The fungal mitochondrial genome project: evolution of fungal mitochondrial genomes and their gene expression

Abstract

The goal of the fungal mitochondrial genome project (FMGP) is to sequence complete mitochondrial genomes for a representative sample of the major fungal lineages; to analyze the genome structure, gene content, and conserved sequence elements of these sequences; and to study the evolution of gene expression in fungal mitochondria. By using our new sequence data for evolutionary studies, we were able to construct phylogenetic trees that provide further solid evidence that animals and fungi share a common ancestor to the exclusion of chlorophytes and protists. With a database comprising multiple mitochondrial gene sequences, the level of support for our mitochondrial phylogenies is unprecedented, in comparison to trees inferred with nuclear ribosomal RNA sequences. We also found several new molecular features in the mitochondrial genomes of lower fungi, including: (1) tRNA editing, which is the same type as that found in the mitochondria of the amoeboid protozoan Acanthamoeba castellanii; (2) two novel types of putative mobile DNA elements, one encoding a site-specific endonuclease that confers mobility on the element, and the other constituting a class of highly compact, structured elements; and (3) a large number of introns, which provide insights into intron origins and evolution. Here, we present an overview of these results, and discuss examples of the diversity of structures found in the fungal mitochondrial genome.

Highly organized structure in the non-coding region of the psbA minicircle from clade C Symbiodinium

“…DNA sequence motifs similar to the twin IRs reported here have been found in the mitochondrial genomes of a range of taxonomically diverse fungal species (Paquin & Lang, 1996;Paquin et al, 1997Paquin et al, , 2000. These motifs, termed double-hairpin elements (DHEs), range in size from 26-79 bases and assume a secondary structure consisting of a 3-5 base loop in each of two adjacent, helical stems, with extensive G-C pairing in at least one stem.…”

Punctuated evolution of mitochondrial gene content: High and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution

“…5). The protein gene content of fungal mtDNAs is nearly as reduced (with two additional genes) and as invariant as in animals (1,2,6). Only one case of fungal gene transfer is known (7), and gene loss is largely restricted to the loss in certain yeasts of all NADH dehydrogenase genes (1, 6) through loss of the protein complex, rather than gene transfer.…”

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

“…In contrast to nuclear trees, several recent phylogenetic analyses of mitochondrial data point to a sister-group relationship between red and green algae; however, these analyses also lack either rigorous statistical or bootstrap support (e.g., Bhattacharya and Schmidt, 1997) or include only a limited number of eukaryotic taxa (e.g., Boyen et al, 1994) or of rhodophyte taxa in particular (e.g., Paquin et al, 1997;Lang et al, 1998). To our knowledge, the mitochondrial phylogeny presented here (Figure 6) is the only analysis to date combining high bootstrap support with broad sampling of mitochondriate eukaryotes, showing robust coherence of members of the red algae, green algae/plants, animals, and fungi, and providing strong evidence for the divergence of red and green algae from a shared ancestor.…”

“…An opposite interpretation contends that the red algae represent a derived group that has secondarily lost many of the distinctive features of the protistan cytoskeleton (Pueschel, 1990;Scott and Broadwater, 1990). Finally, it has been proposed that red algae may have given rise to the fungi (Demoulin, 1985) or that red algae are affiliated with the plant kingdom via common ancestry with green algae (see, e.g., Bhattacharya et al, 1993; Cavalier-Smith, 1993;McFadden et al, 1994;Schlegel, 1994;Paquin et al, 1997;Lang et al, 1998). This broad spectrum of coexisting, mutually exclusive hypotheses highlights our limited knowledge about the phylogenetic relationship between rhodophytes and other eukaryotic phyla.…”

“…Species (with GenBank accession numbers in parentheses) are as follows : Homo, H. sapiens (J01415;Anderson et al, 1981);Mus, M. musculus (J01420;Bibb et al, 1981); Xenopus, X. laevis (M10217; Roe et al, 1985);Strongylocentrotus, S. purpuratus (X12631;Jacobs et al, 1988);Drosophila, D. yakuba (fruitfly;X03240;Clary and Wolstenholme, 1985);Metridium, M. senile (AF000023;Beagley et al, 1998); Rhizopus, R. stolonifer (chytridiomycete fungus; Laforest et al, 1997;Saccharomyces, S. cerevisiae (ascomycete fungus;X84842, V00694, V00695, J01478;de Zamaroczy and Bernardi, 1986); Pichia, P. canadensis (Hansenula wingei) (ascomycete fungus; D31785; Sekito et al, 1995); Aspergillus, A. (Emericella) nidulans (ascomycete fungus; J01387, X15441, X06960; Netzker et al, 1982;Brown, 1993); Neurospora, N. crassa (ascomycete fungus; K01181, A28755 [protein], X01850, K00825, V00668;Collins, 1993);Podospora, P. anserina (ascomycete fungus;X55026;Cummings et al, 1990); Allomyces, A. macrogynus (chytridiomycete fungus; U41288; Paquin and Lang, 1996;Paquin et al, 1997);Acanthamoeba, A. castellanii (rhizopod;U12386;Burger et al, 1995);Malawimonas, M. jakobiformis (jakobids;G. Burger, B.F. Lang, C. O'Kelly, and M.W.…”