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

Abstract

Contents Summary 105 I. Introduction 105 II. Diversity of molecular mechanisms for regulation of photosynthetic electron transport 106 III. Role of FLVs in the regulation of photosynthesis in eukaryotes 107 IV. Why were FLVs lost in angiosperms? 108 V. Conclusions 108 Acknowledgements 109 References 109 SUMMARY: Photosynthetic electron transport requires continuous modulation to maintain the balance between light availability and metabolic demands. Multiple mechanisms for the regulation of electron transport have been identified and are unevenly distributed among photosynthetic organisms. Flavodiiron proteins (FLVs) influence photosynthetic electron transport by accepting electrons downstream of photosystem I to reduce oxygen to water. FLV activity has been demonstrated in cyanobacteria, green algae and mosses to be important in avoiding photosystem I overreduction upon changes in light intensity. FLV-encoding sequences were nevertheless lost during evolution by angiosperms, suggesting that these plants increased the efficiency of other mechanisms capable of accepting electrons from photosystem I, making the FLV activity for protection from overreduction superfluous or even detrimental for photosynthetic efficiency.

Role of cyclic and pseudo‐cyclic electron transport in response to dynamic light changes in Physcomitrella patens

“…Regulation of electron transport in photosynthetic organisms is seminal to maintain the balance between light availability and metabolic demands in a highly dynamic environment. Multiple mechanisms such as CEF around PSI and PCEF pathways capable to divert/feed electrons from/to linear transport chain have been identified unevenly distributed in photosynthetic organisms (Alboresi, Storti, & Morosinotto, ; Shikanai, ; Shikanai & Yamamoto, ).…”

“…On the contrary, overreduced PSI is instead prone to light damage to Fe‐S clusters present on the stromal side of the protein complex (Sonoike, Terashima, Iwaki, & Itoh, ; Tiwari et al, ). To avoid this phenomenon, other mechanisms capable of accepting electron from PSI are still present and likely active in flva pgrl1 KO plants (e.g., NDH‐dependent cyclic electron transport or the Mehler reaction, whose corresponding genes are present in P. patens genome; Alboresi et al, ; Kato, Odahara, Fukao, & Shikanai, ). The photorespiration pathway uses ATP and reducing power to regenerate ribulose‐1,5‐bisphosphate (RuBP) from 2‐phosphoglycolate, and it has also been demonstrated to represent a significant electron sink in bryophytes like mosses (Aro, Gerbaud, & André, ) or liverworts (Hanawa et al, ).…”

Oxidation of P700 Ensures Robust Photosynthesis

“…), in which P700 is rapidly oxidized in response to light exposure in the presence of O 2 to alleviate PSI photoinhibition ( Allahverdiyeva et al, 2013 ; Shirao et al, 2013 ; Roberty et al, 2014 ; Gerotto et al, 2016 ; Shimakawa et al, 2016b , 2017a ; Chaux et al, 2017 ; Ilík et al, 2017 ; Noridomi et al, 2017 ; Takagi et al, 2017b ). Interestingly, angiosperms have lost FLV at the genetic level ( Allahverdiyeva et al, 2015 ; Yamamoto et al, 2016 ; Alboresi et al, 2018 ). Most importantly, P700 oxidation, but not FLV, is essential for oxygenic photoautotrophs to protect PSI against photoinhibition ( Shimakawa et al, 2016b ).…”

Photosynthesis Regulation in Response to Fluctuating Light in the Secondary Endosymbiont Alga Nannochloropsis gaditana

“…Mechanisms for the regulation of electron transport have been shown to be relevant for the protection of PSI from light fluctuations in plants, algae and cyanobacteria. Two molecular mechanisms in particular have been identified to play a significant role in light fluctuations: cyclic electron transport dependent on PGR5/PGRL1 and pseudocyclic electron transport dependent on FLV (Alboresi et al, 2019;Yamori and Shikanai, 2016). The N. gaditana genome was therefore analyzed to assess the presence of these proteins, comparing the results with sequences from other species.…”

“…Photochemical reactions are conserved in all organisms performing oxygenic photosynthesis, while regulatory mechanisms are diversified in various phylogenetic groups (Alboresi et al, 2019;Eberhard et al, 2008), likely as a result of adaptation to different environmental niches. The investigation of the biological role of the regulatory mechanisms of photosynthesis in diverse organisms can therefore complement the information obtained from the characterization of specific mutants.…”