Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
Shopping Cart: ( empty )
You are here: Home > Journals > FP > FP09129
RESEARCH ARTICLE
Contents Vol 36(11)

Feedback limitation of photosynthesis at high CO2 acts by modulating the activity of the chloroplast ATP synthase

Olavi Kiirats A , Jeffrey A. Cruz B , Gerald E. Edwards A and David M. Kramer B C
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, Washington State University, Pullman, WA 99164-4238, USA.

B Institute of Biological Chemistry, 339 Clark Hall, Washington State University, Pullman, WA 99164-6340, USA.

C Corresponding author. Email: dkramer@wsu.edu

This paper originates from a presentation at the 1st International Plant Phenomics Symposium, Canberra, Australia, April 2009.

Functional Plant Biology 36(11) 893-901 https://doi.org/10.1071/FP09129
Submitted: 3 June 2009  Accepted: 11 August 2009   Published: 5 November 2009

Abstract

It was previously shown that photosynthetic electron transfer is controlled under low CO2 via regulation of the chloroplast ATP synthase. In the current work, we studied the regulation of photosynthesis under feedback limiting conditions, where photosynthesis is limited by the capacity to utilise triose-phosphate for synthesis of end products (starch or sucrose), in a starch-deficient mutant of Nicotiana sylvestris Speg. & Comes. At high CO2, we observed feedback control that was progressively reversed by increasing O2 levels from 2 to 40%. The activity of the ATP synthase, probed in vivo by the dark-interval relaxation kinetics of the electrochromic shift, was proportional to the O2-induced increases in O2 evolution from PSII (JO2), as well as the sum of Rubisco oxygenation (vo) and carboxylation (vc) rates. The altered ATP synthase activity led to changes in the light-driven proton motive force, resulting in regulation of the rate of plastoquinol oxidation at the cytochrome b6f complex, quantitatively accounting for the observed control of photosynthetic electron transfer. The ATP content of the cell decreases under feedback limitation, suggesting that the ATP synthesis was downregulated to a larger extent than ATP consumption. This likely resulted in slowing of ribulose bisphosphate regeneration and JO2). Overall, our results indicate that, just as at low CO2, feedback limitations control the light reactions of photosynthesis via regulation of the ATP synthase, and can be reconciled with regulation via stromal Pi, or an unknown allosteric affector.

Additional keywords: electrochromic shift, in vivo spectroscopy, non-photochemical, proton motive force, quenching, regulation.


Acknowledgements

The authors thank Drs Jeremy Harbinson, Thomas Sharkey, Murray Badger, Atsuko Kanazawa, Kaori Kohzuma and Susanne von Caemmerer for interesting discussions. We also acknowledge Mr C. Cody for plant growth management. This work was supported by a grant from the USA Department of Agriculture CREES, NRI Award (2008–02905, DMK) and the National Science Foundation (IBN-0641232, GEE).


References


Avenson TJ, Kanazawa A, Cruz JA, Takizawa K, Ettinger WE, Kramer DM (2005) Integrating the proton circuit into photosynthesis: progress and challenges. Plant, Cell & Environment 28, 97–109.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual Review of Plant Biology 59, 89–113.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Baker N, Harbinson J, Kramer DM (2007) Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant, Cell & Environment 30, 1107–1125.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Cruz JA, Avenson TJ, Kanazawa A, Takizawa K, Edwards GE, Kramer DM (2005) Plasticity in light reactions of photosynthesis for energy production and photoprotection. Journal of Experimental Botany 56, 395–406.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Eichelmann H, Laisk A (1994) CO2 uptake and electron transport rates in wild-type and a starchless mutant of Nicotiana sylvestris: the role and regulation of starch synthesis at saturating CO2 concentrations. Plant Physiology 106, 679–687.
|  CAS | PubMed |
open url image1

Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Flügge UI, Heldt H (1984) The phosphate-triosephosphate-phosphoglycerate translocator of the chloroplast. Trends in Biochemical Sciences 9, 533–535.
| Crossref |
open url image1

Foyer CH (1987) The basis for source–sink interaction in leaves. Plant Physiology and Biochemistry 15, 649–657. open url image1

Genty B, Briantais J, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92.
|  CAS |
open url image1

