Trends in Plant Science
Volume 8, Issue 3, March 2003, Pages 117-122
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Granum revisited. A three-dimensional model – where things fall into place

https://doi.org/10.1016/S1360-1385(03)00015-3Get rights and content

Abstract

The complex structure of higher plant chloroplasts has fascinated researchers for many years. Although the spatial relationship between granum and stroma thylakoids has been known for more than 20 years, most textbooks and research papers continue to include erroneous 3D models and simplified schemes. Here we present a simple computer model, based on electron micrographs from serial section of granum–stroma assemblies, showing the striking 3D structure of the stroma membrane wound around the granum. This model also provides an insight into some previously unknown functions of this intriguing multilamellar membrane system. However, many areas, such as self-assembly, structural flexibility and evolutionary niche, still remain to be explored.

Section snippets

Obsolete models still in use

The first model, proposed by Wilhelm Menke, was developed from early electron microscopic observations [1]. This model, still used in some books and on homepages, postulates that every second granum thylakoid is continued in sheets that intersect several grana (Fig. 2a). This oversimplified scheme does not satisfy the requirement of membrane continuity and is inconsistent with the single intrathylakoidal (lumenal) space.

In a more frequently used, dangerously attractive model, the grana are

Reconstituted 3D model

In the generally accepted, although not widely used model, the thylakoid membranes in the chloroplasts of mesophyll cells of C3 and C4 plants display multiple right-handed helices of stroma lamellae that are wound around the cylindrical grana and form a contiguous system. The helical arrangement of stroma thylakoids around grana was proposed by Dominick J. Paolillo [12] in 1970, and confirmed with the aid of a complete series of sections [13]. For the purpose of better visualization, the

Functions

The pioneering work by Jan M. Anderson and Keith N. Boardman >30 years ago has revealed that the differentiation of thylakoids into granum and stroma membrane regions reflects a compositional and functional difference [16]. The two photosystems are spatially separated: photosystem II (PSII) and its main chlorophyll a/b light-harvesting complex, LHCII, are found predominantly in the stacked membranes; this region is largely deficient in photosystem I (PSI) and LHCI, which are enriched in the

Open questions, perspectives

The ontogeny and evolution of this (type of) granum–stroma assembly and its ancestors are not well understood. Several interesting questions can be posed with regard to the 3D arrangement of this assembly. What is the exact role of this peculiar membrane assembly in the regulation of energy transduction? There are indications that grana and the LHCII-containing macrodomains are needed for the efficient regulation of energy dissipation in excess light 39, 40, but the details of such regulation

Acknowledgements

We are indebted to Peter Simon for the computer graphics, and László Kovács for valuable discussions and help in preparing the figures. This work has been supported by grants from the Hungarian Fund for Basic Research (OTKA T30324, T34188 and T42696).

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