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Duplications and rearrangements of coding genes are major themes in the evolution of mitochondrial genomes, bearing important consequences in the function of mitochondria and the fitness of organisms. Yu et al. (BMC Genomics 2008, 9:477) reported the complete mt genome sequence of the oyster Crassostrea hongkongensis (16,475 bp) and found that a DNA segment containing four tRNA genes (trnK1, trnC, trnQ1 and trnN), a duplicated (rrnS) and a split rRNA gene (rrnL5') was absent compared with that of two other Crassostrea species. It was suggested that the absence was a novel case of "tandem duplication-random loss" with evolutionary significance. We independently sequenced the complete mt genome of three C. hongkongensis individuals, all of which were 18,622 bp and contained the segment that was missing in Yu et al.'s sequence. Further, we designed primers, verified sequences and demonstrated that the sequence loss in Yu et al.'s study was an artifact caused by placing primers in a duplicated region. The duplication and split of ribosomal RNA genes are unique for Crassostrea oysters and not lost in C. hongkongensis. Our study highlights the need for caution when amplifying and sequencing through duplicated regions of the genome.

The positions of post-transcriptionally methylated residues within hamster mitochondrial ribosomal RNA have been established. Comparisons with other mitochondrial rRNA, and with bacterial, eucaryotic and chloroplast rRNA show that the methylated regions i) are comprised of conserved primary sequences and/or secondary structures and ii) are situated at the subunit interface of the ribosome. The comparative analyses also reveal that the ribose-methylated sequence UmGmU of hamster mitochondrial large ribosomal subunit (LSU1) RNA lies in a universally conserved hairpin loop which contains a putative puromycin-reactive nucleotide. The "UmGmU hairpin" is within 100 nucleotides of two chloramphenicol-resistance residues of LSU RNA. We present a secondary structure for this region which is conserved in LSU RNAs. This structure allows physical juxtaposition of the three antibiotic-interacting loci and thus defines RNA components of the ribosomal-binding site for the 3'-terminus of aminoacyl-tRNA.

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The nucleotide sequence of the gene coding for the 18S ribosomal RNA of maize mitochondria has been determined and a model for the secondary structure is proposed. Dot matrix analysis has been used to compare the extent and distribution of sequence similarities of the entire maize mitochondrial 18S rRNA sequence with that of 15 other small subunit rRNA sequences. The mitochondrial gene shows great similarity to the eubacterial sequences and to the maize chloroplast, and less similarity to mitochondrial rRNA genes in animals and fungi. We propose that this similarity is due to a slow rate of nucleotide divergence in plant mtDNA compared to the mtDNA of animals. Sequence comparisons indicate that the evolution of the maize mitochondrial 18S, chloroplast 16S and nuclear 17S ribosomal genes have been essentially independent, in spite of evidence for DNA transfer between organelles and the nucleus.

Sequences similar to mitochondrial large and small subunit rRNAs are found as small scattered fragments on a tandemly reiterated 6 kb element in the human malaria parasite Plasmodium falciparum. The rDNA sequences previously identified include strongly conserved portions of rRNA, suggesting that fragmented rRNAs derived from them are able to associate into functional ribosomes. However, sequences corresponding to other expected rRNA regions were not found. We here report that 10 of the 13 previously described rDNA regions have abundant small transcripts. An additional 10 transcripts were found from regions not previously known to contain genes. Five of the latter have been identified as rRNA fragments, including those corresponding to the 5'end and 790 loop sequences of small subunit rRNA and the sarcin/ ricin loop of large subunit rRNA. Demonstration that most of the previously described rDNA regions have abundant transcripts and the identification of new transcripts with other portions of conventional rRNAs provide support for the hypothesis that these small transcripts comprise functional rRNAs.

