Abstract
Photosynthetic acclimation varies among species, which likely reveals variations at the biochemical level in the pathways that constitute carbon assimilation and energy transfer. Local adaptation and phenotypic plasticity affect the environmental response of photosynthesis. Phenotypic plasticity allows for a wide array of responses from a single individual, encouraging fitness in a broad variety of environments. Rubisco catalyses the first enzymatic step of photosynthesis, and is thus central to life on Earth. The enzyme is well conserved, but there is habitat-dependent variation in kinetic parameters, indicating that local adaptation may occur. Here, we review evidence suggesting that land plants can adjust Rubisco’s intrinsic biochemical characteristics during acclimation. We show that this plasticity can theoretically improve CO2 assimilation; the effect is non-trivial, but small relative to other acclimation responses. We conclude by discussing possible mechanisms that could account for biochemical plasticity in land plant Rubisco.
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References
Adams P, Nelson DE, Yamada S, Chmara W, Jensen RG, Bohnert HJ, Griffiths H (1998) Growth and development of Mesembryanthemum crystallinum (Aizoaceae). New Phytol 138:171–190
Allakhverdiev S, Kreslavski V, Klimov V, Los D, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541–550
Anderson JM, Chow WS, Goodchild DJ (1988) Thylakoid membrane organization in sun shade acclimation. Aust J Plant Physiol 15:11–26
Andersson I, Backlund A (2008) Structure and function of Rubisco. Plant Physiol Biochem 46:275–291
Andrews TJ (1988) Catalysis by cyanobacterial ribulose-bisphosphate carboxylase large subunits in the complete absence of small subunits. J Biol Chem 263:12213–12219
Badger MR, Collatz GJ (1977) Studies on the kinetic mechanism of ribulose-1.5-biophosphate carboxylase and oxygenase reactions, with particular reference to the effect of temperature on kinetic parameters. Carnegie Inst Wash Yearb 76:355–361
Badger MR, Bjorkman O, Armond PA (1982) An analysis of photosynthetic response and adaptation to temperature in higher-plants–temperature acclimation in the desert evergreen Nerium-oleander l. Plant Cell Environ 5:85–99
Badger MR, Andrews TJ, Whitney SM, Ludwig M, Yellowlees D, Leggat W, Price JD (1998) The diversity and coevolution of Rubisco, plastids, pyrenoids, and chloroplast based CO2 concentrating mechanisms in algae. Can J Bot 76:1052–1071
Berry J, Raison J (1981) Responses of macrophytes to temperature. In: Lange O, Nobel P, Osmond C, Ziegler H (eds) Encyclopedia of plant physiology. Springer-Verlag, Berlin, pp 278–338
Berry JO, Nikolau BJ, Carr JP, Klessig DF (1985) Transcriptional and post-transcriptional regulation of ribulose-1,5-bisphosphate carboxylase gene-expression in light-grown and dark-grown amaranth cotyledons. Mol Cell Biol 5:2238–2246
Berry-Lowe SL, Mcknight TD, Shah DM, Meagher RB (1982) The nucleotide sequence expression and evolution of one member of a multigene family encoding the small subunit of ribulose-1,5-bisphosphate carboxylase in soybean. J Mol Appl Genet 1:483–498
Bird IF, Cornelius MJ, Keys AJ (1982) Affinity of RuBP carboxylases for carbon dioxide and inhibition of the enzymes by oxygen. J Exp Bot 33:1004–1013
Bowes G, Ogren WL, Hageman RH (1971) Phosphoglycolate production catalysed by ribulose 1,5-diphosphate carboxylase. Biochem Biophys Res Commun 45:716–722
Broglie R, Coruzzi G, Lamppa G, Keith B, Chua NH (1983) Structural-analysis of nuclear genes-coding for the precursor to the small subunit of wheat ribulose-1,5-bisphosphate carboxylase. Biotechnology 1:55–61
