Journal of Experimental Botany, Vol. 51, No. 351, pp. 1687-1694,
October 2000
© 2000 Oxford University Press
Original Papers |
Rubisco activation state decreases with increasing nitrogen content in apple leaves
Department of Horticulture, Oregon State University, Corvallis, OR 97331, USA
Received 29 February 2000; Accepted 20 May 2000
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionAppendixReferences |
|---|
Based on the curvilinear relationship between leaf nitrogen content and the initial slope of the response of CO2 assimilation (A) to intercellular CO2 concentrations (Ci) in apple, it is hypothesized that Rubisco activation state decreases with increasing leaf N content and this decreased activation state accounts for the curvilinear relationship between leaf N and CO2 assimilation. A range of leaf N content (1.0–5.0 g m-2) was achieved by fertilizing bench-grafted Fuji/M.26 apple (Malus domestica Borkh.) trees for 45 d with different N concentrations, using a modified Hoagland's solution. Analysis of A/Ci curves under saturating light indicated that CO2 assimilation at ambient CO2 fell within the Rubisco limitation region of the A/Ci curves, regardless of leaf N status. Initial Rubisco activity showed a curvilinear response to leaf N. In contrast, total Rubisco activity increased linearly with increasing leaf N throughout the leaf N range. As a result, Rubisco activation state decreased with increasing leaf N. Both light-saturated CO2 assimilation at ambient CO2 and the initial slope of the A/Ci curves were linearly related to initial Rubisco activity, but curvilinearly related to total Rubisco activity. The curvatures in the relationships of both light-saturated CO2 assimilation at ambient CO2 and the initial slope of the A/Ci curves with total Rubisco activity were more pronounced than in their relationships with leaf N. This was because the ratio of total Rubisco activity to leaf N increased with increasing leaf N. As leaf N increased, photosynthetic N use efficiency declined with decreasing Rubisco activation state.
Key words: Apple, CO2 assimilation, leaf N content, Malus domestica, Rubisco activation state.
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionAppendixReferences |
|---|
Whenever a sufficiently wide range of leaf N content has been examined, the relationship between leaf N and light-saturated CO2 assimilation is curvilinear (Evans, 1983
, 1989; DeJong and Doyle, 1985; Sinclair and Horie, 1989). This indicates that CO2 assimilation is less limited by nitrogen as leaf N content increases. However, the mechanism that causes the curvature in the relationship between leaf N and CO2 assimilation is not well understood.
Rubisco (ribulose-1,5-bisphosphate carboxylase/oxygenase) content and its total activity increase linearly with leaf N (Evans, 1983, 1986; Sage et al., 1987; Makino et al., 1992, 1994a, b, 1997; Nakano et al., 1997). In wheat (Triticum aestivum; Evans, 1983); and spinach (Spinacia oleracea; Evans and Terashima, 1988), the initial slope of the response of CO2 assimilation (A) to intercellular CO2 concentrations (Ci) was curvilinearly related to total Rubisco activity. This curvature was attributed to CO2 transfer resistance from the intercellular air spaces to the carboxylation sites in chloroplasts. Based on the C3 photosynthesis model (Farquhar et al., 1980), it has been deduced that if the ratio of CO2 transfer conductance to the maximum activity (Vcmax) of Rubisco does not hold constant, a non-linear relationship between Vcmax and the initial slope of the A/Ci curves is expected (von Caemmerer and Evans, 1991; see also the Appendix).
von Caemmerer and Evans found that CO2 transfer conductance increased with increasing N content in wheat leaves (von Caemmerer and Evans, 1991). As leaf N increases, the ratio of CO2 transfer conductance to Rubisco activity may or may not remain constant. However, when Rubisco is fully activated in vivo, a curvilinear relationship between total Rubisco activity and the initial slope of the A/Ci curves does not necessarily translate into a curvilinear relationship between leaf N and the initial slope, if the ratio of Rubisco to leaf N increases with increasing leaf N. In rice (Oryza sativa) leaves, CO2-limited photosynthesis (at Ci=20 Pa) was curvilinearly related to total Rubisco content, but linearly related to leaf N (Makino et al., 1994a). This was because the ratio of total Rubisco to leaf N increased with increasing leaf N. The increased ratio of Rubisco to leaf N compensated for the curvature in the relationship between Rubisco activity and CO2-limited photosynthesis (Makino et al., 1994a). As leaf N increases, the response of the ratio of Rubisco to total leaf N varies among C3 species. This ratio was independent of leaf N content in wheat (Evans, 1983; Makino et al., 1992), but it increased with increasing leaf N content in rice (Makino et al., 1992, 1994a, 1997), spinach (Makino et al., 1992), pea (Pisum sativum; Makino and Osmond, 1991; Makino et al., 1992) and other species (Evans, 1989; Makino et al., 1992).
