Functional Analyses of the Plant Photosystem I–Light-Harvesting Complex II Supercomplex Reveal That Light-Harvesting Complex II Loosely Bound to Photosystem II Is a Very Efficient Antenna for Photosystem I in State II

Abstract

State transitions are an important photosynthetic short-term response that allows energy distribution balancing between photosystems I (PSI) and II (PSII). In plants when PSII is preferentially excited compared with PSI (State II), part of the major light-harvesting complex LHCII migrates to PSI to form a PSI-LHCII supercomplex. So far, little is known about this complex, mainly due to purification problems. Here, a stable PSI-LHCII supercomplex is purified from Arabidopsis thaliana and maize (Zea mays) plants. It is demonstrated that LHCIIs loosely bound to PSII in State I are the trimers mainly involved in state transitions and become strongly bound to PSI in State II. Specific Lhcb1-3 isoforms are differently represented in the mobile LHCII compared with S and M trimers. Fluorescence analyses indicate that excitation energy migration from mobile LHCII to PSI is rapid and efficient, and the quantum yield of photochemical conversion of PSI-LHCII is substantially unaffected with respect to PSI, despite a sizable increase of the antenna size. An updated PSI-LHCII structural model suggests that the lowenergy chlorophylls 611 and 612 in LHCII interact with the chlorophyll 11145 at the interface of PSI. In contrast with the common opinion, we suggest that the mobile pool of LHCII may be considered an intimate part of the PSI antenna system that is displaced to PSII in State I.

On the origin of a slowly reversible fluorescence decay component in the Arabidopsis npq4 mutant

“…These data are consistent with the behaviour of npq4ch1 that lacks Chlb, and is thus devoid of all LHCs [37,38]; the slow phase of NPQ relaxation was found to be independent of LHC composition, indeed qM amplitude was similar in npq4 and npq4ch1 mutants ( figure 3e and table 2). State transitions lead to quenching of LHCII fluorescence by PSI [39] upon phosphorylation of LHCII, by STN7 kinase, driving its migration from PSII to PSI [40]; by using the mutant npq4stn7, we checked the possibility that state transition were involved in qM. The maximal amplitude of NPQ in npq4stn7 was essentially the same as in npq4 plants (figure 3f).…”

Phosphorylation of the Lhcb2 isoform of Light Harvesting Complex II is central to state transitions

“…Previous reports have shown that the relative phosphorylation of Lhcb1 and Lhcb2 isoforms differs among thylakoid supercomplexes (Galka et al, 2012;Leoni et al, 2013). Here, we address the specific roles of Lhcb1 and Lhcb2 phosphorylation in photosynthetic acclimation.…”

“…The PSI-LHCII complex assembles in state 2 and involves the binding of a mobile trimer, which contains Lhcb1 and Lhcb2 (Galka et al, 2012), to the PSI complex. This association depends on the kinase STN7.…”

“…In the LHCII trimers of these supercomplexes, different classes of Lhcb subunits are distributed differently, suggesting a specific role in light acclimation for each of them (Damkjaer et al, 2009;Pietrzykowska et al, 2014). In the stably bound S trimer, Lhcb1 and Lhcb2 are more abundant, whereas the moderately bound M trimer contains mostly Lhcb1 and Lhcb3 (Galka et al, 2012). PSII supercomplexes isolated from spinach (Spinacia oleracea) showed the presence of an extra LHCII trimer (L trimer); therefore, it is possible that, in Arabidopsis, other trimers are associated with the PSII dimer in a more labile supercomplex that cannot be isolated (Boekema et al, 1999).…”

“…PSII supercomplexes isolated from spinach (Spinacia oleracea) showed the presence of an extra LHCII trimer (L trimer); therefore, it is possible that, in Arabidopsis, other trimers are associated with the PSII dimer in a more labile supercomplex that cannot be isolated (Boekema et al, 1999). A single LHCII trimer, containing Lhcb1 and Lhcb2, stably associates with PSI to constitute the PSI-LHCII supercomplex, whose formation is dependent on LHCII phosphorylation by STN7 in state 2 (Kouril et al, 2005;Galka et al, 2012).…”