Plant mitochondria use two pathways for the biogenesis of tRNA(His)

All tRNA(His) possess an essential extra G(–1) guanosine residue at their 5′ end. In eukaryotes after standard processing by RNase P, G(–1) is added by a tRNA(His) guanylyl transferase. In prokaryotes, G(–1) is genome-encoded and retained during maturation. In plant mitochondria, although trnH genes possess a G(–1) we find here that both maturation pathways can be used. Indeed, tRNA(His) with or without a G(–1) are found in a plant mitochondrial tRNA fraction. Furthermore, a recombinant Arabidopsis mitochondrial RNase P can cleave tRNA(His) precursors at both positions G(+1) and G(–1). The G(–1) is essential for recognition by plant mitochondrial histidyl-tRNA synthetase. Whether, as shown in prokaryotes and eukaryotes, the presence of uncharged tRNA(His) without G(–1) has a function or not in plant mitochondrial gene regulation is an open question. We find that when a mutated version of a plant mitochondrial trnH gene containing no encoded extra G is introduced and expressed into isolated potato mitochondria, mature tRNA(His) with a G(–1) are recovered. This shows that a previously unreported tRNA(His) guanylyltransferase activity is present in plant mitochondria.