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Alternative Outlets for Sustaining Photosynthetic Electron Transport During Dark-To-Light Transitions

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Alternative Outlets for Sustaining Photosynthetic Electron Transport During Dark-To-Light Transitions Alternative outlets for sustaining photosynthetic electron transport during dark-to-light transitions Shai Saroussia,1, Devin A. J. Karnsb, Dylan C. Thomasb, Clayton Blosziesc, Oliver Fiehnc, Matthew C. Posewitzb, and Arthur R. Grossmana,1 aDepartment of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305; bDepartment of Chemistry and Geochemistry, Colorado School of Mines, Golden, CO 80401; and cWest Coast Metabolomics Center, University of California, Davis, CA 95616 Edited by Bob B. Buchanan, University of California, Berkeley, CA, and approved April 22, 2019 (received for review March 4, 2019) Environmental stresses dramatically impact the balance between that ultimately couples the products of the light reactions with the production of photosynthetically derived energetic electrons downstream C metabolism. An efficient coupling promotes cell and Calvin–Benson–Bassham cycle (CBBC) activity; an imbalance growth and division as well as the storage of energy-rich, organic promotes accumulation of reactive oxygen species and causes cell polymers. However, environmental fluctuations in light, nutrient damage. Hence, photosynthetic organisms have developed several availability, and other abiotic factors may create an imbalance strategies to route electrons toward alternative outlets that allow between the products of the photosynthetic light reactions and for storage or harmless dissipation of their energy. In this work, their utilization by the CBBC. Under such circumstances, the we explore the activities of three essential outlets associated with overflow of energetic electrons generated by photosystem I (PSI) Chlamydomonas reinhardtii i photosynthetic electron transport: ( ) and PSII can be photochemically quenched via a number of O2- reduction of O2 to H2O through flavodiiron proteins (FLVs) and (ii) reducing pathways that occur within chloroplasts; some of these iii plastid terminal oxidases (PTOX) and ( ) the synthesis of starch. reactions have been designated H2O-to-H2O (water-to-water) Real-time measurements of O2 exchange have demonstrated that cycles (4, 5). The H2O-to-H2O “electron outlets” include Mehler- FLVs immediately engage during dark-to-light transitions, allow- type reactions (6, 7), in which O2 is directly reduced by electrons to ing electron transport when the CBBC is not fully activated. Under form H2O on the acceptor side of PSI, a process that can also result these conditions, we quantified maximal FLV activity and its over- in the generation of reactive oxygen species (ROS). Electrons can all capacity to direct photosynthetic electrons toward O2 reduc- also be dissipated through a PSI-dependent enzymatic reaction PLANT BIOLOGY tion. However, when starch synthesis is compromised, a greater catalyzed by specific heterodimeric flavodiiron proteins (FLVs, proportion of the electrons is directed toward O2 reduction NADPH:flavin oxidoreductase) that directly reduce O2 to H2O through both the FLVs and PTOX, suggesting an important role without the release of ROS (8–10) (Fig. 1). Mutant organisms for starch synthesis in priming/regulating CBBC and electron trans- unable to synthesize FLVs exhibit compromised growth when ex- port. Moreover, partitioning energized electrons between sustain- posed to fluctuating light as a result of oxidative damage caused by able (starch; energetic electrons are recaptured) and nonsustainable ROS accumulation and a decline in PSI activity (8–11). Moreover, (H2O; energetic electrons are not recaptured) outlets is part of the FLVs can prime PSII electron flow, O2 evolution, and lumen energy management strategy of photosynthetic organisms that al- acidification under conditions in which the CBBC enzymes are not lows them to cope with the fluctuating conditions encountered in fully activated (8, 12). Chlororespiration represents an additional nature. Finally, unmasking the repertoire and control of such ener- outlet in which electrons of quinols in the plastoquinone (PQ) pool getic reactions offers new directions for rational redesign and opti- mization of photosynthesis to satisfy global demands for food and Significance other resources. Most forms of life on Earth cannot exist without photosynthesis. photosynthesis | starch metabolism | alternative electron outlets | Our food and atmosphere depend on it. To obtain high photo- FLV | PTOX synthetic yields, light energy must be efficiently coupled to the fixation of CO2 into organic molecules. Suboptimal environ- hotosynthetic organisms evolved the capacity to transform mental conditions can severely impact the conversion of light Psolar energy to chemical