The trouble with (group II) introns

Qu et al. provide new grist for the introns origin mill (1), adding one more chapter to what has become a very long narrative. Back in the day when spliceosomal introns in the protein-coding genes of eukaryotes were still very new to science (1977–1978), some of us argued that—in an evolutionary sense—they were actually very old (2, 3). According to our soon quite popular “introns-early” theory, pre-mRNA introns were actually the relics of ancient precellular gene assembly processes. We conjectured that these intervening sequences had been lost by “streamlining” in prokaryotes but retained in eukaryotes, where they might continue to play an evolutionary role in “exon shuffling” (4, 5). Despite the heroic efforts of Wally Gilbert to prove this notion right, it has largely fallen out of favor. Anticipated correlations between intron positions and protein module boundaries were never convincingly demonstrated, and the topology of the universal Tree of Life [especially now, with eukaryotes emerging from within archaea (6)] makes introns early unparsimonious. What has taken its place is an “introns-late” view first articulated in 1987 by Tom Cavalier-Smith (7). According to this, spliceosomal introns are the descendants of group II introns introduced into eukaryotes via the genome of the α-proteobacterium that was to become the mitochondrion—a sort of cellular Trojan horse (Fig. 1). Phil Sharp’s aptly titled “Five easy pieces” (8) showed how one or more of the group II introns deposited in nuclear genomes might have over time degenerated into the five snRNAs that now, assisted by many proteins, are the agents of removal of what is left of all of the rest of the invaders. Everything that has happened in the quarter century since then serves to strengthen the belief that structural and functional similarities between group II introns and spliceosomal snRNAs are indeed true …