Does Rubisco control the rate of photosynthesis and plant growth? An exercise in molecular ecophysiology

Abstract

Experiments are described in which tobacco (Nicotiana tabacum L.) transformed with antisense rbcS to decrease expression of ribulose‐1,5‐bisphosphate carboxylase‐oxygenase (Rubisco) was used to evaluate the contribution of Rubisco to the control of photosynthetic rate, and the impact of a changed rate of photosynthesis on whole plant composition, allocation and growth. (1) The concept of flux control coefficients is introduced. It is discussed how, with adequate precautions, a set of wild‐type and transgenic plants with varying expression of an enzyme can be used to obtain experimental values for its flux control coefficient. (2) The flux control coefficient of Rubisco for photosynthesis depends on the short‐term conditions. It increases in high light, or low CO 2. (3) When plants are grown under constant irradiance, the flux control coefficient in the growth conditions is low (<0.2) at irradiances of up to 1000μmol quanta m−2 s−1. In a natural irradiance regime exceeding 1500μmol quanta m−2 s−2 over several hours the flux coefficient rose to 0.8–0.9. It is concluded that plants are able to adjust the balance between Rubisco and the remainder of the photosynthetic machinery, and thereby avoid a one‐sided limitation of photosynthesis by Rubisco over a wide range of ambient growth irradiance regimes. (4) When the plants were grown on limiting inorganic nitrogen, Rubisco had a higher flux control coefficient (0.5). It is proposed that, in many growth conditions, part of the investment in Rubisco may be viewed as a nitrogen store, albeit bringing additional marginal advantages with respect to photosynthetic rate and water use efficiency. (5) A change in the rate of photosynthesis did not automatically translate into a change in growth rate. Several factors are identified which contribute to this buffering of growth against a changed photosynthetic rate. (6) There is an alteration in whole plant allocation, resulting in an increase in the leaf area ratio. The increase is mainly due to a higher leaf water content, and not to changes in shoot/root allocation. This increased investment in whole plant leaf area partly counteracts the decreased efficiency of photosynthesis at the biochemical level. (7) Plants with decreased Rubisco have a lower intrinsic water use efficiency and contain high levels of inorganic cations and anions. It is proposed that these are a consequence of the increased rate of transpiration, and that the resulting osmotic potential might be a contributory factor to the increased water content and expansion of the leaves. (8) Starch accumulation in source leaves is decreased when unit leaf photosynthesis is reduced, allowing a more efficient use of the fixed carbon. (9) Decreased availability of carbohydrates leads to a down‐regulation of nitrate assimilation, acting via a decrease in nitrate reductase activity.