Rubisco must be activated to catalyse the carboxylation and oxygenation reactions. Activation of Rubisco involves the reversible reaction of a CO2 molecule with a lysine residue within the active site to form a carbamate, followed by the rapid binding of a magnesium ion to create an active ternary structure. This activation process in vivo is regulated by Rubisco activase (Portis, 1990, 1992). If only a proportion of the total Rubisco is activated in vivo in high N leaves, the relationship between leaf N and CO2 assimilation will be curvilinear. Evans and Terashima showed that there was no apparent deactivation of Rubisco in spinach leaves under a high N supply (Evans and Terashima, 1988). In contrast, it was found that Rubisco activation state in wheat leaves decreased as the N supply increased (Mächler et al., 1988). However, plants were grown at a relatively low photon flux density (PFD of 540 µmol m-2 s-1), and CO2 assimilation and leaf N were not measured. In addition, it was shown that Rubisco accounted for almost a constant proportion of the soluble proteins in wheat leaves, but CO2 assimilation remained almost constant with increasing amounts of Rubisco in excess of 3 g m-2 (Lawlor et al., 1987). Their calculations suggested that approximately 50% of the Rubisco protein was not activated in high N leaves under low PFD conditions.
Both light-saturated CO2 assimilation at ambient CO2 and the initial slope of the A/Ci curves showed curvilinear relationships with N content in leaves of apple (Malus domestica Borkh.) plants grown under full sunlight (Cheng and Fuchigami, 2000). The objective of this study is to test the hypothesis that Rubisco activation state decreases with increasing leaf N content, and that this decreased activation state accounts for the curvilinear relationship between leaf N and CO2 assimilation.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionAppendixReferences |
|---|
Plant material
‘Fuji’ apple (Malus domestica Borkh.) trees on M.26 rootstocks were used. Bench-grafting was done in late March, 1996 and each grafted tree was planted immediately into a 3.8 l pot containing a mixture of peat moss, pumice and sandy loam soil (1:2:1 by vol.). The plants were grown in a lathhouse until early June. During this period, beginning from budbreak in early May, they were fertilized every 2 weeks with 10.7 mM N, using Plantex® 20N-10P2O5-20K2O water-soluble fertilizer with micronutrients (Plantex Corporation, Ontario, Canada). When the scion shoots were approximately 15 cm tall, plants were selected for uniformity, and moved to full sunlight. Thereafter, they were fertilised weekly with Plantex® for 3 weeks. Beginning on 30 June, plants were fertilized twice weekly with one of seven N concentrations (0, 2.5, 5.0, 7.5, 10.0, 15.0 or 20.0 mM N from NH4NO3) by applying 300 ml of a complete nutrient solution to each pot. The nutrient solution was modified from Hoagland's solution No. 2 (Hoagland and Arnon, 1950
) so that N was supplied solely from NH4NO3. There were four replications for each N treatment in a completely randomized design. Irrigation was provided from a saucer placed at the bottom of each pot to ensure adequate water supply. After 45 d, recent fully expanded leaves at the same developmental stage across the treatments were selected for gas exchange and Rubisco activity measurements.
Gas exchange measurements
Measurements were made using a CIRAS-1 portable photosynthesis system (PP Systems, Hitchin, Herts., UK). For all measurements, leaf temperature and ambient water vapour pressure were kept at 26.2±1.0 °C, and 1.30±0.15 kPa, respectively. Responses of CO2 assimilation to PFD were measured first to determine the PFD that saturates CO2 assimilation for all the leaves over the range of leaf N content used in this study (1.0–5.0 g m-2). The results were very similar to those reported previously (Cheng and Fuchigami, 2000) and the light saturation point for CO2 assimilation was below 1400 µmol m-2s-1 in leaves with the highest N content (data not shown). A PFD of 1700±40 µmol m-2 s-1, a level well above the light saturation point for all the subsequent measurements, was chosen for the study. Light-saturated CO2 assimilation was measured at an ambient CO2 concentration of 350±2 µmol mol-1. The initial slope of the A/Ci curve was estimated as the slope of the linear regression between intercellular CO2 (Ci) and CO2 assimilation (A), from at least three points measured at Ci below 200 µmol mol-1. Responses of A to Ci were determined in ascending order at air CO2 concentrations of 110, 190, 270, 350, 450, 600, 800, 1000, 1200 or 1500 µmol mol-1, until Ci reached approximately 1000 µmol mol-1. At each concentration, CO2 assimilation and stomatal conductance were first measured at 21% O2, after 10 min for them to reach steady state. The O2 supply was then switched to 2% and measurements were made after re-equilibration.
