The three-dimensional network of the thylakoid membranes in plants: quasihelical model of the granum-stroma assembly

Abstract

The three-dimensional (3-D) network of the granum-stroma thylakoid assembly of vascular plant chloroplasts exhibits complex structural/functional heterogeneity. A complete understanding of the ultrastructure of this assembly is critical for our understanding of thylakoid function. The prevailing historical model of thylakoid structure, based on information derived from serial section analyses of electron microscopy (EM) images, suggests a helical arrangement of stroma membranes wound around the granum stacks. More recently, electron tomography has emerged as the leading method for the study of thylakoid ultrastructure, as it provides for higher resolution in the depth dimension. The first detailed 3D topological model derived from electron tomography was in disagreement with the helical model, whereas a more recent electron tomography study, conducted under somewhat different experimental conditions, suggested that basic features of the helical model are still valid. Here, we review the conventional EM data and present a critical discussion of the two electron tomography data sets in an attempt to establish a consensus model that accommodates all the information presently available.

Figure 1.

Comparison of the Helical Model and the Pairwise Organization Model of the Granum-Stroma Thylakoid Membrane System of Vascular Plant Chloroplasts. (A) Computerized form of the helical model constructed from electron micrographs of full serial sectioning of a granum-stroma assembly. (Reprinted from Mustárdy and Garab [2003], Figure 3A, with permission from Elsevier.) (B) Topological model based on electron tomography. α, tilt angle between the granum and stroma thylakoid membranes; GT, granum thylakoid; GTM, granum thylakoid membrane; J, junction between the granum and stroma thylakoids; ST, STM, and STL, stroma thylakoid, thylakoid membrane, and lumen, respectively. (Reprinted from Shimoni et al. [2005], Figure 3.)

Figure 2.

Equidistant Tomographic Sections of Chloroplast Granum-Stroma Thylakoid Assemblies. (A) Close-up views of images from the data set of Mustárdy et al. (2008). (B) Close-up views of images extracted from Supplemental Movie 1 in Shimoni et al. (2005). F, fork-like structures at the junction of the granum and stroma thylakoids; GT, GTL, and GTM, granum thylakoid, thylakoid membrane, and lumen, respectively; J and J', junctions between the granum and stroma thylakoids; ST, STM, and STL, stroma thylakoid, thylakoid membrane, and lumen, respectively.