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Chloroplast Ribosomes and Protein Synthesis ELIZABETH H MICROBIOLOGICAL REVIEWS, Dec. 1994, p. 700-754 Vol. 58, No. 4 0146-0749/94/$04.00+0 Copyright © 1994, American Society for Microbiology Chloroplast Ribosomes and Protein Synthesis ELIZABETH H. HARRIS,`* JOHN E. BOYNTON,' AND NICHOLAS W. GILLHAM2 DCMB Group, Departments of Botany' and Zoology,2 Duke University, Durham, North Carolina 27708-1000 ORIGIN OF CHLOROPLASTS................................................................ .700 CHLOROPLAST GENOME STRUCTURE AND GENE CONTENT.. ..700 THE PROCESS OF CHLOROPLAST PROTEIN SYNTHESIS........... ..702 'rnl Initiation.....................................................................................................................................t.a..i.....n.... ... .....1.... F' kElongation-s - ........17d 03 .4A04 Chloroplast tRNAs and Aminoacyl-tRNA Synthetases..................................................................... 704 PLASTID GENES FOR rRNAs ..................................................................... 704 Phylogenetic Conservation................................................... .................. 704 General Characteristics of Chloroplast rRNA Gene Organization.........................................*707 16S rRNA ..................................................................... 707 23S rRNA.....................................................................709 5S rRNA..................................................................o..709 Introns in rRNA Genes ..................................................................... 709 The 16S-23SSpacer.................................................................... 712 tRNAs Flanking the rRNA Operons..................................................................... 712 Antibiotic Resistance Mutations in the Chloroplast rRNA Genes......................1.....2.0..................712 RIBOSOMAL PROTEINS.......................................................... ........... 714 Number and Nomenclature ..................................................................... 714 Organization of Chloroplast Ribosomal Protein Genes ....................................... ............*.................715 Correspondence of Chloroplast Ribosomal Proteins to Bacterial Ribosomal Proteins................ ...............716 Proteins of the Small Subunit.....................................................................716 Proteins of the Large Subunit............................................ .......................... 726 Chloroplast Ribosomal Proteins with No Obvious Homology to Those of E. coli ................. 729 Comparative Analysis of Ribosomal Proteins.......................................................30 ASSEMBLY OF CHLOROPLAST RIBOSOMES .....................................................................730 SYNTHESIS OF THE COMPONENTS OF CHLOROPLAST RIBOSOMES .............................................., .. 731 Transcription of rRNA Genes..................................................................731 Transcription of Chloroplast Genes Encoding Ribosomal Proteins .....................................................................732 Posttranscriptional Regulatory Mechanisms Affecting Chloroplast mRNAs.......................... ..........733 Membrane Binding of Chloroplast Ribosomes .....................................................................733 HOW ESSENTIAL IS CHLOROPLAST PROTEIN SYNTHESIS?...........-..................'............... .......... 734 CONCLUSIONS ..................................................................... 735 ACKNOWLEDGMENTS.................... ....................... ...........................735 REFERENCES ....................................................I............"o ..73 ORIGIN OF CHLOROPLASTS among these various taxa have produced intriguing directions for future evolutionary studies, while analysis of ribosomal Chloroplasts and mitochondria contain protein synthesizing- protein sequences, particularly among the diverse algal groups, systems more similar to those of bacteria than to those of the promises. to be a valuable tool for determining conserved eukaryotic cytoplasm, consistent with the hypothesis that these regions likely to have essential functions in ribosome assembly organelles had xenogenous (endosymbiotic) rather than autog- or protein synthesis. enous (intracellular differentiation) origins (see. references 5, 205, 220-223, 274, 633, and 694 for discussions). Phylogenies CHLOROPLAST GENOME STRUCTURE AND based mostly on rRNA sequences indicate that the cyanobac- GENE CONTENT teria are ancestral to chloroplasts while the members of the alpha subdivision of the purple sulfur bacteria are the likely Unlike their prokaryotic ancestors, neither chloroplasts nor progenitors of