Rubisco activity measurements
Rubisco extraction and activity measurements were modified from previous methods (Tissue et al., 1993; Sharkey et al., 1991). Briefly, two leaf discs (total of 2 cm2) were taken from each leaf under full sun (PFD of 1700 µmol m-2 s-1) at noon (11.00–12.30 h), cut into small pieces, and placed in an ice-cold test tube with 3 ml extraction buffer [100 mol m-3 Bicine (pH 7.8 at 25 °C), 5 mol m-3 EDTA, 0.75% (w/v) polyethylene glycol (20 000), 14 mol m-3 ß-mercaptoethanol, 1% (v/v) Tween 80, and 1.5% (w/v) insoluble polyvinylpyrrolidone]. The leaf tissue was homogenized for 25–30 s with a Tissuemizer (Tekmar Company, Cincinnati, Ohio, USA) at 18 000 rpm. The extract was then centrifuged at 13000 g for 40 s in an Eppendorf microcentrifuge, and the supernatant was used immediately in the Rubisco activity assay.
Rubisco activity was measured at 25 °C by enzymatically coupling RuBP (ribulose 1,5-bisphosphate) carboxylation to NADH oxidation (Lilley and Walker, 1974). NADH oxidation was monitored at 340 nm in a Shimadzu UV-160 Spectrophotometer (Shimadzu Corp., Kyoto, Japan). For initial Rubisco activity, a 50 µl sample extract was added to a semi-microcuvette containing 900 µl of an assay solution, immediately followed by adding 50 µl 0.5 mol m-3 RuBP, then mixing well. The change of absorbance at 340 nm was monitored for 40 s. For total Rubisco activity, 50 µl of 0.5 mol m-3 RuBP was added 15 min later, after a sample extract was combined with the assay solution to activate all the Rubisco fully. The assay solution for both initial and total activity measurements contained 100 mol m-3 Bicine (pH 8.0 at 25 °C), 25 mol m-3 KHCO3, 20 mol m-3 MgCl2, 3.5 mol m-3 ATP, 5 mol m-3 phosphocreatine, 80 nkat glyceraldehyde-3-phosphate dehydrogenase, 80 nkat 3-phosphoglyceric phosphokinase, 80 nkat creatine phosphokinase, and 0.25 mol m-3 NADH. Rubisco activation state was calculated as the ratio of initial activity to total activity.
Leaf N content
The same leaves used for gas exchange and Rubisco activity measurements were frozen in liquid nitrogen and stored at –80 °C until freeze-dried. Leaf N content was determined by the Kjeldahl procedure (Schuman et al., 1973).
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionAppendixReferences |
|---|
Relationships between leaf N, Rubisco activities and CO2 assimilation
Light-saturated CO2 assimilation at ambient CO2 and the initial slope of the A/Ci curves increased linearly with increasing leaf N at first, then levelled off at a leaf N content of approximately 3 g m-2 (Fig. 1A
, B). Photosynthetic N use efficiency decreased linearly as leaf N increased (Fig. 1C).
|
Initial Rubisco activity showed a curvilinear response to leaf N (Fig. 2A
). Initial activity increased almost linearly with increasing leaf N at first, then began to level off when leaf N exceeded 3 g m-2. In contrast, total Rubisco activity increased linearly throughout the leaf N range (Fig. 2B). As a result, Rubisco activation state decreased with increasing leaf N (Fig. 2C).
|
Both light-saturated CO2 assimilation at ambient CO2 and the initial slope of the A/Ci curves were linearly correlated with initial Rubisco activity (Fig. 3A
, B), but were curvilinearly related to total activity (Fig. 3C, D). The curvatures in the relationships of both light-saturated CO2 assimilation at ambient CO2 and the initial slope of the A/Ci curve with total activity were more pronounced than in their relationships with leaf N. As leaf N increased, the ratio of total activity to leaf N increased (Fig. 4). Photosynthetic N use efficiency decreased as Rubisco activation state decreased (Fig. 5).
|
|
|
Responses of CO2 assimilation to intercellular CO2 concentration at 21% and 2% O2
To determine which process limited light-saturated CO2 assimilation at ambient CO2, A/Ci curves were constructed under both 21% and 2% O2 conditions. Regardless of the leaf N status, light-saturated CO2 assimilation at ambient CO2 fell within the linear region of the A/Ci curves (Fig. 6).