One potential approach for characterizing uncultivated prokaryotes from natural assemblages involves genomic analysis of DNA fragments retrieved directly from naturally occurring microbial biomass. In this study, we sought to isolate large genomic fragments from a widely distributed and relatively abundant but as yet uncultivated group of prokaryotes, the planktonic marine Archaea. A fosmid DNA library was prepared from a marine picoplankton assemblage collected at a depth of 200 m in the eastern North Pacific. We identified a 38.5-kbp recombinant fosmid clone which contained an archaeal small subunit ribosomal DNA gene. Phylogenetic analyses of the small subunit rRNA sequence demonstrated it close relationship to that of previously described planktonic archaea, which form a coherent group rooted deeply within the Crenarchaeota branch of the domain Archaea. Random shotgun sequencing of subcloned fragments of the archaeal fosmid clone revealed several genes which bore highest similarity to archaeal homologs, including large subunit ribosomal DNA and translation elongation factor 2 (EF2). Analyses of the inferred amino acid sequence of archaeoplankton EF2 supported its affiliation with the Crenarchaeote subdivision of Archaea. Two gene fragments encoding proteins not previously found in Archaea were also identified: RNA helicase, responsible for the ATP-dependent alteration of RNA secondary structure, and glutamate semialdehyde aminotransferase, an enzyme involved in initial steps of heme biosynthesis. In total, our results indicate that genomic analysis of large DNA fragments retrieved from mixed microbial assemblages can provide useful perspective on the physiological potential of abundant but as yet uncultivated prokaryotes.

The cultivated Pacific oyster Crassostrea gigas has suffered for decades large scale summer mortality phenomenon resulting from the interaction between the environment parameters, the oyster physiological and/or genetic status and the presence of pathogenic microorganisms including Vibrio species. To obtain a general picture of the molecular mechanisms implicated in C. gigas immune responsiveness to circumvent Vibrio infections, we have developed the first deep sequencing study of the transcriptome of hemocytes, the immunocompetent cells. Using Digital Gene Expression (DGE), we generated a transcript catalog of up-regulated genes from oysters surviving infection with virulent Vibrio strains (Vibrio splendidus LGP32 and V. aestuarianus LPi 02/41) compared to an avirulent one, V. tasmaniensis LMG 20012T. For that an original experimental infection protocol was developed in which only animals that were able to survive infections were considered for the DGE approach. We report the identification of cellular and immune functions that characterize the oyster capability to survive pathogenic Vibrio infections. Functional annotations highlight genes related to signal transduction of immune response, cell adhesion and communication as well as cellular processes and defence mechanisms of phagocytosis, actin cytosqueleton reorganization, cell trafficking and autophagy, but also antioxidant and anti-apoptotic reactions. In addition, quantitative PCR analysis reveals the first identification of pathogen-specific signatures in oyster gene regulation, which opens the way for in depth molecular studies of oyster-pathogen interaction and pathogenesis. This work is a prerequisite for the identification of those physiological traits controlling oyster capacity to survive a Vibrio infection and, subsequently, for a better understanding of the phenomenon of summer mortality.

RNA editing occurs in two higher-plant organelles, chloroplasts and mitochondria. Because chloroplasts and mitochondria exhibit some similarity in editing site selection, we investigated whether mitochondrial RNA sequences could be edited in chloroplasts. We produced transgenic tobacco plants that contained chimeric genes in which the second exon of a Petunia hybrida mitochondrial coxII gene was under the control of chloroplast gene regulatory sequences. coxII transcripts accumulated to low or high levels in transgenic chloroplasts containing chimeric genes with the plastid ribosomal protein gene rps16 or the rRNA operon promoter, respectively. Exon 2 of coxII was chosen because it carries seven editing sites and is edited in petunia mitochondria even when located in an abnormal context in an aberrant recombined gene. When editing of the coxII transcripts in transgenic chloroplasts was examined, no RNA editing at any of the usual sites was detected, nor was there any novel editing at any other sites. These results indicate that the RNA editing mechanisms of chloroplasts and mitochondria are not identical but must have at least some organelle-specific components.

S-adenosyl-l-methionine-dependent rRNA dimethylases mediate the methylation of two conserved adenosines near the 3′ end of the rRNA in the small ribosomal subunits of bacteria, archaea and eukaryotes. Proteins related to this family of dimethylases play an essential role as transcription factors (mtTFBs) in fungal and animal mitochondria. Human mitochondrial rRNA is methylated and human mitochondria contain two related mtTFBs, one proposed to act as rRNA dimethylase, the other as transcription factor. The nuclear genome of Arabidopsis thaliana encodes three dimethylase/mtTFB-like proteins, one of which, Dim1B, is shown here to be imported into mitochondria. Transcription initiation by mitochondrial RNA polymerases appears not to be stimulated by Dim1B in vitro. In line with this finding, phylogenetic analyses revealed Dim1B to be more closely related to a group of eukaryotic non-mitochondrial rRNA dimethylases (Dim1s) than to fungal and animal mtTFBs. We found that Dim1B was capable of substituting the E. coli rRNA dimethylase activity of KsgA. Moreover, we observed methylation of the conserved adenines in the 18S rRNA of Arabidopsis mitochondria; this modification was not detectable in a mutant lacking Dim1B. These data provide evidence: (i) for rRNA methylation in Arabidopsis mitochondria; and (ii) that Dim1B is the enzyme catalyzing this process.

