, Volume 243, Issue 3, pp 687–698 | Cite as

Triose phosphate use limitation of photosynthesis: short-term and long-term effects

  • Jennifer T. Yang
  • Alyssa L. Preiser
  • Ziru Li
  • Sean E. Weise
  • Thomas D. Sharkey
Original Article


Main conclusion

The triose phosphate use limitation was studied using long-term and short term changes in capacity. The TPU limitation caused increased proton motive force; long-term TPU limitation additionally reduced other photosynthetic components.

Photosynthetic responses to CO2 can be interpreted primarily as being limited by the amount or activity of Rubisco or the capacity for ribulose bisphosphate regeneration, but at high rates of photosynthesis a third response is often seen. Photosynthesis becomes insensitive to CO2 or even declines with increasing CO2, and this behavior has been associated with a limitation of export of carbon from the Calvin–Benson cycle. It is often called the triose phosphate use (TPU) limitation. We studied the long-term consequences of this limitation using plants engineered to have reduced capacity for starch or sucrose synthesis. We studied short-term consequences using temperature as a method for changing the balance of carbon fixation capacity and TPU. A long-term and short-term TPU limitation resulted in an increase in proton motive force (PMF) in the thylakoids. Once a TPU limitation was reached, any further increases in CO2 was met with a further increase in the PMF but no increase or little increase in net assimilation of CO2. A long-term TPU limitation resulted in reduced Rubisco and RuBP regeneration capacity. We hypothesize that TPU, Rubisco activity, and RuBP regeneration are regulated so that TPU is normally in slight excess of what is required, and that this results in more effective regulation than if TPU were in large excess.


Feedback Phosphoglucoisomerase Temperature Triose phosphate transporter Triose phosphate use Starch/sucrose partitioning 



This work was funded by US Department of Energy grant DE-SCOOO8509 to TDS and by USDA support of salary of TDS. We thank Professor David Kramer for discussions of these data.


