Probing the biogenesis pathway and dynamics of thylakoid membranes

Huokko, Tuomas; Ni, Tao; Dykes, Gregory F.; Simpson, Deborah M.; Brownridge, Philip; Conradi, Fabian D.; Beynon, Robert J.; Nixon, Peter J.; Mullineaux, Conrad W.; Zhang, Peijun; Liu, Luning

doi:10.1101/2021.05.05.442711

Cited by 4 publications

(6 citation statements)

References 81 publications

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“…Cyanobacterial thylakoid membranes are structurally heterogeneous and highly dynamic, and are formed in vivo following stepwise biogenesis pathways ( Liu, 2016 ; Mullineaux and Liu, 2020 ; Huokko et al, 2021 ; Zabret et al, 2021 ; Zhang et al, 2021 ; Rahimzadeh-Karvansara et al, 2022 ). AFM imaging has delineated diverse assembly patterns and organizational heterogeneity of photosynthetic complexes in thylakoid membranes from different cyanobacterial species, as reflected mainly by the lateral segregation of PSII and PSI.…”

Section: Discussionmentioning

confidence: 99%

“…Thylakoid membrane proteins in their native form were studied by blue native–PAGE according to the previous methods ( Zhang et al, 2012 ) with the exception that 3% (w/v) n-Dodecyl-β- d -maltoside (Anagrade, D310, USA) was used for solubilization ( Zhao et al, 2020 ; Huokko et al, 2021 ). Precast NativePAGE Bis–Tris protein gels with 4%–16% (w/v) gradient (NativePAGE, Thermo Fisher) were used to separate protein complexes.…”

Section: Methodsmentioning

confidence: 99%

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Native architecture and acclimation of photosynthetic membranes in a fast-growing cyanobacterium

Zhao

Chen

et al. 2022

Plant Physiology

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Efficient solar energy conversion is ensured by the organization, physical association, and physiological coordination of various protein complexes in photosynthetic membranes. Here, we visualize the native architecture and interactions of photosynthetic complexes within the thylakoid membranes from a fast-growing cyanobacterium Synechococcus elongatus UTEX 2973 (Syn2973) using high-resolution atomic force microscopy (AFM). In the Syn2973 thylakoid membranes, both photosystem I (PSI)-enriched domains and crystalline photosystem II (PSII) dimer arrays were observed, providing favorable membrane environments for photosynthetic electron transport. The high light (HL)-adapted thylakoid membranes accommodated a large amount of PSI complexes, without the incorporation of iron-stress-induced protein A (IsiA) assemblies and formation of IsiA−PSI supercomplexes. In the iron deficiency (Fe−)-treated thylakoid membranes, in contrast, IsiA proteins densely associated with PSI, forming the IsiA−PSI supercomplexes with varying assembly structures. Moreover, type-I NADH dehydrogenase-like complexes (NDH-1) were upregulated under the HL and Fe− conditions and established close association with PSI complexes to facilitate cyclic electron transport. Our study provides insight into the structural heterogeneity and plasticity of the photosynthetic apparatus in the context of their native membranes in Syn2973 under environmental stress. Advanced understanding of the photosynthetic membrane organization and adaptation will provide a framework for uncovering the molecular mechanisms of efficient light harvesting and energy conversion.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Native architecture and acclimation of photosynthetic membranes in a fast-growing cyanobacterium

Zhao

Chen

et al. 2022

Plant Physiology

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“…The acquisition of the biosynthesis pathway producing a sulfolipid seemed critical for a regular provision of sufficient amounts of anionic lipids, allowing the HexII  Lm phase transition to occur thus forming parietal thylakoids. We designed this model before the very recent description of the spatio-temporal biogenesis process of thylakoid membranes in the rodshaped cyanobacterium Synechococcus elongatus PCC 7942 (Huokko et al, 2021). In this cyanobacterium, the plasma membrane and concentric thylakoid layers have no physical connections and newly synthesized thylakoid membrane fragments emerge between the plasma membrane and pre-existing thylakoids (Huokko et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

“…We designed this model before the very recent description of the spatio-temporal biogenesis process of thylakoid membranes in the rodshaped cyanobacterium Synechococcus elongatus PCC 7942 (Huokko et al, 2021). In this cyanobacterium, the plasma membrane and concentric thylakoid layers have no physical connections and newly synthesized thylakoid membrane fragments emerge between the plasma membrane and pre-existing thylakoids (Huokko et al, 2021). This is strikingly reminiscent of the model described in Figs.…”

