Mitochondrial RNase P RNAs in ascomycete fungi: Lineage-specific variations in RNA secondary structure

Abstract

The RNA subunit of mitochondrial RNase P (mtP-RNA) is encoded by a mitochondrial gene (rnpB) in several ascomycete fungi and in the protists Reclinomonas americana and Nephroselmis olivacea. By searching for universally conserved structural elements, we have identified previously unknown rnpB genes in the mitochondrial DNAs (mtDNAs) of two fission yeasts, Schizosaccharomyces pombe and Schizosaccharomyces octosporus; in the budding yeast Pichia canadensis; and in the archiascomycete Taphrina deformans. The expression of mtP-RNAs of the predicted size was experimentally confirmed in the two fission yeasts, and their precise 5 and 3 ends were determined by sequencing of cDNAs generated from circularized mtP-RNAs. Comparative RNA secondary structure modeling shows that in contrast to mtP-RNAs of the two protists R. americana and N. olivacea, those of ascomycete fungi all have highly reduced secondary structures. In certain budding yeasts, such as Saccharomycopsis fibuligera, we find only the two most conserved pairings, P1 and P4. A P18 pairing is conserved in Saccharomyces cerevisiae and its close relatives, whereas nearly half of the minimum bacterial consensus structure is retained in the RNAs of fission yeasts, Aspergillus nidulans and Taphrina deformans. The evolutionary implications of the reduction of mtP-RNA structures in ascomycetes will be discussed.

Transcription and RNA-processing in fission yeast mitochondria

“…(3) The rnpB RNA was detected at a size of 274 nt (Fig. 3B), confirming an earlier prediction using sequence and structure similarity to other mitochondrial RNase P RNAs, and precise mapping of 5Ј-and 3Ј-ends (Seif et al 2003).…”

“…1) carries genes for two ribosomal RNAs (rnl, rns), a complete set of 25 tRNAs, the RNAencoding RNase P RNA (rnpB) (Seif et al 2003), and a total of eight proteins (Paquin et al 1997;for review, see Schäfer 2003). In the strain used here, the cox1 gene contains two group I introns, whereas the cob gene is endowed with a single group IIA1 intron; all introns are not essential (Schäfer et al 1991).…”

The RNase P family

“…Structures are modified from the RNase P Database. 20,44 transcribed without leaders and the RNase P RNA and associated proteins has been dispensed with entirely. 46,50 It is also likely that the RNase P RNA has been replaced in the RNase P enzyme of the plastids of green plants, but the components of this enzyme have yet to be determined.…”

“…41 RNase P. Ascomycete mitochondrial RNase P RNAs are, on the other hand, highly reduced in size and lack most of the sequence and structural elements conserved in other RNase P RNAs. [42][43][44][45] The human (and presumably other metazoans) mitochondrial RNase P lacks the RNA subunit entirely; the RNase P catalytic function has been replaced by a Rube Goldberg triad of unrelated proteins. 46,47 The secondary structure of RNase P RNAs from primitive plastids are similar to those of cyanobacteria, from which they derive.…”

RNase P enzymes

“…This was first observed in many fungi, where the consensus structure contains only two of the 11 conserved helices found within the minimal bacterial consensus structure. 3 Furthermore, the Saccharomyes cerevisiae mitochondrialencoded RNA associates with a single 105-kDa nuclear-encoded RPM2 protein that shares no homology to any other known RNase P proteins. The deviation in sequence and increased size of RPM2 suggests that the protein moiety could play a more substantial role in catalysis or molecular recognition.…”