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Photosynthesis Research

, Volume 115, Issue 2–3, pp 153–166 | Cite as

Photosynthetic characterization of Rubisco transplantomic lines reveals alterations on photochemistry and mesophyll conductance

  • Jeroni Galmés
  • Juan Alejandro Perdomo
  • Jaume Flexas
  • Spencer M. Whitney
Regular Paper

Abstract

Improving Rubisco catalysis is considered a promising way to enhance C3-photosynthesis and photosynthetic water use efficiency (WUE) provided the introduced changes have little or no impact on other processes affecting photosynthesis such as leaf photochemistry or leaf CO2 diffusion conductances. However, the extent to which the factors affecting photosynthetic capacity are co-regulated is unclear. The aim of the present study was to characterize the photochemistry and CO2 transport processes in the leaves of three transplantomic tobacco genotypes expressing hybrid Rubisco isoforms comprising different Flaveria L-subunits that show variations in catalysis and differing trade-offs between the amount of Rubisco and its activation state. Stomatal conductance (g s) in each transplantomic tobacco line matched wild-type, while their photochemistry showed co-regulation with the variations in Rubisco catalysis. A tight co-regulation was observed between Rubisco activity and mesophyll conductance (g m) that was independent of g s thus producing plants with varying g m/g s ratios. Since the g m/g s ratio has been shown to positively correlate with intrinsic WUE, the present results suggest that altering photosynthesis by modifying Rubisco catalysis may also be useful for targeting WUE.

Keywords

Carboxylation CO2 fixation Crop improvement Water use efficiency 

Notes

Acknowledgments

This research was supported by the ARC Fellowship Grant FT0991407 awarded to SMW and the projects AGL2009-07999 and BFU2011-23294 (Plan Nacional, Spain) awarded to JG and JF, respectively. JAP is supported by a FPI Fellowship of the Government of the Balearic Islands.