Cheng SH, Moore BD, Seemann JR (1998) Effects of short- and long-term elevated CO2 on the expression of ribulose-1,5-bisphosphate carboxylase/oxygenase genes and carbohydrate accumulation in leaves of Arabidopsis thaliana (L) heynh. Plant Physiol 116:715–723
Christin P, Salamin N, Muasya A, Roalson E, Russier F, Besnard G (2008) Evolutionary switch and genetic convergence on rbcL following the evolution of C4 photosynthesis. Mol Biol Evol 25:2361–2368
Clausen JC, Keck DD, Hiesey WM (1940) Experimental studies on the nature of species I. Effect of varied environments on western North American plants. Carnegie Institution of Washington Publication 520, Washington, DC
Clausen JC, Keck DD, Hiesey WM (1948) Experimental studies on the nature of species III. Environment responses of climatic races of Achillea. Carnegie Institution of Washington Publication 581, Washington, DC
Cleland WW, Andrews TJ, Gutteridge S, Hartman FC, Lorimer GH (1998) Mechanism of Rubisco: the carbamate as general base. Chem Rev 98:549–562
Crossland LD, Rodermel SR, Bogorad L (1984) Single gene for the large subunit of ribulosebisphosphate carboxylase in maize yields two differentially regulated messenger RNAs. Proc Natl Acad Sci USA 81:4060–4064
Davies B, Griffiths H (2012) Competing carboxylases: circadian and metabolic regulation of Rubisco in C3 and CAM Mesembryanthemum crystallinum L. Plant Cell Environ 35:1211–1220
Dean C, Pichersky E, Dunsmuir P (1989) Structure, evolution, and regulation of rbcS genes in higher plants. Annu Rev Plant Physiol Plant Mol Biol 40:415–439
Dedonder A, Rethy R, Fredericq H, Van Montagu M, Krebbers E (1993) Arabidopsis rbcS genes are differentially regulated by light. Plant Physiol 101:801–808
Delgado E, Medrano H, Keys AJ, MaJ Parry (1995) Species variation in rubisco specificity factor. J Exp Bot 46:1775–1777
Du YC, Peddi SR, Spreitzer RJ (2003) Assessment of structural and functional divergence far from the large subunit active site of ribulose-1,5-bisphosphate carboxylase/oxygenase. J Biol Chem 278:49401–49405
Evans JR (1988) Acclimation by the thylakoid membranes to growth irradiance and the partitioning of nitrogen between soluble and thylakoid proteins. Aust J Plant Physiol 15:93–106
Farquhar GD, Sv Caemmerer, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90
Firn R, Jones C (2009) A Darwinian view of metabolism: molecular properties determine fitness. J Exp Bot 60:719–726
Flood PJ, Harbinson J, Aarts MGM (2011) Natural genetic variation in plant photosynthesis. Trends Plant Sci 16:327–335
Galmes J, Flexas J, Keys AJ, Cifre J, Mitchell R, Madgwick P, Haslem R, Medrano H, MaJ Parry (2005) Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves. Plant Cell Environ 28:571–579
Genkov T, Spreitzer RJ (2009) Highly conserved small subunit residues influence Rubisco large subunit catalysis. J Biol Chem 284:30105–30112
Genkov T, Meyer M, Griffiths H, Spreitzer RJ (2011) Functional hybrid Rubisco enzymes with plant small subunits and algal large subunits engineered rbcs cDNA for expression in chlamydomonas. J Biol Chem 285:19833–19841
Gesch RW, Vu JCV, Boote KJ, Allen LH, Bowes G (2002) Sucrose-phosphate synthase activity in mature rice leaves following changes in growth CO2 is unrelated to sucrose pool size. New Phytol 154:77–84
Gianazza E (1995) Isoelectric focusing as a tool for the investigation of post-translational processing and chemical modifications of proteins. J Chromatogr A 705:67–87
Greenbaum D, Jansen R, Gerstein M (2002) Analysis of mRNA expression and protein abundance data: an approach for the comparison of the enrichment of features in the cellular population of proteins and transcripts. Bioinformatics 18:585–596
