A Refined Model of State Transitions in Plant Thylakoid Membranes

Many photosynthetic organisms use state transitions to rapidly balance light absorption by photosystems I and II (PSI and PSII) under varying light conditions (see Lemeille and Rochaix, 2010). During state transitions in plants, a major antenna complex in thylakoid membranes, light-harvesting complex II (LHCII), migrates between the two photosystems. Under State II conditions, when PSII is preferentially excited, LHCII associates with PSI, thereby increasing PSI's absorption capacity. LHCII exists as trimers made up of various combinations of several Lhcb isoforms. Based on their association with PSII, there are at least three different types of LHCII trimers: the strong (S), moderate (M), and loose (L) forms. To date, it has not been established unequivocally which LHCII trimers are involved in state transitions. New work from Galka et al. (2963–2978) characterizes the different forms of LHCII trimers and provides a new view of the mobile LHCII trimers involved in state transitions. Galka et al. optimized a method for isolating PSI-LHCII supercomplexes from plant thylakoid membranes, which has proven difficult in the past. The isolation of pure, stable State II supercomplexes from Arabidopsis thaliana and maize (Zea mays), combined with the authors’ finding that they could use another detergent to dissociate the complexes from each other, allowed them to characterize the supercomplex spectroscopically and biochemically. These analyses demonstrated that LHCII is associated with PSI in the supercomplex under State II conditions such that excitation energy of LHCII is rapidly transferred to PSI. These results are consistent with LHCII being tightly associated with PSI under these conditions. Circular dichroism spectroscopy supported that excitation energy can be transferred between chlorophyll a molecules from the two complexes. Galka et al. asked which LHCII trimer(s) are involved in state transitions. When they compared the Lhcb isoforms in their isolated supercomplex to those of LHCII trimers S and M, they found that neither matched. Thus, although L trimers have not been isolated, it appears that the LHCII trimers involved in state transitions are principally the ones that are loosely associated with PSII in State I. Finally, Galka et al. used electron microscopy to analyze the structure of their isolated PSI-LHCII supercomplex. They found only one type of particle, and it had a 1:1 ratio of PSI and LHCII. Based on their results and previous data, the authors were able to build a model of the supercomplex (see Figure). Together, their data support a refined view of state transitions in which a mobile type of LHCII trimer that is loosely associated with PSII migrates to associate with PSI stably under State II conditions. This view, combined with the much faster transfer of excitation energy from LHCII to PSII than to PSI, suggests that these mobile LHCII trimers could be more rightly viewed as a portion of PSI that migrates to PSII under State I conditions. Overall, this work from Galka et al. provides important new information about the mobile LHCII trimers and the PSI-LHCII supercomplex. Model of the PSI-LHCII supercomplex. The top image shows the electron microscopy map generated from isolated PSI-LHCII supercomplexes. The bottom shows the resulting model of the supercomplex. (Image from Galka et al. [2012].)