DOI: 10.1104/pp.110.170647. Three-Dimensional Architecture of Grana and Stroma Thylakoids of Higher Plants as Determined by Electron Tomography

Three-Dimensional Architecture of Grana and Stroma Thylakoids of Higher Plants as Determined by Electron Tomography

10.1104/pp.110.170647

Crossref journal-article

Oxford University Press (OUP)

Plant Physiology (286)

Abstract

Abstract We have investigated the three-dimensional (3D) architecture of the thylakoid membranes of Arabidopsis (Arabidopsis thaliana), tobacco (Nicotiana tabacum), and spinach (Spinacia oleracea) with a resolution of approximately 7 nm by electron tomography of high-pressure-frozen/freeze-substituted intact chloroplasts. Higher-plant thylakoids are differentiated into two interconnected and functionally distinct domains, the photosystem II/light-harvesting complex II-enriched stacked grana thylakoids and the photosystem I/ATP synthase-enriched, nonstacked stroma thylakoids. The grana thylakoids are organized in the form of cylindrical stacks and are connected to the stroma thylakoids via tubular junctions. Our data confirm that the stroma thylakoids are wound around the grana stacks in the form of multiple, right-handed helices at an angle of 20° to 25° as postulated by a helical thylakoid model. The junctional connections between the grana and stroma thylakoids all have a slit-like architecture, but their size varies tremendously from approximately 15 × 30 nm to approximately 15 × 435 nm, which is approximately 5 times larger than seen in chemically fixed thylakoids. The variable slit length results in less periodicity in grana/stroma thylakoid organization than proposed in the original helical model. The stroma thylakoids also exhibit considerable architectural variability, which is dependent, in part, on the number and the orientation of adjacent grana stacks to which they are connected. Whereas some stroma thylakoids form solid, sheet-like bridges between adjacent grana, others exhibit a branching geometry with small, more tubular sheet domains also connecting adjacent, parallel stroma thylakoids. We postulate that the tremendous variability in size of the junctional slits may reflect a novel, active role of junctional slits in the regulation of photosynthetic function. In particular, by controlling the size of junctional slits, plants could regulate the flow of ions and membrane molecules between grana and stroma thylakoid membrane domains.

Bibliography

Austin, J. R., & Staehelin, L. A. (2011). Three-Dimensional Architecture of Grana and Stroma Thylakoids of Higher Plants as Determined by Electron Tomography Â Â . Plant Physiology, 155(4), 1601â1611.

Authors 2

Jotham R. Austin (first)
L. Andrew Staehelin (additional)

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Dates

Type	When
Created	14 years, 7 months ago (Jan. 11, 2011, 9 p.m.)
Deposited	4 years, 2 months ago (May 26, 2021, 6:45 a.m.)
Indexed	25 minutes ago (Aug. 21, 2025, 4:43 a.m.)
Issued	14 years, 7 months ago (Jan. 11, 2011)
Published	14 years, 7 months ago (Jan. 11, 2011)
Published Online	14 years, 7 months ago (Jan. 11, 2011)
Published Print	14 years, 5 months ago (March 1, 2011)

Funders 0

None

BibTeX

@article{Austin_2011, title={Three-Dimensional Architecture of Grana and Stroma Thylakoids of Higher Plants as Determined by Electron Tomography }, volume={155}, ISSN={1532-2548}, url={http://dx.doi.org/10.1104/pp.110.170647}, DOI={10.1104/pp.110.170647}, number={4}, journal={Plant Physiology}, publisher={Oxford University Press (OUP)}, author={Austin, Jotham R. and Staehelin, L. Andrew}, year={2011}, month=jan, pages={1601–1611} }

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  "abstract": "<jats:title>Abstract</jats:title>\n               <jats:p>We have investigated the three-dimensional (3D) architecture of the thylakoid membranes of Arabidopsis (Arabidopsis thaliana), tobacco (Nicotiana tabacum), and spinach (Spinacia oleracea) with a resolution of approximately 7 nm by electron tomography of high-pressure-frozen/freeze-substituted intact chloroplasts. Higher-plant thylakoids are differentiated into two interconnected and functionally distinct domains, the photosystem II/light-harvesting complex II-enriched stacked grana thylakoids and the photosystem I/ATP synthase-enriched, nonstacked stroma thylakoids. The grana thylakoids are organized in the form of cylindrical stacks and are connected to the stroma thylakoids via tubular junctions. Our data confirm that the stroma thylakoids are wound around the grana stacks in the form of multiple, right-handed helices at an angle of 20\u00b0 to 25\u00b0 as postulated by a helical thylakoid model. The junctional connections between the grana and stroma thylakoids all have a slit-like architecture, but their size varies tremendously from approximately 15 \u00d7 30 nm to approximately 15 \u00d7 435 nm, which is approximately 5 times larger than seen in chemically fixed thylakoids. The variable slit length results in less periodicity in grana/stroma thylakoid organization than proposed in the original helical model. The stroma thylakoids also exhibit considerable architectural variability, which is dependent, in part, on the number and the orientation of adjacent grana stacks to which they are connected. Whereas some stroma thylakoids form solid, sheet-like bridges between adjacent grana, others exhibit a branching geometry with small, more tubular sheet domains also connecting adjacent, parallel stroma thylakoids. We postulate that the tremendous variability in size of the junctional slits may reflect a novel, active role of junctional slits in the regulation of photosynthetic function. In particular, by controlling the size of junctional slits, plants could regulate the flow of ions and membrane molecules between grana and stroma thylakoid membrane domains.</jats:p>",
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