The DNA sequence around the beginning of the genes coding for the large and small ribosomal RNAs in yeast mitochondria has been established. In order to determine the 5'-end points of the ribosomal RNAs, DNA fragments were labelled in vitro at a restriction site within each gene and hybridized with ribosomal RNA. The hybrids were then treated with S1 nuclease and the products analysed for size by gel electrophoresis. This enabled us to identify where in the determined DNA sequence the 21S ribosomal RNA and the precursor for 15S ribosomal RNA (15.5S rRNA) start, since both transcripts are initiated de novo (Levens et al. (1981) J.Biol.Chem., 256, 5226-5232). Comparison of the DNA sequences around the start points of transcription reveals the existence of a homologous stretch of 17 nucleotides. This conserved sequence may be an essential element of a promoter in mtDNA.

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The 220 3'-terminal nucleotides of the small ribosomal subunit RNA (13S) of hamster (BHK-21) cell mitochondria have been sequenced and the positions of post-transcriptionally methylated residues within this sequence have been established. Also, we have derived the secondary structure of the 3'-terminus of mitochondrial 13S rRNA by 1) searching nucleotide sequences of 13S rRNA, procaryotic 16S rRNA and eucaryotic 18S rRNA for common secondary structures and 2) using single-strand specific endonucleases to map secondary interactions in 13S rRNA. The pyrimidine tract CCUCC in E. coli 16S rRNA, which participates in base-pairing with bacterial mRNA, is absent in mitochondrial 13S rRNA. We believe that the binding of mRNA to mammalian mitochondrial ribosomes is not mediated by a conventional Shine-Dalgarno interaction.

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A cDNA clone that encodes the large subunit of mitochondrial ribosomal RNA (LSU rRNA) from the liver fluke F. hepatica was isolated and characterized. This RNA molecule is polyadenylated at the 3' end and represents 10% of the poly A+RNA in adult F. hepatica. Fluke LSU rRNA has significant sequence homology to mosquito mitochondria LSU rRNA and is more closely related to the mitochondrial rRNA of hermaphroditic than dioecious trematodes. Mitochondrial DNA constitutes approximately 10% of the total cellular DNA of adult flukes. This percentage is lower in non-embryonated eggs as are the levels of LSU rRNA indicating eggs have lower metabolic activity. Analysis of transcription and the number of mitochondrial genomes in S. mansoni shows that the LSU rRNA is more abundant in females than in males. Restriction endonuclease analysis of the fluke mitochondrial LSU rRNA genes suggests the presence of heterogeneous repeated copies in the mitochondrial genome or heterogeneity among individual genomes of mitochondria.

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The synthesis and processing of the 15S and 21S rRNAs have been studied in isolated yeast mitochondria. When mitochondrial transcripts were labeled with [alpha-32p]UTP in an incubation mixture containing 50 microM ATP, the transcripts from the genes for the large and small ribosomal RNAs accumulated in the form of putative precursor molecules. The labeled pre-21S rRNA was converted to mature 21S rRNA during a chase period in the presence of 1 mM ATP. Thus, the maturation of 21S rRNA, a process which includes trimming at the 3' end and, in omega+ strains, the excision of a 1.1 kb intervening sequence, can occur in isolated mitochondria and appears to be dependent on ATP. In contrast, the maturation of 15S rRNA by the removal of approximately 80 nucleotides from the 5' end of a 15.5S transcript is severely restricted in isolated mitochondria, even in the presence of 2.5 mM ATP.

