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The biogenesis of photosystem I (PSI), cytochrome  b  6  f  (Cyt b  6  f ) and NADH dehydrogenase (NDH) complexes relies on the spatially and temporally coordinated expression and translation of both nuclear and chloroplast genes. Here we report the identification of photosystem biogenesis regulator 1 (PBR1), a nuclear-encoded chloroplast RNA-binding protein that regulates the concerted biogenesis of NDH, PSI and Cyt b  6  f  complexes. We identified  Ycf1 , one of the two largest chloroplast genome-encoded open reading frames as the direct downstream target protein of PBR1. Biochemical and molecular analyses reveal that PBR1 regulates  Ycf1  translation by directly binding to its mRNA. Surprisingly, we further demonstrate that relocation of the chloroplast gene  Ycf1  fused with a plastid-transit sequence to the nucleus bypasses the requirement of PBR1 for  Ycf1  translation, which sufficiently complements the defects in biogenesis of NDH, PSI and Cyt b  6  f  complexes in  PBR1 -deficient plants. Remarkably, the nuclear-encoded PBR1 tightly controls the expression of the chloroplast gene  Ycf1  at the translational level, which is sufficient to sustain the coordinated biogenesis of NDH, PSI and Cyt b  6  f  complexes as a whole. Our findings provide deep insights into better understanding of how a predominant nuclear-encoded factor can act as a migratory mediator and undergoes selective translational regulation of the target plastid gene in controlling biogenesis of photosynthetic complexes.

PBR1 selectively controls biogenesis of photosynthetic complexes by modulating translation of the large chloroplast gene Ycf1 in Arabidopsis