Journal of Experimental Botany, Vol. 51, No. 90001, pp. 383-389,
February 2000
© 2000 Oxford University Press
Photosynthesis, plant growth and N allocation in transgenic rice plants with decreased Rubisco under CO2 enrichment
1 Graduate School of Agricultural Science, Tohoku University, Tsutsumidori-Amamiyamachi, Sendai 981–8555, Japan
2 Research Institute of Agricultural Resources, Ishikawa Agricultural College, Nonomachi, Ishikawa 921–8836, Japan
3 National Institute of Agrobiological Resources, Tsukuba, Ibaraki 305–8602, Japan
Received 26 March 1999; Accepted 4 August 1999
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Abstract |
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 Top Abstract IntroductionEffects of long-term CO2...Photosynthesis in Rubisco...Growth of Rubisco-antisense...Concluding remarksReferences |
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Ribulose-1,5-bisphosphate carboxylase (Rubisco) efficiency for CO2-saturated photosynthesis was examined in leaves of rice (Oryza sativa L.). The amount of Rubisco in a leaf was calculated to be 30–55% in excess for the light-saturated rate of photosynthesis at 100 Pa CO2. Long-term exposure to CO2 enrichment decreased the amount of Rubisco protein. However, N was not reallocated from decreased Rubisco to other components limiting photosynthesis, and the decrease in Rubisco was simply due to a decrease in total leaf-N content by CO2 enrichment. Thus, rice plants did not optimize N allocation into Rubisco at elevated CO2. Transgenic rice plants with decreased Rubisco were obtained by transformation with the rbcS antisense gene. The transformant with 65% wild-type Rubisco was selected as a plant with optimal Rubisco content for CO2-saturated photosynthesis at the level of a single leaf. This selected transgenic plant had 20% lower rates of photosynthesis at normal CO2 (36 Pa), but 5–15% higher rates of photosynthesis at elevated CO2 (100 Pa) for a given leaf N content. However, such transgenic plants did not necessarily show greater production of biomass even under conditions of CO2enrichment. Although they had a higher N-use efficiency for plant growth under such conditions during the middle stage of growth, the growth rate was lower during the early stage of growth. Thus, improvement of N-use efficiency by a single leaf did not necessarily lead to greater production of biomass by the whole plant.
Key words: Elevated CO2, nitrogen, Oryza sativa L., photosynthesis, Rubisco
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Introduction |
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TopAbstractIntroductionEffects of long-term CO2...Photosynthesis in Rubisco...Growth of Rubisco-antisense...Concluding remarksReferences |
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Rubisco is the key enzyme of photosynthesis and the most abundant leaf protein. Rubisco content is thought to be a rate-limiting factor for the light-saturated rate of photosynthesis at present atmospheric CO2 pressures (Makino et al., 1985). Therefore, large amounts of leaf N are allocated into Rubisco protein, accounting for 15–35% of total leaf N in C3 higher plants (Evans, 1989).
However, Rubisco does not always limit photosynthesis. For example, under the conditions of CO2 enrichment, photosynthesis is limited by either electron transport capacity (Farquhar et al., 1980) or the availability of Pi in the chloroplast for ATP synthesis (Sharkey, 1985), and Rubisco is substantially down-regulated (Sage, 1990). These findings indicate that the amount of Rubisco protein is clearly excessive under conditions of CO2 enrichment. Therefore, for plants to have a greater N-use efficiency of photosynthesis at elevated CO2, it is necessary to reduce the N allocation into Rubisco. Nevertheless, it has remained uncertain whether plants are potentially able to acclimate to elevated CO2 and reduce Rubisco to optimize the amount per unit of leaf area during long-term exposure to CO2 enrichment.
Genetic engineering using antisense technology has provided model plants with decreased Rubisco protein. Tobacco (Nicotiana tabacum) has been used to demonstrate that Rubisco content can be reduced by the rbcS antisense gene (Rodermel et al. 1988). Subsequently, tobacco with decreased Rubisco was produced (Hudson et al., 1992). In addition, this antisense technique has been applied to the C4 plant Flaveria bidentis (Furbank et al., 1996). These transgenic plants with decreased Rubisco have been used as new experimental systems to evaluate the contribution of Rubisco itself to the control of leaf photosynthesis and plant growth (for reviews, see Stitt and Schulze, 1994; Andrews et al., 1995; Furbank et al., 1997). However, they have seldom been used to investigate the N economy of photosynthesis and plant growth under conditions of CO2 enrichment (Masle et al., 1993). In addition, such antisense transformation has not been undertaken for a major crop.
