Photosynthesis Research

, Volume 119, Issue 1–2, pp 203–214 | Cite as

Can phenotypic plasticity in Rubisco performance contribute to photosynthetic acclimation?

  • Amanda P. Cavanagh
  • David S. KubienEmail author


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.


Rubisco Photosynthesis Acclimation rbcL rbcS 



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.


  1. Adams P, Nelson DE, Yamada S, Chmara W, Jensen RG, Bohnert HJ, Griffiths H (1998) Growth and development of Mesembryanthemum crystallinum (Aizoaceae). New Phytol 138:171–190CrossRefGoogle Scholar
  2. Allakhverdiev S, Kreslavski V, Klimov V, Los D, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541–550PubMedCrossRefGoogle Scholar
  3. Anderson JM, Chow WS, Goodchild DJ (1988) Thylakoid membrane organization in sun shade acclimation. Aust J Plant Physiol 15:11–26CrossRefGoogle Scholar
  4. Andersson I, Backlund A (2008) Structure and function of Rubisco. Plant Physiol Biochem 46:275–291PubMedCrossRefGoogle Scholar
  5. Andrews TJ (1988) Catalysis by cyanobacterial ribulose-bisphosphate carboxylase large subunits in the complete absence of small subunits. J Biol Chem 263:12213–12219PubMedGoogle Scholar
  6. 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 76:355–361Google Scholar
  7. 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 5:85–99Google Scholar
  8. 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 76:1052–1071Google Scholar
  9. 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 278–338Google Scholar
  10. 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 5:2238–2246PubMedCentralPubMedGoogle Scholar
  11. 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 1:483–498PubMedGoogle Scholar
  12. Bird IF, Cornelius MJ, Keys AJ (1982) Affinity of RuBP carboxylases for carbon dioxide and inhibition of the enzymes by oxygen. J Exp Bot 33:1004–1013CrossRefGoogle Scholar
  13. Bowes G, Ogren WL, Hageman RH (1971) Phosphoglycolate production catalysed by ribulose 1,5-diphosphate carboxylase. Biochem Biophys Res Commun 45:716–722PubMedCrossRefGoogle Scholar
  14. 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 1:55–61CrossRefGoogle Scholar
  15. 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 116:715–723PubMedCentralPubMedCrossRefGoogle Scholar
  16. 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 25:2361–2368PubMedCrossRefGoogle Scholar
  17. 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, DCGoogle Scholar
  18. 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, DCGoogle Scholar
  19. Cleland WW, Andrews TJ, Gutteridge S, Hartman FC, Lorimer GH (1998) Mechanism of Rubisco: the carbamate as general base. Chem Rev 98:549–562PubMedCrossRefGoogle Scholar
  20. 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 81:4060–4064PubMedCrossRefGoogle Scholar
  21. Davies B, Griffiths H (2012) Competing carboxylases: circadian and metabolic regulation of Rubisco in C3 and CAM Mesembryanthemum crystallinum L. Plant Cell Environ 35:1211–1220PubMedCrossRefGoogle Scholar
  22. Dean C, Pichersky E, Dunsmuir P (1989) Structure, evolution, and regulation of rbcS genes in higher plants. Annu Rev Plant Physiol Plant Mol Biol 40:415–439CrossRefGoogle Scholar
  23. Dedonder A, Rethy R, Fredericq H, Van Montagu M, Krebbers E (1993) Arabidopsis rbcS genes are differentially regulated by light. Plant Physiol 101:801–808PubMedCentralPubMedCrossRefGoogle Scholar
  24. Delgado E, Medrano H, Keys AJ, MaJ Parry (1995) Species variation in rubisco specificity factor. J Exp Bot 46:1775–1777CrossRefGoogle Scholar
  25. 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 278:49401–49405PubMedCrossRefGoogle Scholar
  26. 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 15:93–106CrossRefGoogle Scholar
  27. Farquhar GD, Sv Caemmerer, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90PubMedCrossRefGoogle Scholar
  28. Firn R, Jones C (2009) A Darwinian view of metabolism: molecular properties determine fitness. J Exp Bot 60:719–726PubMedCrossRefGoogle Scholar
  29. Flood PJ, Harbinson J, Aarts MGM (2011) Natural genetic variation in plant photosynthesis. Trends Plant Sci 16:327–335PubMedCrossRefGoogle Scholar
  30. 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 28:571–579CrossRefGoogle Scholar
  31. Genkov T, Spreitzer RJ (2009) Highly conserved small subunit residues influence Rubisco large subunit catalysis. J Biol Chem 284:30105–30112PubMedCrossRefGoogle Scholar
  32. 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 285:19833–19841CrossRefGoogle Scholar
  33. 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 154:77–84CrossRefGoogle Scholar
  34. Gianazza E (1995) Isoelectric focusing as a tool for the investigation of post-translational processing and chemical modifications of proteins. J Chromatogr A 705:67–87PubMedCrossRefGoogle Scholar
  35. 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 18:585–596PubMedCrossRefGoogle Scholar
  36. Greenbaum D, Colangelo C, Williams K, Gerstein M (2003) Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol 4:117PubMedCentralPubMedCrossRefGoogle Scholar
