Abstract

Self splicing introns and inteins that rely on a homing endonuclease for propagation are parasitic genetic elements. Their life-cycle and evolutionary fate has been described through the homing cycle. According to this model the homing endonuclease is selected for function only during the spreading phase of the parasite. This phase ends when the parasitic element is fixed in the population. Upon fixation the homing endonuclease is no longer under selection, and its activity is lost through random processes. Recent analyses of these parasitic elements with functional homing endonucleases suggest that this model in its most simple form is not always applicable. Apparently, functioning homing endonuclease can persist over long evolutionary times in populations and species that are thought to be asexual or nearly asexual. Here we review these recent findings and discuss their implications. Reasons for the long-term persistence of a functional homing endonuclease include: More recombination (sexual and as a result of gene transfer) than previously assumed for these organisms; complex population structures that prevent the element from being fixed; a balance between active spreading of the homing endonuclease and a decrease in fitness caused by the parasite in the host organism; or a function of the homing endonuclease that increases the fitness of the host organism and results in purifying selection for the homing endonuclease activity, even after fixation in a local population. In the future, more detailed studies of the population dynamics of the activity and regulation of homing endonucleases are needed to decide between these possibilities, and to determine their relative contributions to the long term survival of parasitic genes within a population. Two outstanding publications on the amoeba Naegleria group I intron (Wikmark et al. BMC Evol Biol 2006, 6:39) and the PRP8 inteins in ascomycetes (Butler et al.BMC Evol Biol 2006, 6:42) provide important stepping stones towards integrated studies on how these parasitic elements evolve through time together with, or despite, their hosts.

Highlights

  • BMC Evolutionary Biology 2006, 6:94 http://www.biomedcentral.com/1471-2148/6/94 host's fitness

  • The molecular parasites have gained their own individuality, and to understand their evolution, one has to consider their life cycle. These parasitic elements are labeled as selfish genes; according to Dawkins [1] all genes are selfish, we prefer the label "parasitic" to reflect the fact that these genes are not cooperating to the benefit of the host organism

  • The spread of these parasites in the population relies on the different alleles being brought together through sex or gene transfer; many mobile elements with homing endonucleases (HE) activity are found in organisms and organelles thought to be nearly clonal or relying on asexual genetic exchange, e.g., fungi [11] and amoeba [12] without known sexual recombination

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Summary

Dawkins R

2. Liu XQ: Protein-splicing intein: Genetic mobility, origin, and evolution. 8. Gimble FS: Invasion of a multitude of genetic niches by mobile endonuclease genes. Cho Y, Palmer JD: Multiple acquisitions via horizontal transfer of a group I intron in the mitochondrial cox gene during evolution of the Araceae family. Goodrich-Blair H, Shub DA: Beyond homing: competition between intron endonucleases confers a selective advantage on flanking genetic markers.

25. Stoltzfus A
31. Mines GR
38. Avise JC

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