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A cloned fragment of spinach chloroplast DNA carrying 140 bp of the 16S rRNA gene and 691 bp upstream this gene has been analysed by DNA sequencing, by in vitro transcription, by S1 mapping with chloroplast RNAs and purified 16S rRNA from 30S ribosomal subunits. A tRNAVal gene has been located between the position 394 and 465. Crude chloroplast RNA polymerase has been purified by heparin sepharose chromatography of a 80 000 g supernatant from pure lysed spinach plastids and used to transcribe the cloned Bg1 II-Pvu II DNA fragment. Four in vitro transcripts of about 830, 550, 350 and 260 bases were obtained whatever RNA polymerase used: the chloroplast or the E. coli enzyme. The transcripts of 550 and 260 bases are initiated by ATP. S1 mapping with in vivo chloroplasts RNAs on 5' labelled separated strands from Bg1 II-Pvu II fragments indicates 2 protected DNA fragments respectively of 140 and 260 bases on the strand which codes for rRNAs and possibly one protected DNA fragment of 550 bases on the other strand. The start site of the 260 bases transcript might correspond to the initiation site of transcription of the rRNA genes. The possibility that the 550 bases transcription of the non coding strand for rRNA genes corresponds to the beginning of a mRNA is discussed.

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In humans, cellular 28S rRNA displays a sequence dimorphism within an evolutionarily conserved motif, with the presence, at position +60, of either a A (like the metazoan consensus) or a G. The relative abundance of the two forms of variant genes in the genome exhibit large differences among individuals. The two variant forms are generally represented in cellular 28S rRNA in proportion of their relative abundance in the genome, at least for leucocytes. However, in some cases, one form of variant may be markedly underexpressed as compared to the other. Thus, in HeLa cells, A-form genes contribute to only 1% of the cellular content in mature 28S rRNA although amounting to 15% of the ribosomal genes. The differential expression seems to result from different transcriptional activities rather than from differences in pre-rRNA processing efficiency or in stabilities of mature rRNAs. G-form ribosomal genes were not detected in other mammals, including chimpanzee, which suggests that the fixation of this variant type is a rather recent event in primate evolution.

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Short base-paired RNA fragments, and fragments containing intra-RNA cross-links, were isolated from E. coli 23S rRNA or 50S ribosomal subunits by two-dimensional gel electrophoresis. The interactions thus found were used as a first basis for constructing a secondary structure model of the 23S rRNA. Sequence comparison with the 23S rDNA from Z. mays chloroplasts, as well as with the 16S (large subunit) rDNA from human and mouse mitochondria, enabled the experimental model to be improved and extrapolated to give complete secondary structures of all four species. The structures are organized in well-defined domains, with over 450 compensating base changes between the two 23S species. Some ribosomal structural "'switches" were found, one involving 5S rRNA.

We present a catalog of sequences of oligonucleotides produced by T1 ribonuclease digestion of 32P-labeled small-ribosomal-subunit RNA ("18S rRNA) isolated from purified wheat embryo mitochondria. This catalog is compared to catalogs published for prokaryotic and chloroplast 16S rRNAs and to preliminary results for wheat cytosol 18S rRNA. These comparisons indicate that: (1) wheat mitochondrial 18S rRNA is clearly prokaryotic in nature, showing significantly more sequence homology with 16S rRNAs than can be expected to arise by chance (p less than 0.000001); (2) shared oligonucleotide sequences include an especially high proportion of those identified as conserved in the evolution of prokaryotic rRNAs; and (3) wheat embryo mitochondrial and cytosol 18S rRNAs retain no more, and perhaps less, than the minimum sequence homology detectable by this sensitive method. These results argue in favor of an endosymbiotic origin for mitochondria.

Comparative sequence analysis of 16S rRNA genes was used to determine the phylogenetic relationship of the genus Cristispira to other spirochetes. Since Cristispira organisms cannot presently be grown in vitro, 16S rRNA genes were amplified directly from bacterial DNA isolated from Cristispira cell-laden crystalline styles of the oyster Crassostrea virginica. The amplified products were then cloned into Escherichia coli plasmids. Sequence comparisons of the gene coding for 16S rRNA (rDNA) insert of one clone, designated CP1, indicated that it was spirochetal. The sequence of the 16S rDNA insert of another clone was mycoplasmal. The CP1 sequence possessed most of the individual base signatures that are unique to 16S rRNA (or rDNA) sequences of known spirochetes. CP1 branched deeply among other spirochetal genera within the family Spirochaetaceae, and accordingly, it represents a separate genus within this family. A fluorescently labeled DNA probe designed from the CP1 sequence was used for in situ hybridization experiments to verify that the sequence obtained was derived from the observed Cristispira cells.