References

  1. Ainsworth EA, Bush DR (2011) Carbohydrate export from the leaf: a highly regulated process and target to enhance photosynthesis and productivity. Plant Physiol 155:64–69PubMedCrossRefGoogle Scholar
  2. Alonso H, Blayney MJ, Beck JL, Whitney SM (2009) Substrate induced assembly of Methanococcoides burtonii d-ribulose-1,5-bisphosphate carboxylase/oxygenase dimers into decamers. J Biol Chem 284:33876–33882PubMedCrossRefGoogle Scholar
  3. Avni A, Edelman M, Rachailovich I, Aviv D, Fluhr R (1989) A point mutation in the gene for the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase affects holoenzyme assembly in Nicotiana tabacum. EMBO J 8:1915–1918PubMedGoogle Scholar
  4. Baker RT, Catanzariti AM, Karunasekara Y, Soboleva TA, Sharwood R, Whitney SM, Board PG (2005) Using deubiquitinylating enzymes as research tools. In: Deshaies RJ (ed) Ubiquitin and protein degradation. Part A. Methods in enzymology. Academic Press, Pasadena, pp 540–554CrossRefGoogle Scholar
  5. Barbour M, Warren CR, Farquhar GD, Forrester G, Brown H (2010) Variability in mesophyll conductance between barley genotypes, and effects on transpiration efficiency and carbon isotope discrimination. Plant Cell Environ 33:1176–1185PubMedGoogle Scholar
  6. Baroli I, Price GD, Badger MR, von Caemmerer S (2008) The contribution of photosynthesis to the red light response of stomatal conductance. Plant Physiol 146:737–747PubMedCrossRefGoogle Scholar
  7. Blayney M, Whitney SM, Beck J (2011) Nano-ESI mass spectrometry of Rubisco and Rubisco activase structures and their interactions with nucleotides and sugar phosphates. J Am Soc Mass Spectrom 22:1588–1601PubMedCrossRefGoogle Scholar
  8. Cen Y-P, Sage RF (2006) The regulation of Rubisco activity to variation in temperature and atmospheric CO2 partial pressure in sweet potato. Plant Physiol 139:979–990CrossRefGoogle Scholar
  9. Eichelmann H, Talts E, Oja V, Padu E, Laisk A (2009) Rubisco in planta k cat is regulated in balance with photosynthetic electron transport. J Exp Bot 60:4077–4088PubMedCrossRefGoogle Scholar
  10. Evans JR, von Caemmerer S (2012) Temperature response of carbon isotope discrimination and mesophyll conductance in tobacco. Plant Cell Environ. doi: 10.1111/j.1365-3040.2012.02591.x Google Scholar
  11. Evans JR, von Caemmerer S, Setchell BA, Hudson GS (1994) The relationship between CO2 transfer conductance and leaf anatomy in transgenic tobacco with a reduced content of Rubisco. Aust J Plant Physiol 21:475–495CrossRefGoogle Scholar
  12. Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90CrossRefGoogle Scholar
  13. Flexas J, Ribas-Carbó M, Hanson DT, Bota J, Otto B, Cifre J, McDowell N, Medrano H, Kaldenhoff R (2006) Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo. Plant J 48:427–439PubMedCrossRefGoogle Scholar
  14. Flexas J, Ribas-Carbó M, Díaz-Espejo A, Galmés J, Medrano H (2007) Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant Cell Environ 30:1284–1298PubMedCrossRefGoogle Scholar
  15. Flexas J, Ribas-Carbó M, Díaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ 31:602–631PubMedCrossRefGoogle Scholar
  16. Flexas J, Galmés J, Gallé A, Gulías J, Pou A, Ribas-Carbó M, Tomàs M, Medrano H (2010) Improving water use efficiency in grapevines: potential physiological targets for biotechnological improvement. Aust J Grape Wine Res 16:106–121CrossRefGoogle Scholar
  17. Flexas J, Barbour MM, Brendel O, Cabrera HM, Carriquí M, Díaz-Espejo A, Douthe C, Dreyer E, Ferrio JP, Gago J, Gallé A, Galmés J, Kodama N, Medrano H, Niinemets U, Peguero-Pina JJ, Pou A, Ribas-Carbó M, Tomás M, Tosens T, Warren CR (2012) Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. Plant Sci 193–194:73–84Google Scholar
  18. Foyer C, Furbank R, Harbinson J, Horton P (1990) The mechanisms contributing to photosynthetic control of electron transport by assimilation in leaves. Photosynth Res 25:83–100CrossRefGoogle Scholar