|
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionAppendixReferences |
|---|
Total Rubisco activity increased linearly with increasing leaf N, whereas initial activity showed a curvilinear response. This resulted in decreased Rubisco activation state with increasing N content (Fig. 2
). Both light-saturated CO2 assimilation at ambient CO2 and the initial slope of the A/Ci curves were linearly related to initial Rubisco activity, but curvilinearly related to total activity (Fig. 3). These results are consistent with the hypothesis that Rubisco activation state decreases with increasing leaf N, and this decreased Rubisco activation state accounts for the curvilinear relationship between leaf N and CO2 assimilation.
Decreased Rubisco activation state in response to an increasing N supply was suggested (Lawlor et al., 1987) and demonstrated (Mächler et al., 1988) in wheat leaves. However, because the plants were grown under relatively low PFD (540
550 µmol m-2 s-1) conditions in both experiments, the possibility that deactivation of Rubisco was caused by low electron transport capacity cannot be ruled out. In this experiment, apple plants were grown under full sunlight, and measurements were made at a PFD well above the light saturation point (Cheng and Fuchigami, 2000). It was found that Rubisco activation state decreased with increasing N content in apple leaves. This contrasts with earlier findings (Evans and Terashima, 1988), where no apparent deactivation of Rubisco in spinach was found under a high N supply. Although CO2 transfer conductance was not measured in this experiment, decreased Rubisco activation state with increasing leaf N alone would result in curvilinear relationships between total Rubisco activity and the initial slope of the A/Ci curves, and between leaf N and the initial slope, even if the ratio of CO2 transfer conductance to the effective Vcmax remained constant (see Appendix). The relationship between total Rubisco activity and the initial slope of the A/Ci curves was more curvilinear than that between leaf N and the initial slope because the ratio of total Rubisco to leaf N increased with increasing leaf N (Fig. 4).
Rubisco activation state in apple leaves is higher at low rather than high leaf N levels (Fig. 2C). High Rubisco activation state in low N leaves indicates that light-saturated CO2 assimilation at ambient CO2 is limited mainly by the amount of Rubisco present. As total activity increases with increasing leaf N, a lower proportion of the Rubisco is active. The amount of Rubisco apparently does not limit CO2 assimilation of apple leaves under saturating light when the N supply is in excess. However, even in high N leaves, CO2 assimilation at ambient CO2 still fell within the linear region of the A/Ci curve (Fig. 6), which is characteristic of Rubisco limitation based on the C3 photosynthesis model of Farquhar et al. (Farquhar et al., 1980). Either Rubisco activation state limits photosynthesis in high N leaves, or decreased Rubisco activation state reflects a regulatory response to an excess N supply to balance a limitation elsewhere in the photosynthetic system (Sage et al., 1988; Sage, 1990). The nature of the response of Rubisco activation state to leaf N obviously deserves further study.
Regardless of the nature of Rubisco regulation, when Rubisco is not fully activated in vivo, it is the amount of activated Rubisco that determines the rate of CO2 assimilation, rather than the total amount of Rubisco. Both the linear relationship between initial Rubisco activity and the initial slope of the A/Ci curves, and the curvilinear relationship between total Rubisco activity and the initial slope found in this experiment indicate that the initial slope reflects the amount of Rubisco that is active in vivo, not the total amount of Rubisco. The total amount is reflected only if all the Rubisco is active in vivo. In spinach leaves the initial slope of the A/Ci curve was also highly correlated with initial Rubisco activity when the phosphorus supply was altered (Brooks, 1986). When light is the only source of variation, in vitro initial Rubisco activity has been closely correlated with the calculated effective Rubisco activity, which represents the CO2- and RuBP-saturated rates achieved by the active sites of Rubisco (von Caemmerer and Edmondson, 1986). In transgenic tobacco plants with an antisense gene directed against Rubisco activase, CO2 assimilation was determined by the number of carbamylated Rubisco sites, not the total Rubisco content (Mate et al., 1996). When Rubisco is not fully activated in vivo under ambient CO2 and saturating light conditions, the current C3 photosynthesis model must be modified to include the Rubisco activation state factor. If, under saturating light conditions, Rubisco activation state at a CO2 partial pressure below ambient is the same as that under ambient CO2 conditions, the only modification to the current model is to replace Vcmax with the effective Vcmax. This can be estimated from the response of CO2 assimilation to intercellular CO2 concentrations at low CO2 concentrations, based on the kinetic properties of Rubisco.
