Distinct functions for the two PsbP-like proteins PPL1 and PPL2 in the chloroplast thylakoid lumen of Arabidopsis.

Seiko Ishihara,Kunio Ido,Tsuyoshi Endo,Kentaro Ifuku,Atsushi Takabayashi,Fumihiko Sato

doi:10.1104/pp.107.105866

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.

Highlights

PsbP, an extrinsic subunit of photosystem II (PSII), is a nuclear-encoded protein that optimizes the water-splitting reaction in vivo
A position-specific iterated-BLAST search of the National Center for Biotechnology Information databases with the sequence of cyanobacterial PsbP homolog (cyanoP) hits eight PsbP homologs in addition to two authentic PsbPs (PsbP1 [At1g06680] and PsbP2 [At2g30790]) in Arabidopsis
We demonstrate that two PPL proteins, PPL1 and PPL2, have distinct functions in the thylakoids in Arabidopsis: PPL1 is required for the efficient repair of photodamaged PSII and PPL2 is crucial for the accumulation of the chloroplastic NAD(P)H dehydrogenase (NDH) complex

Summary

Introduction

PsbP, an extrinsic subunit of photosystem II (PSII), is a nuclear-encoded protein that optimizes the water-splitting reaction in vivo. The stoichiometric level and activity of the chloroplast NDH complex in thylakoids were severely decreased in a ppl 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. PCC6803, cyanoQ is tightly associated with PSII and required for optimal O2 evolution (Roose et al, 2007a), whereas only a small fraction of cyanoP is associated with PSII (Thornton et al, 2004) and its contribution to PSII function is rather small (Ishikawa et al, 2005; Summerfield et al, 2005) These results do not correspond to observations from higher plants, where PsbP is much more important than PsbQ in regulating and stabilizing PSII (Ifuku et al, 2005). Despite this interesting evolutionary feature, molecular function of PsbP homologs in higher plants has been completely unknown

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