The group I intron interrupting the tRNA-Leu (UAA) gene in plastids dates back at least 1 billion years before the present, having entered eukaryotes through endosymbiosis. As such, it is the most ancient known intron and provides a unique opportunity to study the long-term evolution of a group I intron. Group I introns are autocatalytic (i.e., self-splicing) intervening sequences which have conserved primary and secondary structures. Due to these characteristics, they have evoked a great deal of interest in both their biochemical properties and their evolutionary history. Here, we reconstruct the phylogeny of the tRNA-Leu intron in cyanobacteria and in algae/land plants and ask whether differing evolutionary histories are associated with differing self-splicing ability. Our results suggest this to be the case. The present day distribution of the intron in plastids is consistent with an evolutionary history characterized by strict vertical transmission, with no losses in land plants, and pervasive loss among green algae, as well as in the red algae and their secondary derivatives. Interestingly, all land plant introns have lost their ability to self-splice in vitro and presumably have become dependent on a host factor to facilitate splicing in vivo. However, in all other lineages there have been multiple intron losses and at least a partial retention of self-splicing ability. Specifically, all cyanobacterial introns are self-splicing whereas in the remaining lineages (green algae, glaucophytes, and heterokonts), at least the first step of autocatalysis occurs in vitro. Although speculative, the heavily biased distribution of this intron in plastids suggests that its processing in land plants may differ from that in other lineages. Our data also suggest a possible correlation between long-term vertical ancestry of the tRNA-Leu group I intron and loss of self-splicing ability.

Key words: evolution, group I intron, plastid, splicing