The importance of energy balance in improving photosynthetic productivity.

Current proposals to improve photosynthesis to meet our energy and food needs include the following: (1) improving the performance of Rubisco; (2) decreasing photorespiration by turning C3 plants into C4 plants, installing algal or cyanobacterial carbonconcentrating mechanisms into higher plant chloroplasts, or redesigning photorespiratory metabolism; and (3) adding new biosynthetic pathways to increase the flow of carbon into useful products, like starch or oils, etc. While introducing or modifying pathways for these processes will be an important step forward, it is important to note that these approaches may also substantially alter the energetic demands placed on photosynthesis. To successfully translate these modifications into enhanced photosynthesis requires that chloroplasts can meet these altered demands. Chloroplasts have already evolved significant energy flexibility mechanisms, as discussed below, but these are activated under specific environmental and metabolic challenges. We need knowledge of the mechanisms regulating these processes in order to modulate them for increased energy efficiency.Ultimately,we could adjust chloroplast performance to meet altered needs by altering gene regulation or by introducing newbalancing systems. It is thus useful to reviewwhat is known about energy balance in the chloroplast and project how these might be adjusted. The light reactions involve highly reactive species, and if not controlled properly, they can produce deleterious reactive oxygen species. In addition, the synthesis of ATP and NADPH in linear electron flow is tightly coupled (i.e. one cannot occur without the other). If, for example, the substrates for the ATP synthase (ADP, inorganic phosphate) become limiting, then the proton motive force (pmf) builds up, inhibiting electron transfer to NADP. Likewise, if NADP is limiting, photosynthetic electron carriers become reduced, slowing electron transfer and associated proton translocation, thus limiting ATP synthesis. Linear electron flow produces a fixed ATP/NADPH ratio, and each metabolic pathway directly powered by photosynthesis consumes different fixed ATP/NADPH ratios. However, since fluxes through these pathways vary between species and under different physiological conditions, substantial mismatches in the production and demands for ATP/NADPH could arise. Chloroplasts have very limited pools of ATP and NADPH. Consequently, such mismatches will rapidly (within seconds) inhibit photosynthesis (Avenson et al., 2005b; Cruz et al., 2005; Amthor, 2010). The chloroplast must balance the production and consumption of both ATP and NADPH by augmenting production of the limiting intermediate (e.g. by cyclic electron flow) or dissipating the intermediate in excess. Here, we consider recent progress in understanding the mechanisms used by plants and algae to match ATP/NADPH supply with demands, with the aim to guide future efforts at optimizing these processes. Engineered plants may exacerbate the situation by creating demands for ATP/NADPH that differ from those to which the chloroplast has adapted. For example, adding a C4 pathway to a C3 plant would increase the ATP/NADPH demand, whereas increasing the storage of energy in saturated fats or oils would decrease it. Thus, we need to consider two distinct situations: (1) when the ATP/NADPH production ratio is lower than that needed to support downstream metabolism; and (2) when the ATP/NADPH production ratio exceeds demand. Both situations lead to metabolic congestion requiring different flexibility mechanisms. To make the situation more complex, the transthylakoid pmf, which drives ATP synthesis, is also the main “signal” regulating the light reactions (Kramer et al., 2004). Acidification of the lumen associated with a buildup of pmf activates the photoprotective energy-dependent excitation quenching (qE) response (Müller et al., 2001). Down-regulating the conductance of ATP synthase alters electron flux relative to the pmf by reducing quantum efficiency and slowing electron transfer but does not alter the ATP/ NADPH output ratio (Kramer et al., 2004).