Metabolic regulation of photosynthetic membrane structure tunes electron transfer function

The photosynthetic chloroplast thylakoid membrane of higher plants is a complex three-dimensional structure that is morphologically dynamic on a timescale of just a few minutes. The membrane dynamics are driven by the phosphorylation of light-harvesting complex II (LHCII) by the STN7 kinase, which controls the size of the stacked grana region relative to the unstacked stromal lamellae region. Here, I hypothesise that the functional significance of these membrane dynamics is in controlling the partition of electrons between photosynthetic linear and cyclic electron transfer (LET and CET), which determines the ratio of NADPH/ATP produced. The STN7 kinase responds to the metabolic state of the chloroplast by sensing the stromal redox state. A high NADPH/ATP ratio leads to reduction of thioredoxin f (TRXf), which reduces a CxxxC motif in the stromal domain of STN7 leading to its inactivation, whereas a low NADPH/ATP ratio leads to oxidation of TRXf and STN7 activation. Phosphorylation of LHCII leads to smaller grana, which favour LET by speeding up diffusion of electron carriers plastoquinone (PQ) and plastocyanin (PC) between the domains. In contrast, dephosphorylation of LHCII leads to larger grana that slow the diffusion of PQ and PC, leaving the PQ pool in the stroma more oxidised, thus enhancing the efficiency of CET. The feedback regulation of electron transfer by the downstream metabolism is crucial to plant fitness, since perturbations in the NADPH/ATP ratio can rapidly lead to the inhibition of photosynthesis and photo-oxidative stress

Dynamic thylakoid stacking regulates the balance between linear and cyclic photosynthetic electron transfer

An Author Correction to this article was published on 29 May 2018 https://www.nature.com/articles/s41477-018-0163-4 http://eprints.whiterose.ac.uk/131699/ Upon transition of plants from darkness to light the initiation of photosynthetic linear electron transfer (LET) from H2O to NADP+ precedes the activation of CO2 fixation, creating a lag period where cyclic electron transfer (CET) around photosystem I (PSI) has an important protective role. CET generates ΔpH without net reduced NADPH formation, preventing overreduction of PSI via regulation of the cytochrome b 6 f (cytb 6 f) complex and protecting PSII from overexcitation by inducing non-photochemical quenching. The dark-to-light transition also provokes increased phosphorylation of light-harvesting complex II (LHCII). However, the relationship between LHCII phosphorylation and regulation of the LET/CET balance is not understood. Here, we show that the dark-to-light changes in LHCII phosphorylation profoundly alter thylakoid membrane architecture and the macromolecular organization of the photosynthetic complexes, without significantly affecting the antenna size of either photosystem. The grana diameter and number of membrane layers per grana are decreased in the light while the number of grana per chloroplast is increased, creating a larger contact area between grana and stromal lamellae. We show that these changes in thylakoid stacking regulate the balance between LET and CET pathways. Smaller grana promote more efficient LET by reducing the diffusion distance for the mobile electron carriers plastoquinone and plastocyanin, whereas larger grana enhance the partition of the granal and stromal lamellae plastoquinone pools, enhancing the efficiency of CET and thus photoprotection by non-photochemical quenching