This study first investigated how CO2 concentration during growth affected photosynthesis and N allocation into Rubisco in non-transgenic rice plants (Nakano et al., 1997). Second, rice plants were obtained with decreased Rubisco as a consequence of transformation with an antisense rbcS gene and examined whether they showed a higher N-use efficiency with respect to leaf photosynthesis at elevated CO2 (Makino et al., 1997c). Third, the growth of such transgenic plants under conditions of CO2 enrichment was observed (Makino et al., 2000).
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Effects of long-term CO2 enrichment on Rubisco content in a leaf |
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TopAbstractIntroductionEffects of long-term CO2...Photosynthesis in Rubisco...Growth of Rubisco-antisense...Concluding remarksReferences |
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Makino et al. (Makino et al., 1997c) first used wild-type (non-transgenic) plants and estimated the amount of Rubisco per unit of leaf area that is excessive for the maximal rate of photosynthesis at saturating CO2 partial pressures. A cultivar of rice (Oryza sativa L. Notohikari) was used, and the plants were grown with different amounts of supplied N. The ratio of light-saturated photosynthesis measured at 100 Pa CO2 to the maximal Rubisco activity was calculated as the Rubisco efficiency at elevated CO2. The maximal activity of Rubisco was estimated from the Rubisco content and its kinetic constants at 25 °C. Since the activity of Rubisco measured in vitro is often lower than that predicted from gas-exchange measurements (Makino et al., 1994; von Caemmerer et al., 1994), the kinetic constants of Rubisco, which had been corrected by the gas-exchange data (for detailed calculation, see Makino et al., 1997c), were used here.
The Rubisco efficiency depended on leaf N content, and was estimated to range from 70% down to 45% with increases of 60–180 mmol m-2 of leaf N content. This change in Rubisco efficiency was due to an increase in Rubisco content relative to other processes limiting photosynthesis with increasing leaf N content (Makino et al., 1994). Thus, Rubisco was calculated to be 30–55% excessive under such conditions of CO2 enrichment.
Non-transgenic plants were grown with different amounts of N under two CO2 partial pressures of 36 and 100 Pa, and the effects on the photosynthetic rate and the amount of Rubisco in the uppermost, fully expanded leaves of 70- to 80-day-old plants were examined (Nakano et al., 1997). The rate of photosynthesis and Rubisco content were appreciably lower in plants grown at 100 Pa CO2 than in those grown at 36 Pa CO2 for all N treatments. Since total leaf N content was also decreased by CO2 enrichment, the relationship between Rubisco and leaf N contents was analysed (Fig. 1
). No differences between the two CO2 treatments were found in the relationship between photosynthesis and total leaf N nor in the relationship between Rubisco and total leaf N. These results indicate that decreases in the photosynthetic rate and Rubisco content by CO2 enrichment are simply due to a decrease in total leaf N content.
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Photosynthesis at elevated CO2 is limited by electron transport capacity (Farquhar et al., 1980) or the regeneration of Pi during starch and sucrose synthesis (Sharkey, 1985). Therefore, if plants are potentially able to acclimate to elevated CO2, N from Rubisco, the most abundant leaf protein, should be reallocated into electron transport components and/or key enzymes of starch and sucrose synthesis during long-term growth under CO2 enrichment. Contrary to this expectation, the results in Fig. 1 suggested that CO2 enrichment does not affect N allocation into Rubisco. However, many studies have shown that a decrease in Rubisco content by CO2 enrichment is greater than that of other components such as electron transport components (Nie et al., 1995; Theobald et al., 1998), soluble protein (Rogers et al., 1996; Ghannoum et al., 1997) or total leaf N (Sage et al., 1989; Rowland-Bamford et al., 1991; Osborne et al., 1998; Sims et al., 1998). Although these findings suggest that a selective decrease in Rubisco occurs in the elevated-CO2–grown plants, this remains uncertain. Since the decrease in Rubisco by CO2 enrichment is always associated with a decrease in leaf N content, such a phenomenon makes it difficult to evaluate real changes in N allocation to Rubisco and other components of photosynthesis. With decreasing leaf N content, N allocation to Rubisco generally decreases relative to allocation to other components of photosynthesis, irrespective of CO2 during growth (Evans and Terashima, 1988; Makino et al., 1994). Actually, in the results for rice, a relative decrease in Rubisco compared to chlorophyll, cytochrome f or sucrose-phosphate synthase activity was also found in the elevated CO2-grown plants, but there was no difference between the CO2 treatments for any of the components or activities at a given leaf N content (Nakano et al., 1997). Thus, an apparently selective decrease in Rubisco was not the direct result of CO2 enrichment, but rather the result of a decrease in leaf N content induced by CO2 enrichment. Similar results have been reported recently with wheat (Theobald et al., 1998). Thus, although CO2 enrichment leads to a decrease in Rubisco, this does not indicate an optimization of N allocation at elevated CO2. Therefore, there was interest in whether transgenic rice plants with decreased amounts of Rubisco by ‘antisense’ rbcS show a higher N-use efficiency of photosynthesis under conditions of CO2 enrichment.
