Physiological Roles of Flavodiiron Proteins and Photorespiration in the Liverwort Marchantia polymorpha

Abstract

Against the potential risk in oxygenic photosynthesis, that is, the generation of reactive oxygen species, photosynthetic electron transport needs to be regulated in response to environmental fluctuations. One of the most important regulations is keeping the reaction center chlorophyll (P700) of photosystem I in its oxidized form in excess light conditions. The oxidation of P700 is supported by dissipating excess electrons safely to O2, and we previously found that the molecular mechanism of the alternative electron sink is changed from flavodiiron proteins (FLV) to photorespiration in the evolutionary history from cyanobacteria to plants. However, the overall picture of the regulation of photosynthetic electron transport is still not clear in bryophytes, the evolutionary intermediates. Here, we investigated the physiological roles of FLV and photorespiration for P700 oxidation in the liverwort Marchantia polymorpha by using the mutants deficient in FLV (flv1) at different O2 partial pressures. The effective quantum yield of photosystem II significantly decreased at 2kPa O2 in flv1, indicating that photorespiration functions as the electron sink. Nevertheless, it was clear from the phenotype of flv1 that FLV was dominant for P700 oxidation in M. polymorpha. These data suggested that photorespiration has yet not replaced FLV in functioning for P700 oxidation in the basal land plant probably because of the lower contribution to lumen acidification, compared with FLV, as reflected in the results of electrochromic shift analysis.

Manganese excess and deficiency affects photosynthesis and metabolism in Marchantia polymorpha

“…These data further indicate a higher activity of cyclic electron flow under Mn-deficiency. Under both conditions, acceptor side limitation was not observed because Marchantia possesses flavodiiron proteins (Shimakawa et al, 2021).…”

Regulation of the generation of reactive oxygen species during photosynthetic electron transport

“…In green algae and cyanobacteria, O2 photoreduction to water, catalyzed by the flavodiiron enzymes, represents a significant electron transport activity (the optimal rate is almost comparable to the photosynthetic O2 evolution rate) and contributes to the ΔpH, alleviating ROS damage in PSI [63][64][65][66]. The electron flux via flavodiiron proteins is smaller but its physiological roles are still conserved in basal land plants, and finally lost in angiosperms in the evolutionary history [67,68]. The in vivo electron flux via the Mehler reaction (i.e., the non-enzymatic reduction of O2 to O2 •− in PSI) is smaller than that via flavodiiron proteins.…”

Flv3A facilitates O2 photoreduction and affects H2 photoproduction independently of Flv1A in diazotrophic Anabaena filaments

“…Environmental fluctuations in light and nutrient supply might result in the over‐reduction of the photosynthetic machinery. Alleviation of excessive reduction by class‐C flavodiiron proteins (hereafter FDP) has been described in all oxygenic photosynthetic organisms, apart from angiosperms, and red and brown algae (Helman et al ., 2003 ; Zhang et al ., 2009 ; Gerotto et al ., 2016 ; Chaux et al ., 2017 ; Ilík et al ., 2017 ; Jokel et al ., 2018 ; Alboresi et al ., 2019 ; Shimakawa et al ., 2021 ). These proteins act as strong electron outlets downstream of PSI by catalysing the photoreduction of O 2 into H 2 O (the Mehler‐like reaction) (Helman et al ., 2003 ; Allahverdiyeva et al ., 2013 , 2015 ; Santana‐Sánchez et al ., 2019 ).…”