Decreased Rubisco activation state with increasing leaf N accounts for the curvilinear relationship between leaf N and light-saturated CO2 assimilation in apple. It may also explain why photosynthetic N use efficiency decreases with increasing leaf N. However, the exact mechanism that causes deactivation of Rubisco in high N leaves is unclear. Rubisco activity is regulated by the counteraction of tight binding inhibitors and Rubisco activase that removes these inhibitors (Portis, 1992; Salvucci and Ogren, 1996). There are several tight binding inhibitors, including RuBP, and in some plants, 2-carboxyarabinitol 1-phosphate (CA1P), a naturally occurring nocturnal inhibitor. Recently, some unidentified sugar phosphates were shown to reduce Rubisco activity in the light (Keys et al., 1995; Parry et al., 1997). It appears that CA1P does not play any significant role in the light regulation of Rubisco activity in apple leaves because no difference in total Rubisco activity was detected between measurements made at noon under full sunlight and at night (L Cheng and LH Fuchigami, unpublished data). In addition, Rubisco activities were measured at noon under full sunlight in this experiment when CA1P concentration would have been minimal even if apple leaves had considerable amounts of CA1P at night. Therefore, the observed decrease in Rubisco activation state in relation to leaf N may have nothing to do with leaf CA1P level at night. However, it is not known whether N supply would alter the levels of other tight binding inhibitors. One possibility is that the amount of Rubisco activase may not keep pace with the increase in the amount of Rubisco as leaf N increases, resulting in decreased Rubisco activation state. This does not seem to be the case because a 95% reduction in Rubisco activase activity by antisense inhibition of Rubisco activase gene expression was required before Rubisco deactivation and decreased CO2 assimilation were observed in tobacco transgenic plants (Mate et al., 1996). Since ATP hydrolysis is required for Rubisco activase to remove the inhibitors from Rubisco while ADP inhibits this reaction, the activity of Rubisco activase can be regulated by ATP/ADP ratio in vivo (Portis, 1990). In addition, Rubisco activase may be also subject to redox regulation at least in some species (Zhang and Portis, 1999). Therefore, alteration of Rubisco activation state may occur if N supply affects ATP/ADP ratio and/or redox potential. It was shown that an increased Rubisco activation state was associated with an increased ATP/ADP ratio in transgenic tobacco plants with an antisense gene directed against Rubisco mRNA (Quick et al., 1991). When photosynthesis was limited by triose phosphate utilization in sucrose and starch synthesis, deactivation of Rubisco was also associated with a decreased ATP/ADP ratio (Sharkey, 1990). This ratio was higher in wheat leaves under low rather than high N supplies (Mächler et al., 1988). This may provide a mechanism to explain how Rubisco activation state responds to N content in apple leaves.
The finding that Rubisco activation state decreases with increasing N content in apple leaves under saturating light conditions supports the idea that Rubisco can serve as a storage protein when the N supply is in excess. The notion of Rubisco as a form of storage protein is long-standing, but has been controversial. Considering that Rubisco is so expensive in terms of N investment, it has been argued that N resources would be wasted if Rubisco were present in great excess. This argument is generally valid in most cases. Indeed, Rubisco is fully activated or nearly fully activated at ambient to low CO2 under light-saturating conditions (von Caemmerer and Edmondson, 1986; Evans and Terashima, 1988; Sage et al., 1990, 1993). In addition, the initial slope of the A/Ci curve is linearly correlated with total Rubisco activity (von Caemmerer and Farquhar, 1981; Hudson et al., 1992; von Caemmerer et al., 1994). When curvilinear relationships have been observed between total Rubisco activity and the initial slope of the A/Ci curve, factoring in CO2 transfer resistance has accounted for the apparent deviation from the expected behaviour of Rubisco (Evans, 1983; Evans and Seemann, 1984; Evans and Terashima, 1988; von Caemmerer and Evans, 1991; Makino et al., 1994a). However, under an excess N supply, accumulating surplus Rubisco may benefit plants in terms of N acquisition and reutilization because N is such an important resource for plant growth and development. Especially for plants such as apple, which have very low nitrate concentrations in leaves even under a high nitrate supply (Lee and Titus, 1992), Rubisco apparently serves as a storage protein. Compared with a strict storage protein, an excessive amount of Rubisco in high N leaves may also offer advantages such as slightly higher steady-state CO2 assimilation and higher water use efficiency. This has been seen in comparisons between wild tobacco plants and antisense Rubisco plants (Quick et al., 1991).
