Chloroplast remodeling during state transitions in Chlamydomonas reinhardtii as revealed by noninvasive techniques in vivo

Abstract

Plants respond to changes in light quality by regulating the absorption capacity of their photosystems. These short-term adaptations use redox-controlled, reversible phosphorylation of the lightharvesting complexes (LHCIIs) to regulate the relative absorption cross-section of the two photosystems (PSs), commonly referred to as state transitions. It is acknowledged that state transitions induce substantial reorganizations of the PSs. However, their consequences on the chloroplast structure are more controversial. Here, we investigate how state transitions affect the chloroplast structure and function using complementary approaches for the living cells of Chlamydomonas reinhardtii. Using small-angle neutron scattering, we found a strong periodicity of the thylakoids in state 1, with characteristic repeat distances of ∼200 Å, which was almost completely lost in state 2. As revealed by circular dichroism, changes in the thylakoid periodicity were paralleled by modifications in the long-range order arrangement of the photosynthetic complexes, which was reduced by ∼20% in state 2 compared with state 1, but was not abolished. Furthermore, absorption spectroscopy reveals that the enhancement of PSI antenna size during state 1 to state 2 transition (∼20%) is not commensurate to the decrease in PSII antenna size (∼70%), leading to the possibility that a large part of the phosphorylated LHCIIs do not bind to PSI, but instead form energetically quenched complexes, which were shown to be either associated with PSII supercomplexes or in a free form. Altogether these noninvasive in vivo approaches allow us to present a more likely scenario for state transitions that explains their molecular mechanism and physiological consequences.green algae | photosynthesis | thylakoid membrane T he efficient operation of the photosynthetic machinery of oxygenic photosynthetic organisms requires a balanced energy supply to the two photosystems (PSs) under changing environments. To avoid unbalanced excitations of the two PSs, a rapid acclimation mechanism, state transitions (STs), takes place, which allows redistributing the excitation energy between the two PSs. ST is seen in green algae and vascular plants and is modulated by the redox-controlled, reversible phosphorylation of LHCII, the light-harvesting chlorophyll a/b antenna complex. A serine-threonine protein kinase, STN7 in vascular plants (1) and Stt7 in green algae (2), is responsible for this phosphorylation. Stt7/STN7 activity depends on the redox state of the plastoquinone (PQ) pool, which is sensed by the cytochrome b 6 f complex (3).According to the current model of STs, preferential PSII excitation leads to PQ reduction, and thus to LHCII phosphorylation by the kinase. The PQ pool can also be reduced in dark anaerobic conditions in algal suspensions. In this state, called state 2 (S2), phosphorylated LHCII dissociates from PSII, thereby reducing its absorption cross-section, and associates to PSI, acting as an additional antenna for this complex. In the reverse process, prefere...

Low-pH induced reversible reorganizations of chloroplast thylakoid membranes — As revealed by small-angle neutron scattering

“…In general, these results, in line with similar observations [29,39,[41][42][43], underline the remarkable flexibility of the thylakoid membrane ultrastructure, which should thus not be portrayed as simply providing a scaffold for the photosynthetic functions but also actively participating in the energy conversion steps and in different regulatory functions.…”

STATE TRANSITION7-Dependent Phosphorylation Is Modulated by Changing Environmental Conditions, and Its Absence Triggers Remodeling of Photosynthetic Protein Complexes

“…Recently, the process of state transitions was revisited in C. reinhardtii (Nagy et al, 2014;Ünlü et al, 2014). Interestingly, these new data indicated that although 70% to 80% of LHCII detached from PSII in state 2 conditions, only a fraction of about 20% was attached to PSI.…”

“…The proportion of mobile LHCII antenna is about 80% in the alga, whereas in Arabidopsis, only 15% to 20% of LHCII is transferred to PSI under state 2 conditions . However, the large increase in PSI antenna size in C. reinhardtii has recently been challenged (Nagy et al, 2014;Ünlü et al, 2014): while 70% to 80% of mobile LHCII detached from PSII in response to transition to state 2 conditions, only a fraction of about 20% functionally attached to PSI.…”

Induction of Photosynthetic Carbon Fixation in Anoxia Relies on Hydrogenase Activity and Proton-Gradient Regulation-Like1-Mediated Cyclic Electron Flow in Chlamydomonas reinhardtii

“…Because state 2 facilitates induction of PSII activity in the absence of hydrogenase , we propose that the increase of PSI antenna size upon state 2 might enhance PSI-CEF rate (Cardol et al, 2009;Alric, 2010Alric, , 2014 and therefore promote ATP synthesis and CBB cycle activity. Nevertheless, the attachment of LHCII to PSI in state 2 has been recently called into question (Nagy et al, 2014;Ünlü et al, 2014). In this .…”