mitochondria (221, 222). Whether the, chloro- mitochondria are genetically autonomous, and information phyte algae and land plants on the one hand, and the rhodo- specifying components of the organelle protein synthesizing phyte, chromophyte, and euglenoid algae on the other repre- systems is divided between organelle and nucleus. Separation sent more than one endosymbiotic event remains unresolved of the genes encoding these RNAs and proteins between two (130, 403, 434). Comparisons of gene order and arrangement discrete cellular compartments suggests that mechanisms must have evolved to coordinate expression of these genes so that protein synthesis in the organelle can proceed efficiently. * Corresponding author. Mailing address: DCMB, Duke University Whereas chloroplast genomes of land plants usually have a Box 91000, Durham, NC 27708-1000. Phone: (919) 613-8164. Fax: common organization and gene content, a great deal more (919) 613-8177. Electronic mail address: [email protected]. variability is encountered among the algae, particularly with 700 VOL. 58, 1994 CHLOROPLAST RIBOSOMES AND PROTEIN SYNTHESIS 701 Fabaceae (314, 482, 487), which have lost the inverted repeat and thus contain only a single copy of each of the rRNA genes. Black pine (Pinus thunbergii) chloroplast DNA does possess a short inverted repeat sequence, which contains a tRNA gene and part of the 3' portion of the psbA gene, but not the rRNA genes (654). In contrast, species with the largest chloroplast genomes often have expanded inverted repeats (e.g., Pelargo- nium hortorum has a 76-kb inverted repeat encompassing nearly half of the 216-kb chloroplast genome, in which many genes normally in the single-copy region have been duplicated [482]). Chloroplast genomes from land plants specify a relatively constant set of components for the protein-synthesizing ma- chinery of the organelle (4 rRNAs, 30 to 31 tRNAs, 21 ribosomal proteins, and 4 RNA polymerase subunits) and for photosynthesis (28 thylakoid proteins plus 1 soluble protein, the ribulose-1,5-bisphosphate carboxylase/oxygenase [Rubisco] large subunit). In addition, homologs of 11 subunits of mam- malian mitochondrial complex I (the ndh genes) have now been found to be encoded by chloroplast DNA in flowering plants and Marchantia species (9,713). Chloroplast genomes of FIG. 1. Schematic diagram of a typical land plant chloroplast genome (tobacco), showing the positions of the inverted repeat, rRNA gymnosperms, liverworts, and algae (e.g., Chlamydomonas genes, and genes encoding ribosomal proteins. Gene locations are reinhardtii) which synthesize chlorophyll in darkness possess from reference 560. genes encoding three subunits of a light-independent proto- chlorophyllide reductase that is also found in photosynthetic prokaryotes (see reference 367 for a summary). These genes are absent from the tobacco and rice chloroplast genomes. regard to the ribosomal protein genes that have been retained Mapping and sequencing studies of chloroplast genomes in the organelle. In this section we review the chloroplast from widely different algal taxa reveal that these are much genome structure of land plants and the algal genera that have more variable in organization and gene content than those of been investigated to date with respect to composition and land plants. The well-characterized chloroplast genomes of organization of genes encoding rRNAs and ribosomal pro- three species of unicellular green algae in the genus Chlamyd- teins. omonas are substantially larger (C. reinhardtii, 196 kb; C. Chloroplasts are highly polyploid organelles containing cir- eugametos, 243 kb; C. moewusii, 292 kb) than the chloroplast cular DNA molecules of 85 to 200 kb organized into discrete genomes of land plants (42, 43, 50, 247). In these species the membrane-associated nucleoids (see references 50, 206, 260, two copies of the large inverted repeat encoding the rRNAs 337, 482, 483, 558, 613, and 614 for reviews). Three land plant are separated by unique sequence regions of roughly equal chloroplast genomes have been completely sequenced: the size. Chloroplast genes in Chlamydomonas species are also dicotyledon tobacco (Nicotiana tabacum, 156 kb [560, 561]), extensively rearranged between distantly related species and the monocotyledon rice (Oryza sativa, 135 kb [265]); and a with respect to land plants (43). The green alga Spirogyra liverwort (Marchantia polymorpha, 121 kb [471-473]). Each maxima, in the charophyte lineage presumed to be ancestral to contains 110 to 120 genes (482, 614). These sequences, as well land plants, lacks an inverted repeat and shows altered gene as restriction maps and partial sequences from many other order relative to land plants (352, 393). species, indicate that the basic chloroplast genome structure The organization,
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