State transitions reveal the dynamics and flexibility of the photosynthetic apparatus

Abstract

The chloroplast-based photosynthetic apparatus of plants and algae associates various redox cofactors and pigments with approximately 70 polypeptides to form five major transmembrane protein complexes. Among these are two photosystems that have distinct light absorption properties but work in series to produce reducing equivalents aimed at the fixation of atmospheric carbon. A short term chromatic adaptation known as 'State transitions' was discovered thirty years ago that allows photosynthetic organisms to adapt to changes in light quality and intensity which would otherwise compromise the efficiency of photosynthetic energy conversion. A two-decade research effort has finally unraveled the major aspects of the molecular mechanism responsible for State transitions, and their physiological significance has been revisited. This review describes how a-still elusive-regulatory kinase senses the physiological state of the photosynthetic cell and triggers an extensive supramolecular reorganization of the photosynthetic membranes. The resulting picture of the photosynthetic apparatus is that of a highly flexible energy convertor that adapts to the ever-changing intracellular demand for ATP and/or reducing power.

Fig. 1. The early view of State transitions: two photosystems, Photosystem I (PSI) and Photosystem II (PSII), cooperate in gathering light energy aimed at a photosynthesis-dependent carbon fixation. Light harvesting is improved by the association of distinct and specific chlorophyll beds to PSI and PSII. The PSI antenna is enriched in far-red light absorbing holochromes of Chla whereas the PSII antenna is enriched in Chlb whose absorption peak is at 650 nm in the red region. When exposed to light preferentially absorbed by PSI (far red light), plants or algae display an antenna distribution that favors PSII (State I). In contrast, when exposed to light preferentially absorbed by PSII (650 nm light), plants or algae display an antenna distribution that favors PSI (State II).

Fig. 2. Schematic representation of the main steps in a transition to State II: upon illumination of plants or algae with a light preferentially absorbed by PSII, or upon intracellular ATP depletion, the intersystem electron carriers (IEC) of the photosynthesis electron transfer chain switch to a more reduced state. A regulatory kinase becomes activated in these reducing conditions and phosphorylates the chla/b-containing peripheral antenna, termed LHCII. Phospho-LHCII moves away from PSII and is associated with PSI, thereby changing the relative absorption cross-sections of the two photosystems.

Fig. 3. A hypothetical model for the cytochrome b₆f-mediated activation of the LHCII-kinase: cytochrome b₆f complexes stand as dimers in the thylakoid membranes with most of the Rieske protein (in black) exposed to the lumen, in either a distal or proximal position with respect to the thylakoid membranes. The reversible binding of reduced plastoquinones (, PQH2) drives the Rieske protein from one position to the other. A transmembrane reorganization of the cytochrome b₆f complexes takes place when the Rieske switches from a distal to a proximal position. New interactions then develop with the LHCII-kinase, whose catalytic site, facing the stroma, becomes activated. The active kinase phosphorylates a subunit of the cytochrome b₆f complex. It is released in the membrane space when the Rieske protein moves back to its distal position because of the binding turnover of PQH2 at the Qo site. Upon its release, the active kinase can interact with LHCII and promote its phosphorylation ().

Fig. 4. The present view of State transitions: in State I, the supramolecular organization of the photosynthetic apparatus is adapted to the fixation of CO₂ in the Calvin cycle. A linear electron flow from PSII (which extracts electrons from water leading to O₂ evolution) to PSI generates reducing power (NADPH) and ATP, both of which are required for the biosynthesis of carbohydrates. In State II, an extensive supramolecular reorganization converts the photosynthesis apparatus in an ATP generator. A fraction of the major antenna proteins (LHCII) and cytochrome b₆f complexes undergo a lateral redistribution from the PSII membrane domains to the PSI membrane domains, which switches on a cyclic electron flow around PSI exclusively aimed at ATP synthesis. The flexibility in the functional organization of the photosynthetic apparatus is established for work with the unicellular eukaryote Chlamydomonas reinhardtii. The extent to which it also applies to higher plant photosynthesis remains to be assessed.