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

Fisher, Nicholas; Bricker, Terry M.; Kramer, David M.

doi:10.1016/j.bbabio.2019.148081

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

Journal Article · Fri Nov 01 00:00:00 EDT 2019 · Biochimica et Biophysica Acta - Bioenergetics

DOI:https://doi.org/10.1016/j.bbabio.2019.148081· OSTI ID:1703107

Fisher, Nicholas; Bricker, Terry M.; Kramer, David M.

Cylic electron flow (CEF) around Photosystem I in photosynthetic eukaryotes is anticipated 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. In this work, 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 K_i 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 K_i 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.

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Research Organization:: Louisiana State Univ., Baton Rouge, LA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division

Grant/Contract Number:: FG02-98ER20310; FG02-91ER20021

OSTI ID:: 1703107

Alternate ID(s):: OSTI ID: 1593968

Journal Information:: Biochimica et Biophysica Acta - Bioenergetics, Journal Name: Biochimica et Biophysica Acta - Bioenergetics Vol. 1860 Journal Issue: 11; ISSN 0005-2728

Publisher:: ElsevierCopyright Statement

Country of Publication:: Netherlands

Language:: English

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Cited by: 15 works

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

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