Section: Discussionmentioning

confidence: 99%

Origin of cyanobacterial thylakoids via a non-vesicular glycolipid phase transition and their impact on the Great Oxygenation Event

Guéguen

Maréchal

2021

Journal of Experimental Botany

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Appearance of oxygenic photosynthesis in Cyanobacteria is a major event in the evolution of Life. It had an irreversible impact on our planet, promoting the Great Oxygenation Event (GOE), ~2.4 b.y.a. Ancient Cyanobacteria predating the GOE were Gloeobacter-type cells, having no thylakoids. They hosted photosystems in their cytoplasmic membrane. The driver of the GOE was proposed to be the transition from unicellular to filamentous Cyanobacteria. However, the appearance of thylakoids expanded the photosynthetic surface by multiple logs: this multiplier effect would be more coherent with an impact on the atmosphere. Primitive thylakoids self-organize as concentric parietal uninterrupted multilayers. The quest for their origin resists vesicular-based scenarios. This review reports studies supporting that Hexagonal II-forming gluco- and galactolipids at the periphery of the cytosolic membrane could be turned within nanoseconds and without any external source of energy into membrane multilayers. Comparison of lipid biosynthetic pathways further shows that ancient Cyanobacteria contained only one anionic Lamellar-forming lipid, phosphatidylglycerol. Acquisition of sulfoquinovosyldiacylglycerol biosynthesis correlates with thylakoid emergence, possibly enabling a sufficient provision of anionic lipids to trigger an Hexagonal II-to-Lamellar phase transition. With this non-vesicular lipid-phase transition, a framework is also available to reexamine the role of companion proteins in thylakoid biogenesis processes.

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“…As chloroplasts are very sensitive to environmental fluctuations, dynamic proteome changes may represent a key factor for understanding their responses to abiotic stresses [11]. The most recent chloroplast proteomics studieshave aimed to identify (1) changes induced by biotic and abiotic stresses [12][13][14][15][16], (2) mechanisms of remodeling and reprogramming of plant metabolism [17,18], (3) biogenesis and senescence [19][20][21], (4) chloroplast development [22,23],in addition to (5) novel techniques for increasing proteome coverage [24][25][26].…”

Section: Introductionmentioning

confidence: 99%

The Eucalyptus grandis chloroplast proteome: leaf development and seasonal variations

Baldassi

Balbuena

2022

Preprint

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Chloroplast metabolism is very sensitive to environmental fluctuations and is intimately related to plant leaf development. Characterization of the chloroplast proteome dynamics may contribute to enlarge the understanding on plant adaptation to different climate scenarios and leaf development processes. Herein, we carried out a discovery-driven proteome analysis of the Eucalyptus grandis chloroplast proteome during leaf maturation and throughout different seasons of the year. The chloroplast proteome from young leaves differed the most from all assessed samples. Most up-regulated proteins identified in mature and young leaves were those related to catabolic-redox signaling and biogenesis processes, respectively. Seasonal dynamics revealed unique proteome features in the autumn and spring periods. The most abundant chloroplast protein in humid (wet) seasons (spring and summer) was a small subunit of RuBisCO, while in the dry periods (fall and winter) the proteins that showed the most pronounced accumulation were associated with photo-oxidative damage, Calvin cycle, shikimate pathway, and detoxification. Our investigation of the chloroplast proteome dynamics during leaf development revealed significant alterations in relation to the maturation event. Our findings also suggest that transient seasons induced the most pronounced chloroplast proteome changes over the year. This study contributes to a more comprehensive understanding on the subcellular mechanisms that lead to plant leaf adaptation and ultimately to Eucalyptus grandis productivity. Mass spectrometric data are available via ProteomeXchange under identifier PXD029004.

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Probing the biogenesis pathway and dynamics of thylakoid membranes

Cited by 4 publications

References 81 publications

Native architecture and acclimation of photosynthetic membranes in a fast-growing cyanobacterium

Native architecture and acclimation of photosynthetic membranes in a fast-growing cyanobacterium

Origin of cyanobacterial thylakoids via a non-vesicular glycolipid phase transition and their impact on the Great Oxygenation Event

The Eucalyptus grandis chloroplast proteome: leaf development and seasonal variations

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