of rubisco towards oxygenase, enhances photorespiration and dark respiration, and increases the sink re- sponse relative to the source. Thus, positive ef- fects of C02 -enrichment are potentially greater as the temperature rises. Long (1991) calculated that with no down-regulation of rubisco an in- crease in atmospheric C0 2 to 650 prnol mol” 1 could increase light-saturated assimilation by 20% at 10°C but 105% at 35°C, and raise the temperature optimum for photosynthesis by 5°C. Interactive effects ofelevated [COJ and tem- perature on photosynthesis are demonstrated experimentally in Table 1. For rice, the differ- ence in photosynthetic rate between the ambient and twice-ambient [C0 2 ] treatment was about 60% at all growth temperatures. However, with soybean the difference increased with growth temperature, being 49% at 32°C but 95% at 40°C (Table 1). In both species, the adverse effects of elevated temperature on photosynthesis were 266 AGRICULTURAL AND FOOD SCIENCE IN FINLAND moderated by C02 enrichment, but the soybean response was closer to the Long model. Photosynthetic gains may not always be re- alized in long-term growth and yield due to an interplay offactors that complicate the issue. For example, leaves compensate for increased air temperatures by greater transpiration; whereas C02 enrichment tends to raise foliar temperatures by reducing transpiration (Allen 1990, Campbell et al. 1990, Long 1991). Furthermore, species within just the C 3 category differ markedly in the temperature regimes to which they are adapt- ed, and in tolerance of the low and high extremes where temperature becomes stressful. Tempera- ture regimes that enhance C02 -stimulated vege- tative growth can negatively impact reproduc- tive growth. The grain yield ofC02 -enriched rice showed about a 10% decline for each I°C rise above 26°C, and similar scenarios have been reported for soybean and wheat (Baker et al. 1989, 1992, Mitchell et al. 1993). This is because growth and reproduction reflect the integrated temperature response of metabolism and devel- opmental processes. As a consequence, species, developmental stage, light regime, nutrient sta- tus, and the temperature range, all modify tem- perature x C02 responses (Rawson 1992). In rice and soybean there was an interplay between elevated growth temperatures and [C02] on rubisco parameters (Table 1). For both spe- cies, rubisco protein concentration declined with increasing temperature, as well as with elevated [C0 2 ]. Similarly, the activation of rubisco from both species declined with higher temperatures and [COJ. Rice and soybean differed in terms of the response of rubisco’s catalytic turnover rate. For rice there was no effect of temperature or [COJ. In contrast, the K it for soybean rubis- co was increased by both elevated temperature and [C0 2 ] (Table 1). Despite the down-regula- tion in rubisco concentration and activation, the substrate effect from C02 -enrichment maintained relatively high leaf photosynthetic rates at unfa- vorably high temperatures (Table 1). In addition to effects on photosynthetic and rubisco activity, elevated temperatures influence carbohydrate metabolism. In C02-enriched rice plants, SPS activity was increased by tempera- tures up to 34°C, but thereafter declined (Table 2). Total non-structural carbohydrates declined with increasing growth temperature, but the de- cline in starch content was much greater than for sucrose (Table 2). Consequently, the sucrose to starch ratio increased with temperature. This was opposite to the effect of C02 enrichment, which tended to decrease the ratio. We have found that although C02 -enriehed soybeans synthesized more starch, ADP-glucose pyrophosphorylase activity was not greatly al- tered by temperature or [C0 2 ], However, high temperature (40°C) caused a dramatic fall-out of starch branching enzyme (Q-enzyme) activi- ty, which was ameliorated by C02 -enrichment (Pennanen et al. 1995). These data with rice and soybean suggest that high temperatures not only influence the amount of carbohydrate produced, but also its composi- tion, possibly shifting the amylose-to-amylopec- tin ratio in favor of the