In conclusion, Rubisco activation state decreases with increasing N content in apple leaves and Rubisco may serve as a storage protein in leaves with a high N content. The mechanism of deactivation of Rubisco in high N leaves under saturating light conditions deserves further research.
|
Appendix |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionAppendixReferences |
|---|
The initial slope of the A/Ci curve in relation to Rubisco activities
When Rubisco is fully activated in vivo at low CO2 under saturating light, the initial slope of the response of CO2 assimilation (A) to intercellular CO2 concentrations (Ci) is given as (von Caemmerer and Evans, 1991
):
 | (1) |
).
At the photocompensation point of the CO2 partial pressure in the chloroplast, 
*, where photorespiratory CO2 evolution equals the rate of carboxylation,
 | (2) |
 | (3) |
):
 | (4) |
When Rubisco is not fully activated in vivo under saturating light, Vcmax is replaced by the effective Vcmax(V'cmax)
 | (5) |
 | (6) |
 | (7) |
, and rearranging:
 | (8) |
 | (9) |
remains constant as leaf N increases, it is obvious from equations 5, 8, and 9 that deactivation of Rubisco alone will cause curvilinear relationships between Vcmax and the initial slope of the A/Ci curves, and between leaf N and the initial slope of the A/Ci curves.
|
Acknowledgments |
|---|
The authors are grateful to Drs J Lewis and T Sharkey for their help on Rubisco activity measurements and to Priscilla Licht for editorial assistance.
|
Notes |
|---|
1 To whom correspondence should be addressed at Department of Horticulture, 134A Plant Science Building, Cornell University, Ithaca, NY 14853-4203, USA. Fax: +1 607 255 0599. E-mail: LC89{at}Cornell.edu
|
Abbreviations |
|---|
A, CO2 assimilation; Ci, intercellular CO2 concentration; Rubisco, ribulose-1,5-bisphosphate carboxylase/oxygenase; RuBP, ribulose 1,5-bisphosphate; Vcmax, maximum activity of Rubisco.
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionAppendixReferences |
|---|
Brooks A.1986. Effects of phosphorus nutrition on ribulose-1,5-bisphosphate carboxylase activation, photosynthetic quantum yield and amounts of some Calvin-cycle metabolites in spinach leaves. Australian Journal of Plant Physiology 13, 231–237.
Cheng L, Fuchigami LH.2000. CO2 assimilation in relation to nitrogen in apple leaves. Journal of Horticultural Science and Biotechnology 75, 383–387.
DeJong TM, Doyle JF.1985. Seasonal relationships between leaf nitrogen content (photosynthetic capacity) and leaf canopy light exposure in peach (Prunus persica). Plant Cell and Environment 8, 701–706.
Evans JR.1983. Nitrogen and photosynthesis in the flag leaf of wheat (Triticum aestivum L.). Plant Physiology 72, 297–302.
Evans JR.1986. The relationship between carbon-dioxide-limited photosynthetic rate and ribulose-1,5-bisphosphate-carboxylase content in two nuclear-cytoplasm substitution lines of wheat, and the co-ordination of ribulose-bisphosphate-carboxylation and electron-transport capacities. Planta 167, 351–358.[Web of Science]
Evans JR.1989. Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78, 9–19.[Web of Science]
Evans JR, Seemann JR.1984. Differences between wheat genotypes in specific activity of ribulose-1,5-bisphosphate carboxylase and the relationship to photosynthesis. Plant Physiology 74, 759–765.
Evans JR, Terashima I.1988. Photosynthetic characteristics of spinach leaves grown with different nitrogen treatments. Plant Cell Physiology 29, 157–165.
Farquhar GD, von Caemmerer S, Berry JA.1980. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.[Web of Science]
Hoagland DR, Arnon DI.1950. The water-culture method for growing plants without soil. California Agricultural Experiment Station Circular, 347.
Hudson GS, Evans JR, von Caemmerer S, Arvidsson YBC, Andrews TJ.1992. Reduction of ribulose-1,5-bisphosphate carboxylase/oxygenase content by antisense RNA reduces photosynthesis in transgenic tobacco plants. Plant Physiology 98, 294–302.
Keys AJ, Major I, Parry MAJ.1995. Is there another player in the game of Rubisco regulation? Journal of Experimental Botany 46, 1245–1251.[Abstract]
Lawlor DW, Boyle FA, Young AT, Keys AJ, Kendall AC.1987. Nitrate nutrition and temperature effects on wheat: photosynthesis and photorespiration of leaves. Journal of Experimental Botany 38, 393–408.
