The GC clusters of the mitochondrial genome of yeast and their evolutionary origin

doi:10.1016/0378-1119(86)90262-3

Gene

Volume 41, Issue 1, 1986, Pages 1-22

https://doi.org/10.1016/0378-1119(86)90262-3 Get rights and content

Abstract

We have studied the primary and secondary structures, the location and the orientation of the 196 GC clusters present in the 90% of the mitochondrial genome of Saccharomyces cerevisiae which have already been sequenced. The vast majority of GC clusters is located in intergenic sequences (including ori sequences, intergenic open reading frames and the gene varl which probably arose from an intergenic spacer) and in intronic closed reading frames (CRF's); most of them can be folded into stem-and-loop systems; both orientations are equally frequent.

The primary structures of GC clusters permit to group them into eight families, seven of which are related to the family formed by clusters A, B and C of the ori sequences. On the basis of the present work, we propose that the latter derive from a primitive ori sequence (probably made of only a monomeric cluster C and its flanking sequences $r^{∗}$ and r) through (i) a series of duplication inversions generating clusters A and B; and (ii) an expansion process producing the AT stretches of ori sequences. Most GC clusters apparently originated from primary clusters also derived from the primitive ori sequence in the course of its evolution towards the present ori sequences. Finally, we propose that the function of GC clusters is predominantly, or entirely, associated with the structure and organization of the mitochondrial genome of yeast and, indirectly, with the regulation of its expression.

References (56)

G. Bernardi
Dimeric structure and allosteric properties of spleen acid deoxyribonuclease
J. Mol. Biol.
(1965)
G. Bernardi et al.
Separation and characterization of a satellite DNA from a yeast cytoplasmic “petite” mutant
J. Mol. Biol.
(1968)
G. Bernardi et al.
Mitochondrial DNA's from respiratory-sufficient and cytoplasmic respiratory-deficient mutant yeast
J. Mol. Biol.
(1970)
G. Bernardi et al.
Optical rotatory dispersion and circular dichroism. Properties of yeast mitochondrial DNA's
J. Mol. Biol.
(1970)
G. Bernardi et al.
The mitochondrial genome of wild-type yeast cells. I. Preparation and heterogeneity of mitochondrial DNA
J. Mol. Biol.
(1972)
G. Bernardi et al.
Repeated sequences in the mitochondrial genome of yeast
FEBS Lett.
(1980)
R.A. Butow
Nonreciprocal exchanges in the yeast mitochondrial genome — A review
Trends Genet.
(1985)
T. Christianson et al.
Identification of multiple transcriptional initiation sites on the yeast mitochondrial genome by in vitro capping with guanylyltransferase
J. Biol. Chem.
(1983)
Y. Colin et al.
A new putative gene in the mitochondrial genome of Saccharomyces cerevisiae
Gene
(1985)
J. Cosson et al.
Sequence homologies of (guanosine + cytidine)-rich regions of mitochondrial DNA of Saccharomyces cerevisiae
J. Biol. Chem.
(1979)

M. de Zamaroczy et al.

Excision sequences in the mitochondrial genome of yeast

Gene

(1983)

M. de Zamaroczy et al.

The ori sequences of the mitochondrial genome of a wild-type yeast strain: number, location, orientation and structure

Gene

(1984)

M. de Zamaroczy et al.

Sequence organization of the mitochondrial genome of yeast — a review

Gene

(1985)

B. Dujon

Sequence of the intron and flanking exons of the mitochondrial 21S rRNA gene of yeast strains having different alleles at the ω and ribl loci

Cell

(1980)

S.D. Ehrlich et al.

The mitochondrial genome of wild-type yeast cells, III. The pyrimidine tracts of mitochondrial DNA

J. Mol. Biol.

(1972)

G. Faugeron-Fonty et al.

A comparative study of the ori sequences from the mitochondrial genomes of twenty wildtype yeast strains

Gene

(1984)

G. Faugeron-Fonty et al.

The mitochondrial genomes of spontaneous ori^r petite mutants of yeast have rearranged repeat units organized as inverted tandem dimers

Gene

(1983)

G. Fonty et al.

The mitochondrial genome of wild-type yeast cells, VII. Recombination in crosses

J. Mol. Biol.

(1978)

M.E.S. Hudspeth et al.

Location and structure of the varl gene on yeast mitochondrial DNA: nucleotide sequence of the 40.0 allele

Cell

(1982)

M. Mangin et al.

The ori^r to ori⁺ mutation in spontaneous yeast petites is accompanied by a drastic change in mitochondrial genome replication

Gene

(1983)

F.G. Nobrega et al.

Assembly of the mitochondrial membrane system. DNA sequence and organization of the cytochrome b gene in Saccharomyces cerevisiae D273-10B

J. Biol. Chem.

(1980)

G. Piperno et al.

The mitochondrial genome of wild-type yeast cells, II. Investigations on the compositional heterogeneity of mitochondrial DNA

J. Mol. Biol.

(1972)

A. Prunell et al.

The mitochondrial genome of wild-type yeast cells, IV. Genes and spacers

J. Mol. Biol.

(1974)

A. Tzagoloff et al.

Organization of mitochondrial DNA in yeast

R.B. Waring et al.

