Recurrent invasion and extinction of a selfish gene

Abstract

Homing endonuclease genes show super-Mendelian inheritance, which allows them to spread in populations even when they are of no benefit to the host organism. To test the idea that regular horizontal transmission is necessary for the long-term persistence of these genes, we surveyed 20 species of yeasts for the -homing endonuclease gene and associated group I intron. The status of could be categorized into three states (functional, nonfunctional, or absent), and status was not clustered on the host phylogeny. Moreover, the phylogeny of differed significantly from that of the host, strong evidence of horizontal transmission. Further analyses indicate that horizontal transmission is more common than transposition, and that it occurs preferentially between closely related species. Parsimony analysis and coalescent theory suggest that there have been 15 horizontal transmission events in the ancestry of our yeast species, through simulations indicate that this value is probably an underestimate. Overall, the data support a cyclical model of invasion, degeneration, and loss, followed by reinvasion, and each of these transitions is estimated to occur about once every 2 million years. The data are thus consistent with the idea that frequent horizontal transmission is necessary for the long-term persistence of homing endonuclease genes, and further, that this requirement limits these genes to organisms with easily accessible germ lines. The data also show that mitochondrial DNA sequences are transferred intact between yeast species; if other genes do not show such high levels of horizontal transmission, it would be due to lack of selection, rather than lack of opportunity. H oming endonuclease genes (HEGs) are optional or nonessential genes widely distributed in fungi, protists, bacteria, and viruses (1, 2). At least among eukaryotes, where they are often found in organelles associated with group I self-splicing introns, they have no known host function. Rather, they are thought to be selfish or parasitic genes that spread in populations because their catalytic activity results in self-propagation, as they code for a sequence-specific endonuclease (i.e., a protein that cleaves DNA at a particular recognition sequence, in this case usually 12-40 bp long). In heterozygous or heteroplasmic individuals, in which there are both HEG ϩ and HEG Ϫ chromosomes, the protein recognizes and cuts the HEG Ϫ chromosomes; the HEG ϩ chromosomes are protected because the presence of the gene interrupts the recognition sequence. A cut chromosome turns on the cell's recombinational repair system (3), which uses the homologous chromosome (in this case HEG ϩ ) as a template. After repair, the HEG is found on both chromosomes, and the cell is then homozygous HEG ϩ . Consequently, these genes show strong transmission ratio distortion; they are often inherited by more than 95% of progeny, rather than the Mendelian 50% (4, 5).This process of ''homing'' easily explains how such a gene can increase in frequency and become fixed within a population. F...

Evolutionary maintenance of selfish homing endonuclease genes in the absence of horizontal transfer

“…S2. The result is consistent with cyclical models of the gain, degeneration and loss of homing endonuclease genes that are formulated based on the presence of horizontal transfer (3,5). Results under different cost and mutation parameter settings are summarized in Fig.…”

“…Although cyclical models of the gain, degeneration, and loss of homing endonuclease genes based on their horizontal transfer have been formulated (3,5), the present work is, to our knowledge, the first published theoretical analysis to successfully summarize the parameter dependence of the conditions for the cycle in the absence of horizontal gene transfer. Whether the evolutionary maintenance of homing endonuclease genes through periodic oscillation without horizontal gene transfer occurs in nature is worth exploring.…”

“…Homing endonuclease of yeast mitochondria are another example. Mitochondria are biparentally inherited in S. cerevisiae and recombine through a haploid-diploid-like cycle in which a double-strand break induces homologous recombination and gene conversion (5).…”

Multiple self-splicing introns in the 16S rRNA genes of giant sulfur bacteria

“…All ORFs in the introns described here encoded IEPs typical of a common family of homing endonucleases, suggesting that the introns spread into cognate sites as DNA elements via homing (20). The existence of variants that lack, or have truncated IEPs, is considered to be a consequence of introns saturating all possible insertion sites and of IEPs for intron homing becoming redundant (52).…”

Recurrent insertion of 5′-terminal nucleotides and loss of the branchpoint motif in lineages of group II introns inserted in mitochondrial preribosomal RNAs

“…However, whereas degeneration of the middle part of domain VI, which closely precedes or follows the insertion of nucleotides at the 59 splice site, must be irreversible, acquisition of the coding sequence of a homing endonuclease is likely temporary. The reason is that, in a panmictic host population, the selective advantage provided by homing decreases rapidly as previously empty insertion sites become filled by a copy of the intron (Goddard and Burt 1999), so that the coding sequence of the endonuclease should soon begin to accumulate deleterious mutations and degenerate beyond recognition. That is, unless the protein has become essential to its host by acquiring ''maturase'' activity.…”