former. However, C02 - enrichment moderates the differences, and can have positive effects in a stress situation. Future increases in atmospheric C02 and day temperatures have the potential for positive in- teractive effects with many C 3 species, though in some regions the photosynthetic gains may not translate into greater yields, because oftem- perature stress on reproductive processes (Allen 1990, Bowes 1993). If mean global night tem- peratures increase the outcome is less predicta- ble. Higher temperatures at night could negate the lower respiration of C02-enriched species (Amthor et al. 1992), and increase damage to the reproductive system (Ahmed et al. 1993); but in heat-tolerantplants it may improve carbohydrate mobilization and ease sink limitations on pho- tosynthesis (Ahmed et al. 1993). In summary, among C 3 species the response to CO, enrichment is variable. Restrictive growth conditions can be influential, but evidence also points to the existence of inherent interspecific and intraspecific differences, reflective of dif- ferent RuBP regeneration and sink capacities. Limitations in these capacities can lower the in- creases that might otherwise be anticipated from 267 Vol. 5 (1996): 261-270. AGRICULTURAL AND FOOD SCIENCE IN FINLAND Bowes, G. etai: Metabolic regulation under high C02 and temperature rubisco kinetics alone. There is evidence that the rise in [C0 2 ] could offset the negative effects of high temperature regimes on photosynthesis and growth. Acknowledgements. Work in my laboratory was supported by the USDA/SEA NRICG Photosynthesis and Respira- tion Program, Grant No. 93-37306-9386 (GB), USDOE Grant No. DE-AIOS-88ER69014 (LHA Jr), and Finnish Academy of Science Grant No. 1022668 (AHP). References Ahmed, F.E., Hall, A.E. & Madore, M.A. 1993. Interac- tive effects of high temperature and elevated carbon di- oxide concentration on cowpea [Vigna unguiculata (L.) Walp.], Plant, Cell & Environment 16: 835-842. Allen, L.H., Jr. 1990. Plant responses to rising carbon dioxide and potential interactions with air pollutants. Jour- nal of Environmental Quality 19: 15-34. Amthor, J.S., Koch, G.W. & Bloom, A.J. 1992.CQ 2 in- hibits respiration in leaves of Rumex crispus L. Plant Physiology 98: 757-760. Arp, W.J. 1991. Effects of source-sink relations on pho- tosynthetic acclimation to C02 . Plant, Cell & Environment 14: 869-875. Badger, M.R. 1992. Manipulating agricultural plants for a future high CQ2 environment. Australian Journal of Botany 40: 421-429. Baker, J.T., Allen, L.H., Jr., Boote, K.J., Jones, P. & Jones, J.W. 1989. Response of soybean to air tempera- tureand carbon dioxide concentration. Crop Science 29: 98-105. -, Allen, L.H., Jr. & Boote, K.J. 1992. Temperature ef- fects on rice at elevated C02 concentration. Journal of Experimental Botany 43: 959-964. -, Allen, L.H., Jr., Boote, K.J., Jones, P. & Jones, J.W. 1990, Rice photosynthesis and evapotranspirafion in sub- ambient, ambient, and superambient carbon dioxide con- centrations. Agronomy Journal 82: 834-840. Berner, R.A. 1993. Paleozoic atmospheric C02 : impor- tance of solar radiation and plant evolution. Science 261: 68-70. Besford, R.T., Ludwig, L.J. & Withers, A.C. 1990. The greenhouse effect: acclimation of tomato plants growing in high CQ 2 , photosynthesis and ribulose-1, 5-bisphos- phate carboxylase protein. Journalof Experimental Bot- any 41: 925-931. Böger, P. 1980. The 02/C02 cycle: developmentand at- mospheric consequences. In: San Pietro, A. (ed ). Bio- chemical and PhotosyntheticAspects of Energy Produc- tion. Academic Press, New York. p. 175-190. Bowes, G. 1991. Growth at elevated C02 : photosynthet- ic responses mediated through Rubisco. Plant, Cell & Environment 14: 795-806. - 1993. Facing the inevitable; plants and increasing at- mospheric C02 . Annual Review of Plant Physiology and Plant Molecular Biology 44: 309-332. Budyko, M.1., Ronov, A.B. & Yanshin, A.L. 1987. His- tory of the Earth’s Atmosphere. Springer-Verlag, New York. 139 p. Campbell, W.J., Allen, L.H., Jr. & Bowes, G. 1988. Ef- fects of C02 concentration on rubisco activity, amount, and photosynthesis in soybean leaves. Plant Physiology 88: 1310-1316. Allen, L.H., Jr. & Bowes, G. 