Greenbaum D, Colangelo C, Williams K, Gerstein M (2003) Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol 4:117
Gutteridge S (1991) The relative catalytic specificities of the large subunit core of Synechcoccus ribulose bisphosphate carboxylase oxygenase. J Biol Chem 266:7359–7362
Gygi SP, Rochon Y, Franza BR, Aebersold R (1999) Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19:1720–1730
Holaday A, Martindale W, Alred R, Brooks AL, Leegood RC (1992) Changes in activities of enzymes of carbon metabolism in leaves during exposure of plants to low-temperature. Plant Physiol 98:1105–1114
Houtz RL, Portis AR (2003) The life of ribulose 1,5-bisphosphate carboxylase/oxygenase-posttranslational facts and mysteries. Arch Biochem Biophys 414:150–158
Houtz RL, Magnani R, Nayak NR, Dirk LMA (2008) Co- and post-translational modifications in Rubisco: unanswered questions. J Exp Bot 59:1635–1645
Huner NPA, Hayden DB (1982) Changes in the heterogeneity of ribulose bisphosphate carboxylase–oxygenase in winter rye induced by cold hardening. Can J Biochem 60:897–903
Huner NPA, Macdowall FDH (1978) Evidence for an in vivo conformational change in ribulose bisphosphate carboxylase-oxygenase from puma rye during cold adaptation. Can J Biochem 56:1154–1161
Huner NPA, Macdowall FDH (1979) Effects of low-temperature acclimation of winter rye on catalytic properties of its ribulose bisphosphate carboxylase-oxygenase. Can J Biochem 57:1036–1041
Huner N, Oquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230
Hurry VM, Malmberg G, Gardestrom P, Oquist G (1994) Effects of a short-term shift to low-temperature and of long-term cold hardening on photosynthesis and ribulose-1,5-bisphosphate carboxylase oxygenase and sucrose-phosphate synthase activity in leaves of winter rye (Secale cereale). Plant Physiol 106:983–990
Ishikawa C, Hatanaka T, Misoo S, Miyake C, Fukayama H (2011) Functional incorporation of sorghum small subunit increases the catalytic turnover rate of Rubisco in transgenic rice. Plant Physiol 156:1603–1611
Izumi M, Tsunoda H, Suzuki Y, Makino A, Ishida H (2012) RBCS1a and RBCS3b, two major members within the Arabidopsis rbcS multigene family, function to yield sufficient Rubisco content for leaf photosynthetic capacity. J Exp Bot 63:2159–2170
Jansen R, Greenbaum D, Gerstein M (2002) Relating whole-genome expression data with protein–protein interactions. Genome Res 12:37–46
Johnson X, Wostrikoff K, Finazzi G, Kuras R, Schwarz C, Bujaldon S, Nickelsen J, Stern DB, Wollman FA, Vallon O (2010) MRL1, a conserved Pentatricopeptide repeat protein, is required for stabilization of rbcL mRNA in Chlamydomonas and Arabidopsis. Plant Cell 22:234–248
Jordan DB, Ogren WL (1981) Species variation in the specificity of ribulose-bisphosphate carboxylase-oxygenase. Nature 291:513–515
Jordan DB, Ogren WL (1984) The CO2/O2 specificity of ribulose 1,5-bisphosphate carboxylase oxygenase - dependence on ribulosebisphosphate concentration, pH and temperature. Planta 161:308–313
Kapralov MV, Filatov DA (2007) Widespread positive selection in the photosynthetic Rubisco enzyme. BMC Evol Biol 7:73
Kapralov MV, Kubien DS, Andersson I, Filatov DA (2011) Changes in Rubisco kinetics during the evolution of C4 photosynthesis in Flaveria (asteraceae) are associated with positive selection on genes encoding the enzyme. Mol Biol Evol 28:1491–1503
Karkehabadi S, Taylor TC, Spreitzer RJ, Andersson I (2005) Altered intersubunit interactions in crystal structures of catalytically compromised ribulose-1,5-bisphosphate carboxylase/oxygenase. Biochemistry 44:113–120
