A quantitative model of the domain structure of the photosynthetic membrane

doi:10.1016/S1360-1385(01)02021-0

Trends in Plant Science

Volume 6, Issue 8, 1 August 2001, Pages 349-354

https://doi.org/10.1016/S1360-1385(01)02021-0 Get rights and content

Abstract

A model is presented that gives a quantitative picture of the distribution of the photosynthetic components in the photosynthetic membrane of higher plants. A salient feature of the model is that most of the pigments are located in the grana where photosystem I and II carry out linear electron transport, whereas the stroma lamellae, which harbour <20% of the pigments, carry out photosystem-I-mediated cyclic electron transport. This arrangement derives from the observation that more pigments are associated with photosystem I, which therefore captures more quanta than photosystem II. The excess pigments associated with photosystem I are thought to be located in the stroma lamellae.

Section snippets

Structure from electron microscopy

The photosynthetic membrane (also named the thylakoid membrane) consists of a system of paired membranes enclosing between them the lumen and separating it from the surrounding stroma of the chloroplast. In addition to the asymmetry across the membrane, there is also a lateral asymmetry such that one can distinguish between different domains with different biochemical composition and function ¹ (Fig. 1).

The grana are stabilized by ‘stacking’ forces between the outer surface of thylakoids in the

Fragmentation and separation analysis

One way to study the organization and structure of a complex biological object is to disintegrate it, separate the components, determine their composition and properties and then try to construct a model of the original object. When applied to the thylakoid membrane this approach has given us important knowledge about its components and their organization and function in the membrane. Press treatment or sonication gives rise to membrane vesicles that originate from the different parts of the

More quanta are captured by photosystem I than photosystem II

A fundamental question in photosynthesis is how the light quanta captured by the pigments are distributed between the two photosystems. Because the separation of thylakoid vesicles is quantitative, it is possible to determine the distribution of chlorophyll and carotenoid between PSI and PSII (Refs 6, 7). It turns out that there is more chlorophyll associated with PSI than with PSII, the excess being in the range 14–20% (i.e. per 100 chlorophyll molecules 57–60 are associated with PSI and 40–43

A model for the thylakoid membrane

According to the model (Fig. 2), 80% of the membrane is in the form of grana and 20% as stroma lamellae. Linear electron transport (Box 1) occurs in the grana where PSII, localized in the appressed core of the grana, cooperates with PSI in the margin, which forms an annulus (ring) surrounding the grana core. The margin covers 40% of the circular grana disc to accommodate ∼40% of the chlorophyll localized in a grana disc, which is associated with PSIα (Table 1).

PSII of the appressed grana and

Why are photosystem I and photosystem II laterally segregated in the thylakoid membrane?

This is a frequently asked question. One can answer ‘Why not?'It has been known for many years that macromolecules do not readily mix in solutions; mixing is the exception rather than the rule in polymer mixtures, both in water and in organic solvents ¹⁹. This is because of the large size of macromolecules, resulting in a domination of the interaction between the macromolecules over the entropy of mixing. If the interaction between like molecules is more attractive than between unlike

What is the functional advantage with patches of photosystem II that form grana stacks?

This question has been discussed ever since grana were discovered. It has been suggested that grana can facilitate light harvesting and its regulation 17, 21, protect against photodamage ¹⁷ and prevent quanta captured by PSII from ending up in PSI (Ref. 22).

A feature of the present model is that the formation of grana prevents competition between linear and cyclic electron transport. The grana and the stroma lamellae should complement each other and not compete when carrying out their

Light-induced protein phosphorylation

What has been written above holds for conditions when light is limiting. Dramatic changes occur when light intensity increases ²⁵: PSII is down regulated, its functional antenna decreases, oxygen evolution becomes eventually saturated, the antenna of PSI might increase, cyclic electron transport increases relative to the linear, several proteins are phosphorylated, photosystems are damaged and repaired.

The net result is that the excess of quanta captured by PSI becomes even larger than under

Acknowledgements

My thanks to John F. Allen and Jonathan Park for critically reading the manuscript.

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Trends in Plant Science

OpinionA quantitative model of the domain structure of the photosynthetic membrane

Abstract

Section snippets

Structure from electron microscopy

Fragmentation and separation analysis

More quanta are captured by photosystem I than photosystem II

A model for the thylakoid membrane

Why are photosystem I and photosystem II laterally segregated in the thylakoid membrane?

What is the functional advantage with patches of photosystem II that form grana stacks?

Light-induced protein phosphorylation

Acknowledgements

J. Biol. Chem.

Photosynth. Res.

Recent Res. Dev. Bioenergetics

Biochim. Biophys. Acta

Biochim. Biophys. Acta

Biochim. Biophys. Acta

Biochim. Biophys. Acta

Biochim. Biophys. Acta

Aust. J. Plant Physiol.

Planta

Biochim. Biophys. Acta

Aust. J. Plant Physiol.

Opinion
A quantitative model of the domain structure of the photosynthetic membrane