1990. Response of soy- bean canopy photosynthesis to C02 concentration, light, and temperature. Journal of Experimental Botany 41: 427-433. Carter, T.R. 1996. Developing scenarios of atmosphere, weather and climate for northern regions. Agricultural and Food Science in Finland 5: 235-249. (this issue) Conroy, J. & Hocking, P. 1993, Nitrogen nutrition of C 3 plants at elevated atmospheric C02 concentrations. Phys- iologia Plantarum 89: 570-576. Dansgaard, W., Johnsen, S.J., Clausen, H.8., Dahl- Jensen, D., Gundestrup, N.S., Hammer, C.U., Hvid- berg, C.S., Steffensen, J.P., Sveinbjornsdottir, A.E., Jouzel, J. & Bond, G. 1993. Evidence for general insta- bility of past climate from a 250-kyr ice-core record. Na- ture 364: 218-220. Farquhar, G.D., Caemmerer, S. von & Berry, J.A. 1980. A biochemical model of photosynthetic CQ 2 assimilation in leaves of C 3 species. Planta 149: 78-90 Farrar, J.F. & Williams, M.L. 1991. The effects of in- creased atmospheric carbon dioxide and temperature on carbon partitioning, source-sink relations and respiration. Plant, Cell & Environment 14: 819-830. Gifford, R.M. 1992. Interaction of carbon dioxide with growth-limiting environmental factors in vegetation pro- ductivity: implications for the global carbon cycle. In: Stan- hill, G. (ed.). Advances in Bioclimatology, Volume 1. Springer Verlag, New York, p.24-58. King, A.W., Emanuel, W.R. & Post, W.M. 1992. Pro- jecting future concentrations of atmospheric C0 2 with global carbon cycle models: the importance of simulat- ing historical changes. Environmental Management 16: 91-108. Krapp, A., Hofmann, 8., Schaefer, C. & Stitt, M. 1993 Regulation of the expression of rbcS and other photo- synthetic genes by carbohydrates: a mechanism for the ‘sink regulation' of photosynthesis? Plant Journal 3:817- 828. Long, S.P. 1991. Modification of the response of photo- synthetic productivity to rising temperature by atmospher- ic C02 concentrations: Has its importance been under- estimated? Plant, Cell & Environment 14: 729-739. -, Baker, N.R. & Raines, C.A. 1993. Analysing the re- sponses of photosynthetic C02 assimilation to long-term elevation of atmospheric CQ 2 . Vegetatio 104/105: 33- 45. Mitchell, R.A.C., Mitchell, V.J., Driscoll, S.P., Frank- lin, J. & Lawlor, D.W. 1993. Effects of increased CQ 2 268 AGRICULTURAL AND FOOD SCIENCE IN FINLAND Vol. 5 (1996): 261-270. concentration and temperature on growth and yield of winter wheat at two levels of nitrogen application. Plant, Cell & Environment 16: 521-529. Pennanen, A.H., Vu, J.C.V., Allen, L.H., Jr. & Bowes, G. 1995. Elevated C02 and temperature effects on en- zymes of sucrose and starch synthesis in soybean. Plant Physiology 108: 90, Pettersson, R. & McDonald, A.J.S. 1994. Effects of ni- trogen supply on acclimation of photosynthesis to ele- vated C02 . Photosynthesis Research 39: 389-400. Post, W.M., Peng, T.-H., Emanuel, W.R., King, A.W., Dale, V.H. & DeAngelis, D.L. 1990. The global carbon cycle. American Scientist 78: 310-326. Rawson, H.M. 1992. Plant responses to temperature under conditions of elevated C02 . Australian Journal of Botany 40: 473-490. Rowland-Bamford, A.J., Baker, J.T., Allen, L.H., Jr. & Bowes, G. 1991. Acclimation of rice to changing atmos- pheric carbon dioxide concentration. Plant, Cell & Envi- ronment 14: 577-583. Sage, R.F. 1994. Acclimation of photosynthesis to in- creasing atmospheric C02 : the gas exchange perspec- tive. Photosynthesis Research 39: 351-368. -, Sharkey, T.D. & Seemann, J.R. 1989. Acclimation of photosynthesis to elevated C02 in five C 3 species. Plant Physiology 89: 590-596. Sharkey, T.D. & Vanderveer, P.J. 1989. Stromal phos- phate concentration is low during feedback limited pho- tosynthesis. Plant Physiology 91: 679-684. Sheen, J. 1994. Feedback control of gene expression. Photosynthesis Research 39: 427-438. Sodas, F.X., Medrano, H. & Sharkey, T.D. 1993. Feed- back limitation of photosynthesis of Phaseolus vulgaris L. grown in elevated C02 . Plant, Cell & Environment 16: 81-86. Spencer, W. & Bowes, G. 1986. Photosynthesis and growth of water hyacinth under C02 enrichment. Plant Physiology 82: 528-533. Stitt, M. 1991. Rising