Khrebtukova I, Spreitzer RJ (1996) Elimination of the chlamydomonas gene family that encodes the small subunit of ribulose-1,5-bisphosphate carboxylase oxygenase. Proc Natl Acad Sci USA 93:13689–13693
Knight S, Andersson I, Branden C-I (1990) Crystallographic analysis of ribulose 1,5-bisphosphate carboxylase from spinach at 2.4 A resolution: subunit interactions and active site. J Mol Biol 215:113–160
Krebbers E, Seurinck J, Herdies L, Cashmore AR, Timko MP (1988) Four genes in two diverged subfamilies encode the ribulose-1,5-bisphosphate carboxylase small subunit polypeptide of Arabidopsis thaliana. Plant Mol Biol 11:745–759
Ku S-B, Edwards GE (1977) Oxygen inhibition of photosynthesis: i. Temperature dependence and relation to O2/CO2 solubility ratio. Plant Physiol 59:986–990
Kubien DS, Sage RF (2004) Low-temperature photosynthetic performance of a C4 grass and a co-occurring C3 grass native to high latitudes. Plant Cell Environ 27:907–916
Kubien DS, Sage RF (2008) The temperature response of photosynthesis in tobacco with reduced amounts of Rubisco. Plant Cell Environ 31:407–418
Kubien DS, Whitney SM, Moore PV, Jesson LK (2008) The biochemistry of Rubisco in Flaveria. J Exp Bot 59:1767–1777
Laing WA, Ogren WL, Hageman RH (1974) Regulation of soybean net photosynthesis CO2 fixation by interaction of CO2, O2, and Ribulose 1,5-diphosphate carboxylase. Plant Physiol 54:678–685
Langridge P (1981) Synthesis of the large subunit of spinach ribulose bisphosphate carboxylase may involve a precursor polypeptide. FEBS Lett 123:85–89
Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J Exp Bot 60:2859–2876
Mehrotra S, Trivedi PK, Sethuraman A, Mehrotra R (2011) The rbcL gene of Populus deltoides has multiple transcripts and is redox-regulated in vitro. J Plant Physiol 168:466–473
Mitchell RaC, Keys AJ, Madgwick PJ, MaJ Parry, Lawlor DW (2005) Adaptation of photosynthesis in marama bean Tylosema esculentum (burchell a. Schreiber) to a high temperature, high radiation, drought-prone environment. Plant Physiol Biochem 43:969–976
Monson RK, Stidham MA, Williams GJ, Edwards GE, Uribe EG (1982) Temperature dependence of photosynthesis in Agropyron smithii Rydb. I. Factors affecting net CO2 uptake in intact leaves and contribution from Ribulose-1,5-bisphosphate carboxylase measured in vivo and in vitro. Plant Physiol 69:921–928
Moore BD, Cheng SH, Rice J, Seemann JR (1998) Sucrose cycling, Rubisco expression, and prediction of photosynthetic acclimation to elevated atmospheric CO2. Plant Cell Environ 21:905–915
Moore BD, Cheng SH, Sims D, Seemann JR (1999) The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2. Plant Cell Environ 22:567–582
Morell MK, Wilkin JM, Kane HJ, Andrews TJ (1997) Side reactions catalyzed by ribulose-bisphosphate carboxylase in the presence and absence of small subunits. J Biol Chem 272:5445–5451
Mueller-Cajar O, Whitney SM (2008) Directing the evolution of Rubisco and Rubisco activase: first impressions of a new tool for photosynthesis research. Photosynth Res 98:667–675
Mullet JE, Orozco EM, Chua NH (1985) Multiple transcripts for higher-plant rbcL and atpb genes and localization of the transcription initiation site of the rbcL gene. Plant Mol Biol 4:39–54
Palmer JD, Edwards H, Jorgensen RA, Thompson WF (1982) Novel evolutionary variation in transcription and location of 2 chloroplast genes. Nucleic Acids Res 10:6819–6832
Paul K, Yeoh HH (1988) Characteristics of ribulose 1,5-bisphosphate carboxylase from cassava leaves. Plant Physiol Biochem 26:615–618
Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209:2361–2367
Poulsen C (1984) 2 messenger-RNA species differing by 258-nucleotides at the 5′ end are formed from the barley chloroplast rbcL gene. Carlsberg Res Commun 49:89–104
