Group I Intron–Mediated Trans-splicing in Mitochondria of Gigaspora rosea and a Robust Phylogenetic Affiliation of Arbuscular Mycorrhizal Fungi with Mortierellales

Abstract

Gigaspora rosea is a member of the arbuscular mycorrhizal fungi (AMF; Glomeromycota) and a distant relative of Glomus species that are beneficial to plant growth. To allow for a better understanding of Glomeromycota, we have sequenced the mitochondrial DNA of G. rosea. A comparison with Glomus mitochondrial genomes reveals that Glomeromycota undergo insertion and loss of mitochondrial plasmid-related sequences and exhibit considerable variation in introns. The gene order between the two species is almost completely reshuffled. Furthermore, Gigaspora has fragmented cox1 and rns genes, and an unorthodox initiator tRNA that is tailored to decoding frequent UUG initiation codons. For the fragmented cox1 gene, we provide evidence that its RNA is joined via group I-mediated trans-splicing, whereas rns RNA remains in pieces. According to our model, the two cox1 precursor RNA pieces are brought together by flanking cox1 exon sequences that form a group I intron structure, potentially in conjunction with the nad5 intron 3 sequence. Finally, we present analyses that address the controversial phylogenetic association of Glomeromycota within fungi. According to our results, Glomeromycota are not a separate group of paraphyletic zygomycetes but branch together with Mortierellales, potentially also Harpellales.

Mitochondrial Genome Rearrangements in Glomus Species Triggered by Homologous Recombination between Distinct mtDNA Haplotypes

“…1). The G. irregulare isolate DAOM-234179 mtDNA has a genome size of 75,075 bp with a GC content of 36.7%, which is within range of the sizes of other sequences reported for this species (68,995–87,754 bp with a ≈37% average GC content) (Lee and Young 2009; Formey et al 2012; Nadimi et al 2012). The only true outlying G. irregulare isolate with respect to its mitochondrial genome was reported by Formey et al (2012) (i.e., MUCL43204) and has a size of 87,754 bp, whereas its conserved mitochondrial genes show only 65.8% identity (including introns and ORFs) with G. irregulare isolate 494.…”

“…The Gi g . rosea putative mitochondrial plasmid that was previously described (Nadimi et al 2012) was also one of the singletons. The two G. cerebriforme dpo copies (light green circles) were the sole representatives of similarity group 12.…”

Mosaic genome of endobacteria in arbuscular mycorrhizal fungi: Transkingdom gene transfer in an ancient mycoplasma-fungus association

“…DhMRE belongs to a bacterial lineage closely related to the pneumoniae and hominis mycoplasma groups, which mainly occur as biotrophic extracellular parasites of animals (23). The DhMRE gene homologs we detected in the nuclear genome of M. verticillata (Mortierellales), together with the recent findings of MRE in Endogone (Endogonales) species (24), indicate that the MRE association with fungi was already present in a common ancestor of the Glomeromycota and Mucoromycotina (25).…”

Genome diversity in arbuscular mycorrhizal fungi

“…Mitochondrial sequences have been determined for two Gigaspora isolates belonging to different species [4,5]. They are both large (>90 kb) and, unlike R. irregularis, have genes encoded on both strands, as well as unusual trans-spliced introns.…”

“…All known arbuscular mycorrhizal (AM) fungi are in the phylum Glomeromycota, and all known Glomeromycota are AM fungi, with the exception of Geosiphon, which forms a symbiosis with cyanobacteria [2]. The Glomeromycota are probably the sister group of the Mucoromycotina [3][4][5]6 ] which, interestingly, form mycorrhiza-like associations with basal plant lineages [7], although the last common ancestor of these two fungal groups probably lived well before plants colonised land [8 ]. AM fungi cannot be cultured without their plant partner.…”