Elimination of photorespiration by elevation of CO, leads to a large increase in photosynthesis in rice. Clearly, there is enough electron transport and Calvin cycle activity to support a much higher rate of carbon assimilation. However, the elimination of photorespiration by introduction of C4 is not equivalent to merely elevating the CO, level in terms of the requirements for electron transport. The C4 pathway requires an increase in the ATP requirement relative to NADPH. ForC3 photosynthesis in high CO,, this is approximately 1.5, but, in C4 (of the NADP-ME type), it is estimated to be 2.75. In such C4 plants, this is achieved by bundle sheath chloroplasts operating only as producers of ATP by cyclic electron transport around PSI. This division of noncyclic and cyclic electron transport between two chloroplast types may be essential to provide this high ratio of ATP/NADPH. Knowledge of thylakoid membrane structure and function now allows us to predict with some certainty the ATP/NADPH production of noncyclic electron transport, since 6 H+ are translocated for each 2 e transferred from H,0 to NADP, and 4 H+ are required for each ATP synthesized, that is, the maximum overall stoichiometry is 1.5 ATP/NADPH. To raise this value to that required for C4 photosynthesis in a single-cell type requires either the operation of cyclic electron transport around PSI or the operation of the Mehler pathway as an alternative pathway to NADP reduction.
The capacity of cyclic electron transport under light-limiting conditions will depend on the partitioning of Chi appropriately between PSII and PSI—the presence of cyclic electron transport requires an excess of PSI over PSII compared with noncyclic transport alone. This partitioning of Chi depends on both the regulation of the content of PSII and PSI reaction centers and the levels of the light-harvesting proteins. This regulation has not been studied in rice, but in Arabidopsis thaliana fairly complex interactions are found: growth in high light results in an increase in PSII reaction centers but a loss of light harvesting. In very low light, the content of PSI increases dramatically. Not only light intensity but also light quality exert control over the levels of these proteins. A comparative study of a range of species showed how the ratio of PSII and PSI is antagonistically controlled by the two components of the shade environment, low irradiance and enrichment in far-red light. The balance between these two forces established how the ratio changed in shade compared with unshaded conditions. There is no information on how these acclimation responses affect the efficiency of cyclic electron transport imposed by the enhanced metabolic demand for ATP. In addition to the acclimation of the thylakoid membrane composition to the requirements of photosystem activation, state transitions provide a mechanism for short-term responses to changes in either the spectral quality of light or the demand for cyclic electron transport. State transitions depend on the reversible phosphorylation of the Lhcbl and 2 polypeptides of LHCII, and it has been estimated that the mobile pool of LHCII accounts for about 20% of the antenna of PSII. If the relative antenna size of PSI/PSII were 1:1 in state 1. then in state 2 this ratio could increase to 1.5, provided phospho-LHCII is efficiently coupled to PSI. The latter is substantiated by recent investigation of the state transition in Arabidopsis leaves (Horton 1999). In C4 mesophyll chloroplasts, it was shown that the phosphorylation state of LHCII depended on the metabolic demand for ATP (Horton et al 1990), suggesting that in these chloroplasts at least there is sufficient flexibility in photosystem function to accommodate quite large shifts in ATP/NADPH requirement.
At photosynthetic saturation, electron and proton transport are proceeding close to capacity. ApH is high to drive ATP synthesis at high rates. Under such conditions, photosynthetic performance could be impaired by slippage of the Q-cycle, reducing the efficiency of H+ translocation, and by passive leakage of H+ through the thylakoid membrane. The higher ATP/ NADPH demanded of the C4 pathway may not be sustainable under these conditions, and may reduce photosynthetic capacity. Conversely, in C, chloroplasts, there have been observations consistent with an excessive ApH, arising from operation of the Q-cycle and alternative electron transfer pathways, if there are limitations to NADPH turnover. An excessive ApH may also arise if the supply of phosphate is in some way limited, as may occur under conditions when triose phosphate supply from the chloroplast exceeds the capacity to synthesize sucrose. An excessive ApH can be relieved in isolated chloroplasts by mild uncoupling. In C4 mesophyll chloroplasts, such inhibition has also been observed when phosphoglycerate is supplied as the only electron acceptor. Interestingly, stimulation of ATP turnover by pyruvate, Pi dikinase activity relieved such inhibition. The higher rate of turnover of ATP in the C4 pathway could mean that photosynthetic electron transport could proceed at a faster rate.
The decline in photosynthetic capacity observed during grain filling in some rice varieties suggests that an increased rate of photosynthesis from the introduction of C4 could enhance grain filling. However, as with many of the discussions above, the key questions relate to why photosynthesis is declining. Is the flag leaf photosynthesis so tightly coupled to grain filling that there would be no gain from a higher capacity of photosynthesis? During grain filling, the dominant sink for photosynthate is the developing grain—the level of carbohydrate in the leaf would then serve as a signal that down-regulates photosynthesis to meet the demand of the developing grain. If this were the case, with a C4 pathway, there would be no gain. On the other hand, however, the C4 pathway would allow the same rate of photosynthesis with less electron transport capacity and lower Rubisco. Since the supply of N to the grain depends on the degradation of leaf proteins, including thylakoid proteins and Rubisco, C4 may confer distinct advantages during the grain-filling period, provided that levels of leaf protein are high enough in the first place.
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