Spatial organization of thylakoid network in higher plants

ABSTRACT

An intricate network of internal plastid membrane is formed in chloroplasts during plant ontogenesis. The network develops directly from a simple membrane system in proplastids or through a paracrystalline tubular prolamellar body (PLB) in etioplasts. A complex spatial structure of PLB interconnected with porous prothylakoids (PTs) is formed when the seedling growth proceeds without light. Upon illumination, PLB transforms through a multistage process into a lamellar system of stacked (grana) and loosely arranged (stroma) thylakoids. The chloroplast thylakoid network, the site of photochemical reactions, is one of the most important as well as most complicated membrane systems in nature. Thus, extensive studies on its possible spatial rearrangements are important for a better understanding of the crucial role of the thylakoid structure in the regulation of photosynthesis. Complementary structural methods are necessary to provide a complex image of spatial thylakoid arrangement. Therefore, in this review, we describe the results obtained by methods using both fixed and in vivo samples. The main goal of this review is to present the state of research on the three-dimensional (3D) structure of internal plastid membrane network, its spatial arrangement during plant ontogenesis and its modifications caused by different factors. Influence of different membrane components on the formation of the thylakoid network shape is also described. Additionally, we summarize recent 3D structural results in the field of thylakoid dynamics induced by environmental factors, especially of light-triggered changes related to rearrangements of the photosynthetic complexes.

KEYWORDS:

• Chloroplast ultrastructure
• electron tomography
• electron microscopy
• confocal microscopy
• thylakoids
• prolamellar body
• 3D ultrastructure
• etioplast

Acknowledgments

This work was financed by the National Science Centre (NCN), grant 2014/13/B/NZ3/00413.

TEM images were performed by authors in the Laboratory of Electron Microscopy, Nencki Institute of Experimental Biology, using a JEM 1400 electron microscope (Jeol).

Presented tomograms were reconstructed and segmented using TomoJ software (Messaoudii et al. 2007) and 3DMOD software (IMOD; Kremer, Mastronarde, and McIntosh 1996) or Imaris 8.4.2, respectively, CLSM data were collected using a Nikon A1 MP microscope and modelled using Imaris 8.4.2, 3D theoretical models were performed with Autodesk Fusion 360 software, macroscopic images of plants were taken using Nikon D750 camera.

We thank Szymon Suski for the operation of tomography supply.

Disclosure statement

No potential conflict of interest was reported by the authors.

Additional information

Funding

This work was supported by the National Science Centre (NCN) [2014/13/B/NZ3/00413].

Notes on contributors

Łucja Kowalewska

Łucja Kowalewska is an Assistant professor at the Faculty of Biology of the University of Warsaw in Poland. She works on structural and molecular aspects of chloroplast function with a special interest in the basis of the plasticity of their spatial structure.

Contribution: she wrote the manuscript and designed the figures.

Michał Bykowski

Michał Bykowski is a Ph.D. student at the Faculty of Biology of the University of Warsaw in Poland. He works on the structural role of carotenoids in chloroplast biogenesis.

Contribution: he designed and made the figures.

Agnieszka Mostowska

Agnieszka Mostowska is a Professor at the Faculty of Biology of the University of Warsaw in Poland; currently, she is also the Dean of the Faculty of Biology. She works on structural aspects of developing and mature chloroplasts with close relation to plant ontogenesis.

Contribution: she proposed the scope of the article and wrote the manuscript.