A sequence encoding a maturase-related protein in a group II intron of a plant mitochondrial nad1 gene.

Abstract

We have determined from nucleotide sequence analysis that the subterminal and terminal exons of a respiratory-chain NADH dehydrogenase subunit I gene in broad bean mitochondrial DNA (mtDNA) are separated by a group II intron. Within this intron is a 687-codon open reading frame that, from considerations of similarity between amino acid sequences predicted from this open reading frame and maturase-coding sequences in group II introns ofcertain fungal mitochondrial genes, appears to encode a maturase-related protein. Transcripts complementary to this broad bean sequence (designated a mat-r gene) were detected among RNAs isolated from broad bean mitochondria. Data obtained from DNADNA hybridizations indicated that soybean and corn mtDNAs also contain a mat-r gene and suggested that only one copy of this gene occurs in each plant mtDNA. The putative protein specified by the broad bean mat-r gene contains amino acid sequences characteristic of reverse transcriptases. Because of this, consideration is given to the possibility that the maturase-related protein may be functional in the mechanisms by which plant mtDNA sequences are rearranged and foreign sequences are incorporated into plant mtDNAs.Plant mitochondrial DNAs (mtDNAs) contain the genes for a number of subunits of proteins involved in oxidative phosphorylation and genes for three ribosomal proteins (rpS12, rpS13, and rpS14) (1-3). Introns have been reported only in some plant coxIf genes, in the corn and watermelon nadl genes, and in the nadS gene of Oenothera (4-7). Each of these introns is of the group II type found only in organelle genes (8, 9). Unlike the situation in yeast and other fungi, where some group II (and group I) introns encode enzymes (maturases) necessary for excision of the maturase-encoding intron from RNA transcripts of the gene (10-12), none of the aforementioned plant mitochondrial (mt) introns appears to encode a protein.In this paper, we report the occurrence within a group II RESULTSThe nucleotide sequence of a 4481-nucleotide-pair (ntp) segment of broad bean mtDNA is given in Fig. 1 and our analysis of this sequence is summarized in Fig. 2. Three regions of the amino acid sequence predicted from a 2061-ntp (687 codons) open reading frame within this sequence show considerable similarity to corresponding consecutive regions ofamino acid sequences of the maturase encoded by the all intron of the cytochrome c oxidase subunit I (coxI) gene of Saccharomyces cerevisiae and by the following fungal putative maturase gene-containing mt intron sequences (Fig. 3): aI2 of the coxI gene of S. cerevisiae (14), I and IA of the coxI gene of Podospora anserina (15,16), and bl of the cytochrome b (cob) gene of Schizosaccharomyces pombe (17). Because of these amino acid sequence similarities, we have designated the putative broad bean protein a maturase-related protein (MAT-R) and the sequence that encodes it a mat-r gene.The broad bean mat-r gene, like the S. cerevisiae, P. anserina, and Sc. pombe mat genes, is contained in a group II intro...

Miniaturized mitogenome of the parasitic plant Viscum scurruloideum is extremely divergent and dynamic and has lost all nad genes

“…However, because matR resides within nad1 intron 4, it is more likely that matR was lost along within the entire suite of mitochondrial nad genes in Viscum. MatR is the only mitochondrial-specified maturase homolog present in angiosperms, and although the precise function of MatR in mitochondria is uncertain, it is clearly homologous to proteins known to assist in group II intron splicing in other mitochondrial genomes (22). Furthermore, preliminary data suggest that MatR binds to several group II introns in vivo (23).…”

Multiple trans-splicing events are required to produce a mature nad1 transcript in a plant mitochondrion.

“…The protein sequence predicted from this gene is similiar to the maturases encoded within fungal mitochondrial introns (Wahleithner et al 1990). As yet, it is not known whether the plant mat-r sequences actually specify a protein with maturase activity.…”

The plant mitochondrial mat-r gene/nad1 gene complex

“…A similar exon-intron organization has been reported for the wheat and Petunia nadl genes (Chapdelaine and Bonen, 1991;. In broad bean, soybean, Oenothera, and Arabidopsis, the D and E exons are joined by a continuous group II intron (Wahleithner et al, 1990;Wolstenholme et al, 1990;Wissinger et al, 1990Wissinger et al, , 1991Thomson et al, 1994;Brennicke et al 1996).…”

“…A gene designated mat-r (first described by us in broad bean mtDNA [Wahleithner et al, 1990]) for a protein related to yeast group 11intron maturases (Carignani et al, 1983) is contained within the partial group II intron upstream from the maize nadl exon E. In broad bean, soybean, Oenothera, and Arabidopsis, this gene is contained in the continuous intron between exons D and E (Wahleithner et al, 1990;Wolstenholme et al, 1990Wolstenholme et al, , 1993Wissinger et al, 1991;Thomson et al, 1994). In Petunia, the mat-r gene is contained in the portion of the split d/e intron linked to exon D .…”

“…The first ATG from the 5' end of the MAT-R-encoding ORF is either codon 23 (broad bean and Oenothera) or codon 27 (maize, wheat, soybean). We were hesitant to interpret these ATGs as translation initiation codons because the amino acid sequences predicted from the region upstream of these codons are almost completely conserved among the five angiosperms, and are highly conserved relative to the amino acid sequences of fungal maturases (Wahleithner et al, 1990). However, examination of sequences of cDNAs of transcripts of regions upstream from, and including the 5' end of the ORF, and sequences of cDNAs primed within the 5' end region of the ORF, rule out the possibilities that in transcripts, either a new AUG is created or the ORF is extended upstream as the result of either RNA editing (nucleotide substitution or deletion/insertion) or of RNA ., splicing.…”