‘Why genomes in pieces?’ revisited: Sucking lice do their own thing in mtDNA circle game

Abstract

About 30 yr ago, an organizational nightmare emerged in the budding field of genomics. Several independent groups discovered that the genetic information encoding genes was not arranged in a continuous linear format of adjacent nucleotides. To everyone's surprise, the coding information for proteins was interrupted by noncoding sequences that were removed from initial RNA transcripts before translation continued the job of the central dogma: information transfer from DNA to RNA to protein. Walter Gilbert made sense of all of this (Gilbert 1978) when, in a few hundred words, he coined the terms intron and exon, predicted that the protein coding content of genomes would comprise only a fraction of the total DNA, triggered the “introns-early” versus “introns-late” debate, and set the seed for the notion that RNA was the early form genetic material. The field of genomics survived this chaos and now relishes these confusing disruptions, where our understanding of how the world works is turned on its head by some odd fact. In hindsight, there often seems to be an appealing reason for why a genome would engage in something so illogical. Gilbert suggested that introns facilitate higher rates of per-gene recombination, promoting diversity and permitting faster evolutionary change (Gilbert 1978). Some of the biggest questions in genomics today are focusing on phenomena that we might never have imagined only a generation ago: epigenetic modification of expression and transmission, microRNAs and RNA interference, arms of sex chromosomes and autosomes jumping ship and going over to the other side, among others. One might think that all strange facts of genome organization and expression should have been discovered by now, but even in the heavily scrutinized world of mitochondrial genomics, fascinating novelties are still emerging. The study by Shao et al. (2009) in this issue, reports an almost comical departure from the standard single-circle mitochondrial genome organization found in most animals. It appears that sucking lice associated with humans—and not other lice—have evolved a multiple minichromosome organization for mtDNA that begs the question: Why genomes in pieces? This same question has been asked before in the context of mtDNA organization (Landweber 2007), but animals were not the topic of concern. Departures from the “standard” single-circle mtDNA organization have been observed in protists, such as Diplonema, where genes (and notably parts of genes) are fragmented across many minicircles (Marande and Burger 2007). In the Kinetoplastida (a group including Trypanosomes), mitochondrial genes are distributed among thousands of catenated circles in a network of mini- and maxicircles (for review, see Lukes et al. 2002). Across all of eukaryotic biodiversity, the “standard” single-circle mtDNA may in fact not be the standard, but in animals it is indeed the norm that highlights Shao et al.'s intriguing exception.