Molecular Biology and Evolution 19:239-246 (2002)
© 2002 Society for Molecular Biology and Evolution
Adaptation for Horizontal Transfer in a Homing Endonuclease
*Department of Biology
NERC Centre for Population Biology, Imperial College, Silwood Park, Ascot, Berkshire, U.K
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Selfish genes of no function other than self-propagation are susceptible to degeneration if they become fixed in a population, and regular transfer to new species may be the only means for their long-term persistence. To test this idea we surveyed 24 species of yeast for VDE, a nuclear, intein-associated homing endonuclease gene (HEG) originally discovered in Saccharomyces cerevisiae. Phylogenetic analyses show that horizontal transmission has been a regular occurrence in its evolutionary history. Moreover, VDE appears to be specifically adapted for horizontal transmission. Its 31-bp recognition sequence is an unusually well-conserved region in an unusually well-conserved gene. In addition, the nine nucleotide sites most critical for homing are also unusually well conserved. Such adaptation for horizontal transmission presumably arose as a consequence of selection, both among HEGs at different locations in the genome and among variants at the same location. The frequency of horizontal transmission must therefore be a key feature constraining the distribution and abundance of these genes.
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResults and DiscussionConclusionsAcknowledgementsReferences |
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Homing endonuclease genes (HEG) are nonessential genes with no known function, at least in eukaryotes (Mueller et al. 1993
; Belfort and Roberts 1997
; Jurica and Stoddard 1999
; Gimble 2000
). Rather, they are thought to be selfish or parasitic genes that spread and persist in populations because their catalytic activity results in super-Mendelian inheritance. Frequent horizontal transmission has previously been demonstrated for mitochondrial HEGs associated with self-splicing introns in both plants and fungi (Cho et al. 1998
; Goddard and Burt 1999
). HEGs also exist in the nucleus (Dalgaard et al. 1997a
; Perler, Olsen, and Adam 1997
), where horizontal transmission might be expected to be more difficult. VDE (also known as PI-SceI) is an apparently selfish element inside the VMA1 gene of Saccharomyces cerevisiae (Gimble and Thorner 1992
). It encodes a compound protein consisting of a self-splicing intein domain (analogous to a self-splicing intron but operating at the protein level) and an endonuclease domain with two LAGLIDADG motifs. These two domains are functionally independent and have had separate evolutionary origins (Dalgaard et al. 1997a
; Derbyshire et al. 1997
). VMA1 genes that contain VDE are translated into a polypeptide, and then VDE is spliced out in an autocatalytic reaction which ligates the two flanking regions, leaving a functional VMA1 protein. In individuals heterozygous for the presence of VDE, the excised VDE protein recognizes a 31-bp sequence of the VDE- allele and cuts it; the VDE+ allele is immune to cutting as the VDE gene interrupts the 31-bp sequence. The presence of the cut allele induces the cell's recombinational repair system, which uses the VDE-containing homologue as a template for repair, after which both alleles are VDE+. This "homing" mechanism results in VDE being inherited in 90% of meiotic products, rather than the Mendelian 50% (Gimble and Thorner 1992
), which should allow it to increase in frequency and go to fixation within a population. However, once fixed, there would be little or no selection maintaining endonuclease function, as there would be no chromosomes left to cut (except for rare deletion mutations), and one might expect the endonuclease domain to degenerate over evolutionary time because of mutation pressure, aided perhaps by natural selection if there is any cost to the host cell of producing a functional endonuclease (Goddard and Burt 1999
; Gimble 2000
). The splicing domain, however, should remain functional, regardless of saturation, as there will always be strong selection for a functional VMA1 gene.
If fixation is followed by degeneration, then the only way for VDE to persist as a HEG over long evolutionary time spans would be to occasionally move to a new location, on average at least once before degeneration. In principle, movement might be to a new place in the same genome (transposition) or to a different species (horizontal transmission). For mitochondrial HEGs associated with self-splicing introns, horizontal transmission is much more common than transposition (Cho et al. 1998
; Goddard and Burt 1999
). In no case is the mechanism of horizontal transmission known, and unlike transposable elements, there is no extrachromosomal phase in the normal propagation of a HEG which might facilitate horizontal transmission. For yeasts, perhaps the simplest scenario is that there is occasionally some leakage of mtDNA during the preliminary phase of interspecific matings that are subsequently aborted. Such direct transfer might be more difficult for a nuclear HEG, as it would seem to require full nuclear fusion, and hybrids of even close relatives are usually sterile (Naumov 1987
; Marinoni et al. 1999
). It is for these reasons that the study of a nuclear HEG is of interest. Furthermore, note that, whatever the mechanism of crossing the species barrier, a key prerequisite for the successful transfer and spread of a HEG is that the recognition sequence exists in the recipient species. If the ability to undergo horizontal transmission is an important factor in the persistence of a HEG, then one expects there to have been selection against HEGs with poorly conserved recognition sequences. VDE, which has persisted, should therefore have an unusually well-conserved recognition sequence.
