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, 9 (1), 180237

A Brief History of Thylakoid Biogenesis

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A Brief History of Thylakoid Biogenesis

Annabel Mechela et al. Open Biol.

Abstract

The thylakoid membrane network inside chloroplasts harbours the protein complexes that are necessary for the light-dependent reactions of photosynthesis. Cellular processes for building and altering this membrane network are therefore essential for life on Earth. Nevertheless, detailed molecular processes concerning the origin and synthesis of the thylakoids remain elusive. Thylakoid biogenesis is strongly coupled to the processes of chloroplast differentiation. Chloroplasts develop from special progenitors called proplastids. As many of the needed building blocks such as lipids and pigments derive from the inner envelope, the question arises how these components are recruited to their target membrane. This review travels back in time to the beginnings of thylakoid membrane research to summarize findings, facts and fictions on thylakoid biogenesis and structure up to the present state, including new insights and future developments in this field.

Keywords: chloroplast; chloroplast vesicle transport; resurrection plants; thylakoid biogenesis; thylakoid membrane.

Conflict of interest statement

We declare we have no competing interests.

Figures

Figure 1.
Figure 1.
Chloroplast structure and development in the past and today. Already at the beginning of the 1950s, the first electron microscopic pictures of chloroplasts of land plants were taken. (a) The first cross-section through a tulip chloroplast [14]. (b) The inside of chloroplasts was considered to consist of stroma and connected grana thylakoids that were believed to be arranged like rolls of coins [15]. (c) Differentiation towards mature chloroplasts was suggested to happen from a progenitor via invaginations of the inner envelope. Invaginations would then split into disc-shaped vesicles that stacked together to be eventually interconnected [16]. (d) The modern view on chloroplast differentiation is very similar to that of the past. The progenitors are proplastids that contain only few internal membranes and vesicles that finally assemble the thylakoid membrane network in the presence of light. (e) Modern electron micrographs provide insights into the actual arrangement of the grana stacks. The complex internal organization of a chloroplast is depicted in (f) with thylakoids forming a highly interconnected fretwork.
Figure 2.
Figure 2.
Thylakoid structure and biogenesis in cyanobacteria, green algae and land plants. Thylakoids of cyanobacteria and green algae are less complex than those of land plants. (a) Cyanobacterial thylakoids consist of single lamellae. Specialized membrane regions are believed to function as thylakoid biogenesis centres. These PDMs appear at convergence zones of the thylakoid and the plasma membrane [50]. (b) Green algae contain only one single chloroplast with concentric thylakoids. The pyrenoid, a plastid microcompartment, supports with the fixation of CO2. Around the pyrenoid, the translation zone is also believed to function in thylakoid biogenesis [50,51]. (c) Chloroplasts of land plants differ from those of cyanobacteria and green algae as they build an intertwined network of stroma lamellae and grana lamellae. (d) As it is known that many important building blocks for the thylakoids derive from the inner envelope, three ideas exist on how this transfer could happen. Components could either bridge the stroma via invaginations from the inner envelope as shown in (i). Alternatively, they could travel as cargo of plastid vesicles (ii) or be shuttled by soluble transfer proteins (iii, proteins and lipids attached to a cargo protein are shown) [52]. (e) Arrows pinpoint vesicles and invaginations as seen in young pea chloroplasts. The upper part of the figure shows tubular invaginations extending from the inner membrane to the thylakoids. The lower part shows plastic vesicles, which occur freely in the stroma and are no longer connected to the inner membrane. In the bottom panel, one can see stromal vesicles docking to the thylakoid membrane.
Figure 3.
Figure 3.
Suggestion of processes contributing to thylakoid biogenesis in chloroplasts of land plants. Lipids, prenyl lipids, pigments and proteins are needed to build a functional thylakoid membrane. These components must somehow travel through the aqueous stroma to reach the thylakoids. 1. The galactolipids DGDG and MGDG are synthesized from their synthases DGD1 and MGD1 at the outer and inner envelope, respectively [69,85,128]. 2. Together with prenyl lipids [129] and carotenoids [130] that are also made at the inner envelope, they could be a putative cargo of a suggested plastid vesicle transport system. Vesicles are thought to bud off from the inner envelope, travel across the stroma to finally fuse with the thylakoid membrane to deliver their cargo. 3. Another connection between both membranes could be provided by invaginations forming lateral fusions. Plastid-targeted proteins like LHCII are imported via the TOC and TIC translocons residing in the envelope membranes. These proteins could furthermore be pre-assembled with chlorophylls [86,87] in the incipient invaginating membrane before being delivered to their target membrane.

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