  37. Gutteridge S (1991) The relative catalytic specificities of the large subunit core of Synechcoccus ribulose bisphosphate carboxylase oxygenase. J Biol Chem 266:7359–7362PubMedGoogle Scholar
  38. Gygi SP, Rochon Y, Franza BR, Aebersold R (1999) Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19:1720–1730PubMedCentralPubMedGoogle Scholar
  39. 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 98:1105–1114PubMedCentralPubMedCrossRefGoogle Scholar
  40. Houtz RL, Portis AR (2003) The life of ribulose 1,5-bisphosphate carboxylase/oxygenase-posttranslational facts and mysteries. Arch Biochem Biophys 414:150–158PubMedCrossRefGoogle Scholar
  41. Houtz RL, Magnani R, Nayak NR, Dirk LMA (2008) Co- and post-translational modifications in Rubisco: unanswered questions. J Exp Bot 59:1635–1645PubMedCrossRefGoogle Scholar
  42. Huner NPA, Hayden DB (1982) Changes in the heterogeneity of ribulose bisphosphate carboxylase–oxygenase in winter rye induced by cold hardening. Can J Biochem 60:897–903PubMedCrossRefGoogle Scholar
  43. 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 56:1154–1161PubMedCrossRefGoogle Scholar
  44. 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 57:1036–1041PubMedCrossRefGoogle Scholar
  45. Huner N, Oquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230CrossRefGoogle Scholar
  46. 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 106:983–990PubMedCentralPubMedGoogle Scholar
  47. 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 156:1603–1611PubMedCentralPubMedCrossRefGoogle Scholar
  48. 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 63:2159–2170PubMedCrossRefGoogle Scholar
  49. Jansen R, Greenbaum D, Gerstein M (2002) Relating whole-genome expression data with protein–protein interactions. Genome Res 12:37–46PubMedCrossRefGoogle Scholar
  50. 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 22:234–248PubMedCentralPubMedCrossRefGoogle Scholar
  51. Jordan DB, Ogren WL (1981) Species variation in the specificity of ribulose-bisphosphate carboxylase-oxygenase. Nature 291:513–515CrossRefGoogle Scholar
  52. Jordan DB, Ogren WL (1984) The CO2/O2 specificity of ribulose 1,5-bisphosphate carboxylase oxygenase - dependence on ribulosebisphosphate concentration, pH and temperature. Planta 161:308–313PubMedCrossRefGoogle Scholar
  53. Kapralov MV, Filatov DA (2007) Widespread positive selection in the photosynthetic Rubisco enzyme. BMC Evol Biol 7:73PubMedCentralPubMedCrossRefGoogle Scholar
  54. 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 28:1491–1503PubMedCrossRefGoogle Scholar
  55. 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 44:113–120PubMedCrossRefGoogle Scholar
  56. 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 93:13689–13693PubMedCrossRefGoogle Scholar
  57. 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 215:113–160PubMedCrossRefGoogle Scholar
  58. 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 11:745–759PubMedCrossRefGoogle Scholar
  59. Ku S-B, Edwards GE (1977) Oxygen inhibition of photosynthesis: i. Temperature dependence and relation to O2/CO2 solubility ratio. Plant Physiol 59:986–990PubMedCentralPubMedCrossRefGoogle Scholar
  60. 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 27:907–916CrossRefGoogle Scholar
  61. Kubien DS, Sage RF (2008) The temperature response of photosynthesis in tobacco with reduced amounts of Rubisco. Plant Cell Environ 31:407–418PubMedCrossRefGoogle Scholar
  62. Kubien DS, Whitney SM, Moore PV, Jesson LK (2008) The biochemistry of Rubisco in Flaveria. J Exp Bot 59:1767–1777PubMedCrossRefGoogle Scholar
  63. 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 54:678–685PubMedCentralPubMedCrossRefGoogle Scholar
  64. Langridge P (1981) Synthesis of the large subunit of spinach ribulose bisphosphate carboxylase may involve a precursor polypeptide. FEBS Lett 123:85–89CrossRefGoogle Scholar
  65. 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 60:2859–2876PubMedCrossRefGoogle Scholar
  66. 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 168:466–473PubMedCrossRefGoogle Scholar
  67. 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 43:969–976PubMedCrossRefGoogle Scholar
  68. 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 69:921–928PubMedCentralPubMedCrossRefGoogle Scholar
  69. 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 21:905–915CrossRefGoogle Scholar
  70. Moore BD, Cheng SH, Sims D, Seemann JR (1999) The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2. Plant Cell Environ 22:567–582CrossRefGoogle Scholar
  71. 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 272:5445–5451PubMedCrossRefGoogle Scholar
  72. 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 98:667–675PubMedCentralPubMedCrossRefGoogle Scholar
  73. 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 4:39–54PubMedCrossRefGoogle Scholar
  74. Palmer JD, Edwards H, Jorgensen RA, Thompson WF (1982) Novel evolutionary variation in transcription and location of 2 chloroplast genes. Nucleic Acids Res 10:6819–6832PubMedCentralPubMedCrossRefGoogle Scholar
  75. Paul K, Yeoh HH (1988) Characteristics of ribulose 1,5-bisphosphate carboxylase from cassava leaves. Plant Physiol Biochem 26:615–618Google Scholar