Read BA, Tabita FR (1992a) Amino-acid substitutions in the small subunit of ribulose-1,5-bisphosphate carboxylase oxygenase that influence catalytic activity of the holoenzyme. Biochemistry 31:519–525
Read BA, Tabita FR (1992b) A hybrid ribulosebisphosphate carboxylase oxygenase enzyme exhibiting a substantial increase in substrate specificity factor. Biochemistry 31:5553–5560
Rodermel S, Haley J, Jiang CZ, Tsai CH, Bogorad L (1996) A mechanism for intergenomic integration: abundance of ribulose bisphosphate carboxylase small-subunit protein influences the translation of the large-subunit mRNA. Proc Natl Acad Sci USA 93:3881–3885
Sage RF (2002) Variation in the k cat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature. J Exp Bot 53:609–620
Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant Cell Environ 30:1086–1106
Sage RF, Way DA, Kubien DS (2008) Rubisco, Rubisco activase, and global climate change. J Exp Bot 59:1581–1595
Salvucci ME, Crafts-Brandner SJ (2004a) Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiol Plan 120:179–186
Salvucci ME, Crafts-Brandner SJ (2004b) Mechanism for deactivation of Rubisco under moderate heat stress. Physiol Plan 122:513–519
Sasanuma T (2001) Characterization of the rbcs multigene family in wheat: subfamily classification, determination of chromosomal location and evolutionary analysis. Mol Genet Genom 265:161–171
Savir Y, Noor E, Milo R, Tlusty T (2010) Cross-species analysis traces adaptation of Rubisco toward optimality in a low-dimensional landscape. Proc Natl Acad Sci USA 107:3475–3480
Schlichting CD (1986) The evolution of phenotypic plasticity in plants. Annu Rev Ecol Syst 17:667–693
Schlichting C (2002) Phenotypic plasticity in plants. Plant Spec Biol 17:85–88
Schlichting C, Pigliucci M (1993) Control of phenotypic plasticity via regulatory genes. Am Nat 142:366–370
Schlichting CD, Pigliucci M (1995) Gene-regulation, quantitative genetics and the evolution of reaction norms. Evol Ecol 9:154–168
Sharkey TD (1985) Photosynthesis in intact leaves of C3 plants - physics, physiology and rate limitations. Bot Rev 51:53–105
Sharwood RE, von Caemmerer S, Maliga P, Whitney SM (2008) The catalytic properties of hybrid Rubisco comprising tobacco small and sunflower large subunits mirror the kinetically equivalent source Rubiscos and can support tobacco growth. Plant Physiol 146:83–96
Slatyer RO (1977) Altitudinal variation in photosynthetic characteristics of snow gum, eucalyptus pauciflora sieb ex spreng.IV Temperature response of four populations grown at different temperatures. Aust J Plant Physiol 4:583–594
Spreitzer RJ (2003) Role of the small subunit in ribulose-1,5-biphosphate carboxylase/oxygenase. Arch Biochem Biophys 414:141–149
Spreitzer RJ, Esquivel MG, Du YC, Mclaughlin PD (2001) Alanine-scanning mutagenesis of the small-subunit beta a-beta b loop of chloroplast ribulose-1,5-bisphosphate carboxylase/oxygenase: substitution at arg-71 affects thermal stability and CO2/O2 specificity. Biochemistry 40:5615–5621
Spreitzer RJ, Peddi SR, Satagopan S (2005) Phylogenetic engineering at an interface between large and small subunits imparts land-plant kinetic properties to algal Rubisco. Proc Natl Acad Sci USA 102:17225–17230
Strand A, Hurry V, Henkes S, Huner N, Gustafsson P, Gardestrom P, Stitt M (1999) Acclimation of Arabidopsis leaves developing at low temperatures. Increasing cytoplasmic volume accompanies increased activities of enzymes in the calvin cycle and in the sucrose-biosynthesis pathway. Plant Physiol 119:1387–1397