  19. Furbank RT, Chitty JA, von Caemmerer S, Jenkins CLD (1996) Antisense RNA inhibition of rbcS gene expression reduces Rubisco level and photosynthesis in the C4 plant Flaveria bidentis. Plant Physiol 111:725–734PubMedGoogle Scholar
  20. Gallé A, Florez-Sarasa ID, Tomas M, Medrano H, Ribas-Carbó M, Flexas J (2009) The role of mesophyll conductance during water stress and recovery in tobacco (Nicotiana sylvestris): acclimation or limitation? J Exp Bot 60:2379–2390PubMedCrossRefGoogle Scholar
  21. Galmés J, Flexas J, Keys AJ, Cifre J, Mitchell RAC, Madgwick PJ, Haslam RP, Medrano H, Parry MAJ (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
  22. Galmés J, Medrano H, Flexas J (2007) Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms. New Phytol 175:81–93PubMedCrossRefGoogle Scholar
  23. Galmés J, Conesa MA, Ochogavía JM, Perdomo JA, Francis D, Ribas-Carbó M, Savé R, Flexas J, Medrano H, Cifre J (2011) Physiological and morphological adaptations in relation to water use efficiency in Mediterranean accessions of Solanum lycopersicum. Plant Cell Environ 34:245–260PubMedCrossRefGoogle Scholar
  24. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92CrossRefGoogle Scholar
  25. Getzoff TP, Zhu GH, Bohnert HJ, Jensen RG (1998) Chimeric Arabidopsis thaliana Rubisco containing a pea small subunit protein is compromised in carbamylation. Plant Physiol 116:695–702PubMedCrossRefGoogle Scholar
  26. Grassi G, Magnani F (2005) Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees. Plant Cell Environ 28:834–849CrossRefGoogle Scholar
  27. Hammond ET, Andrews TJ, Mott KA, Woodrow IE (1998) Regulation of Rubisco activation in antisense plants of tobacco containing reduced levels of Rubisco activase. Plant J 14:101–110PubMedCrossRefGoogle Scholar
  28. Hanba YT, Shibasaka M, Hayashi Y, Hayakawa T, Kasamo K, Terashima I, Katsuhara M (2004) Overexpression of the barley aquaporin HvPIP2;1 increases internal CO2 conductance and CO2 assimilation in the leaves of transgenic rice plants. Plant Cell Physiol 45:521–529PubMedCrossRefGoogle Scholar
  29. Harley PC, Loreto F, Di Marco G, Sharkey TD (1992) Theoretical considerations when estimating the mesophyll conductance to CO2 flux by the analysis of the response of photosynthesis to CO2. Plant Physiol 98:1429–1436PubMedCrossRefGoogle Scholar
  30. He Z, von Caemmerer S, Hudson GS, Price GD, Badger MR, Andrews TJ (1997) Ribulose-l,5-bisphosphate carboxylase/oxygenase activase deficiency delays senescence of ribulose-l,5-bisphosphate carboxylase/oxygenase but progressively impairs its catalysis during tobacco leaf development. Plant Physiol 115:1569–1580PubMedCrossRefGoogle Scholar
  31. Hendrickson L, Sharwood R, Ludwig M, Whitney SM, Badger MR, von Caemmerer S (2008) The effects of Rubisco activase on C4 photosynthesis and metabolism at high temperature. J Exp Bot 59:1789–1798PubMedCrossRefGoogle Scholar
  32. Hoagland DR, Snyder WC (1933) Nutrition of strawberry plants under controlled conditions: (a) effects of deficiencies of boron and certain other elements; (b) susceptibility to injury from sodium salts. Proc Am Soc Hortic Sci 30:288–294Google Scholar
  33. 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 Physiol 98:294–302PubMedCrossRefGoogle Scholar
  34. 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 156:1603–1611PubMedCrossRefGoogle Scholar
  35. Kaldenhoff R (2012) Mechanisms underlying CO2 diffusion in leaves. Curr Opin Plant Biol 15:276–281PubMedCrossRefGoogle Scholar
  36. Kanevski I, Maliga P, Rhoades DF, Gutteridge S (1999) Plastome engineering of ribulose-1,5-bisphosphate carboxylase/oxygenase in tobacco to form a sunflower large subunit and tobacco small subunit hybrid. Plant Physiol 119:133–141PubMedCrossRefGoogle Scholar
  37. Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch H-J, Rosenkranz R, Stäbler N, Schönfeld B, Kreuzaler F, Peterhänsel C (2007) Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nature 25:593–599CrossRefGoogle Scholar
  38. Lefebvre S, Lawson T, Zakhleniuk OV, Lloyd JC, Raines CA (2005) Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. Plant Physiol 138:451–460PubMedCrossRefGoogle Scholar
