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

Abstract

Abstract.It was previously shown that photosynthetic electron transfer is controlled under low CO 2 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 CO 2 , we observed feedback control that was progressively reversed by increasing O 2 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 O 2 -induced increases in O 2 evolution from PSII (J O 2 ), as well as the sum of Rubisco oxygenation (v o ) and carboxylation (v c ) 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 b 6 f 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 J O 2 ). Overall, our results indicate that, just as at low CO 2 , feedback limitations control the light reactions of photosynthesis via regulation of the ATP synthase, and can be reconciled with regulation via stromal P i , or an unknown allosteric affector.Additional keywords: electrochromic shift, in vivo spectroscopy, non-photochemical, proton motive force, quenching, regulation.

ATP Synthase Repression in Tobacco Restricts Photosynthetic Electron Transport, CO2 Assimilation, and Plant Growth by Overacidification of the Thylakoid Lumen

“…It is noteworthy that the maximum ATP synthase activity was not yet reached at 350 ppm CO 2 , implying that ATP synthase is partly downregulated at ambient CO 2 . Maximum ATP synthase activity was established at 500 ppm CO 2 , followed by a minor decrease when CO 2 contents were further increased up to 2000 ppm (Kiirats et al, 2009). All these data suggest that the ATP synthase is dynamically regulated, and significant reductions in complex content can be compensated by upregulating the enzymatic activity.…”

“…NADP + limitation would result in electron transfer to alternative acceptors, such as O 2 , generating reactive oxygen species. These can damage the photosynthetic apparatus itself and also initiate cell death responses (Kim et al, 2008).Reduced ADP and P i regeneration results in substrate limitation of the thylakoid ATP synthase, reducing proton efflux from the lumen and resulting in an increase of the proton motive force (pmf) across the thylakoid membrane (Takizawa et al, 2008;Kiirats et al, 2009). Under standard growth conditions, the pmf is partitioned into an electrochemical component (DC) and a proton gradient (DpH) in such a way that the pH value of the thylakoid lumen is usually kept between 7.0 and 6.5 (Takizawa et al, 2007).…”

Understanding Forest Health with Remote Sensing-Part II—A Review of Approaches and Data Models

“…The regulation of photosynthetic electron transport, as well as its feedback processes and the assessment of photosynthetic efficiency and stress in crops, grassland and forest canopies, have been investigated with sun-induced chlorophyll fluorescence methods at leaf [41], field, and regional levels [42][43][44][45]. Spectroscopic techniques for the detection of chlorophyll fluorescence forms the basis for the European Space Agency (ESA) Fluorescence Explorer Sensors (FLEX, [45,46,70]) to be launched in 2018.…”

Enhancing C3 Photosynthesis

“…It was possible to increase electron transport in Arabidopsis through the expression of Porphyra cytochrome c 6 , introducing a parallel electron carrier between cytochrome f and PSI (see Peterhansel et al, 2008). ATPase regulation provides feedback control between carbon metabolism and light reactions (Kiirats et al, 2009). In a future high-CO 2 world, C 3 photosynthesis will be increasingly limited by RuBP regeneration, and research is needed to explore how greater amounts of cytochrome b 6 f and ATPase complexes can be assembled, given that they contain both nucleus-and chloroplast-encoded subunits.…”