The Importance of Energy Balance in Improving Photosynthetic Productivity  

Abstract

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 C 3 plants into C 4 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 new balancing systems. It is thus useful to review what 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 f...

The Operation of Two Decarboxylases, Transamination, and Partitioning of C4 Metabolic Processes between Mesophyll and Bundle Sheath Cells Allows Light Capture To Be Balanced for the Maize C4 Pathway

“…In fact, increasing ATP production at the electron transport chain level would require light (Takabayashi et al, 2005;Kramer and Evans, 2011), whose availability is not under metabolic control. At the same time, the electron transport-mediated dark production of ATP (Morstadt et al, 2002;Bukhov and Carpentier, 2004;Egorova and Bukhov, 2004;Kuntz, 2004) has low conversion efficiency (Kramer and Evans, 2011); hence, an engagement of ATP chemiosynthesis would be incompatible with the observed pattern of J ATP /GA. ATP itself is not a suitable shuttle to rebalance ATP deficits because the ATP molecule is relatively big, it has a relatively small pool, and homeostasis is critical; therefore, every chloroplast has an independent ATP pool.…”

“…PEPCK (Walker et al, 1986;Furumoto et al, 1999Furumoto et al, , 2000Wingler et al, 1999) and glyoxylate recycling (Yoshimura et al, 2004) were allocated to BS; LEF (Meierhoff and Westhoff, 1993;Romanowska et al, 2006;Majeran and van Wijk, 2009;Friso et al, 2010;Kramer and Evans, 2011) and PPDK (see "Discussion") were allocated to M; R LIGHT was split equally between M and BS (von Caemmerer, 2000;Kromdijk et al, 2010;Ubierna et al, 2011); PR and SS were variably allocated. T was equal in BS and M, as the pool of Asp and Ala is shared.…”

“…1). Additionally, energetic partitioning can also vary between cell types, since the total ATP produced (J ATP ) per CO 2 fixed in GA (J ATP /GA) may be produced in BS (mainly through cyclic electron flow [CEF] around PSI) or in M (mainly through linear electron flow [LEF]), depending on the light locally available in BS or M (Kramer and Evans, 2011;Yin and Struik, 2012). Furthermore, although all NADPH is produced in M, the only compartment operating linear electron transport and oxidizing water, some NADPH is exported to BS through MAL diffusion, to meet the reducing power demand therein (NADPH BS ).…”

The Rubisco Chaperone BSD2 May Regulate Chloroplast Coverage in Maize Bundle Sheath Cells

“…Due to the tight link between the light and lightindependent reactions of photosynthesis, decreased carbon fixation might, in turn, decrease the rate of consumption of light reaction products (ATP and NADPH), lowering PSII efficiency (Kramer and Evans, 2011). To assess the light reactions, pulse amplitude fluorometry was used to measure the light intensity dependence of PSII operating efficiency (ФPSII) and nonphotochemical quenching (NPQ), as shown in Figure 6.…”

Focus Issue on Metabolism: Metabolites, Metabolites Everywhere

“…It describes how this can be used to access important aspects of metabolism such as redox and energy metabolism (Kramer and Evans, 2011) that are properties of the cellular system as a whole (Nikoloski et al, 2015). In doing so, they cover both isotope-and stoichiometric constraint-based approaches toward this goal and list biological insights that they have afforded and the ability to perform cellular accountancy via the latter approach.…”