Regulation of photosynthetic cyclic electron flow pathways by adenylate status in higher plant chloroplasts

• Published in: Biochimica et biophysica acta. Bioenergetics Vol. 1860; no. 11; p. 148081
• Main Authors: Fisher, Nicholas, Bricker, Terry M., Kramer, David M.
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier B.V 01.11.2019; Elsevier
• Subjects: Adenosine Diphosphate - metabolism; Adenosine Triphosphate - metabolism; Amaranthus; Arabidopsis; BASIC BIOLOGICAL SCIENCES; Chloroplasts - metabolism; Cyclic electron flow; Electrons; Enzymology; NADH Dehydrogenase - metabolism; NADP - metabolism; Photosynthesis; Photosynthesis - physiology; Plant Proteins - metabolism; Regulation; Spinacia oleracea; Cyclic electron flow; Regulation; Photosynthesis; Enzymology
• ISSN: 0005-2728; 1879-2650
• DOI: 10.1016/j.bbabio.2019.148081

Cylic electron flow (CEF) around Photosystem I in photosynthetic eukaryotes is likely to be necessary to augment ATP production, rapidly- and precisely balancing the plastid ATP/NADPH energy budget to meet the demands of downstream metabolism. Many regulatory aspects of this process are unclear. Here we demonstrate that the higher plant plastid NADH/Fd:plastoquinone reductase (NDH) and proposed PGR5/PGRL1 ferredoxin:plastoquinone reductase (FQR) pathways of CEF are strongly, rapidly and reversibly inhibited in vitro by ATP with Ki values of 670 μM and 240 μM respectively, within the range of physiological changes in ATP concentrations. Control experiments ruled out effects on secondary reactions, e.g. FNR- and cytochrome b6f activity, nonphotochemical quenching of chlorophyll fluorescence etc., supporting the view that ATP is an inhibitor of CEF and its associated pmf generation and subsequent ATP production. The effects are specific to ATP, with the ATP analog AMP-PNP showing little inhibitory effect, and ADP inhibiting only at higher concentrations. For the FQR pathway, inhibition was found to be classically competitive with Fd, and the NDH pathway showing partial competition with Fd. We propose a straightforward model for regulation of CEF in plants in which CEF is activated under conditions when stromal ATP low, but is downregulated as ATP levels build up, allowing for effective ATP homeostasis. The differences in Ki values suggest a two-tiered regulatory system, where the highly efficient proton pumping NDH is activated with moderate decreases in ATP, with the less energetically-efficient FQR pathway being activated under more severe ATP depletion. •Regulation of cyclic photophosphorylation in plant chloroplasts was investigated.•ATP acts as competitive inhibitor for ferredoxin in the NDH and FQR/PGR5 pathways.•The FQR/PGR5 pathway is more sensitive to adenylate inhibition than NDH.•The more energetically-efficient (NDH) pathway is less sensitive to ATP depletion.