Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

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

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).


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