A Thylakoid Membrane Protein Harboring a DnaJ-type Zinc Finger Domain Is Required for Photosystem I Accumulation in Plants

Rikard Fristedt,Rosalind Williams-Carrier,Sabeeha S Merchant,Alice Barkan

doi:10.1074/jbc.m114.587758

Rikard Fristedt, Rosalind Williams-Carrier + Show 2 more

Open Access

https://doi.org/10.1074/jbc.m114.587758

Copy DOI

Abstract

Photosystem I (PSI) is a large pigment-protein complex and one of the two photosystems that drive electron transfer in oxygenic photosynthesis. We identified a nuclear gene required specifically for the accumulation of PSI in a forward genetic analysis of chloroplast biogenesis in maize. This gene, designated psa2, belongs to the "GreenCut" gene set, a group of genes found in green algae and plants but not in non-photosynthetic organisms. Disruption of the psa2 ortholog in Arabidopsis likewise resulted in the specific loss of PSI proteins. PSA2 harbors a conserved domain found in DnaJ chaperones where it has been shown to form a zinc finger and to have protein-disulfide isomerase activity. Accordingly, PSA2 exhibited protein-disulfide reductase activity in vitro. PSA2 localized to the thylakoid lumen and was found in a ∼250-kDa complex harboring the peripheral PSI protein PsaG but lacking several core PSI subunits. PSA2 mRNA is coexpressed with mRNAs encoding various proteins involved in the biogenesis of the photosynthetic apparatus with peak expression preceding that of genes encoding structural components. PSA2 protein abundance was not decreased in the absence of PSI but was reduced in the absence of the PSI assembly factor Ycf3. These findings suggest that a complex harboring PSA2 and PsaG mediates thiol transactions in the thylakoid lumen that are important for the assembly of PSI.

Highlights

Photosystem I is a large protein/pigment assembly required for photosynthesis
The GreenCut Gene psa2 Is Required for the Accumulation of Photosystem I in Maize and Arabidopsis—The psa2 gene was identified during the systematic analysis of mutants in the Photosynthetic Mutant Library, a large collection of chloroplastdefective mutants that arose in maize lines with active Mu transposons [17]
A role in Photosystem I (PSI) assembly rather than PSI homeostasis is supported by (i) the fact that PSA2 was required for PSI accumulation even after prolonged dark adaptation (Fig. 3A), (ii) the loss of PSA2 in a mutant lacking the PSI assembly factor Ycf3 (Fig. 5C), and (iii) the coexpression of PSA2 with proteins known to function in the assembly of the photosynthetic apparatus

Summary

Background

Results: The PSA2 protein harbors a DnaJ-type zinc finger domain, is required for Photosystem I accumulation, and is found in a PsaG-containing complex in the thylakoid lumen. We identified a nuclear gene required for the accumulation of PSI in a forward genetic analysis of chloroplast biogenesis in maize This gene, designated psa, belongs to the “GreenCut” gene set, a group of genes found in green algae and plants but not in non-photosynthetic organisms. PSA2 protein abundance was not decreased in the absence of PSI but was reduced in the absence of the PSI assembly factor Ycf3 These findings suggest that a complex harboring PSA2 and PsaG mediates thiol transactions in the thylakoid lumen that are important for the assembly of PSI.

EXPERIMENTAL PROCEDURES

RESULTS

DISCUSSION