Limitation of Photosynthesis by Carbon Metabolism

Abstract

The occurrence of O2-insensitive photosynthesis at high quantum flux and moderate temperature in Spinacia oleracea was characterized by analytical gas exchange measurements on intact leaves. In addition photosynthetic metabolite pools were measured in leaves which had been rapidly frozen under defined gas conditions. Upon switching to low 0°in 02-insensitive conditions the ATP/ADP ratio fell dramatically within one minute. The P-glycerate pool increased over the same time. Ribulose bisphosphate initially declined, then increased and exceeded the pool size measured in air. The pools of hexose monophosphates and UDPglucose were higher at a partial pressure of 02 of 21 millibars than at 210 millibars. These results are consistent with the hypothesis that the rate of sucrose synthesis limited the overall rate of assimilation under O2-insensitive conditions.In this article we ask whether manipulating the ambient 02 concentration provides a way of recognizing a situation in which sucrose or starch synthesis limit the rate of photosynthesis. During photosynthesis, CO2 and Pi are converted to triose-P in the chloroplast. The triose-P is converted to sucrose in the cytosol, or starch in the chloroplast, liberating Pi for use in subsequent CO2 fixation. The production of triose-P in the chloroplast requires electron transport, regeneration of RuBP3 and activity of Rubisco. As all these processes are also needed for photorespiration, there is normally a stimulation of photosynthesis when the ambient 02 concentration is lowered to suppress photorespiration. However, photorespiration does not compete for the reactions by which triose-P is converted into end products such as sucrose and starch. This means that the rate of photosynthesis would not be reduced by photorespiration when photosynthesis is limited by the utilization of photosynthesis products provided there is adequate electron transport and carbon reduction cycle activity to cope with the additional fluxes required when photorespiration occurs. The rate of photosynthesis would then be independent of the ambient 02 level. It has been observed that decreasing the 02 concentration from 210 to 21 mbar does not always lead to an increase of photosynthesis, especially when the light intensity is high and the temperature is below 20°C (3,12,14,24). It has been proposed that this 02 insensitivity of photosynthesis is due to a limitation of photosynthate utilization, in particular triose-P utilization for sucrose and starch synthesis (17, 18). When 02 sensitivity is lost photosynthesis also fails to respond to CO2 (18) indicating that the phenomenon is not simply an effect of 02 on pseudo-cyclic photophosphorylation.A limitation ofthe utilization of phosphorylated intermediates would lead to a fall of the stromal Pi. Many studies have shown that the rate of CO2 fixation in isolated chloroplasts depends on the stromal Pi level. Upon lowerng the stromal Pi concentration from 7 to 2 mM, CO2 fixation was decreased by 40% (11) and this inhibition of CO2 fixation was acco...

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)

“…But in the mutant the high-CO2 decline of photosynthesis is present in both 21 and 1.2% 0 2 , showing that this effect is not related to the glycolate pathway but, rather, to the slow starch synthesis. A possible explanation is based on differences in T3P utilization (Sharkey et al, 1986), specifically on trapping of phosphate in HePs. This makes phosphate less available for the photosynthetic tumover in the mutant.…”

Control of Photosynthesis and Stomatal Conductance in Ricinus communis L. (Castor Bean) by Leaf to Air Vapor Pressure Deficit

“…In contrast, there was a decrease in relative inhibition of photosynthesis by photorespiring conditions under low VPD with increasing light intensity. This likely occurs because O2-insensitive photosynthesis can occur under conditions where the capacity for photosynthesis is high, but is limited by triose-P utilization (27). With increasing irradiance, the relative inhibition of photosynthesis by 02 also decreased in potatoes under a VPD of 11 to 15 mbar (15).…”

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

“…With ample CO 2 and high light, the flux through the Benson-Calvin cycle is controlled by the capacity for RuBP regeneration (e.g. capacity of photochemistry to provide energy for regeneration), or by 'feedback limitation' via limited capacity to utilise triose-P for synthesis of end products such as starch and sucrose (Sharkey et al 1986;Foyer 1987;Sage and Sharkey 1987;Sharkey 1990;Paul and Foyer 2001;Paul and Pellny 2003).…”