  1. Avenson TJ, Kanazawa A, Cruz JA, Takizawa K, Ettinger WE, Kramer DM (2005) Integrating the proton circuit into photosynthesis: progress and challenges. Plant Cell Environ 28:97–109CrossRefGoogle Scholar
  2. Badger MR, Sharkey TD, von Caemmerer S (1984) The relationship between steady-state gas exchange of bean leaves and the levels of carbon-reduction-cycle intermediates. Planta 160:305–313CrossRefPubMedGoogle Scholar
  3. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113CrossRefPubMedGoogle Scholar
  4. Baker NR, Harbinson J, Kramer DM (2007) Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant Cell Environ 30:1107–1125CrossRefPubMedGoogle Scholar
  5. Cen YP, Sage RF (2005) The regulation of Rubisco activity in response to variation in temperature and atmospheric CO2 partial pressure in sweet potato. Plant Physiol 139:979–990PubMedCentralCrossRefPubMedGoogle Scholar
  6. Chia T, Thorneycraft D, Chapple A, Messerli G, Chen J, Zeeman S, Smith SM, Smith AM (2004) A cytosolic glycosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night. Plant J 37:853–863CrossRefPubMedGoogle Scholar
  7. Dahal K, Wang J, Martyn GD, Rahimy F, Vanlerberghe GC (2014) Mitochondrial alternative oxidase maintains respiration and preserves photosynthetic capacity during moderate drought in tobacco. Plant Physiol 166:1560–1574PubMedCentralCrossRefPubMedGoogle Scholar
  8. Dahal K, Martyn GD, Vanlerberghe GC (2015) Improved photosynthetic performance during severe drought in Nicotiana tabacum overexpressing a nonenergy conserving respiratory electron sink. New Phytol 208:382–395CrossRefPubMedGoogle Scholar
  9. Dyson BC, Allwood JW, Feil R, Xu YUN, Miller M, Bowsher CG, Goodacre R, Lunn JE, Johnson GN (2015) Acclimation of metabolism to light in Arabidopsis thaliana: the glucose 6-phosphate/phosphate translocator GPT2 directs metabolic acclimation. Plant Cell Environ 38:1404–1417CrossRefPubMedGoogle Scholar
  10. Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90CrossRefPubMedGoogle Scholar
  11. Fettke J, Malinova I, Albrecht T, Hejazi M, Steup M (2011) Glucose-1-phosphate transport into protoplasts and chloroplasts from leaves of Arabidopsis. Plant Physiol 155:1723–1734PubMedCentralCrossRefPubMedGoogle Scholar
  12. Flügge UI (1999) Phosphate translocators in plastids. Annu Rev Plant Physiol Plant Mol Biol 50:27–45CrossRefPubMedGoogle Scholar
  13. Gibon Y, Blasing OE, Palacios-Rojas N, Pankovic D, Hendriks JH, Fisahn J, Hohne M, Gunther M, Stitt M (2004) Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. Plant J 39:847–862CrossRefPubMedGoogle Scholar
  14. Harley PC, Weber JA, Gates DM (1985) Interactive effects of light, leaf temperature, CO2 and O2 on photosynthesis in soybean. Planta 165:249–263CrossRefPubMedGoogle Scholar
  15. Harley PC, Thomas RB, Reynolds JF, Strain BR (1992) Modelling photosynthesis of cotton grown in elevated CO2. Plant Cell Environ 15:271–282CrossRefGoogle Scholar
  16. Harris GC, Cheesbrough JK, Walker DA (1983) Effects of mannose on photosynthetic gas exchange in spinach leaf discs. Plant Physiol 71:108–111PubMedCentralCrossRefPubMedGoogle Scholar
  17. Hattenbach A, Müller-Röber B, Nast G, Heineke D (1997) Antisense repression of both ADP-glucose pyrophosphorylase and triose phosphate translocator modifies carbohydrate partitioning in leaves. Plant Physiol 115:471–475PubMedCentralPubMedGoogle Scholar
  18. Hoagland DR, Arnon DI (1938) The water culture method for growing plants without soil. In: UC Agric. Exp. Sta. Circular 347, Berkley, pp 1–39Google Scholar
  19. Jolliffe PA, Tregunna EB (1973) Environmental regulation of the oxygen effect on apparent photosynthesis in wheat. Can J Bot 51:841–853CrossRefGoogle Scholar
  20. Kanazawa A, Kramer DM (2002) In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase. Proc Natl Acad Sci USA 99:12789–12794PubMedCentralCrossRefPubMedGoogle Scholar
  21. Kiirats O, Cruz JA, Edwards GE, Kramer DM (2009) Feedback limitation of photosynthesis at high CO2 acts by modulating the activity of the chloroplast ATP synthase. Funct Plant Biol 36:893–901CrossRefGoogle Scholar
  22. Kiss JZ, Wright JB, Caspar T (1996) Gravitropism in roots of intermediate-starch mutants of Arabidopsis. Physiol Plant 97:237–244CrossRefPubMedGoogle Scholar
  23. Kohzuma K, Cruz JA, Akashi K, Hoshiyasu S, Munekage YN, Yokota A, Kramer DM (2009) The long-term responses of the photosynthetic proton circuit to drought. Plant Cell Environ 32:209–219CrossRefPubMedGoogle Scholar
  24. Kohzuma K, Dal Bosco C, Meurer J, Kramer DM (2013) Light- and metabolism-related regulation of the chloroplast ATP synthase has distinct mechanisms and functions. J Biol Chem 288:13156–13163PubMedCentralCrossRefPubMedGoogle Scholar
