**3. The Structure of the Energy Network Simplifies ATP and NADPH Balancing**

Once the total demand for NADPH is satisfied via the interplay between LEF and NPQ, other processes fine tune ATP/NADPH production ratios to match metabolic demand precisely. Downstream metabolism of an illuminated leaf (discussed in more detail below) requires ATP/NADPH ratios above 1.5, meaning that extra ATP is needed to achieve energy balancing. By poising metabolic demand at a higher ATP/NADPH ratio than that produced by LEF, the system can first produce the necessary NADPH, with coupled baseline production of ATP, before then producing the supplemental ATP needed for the specific metabolic context. This greatly simplifies the requirements of energy balancing since ATP and NADPH production ratios do not need to be independently re-adjusted following changes in total demand and total production capacity can be adjusted first based on a single factor (NADPH demand) before supplemental processes overcome the ATP deficit. In higher plants, three mechanisms are proposed to supply the additional ATP: (1) cyclic electron flux around PSI (CEF), (2) the malate valve and (3) the Mehler reaction. All three of these mechanisms have received extensive coverage in past reviews [6,32–34], and so we will focus on their basic mechanisms and relevance to the particular focus of this perspective.

#### **4. Introduction to Supply-Side Mechanisms for Energy Balancing**

## *4.1. Cyclic Electron Flux around Photosystem I*

CEF contributes to the transthylakoid *pmf* without net production of NADPH by cycling electrons from photoexcited PSI via ferredoxin (Fd) back into the thylakoid plastoquinone (PQ) pool via the activity of Fd:PQ reductases (PQR) and the cytochrome *b6f* complex [35]. Aside from ATP generation, the proton gradient generated by CEF may also serve a photoprotective function by triggering qE ('energy dependent') NPQ, although CEF in itself is not essential for this process [8,36]. Many of the details of the electron transport pathways of CEF remain obscure. At least three PQR pathways have been postulated to function in CEF, which may operate in an organism-specific manner; (i) the antimycin A-sensitive Fd:PQ reductase (FQR), which has been proposed to be associated with the PGR5 and/or PGRL1 proteins [37–39], (but see [8,40–43] for additional viewpoints); (ii) the respiratory Complex I-like NADPH/Fd:PQ dehydrogenase (NDH) [44–47] and iii) direct reduction of *b6f*-bound PQ through Qi-associated FNR/Fd via *b6* hemes *bH*/*ci* [41,48–50]. Of these CEF pathways, those utilizing the proton motive NDH complex is likely to be the most energetically efficient, with a net H+/2e<sup>−</sup> ratio of 8 [46], with the PGR5/PGRL1 and *b6f* Qi pathways yielding an H+/2e<sup>−</sup> ratio of 4 by virtue of the (b6f-associated) Q-cycle alone [35].

The NDH pathway is, for the most part, associated with plant (and cyanobacterial) CEF, as this enzyme is absent from the majority of algal genera, although it should be noted that it is also absent from certain orchids, cacti and gymnosperms [51]. In general, the electron flux through CEF during steady-state photosynthesis in healthy, non-stressed C3 plants is considered to be small compared to LEF (i.e., -15%) [8,9,50], although it is likely to be (significantly) up-regulated during environmental stress like drought or during the induction of photosynthesis in dark-adapted plants, conditions under which increased ATP demand may be expected [48,52,53]. Nevertheless, this small flux is of vital importance for balancing the ATP and NADPH demands of metabolic supply and demand. Furthermore, CEF is likely to be of particular importance to C4 photosynthetic species and aquatic algae to generate ATP and proton/ion gradients necessary for the carbon-concentrating mechanisms of these organisms [46,54–56]