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Photosynthesis in Rubisco-antisense plants with decreased Rubisco content at elevated CO2 |
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TopAbstractIntroductionEffects of long-term CO2...Photosynthesis in Rubisco...Growth of Rubisco-antisense...Concluding remarksReferences |
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To obtain transgenic plants with optimal Rubisco content at elevated CO2, it was necessary to determine to what degree Rubisco protein should be reduced. Since Rubisco efficiency at elevated CO2 ranged from 70% down to 45% with increases of 60–180 mmol m-2 of leaf N content, an attempt was made to construct a transformant with 60–70% wild-type Rubisco as an ‘ideal’ transgenic plant (Makino et al., 1997c).
The same cultivar, Notohikari, was used, and transgenic plants with decreased Rubisco were obtained by transformation with the rice rbcS antisense gene under the control of the rice rbcS promoter (Makino et al., 1997c). The antisense gene was introduced by particle bombardment (Shimada et al., 1995). Twenty-three transformants were obtained, and screened for the Rubisco to leaf N ratio in their uppermost, fully expanded leaves. For several transformants, the Rubisco to leaf N ratio was reduced by up to 30%, compared with the wild type. Among them, a transformant with 65% wild-type Rubisco (AS-77) was selected as a target antisense plant. In addition, a transformant with 40% wild-type Rubisco (AS-71) was chosen as another control. This transformant had the lowest Rubisco content among the fertile transformants. Both transformants were allowed to self-fertilize, and the seeds were obtained. The segregation of the Rubisco content of the R1 population from both transformants was about 3 : 1: one group had a Rubisco content similar to that of each primary transformant and the other was similar to the wild type. The respective R1 plants with decreased Rubisco were grown hydroponically at a PPFD of 1000 µmol quanta m-2 s-1, a day/night temperature of 25/20 °C, and three N concentrations, i.e. 0.5, 2.0 and 8.0 mM N. Assays were carried out on the uppermost, fully expanded leaves of about 3-month-old plants.
A positive correlation between Rubisco content and leaf N content was also found for both R1 antisense plants, and Rubisco contents of the respective antisense plants were 65% and 40% of that in the wild-type plants at the same leaf N content, irrespective of N treatment. Gas exchange characteristics were examined at normal CO2 (36 Pa) and elevated CO2 (100 Pa) in the leaves of these three genotypes (Fig. 2). At 36 Pa CO2, the photosynthetic rates in both antisense plants were lower than that in the wild-type plants. At 100 Pa, however, the antisense plants with 65% wild-type Rubisco (AS-77) showed 5–15% higher rates of photosynthesis than the wild-type plants for the same leaf N content. This increase in photosynthesis in the antisense plant AS-77 was accompanied by a 5–15% greater content of chlorophyll, cytochrome f and coupling factor 1 at the same leaf N content (Makino et al., 1997c). In addition, these incremental ratios exactly corresponded to the ratio of decreased fraction of leaf N present as Rubisco. This means that non-specific reallocation of N from decreased Rubisco occurred. Since a decrease in Rubisco content by antisense rbcS led to increases in the amounts of thylakoid components, N may have been optimally distributed between Rubisco and its components limiting CO2-saturated photosynthesis. Therefore, the selected antisense plants had higher rates of CO2-saturated photosynthesis for a given leaf N content. This reallocation of N from Rubisco was clearer in other antisense plants with greatly decreased Rubisco (AS-71). These plants had more thylakoid components compared with the selected antisense plants. However, such antisense plants never had higher rates of photosynthesis, even under CO2 enrichment (Fig. 2). This is because N was not optimally distributed. Thus, it was concluded that rice plants with optimal Rubisco content at elevated CO2 show a higher N-use efficiency of photosynthesis under CO2 enrichment.