Suzuki Y, Makino A (2012) Availability of Rubisco small subunit up-regulates the transcript levels of large subunit for stoichiometric assembly of its holoenzyme in rice. Plant Physiol 160:533–540
Tallman G, Zhu JX, Mawson BT, Amodeo G, Nouhi Z, Levy K, Zeiger E (1997) Induction of CAM in Mesembryanthemum crystallinum abolishes the stomatal response to blue light and light-dependent zeaxanthin formation in guard cell chloroplasts. Plant Cell Physiol 38:236–242
Tcherkez GGB, Farquhar GD, Andrews TJ (2006) Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc Natl Acad Sci USA 103:7246–7251
von Caemmerer S (2000) Biochemical models of leaf photosynthesis. CSIRO Publishing, Collingwood
von Caemmerer S, Quick WP (2000) Rubisco: physiology in vivo. In: Leegood RC, Sharkey TD, von Caemmerer S (eds) Photosynthesis: advances in photosynthesis and respiration, vol 9. Springer, Dordrecht, pp 85–113
Vu JCV, Allen LH, Boote KJ, Bowes G (1997) Effects of elevated CO2 and temperature on photosynthesis and Rubisco in rice and soybean. Plant Cell Environ 20:68–76
Vu JCV, Newman YC, Allen LH, Gallo-Meagher M, Zhang MQ (2002) Photosynthetic acclimation of young sweet orange trees to elevated growth CO2 and temperature. J Plant Physiol 159:147–157
Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150:563–565
Wang D, Naidu SL, Portis AR, Moose SP, Long SP (2008) Can the cold tolerance of C4 photosynthesis in Miscanthusxgiganteus relative to zea mays be explained by differences in activities and thermal properties of Rubisco? J Exp Bot 59:1779–1787
Wanner LA, Gruissem W (1991) Expression dynamics of the tomato rbcS gene family during development. Plant Cell 3:1289–1303
Warren CR, Dreyer E (2006) Temperature response of photosynthesis and internal conductance to CO2: results from two independent approaches. J Exp Bot 57:3057–3067
Wasmann CC, Ramage RT, Bohnert HJ, Ostrem JA (1989) Identification of an assembly domain in the small subunit of ribulose-1,5-bisphosphate carboxylase. Proc Natl Acad Sci USA 86:1198–1202
Whitney SM, Sharwood RE, Orr D, White SJ, Alonso H, Galmes J (2011) Isoleucine 309 acts as a C4 catalytic switch that increases ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) carboxylation rate in Flaveria. Proc Natl Acad Sci USA 108:14688–14693
Yamori W, Noguchi K, Terashima I (2005) Temperature acclimation of photosynthesis in spinach leaves: analyses of photosynthetic components and temperature dependencies of photosynthetic partial reactions. Plant Cell Environ 28:536–547
Yamori W, Noguchi K, Hanba YT, Terashima I (2006a) Effects of internal conductance on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. Plant Cell Physiol 47:1069–1080
Yamori W, Suzuki K, Noguchi K, Nakai M, Terashima I (2006b) Effects of Rubisco kinetics and Rubisco activation state on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. Plant Cell Environ 29:1659–1670
Yeoh HH, Badger MR, Watson L (1981) Variations in kinetic-properties of ribulose-1,5-bisphosphate carboxylases among plants. Plant Physiol 67:1151–1155
Yoon M, Putterill JJ, Ross GS, Laing WA (2001) Determination of the relative expression levels of rubisco small subunit genes in arabidopsis by rapid amplification of cDNA ends. Anal Biochem 291:237–244
Zhang X-H, Webb J, Huang Y-H, Lin L, Tang R-S, Liu A (2011) Hybrid Rubisco of tomato large subunits and tobacco small subunits is functional in tobacco plants. Plant Sci 180:480–488
Acknowledgments
The authors wish to thank two anonymous reviewers for helpful suggestions on a previous version of this manuscript. This work was supported by a National Science and Engineering Research Council of Canada (NSERC) PGS-D scholarship to APC, and a Discovery Grant (327103-2008) to DSK.
