1 Department of Biology, Concordia University, 7141 Sherbrooke W, Montreal, Quebec, H4B 1R6, Canada.
2 Department of Anatomy and Cell Biology, McGill University, 3640 University, Montreal, Quebec, H3A 0C7, Canada.
3 Lab. of Molecular Genetics, Center for Advanced Biomedical Sciences, Waseda University, Wakamatsu-cho 2-2, Shinjuku-ku, Tokyo 162-0056, Japan.
4 School of Life Sciences, Institute of Life Sciences and Green Development, Hebei University, Baoding, Hebei Province 071002, China.
5 Centre for Microscopy and Cell Imaging, Concordia University, 7141 Sherbrooke W., Montreal, Quebec, H4B 1R6, Canada.

The localization of translation can direct the polypeptide product to the proper intracellular compartment. Our results reveal translation by cytosolic ribosomes on a domain of the chloroplast envelope in the unicellular green alga Chlamydomonas (Chlamydomonas reinhardtii). We show that this envelope domain of isolated chloroplasts retains translationally active ribosomes and mRNAs encoding chloroplast proteins. This domain is aligned with localized translation by chloroplast ribosomes in the translation zone, a chloroplast compartment where photosystem subunits encoded by the plastid genome are synthesized and assembled. Roles of localized translation in directing newly synthesized subunits of photosynthesis complexes to discrete regions within the chloroplast for their assembly are suggested by differences in localization on the chloroplast of mRNAs encoding either subunit of the light-harvesting complex II or the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Transcription of the chloroplast genome is spatially coordinated with translation, as revealed by our demonstration of a subpopulation of transcriptionally active chloroplast nucleoids at the translation zone. We propose that the expression of chloroplast proteins by the nuclear-cytosolic and organellar genetic systems is organized in spatially aligned subcompartments of the cytoplasm and chloroplast to facilitate the biogenesis of the photosynthetic complexes.