The Liverwort, Marchantia, Drives Alternative Electron Flow Using a Flavodiiron Protein to Protect PSI

Abstract

The diffusion efficiency of oxygen in the atmosphere, like that of CO 2 , is approximately 10 4 times greater than that in aqueous environments. Consequently, terrestrial photosynthetic organisms need mechanisms to protect against potential oxidative damage. The liverwort Marchantia polymorpha, a basal land plant, has habitats where it is exposed to both water and the atmosphere. Furthermore, like cyanobacteria, M. polymorpha has genes encoding flavodiiron proteins (FLV). In cyanobacteria, FLVs mediate oxygen-dependent alternative electron flow (AEF) to suppress the production of reactive oxygen species. Here, we investigated whether FLVs are required for the protection of photosynthesis in M. polymorpha. A mutant deficient in the FLV1 isozyme (DMpFlv1) sustained photooxidative damage to photosystem I (PSI) following repetitive short-saturation pulses of light. Compared with the wild type (Takaragaike-1), DMpFlv1 showed the same photosynthetic oxygen evolution rate but a lower electron transport rate during the induction phase of photosynthesis. Additionally, the reaction center chlorophyll in PSI, P700, was highly reduced in DMpFlv1 but not in Takaragaike-1. These results indicate that the gene product of MpFlv1 drives AEF to oxidize PSI, as in cyanobacteria. Furthermore, FLV-mediated AEF supports the production of a proton motive force to possibly induce the nonphotochemical quenching of chlorophyll fluorescence and suppress electron transport in the cytochrome b 6 /f complex. After submerging the thalli, a decrease in photosystem II operating efficiency was observed, particularly in DMpFlv1, which implies that species living in these sorts of habitats require FLV-mediated AEF.

Diversity of strategies for escaping reactive oxygen species production within photosystem I among land plants: P700 oxidation system is prerequisite for alleviating photoinhibition in photosystem I

“…In addition to this, Flvs functions to release electrons from PSI in cyanobacteria (Shimakawa et al ). In land plants, liverworts and mosses also have functional Flv protein to stimulate the oxidation of P700 (Gerotto et al , Shimakawa et al ). In the present study, we have extended the importance of Flv protein in ferns and gymnosperms for immediate oxidation of P700 against a sudden over‐accumulation of electrons in photosynthetic electron transport chain.…”

“…The fully expanded leaves of 3‐ to 4‐week‐old plants were used for physiological measurements. Meanwhile, WT and Δ flv liverwort ( Marchantia polymorpha ) were also analyzed (Shimakawa et al ). A male accession of M .…”

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

“…In addition, Takagi et al (2016) found that the production of ROS such as superoxide and singlet oxygen is suppressed when P700 is kept in its oxidized form (P700 + ). In fact, the oxidation of P700 has been frequently observed in the photosynthetic organisms as a physiological response to excessive light conditions (Klughammer and Schreiber, 1994;Golding and Johnson, 2003;Shimakawa et al, 2017). Thus, P700 oxidation may lead to the alleviation of PSI photodamage by ROS in the thylakoid membranes.…”

Flavodiiron Proteins Promote Fast and Transient O2 Photoreduction in Chlamydomonas

“…While the role of Flv in driving O 2 photoreduction in a photosynthetic organism has been first demonstrated in cyanobacteria (Helman et al, 2003), recent studies performed in the moss P. patens (Gerotto et al, 2016) and liverwort (Shimakawa et al, 2017), and mainly based on chlorophyll fluorescence measurements, concluded that Flv drive alternative electron flow and protect PSI particularly under fluctuating light. However, there was no experimental evidence until now of an Flv-catalyzed O 2 photoreduction in microalgae (Curien et al, 2016).…”

“…Based on the accumulation of Flv proteins in a Chlamydomonas reinhardtii mutant (pgrl1) lacking photosynthetic control due to a deficiency in CEF, it was suggested that Flvs are induced to catalyze O 2 photoreduction when PSI acceptors are overreduced (Dang et al, 2014). More recently, Flv mutants have been characterized in the moss Physcomitrella patens (Gerotto et al, 2016) and in the liverwort Marchantia (Shimakawa et al, 2017), showing that these proteins are involved in alternative electron flow and are required for growth of the moss under fluctuating light. However, so far there is no experimental evidence for a Flv-mediated oxygen photoreduction in eukaryotic microalgae (Curien et al, 2016).…”