When two species of shellstock oysters were artificially contaminated with Vibrio vulnificus, the bacterium survived when the oysters were stored at 10 degrees C and below. Large numbers of endogenous V. vulnificus cells were found after 7 days at both 0.5 and 10 degrees C in uninoculated control oysters (Crassostrea virginica). Oysters allowed to take up V. vulnificus from seawater retained the bacterium for 14 days at 2 degrees C. The presence of V. vulnificus in the drip exuded from the shellstock presented a possibility of contamination of other shellstock in storage. V. vulnificus injected into shucked Pacific (Crassostrea gigas) and Eastern (C. virginica) oysters survived at 4 degrees C for at least 6 days. An 18-h most-probable-number enrichment step in alkaline peptone water gave higher recovery levels of V. vulnificus than did direct plating to selective agars. The survival of this pathogen in both shellstock and shucked oysters suggests a potential for human illness, even though the product is refrigerated.

Ribosomal DNA fragments from the human malaria parasite Plasmodium falciparum have been cloned and analysed in detail. Restriction mapping shows that the cloned fragments are different. However, they do have some similarities, in particular a small stretch of A+T-rich DNA located between the small and large subunit rRNA genes. A small rRNA gene has been mapped to this A+T-rich region. Copy number analysis reveals that each fragment is represented approximately 4 times in the genome, and implies that there are a total of 8 rRNA genes organised into at least two classes of transcription unit. Analysis of a third overlapping rDNA fragment indicates that the large subunit rRNA gene of at least one transcription unit contains an intervening sequence.

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The DNA sequence has been determined of the 3' terminus from the mitochondrial large subunit ribosomal RNA (LSUrRNA) gene of the eukaryotic green alga Scenedesmus obliquus (strain KS3/2). The gene contains two intervening sequences with characteristic sequence motifs of group II and group I introns respectively. The exon/intron boundaries of the introns have been revealed by sequence determination of the mature rRNA. During RNA processing of the precursor RNA, several abundant RNA molecules are stably maintained in addition to the mature rRNA in vivo. In vitro transcripts of the LSUrRNA gene containing the group II intron (608 bp) display a strong 'self-splicing' activity under high salt conditions. The 608 bp intron is the first group II intron reported to be integrated into a LSUrRNA gene and represents the smallest self-splicing group II intron from eukaryotic organelles so far described.

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Protein translation is essential for all forms of life and is conducted by a macromolecular complex, the ribosome. Evolutionary changes in protein and RNA sequences can affect the three-dimensional organization of structural features in ribosomes in different species. The most dramatic changes occur in animal mitochondria, whose genomes have been significantly reduced and altered. The RNA component of the mitochondrial ribosome (mitoribosome) is reduced in size, with a compensatory increase in protein content. Until recently, it was unclear how these changes affect the three-dimensional structure of the mitoribosome. Here we present a structural model of the large subunit (LSU) of the mammalian mitoribosome developed by combining molecular modeling techniques with cryo-electron microscopic (cryo-EM) studies. The model contains 93% of the mitochondrial rRNA (mito-rRNA) sequence and 16 mitochondrial ribosomal proteins (MRPs) in the large subunit of the mitoribosome. Despite the smaller mitochondrial rRNA, the spatial positions of RNA domains known to be directly involved in protein synthesis are essentially the same as in Bacterial and Archaeal ribosomes. However, the dramatic reduction in rRNA content necessitates evolution of unique structural features to maintain connectivity between RNA domains. The smaller rRNA sequence also limits the likelihood of tRNA binding at E-site of the mitoribosome, and correlates with the reduced size of D- and T-loops in some animal mitochondrial tRNAs, suggesting co-evolution of mitochondrial rRNA and tRNA structures.

