Land plants drive photorespiration as higher electron‐sink: comparative study of post‐illumination transient O₂‐uptake rates from liverworts to angiosperms through ferns and gymnosperms

Abstract

In higher plants, the electron-sink capacity of photorespiration contributes to alleviation of photoinhibition by dissipating excess energy under conditions when photosynthesis is limited. We addressed the question at which point in the evolution of photosynthetic organisms photorespiration began to function as electron sink and replaced the flavodiiron proteins which catalyze the reduction of O at photosystem I in cyanobacteria. Algae do not have a higher activity of photorespiration when CO assimilation is limited, and it can therefore not act as an electron sink. Using land plants (liverworts, ferns, gymnosperms, and angiosperms) we compared photorespiration activity and estimated the electron flux driven by photorespiration to evaluate its electron-sink capacity at CO -compensation point. In vivo photorespiration activity was estimated by the simultaneous measurement of O -exchange rate and chlorophyll fluorescence yield. All C3-plants leaves showed transient O -uptake after actinic light illumination (post-illumination transient O -uptake), which reflects photorespiration activity. Post-illumination transient O -uptake rates increased in the order from liverworts to angiosperms through ferns and gymnosperms. Furthermore, photorespiration-dependent electron flux in photosynthetic linear electron flow was estimated from post-illumination transient O -uptake rate and compared with the electron flux in photosynthetic linear electron flow in order to evaluate the electron-sink capacity of photorespiration. The electron-sink capacity at the CO -compensation point also increased in the above order. In gymnosperms photorespiration was determined to be the main electron-sink. C3-C4 intermediate species of Flaveria plants showed photorespiration activity, which intermediate between that of C3- and C4-flaveria species. These results indicate that in the first land plants, liverworts, photorespiration started to function as electron sink. According to our hypothesis, the dramatic increase in partial pressure of O in the atmosphere about 0.4 billion years ago made it possible to drive photorespiration with higher activity in liverworts.

Changing frequency of fluctuating light reveals the molecular mechanism for P700 oxidation in plant leaves

“…On the acceptor side, photosynthetic CO 2 assimilation and dependent alternative electron transport function as electron sinks, thereby contributing to P700 oxidation. In C 3 plants, the flux of electrons to O 2 is mainly driven by photorespiration (Hanawa et al., ; Sejima et al., ; Wiese, Shi, & Heber, ). Even although photorespiration is the largest alternative electron sink in land plants (except for C 4 plants; Hanawa et al., ), it is not used as the main alternative electron sink by many prokaryotic and eukaryotic algae (Hayashi et al., ; Shimakawa et al., ; Shimakawa, Akimoto et al., ; Shimakawa, Matsuda et al., ).…”

“…In C 3 plants, the flux of electrons to O 2 is mainly driven by photorespiration (Hanawa et al., ; Sejima et al., ; Wiese, Shi, & Heber, ). Even although photorespiration is the largest alternative electron sink in land plants (except for C 4 plants; Hanawa et al., ), it is not used as the main alternative electron sink by many prokaryotic and eukaryotic algae (Hayashi et al., ; Shimakawa et al., ; Shimakawa, Akimoto et al., ; Shimakawa, Matsuda et al., ). Cyanobacteria, which are the ancestors of chloroplasts in land plants, use flavodiiron proteins (FLV) to mediate electron flow to O 2 , instead of photorespiration (Helman, Barkan, Eisenstadt, Luz, & Kaplan, ; Helman et al., ; Shimakawa et al., ), and to alleviate photo‐oxidative damage (Allahverdiyeva et al., ; Shimakawa, Shaku et al., ; Zhang, Allahverdiyeva, Eisenhut, & Aro, ).…”

PROTON GRADIENT REGULATION 5 supports linear electron flow to oxidize photosystem I

“…H + ‐influx regulation involving CEF‐PSI, and H + ‐efflux regulation involving ATP synthase are proposed to stimulate the lumenal acidification (Munekage et al , Shikanai , DalCorso et al , Takagi et al ). At the acceptor side of PSI, photorespiration contributes to the extraction of electrons from PSI in land plants (Takagi et al , , Hanawa et al ). In gymnosperms, ferns, mosses, and liverworts, the flavodiiron protein also functions to oxidize PSI (Shimakawa et al , , Takagi et al ).…”

“…1). As PSI acceptor side regulation, photorespiration consumes excess electrons from PSI when the CO 2 fixation reaction is limited, and reduces the risk of ROS production within PSI (Takagi et al 2016b, Hanawa et al 2017. The flavodiiron protein also efficiently consumes electrons in PSI in gymnosperms, ferns, mosses, and liverworts (Gerotto et al 2016, Shimakawa et al 2016, Takagi et al 2017a.…”

From light capture to metabolic needs, oxygenic photosynthesis is an ever‐expanding field of study in plants, algae and cyanobacteria

“…The discovery of their enzymatic function, which possibly corresponds to the historical Mehler reaction, opened a new field of investigation, especially with respect to PSI photoprotection. The increasing importance of photorespiration in species lacking flavodiiron enzymes during evolution is shown in the article by Hanawa et al (2017).…”