  39. Makino A, Sage RF (2007) Temperature response of photosynthesis in transgenic rice transformed with ‘sense’ or ‘antisense’ rbcS. Plant Cell Physiol 48:1472–1483PubMedCrossRefGoogle Scholar
  40. Ogren WL, Bowes G (1971) Ribulose diphosphate carboxylase regulates soybean photorespiration. Nature 230:159–160Google Scholar
  41. Parry MAJ, Keys AJ, Madgwick PJ, Carmo-Silva E, Andralojc J (2008) Rubisco regulation: a role for inhibitors. J Exp Bot 59:1569–1580PubMedCrossRefGoogle Scholar
  42. Parry MAJ, Andralojc PJ, Scales JC, Salvucci ME, Carmo-Silva AE, Alonso H, Whitney SM (2013) Rubisco activity and regulation as targets for crop improvement. J Exp Bot 64:717–730PubMedCrossRefGoogle Scholar
  43. Peterhansel C, Maurino VG (2011) Photorespiration redesigned. Plant Physiol 155:49–55PubMedCrossRefGoogle Scholar
  44. Pierce J, Tolbert NE, Barker R (1980) Interaction of ribulosebisphosphate carboxylase/oxygenase with transition-state analogues. Biochemistry 19:934–942PubMedCrossRefGoogle Scholar
  45. Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Caused and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588PubMedCrossRefGoogle Scholar
  46. Price DG, von Caemmerer S, Evans JR, Yu JW, Lloyd J, Oja V, Kell P, Harrison K, Gallagher A, Badger M (1994) Specific reduction of chloroplast carbonic anhydrase activity by antisense RNA in transgenic tobacco plants has a minor effect on photosynthetic CO2 assimilation. Planta 193:331–340CrossRefGoogle Scholar
  47. Price DG, Badger MR, von Caemmerer S (2011) The prospect of using cyanobacterial bicarbonate transporters to improve leaf photosynthesis in C3 crop plants. Plant Physiol 155:20–26PubMedCrossRefGoogle Scholar
  48. 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 183:542–554CrossRefGoogle Scholar
  49. Raines CA (2011) Increasing photosynthetic carbon assimilation in C3 plants to improve crop yield: current and future strategies. Plant Physiol 155:36–42PubMedCrossRefGoogle Scholar
  50. Ruuska S, Andrews TJ, Badger MR, Hudson GS, Laisk A, Price DG, von Caemmerer S (1998) The interplay between limiting processes in C3 photosynthesis studied by rapid-response gas exchange using transgenic tobacco impaired in photosynthesis. Aust J Plant Physiol 25:859–870CrossRefGoogle Scholar
  51. Ruuska SA, Badger MR, Andrews TJ, von Caemmerer S (2000) Photosynthetic electron sinks in transgenic tobacco with reduced amounts of Rubisco: little evidence for significant Mehler reaction. J Exp Bot 51:357–368PubMedCrossRefGoogle Scholar
  52. Sage RF (2002) Variation in the kcat 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
  53. Sharkey TD (1998) Photosynthetic carbon reduction. In: Raghavendra AS (ed) Photosynthesis: a comprehensive treatise. Cambridge University Press, Cambridge, pp 111–122Google Scholar
  54. Sharwood RE, Whitney SM (2010) Engineering the sunflower Rubisco subunits into tobacco chloroplasts: new considerations, Chap. 19. In: Rebeiz CA (ed) The chloroplast: advances in photosynthesis and respiration, vol 31. Springer, Dordrecht, pp 285–306Google Scholar
  55. 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 146:83–96PubMedCrossRefGoogle Scholar
  56. Shikanai T, Foyer CH, Dulieu H, Parry MAJ, Yokota A (1996) A point mutation in the gene encoding the Rubisco large subunit interferes with holoenzyme assembly. Plant Mol Biol 31:399–403PubMedCrossRefGoogle Scholar
  57. Stotz M, Mueller-Cajar O, Ciniawsky S, Wendler P, Ulrich-Hartl F, Bracher A, Hayer-Hartl M (2011) Structure of green-type Rubisco activase from tobacco. Nat Struct Mol Biol 18:1366–1370PubMedCrossRefGoogle Scholar
  58. Suzuki Y, Ohkubo M, Hatakeyama H, Ohashi K, Yoshizawa R, Kojima S, Hayakawa T, Yamaya T, Mae T, Makino A (2007) Increased Rubisco content in transgenic rice transformed with the ‘Sense’ rbcS gene. Plant Cell Physiol 48:626–637PubMedCrossRefGoogle Scholar