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) and the R1 progeny of primary transformants AS-77 (
) and AS-71 (
). All plants were grown hydroponically with different N levels. Measurements were made at a PPFD of 1800 µmol quanta m-2 s-1, a leaf temperature of 25 °C and a leaf-to-air vapour pressure difference of 1.0–1.2 kPa. Some data are taken from Makino et al. (In the studies with tobacco plants, a decrease in Rubisco by antisense ‘rbcS’ had little effect on chlorophyll content or other components of photosynthesis (Andrews et al., 1995; Stitt and Schulze, 1994), and, therefore, it is not clear whether N reallocation from Rubisco to other components occurred. Indeed, decrease in Rubisco never led to higher rates of photosynthesis under conditions of CO2 enrichment (Quick et al., 1991; Masle et al., 1993; von Caemmerer et al., 1994). This difference may be due to a species-dependent difference between rice and tobacco in N allocation in a leaf. Since rice plants have genetically greater Rubisco content per unit of leaf N than tobacco plants (cf. Evans et al., 1994), the effect on reallocation of N may have been greater in rice. In addition, rice plants do not accumulate nitrate in their leaves (Makino et al., 1997b). In fact, the nitrate pool was less than 1% of total leaf N in the wild type or in the antisense plants (Makino et al., 1997c). By contrast, the nitrate pool in tobacco is very big and that in the antisense plants was greater than the decrease in N allocated to Rubisco (Fichtner et al., 1993; Masle et al., 1993). Thus, genetic manipulation of Rubisco in rice may have directly affected N allocation to other components of photosynthesis, whereas in tobacco it was almost compensated for by an increase in nitrate.
Since these results showed that the selected antisense plants have a higher N-use efficiency at the level of a single leaf, attention was directed to whether such transgenic plants grow more adaptively in elevated-CO2 environments. High yields of rice strongly depend on a large input of N fertilizer. Therefore, improvements in N-use efficiency are essential for increasing yields while reducing the input of N fertilizer. Our final purpose was to develop rice plants that perform better in future elevated-CO2 environments.
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Growth of Rubisco-antisense plants with decreased Rubisco content under CO2 enrichment |
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TopAbstractIntroductionEffects of long-term CO2...Photosynthesis in Rubisco...Growth of Rubisco-antisense...Concluding remarksReferences |
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Analyses were carried out on the R2 progeny of the antisense plants AS-77 and AS-71 (Makino et al., 2000). To analyse the growth of the whole plant, the segregants which had Rubisco content similar to that of each primary transformant were selected first. The selected plants were grown hydroponically in a growth chamber equipped with a CO2 partial pressure controller. The chamber was maintained with a 14 h photoperiod, 25/20 °C day/night temperature, and a PPFD of 1000 µmol quanta m-2 s-1 during the day. After germination, the seedlings during the first 21 d were grown with only tap water, and then transplanted to 3.5 l pots containing nutrient solution (4 plants per pot). Plants were sampled on days 21, 42 and 70 after germination. After germination two CO2 treatments were imposed, 36 and 100 Pa. The basal nutrient solution was as described previously (Makino et al., 1985). The solution was renewed once a week, and concentration increased from one-eighth to 2-fold strength as the plants grew.
