Cyclic electron flow inChlamydomonas reinhardtii

Abstract

Abstract:Cyclic electron flow (CEF), one of the major alternative electron transport pathways to the primary linear electron flow (LEF) in chloroplasts has been discovered in the middle of the last century. It is defined as a return of the reductants from the acceptor side of the Photosystem I (PSI) to the pool of its donors via the cytochrome b 6 f, and has proven essential for photosynthesis. However, despite many efforts aimed at its characterisation, the pathway and regulation of CEF remain equivocal, and its physiological significance remains to be properly defined. Here we use novel spectroscopic approaches to measure CEF in transitory conditions in the green alga Chlamydomonas reinhardtii. We show that CEF operates at the same maximal rate regardless of the oxygen concentration, and that the latter influences LEF, rather than CEF in vivo, which questions the recent hypotheses about the CEF supercomplex formation. We further reveal that the pathways proposed for CEF in the literature are inconsistent with the kinetic information provided by our measurements. We finally provide cues on the regulation of CEF by light.

The multiple routes of photosynthetic electron transfer in Chlamydomonas reinhardtii

“…This latter hypothesis is supported by higher rates of CEF measured in anoxic conditions, where the reducing power generated by glycolysis in the chloroplast maintain reducing pressure on the PETC. In these conditions (DCMU and anoxia), rates as high as 60 electrons per second per PSI were measured (Alric et al, 2010), which were further corroborated during the first seconds following a dark-to-light transition in the absence of DCMU (Nawrocki et al, 2019b).…”

“…This discrepancy could stem from a different redox state of the stromal reductants in the two experiments: the rate of NDA2 would be limited by the availability of NAD(P)H in oxic conditions. In Chlamydomonas, PGRL1 mutants were shown to exhibit transiently the same maximal CEF rate as wildtype (Nawrocki et al, 2019b). This was also the case in PGR5 mutants of Arabidopsis where the CEF maximal rate was not affected compared to the wild type (Nandha et al, 2007).…”

“…To evaluate the physiological importance of the CEF around PSI, the value of the maximal rate of CEF, relatively to the maximal rate of the LEF, has been a long-lasting question. In Chlamydomonas, the maximal rate of LEF is usually in the 100-150 electron per second per photosystem Biggins 1976, Alric, 2010;Nawrocki et al, 2019b). In the presence of DCMU, the rate of P700 + re-reduction at the offset of a saturating light was used as a direct measure of the rate of CEF and provided typical values of 5-15 electrons per second per PSI in oxic conditions (Maxwell & Biggins, 1976, Alric et al, 2010Takahashi et al, 2013).…”

The labile interactions of cyclic electron flow effector proteins

“…Based on our current observations, we favor the concept proposed by Joliot et al (15), where Cyt-b 6 f-associated FNR (13,14) facilitates the reinjection of electrons at the Q i site via heme c i . During this process, the CEF effectors PGR5/ PGRL1 and ANR1/PETO likely play FNR-coordinating (58) and Fd-coordinating roles (55,56) that are functionally redundant because none of the single knockout/knockdown strains is truly CEF-impaired (12,22,23,63).…”

“…Another pathway, the PGR-dependent CEF, involves the proteins proton gradient regulation 5 (PGR5) and pgr5-like photosynthetic phenotype 1 (PGRL1), which has been proposed to have a ferredoxin-PQ oxidoreductase activity (9 -11). However, a PGRL1-defective mutant of Chlamydomonas is still capable of high rates of CEF (12). Thus, a third route, still awaiting further documentation, involves direct electron donation through the ferredoxin-NADP ϩ oxidoreductase (FNR) bound to Cyt-b 6 f, making use of heme c i next to the PQ binding site Q i (8,(13)(14)(15).…”