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Appendix
The modelling in Fig. 1 reflects the acclimation of Rubisco S c/o reported by Yamori et al. (2006b). The ratio of the two reaction efficiencies describes the relative CO2/O2 specificity of Rubisco (S c/o):
where \( k_{{{\text{cat}} - {\text{CO}}_{ 2} }} \) and \( k_{{{\text{cat-O}}_{ 2} }} \) represent the turnover capacity of carboxylation and oxygenation, respectively, and K c and K o are the Michaelis–Menten constants for CO2 and O2. The photorespiratory CO2 compensation point (Γ*) is:
where pO2 is the partial pressure of O2 in the stroma (21 kPa).
We determined the effect of altered spinach S c/o (Yamori et al. 2006b) on Rubisco-limited A:
where C is the level of CO2; V c is the realized rate of carboxylation; \( V_{{c_{\hbox{max} } }} \) is the maximum rate of carboxylation (\( V_{{c_{\hbox{max} } }} \) = \( k_{{{\text{cat}} - {\text{CO}}_{ 2} }} \) * site concentration * activation state); and R d is the rate of non-photorespiratory mitochondrial respiration in the light. We assumed complete Rubisco activation. To incorporate mesophyll conductance, and hence assess A at stromal CO2 (e.g. C c), we followed the solution of Warren and Dreyer (2006, their equation 6).
We used the cubic equation reported by Yamori et al. (Yamori et al. 2006b, their Fig. 4) to calculate S c/o for HT and LT Rubisco, and assigned this to \( k_{{{\text{cat}} - {\text{CO}}_{ 2} }} \), K c, or K o, by re-arranging Equation 1, keeping the other parameters constant. We assumed that \( k_{{{\text{cat - O}}_{ 2} }} \) = \( k_{{{\text{cat}} - {\text{CO}}_{ 2} }} \)/4 (von Caemmerer 2000, p. 45). The 25 °C values and E a (Table 1) were from Jordan and Ogren (1984), and Kubien et al. (2008). Rubisco site concentration was 20 μmol m−2, giving \( V_{{c_{\hbox{max} } }} \) of 64 μmol m−2 s−1 for the default \( k_{{{\text{cat}} - {\text{CO}}_{ 2} }} \). We also calculated the effect of allowing the different S c/o to affect Γ* only, keeping the other parameters constant for HT and LT leaves.
We calculated the effect of Rubisco plasticity only, at C i (e.g. infinite mesophyll conductance) and at C c, with R d = 0 (e.g. gross A). We then calculated a more general acclimation potential, assigning HT and LT values for Rubisco content and R d (Yamori et al. 2005, their Table 1 and Fig. 2), and g m (Yamori et al. 2006a, their Fig. 1) (Fig. 2). We left the site concentration for LT leaves at 20 μmol m−2; adjusting for the HT/LT Rubisco ratio reported by Yamori et al. (2005) gives an HT content of 10.3 μmol m−2, and thus a \( V_{{c_{\hbox{max} } }} \) of 33 μmol m−2 s−1 at 25 °C.
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Cavanagh, A.P., Kubien, D.S. Can phenotypic plasticity in Rubisco performance contribute to photosynthetic acclimation?. Photosynth Res 119, 203–214 (2014). https://doi.org/10.1007/s11120-013-9816-3
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DOI: https://doi.org/10.1007/s11120-013-9816-3