Alternative electron transport mediated by flavodiiron proteins is operational in organisms from cyanobacteria up to gymnosperms

Abstract

Photo-reduction of O to water mediated by flavodiiron proteins (FDPs) represents a safety valve for the photosynthetic electron transport chain in fluctuating light. So far, the FDP-mediated O photo-reduction has been evidenced only in cyanobacteria and the moss Physcomitrella; however, a recent phylogenetic analysis of transcriptomes of photosynthetic organisms has also revealed the presence of FDP genes in several nonflowering plant groups. What remains to be clarified is whether the FDP-dependent O photo-reduction is actually operational in these organisms. We have established a simple method for the monitoring of FDP-mediated O photo-reduction, based on the measurement of redox kinetics of P700 (the electron donor of photosystem I) upon dark-to-light transition. The O photo-reduction is manifested as a fast re-oxidation of P700. The validity of the method was verified by experiments with transgenic organisms, namely FDP knock-out mutants of Synechocystis and Physcomitrella and transgenic Arabidopsis plants expressing FDPs from Physcomitrella. We observed the fast P700 re-oxidation in representatives of all green plant groups excluding angiosperms. Our results provide strong evidence that the FDP-mediated O photo-reduction is functional in all nonflowering green plant groups. This finding suggests a major change in the strategy of photosynthetic regulation during the evolution of angiosperms.

Cyclic electron flow inChlamydomonas reinhardtii

“…We were then able to exclude that initial redox state of the PQ pool or PSI acceptors was the reason for a lag in PSI photochemistry in hypoxia, but rather that it was the suppression of oxygen-reducing reactions which caused CEF enhancement. The recent discovery of flavo-diiron proteins (Flvs) in Chlamydomonas (47,48) is consistent with these observations -especially given that Flvs are absent in angiosperms where the PSI oxidation lag in the presence of DCMU is lengthy (26). We exclude the involvement of the Mehler reaction -a direct oxygen reduction by the F A /F B ISCs -because it is not sensitive to oxygen in our range of concentrations.…”

“…Consequently, competition between CEF and LEF for reduced Fd is in our view the hub where those two pathways necessitate regulatory actions. As outlined before, Fd red can be readily oxidized by the CBB cycle and apart from plants, by flavodiiron proteins (47). Such oxidation was shown here to be decreased in low oxygen concentrations, and an increase of the duration of CEF also observed in Flv mutant of moss (51), yet it was interpreted as a compensatory increase in CEF rather than a decrease of the electron leak.…”

Balancing protection and efficiency in the regulation of photosynthetic electron transport across plant evolution

“…FLVs are instead more unevenly distributed, with up to six genes found in cyanobacteria (Zhang et al ., ) involved in the photoprotection of both PSI and PSII (Allahverdiyeva et al ., ). Eukaryotic photosynthetic organisms have maintained only two genes (named FLVA and FLVB ), and molecular evidence of FLV activity has recently emerged in chlorophyte algae (Jokel et al ., ; Chaux et al ., ), nonvascular plants (Gerotto et al ., ; Shimakawa et al ., ) and gymnosperms (Ilík et al ., ), whereas the corresponding genes are not found in any known angiosperm (Fig. ).…”

Flavodiiron Protein Substitutes for Cyclic Electron Flow without Competing CO2 Assimilation in Rice

“…An FLV2/FLV4 heterodimer, which occurs exclusively in b-cyanobacteria, functions in the photoprotection of PSII (Zhang et al, 2009, Bersanini et al, 2014. Genes homologous to cyanobacterial FLV1 and FLV3 and the O 2 photoreduction activities in response to abrupt strong illumination are found in other photosynthetic organisms such as green algae and upland plants from bryophyta to gymnosperms (Ilík et al, 2017). FLVdeficient strains of Chlamydomonas reinhardtii, a green alga, and Physcomitrella patens, a moss, experience photodamage to PSI and reduced growth under fluctuating light.…”