An intact light harvesting complex I antenna system is required for complete state transitions in Arabidopsis

Abstract

Abstract:Efficient photosynthesis depends on balancing the rate of light-driven electron transport occurring in the photosystem I (PSI) and photosystem II (PSII) reaction centers of plant chloroplast thylakoid membranes. Balance is achieved through a process called state transitions which, via redox control of the phosphorylation state of light harvesting antenna complex II (LHCII), increases its energy transfer towards PSI (State II) when PSII is overexcited, and vice versa (State I). In addition to LHCII, PSI is also served by four light harvesting antenna complex I (LHCI) subunits, Lhca1, 2, 3 and 4. Here we demonstrate that despite unchanged levels of LHCII phosphorylation, absence of specific Lhca subunits in the Lhca1, 2, 3 and 4 mutants reduces state transitions in Arabidopsis. The severest phenotype is observed in Lhca4, with a 69% reduction compared to the wild-type. Surprisingly, the amounts of the PSI-LHCI-LHCII supercomplex isolated by native-PAGE from digitonin-solubilized thylakoids were similar in the wild-type and Lhca mutants. Fluorescence excitation spectroscopy revealed that in the wildtype this PSI-LHCI-LHCII supercomplex is supplemented by energy transfer from additional LHCII trimers in State II, whose binding is sensitive to digitonin, and which are absent in Lhca4. The grana margins of the thylakoid membrane were found to be the primary site of interaction between this 'extra' LHCII and the PSI-LHCI-LHCII supercomplex in State II. The results suggest that the LHCI complexes mediate energetic interactions between the 'extra' LHCII and PSI in the intact membrane.3

Comparative Analysis of Light-Harvesting Antennae and State Transition in chlorina and cpSRP Mutants

“…In mutants defective in LHCI formation, only PSI core complexes are observed (Havaux et al, 2007;Wientjes et al, 2009;Takabayashi et al, 2011;Benson et al, 2015). A dominant band of PSI core complexes was observed in the chaos mutant (Fig.…”

“…1 and 2) led to further exploration of the association of LHCII with PSI or PSII during state transitions. It was recently shown that an intact LHCI complex is required for a complete state I-to-state II transition (Benson et al, 2015). To explore these findings further, we compared state transitions in ch1-2 and chaos with control seedlings.…”

“…The localization of P-LHCII could result from a failure to dissociate from PSII or an inability to dock at PSI. The latter prospect is challenged by the elevated accumulation of LHCII-PSI core complexes in the lhca4 mutant (Benson et al, 2015) and the DLhca mutant (Bressan et al, 2016), which were adapted to state II conditions. Structural studies of LHCII-PSI-LHCI complexes showed an opposite localization of P-LHCII and LHCI within the statetransition supercomplexes (Kouril et al, 2005;Drop et al, 2014).…”

“…Although the Arabidopsis knock-out mutants lacking one of the four LHCI proteins (LHCA1-4) showed enhanced accumulation of LHCII-PSI complexes, the absorption crosssection of PSI under state II conditions was still compromised in the lhca1-4 mutants, and it is suggested that LHCI mediates the detergent-sensitive interaction between 'extra LHCII' and PSI (Benson et al, 2015;Grieco et al, 2015). Furthermore, the Arabidopsis mutant DLhca lacking all LHCA1-4 proteins was shown to be compensated for the deficiency of LHCI by binding LHCII under state II conditions (Bressan et al, 2016).…”

“…Intriguingly, we found that impaired Chl b biosynthesis in chlorina1-2 (ch1-2) led to preferentially stabilized LHCI rather than LHCII, while the contents of both LHCI and LHCII were equally depressed in the cpSRP43-deficient mutant (chaos). In view of recent findings on the modified state transitions in LHCI-deficient mutants (Benson et al, 2015), the ch1-2 and chaos mutants were used to assess the influence of varying LHCI/LHCII antenna size on state transitions. Under state II conditions, LHCII-PSI supercomplexes were not formed in both ch1-2 and chaos plants.…”