Dynamic thylakoid stacking and state transitions work synergistically to avoid acceptor-side limitation of photosystem I

Hepworth, Christopher; Wood, William H.; Emrich-Mills, Tom Z.; Proctor, Matthew S.; Casson, Stuart A.; Johnson, Matthew P.

doi:10.1038/s41477-020-00828-3

Cited by 46 publications

(51 citation statements)

References 89 publications

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“…Any excessive high light situation could be exacerbated further with a co-occurring high temperature ( Sun et al, 2017 ; Lu et al, 2020 ), low temperature ( Liu et al, 2013 ; Song et al, 2020 ; Wu et al, 2020 ), phosphorus deficiency ( Carstensen et al, 2018 ; Shi et al, 2019 ) and drought ( Wada et al, 2019 ). Plants have evolved several adaptations to cope with the unfavorable light situation: adjusting leaf orientation, ROS scavenging competence ( Gill and Tuteja, 2010 ), xanthophyll cycle ( Kuczynska et al, 2020 ), state transitions strategy ( Hepworth et al, 2021 ), cyclic electron transport (CET; Yadav et al, 2020 ) and photorespiration ( Storti et al, 2019 ). This review summarizes the main biochemical processes of PGR5/PGRL1-dependent CET pathway.…”

Section: Introductionmentioning

confidence: 99%

The Physiological Functionality of PGR5/PGRL1-Dependent Cyclic Electron Transport in Sustaining Photosynthesis

Liu

Bai

et al. 2021

Front. Plant Sci.

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The cyclic electron transport (CET), after the linear electron transport (LET), is another important electron transport pathway during the light reactions of photosynthesis. The proton gradient regulation 5 (PGR5)/PRG5-like photosynthetic phenotype 1 (PGRL1) and the NADH dehydrogenase-like complex pathways are linked to the CET. Recently, the regulation of CET around photosystem I (PSI) has been recognized as crucial for photosynthesis and plant growth. Here, we summarized the main biochemical processes of the PGR5/PGRL1-dependent CET pathway and its physiological significance in protecting the photosystem II and PSI, ATP/NADPH ratio maintenance, and regulating the transitions between LET and CET in order to optimize photosynthesis when encountering unfavorable conditions. A better understanding of the PGR5/PGRL1-mediated CET during photosynthesis might provide novel strategies for improving crop yield in a world facing more extreme weather events with multiple stresses affecting the plants.

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Section: Introductionmentioning

confidence: 99%

The Physiological Functionality of PGR5/PGRL1-Dependent Cyclic Electron Transport in Sustaining Photosynthesis

Liu

Bai

et al. 2021

Front. Plant Sci.

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“…Since dephosphorylation of LHCII is promoted by high light (Mekala et al, 2015 ; Rintamäki et al, 1997 ) the result is a shift to State I. This shift in the Field plants is also corroborated by their increased grana diameter relative to Lab plants, since dephosphorylation of LHCII promotes this effect (Hepworth et al, 2021 ; Wood et al, 2019 ). Indeed, decreased LHCII phosphorylation and reduction in the levels of LHCB1 containing trimers may overrule the increased relative abundance of CURT1A and CURT1B in Field plants that otherwise would be anticipated to increase the number of membrane layers per granum (Armbruster et al, 2013 ; Pietrzykowska et al, 2014 ).…”

Section: Resultsmentioning

confidence: 99%

“…Phosphorylation of LHCII and PSII by the STN7 and STN8 kinases, respectively, decreases grana stacking by increasing electrostatic repulsion on the stromal side of the membrane while dephosphorylation by TAP38 increases stacking (Armbruster et al, 2013 ; Fristedt, Willig, et al, 2009 ; Hepworth et al, 2021 ; Samol et al, 2012 ; Wood et al, 2019 ). Unexpectedly, although STN7 and STN8 both increase with growth light intensity under laboratory conditions (Albanese et al, 2018 ; Flannery et al, 2021 ), our analysis shows contrasting behavior of STN7 and STN8 in the field (Figure 4e ).…”

Section: Resultsmentioning

confidence: 99%

Comparative proteomics of thylakoids from Arabidopsis grown in laboratory and field conditions