The total biomass of the three genotypes at final harvest is shown in Fig. 3. When the plants were grown in 36 Pa CO2, the wild-type plant was the largest and the antisense plant AS-71, which had the lowest Rubisco content, was smallest. Thus, the biomass production at 36 Pa CO2 was correlated with Rubisco content per unit of leaf area. The shoot/root ratio was higher in the antisense plants, and this was due to the predominant decrease in the biomass of the roots. The RGR, which had been estimated as the dry weight increment per dry weight per day, was also smaller in the antisense plants than in the wild-type plants (Makino et al., 2000). This was mainly caused by decreased NAR (Fig. 5). However, the LAR was greater in the antisense plants. Although species with a small RGR generally have a decreased LAR, the increased LAR in the antisense plants may be one of the compensation phenomena for decreased photosynthesis by the Rubisco-antisense effect. Similar responses were observed in tobacco antisense plants with decreased Rubisco (Stitt and Schulze, 1994). On the other hand, when the plants were grown in 100 Pa CO2, there was no significant difference in total biomass between the antisense plant AS-77 and the wild-type plant (Fig. 3). The shoot/root ratio was also similar. Although the CO2 sensitivity of the biomass was much greater in the antisense plants than in the wild-type plants, this means that the antisense plants selected do not necessarily perform better in elevated-CO2 environments. Growth analysis indicated that the RGR during the early stage of the growth between days 21 and 42 was smaller in the antisense plant AS-77 than in the wild-type plant (Fig. 4). The reason for this is not known, but this decreased RGR was associated with a decrease in the NAR during this period (Makino et al., 2000). In addition, the amount of N uptake during this period was also smaller in the antisense plants. By contrast, the RGR between days 42 and 70 was greater in both antisense plants than in the wild-type plant. The NAR tended to be slightly enhanced in the antisense plant AS-77 (Fig. 5). The amount of N uptake was not different among the three genotypes.
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Finally, N-use efficiency for plant growth was examined in these three genotypes. It was calculated by dividing the NAR by the average leaf N content per total leaf area in all leaves during the growth analysis period (Fig. 5). For growth at 36 Pa CO2, both NAR and N-use efficiency were smaller in the antisense plants. This may have been caused by decreased Rubisco content per unit of leaf area. For growth at 100 Pa CO2, N-use efficiency in the antisense plant AS-77 was significantly higher than that in the wild-type plant, because the NAR tended to be a little greater in the antisense plant AS-77 and because its leaf N content was slightly smaller. Thus, it was concluded that a higher N-use efficiency of a single leaf does not necessarily lead to greater production of biomass, but can enhance N-use efficiency of the whole plant.
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Concluding remarks |
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TopAbstractIntroductionEffects of long-term CO2...Photosynthesis in Rubisco...Growth of Rubisco-antisense...Concluding remarksReferences |
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CO2 enrichment leads to a decrease in Rubisco content in rice leaves, but this does not mean an optimization of N allocation at elevated CO2. This decrease in Rubisco is simply due to a decrease in leaf N content by CO2 enrichment. Rubisco content in a leaf can be altered by the antisense technology, and the transgenic plants with 65% wild-type Rubisco content at elevated CO2 have a higher N-use efficiency for leaf photosynthesis and plant growth under conditions of CO2 enrichment. However, such an improvement does not necessarily lead to greater production of biomass. Although the reason for this is not known, it is felt that there is a limit to improvement which can be achieved by changes of leaf biochemistry. It is considered that the physiological implications of the decrease in leaf N content induced by CO2 enrichment are of crucial importance for plant growth under CO2 enrichment. This decrease in leaf N content is not due to dilution of N caused by relative increases in leaf area or plant mass. It was found that the decrease in leaf N content is the result of a change in N allocation of the whole plant (Makino et al., 1997a). During long-term growth under conditions of elevated CO2, rice plants reallocated N away from leaf blades to leaf sheaths and roots. This means that plants regulate photosynthesis by changing N allocation within the whole plant. Such responses may also be important for plants as an adaptation strategy in elevated-CO2 environments.
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Acknowledgements |
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We wish to thank Professors K Shimamoto and M Matsuoka for the supply of the rice rbcS promoter and the rice rbcS cDNA, respectively, and for their advice and invaluable comments on the production of transgenic plants. We also thank M Harada for assistance in the growth analysis. This work was supported by funds from the Science and Technology Agency, Japan to NIAR for the Special Coordination Fund for Promoting Science and Technology, Enhancement of Center-of-Excellence, by funds from the Ministry of Agriculture, Forestry and Fisheries, Japan for the Bio Design Program (BDP-99-I-1–2), and by funds from the Japan Society for the Promotion of Science for the Research for the Future (JSPS-RFTF 96L00604).
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Footnotes |
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4 To whom correspondence should be addressed. Fax: +81 22 717 8765. E-mail:makino{at}biochem.tohoku.ac.jp
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Abbreviations |
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LAR, leaf area ratio; NAR, net assimilation rate; PPFD, photosynthetic photon flux density; RGR, relative growth rate; Rubisco, ribulose-1,5-bisphosphate carboxylase.
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References |
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TopAbstractIntroductionEffects of long-term CO2...Photosynthesis in Rubisco...Growth of Rubisco-antisense...Concluding remarksReferences |
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