  76. Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209:2361–2367Google Scholar
  77. 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 49:89–104CrossRefGoogle Scholar
  78. 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 31:519–525PubMedCrossRefGoogle Scholar
  79. Read BA, Tabita FR (1992b) A hybrid ribulosebisphosphate carboxylase oxygenase enzyme exhibiting a substantial increase in substrate specificity factor. Biochemistry 31:5553–5560PubMedCrossRefGoogle Scholar
  80. 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 93:3881–3885PubMedCrossRefGoogle Scholar
  81. 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 53:609–620PubMedCrossRefGoogle Scholar
  82. Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant Cell Environ 30:1086–1106PubMedCrossRefGoogle Scholar
  83. Sage RF, Way DA, Kubien DS (2008) Rubisco, Rubisco activase, and global climate change. J Exp Bot 59:1581–1595PubMedCrossRefGoogle Scholar
  84. 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 120:179–186CrossRefGoogle Scholar
  85. Salvucci ME, Crafts-Brandner SJ (2004b) Mechanism for deactivation of Rubisco under moderate heat stress. Physiol Plan 122:513–519CrossRefGoogle Scholar
  86. Sasanuma T (2001) Characterization of the rbcs multigene family in wheat: subfamily classification, determination of chromosomal location and evolutionary analysis. Mol Genet Genom 265:161–171CrossRefGoogle Scholar
  87. 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 107:3475–3480PubMedCrossRefGoogle Scholar
  88. Schlichting CD (1986) The evolution of phenotypic plasticity in plants. Annu Rev Ecol Syst 17:667–693CrossRefGoogle Scholar
  89. Schlichting C (2002) Phenotypic plasticity in plants. Plant Spec Biol 17:85–88CrossRefGoogle Scholar
  90. Schlichting C, Pigliucci M (1993) Control of phenotypic plasticity via regulatory genes. Am Nat 142:366–370PubMedCrossRefGoogle Scholar
  91. Schlichting CD, Pigliucci M (1995) Gene-regulation, quantitative genetics and the evolution of reaction norms. Evol Ecol 9:154–168CrossRefGoogle Scholar
  92. Sharkey TD (1985) Photosynthesis in intact leaves of C3 plants - physics, physiology and rate limitations. Bot Rev 51:53–105CrossRefGoogle Scholar
  93. 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 146:83–96PubMedCentralPubMedCrossRefGoogle Scholar
  94. 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 4:583–594CrossRefGoogle Scholar
  95. Spreitzer RJ (2003) Role of the small subunit in ribulose-1,5-biphosphate carboxylase/oxygenase. Arch Biochem Biophys 414:141–149PubMedCrossRefGoogle Scholar
  96. 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 40:5615–5621PubMedCrossRefGoogle Scholar
  97. 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 102:17225–17230PubMedCrossRefGoogle Scholar
  98. 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 119:1387–1397PubMedCentralPubMedCrossRefGoogle Scholar
  99. 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 160:533–540PubMedCentralPubMedCrossRefGoogle Scholar
  100. 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 38:236–242CrossRefGoogle Scholar
  101. 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 103:7246–7251PubMedCrossRefGoogle Scholar
  102. von Caemmerer S (2000) Biochemical models of leaf photosynthesis. CSIRO Publishing, CollingwoodGoogle Scholar
  103. 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 85–113CrossRefGoogle Scholar
  104. 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 20:68–76CrossRefGoogle Scholar
  105. 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 159:147–157CrossRefGoogle Scholar
  106. Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150:563–565CrossRefGoogle Scholar
  107. 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 59:1779–1787PubMedCrossRefGoogle Scholar
  108. Wanner LA, Gruissem W (1991) Expression dynamics of the tomato rbcS gene family during development. Plant Cell 3:1289–1303PubMedCentralPubMedGoogle Scholar
  109. Warren CR, Dreyer E (2006) Temperature response of photosynthesis and internal conductance to CO2: results from two independent approaches. J Exp Bot 57:3057–3067Google Scholar
  110. 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 86:1198–1202PubMedCrossRefGoogle Scholar
  111. 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 108:14688–14693PubMedCrossRefGoogle Scholar
  112. 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 28:536–547CrossRefGoogle Scholar
  113. 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 47:1069–1080PubMedCrossRefGoogle Scholar
  114. 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 29:1659–1670PubMedCrossRefGoogle Scholar
  115. Yeoh HH, Badger MR, Watson L (1981) Variations in kinetic-properties of ribulose-1,5-bisphosphate carboxylases among plants. Plant Physiol 67:1151–1155PubMedCentralPubMedCrossRefGoogle Scholar
  116. 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 291:237–244PubMedCrossRefGoogle Scholar
  117. 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 180:480–488PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Department of BiologyUniversity of New BrunswickFrederictonCanada

Personalised recommendations