et al. 2021

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Compared to controlled laboratory conditions, plant growth in the field is rarely optimal since it is frequently challenged by large fluctuations in light and temperature which lower the efficiency of photosynthesis and lead to photo‐oxidative stress. Plants grown under natural conditions therefore place an increased onus on the regulatory mechanisms that protect and repair the delicate photosynthetic machinery. Yet, the exact changes in thylakoid proteome composition which allow plants to acclimate to the natural environment remain largely unexplored. Here, we use quantitative label‐free proteomics to demonstrate that field‐grown Arabidopsis plants incorporate aspects of both the low and high light acclimation strategies previously observed in laboratory‐grown plants. Field plants showed increases in the relative abundance of ATP synthase, cytochrome b6f, ferredoxin‐NADP+ reductases (FNR1 and FNR2) and their membrane tethers TIC62 and TROL, thylakoid architecture proteins CURT1A, CURT1B, RIQ1, and RIQ2, the minor monomeric antenna complex CP29.3, rapidly‐relaxing non‐photochemical quenching (qE)‐related proteins PSBS and VDE, the photosystem II (PSII) repair machinery and the cyclic electron transfer complexes NDH, PGRL1B, and PGR5, in addition to decreases in the amounts of LHCII trimers composed of LHCB1.1, LHCB1.2, LHCB1.4, and LHCB2 proteins and CP29.2, all features typical of a laboratory high light acclimation response. Conversely, field plants also showed increases in the abundance of light harvesting proteins LHCB1.3 and CP29.1, zeaxanthin epoxidase (ZEP) and the slowly‐relaxing non‐photochemical quenching (qI)‐related protein LCNP, changes previously associated with a laboratory low light acclimation response. Field plants also showed distinct changes to the proteome including the appearance of stress‐related proteins ELIP1 and ELIP2 and changes to proteins that are largely invariant under laboratory conditions such as state transition related proteins STN7 and TAP38. We discuss the significance of these alterations in the thylakoid proteome considering the unique set of challenges faced by plants growing under natural conditions.

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“…Still, they fail in detailed grana visualization at the level of particular thylakoid layers. Typical grana structural parameters obtained using an in vivo approach are granum diameter (Uwada et al, 2017;Wood et al, 2019;Hepworth et al, 2021), also defined as full-width at half-maximum fluorescence intensity of the fluorescent spots (grana; Herbstova et al, 2012;Iwai et al, 2018;Wood et al, 2018;Flannery et al, 2021), and parameters describing the whole network. These parameters include: the number of grana stacks per chloroplast (Wood et al, 2018(Wood et al, , 2019Mazur et al, 2019), their distribution (Herbstova et al, 2012;Chen et al, 2014), and average grana sizes determined indirectly by the surface/volume ratio for 3D models of chlorophyll fluorescence (Bykowski et al, 2021).…”

Section: Methods Used In the Visualization Of Granum Morphology And Their Limitationsmentioning

confidence: 99%

“…Detailed analysis of grana structure provides important information about the thylakoid membrane remodeling forced by plant ontogenesis (Kowalewska et al, 2016;Armarego-Marriott et al, 2019;Pipitone et al, 2021), light intensity and quality (Rozak et al, 2002;Yamamoto et al, 2014;Demmig-Adams et al, 2015;Schumann et al, 2017;Flannery et al, 2021), and other environmental factors (Fq et al, 2012;Jiang et al, 2017;Chen et al, 2018a;Zechmann, 2019;Mazur et al, 2020). However, structural analysis indirectly indicates the organization and efficiency of the photosynthetic light reaction machinery (Pribil et al, 2018;Mazur et al, 2019;Wood et al, 2019;Hepworth et al, 2021) and photonic effects in the thylakoid network (Capretti et al, 2019).…”

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confidence: 99%

How to Measure Grana – Ultrastructural Features of Thylakoid Membranes of Plant Chloroplasts

2021

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Granum is a basic structural unit of the thylakoid membrane network of plant chloroplasts. It is composed of multiple flattened membranes forming a stacked arrangement of a cylindrical shape. Grana membranes are composed of lipids and tightly packed pigment-protein complexes whose primary role is the catalysis of photosynthetic light reactions. These membranes are highly dynamic structures capable of adapting to changing environmental conditions by fine-tuning photochemical efficiency, manifested by the structural reorganization of grana stacks. Due to a nanometer length scale of the structural granum features, the application of high-resolution electron microscopic techniques is essential for a detailed analysis of the granum architecture. This mini-review overviews recent approaches to quantitative grana structure analyses from electron microscopy data, highlighting the basic manual measurements and semi-automated workflows. We outline and define structural parameters used by different authors, for instance, granum height and diameter, thylakoid thickness, end-membrane length, Stacking Repeat Distance, and Granum Lateral Irregularity. This article also presents insights into efficient and effective measurements of grana stacks visualized on 2D micrographs. The information on how to correctly interpret obtained data, taking into account the 3D nature of grana stacks projected onto 2D space of electron micrograph, is also given. Grana ultrastructural observations reveal key features of this intriguing membrane arrangement, broadening our knowledge of the thylakoid network’s remarkable plasticity.

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Dynamic thylakoid stacking and state transitions work synergistically to avoid acceptor-side limitation of photosystem I

Abstract: This is a repository copy of Dynamic thylakoid stacking and state transitions work synergistically to avoid acceptor-side limitation of photosystem I.

Cited by 46 publications

References 89 publications

The Physiological Functionality of PGR5/PGRL1-Dependent Cyclic Electron Transport in Sustaining Photosynthesis

The Physiological Functionality of PGR5/PGRL1-Dependent Cyclic Electron Transport in Sustaining Photosynthesis

Comparative proteomics of thylakoids from Arabidopsis grown in laboratory and field conditions

How to Measure Grana – Ultrastructural Features of Thylakoid Membranes of Plant Chloroplasts

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