Ninety-four percent of human genes are discontinuous such that segments expressed as mRNA are contained within exons and separated by intervening segments, called introns. Following transcription, genes are expressed as precursor mRNAs (pre-mRNAs) which are spliced co-transcriptionally and the flanking exons are joined together to form a continuous mRNA. One advantage of this architecture is that it allows alternative splicing by differential use of exons to generate multiple mRNAs from individual genes. Regulatory elements located within introns and exons guide the splicing complex, the spliceosome, and auxiliary RNA binding proteins to the correct sites for intron removal and exon joining. Misregulation of splicing and alternative splicing can result from mutations in cis regulatory elements within the affected gene or from mutations that affect the activities of trans-acting factors that are components of the splicing machinery. Mutations that affect splicing can cause disease directly or contribute to the susceptibility or severity of disease. An understanding of the role of splicing in disease expands potential opportunities for therapeutic intervention by either directly addressing the cause or by providing novel approaches to circumvent disease processes.

Background

The mitochondrial genome in the human malaria parasite Plasmodium falciparum is most unusual. Over half the genome is composed of the genes for three classic mitochondrial proteins: cytochrome oxidase subunits I and III and apocytochrome b. The remainder encodes numerous small RNAs, ranging in size from 23 to 190 nt. Previous analysis revealed that some of these transcripts have significant sequence identity with highly conserved regions of large and small subunit rRNAs, and can form the expected secondary structures. However, these rRNA fragments are not encoded in linear order; instead, they are intermixed with one another and the protein coding genes, and are coded on both strands of the genome. This unorthodox arrangement hindered the identification of transcripts corresponding to other regions of rRNA that are highly conserved and/or are known to participate directly in protein synthesis.

Principal Findings

The identification of 14 additional small mitochondrial transcripts from P. falcipaurm and the assignment of 27 small RNAs (12 SSU RNAs totaling 804 nt, 15 LSU RNAs totaling 1233 nt) to specific regions of rRNA are supported by multiple lines of evidence. The regions now represented are highly similar to those of the small but contiguous mitochondrial rRNAs of Caenorhabditis elegans. The P. falciparum rRNA fragments cluster on the interfaces of the two ribosomal subunits in the three-dimensional structure of the ribosome.

Significance

All of the rRNA fragments are now presumed to have been identified with experimental methods, and nearly all of these have been mapped onto the SSU and LSU rRNAs. Conversely, all regions of the rRNAs that are known to be directly associated with protein synthesis have been identified in the P. falciparum mitochondrial genome and RNA transcripts. The fragmentation of the rRNA in the P. falciparum mitochondrion is the most extreme example of any rRNA fragmentation discovered.

The protozoan oyster parasite Perkinsus marinus can be cultured in vitro in a variety of media; however, this has been associated with a rapid attenuation of infectivity. Supplementation of defined media with products of P. marinus-susceptible (Crassostrea virginica) and -tolerant (Crassostrea gigas, Crassostrea ariakensis) oysters alters proliferation and protease expression profiles and induces differentiation into morphological forms typically seen in vivo. It was not known if attenuation could be reversed by host extract supplementation. To investigate correlations among these changes as well as their association with infectivity, the effects of medium supplementation with tissue homogenates from both susceptible and tolerant oyster species were examined. The supplements markedly altered both cell size and proliferation, regardless of species; however, upregulation of low-molecular-weight protease expression was most prominent with susceptible oysters extracts. Increased infectivity occurred with the use of oyster product-supplemented media, but it was not consistently associated with changes in cell size, cell morphology, or protease secretion and was not related to the susceptibility of the oyster species used as the supplement source.

Protist mitochondrial genomes show a very wide range of gene content, ranging from three genes for respiratory chain components in Apicomplexa and dinoflagellates to nearly 100 genes in Reclinomonas americana. In many organisms the rRNA genes are fragmented, although still functional. Some protist mitochondria encode a full set of tRNAs, while others rely on imported molecules. There is similarly a wide variation in mitochondrial genome organization, even among closely related groups. Mitochondrial gene expression and control are generally poorly characterized. Transcription probably relies on a ‘viral-type’ RNA polymerase, although a ‘bacterial-type’ enzyme may be involved in some cases. Transcripts are heavily edited in many lineages. The chloroplast genome generally shows less variation in gene content and organization, although greatly reduced genomes are found in dinoflagellate algae and non-photosynthetic organisms. Genes in the former are located on small plasmids in contrast to the larger molecules found elsewhere. Control of gene expression in chloroplasts involves transcriptional and post-transcriptional regulation. Redox poise and the ATP/ADP ratio are likely to be important determinants. Some protists have an additional extranuclear genome, the nucleomorph, which is a remnant nucleus. Nucleomorphs of two separate lineages have a number of features in common.