REVIEW Folia Microbiol. 54 (4), 303–321 (2009) http://www.biomed.cas.cz/mbu/folia/ On the Origin of Chloroplasts, Import Mechanisms of Chloroplast-Targeted Proteins, and Loss of Photosynthetic Ability — review M. VESTEG, R. VACULA, J. KRAJČOVIČ* Institute of Cell Biology, Faculty of Natural Science, Comenius University, 842 15 Bratislava, Slovakia Received 19 November 2008 Revised version 31 March 2009 ABSTRACT. Primary plastids of green algae (including land plants), red algae and glaucophytes are boun- ded by two membranes and are thought to be derived from a single primary endosymbiosis of a cyanobacte- rium in a eukaryotic host. Complex plastids of euglenids and chlorarachneans bounded by three and four membranes, respectively, most likely arose via two separate secondary endosymbioses of a green alga in a eukaryotic host. Secondary plastids of cryptophyta, haptophyta, heterokontophyta and apicomplexan para- sites bounded by four membranes, and plastids of dinoflagellates bounded by three membranes could have arisen via a single secondary endosymbiosis of a red alga in a eukaryotic host (chromalveolate hypothesis). However, the scenario of separate tertiary origins (symbioses of an alga possessing secondary plastids in a eukaryotic host) of some (or even most) chromalveolate plastids can be also consistent with the current data. The protein import into complex plastids differs from the import into primary plastids, as complex plastids contain one or two extra membrane(s). In organisms with primary plastids, plastid-targeted proteins contain N-terminal transit peptide which ferries proteins through the protein import machineries (multipro- tein complexes) of the two (originally cyanobacterial) membranes. In organisms with complex plastids, the secretory signal sequence directing proteins to endomembrane system and afterwards through extra outer- most membrane(s) is generally present upstream of the classical transit peptide. Several free-living as well as parasitic eukaryotes possess non-photosynthetic plastids. These plastids have generally retained the plastid genome, functional plastid transcriptional and translational apparatus, and various metabolic pathways, suggesting that though these plastids lost their photosynthetic ability, they are essential for the mentioned orga- nisms. Nevertheless, some eukaryotes could have lost chloroplast compartment completely. Abbreviations ER endoplasmic reticulum rpl36 chloroplast gene encoding ribosomal protein L36 ERAD ER-associated degradation Rubisco SSU small subunit of ribulose-1,5-bisphosphate FBA fructose-1,6-bisphosphate aldolase carboxylase/oxygenase GAPDH glyceraldehyde-3-phosphate dehydrogenase Toc translocon of the chloroplast outer membrane PRK phosphoribulokinase Tic translocon of the chloroplast inner membrane rbcL gene encoding large subunit of ribulose 1,5-bisphosphate carboxylase/oxygenase CONTENTS 1 Introduction 304 2 Primary plastids 304 3 Secondary plastids 306 4 Origin of chlorarachnean and euglenoid plastids 307 5 Complex plastids of red algal origin 308 5.1 Chromalveolate hypothesis 309 5.2 Tertiary endosymbioses, plastid losses and replacements 309 6 Import of proteins into plastids 311 6.1 Presequences and translocons 311 6.2 Protein import into plastids bounded by four membranes 312 6.3 Protein import into plastids bounded by three membranes 313 7 Multiple losses of photosynthetic ability 314 7.1 Reductive evolution of plastids in euglenids 314 7.2 Examples of non-photosynthetic plastids 314 7.3 Loss of chloroplasts in trypanosomatids? 315 7.4 Reduced mitochondria 316 8 Concluding remarks 316 References 316 *Corresponding author; e-mail krajcovic@fns.uniba.sk .