Tetratricopeptide repeat protein protects photosystem I from oxidative disruption during assembly

Abstract

A Chlamydomonas reinhardtii mutant lacking CGL71, a thylakoid membrane protein previously shown to be involved in photosystem I (PSI) accumulation, exhibited photosensitivity and highly reduced abundance of PSI under photoheterotrophic conditions. Remarkably, the PSI content of this mutant declined to nearly undetectable levels under dark, oxic conditions, demonstrating that reduced PSI accumulation in the mutant is not strictly the result of photodamage. Furthermore, PSI returns to nearly wild-type levels when the O 2 concentration in the medium is lowered. Overall, our results suggest that the accumulation of PSI in the mutant correlates with the redox state of the stroma rather than photodamage and that CGL71 functions under atmospheric O 2 conditions to allow stable assembly of PSI. These findings may reflect the history of the Earth's atmosphere as it transitioned from anoxic to highly oxic (1-2 billion years ago), a change that required organisms to evolve mechanisms to assist in the assembly and stability of proteins or complexes with O 2 -sensitive cofactors.oxidative disruption | photosystem I biogenesis | photosynthesis | GreenCut

PSA3, a Protein on the Stromal Face of the Thylakoid Membrane, Promotes Photosystem I Accumulation in Cooperation with the Assembly Factor PYG7

“…However, loss of Ycf37 has only a small effect on PSI activity in cyanobacteria (Dühring et al, 2006), contrasting with the severe PSI deficiency observed in mutants lacking PYG7 in Arabidopsis, maize, and Chlamydomonas ( Fig. 7; Stöckel et al, 2006;Heinnickel et al, 2016). PSA3 may have coevolved with PYG7 in photosynthetic eukaryotes to adapt to the increase in oxidative stress resulting from partitioning photosynthesis and respiration into different compartments and from increasing atmospheric O 2 (see discussion in Heinnickel et al [2016]).…”

“…It was recently shown that the PYG7 ortholog in Chlamydomonas is required for PSI accumulation only when cells are grown in the presence of O 2 (Heinnickel et al, 2016). This intriguing finding led to a model in which PYG7 protects PSI from oxidative damage.…”

“…7; Stöckel et al, 2006;Heinnickel et al, 2016). PSA3 may have coevolved with PYG7 in photosynthetic eukaryotes to adapt to the increase in oxidative stress resulting from partitioning photosynthesis and respiration into different compartments and from increasing atmospheric O 2 (see discussion in Heinnickel et al [2016]). The PSI assembly factors PPD1, PSA2, and Y3IP1 are also specific to photosynthetic eukaryotes (Albus et al, 2010;Liu et al, 2012;Fristedt et al, 2014).…”

“…S9). It has been proposed that PYG7 interacts with PsaC to promote PSI assembly or stability (Heinnickel et al, 2016;Yang et al, 2017). Thus, it is reasonable to speculate that PSA3, PYG7, and PsaC are all found in close proximity despite the negative result for a PSA3-PsaC interaction in the yeast two-hybrid assay.…”

“…PPD1 and PSA2 associate with the lumenal face of the thylakoid membrane (Liu et al, 2012;Fristedt et al, 2014;Roose et al, 2014), whereas PYG7 is an integral membrane protein (Stöckel et al, 2006). A recent study of the PYG7 ortholog in Chlamydomonas reported that it is required for PSI biogenesis specifically in the presence of molecular oxygen, which led to a model in which PYG7 shields Fe-S clusters or the cysteines that bind them from oxidation during PSI assembly (Heinnickel et al, 2016). Despite this progress, the biochemical roles of these proteins in PSI biogenesis remain unknown.…”