  25. Kölling K, Müller A, Flütsch P, Zeeman SC (2013) A device for single leaf labelling with CO2 isotopes to study carbon allocation and partitioning in Arabidopsis thaliana. Plant Methods 9:45PubMedCentralCrossRefPubMedGoogle Scholar
  26. Kölling K, Thalmann M, Müller A, Jenny C, Zeeman SC (2015) Carbon Partitioning in Arabidopsis thaliana is a dynamic process controlled by the plants’ metabolic status and its circadian clock. Plant Cell Environ 38:1965–1979PubMedCentralCrossRefPubMedGoogle Scholar
  27. Kramer DM, Cruz JA, Kanazawa A (2003) Balancing the central roles of the thylakoid proton gradient. Trends Plant Sci 8:27–32CrossRefPubMedGoogle Scholar
  28. Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218CrossRefPubMedGoogle Scholar
  29. Li Z, Gao J, Benning C, Sharkey TD (2012) Characterization of photosynthesis in Arabidopsis ER-to-plastid lipid trafficking mutants. Photosynth Res 112:49–61CrossRefPubMedGoogle Scholar
  30. Lu Y, Sharkey TD (2004) The role of amylomaltase in maltose metabolism in the cytosol of photosynthetic cells. Planta 218:466–473CrossRefPubMedGoogle Scholar
  31. Mott KA, Jensen RG, O’Leary JW, Berry JA (1984) Photosynthesis and ribulose 1,5-bisphosphate concentrations in intact leaves of Xanthium strumarium L. Plant Physiol 76:968–971PubMedCentralCrossRefPubMedGoogle Scholar
  32. Neuhaus HE, Kruckeberg AL, Feil R, Stitt M (1989) Reduced-activity mutants of phosphoglucose isomerase in the cytosol and chloroplast of Clarkia xantiana. II. Study of the mechanisms which regulate photosynthate partitioning. Planta 178:110–122CrossRefPubMedGoogle Scholar
  33. Nittylä T, Messerli G, Trevisan M, Chen J, Smith AM, Zeeman SC (2004) A novel maltose transporter is essential for starch degradation in leaves. Science 303:87–89CrossRefGoogle Scholar
  34. Pracharoenwattana I, Zhou W, Keech O, Francisco PB, Udomchalothorn T, Tschoep H, Stitt M, Gibon Y, Smith SM (2010) Arabidopsis has a cytosolic fumarase required for the massive allocation of photosynthate into fumaric acid and for rapid plant growth on high nitrogen. Plant J 62:785–795CrossRefPubMedGoogle Scholar
  35. Riesmeier JW, Flügge UI, Schulz B, Heineke D, Heldt HW, Willmitzer L, Frommer WB (1993) Antisense repression of the chloroplast triose phosphate translocator affects carbon partitioning in transgenic potato plants. Proc Natl Acad Sci USA 90:6160–6164PubMedCentralCrossRefPubMedGoogle Scholar
  36. Rott M, Martins NdF, Thiele W, Lein W, Bock R, Kramer DM, Schöttler MA (2011) ATP synthase repression in tobacco restricts photosynthetic electron transport, CO2 assimilation, and plant growth by overacidification of the thylakoid lumen. The Plant Cell Online 23:304–321CrossRefGoogle Scholar
  37. Sacksteder C, Jacoby M, Kramer D (2001) A portable, non-focusing optics spectrophotometer (NoFOSpec) for measurements of steady-state absorbance changes in intact plants. Photosynth Res 70:231–240CrossRefPubMedGoogle Scholar
  38. 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 Physiol 94:1728–1734PubMedCentralCrossRefPubMedGoogle Scholar
  39. Sage RF, Sharkey TD (1987) The effect of temperature on the occurrence of O2 and CO2 insensitive photosynthesis in field grown plants. Plant Physiol 84:658–664PubMedCentralCrossRefPubMedGoogle Scholar
  40. Sage RF, Sharkey TD, Seemann JR (1988) The in vivo response of ribulose-1,5-bisphosphate carboxylase activation state and pool sizes of photosynthetic metabolites to elevated CO2 in Phaseolus vulgaris L. Planta 174:407–416CrossRefPubMedGoogle Scholar
  41. Schneider A, Häusler RE, Kolukisaoglu Ü, Kunze R, Van Der Graaff E, Schwacke R, Catoni E, Desimone M, Flügge U-I (2002) An Arabidopsis thaliana knock-out mutant of the chloroplast triose phosphate/phosphate translocator is severely compromised only when starch synthesis, but not starch mobilisation is abolished. Plant J 32:685–699CrossRefPubMedGoogle Scholar
  42. Sharkey TD (1985) O2-insensitive photosynthesis in C3 plants: its occurrence and a possible explanation. Plant Physiol 78:71–75PubMedCentralCrossRefPubMedGoogle Scholar
  43. Sharkey TD (2012) Mesophyll conductance: constraint on carbon acquisition by C3 plants. Plant Cell Environ 35:1881–1883CrossRefPubMedGoogle Scholar
  44. Sharkey TD, Bernacchi CJ (2012) Photosynthetic responses to high temperature. In: Flexas J, Loreto F, Medrano H (eds) Terrestrial photosynthesis in a changing environment: a molecular, physiological, and ecological approach. Cambridge University Press, Cambridge, pp 294–302Google Scholar
  45. Sharkey TD, Vanderveer PJ (1989) Stromal phosphate concentration is low during feedback limited photosynthesis. Plant Physiol 91:679–684PubMedCentralCrossRefPubMedGoogle Scholar
  46. Sharkey TD, Berry JA, Raschke K (1985) Starch and sucrose synthesis in Phaseolus vulgaris as affected by light, CO2 and abscisic acid. Plant Physiol 77:617–620PubMedCentralCrossRefPubMedGoogle Scholar