C02 levels and their potential sig- nificance for carbon flow in photosynthetic cells. Plant, Cell & Environment 14: 741-762. Schaewen, A. von & Willmitzer, L. 1990. “Sink" reg- ulation of photosynthetic metabolism in transgenic tobac- co plants expressing yeast invertase in their cell wall in- volves a decrease of the Calvin-cycle enzymes and an increase of glycolytic enzymes. Planta 183: 40-50. - & Schulze, D. 1994. Does Rubisco control the rate of photosynthesis and plant growth? An exercise in molec- ular ecophysiology. Plant, Cell & Environment 17: 465- 487. -Wilke, 1., Fiel, R. & Heldt H.W. 1988. Coarse control of sucrose phosphate synthase in leaves: alterations of kinetic properties in response to the rate of photosynthe- sis and the accumulation of sucrose. Planta 174: 217- 230. Takahashi, T., Tans, P. & Fung, I. 1992. Balancing the budget. Carbon dioxide sources and sinks, and the ef- fects of industry. Oceanus 35: 18-28. Thomson, K.S. 1993. Northern exposures. American Scientist 81: 522-525. Tissue, D.T., Thomas, R.B. & Strain, B.R. 1993. Long- term effects of elevated C02 and nutrients on photosyn- thesis and rubisco in loblolly pine seedlings. Plant, Cell & Environment 16: 859-865. Van Oosten, J.J., Wilkins, D. & Besford, R.T. 1994. Regulation of the expression of photosynthetic nuclear genes by high CC2 is mimicked by carbohydrates: a mechanism for the acclimation of photosynthesis to high C02 ? Plant, Cell & Environment 17: 913-923, Vu, J.C.V., Allen, L.H., Jr. & Bowes, G. 1987. Drought stress and elevated C02 effects on soybean ribulose bi- sphosphate carboxylase activity and canopy photosyn- thelic rates. Plant Physiology 83: 573-578. - & Yelenosky, G. 1988. Water deficit and associated changes in some photosynthetic parameters in leaves of ‘Valencia’ orange (Citrus sinensis (L.) Osbeck). Plant Physiology 88: 375-378 Woodrow, I.E. 1994. Optimal acclimation of the C 3 pho- tosynthetic system under enhanced C02 . Photosynthe- sis Research 39: 401-412. Yapp, C.J. & Poths, H. 1992. Ancient atmospheric C02 pressures inferred from natural geothites. Nature 355: 342-344. Yelle, S., Beeson, R.C., Jr., Trudel, M.J. & Gosselln, A. 1989. Acclimation of two tomato species to high at- mospheric C02 . 11. Ribulose-1,5-bisphosphate carboxy- lase/oxygenase and phosphoenolpyruvate carboxylase. Plant Physiology 90: 1473-1477. 269 AGRICULTURAL AND FOOD SCIENCE IN FINLAND Bowes, G. et ai: Metabolic regulation under high C02 and temperature SELOSTUS Hiilihydraatti- ja proteiiniaineenvaihdunnan säätely kohonneen hiilidioksidipitoisuuden ja lämpötilan vallitessa George Bowes, Joseph CV. Vu, Mian W. Hussain, Arja H. Pennanen ja L. Hartwell Allen, Jr. University of Florida, USA ja Helsingin yliopisto Ilmakehän nykyinen C0 2 -pitoisuus ei kyllästä C3-fo- tosynteesiä, joten fotosynteesi tehostuu C0 2 - pitoi- suuden kaksinkertaistumisen seurauksena. Tehostu- minen ei kuitenkaan ole aina yhtä voimakasta. Kas- vin mukautuminen korkeaan C0 2 -pitoisuuteen kasvun aikana voi hidastaa fotosynteesiä, jotta hiilen saanti ja hyödyntäminen olisivat optimaalisia. Päätekijä mukautumisessa on rubiscon väheneminen. Rubisco on entsyymi, joka liittää hiilidioksidia sokerifosfaat- tiin Calvinin kierrossa. Kasvien aineenvaihduntaa korkeassa C02 -pitoisuudessa ja lämpötilassa tutkit- tiin riisillä ja soijapavulla. Riisin fotosynteesi ja kas- vu olivat huipussaan 500 ppm:n ja soijapavulla 990 ppm:n C0 2-pitoisuudessa. Rubiscon pitoisuus vähe- ni C0 2-pitoisuuden ja lämpötilan noustessa etenkin riisillä. C02 -pitoisuuden tai lämpötilan nousu eivät vaikuttaneet rubiscon aktiivisuuteen riisillä, mutta soijapavulla vaikutus havaittiin. Riisin kykyä käsitel- lä hiilihydraattia mitattiin sakkaroosifosfaattisyntaa- sin aktiivisuudella, joka nousi C02 -pitoisuuden myö- tä, mutta ei muuttunut lämpötilan kohotessa. C0 2-pi- toisuuden nousu lisäsi lehtien hiilihydraattipitoisuut- ta, mutta korkeampi lämpötila vähensi etenkin tärk- kelyksen osuutta. Vaikka C 3 -lajit reagoivat hiilidiok- sidiin ja lämpötilaan eri tavoin, C0 2-pitoisuuden nou- su voi lieventää äärilämpötiloista johtuvia epäsuotui- sia reaktioita. 270 AGRICULTURAL AND FOOD SCIENCE IN FINLAND