Assessment of a model for intron RNA secondary structure relevant to RNA selfsplicing—a review

Gene

(1984)

S. Yin et al.

Highly conserved GC-rich palindromic DNA sequences flank tRNA genes in Neurospora crassa mitochondria

Cell

(1981)

S. Anderson et al.

Sequence and organization of the human mitochondrial genome

Nature

(1981)

G. Baldacci et al.

The initiation of DNA replication in the mitochondrial genome of yeast

EMBO J.

(1984)

Cited by (73)

Small inverted repeats drive mitochondrial genome evolution in Lake Baikal sponges
2012, Gene
Citation Excerpt :
The research on Lake Baikal sponges also benefits from the presence of a fossil record of the group that can be used to investigate the absolute as well as relative rates of evolution. Several previous studies suggested possible functions for organellar hairpins and palindromes, including mRNA processing, translation, and stabilization (Andre et al., 1992; Yin et al., 1981) as well as DNA recombination (de Zamaroczy and Bernardi, 1986; Dieckmann and Gandy, 1987). In bilaterian animals hairpin structures in the non-coding “control” region(s) have long been associated with the origin and termination of replication and transcription (Clayton, 1982; Lavrov et al., 2002).
Demosponges, the largest and most diverse class in the phylum Porifera, possess mitochondrial DNA (mtDNA) markedly different from that in other animals. Although several studies investigated evolution of demosponge mtDNA among major lineages of the group, the changes within these groups remain largely unexplored. Recently we determined mitochondrial genomic sequence of the Lake Baikal sponge Lubomirskia baicalensis and described proliferation of small inverted repeats (hairpins) that occurred in it since the divergence between L. baicalensis and the most closely related cosmopolitan freshwater sponge Ephydatia muelleri. Here we report mitochondrial genomes of three additional species of Lake Baikal sponges: Swartschewskia papyracea, Rezinkovia echinata and Baikalospongia intermedia morpha profundalis (Demospongiae, Haplosclerida, Lubomirskiidae) and from a more distantly related freshwater sponge Corvomeyenia sp. (Demospongiae, Haplosclerida, Metaniidae). We use these additional sequences to explore mtDNA evolution in Baikalian sponges, paying particular attention to the variation in the rates of nucleotide substitutions and the distribution of hairpins, abundant in these genomes. We show that most of the changes in Lubomirskiidae mitochondrial genomes are due to insertion/deletion/duplication of these elements rather than single nucleotide substitutions. Thus inverted repeats can act as an important force in evolution of mitochondrial genome architecture and be a valuable marker for population- and species-level studies in this group. In addition, we infer (((Rezinkovia + Lubomirskia) + Swartschewskia) + Baikalospongia) phylogeny for the family Lubomirskiidae based on the analysis of mitochondrial coding sequences from freshwater sponges.
Global identification of yeast chromosome interactions using Genome conformation capture
2009, Fungal Genetics and Biology
The association of chromosomes with each other and other nuclear components plays a critical role in nuclear organization and Genome function. Here, using a novel and generally applicable methodology (Genome conformation capture [GCC]), we reveal the network of chromosome interactions for the yeast Saccharomyces cerevisiae. Inter- and intra-chromosomal interactions are non-random and the number of interactions per open reading frame depends upon the dispensability of the gene product. Chromosomal interfaces are organized and provide evidence of folding within chromosomes. Interestingly, the genomic connections also involve the 2 μm plasmid and the mitochondrial genome. Mitochondrial interaction partners include genes of α-proteobacterial origin and the ribosomal DNA. Organization of the 2 μm plasmid aligns two inverted repeats (IR1 and IR2) and displays the stability locus on a prominent loop thus making it available for plasmid clustering. Our results form the first global map of chromosomal interactions in a eukaryotic nucleus and demonstrate the highly connected nature of the yeast genome. These results have significant implications for understanding eukaryotic genome organization.
Lessons from a small, dispensable genome: The mitochondrial genome of yeast
2005, Gene
This article reviews the investigations on the mitochondrial genomes of yeast carried out in the author's laboratory during a quarter of a century (to be precise between 1966 and 1992). Our studies dealt with the structural basis for the cytoplasmic petite mutation, the replication, the transcription and the recombination of the mitochondrial genome, a genome which is dispensable and which comprises abundant non-coding sequences. This work led to some general conclusions on the nuclear genome of eukaryotes. Some recent results in apparent contradiction with our conclusions on ori sequences will also be briefly discussed.
Complete nucleotide sequence of the mitochondrial DNA from Kluyveromyces lactis
2005, FEMS Yeast Research