bond energy stored in C backbones energy to biomass and lead to reactive oxygen production, that fuel most biosynthetic processes. The photosynthetic “light which in turn can cause cellular damage and loss of productivity. reactions” drive the oxidation of water by photosystem II (PSII) Hence, plants, algae, and photosynthetic bacteria have evolved a and both linear photosynthetic electron flow and cyclic photo- network of alternative outlets to sustain the flow of photosyn- synthetic electron flow (CEF) that ultimately generate ATP, thetically derived electrons. Our work is focused on the nature NADPH, and other reduced electron carriers, including ferre- and integration of these outlets, which will inform a rational doxins and thioredoxins (Fig. 1); these compounds support the engineering of crop plants and algae to optimize photosynthesis energetic demands of most cellular processes. While light-driven and meet the increased global demand for food. electron transport can be described as an energy generator, a second set of photosynthetic reactions that comprise the Calvin– Author contributions: S.S., M.C.P., and A.R.G. designed research; S.S., D.A.J.K., D.C.T., and Benson–Bassham cycle (CBBC) utilizes the ATP and NADPH C.B. performed research; O.F. and M.C.P. contributed new reagents/analytic tools; S.S., D.A.J.K., C.B., O.F., and A.R.G. analyzed data; and S.S. and A.R.G. wrote the paper with for the fixation of CO2 into simple phosphorylated organic C input from all other coauthors. compounds such as glyceraldehyde 3-phosphate (G3P) and The authors declare no conflict of interest. fructose 6-phosphate (F6P). Some CBBC enzymes are indirectly This article is a PNAS Direct Submission. activated by light through a redox switch controlled by thio- This open access article is distributed under Creative Commons Attribution-NonCommercial- redoxin. Hence, before activation, photosynthetic electron transport NoDerivatives License 4.0 (CC BY-NC-ND). (PET) and C metabolism are not optimally coupled. Full activation 1To whom correspondence may be addressed. Email: [email protected] or of CBBC enzymes during a dark-to-light transition, which can in- [email protected]. crease their activities by up to 40-fold, can take 2 to 3 min (1–3). This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. The anabolic use of photosynthetically derived electrons and 1073/pnas.1903185116/-/DCSupplemental. ATP is governed by an extensive network of integrated reactions www.pnas.org/cgi/doi/10.1073/pnas.1903185116 PNAS Latest Articles | 1of10 Downloaded by guest on September 29, 2021 as low nutrient availability (refs. 35 and 36 and reviewed in ref. 37). The pathway for starch synthesis requires several enzymes, as shown in Fig. 1 (reviewed in ref. 38) and is fueled by ATP derived primarily from photosynthesis and C backbones synthe- sized by the CBBC. The rate-limiting step in starch synthesis involves the enzyme ADP glucose pyrophosphorylase (AGPase, encoded by the STA6 locus) which uses ATP to convert glucose- 1-phosphate (G1P) to ADP-glucose while releasing pyrophos- phate (PPi) (Fig. 1). In the last few decades, various Chlamy- domonas “starchless” mutants have been isolated and characterized (38). One such mutant, disrupted for the gene encoding AGPase (designated sta6), accumulates no detectable starch (38, 39). The sta6 mutant also exhibited a marked re- duction in photosynthetic capacity, although the mechanism underlying this phenomenon remains speculative (40, 41) We have begun to appreciate the critical nature of the light- driven reduction of O2 for cell survival. However, we still know Fig. 1. Integration of photosynthetic light reactions and C metabolism. The little about how these electron-consuming pathways are co- light reactions include the reaction center/electron transport components PSI ordinated with PET, CBBC activity, and the activity of other C and PSII (green), cytochrome b6f (b6f) (orange), and ATP synthase (blue), with assimilatory/storage pathways like starch metabolism. In this CBBC (cycle, Upper Right) and starch biosynthesis (pathway, Upper Left)using work, we explore the dynamics of alternative electron outlets the products of these reactions. Metabolites: G3P, glyceraldehyde 3-phosphate; during dark-to-light transitions, a situation in which PET is not F6P, fructose 6-phosphate; G6P, glucose 6-phosphate; G1P, glucose 1-phos- optimally integrated with downstream C metabolism (the CBBC phate. C metabolism-related enzymes are highlighted in gold filled rectangles (Rubisco, ribulose bisphosphate carboxylase oxygenase; PGM, phosphogluco- requires minutes to become activated upon exposure to light) mutase; SS, starch synthase). Other enzymes/electron transfer components are (2). We demonstrate the importance of starch synthesis as a PC, plastocyanin (gray-filled circle, involved in transferring electrons
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