Dinoflagellate 17S rRNA sequence inferred from the gene sequence: Evolutionary implications

Abstract

We present the complete sequence of the nuclear-encoded small-ribosomal-subunit RNA inferred from the cloned gene sequence of the dinoflagellate Prorocentrum micans. The dinoflagellate 17S rRNA sequence of 1798 nucleotides is contained in a family of 200 tandemly repeated genes per haploid genome. A tentative model of the secondary structure of P. micans 17S rRNA is presented. This sequence is compared with the small-ribosomal-subunit rRNA of Xenopus laevis (Animalia), Saccharomyces cerevisiae (Fungi), Zea mays (Planta), Dictyostelium discoideum (Protoctista), and Halobacterium volcanii (Monera). Although the secondary structure of the dinoflagellate 17S rRNA presents most of the eukaryotic characteristics, it contains sufficient archaeobacterial-like structural features to reinforce the view that dinoflagellates branch off very early from the eukaryotic lineage.In the five-kingdom system for classification of organisms (1) (3) and possessing a number of peculiar traits of nuclear organization (4) suggestive ofthe prokaryotic state. Among this unusual primitive pattern of nuclear organization, the most striking feature is the now well-documented absence of histones and nucleosomal structures. Dinoflagellate chromatin fibrils, which appear as smooth filaments in electron microscopy, are associated with a low amount of one or two major basic proteins whose amino acid composition is different from known prokaryotic basic proteins or eukaryotic histones (5-7). Nuclease digestion of purified nuclei lends to a smear with no recognizable discrete DNA fragments (8, 9). Permanently condensed chromosomes are stabilized by divalent cations and RNA (10, 11). In eukaryotes histones and especially the histone H1, which is thought to be primarily responsible for organizing higherorder structure of nucleosomes, are involved in gene repression (12). Thus, the problem of gene regulation in such organisms is still unsolved, with a prokaryotic-like chromatin organization and some of the following eukaryotic nuclear traits: (i) The portion of repeated sequences (around 60%) is typical for eukaryotes (13). (ii) The rRNA is synthesized as a precursor of 38S, and a 5.8S rRNA has been reported to be released from the 27S precursor to give rise to the final 24S RNA (14). (iii) The 5S rRNA sequence shows greater homology with that of higher eukaryotes than that of eubacteria (15), but additional molecular data (16) indicate that it contains some conserved residues specific for lower eukaryotes (unpublished data) and that the general structure of the 5S rRNA from sulfolobale and thermoplasmale archaeobacteria is also closer to that of eukaryotes than that of eubacteria (17). (iv) Poly(ADP-ribose) polymerase activity is detectable (18). (v) The small nuclear RNAs U1-U5 have been isolated (19). The U5 dinoflagellate sequence shows strong homology (63%) with that of vertebrates (20), but appears to be more homologous to that of Tetrahymena (70%) (ref. 21, and unpublished data). Thus these molecular data, in addition to the interpretat...

Classification and Phylogenetic Analysis of the cAMP-Dependent Protein Kinase Regulatory Subunit Family

“…Most phylogenetic analysis based on rRNA (McCarrol et al 1983;Hasegawa et al 1985;Herzog and Maroteaux 1986;Hendricks et al 1991;Douglas et al 1991) and some based on protein sequence analysis (Kuma et al 1995;Baldauf and Doolittle 1997;Baldauf et al 2000) place Dictyostelium as outgroup to Fungi and Animals. Conversely, other models based on protein sequence analysis suggest that Fungi diverged from the line leading to Animals before the divergence of Dictyostelium and Animals Smith 1990, 1995;Roger et al 1996;Kalhor et al 1999;Norian et al 1999;Swigart et al 2000).…”

A phylogenetic analysis of the 18S ribosomal RNA sequence of the coelacanth Latimeria chalumnae

“…One molecule with a highly conserved primary structure that previously has not been examined in the coelacanth or an extensive sample of other gnathostome taxa is the 18s ribosoma1 RNA (rRNA). The conservative nature of this molecule is demonstrated by its use in phylogenetic studies of the relationship of eukaryotes to the main prokaryotic lineages (Woese 1987, Olsen 1987, Cedergren et al 1988, Lake 1988, the interrelationships of lower eukaryotes (McCarroll et al 1983, Elwood et al 1985, Herzog & Maroteaux 1986, Gunderson et al 1987, Vossbrinck et al 1987, Clark & Cross 1988, the interrelationships of the higher eukaryotic kingdoms (Hasegawa et al 1985, Gouy & Li 1989, the interrelationships of higher level taxa of plants (Nairn & Ferl 1988, Zimmer et al 1989, the interrelationships of animal phyla (Field et al 1988), the interrelationships of higher level taxa of echinoderms (Raff et al 1987) and the interrelationships of insect orders (Wheeler 1989). Despite this extreme conservation of certain regions of the 18s rRNA, some regions exhibit sequence variation within the Vertebrata, as pointed out by Raynal et al (1984) and McCallum & Maden (1985), and as illustrated by the present study.…”

The Biosynthesis of Polyketide Metabolites by Dinoflagellates

“…Relatively large amount of DNA Spector, 1984 Unusual sterols Withers, 1983 Hypermethylated DNA Ten Lohuis and Miller, 1998 Hydroxymethyluracil substituted for thymine Rae, 1976 Most are uninucleates, but some binucleates exist Rizzo, 2003 Permanently condensed chromosomes Rizzo, 2003 Lack histones and nucleosomes Moreno Diaz et al, 2005 Possess a vegetative haploid nuclear phase Santos and Coffroth, 2003 Typical eukaryotic nuclear envelope, but it remains intact during mitosis Bhaud et al, 2000 Typical eukaryotic 9 + 2 axoneme flagella Maruyama, 1985 Membrane-bound organelles (endoplasmic reticula, Golgi apparatus, mitochondria, and chloroplasts) Spector, 1984 Percentages of repetitive DNA (50-60%) consistent with higher eukaryotic genomes Moreno Diaz et al, 2005 Typical eukaryotic cell cycle Moreno Diaz et al, 2005 Heavy (28S) and light (17S) rRNA that is structurally similar to higher eukaryotes Herzog and Maroteaux, 1986 Lack the TATA-box (typical eukaryotic promoter) Guillebault et al, 2002 …”