The Low Molecular Weight Protein PsaI Stabilizes the Light-Harvesting Complex II Docking Site of Photosystem I

Abstract

PsaI represents one of three low molecular weight peptides of PSI. Targeted inactivation of the plastid PsaI gene in Nicotiana tabacum has no measurable effect on photosynthetic electron transport around PSI or on accumulation of proteins involved in photosynthesis. Instead, the lack of PsaI destabilizes the association of PsaL and PsaH to PSI, both forming the light-harvesting complex (LHC)II docking site of PSI. These alterations at the LHCII binding site surprisingly did not prevent state transition but led to an increased incidence of PSI-LHCII complexes, coinciding with an elevated phosphorylation level of the LHCII under normal growth light conditions. Remarkably, LHCII was rapidly phosphorylated in DpsaI in darkness even after illumination with far-red light. We found that this dark phosphorylation also occurs in previously described mutants impaired in PSI function or state transition. A prompt shift of the plastoquinone (PQ) pool into a more reduced redox state in the dark caused an enhanced LHCII phosphorylation in DpsaI. Since the redox status of the PQ pool is functionally connected to a series of physiological, biochemical, and gene expression reactions, we propose that the shift of mutant plants into state 2 in darkness represents a compensatory and/or protective metabolic mechanism. This involves an increased reduction and/or reduced oxidation of the PQ pool, presumably to sustain a balanced excitation of both photosystems upon the onset of light.PSI is indisputably the most efficient solar energy converter with a potential quantum efficiency close to 100% (Nelson and Yocum, 2006;Nelson, 2009). It mediates the oxidation of plastocyanin and, subsequently, the reduction of ferredoxin resulting in the production of NADPH. The connection between PSII and PSI in the linear electron transport is provided by the cytochrome b 6 f complex. The electrochemical proton gradient build-up during the light-driven electron transport across the thylakoid membrane provides the proton motive force used for the conversion of ADP to ATP. Besides the linear electron transport, which leads to the production of both ATP and NADPH, PSI is also able to perform cyclic electron transport without the involvement of PSII and resulting solely in the generation of ATP (Yamori and Shikanai, 2016). Two routes of cyclic electron transport exist, the PROTON GRADIENT REGULATION (PGR)5/PGRL1-and the NAD(P)H dehydrogenase (NDH)-dependent pathway providing the possibility to adjust the ATP/NADPH ratio to handle changing metabolic demands and to prevent especially PSI from photoinhibition under challenging light regimes (Munekage et al., 2002;Kramer et al., 2004;Joliot and Johnson, 2011;Suorsa et al., 2012).Although the catalytic core and the function of PSI in cyanobacteria and plants remained very similar since the endosymbiotic event, its structural organization strikingly changed during plant evolution Nelson, 2008, 2009). The size of the entire plant PSI complex increased compared to the cyanobacterial PSI (Jordan et al., 2001;Amun...

Extensive gain and loss of photosystem I subunits in chromerid algae, photosynthetic relatives of apicomplexans

“…The PsaI protein stabilises PsaL in the cyanobacterium Synechocystis 39 ; PsaL and PsaH form a docking site for light-harvesting complex II (LHCII) during state transitions in tobacco 40 and the stability of this site relies on PsaI 41 . PsaI is present in all taxa considered here except for Chromera , Vitrella , Aureococcus , and the secondary green algae Bigelowiella natans and Euglena gracilis (Fig.…”

The plastid-encoded PsaI subunit stabilizes photosystem I during leaf senescence in tobacco

“…Thylakoid membranes were isolated as described previously ( Schöttler et al , 2004 ). The chlorophyll content and a/b ratio were determined in 80% (v/v) acetone according to Porra et al (1989) . The contents of PSII and the b 6 f were determined from difference absorbance signals of cytochrome b 559 (PSII) and the cytochromes b 6 and f in destacked thylakoids equivalent to 50 µg chlorophyll mL −1 ( Kirchhoff et al , 2002 ).…”

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

“…These findings yielded further insights into the reorganization of supercomplexes associated with state transitions, and it was suggested that phosphorylation of LHCB2 rather than LHCB1 is the essential trigger for the formation of state transition supercomplexes (Leoni et al, 2013;Pietrzykowska et al, 2014;Crepin and Caffarri, 2015;Longoni et al, 2015). Furthermore, characterization of mutants deficient in individual PSI core subunits indicates that PsaH, L, and I are required for docking of LHCII at PSI (Lunde et al, 2000;Zhang and Scheller, 2004;Kouril et al, 2005;Plöchinger et al, 2016).…”