Complete Sequence of the Mitochondrial DNA of the Red Alga Porphyra purpurea: Cyanobacterial Introns and Shared Ancestry of Red and Green Algae

In recent years a great deal of biochemical and genetic research has focused on the C-terminal domain (CTD) of the largest subunit (RPB1) of DNA-dependent RNA polymerase II. This strongly conserved domain of tandemly repeated heptapeptides has been linked functionally to important steps in the initiation and processing of mRNA transcripts in both animals and fungi. Although they are absolutely required for viability in these organisms, C-terminal tandem repeats do not occur in RPB1 sequences from diverse eukaryotic taxa. Here we present phylogenetic analyses of RPB1 sequences showing that canonical CTD heptads are strongly conserved in only a subset of eukaryotic groups, all apparently descended from a single common ancestor. Moreover, eukaryotic groups in which the most complex patterns of ontogenetic development occur are descended from this CTD-containing ancestor. Consistent with the results of genetic and biochemical investigations of CTD function, these analyses suggest that the enhanced control over RNA polymerase II transcription conveyed by acquired CTD͞protein interactions was an important step in the evolution of intricate patterns of gene expression that are a hallmark of large, developmentally complex eukaryotic organisms. development ͉ RPB1 ͉ transcription E ach of the core subunits present in all cellular DNAdependent RNA polymerase (pol) enzymes shares a common evolutionary origin (1, 2). The largest of these subunits contains eight highly conserved domains, designated regions A through H (2), which are common to all prokaryotic and eukaryotic homologues (3). Unlike all other members of this protein family, however, the largest subunit of eukaryotic RNA pol II has an additional C-terminal domain (CTD), comprising a varied number of tandemly repeated heptapeptides with the consensus sequence Tyr-1-Ser-2-Pro-3-Thr-4 -Ser-5-Pro-6 -Ser-7 (4). In animals and yeast, where the mechanics of transcription are understood most clearly, the CTD has become a focal point of investigations into the interactions between RNA pol II and a variety of transcription-related proteins.Reversible phosphorylation of the CTD regulates the cycling of RNA pol II between a hypophosphorylated (IIO) form, which is competent to enter the preinitiation complex, and a hyperphosphorylated (IIA) form capable of processive transcript elongation (5). Throughout this cycle the CTD binds essential transcription-related proteins that help to regulate gene expression (6-9), promote efficient elongation (10), and effectively couple transcription to pre-mRNA processing (11-15). So central is its role in these interactions that the CTD has been called, by one reviewer, ''the tail that wags the dog'' of RNA pol II (16).Tandemly repeated CTD heptads occur in all RNA pol II largest subunits isolated to date from animals, fungi, and green plants. Given the importance of the CTD for pol II function, it is not surprising that it has been conserved so strongly during the evolution of these groups. A typical CTD also is present in certain protists;...

Section: Resultsmentioning

confidence: 93%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

See 1 more Smart Citation

Evolution of the RNA polymerase II C-terminal domain

Stiller

Hall

2002

“…This finding is not unexpected because the size of the commonly used genes is Ϸ300 positions, which provide little information to resolve such ancient events as the diversification of eukaryotes. It is thus not surprising that much recent progress has been based on the analysis of combined protein data sets (24,34,39).…”

mentioning

confidence: 99%

The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium , Entamoeba , and Mastigamoeba

Bapteste

Brinkmann

Lee

et al. 2002

348

222

The phylogenetic relationships of amoebae are poorly resolved. To address this difficult question, we have sequenced 1,280 expressed sequence tags from Mastigamoeba balamuthi and assembled a large data set containing 123 genes for representatives of three phenotypically highly divergent major amoeboid lineages: Pelobionta, Entamoebidae, and Mycetozoa. Phylogenetic reconstruction was performed on Ϸ25,000 aa positions for 30 species by using maximum-likelihood approaches. All well-established eukaryotic groups were recovered with high statistical support, validating our approach. Interestingly, the three amoeboid lineages strongly clustered together in agreement with the Conosa hypothesis [as defined by T. Cavalier-Smith (1998) Biol. Rev. Cambridge Philos. Soc. 73, 203-266]. Two amitochondriate amoebae, the free-living Mastigamoeba and the human parasite Entamoeba, formed a significant sister group to the exclusion of the mycetozoan Dictyostelium. This result suggested that a part of the reductive process in the evolution of Entamoeba (e.g., loss of typical mitochondria) occurred in its free-living ancestors. Applying this inexpensive expressed sequence tag approach to many other lineages will surely improve our understanding of eukaryotic evolution.

“…Because of the existence of an ␣-proteobacterial-type mitochondrial FtsZ (MtFtsZ) gene in red algae, which share a common ancestry with green algae and green plants (13,14), it is possible that higher plants have mitochondrial FtsZ genes in their genomes. But no ␣-proteobacterial-type FtsZ has been identified in the nuclear or mitochondrial genome of Arabidopsis thaliana (15,16).…”

mentioning

confidence: 99%

A dynamin-like protein (ADL2b), rather than FtsZ, is involved in Arabidopsis mitochondrial division

Arimura

Tsutsumi

2002

183

139

Recently, the FtsZ protein, which is known as a key component in bacterial cell division, was reported to be involved in mitochondrial division in algae. In yeast and animals, however, mitochondrial fission depends on the dynamin-like proteins Dnm1p and Drp1, respectively, whereas in green plants, no potential mitochondrial division genes have been identified. BLAST searches of the nuclear and mitochondrial genome sequences of Arabidopsis thaliana did not find any obvious homologue of the ␣-proteobacterial-type ftsZ genes. To determine whether mitochondrial division of higher plants depends on a dynamin-like protein, we cloned a cDNA for ADL2b, an Arabidopsis homologue of Dnm1p, and tested its subcellular localization and its dominant-negative effect on mitochondrial division. The fusion protein of green fluorescent protein and ADL2b was observed as punctate structures localized at the tips and at the constriction sites of mitochondria in live plant cells. Cells expressing dominant-negative mutant ADL2b proteins (K56A and T77F) showed a significant fusion, aggregation, and͞or tubulation of mitochondria. We propose that mitochondrial division in higher plants is conducted by dynamin-like proteins similar to ADL2b in Arabidopsis. The evolutional points of loss of mitochondrial FtsZ and the functional acquisition of dynamin-like proteins in mitochondrial division are discussed.