Distinct Functions for the Two PsbP-Like Proteins PPL1 and PPL2 in the Chloroplast Thylakoid Lumen of Arabidopsis

Abstract

PsbP, an extrinsic subunit of photosystem II (PSII), is a nuclear-encoded protein that optimizes the water-splitting reaction in vivo. In addition to PsbP, higher plants have two nuclear-encoded genes for PsbP homologs (PsbP-like proteins [PPLs]) that show significant sequence similarity to a cyanobacterial PsbP homolog (cyanoP); however, the function of PPLs in higher plants has not yet been elucidated. In this study, we characterized Arabidopsis (Arabidopsis thaliana) mutants lacking either of two PPLs, PPL1 and PPL2. Phylogenetic analysis suggests that PPL1 would be an ortholog of cyanoP, and PPL2 and PsbP may have a paralogous relationship with PPL1. Analysis on mRNA expression profiles showed that PPL1 expressed under stress conditions and PPL2 coexpressed with the subunits of chloroplast NAD(P)H dehydrogenase (NDH) complex. Consistent with these suggestions, PSII activity in a ppl1 mutant was more sensitive to high-intensity light than wild type, and the recovery of photoinhibited PSII activity was delayed in ppl1 plants. Therefore, PPL1 is required for efficient repair of photodamaged PSII. Furthermore, the stoichiometric level and activity of the chloroplast NDH complex in thylakoids were severely decreased in a ppl2 mutant, demonstrating that PPL2 is a novel thylakoid lumenal factor required for accumulation of the chloroplast NDH complex. These results suggest that during endosymbiosis and subsequent gene transfer to the host nucleus, cyanoP from ancient cyanobacteria evolved into PPL1, PPL2, and PsbP, and each of them has a distinct role in photosynthetic electron transfer in Arabidopsis.

Supercomplex Formation with Photosystem I Is Required for the Stabilization of the Chloroplast NADH Dehydrogenase-Like Complex in Arabidopsis

“…1C). So far, a total of 25 NDH subunits have been identified by various approaches (Rumeau et al, 2005;Ishihara et al, 2007;Ishikawa et al, 2008;Majeran et al, 2008;Shimizu et al, 2008;Peng et al, 2009;Sirpiö et al, 2009aSirpiö et al, , 2009bTakabayashi et al, 2009;Suorsa et al, 2010;Yabuta et al, 2010). If we assume that only one copy of each subunit is included in the complex, the calculated molecular mass of NDH is approximately 690 kD, which is almost identical to that of the NDH complex detected in lhca5 lhca6.…”

Evidence for a Role for NAD(P)H Dehydrogenase in Concentration of CO2 in the Bundle Sheath Cell of Zea mays

“…Studies with Arabidopsis and tobacco have shown that failure to form an active chloroplast NDH complex results in a characteristic change in the kinetics of Chl fluorescence in response to darkening , Rumeau et al, 2005, Munshi et al, 2006, Ishihara et al, 2007, Ishikawa et al2008, Peng et al, 2009, Takabayashi et al, 2009, Suorsa et al, 2010, Yabuta et al, 2010. Figure 2 compares this light-dark transient for the maize mutants ZmNdho and ZmNdhn and respective normal sibling controls.…”

“…At least 11 plastid and 25 nuclear genes encode NDH subunits and related protein factors in Arabidopsis (Ifuku et al, 2011. Serial disruption of several nuclear genes encoding structural subunits or assembly factors resulted in failed NDH supercomplex assembly and disrupted electron flow to PQ (plastoquinone) in the dark (Rumeau et al, 2005, Munshi et al, 2006, Ishihara et al, 2007, Ishikawa et al, 2008, Takabayashi et al, 2009, Peng et al, 2010, Suorsa et al, 2010, Yabuta et al, 2010, Armbruster et al, 2013. Chloroplastic NDH has been assigned to a redundant NAD(P)H-dependent PSI cyclic electron transport pathway in C 3 plants (Nixon 2000).…”

An Orange Ripening Mutant Links Plastid NAD(P)H Dehydrogenase Complex Activity to Central and Specialized Metabolism during Tomato Fruit Maturation

“…Since it has been well established that the presence of all NDH subunits is required for the assembly and functioning of the complex (Rumeau et al, 2005;Ishihara et al, 2007;Shikanaï, 2007aShikanaï, , 2007bSirpiö et al, 2009;Takabayashi et al, 2009), the presence of the Ndh complex in the different genotypes was investigated using an anti-NDH-H (a different subunit of the Ndh complex) antiserum (Figure 4). Compared with the levels of the wild-type protein, the homozygous line retained <10 and 50% of the protein (NDH-H) in leaves and the immature green fruit, respectively ( Figures 4B and 4D).…”

“…Several Arabidopsis mutants affected in these pathways have been studied (Munekage et al, 2002;Rumeau et al, 2005;Ishihara et al, 2007;Shikanaï, 2007a;DalCorso et al, 2008;Peng et al, 2009;Sirpiö et al, 2009;Takabayashi et al, 2009) and showed no change in their carotenoid content. However, participation of PQ redox state in carotenogenesis in other tissues than leaves cannot be excluded.…”