Flexibility in the Energy Balancing Network of Photosynthesis Enables Safe Operation under Changing Environmental Conditions

Abstract

Given their ability to harness chemical energy from the sun and generate the organic compounds necessary for life, photosynthetic organisms have the unique capacity to act simultaneously as their own power and manufacturing plant. This dual capacity presents many unique challenges, chiefly that energy supply must be perfectly balanced with energy demand to prevent photodamage and allow for optimal growth. From this perspective, we discuss the energy balancing network using recent studies and a quantitative framework for calculating metabolic ATP and NAD(P)H demand using measured leaf gas exchange and assumptions of metabolic demand. We focus on exploring how the energy balancing network itself is structured to allow safe and flexible energy supply. We discuss when the energy balancing network appears to operate optimally and when it favors high capacity instead. We also present the hypothesis that the energy balancing network itself can adapt over longer time scales to a given metabolic demand and how metabolism itself may participate in this energy balancing.

Features of the Duckweed Lemna That Support Rapid Growth under Extremes of Light Intensity

“…Nevertheless, our result that either F v /F m × q P or xanthophyll cycle pool conversion correlated closely with the light-use efficiency of plant productivity in duckweed is consistent with the assumption that the activity of any additional dissipative processes varies in proportion with the regulated non-photochemical dissipation of excitation energy associated with de-epoxidized xanthophyll cycle components in this species. Future research should examine a possible involvement of alternative photochemical sinks for excitation energy (other than carbon fixation [54]; see also [55,56]) such as oxygen reduction by electron transport, photorespiration, and nitrogen reduction (especially by plastid nitrite reductase). In Lemna, nitrogen reduction could be of interest because of the demonstrated enrichment in the duckweed genome of core enzymes in amino acid synthesis [34] and the propensity of duckweed to produce vegetative storage protein.…”

The roles of photorespiration and alternative electron acceptors in the responses of photosynthesis to elevated temperatures in cowpea

“…The light and assimilatory reactions are tightly co‐regulated to balance the needs for efficient energy capture, while balancing energy storage into ATP and NADPH to meet the needs of downstream metabolic reactions and prevent the accumulation of reactive intermediates that can lead to photodamage (Kramer & Evans, 2011; Walker, Kramer, Fisher, & Fu, 2020). The thylakoid proton motive force ( pmf ) plays a central role in this co‐regulatory network (Avenson et al, 2005; Kanazawa & Kramer, 2002).…”

The flexibility of metabolic interactions between chloroplasts and mitochondria in Nicotiana tabacum leaf

“…As outlined below, chloroplasts exhibit a number of processes that may act, at least in part, to adjust the production ratio of ATP to NADPH dynamically, and/or prevent a build‐up of electrons in the cETC. Such processes are potentially important to prevent both metabolic bottlenecks and photodamage (Kramer and Evans, 2011; Walker et al , 2020).…”

“…Of particular interest is the relative contribution of the above pathways of electron flow (Mehler reaction, malate valve, CET, PTOX) to the ΔpH‐dependent regulation of electron flow and/or balancing of the chloroplast ATP/NADPH budget under different metabolic and environmental conditions (Backhausen et al , 2000; Kramer and Evans, 2011). CET and the malate valve are the paths that probably have quantitatively prominent roles in this regard (Walker et al , 2020). Between these paths, the malate valve is one that probably depends upon a direct interaction between the chloroplast and mitochondrion.…”