Plastocyanin is the long-range electron carrier between photosystem II and photosystem I in plants

Ricarda Höhner,  Mathias Pribil, Miroslava Herbstová,  Laura Susanna Lopez,  Hans-Henning Kunz,  Meng Li, Magnus Wood, Vaclav Svoboda,  Sujith Puthiyaveetil,  Dario Leister, and Helmut Kirchhoff

PNAS June 30, 2020 117 (26) 15354-15362

Significance

Biological energy conversion relies on a well-defined sequence of redox reactions within the membrane-embedded electron transport chains of chloroplasts and mitochondria. In plants, the photosynthetic electron transport between the two photosystems has to cover distances of a few hundred nanometers. This is due to unique architectural features of the photosynthetic thylakoid membranes, which fold into stacked grana and unstacked stroma thylakoids. It is a long-standing question which of the mobile electron carriers, plastoquinone or plastocyanin, shuttles electrons over long distances from PSII in stacked regions to PSI in unstacked regions. By employing mutants with different grana diameters, we identify PC as the long-range electron carrier. This finding has important consequences for the control of photosynthetic electron transport.

Abstract

In photosynthetic electron transport, large multiprotein complexes are connected by small diffusible electron carriers, the mobility of which is challenged by macromolecular crowding. For thylakoid membranes of higher plants, a long-standing question has been which of the two mobile electron carriers, plastoquinone or plastocyanin, mediates electron transport from stacked grana thylakoids where photosystem II (PSII) is localized to distant unstacked regions of the thylakoids that harbor PSI. Here, we confirm that plastocyanin is the long-range electron carrier by employing mutants with different grana diameters. Furthermore, our results explain why higher plants have a narrow range of grana diameters since a larger diffusion distance for plastocyanin would jeopardize the efficiency of electron transport. In the light of recent findings that the lumen of thylakoids, which forms the diffusion space of plastocyanin, undergoes dynamic swelling/shrinkage, this study demonstrates that plastocyanin diffusion is a crucial regulatory element of plant photosynthetic electron transport.

See https://www.pnas.org/content/117/26/15354

Fig.5: Computer model of PC diffusion from stacked to unstacked thylakoid domains. (A) Model thylakoid membrane describing the structural relationship between stacked und unstacked domains. For further details, see Methods. (B) Model with PSII protrusions populating the lumen of stacked domains (“z”-shaped black particles). The (random) distribution of PSI (unstacked) and PC (stacked) complexes is indicated. (C) Models for thylakoid lumen with a grana diameter of 400 or 1,600 nm, respectively. The ratio between stacked and unstacked areas is assumed to be constant (see Chl yield data, Fig. 2B). (D) Diffusion kinetics of PC in stacked thylakoid domains to reach PSI in unstacked regions (see B for an example). The different grana diameters are given on the Right. For further details, see the text. (E) Plot of PC diffusion half-time (derived from D) versus grana diameter. The crossing point where the slope changes was derived from interpolation of the two red slope lines.