Lee HJ, Titus JS.1992. Nitrogen accumulation and nitrate reductase activity in MM. 106 apple trees as affected by nitrate supply. Journal of Horticultural Science 67, 273–281.
Lilley RM, Walker DA.1974. An improved spectrophotometric assay of ribulose-bisphosphate carboxylase. Biochimica et Biophysica Acta 358, 226–229.[Medline]
Mächler F, Oberson A, Grub A, Nösberger J.1988. Regulation of photosynthesis in nitrogen-deficient wheat seedlings. Plant Physiology 87, 46–49.
Makino A, Osmond B.1991. Effects of nitrogen nutrition on nitrogen partitioning between chloroplasts and mitochondria in pea and wheat. Plant Physiology 96, 355–362.
Makino A, Sakashita H, Hidema J, Mae T, Ojima K, Osmond B.1992. Distinctive responses of ribulose-1,5-bisphosphate carboxylase and carbonic anhydrase in wheat leaves to nitrogen nutrition and their possible relationships to CO2-transfer resistance. Plant Physiology 100, 1737–1743.
Makino A, Nakano H, Mae T.1994a. Responses of ribulose-1,5-phosphate carboxylase, cytochrome f, and sucrose synthesis enzymes in rice leaves to leaf nitrogen and their relationships to photosynthesis. Plant Physiology 105, 173–179.[Abstract]
Makino A, Nakano H, Mae T.1994b. Effects of growth temperature on the response of ribulose-1,5-bisphosphate carboxylase, electron transport components and sucrose synthesis enzymes to leaf nitrogen in rice, and their relationships to photosynthesis. Plant Physiology 105, 1231–1238.[Abstract]
Makino A, Sato T, Nakano H, Mae T.1997. Leaf photosynthesis, plant growth and nitrogen allocation in rice under different irradiances. Planta 203, 390–398.[Web of Science]
Mate CJ, von Caemmerer S, Evans JR, Hudson GS, Andrews TJ.1996. The relationship between CO2-assimilation rate, Rubisco carbamylation and Rubisco activase content in activase-deficient transgenic tobacco suggests a simple model of activase action. Planta 198, 604–613.[Web of Science]
Nakano H, Makino A, Mae T.1997. The effect of elevated partial pressure of CO2 on the relationship between photosynthetic capacity and N content in rice leaves. Plant Physiology 115, 191–198.[Abstract]
Parry MAJ, Andralojc PJ, Parmar S, Keys AJ, Habash D, Paul MJ, Alred R, Quick WP, Servaites JC.1997. Regulation of Rubisco by inhibitors in the light. Plant, Cell and Environment 20, 528–534.
Portis Jr AR.1990. Rubisco activase. Biochimica et Biophysica Acta 1015, 15–28.[Medline]
Portis Jr AR.1992. Regulation of ribulose-1,5-bisphosphate carboxylase/oxygenase activity. Annual Review of Plant Physiology and Plant Molecular Biology 43, 415–437.[Web of Science]
Quick WP, Schurr U, Scheibe R, Schulze E-D, Rodermel SR, Bogorad L, Stitt M.1991. Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with ‘antisense’ rbcS. I. Impact on photosynthesis in ambient growth conditions. Planta 183, 542–554.[Web of Science]
Sage RF.1990. A model describing the regulation of ribulose-1,5-bisphosphate carboxylase, electron transport and triose phosphate use in response to light intensity and CO2 in C3 plants. Plant Physiology 94, 1728–1734.
Sage RF, Pearcy RW, Seemann JR.1987. The nitrogen use efficiency of C3 and C4 plants. III. Leaf nitrogen effects on the activity of carboxylating enzymes in Chenopodium album (L.) and Amaranthus retroflexus (L.). Plant Physiology 85, 355–359.
Sage RF, Reid CD, Moore BD, Seemann JR.1993. Long-term kinetics of the light-dependent regulation of ribulose-1,5-bisphosphate carboxylase/oxygenase activity in plants with and without 2-carboxyarabinitol 1-phosphate. Planta 191, 222–230.[Web of Science]
Sage RF, Sharkey TD, Seemann JR.1988. The in vivo response of the ribulose-1,5-bisphosphate carboxylase activation state and the pool sizes of photosynthetic metabolites to elevated CO2 in Phaseolus vulgaris L. Planta 174, 407–416.[Web of Science]
Sage RF, Sharkey TD, Seemann JR.1990. Regulation of ribulose-1,5-bisphosphate carboxylase activity in response to light intensity and CO2 in the C3 annuals Chenopodium album L. and Phaseolus vulgaris L. Plant Physiology 94, 1735–1742.