The total nucleotide sequence of the mitochondrial genome of the yeast Kluyveromyces lactis was determined. The DNA is a circular molecule of 40,291 base pairs, with 26.1% GC. It contains a set of protein- and RNA-coding genes equivalent to those of the Saccharomyces cerevisiae mitochondrial genome. The genome size is about one half of that of S. cerevisiae mitochondrial DNA. The difference in size is due essentially to a reduced proportion of intergenic and intronic sequences. The coding sequences occupy about one third of the genome, the rest being composed of AT-rich sequences and numerous short GC-rich clusters that are dispersed mostly in the non-coding regions and a few within coding sequences. The presence of these GC clusters is a characteristic feature common to K. lactis and S. cerevisiae mitochondrial DNA, although their sequence patterns are different. The absence of the NADH dehydrogenase subunit genes distinguishes this yeast and S. cerevisiae from the typically aerobic species. The genetic code appears to be that of the standard fungal mitochondrial genomes, with UGA as a tryptophan codon. There are only 22 transfer RNA genes, those corresponding to CUN and CGN codons being missing. CUN codons are absent in the protein-coding sequences. There are five CGN codons within the open reading frames, but they are located exclusively in the introns, rendering them untranslatable. Introns are found only the genes in KlCOX1 and LrRNA. The transcription promoter motif known in S. cerevisiae and several other yeast species is also present. All genes are transcribed from the same strand, except those on a single 7-kilobase pairs segment (EMBL Accession No. AY654900).
The analysis of the complete mitochondrial genome of Lecanicillium muscarium (synonym Verticillium lecanii) suggests a minimum common gene organization in mtDNAs of Sordariomycetes: Phylogenetic implications
2004, Fungal Genetics and Biology
The mitochondrial genome (mtDNA) of the entomopathogenic fungus Lecanicillium muscarium (synonym Verticillium lecanii) with a total size of 24,499-bp has been analyzed. So far, it is the smallest known mitochondrial genome among Pezizomycotina, with an extremely compact gene organization and only one group-I intron in its large ribosomal RNA (rnl) gene. It contains the 14 typical genes coding for proteins related to oxidative phosphorylation, the two rRNA genes, one intronic ORF coding for a possible ribosomal protein (rps), and a set of 25 tRNA genes which recognize codons for all amino acids, except alanine and cysteine. All genes are transcribed from the same DNA strand. Gene order comparison with all available complete fungal mtDNAs—representatives of all four Phyla are included—revealed some characteristic common features like uninterrupted gene pairs, overlapping genes, and extremely variable intergenic regions, that can all be exploited for the study of fungal mitochondrial genomes. Moreover, a minimum common mtDNA gene order could be detected, in two units, for all known Sordariomycetes namely nad1–nad4–atp8–atp6 and rns-cox3–rnl, which can be extended in Hypocreales, to nad4L–nad5–cob-cox1–nad1–nad4–atp8–atp6 and rns-cox3–rnl nad2–nad3, respectively. Phylogenetic analysis of all fungal mtDNA essential protein-coding genes as one unit, clearly demonstrated the superiority of small genome (mtDNA) over single gene comparisons.
Inheritance and organisation of the mitochondrial genome differ between two Saccharomyces yeasts
2002, Journal of Molecular Biology
Petite-positive Saccharomyces yeasts can be roughly divided into the sensu stricto, including Saccharomyces cerevisiae, and sensu lato group, including Saccharomyces castellii; the latter was recently studied for transmission and the organisation of its mitochondrial genome. S. castellii mitochondrial molecules (mtDNA) carrying point mutations, which confer antibiotic resistance, behaved in genetic crosses as the corresponding point mutants of S. cerevisiae. While S. castellii generated spontaneous petite mutants in a similar way as S. cerevisiae, the petites exhibited a different inheritance pattern. In crosses with the wild type strains a majority of S. castellii petites was neutral, and the suppressivity in suppressive petites was never over 50%. The two yeasts also differ in organisation of their mtDNA molecules. The 25,753 bp sequence of S. castellii mtDNA was determined and the coding potential of both yeasts is similar. However, the S. castellii intergenic sequences are much shorter and do not contain sequences homologous to the S. cerevisiae biologically active intergenic sequences, as ori/rep/tra, which are responsible for the hyper-suppressive petite phenotype found in S. cerevisiae. The structure of one suppressive S. castellii mutant, CA38, was also determined. Apparently, a short direct intergenic repeat was involved in the generation of this petite mtDNA molecule.

View all citing articles on Scopus

View full text

The GC clusters of the mitochondrial genome of yeast and their evolutionary origin

Abstract

J. Mol. Biol.

J. Mol. Biol.

J. Mol. Biol.

J. Mol. Biol.

J. Mol. Biol.

FEBS Lett.

Trends Genet.

J. Biol. Chem.

Gene

J. Biol. Chem.

Gene

Gene

Gene

Cell

J. Mol. Biol.

Gene

Gene

J. Mol. Biol.

Cell

Gene

J. Biol. Chem.

J. Mol. Biol.

J. Mol. Biol.

Gene

Cell

Sequence and organization of the human mitochondrial genome

Nature

The initiation of DNA replication in the mitochondrial genome of yeast

EMBO J.