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

Shimakawa, Ginga; Hanawa, Hitomi; Wada, Shin‐Ichiro; Hanke, Guy; Matsuda, Yusuke; Miyake, Chikahiro

doi:10.3389/fpls.2021.668805

Cited by 4 publications

(4 citation statements)

References 79 publications

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“…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).…”

Section: Part Ii: Mn Deficiency Affects the Photosynthetic Apparatus And May Favour Cyclic Electron Flowmentioning

confidence: 95%

Manganese excess and deficiency affects photosynthesis and metabolism in Marchantia polymorpha

Krieger‐Liszkay

Messant

Thomine

et al. 2022

Preprint

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Manganese is an essential metal for plant growth. The most important Mn-containing enzyme is the Mn4CaO5 cluster that catalyses water oxidation in Photosystem II. Mn deficiency primarily affects photosynthesis, while Mn excess is generally toxic. Mn excess and deficiency were studied in the liverwort Marchantia polymorpha, an emerging model ideally suited for analysis of metal stress since it accumulates rapidly toxic substances due to the absence of well-developed vascular and radicular systems and a reduced cuticle. We established growth conditions for Mn excess and deficiency, performed analysis of metal content in thalli and isolated chloroplasts and determined metabolites. Metabolome analysis revealed a strong accumulation of N-methylalanine upon exposure to Mn excess and a different response of Marchantia to heavy metal stress than that known for higher plants. We investigated photosynthetic performance by chlorophyll fluorescence at room temperature and at 77K, P700 absorption and by studying the susceptibility of thalli to photoinhibition. In vivo super-resolution fluorescence microscopy was used to visualize changes in the organization of the thylakoid membrane under Mn excess and deficiency. Non-optimal Mn concentrations changed the ratio of photosystem I to photosystem II and altered the organisation of thylakoid membranes. Mn deficiency seems to favour cyclic electron flow around photosystem I protecting thereby photosystem II against photoinhibition.

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Section: Part Ii: Mn Deficiency Affects the Photosynthetic Apparatus And May Favour Cyclic Electron Flowmentioning

confidence: 95%

Manganese excess and deficiency affects photosynthesis and metabolism in Marchantia polymorpha

Krieger‐Liszkay

Messant

Thomine

et al. 2022

Preprint

View full text Add to dashboard Cite

show abstract

“…Under both conditions, acceptor side limitation at the stromal side of PSI was not observed because Marchantia possesses flavodiiron proteins that use ferredoxin as electron donor to reduce oxygen to water (Shimakawa et al, 2021).…”

Section: Part Ii: Mn Deficiency Affects the Photosynthetic Apparatus ...mentioning

confidence: 99%

Manganese concentration affects chloroplast structure and the photosynthetic apparatus in Marchantia polymorpha

et al. 2023

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Manganese (Mn) is an essential metal for plant growth. The most important Mn-containing enzyme is the Mn4CaO5 cluster that catalyzes water oxidation in Photosystem II. Mn deficiency primarily affects photosynthesis, while Mn excess is generally toxic. Here, we studied Mn excess and deficiency in the liverwort Marchantia polymorpha, an emerging model ideally suited for analysis of metal stress since it accumulates rapidly toxic substances due to the absence of well-developed vascular and radicular systems and a reduced cuticle. We established growth conditions for Mn excess and deficiency and analyzed the metal content in thalli and isolated chloroplasts. In vivo super-resolution fluorescence microscopy and transmission electron microscopy revealed changes in the organization of the thylakoid membrane under Mn excess and deficiency. Both Mn excess and Mn deficiency increased the stacking of the thylakoid membrane. We investigated photosynthetic performance by measuring chlorophyll fluorescence at room temperature and 77 K, measuring P700 absorbance, and studying the susceptibility of thalli to photoinhibition. Non-optimal Mn concentrations changed the ratio of photosystem I to photosystem II. Upon Mn deficiency, higher non-photochemical quenching was observed, electron donation to photosystem I was favored, and photosystem II was less susceptible to photoinhibition. Mn deficiency seemed to favor cyclic electron flow around photosystem I, thereby protecting photosystem II in high light. The results presented here suggest an important role of Mn for the organization of the thylakoid membrane and photosynthetic electron transport.

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“…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.…”

Section: Regulatory Mechanisms To Suppress Ros Generationmentioning

confidence: 99%

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

Krieger‐Liszkay

Shimakawa

2022

Biochemical Society Transactions

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Light capture by chlorophylls and photosynthetic electron transport bury the risk of the generation of reactive oxygen species (ROS) including singlet oxygen, superoxide anion radicals and hydrogen peroxide. Rapid changes in light intensity, electron fluxes and accumulation of strong oxidants and reductants increase ROS production. Superoxide is mainly generated at the level of photosystem I while photosystem II is the main source of singlet oxygen. ROS can induce oxidative damage of the photosynthetic apparatus, however, ROS are also important to tune processes inside the chloroplast and participate in retrograde signalling regulating the expression of genes involved in acclimation responses. Under most physiological conditions light harvesting and photosynthetic electron transport are regulated to keep the level of ROS at a non-destructive level. Photosystem II is most prone to photoinhibition but can be quickly repaired while photosystem I is protected in most cases. The size of the transmembrane proton gradient is central for the onset of mechanisms that protect against photoinhibition. The proton gradient allows dissipation of excess energy as heat in the antenna systems and it regulates electron transport. pH-dependent slowing down of electron donation to photosystem I protects it against ROS generation and damage. Cyclic electron transfer and photoreduction of oxygen contribute to the size of the proton gradient. The yield of singlet oxygen production in photosystem II is regulated by changes in the midpoint potential of its primary quinone acceptor. In addition, numerous antioxidants inside the photosystems, the antenna and the thylakoid membrane quench or scavenge ROS.

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

Cited by 4 publications

References 79 publications

Manganese excess and deficiency affects photosynthesis and metabolism in Marchantia polymorpha

Manganese excess and deficiency affects photosynthesis and metabolism in Marchantia polymorpha

Manganese concentration affects chloroplast structure and the photosynthetic apparatus in Marchantia polymorpha

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

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