Giersch C, Robinson SP (1987) Regulation of photosynthetic carbon metabolism during phosphate limitation of photosynthesis in isolated spinach chloroplasts. Photosynthesis Research 14, 211–227.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Hanson KR (1990) Steady-state and oscillating photosynthesis by a starchless mutant of Nicotiana sylvestris. Plant Physiology 93, 1212–1218.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Hanson KR (1992) Evidence for mitochondrial regulation of photosynthesis by a starchless mutant of Nicotiana sylvestris. Plant Physiology 99, 276–283.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Hanson KR, McHale NA (1988) A starchless mutant of Nicotiana sylvestris containing a modified plastid glucomutase. Plant Physiology 88, 838–844.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Hope AB, Valente P, Matthews DB (1994) Effects of pH on the kinetics of redox reaction in and around the cytochrome bf complex in an isolated system. Photosynthesis Research 42, 111–120.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annual Review of Plant Biology 47, 655–684.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Huber SC, Hanson KR (1992) Carbon partitioning and growth of a starchless mutant of Nicotiana sylvestris. Plant Physiology 99, 1449–1454.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kanazawa A, Kramer DM (2002) In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase. Proceedings of the National Academy of Sciences of the United States of America 99, 12789–12794.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kiirats O, Lea PJ, Franceschi VR, Edwards GE (2002) Bundle sheath diffusive resistance to CO2 and effectiveness of C4 photosynthesis and refixation of photorespired CO2 in a C4 cycle mutant and wild-type Amaranthus edulis. Plant Physiology 130, 964–976.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kirchhoff H, Schottler MA, Maurer J, Weis E (2004) Plastocyanin redox kinetics in spinach chloroplasts: evidence for disequilibrium in the high potential chain. Biochimica et Biophysica Acta 1659, 63–72.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kohzuma K, Cruz JA, Akashi K, Hoshiyasu S, Munekage Y, Yokota A, Kramer DM (2009) The long-term responses of the photosynthetic proton circuit to drought. Plant, Cell & Environment 32, 209–219.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Krall JP, Edwards GE (1992) Relationship between photosystem II activity and CO2 fixation in leaves. Physiologia Plantarum 86, 180–187.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Kramer DM, Sacksteder CA (1998) A diffused-optics flash kinetic spectrophometer (DOFS) for measurements of absorbance changes in intact plants in the steady-state. Photosynthesis Research 56, 103–112.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Kramer DM, Sacksteder CA, Cruz JA (1999) How acidic is the lumen? Photosynthesis Research 60, 151–163.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Kramer DM, Avenson TJ, Edwards GE (2004a) Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton reactions. Trends in Plant Science 9, 349–357.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kramer DM, Johnson G, Kiirats O, Edwards GE (2004b) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynthesis Research 79, 209–218.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Laisk A, Loreto F (1996) Determining photosynthetic parameters from leaf CO2 exchange and chlorophyll fluorescence. Plant Physiology 110, 903–912.
|  CAS | PubMed |
open url image1

Laisk A, Oja V, Rasulov B, Ramma H, Eichelmann H, Kasparova I, Pettai H, Padu E, Vapaavuori E (2002) A computer-operated routine of gas exchange and optical measurements to diagnose photosynthetic apparatus in leaves. Plant, Cell & Environment 25, 923–943.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Leegood RC , Edwards G (1996) Carbon metabolism and photorespiration: temperature dependence in relation to other environmental factors. In ‘Photosynthesis and the environment’. (Ed. NR Baker) pp. 191–221. (Kluwer Academic Publishers: The Netherlands)

Leegood RC, Furbank RT (1986) Stimulation of photosynthesis by 2% oxygen at low temperatures is restored by phosphate. Planta 168, 84–93.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Neuhaus EH, Stitt M (1990) Control analysis of photosynthate partitioning. Impact of reduced activity of ADP-glucose pyrophosphorylase or plastid phosphoglucomutase on the fluxes to starch and sucrose in Arabidopsis thaliana (L.) Heynh. Planta 182, 445–454.
|  CAS | Crossref |
open url image1

Nishio JN, Whitmarsh J (1991) Dissipation of the proton electrochemical potential in intact and lysed chloroplasts. Plant Physiology 95, 522–528.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Niyogi KK (2000) Safety valves for photosynthesis. Current Opinion in Plant Biology 3, 455–460.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. Journal of Experimental Botany 52, 1383–1400.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Paul MJ, Pellny TK (2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. Journal of Experimental Botany 54, 539–547.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Peterson RB, Hanson KR (1991) Changes in photochemical and fluorescence yields in leaf tissue from normal and starchless Nicotiana sylvestris with increasing irradiance. Plant Science 76, 143–151.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Preiss J (1991) Biology and molecular biology of starch synthesis and regulation. In ‘Oxford surveys of plant molecular and cellular biology. Vol. 7’. (Ed. BJ Miflin) pp. 59–114. (Oxford University Press: Oxford)