  59. Suzuki Y, Miyamoto T, Yoshizawa R, Mae T, Makino A (2009) Rubisco content and photosynthesis of leaves at different positions in transgenic rice with an overexpression of rbcS. Plant Cell Environ 32:417–427PubMedCrossRefGoogle Scholar
  60. Terashima I, Hanba YT, Tholen D, Niinemets U (2011) Leaf functional anatomy in relation to photosynthesis. Plant Physiol 155:108–116PubMedCrossRefGoogle Scholar
  61. Tholen D, Ethier G, Genty B, Pepin S, Zhu XG (2012) Variable mesophyll conductance revisited: theoretical background and experimental implications. Plant Cell Environ 35:2087–2103PubMedCrossRefGoogle Scholar
  62. Uehlein N, Otto B, Hanson DT, Fischer M, McDowell N, Kaldenhoff R (2008) Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability. Plant Cell 20:648–657PubMedCrossRefGoogle Scholar
  63. Valentini R, Epron D, De Angelis P, Matteucci G, Dreyer E (1995) In situ estimation of net CO2 assimilation, photosynthetic electron flow and photorespiration in Turkey oak (Quercus cerris L.) leaves: diurnal cycles under different levels of water supply. Plant Cell Environ 18:631–640CrossRefGoogle Scholar
  64. Varone L, Ribas-Carbó M, Cardona C, Gallé A, Medrano H, Gratani L, Flexas J (2012) Stomatal and non-stomatal limitations to photosynthesis in seedlings and samplings of Mediterranean species pre-conditioned and aged in nurseries: different response to water stress. Environ Exp Bot 75:235–247CrossRefGoogle Scholar
  65. 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 195:88–97CrossRefGoogle Scholar
  66. von Caemmerer S, Lawson T, Oxborough K, Baker NR, Andrews TJ, Raines C (2004) Stomatal conductance does not correlate with photosynthetic capacity in transgenic tobacco with reduced amounts of Rubisco. J Exp Bot 55:1157–1166CrossRefGoogle Scholar
  67. Wang Z-Y, Snyder GW, Easu BD, Portis AR Jr, Ogren WL (1992) Sequence dependent variation in the interaction of substrate bound ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and Rubisco activase. Plant Physiol 100:1858–1862PubMedCrossRefGoogle Scholar
  68. Whitney SM, Andrews TJ (2001) Plastome-encoded bacterial ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) supports photosynthesis and growth in tobacco. Proc Natl Acad Sci USA 98:14738–14743PubMedCrossRefGoogle Scholar
  69. Whitney SM, Andrews TJ (2003) Photosynthesis and growth of tobacco with a substituted bacterial Rubisco mirror the properties of the introduced enzyme. Plant Physiol 133:287–294PubMedCrossRefGoogle Scholar
  70. Whitney SM, Houtz RL, Alonso H (2011a) Advancing our understanding and capacity to engineer nature’s CO2-sequestering enzyme, Rubisco. Plant Physiol 155:27–35PubMedCrossRefGoogle Scholar
  71. Whitney SM, Sharwood RE, Orr D, White SJ, Alonso H, Galmés J (2011b) 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
  72. Williams TG, Flanagan LB, Coleman JR (1996) Photosynthetic gas exchange and discrimination against 13CO2, and C18O16O in tobacco plants modified by an antisense construct to have low chloroplastic carbonic anhydrase. Plant Physiol 112:319–326PubMedGoogle Scholar
  73. Woodrow IE, Mott KA (1989) Rate limitation of non-steady-state photosynthesis by ribulose-1,5-bisphosphate carboxylase in spinach. Aust J Plant Physiol 16:487–500CrossRefGoogle Scholar
  74. Yamori W, von Caemmerer S (2009) Effect of Rubisco activase deficiency on the temperature response of CO2 assimilation rate and Rubisco activation state: insights from transgenic tobacco with reduced amounts of Rubisco activase. Plant Physiol 151:2073–2082PubMedCrossRefGoogle Scholar
  75. Zhu X-G, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Annu Rev Plant Biol 61:235–261PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Jeroni Galmés
    • 1
  • Juan Alejandro Perdomo
    • 1
  • Jaume Flexas
    • 1
  • Spencer M. Whitney
    • 2
  1. 1.Research Group on Plant Biology under Mediterranean ConditionsUniversitat de les Illes BalearsPalmaSpain
  2. 2.Plant Sciences Division, Research School of BiologyAustralian National UniversityCanberraAustralia

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