A horizontally transferred tRNA^Cys gene in the sugar beet mitochondrial genome: evidence that the gene is present in diverse angiosperms and its transcript is aminoacylated

Abstract

SUMMARYOf the two tRNA Cys (GCA) genes, trnC1-GCA and trnC2-GCA, previously identified in mitochondrial genome of sugar beet, the former is a native gene and probably a pseudo-copy, whereas the latter, of unknown origin, is transcribed into a tRNA [tRNA Cys2(GCA)]. In this study, the trnC2-GCA sequence was mined from various public databases. To evaluate whether or not the trnC2-GCA sequence is located in the mitochondrial genome, the relative copy number of its sequence to nuclear gene was assessed in a number of angiosperm species, using a quantitative real-time PCR assay. The trnC2-GCA sequence was found to exist sporadically in the mitochondrial genomes of a wide range of angiosperms. The mitochondrial tRNA Cys2 (GCA) species from sugar beet (Beta vulgaris), spinach (Spinacea oleracea) and cucumber (Cucumis sativus) were found to be aminoacylated, indicating that they may participate in translation. We also identified a sugar beet nuclear gene that encodes cysteinyl-tRNA synthetase, which is dual-targeted to mitochondria and plastids, and may aminoacylate tRNA Cys2 (GCA). What is of particular interest is that trnC1-GCA and trnC2-GCA co-exist in the mitochondrial genomes of eight diverse angiosperms, including spinach, and that the spinach tRNA Cys1 (GCA) is also aminoacylated. Taken together, our observations lead us to surmise that trnC2-GCA may have been horizontally transferred to a common ancestor of eudicots, followed by co-existence and dual expression of trnC1-GCA and trnC2-GCA in mitochondria with occasional loss or inactivation of either trnC-GCA gene during evolution.

The “fossilized” mitochondrial genome of Liriodendron tulipifera: ancestral gene content and order, ancestral editing sites, and extraordinarily low mutation rate

“…Plant mitochondrial genomes contain tRNAs of diverse origin – native mitochondrial, plastid [7], and one, trnC(GCA) , that appears to have been horizontally transferred from bacteria [8]. The Liriodendron mitochondrial genome possesses intact copies of 12 of the 13 tRNA genes of mitochondrial origin found variously across angiosperms, as well as a truncated remnant of the other, trnD ( GTC) .…”

“…In addition, no sequenced angiosperm mitochondrial genome contains a full set of native tRNAs necessary for the translation of its full gene complement [6]. Moreover, tRNA content varies widely among species, with each genome containing some mixture of tRNAs of mitochondrial, plastid and possibly bacterial origin [3,7,8]. Missing tRNAs are encoded in the nucleus and imported from the cytosol.…”

Unusual and Typical Features of a NovelRestorer-of-FertilityGene of Sugar Beet (Beta vulgarisL.)

“…A PCR fragment corresponding to the first 58 amino acids of Arabidopsis RuBisCo activase was amplified and then substituted for the Arabidopsis F1-ATPase δ-subunit region of pMt-R. The resulting plasmid was designated pCp-R (Kitazaki et al 2011). Plasmid DNA was ethanol precipitated with gold particles of 1 μm diameter (Bio-Rad Laboratories) and then introduced into the epidermal cells of onion bulbs or Welsh onion sheaths using a GIE-III IDERA system (Tanaka, Ishikari, Japan).…”

Horizontal Transfer of Entire Genomes via Mitochondrial Fusion in the Angiosperm Amborella

“…S2, S4) (13). This would not be surprising, because cognate tRNAs of diverse origin (plastid, nuclear, bacterial) often replace native tRNAs in plant mitochondrial translation (6,11,20,21). Moreover, even a modest number of tRNA gene replacements could have led to the fixation, via genetic hitchhiking, of a considerable portion of the foreign mtDNA in Amborella.…”

“…S13). These, and even some of the native tRNA genes still present (20), may have been functionally replaced by some of its dozens of intact foreign tRNA genes (figs. S2, S4) (13).…”