Robinson SP, Giersch C (1987) Inorganic phosphate concentration in the stroma of isolated chloroplasts and its influence on photosynthesis. Australian Journal of Plant Physiology 14, 451–462.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Ruuska S, Andrews TJ, Badger MR, Price GD, von Caemmerer S (2000) The role of chloroplast electron transport and metabolites in modulating Rubisco activity in tobacco. Insights from transgenic plants with reduced amounts of cytochrome b/f complex or glyceraldehyde 3-phosphate dehydrogenase. Plant Physiology 122, 491–504.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Sacksteder CA, Kramer DM (2000) Dark-interval relaxation kinetics (DIRK) of absorbance changes as a quantitative probe of steady-state electron transfer. Photosynthesis Research 66, 145–158.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Sacksteder CA, Kanazawa A, Jacoby ME, Kramer DM (2000) The proton to electron stoichiometry of steady-state photosynthesis in living plants: a proton-pumping Q-cycle is continuously engaged. Proceedings of the National Academy of Sciences of the United States of America 97, 14283–14288.
|  CAS | Crossref | PubMed |
open url image1

Sacksteder CA, Jacoby ME, Kramer DM (2001) A portable, non-focusing optics spectrophotometer (NoFOSpec) for measurements of steady-state absorbance changes in intact plants. Photosynthesis Research 70, 231–240.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Sage RF, Sharkey TD (1987) The effect of temperature on the occurrence of O2 and CO2 insensitive photosynthesis in field grown plants. Plant Physiology 84, 658–664.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sharkey TD (1990) Feedback limitation of photosynthesis and the physiological role of ribulose bisphosphate carboxylase carbamylation. Botanical Magazine, Tokyo 2, 87–105. open url image1

Sharkey DJ, Vanderveer PJ (1989) Stromal phosphate concentration is low during feedback limited photosynthesis. Plant Physiology 91, 679–684.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Sharkey TD, Vassey TL (1989) Low oxygen inhibition of photosynthesis is caused by inhibition of starch synthesis. Plant Physiology 90, 385–387.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Sharkey TD, Stitt M, Heineke D, Gerhardt R, Raschke K, Heldt HW (1986) Limitation of photosynthesis by carbon metabolism. Plant Physiology 81, 1123–1129.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Sharkey TD, Kobza J, Seemann JR, Brown RH (1988) Reduced cytosolic fructose-1,6-bisphosphatase activity leads to loss of O2 sensitivity in a Flaveria linearis mutant. Plant Physiology 86, 667–671.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Sharkey TD , Laporte MM , Micallef BJ , Shewmaker CK , Oakes JV (1995) Sucrose synthesis, temperature, and plant yield. In ‘Photosynthesis: from light to biosphere. Vol. V’. (Ed. P Mathis) pp. 635–640. (Kluwer Academic Publishers: Dordrecht)

Strehler BL, McElroy WC (1957) Assay of adenosine triphosphate. Methods in Enzymology 3, 871–873.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Sun J, Edwards GE, Okita TW (1999a) Feedback inhibition of photosynthesis in rice measured by O2 dependent transients. Photosynthesis Research 59, 187–200.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Sun J, Okita TW, Edwards GE (1999b) Modification of carbon partitioning, photosynthetic capacity, and O2 sensitivity in Arabidopsis plants with low ADP-glucose pyrophosphorylase activity. Plant Physiology 119, 267–276.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Takizawa K, Kanazawa A, Cruz JA, Kramer DM (2007) In vivo thylakoid proton motive force. Quantitative non-invasive probes show the relative lumen pH-induced regulatory responses of antenna and electron transfer. Biochimica et Biophysica Acta 1767, 1233–1244.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Takizawa K, Cruz JA, Kramer DM (2008) Depletion of stromal inorganic phosphate induces high ‘energy-dependent’ antenna exciton quenching (qE) by decreasing proton conductivity at CF0-CF1 ATP synthase. Plant, Cell & Environment 31, 235–243.
|  CAS | PubMed |
open url image1

Wirtz W, Stitt M, Heldt HW (1980) Enzymic determination of metabolites in the subcellular compartments of spinach protoplasts. Plant Physiology 66, 187–193.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Woodrow IE, Berry JA (1988) Enzymatic regulation of photosynthetic CO2 fixation in C3 plants. Annual Review of Plant Biology 39, 533–594.
|  CAS |
open url image1