Salvucci ME, Ogren WL.1996. The mechanism of Rubisco activase: insights from studies of the properties and structure of the enzyme. Photosynthesis Research 47, 1–11.
Schuman GE, Stanley AM, Knudsen D.1973. Automated total nitrogen analysis of soil and plant samples. Proceedings of the Soil Science Society of America 37, 480–481.
Sharkey TD.1990. Feedback limitation of photosynthesis and the physiological role of ribulose bisphosphate carboxylase carbamylation. Botanical Magazine, Tokyo Special Issue 2, 87–105.
Sharkey TD, Savitch LV, Butz ND.1991. Photometric method for routine determination of Kcat and carbamylation of Rubisco. Photosynthesis Research 28, 41–48.
Sinclair TR, Horie T.1989. Leaf nitrogen, photosynthesis and crop radiation use efficiency: a review. Crop Science 29, 90–98.
Tissue DT, Thomas RB, Strain BR.1993. Long-term effects of elevated CO2 and nutrients on photosynthesis and Rubisco in loblolly pine seedlings. Plant, Cell and Environment 16, 859–865.
von Caemmerer S, Edmondson DL.1986. Relationship between steady-state gas exchange, in vivo ribulose bisphosphate carboxylase activity and some carbon reduction cycle intermediates in Raphanus sativus. Australian Journal of Plant Physiology 13, 669–688.[Web of Science]
von Caemmerer S, Evans JR.1991. Determination of the average partial pressure of CO2 in chloroplasts from leaves of several C3 species. Australian Journal of Plant Physiology 18, 287–305.[Web of Science]
von Caemmerer S, Farquhar GD.1981. Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387.[Web of Science]
von Caemmerer S, Evans JR, Hudson GS, Andrews TJ.1994. The kinetics of ribulose-1,5-bisphosphate carboxylase/ oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco. Planta 195, 88–97.[Web of Science]
Zhang N, Portis Jr AR.1999. Mechanism of light regulation of Rubisco: a specific role for the larger Rubisco activase isoform involving reductive activation by thioredoxin-f. Proceedings of National Academy of Sciences, USA 96, 9438–9443.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  H. Eichelmann, E. Talts, V. Oja, E. Padu, and A. Laisk Rubisco in planta kcat is regulated in balance with photosynthetic electron transport J. Exp. Bot., October 1, 2009; 60(14): 4077 - 4088. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. Hu, Z. Wang, and B. Huang Photosynthetic Responses of Bermudagrass to Drought Stress Associated with Stomatal and Metabolic Limitations Crop Sci., August 7, 2009; 49(5): 1902 - 1909. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. D. Jimenez, M. Pardos, J. Puertolas, L. A. Kleczkowski, and J. A. Pardos Deep shade alters the acclimation response to moderate water stress in Quercus suber L. Forestry, July 1, 2009; 82(3): 285 - 298. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Li, Y. Gao, X. Xu, Q. Shen, and S. Guo Light-saturated photosynthetic rate in high-nitrogen rice (Oryza sativa L.) leaves is related to chloroplastic CO2 concentration J. Exp. Bot., May 1, 2009; 60(8): 2351 - 2360. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Xia, L. Cheng, A. Lakso, and M. Goffinet Effects of Nitrogen Supply on Source-sink Balance and Fruit Size of 'Gala' Apple Trees J. Amer. Soc. Hort. Sci., January 1, 2009; 134(1): 126 - 133. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. K. Manter and J. Kerrigan A/Ci curve analysis across a range of woody plant species: influence of regression analysis parameters and mesophyll conductance J. Exp. Bot., December 1, 2004; 55(408): 2581 - 2588. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L.-S. Chen and L. Cheng Both xanthophyll cycle-dependent thermal dissipation and the antioxidant system are up-regulated in grape (Vitis labrusca L. cv. Concord) leaves in response to N limitation J. Exp. Bot., September 1, 2003; 54(390): 2165 - 2175. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Cheng Xanthophyll cycle pool size and composition in relation to the nitrogen content of apple leaves J. Exp. Bot., January 2, 2003; 54(381): 385 - 393. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Cheng, L. H. Fuchigami, and P. J. Breen The relationship between photosystem II efficiency and quantum yield for CO2 assimilation is not affected by nitrogen content in apple leaves J. Exp. Bot., September 1, 2001; 52(362): 1865 - 1872. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||