  47. Sharkey TD, Seemann JR, Berry JA (1986a) Regulation of ribulose-1,5-bisphosphate carboxylase activity in response to changing partial pressure of O2 and light in Phaseolus vulgaris. Plant Physiol 81:788–791PubMedCentralCrossRefPubMedGoogle Scholar
  48. Sharkey TD, Stitt M, Heineke D, Gerhardt R, Raschke K, Heldt HW (1986b) Limitation of photosynthesis by carbon metabolism. II O2 insensitive CO2 uptake results from limitation of triose phosphate utilization. Plant Physiol 81:1123–1129PubMedCentralCrossRefPubMedGoogle Scholar
  49. Sharkey TD, Berry JA, Sage RF (1988a) Regulation of photosynthetic electron-transport as determined by room-temperature chlorophyll a fluorescence in Phaseolus vulgaris L. Planta 176:415–424CrossRefPubMedGoogle Scholar
  50. Sharkey TD, Kobza J, Seemann JR, Brown RH (1988b) Reduced cytosolic fructose-1,6-bisphosphatase activity leads to loss of O2 sensitivity in a Flaveria linearis mutant. Plant Physiol 86:667–671PubMedCentralCrossRefPubMedGoogle Scholar
  51. Sharkey TD, Savitch LV, Vanderveer PJ, Micallef BJ (1992) Carbon partitioning in a Flaveria linearis mutant with reduced cytosolic fructose bisphosphatase. Plant Physiol 100:210–215PubMedCentralCrossRefPubMedGoogle Scholar
  52. Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant Cell Environ 30:1035–1040CrossRefPubMedGoogle Scholar
  53. Takizawa K, Cruz JA, Kanazawa A, Kramer DM (2007) The thylakoid proton motive force in vivo. Quantitative, non-invasive probes, energetics, and regulatory consequences of light-induced pmf. Biochim Biophys Acta 1767:1233–1244CrossRefPubMedGoogle Scholar
  54. Takizawa K, Kanazawa A, Kramer DM (2008) Depletion of stromal P i induces high ‘energy-dependent’ antenna exciton quenching (q E) by decreasing proton conductivity at CFO-CF1 ATP synthase. Plant Cell Environ 31:235–243CrossRefPubMedGoogle Scholar
  55. Tezara W, Mitchell VJ, Driscoll SD, Lawlor DW (1999) Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 401:914–917CrossRefGoogle Scholar
  56. Vassey TL, Quick WP, Sharkey TD, Stitt M (1991) Water stress, carbon dioxide, and light effects on sucrose-phosphate synthase activity in Phaseolus vulgaris. Physiol Plant 81:37–44CrossRefGoogle Scholar
  57. von Caemmerer S, Edmondson DL (1986) The relationship between steady-state gas exchange, in vivo RuP2 carboxylase activity and some carbon reduction cycle intermediates in Raphanus sativus. Aust J Plant Physiol 13:669–688CrossRefGoogle Scholar
  58. von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387CrossRefGoogle Scholar
  59. von Caemmerer S, Farquhar GD (1984) Effects of partial defoliation, changes in irradiance during growth, short-term water stress, and growth at enhanced p(CO2) on the photosynthetic capacity of leaves of Phaseolus vulgaris L. Planta 160:320–329CrossRefGoogle Scholar
  60. von Caemmerer S, Farquhar GD, Viil J, Laisk A (1985) Kinetics and activation of Rubisco and some preliminary modelling of the RuP2 pool sizes. In: Kinetics of photosynthesis. Tallin, pp 46–58Google Scholar
  61. Walters RG, Ibrahim DG, Horton P, Kruger NJ (2004) A mutant of Arabidopsis lacking the triose-phosphate/phosphate translocator reveals metabolic regulation of starch breakdown in the light. Plant Physiol 135:891–906PubMedCentralCrossRefPubMedGoogle Scholar
  62. Weise SE, Weber A, Sharkey TD (2004) Maltose is the major form of carbon exported from the chloroplast at night. Planta 218:474–482CrossRefPubMedGoogle Scholar
  63. Wellburn AR, Lichtenthaler H (1984) Formulae and program to determine total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Adv Photosynth Res II:9–12CrossRefGoogle Scholar
  64. Wise RR, Olson AJ, Schrader SM, Sharkey TD (2004) Electron transport is the functional limitation of photosynthesis in field-grown Pima cotton plants at high temperature. Plant Cell Environ 27:717–724CrossRefGoogle Scholar
  65. Zhang R, Cruz JA, Kramer DM, Magallanes-Lundback ME, Dellapenna D, Sharkey TD (2009) Moderate heat stress reduces the pH component of the transthylakoid proton motive force in light-adapted, intact tobacco leaves. Plant Cell Environ 32:1538–1547CrossRefPubMedGoogle Scholar
  66. Zrenner R, Krause KP, Apel P, Sonnewald U (1996) Reduction of the cytosolic fructose-1,6-bisphosphatase in transgenic potato plants limits photosynthetic sucrose biosynthesis with no impact on plant growth and tuber yield. Plant J 9:671–681CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Jennifer T. Yang
    • 1
    • 2
  • Alyssa L. Preiser
    • 1
  • Ziru Li
    • 1
  • Sean E. Weise
    • 1
  • Thomas D. Sharkey
    • 1
  1. 1.Department of Biochemistry and Molecular BiologyMichigan State UniversityEast LansingUSA
  2. 2.Intercollege Program of Plant BiologyThe Pennsylvania State UniversityState CollegeUSA

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