To test whether VDE shows horizontal transmission, we surveyed 22 species of saccharomycete yeasts from four closely related genera (Saccharomyces, Torulaspora, Zygosaccharomyces, and Kluyveromyces) for the presence or absence of VDE in the VMA1 gene or elsewhere in the genome and combined our results with published data from two more distantly related yeasts, Candida tropicalis (Gu et al. 1993
) and C. albicans (Stanford DNA Sequencing and Technology Centre; http://www-sequence.Stanford.edu/group/candida). We then analyzed the distribution of VDE in the 24 species and compared the phylogenetic relationships among all VDEs recovered with those of the host species. To examine whether VDE might be specifically adapted for horizontal transmission, we tested whether the VDE recognition site is an unusually well-conserved region of the genome.
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Materials and Methods |
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Yeast Strains and Molecular Methods
All strains were obtained from the Centraalbureau Voor Schimmelcultures (CBS; Delft, The Netherlands), except S. paradoxus, S. cariocanus, and S. kudriavzevii, which were obtained from Dr. Edward Louis, Leicester. Strains were grown overnight and DNA extracted (Strathern and Higgins 1991
). Presence or absence of VDE in the VMA1 gene was assayed by PCR using degenerate primers flanking the VDE insertion site, 83-bp upstream and 291-bp downstream, based on VMA1 sequences from S. cerevisiae, C. tropicalis, Schizosaccharomyces pombe, and Neurospora crassa (primer sequences, 5' to 3': VR1: GGI GCI TTY GGI TGY GGI AA; VR2: GAA ICC TTG RTC IGC IAG CAT, where I is inosine, Y is C + T and R is A + G). All PCR products, both with and without VDE, were sequenced directly using an ABI 373 automated sequencer (EMBL accession numbers AJ307891–902 and AJ312425–33). To screen for VDE elsewhere in the genome, total genomic DNA from the 22 species was digested with HaeIII, electrophoresed, and transferred to a nylon membrane. It was then probed with PCR products from VDE sequences obtained using primers internal and near the two ends of VDE. For control, the membrane was also probed separately with PCR products from empty (i.e., VDE-) VMA1 alleles, amplified with primers VR1 and VR2.
Phylogenetic Analyses
DNA sequences were translated using the ABI Sequence Navigator program and amino acid sequences aligned with Clustal W (Thompson, Higgins, and Gibson 1994
). To reconstruct the host phylogeny, nuclear 18S, 26S, and ITS1-5.8S-ITS2 data were obtained from GenBank (Cai, Roberts, and Collins 1996
; James et al. 1997
; Kurtzman and Robnet 1998
; Goddard and Burt 1999
). Sequence alignments can be obtained from the authors. Phylogenetic analyses were performed with PAUP* (Version 4.0d64) (Swofford 1999
), MacClade (Version 3.07) (Maddison and Maddison 1992
), MultiLocus (Version 1.0b; http://www.bio.ic.ac.uk/evolve/software/multilocus), and Mathematica (Version 3.0.1) (Wolfram 1996
).
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Results and Discussion |
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Detection and Isolation
All species gave a single, unambiguous PCR product, the size of which indicated whether it was VDE+ or VDE-, except Z. rouxii, which gave both VDE+ and VDE- amplicons. These latter bands were reconfirmed by multiple isolations and PCR-amplifications of VMA1 from genomic DNA initially derived from single cell cultures. Both amplicons were sequenced, and the VMA1 fragments differed at 12% of nucleotide sites (all changes but one were silent). This is substantially more than would be expected for alleles at a single locus and is greater than the divergence between some pairs of species (e.g., 3.6% nucleotide divergence for S. cerevisiae-S. cariocanus VMA1 fragments), suggesting that there has been a gene duplication event in the lineage leading to Z. rouxii. Note that the high divergence of the empty VMA1 allele might prevent it from being repaired by the other copy of the gene were it cut by the endonuclease. Only the VDE+ gene is included in our analyses. Of the 24 species, 14 had a VDE insertion in the VMA1 gene (fig. 1 ). VDE genes varied in length from 1,230 to 1,551 bp, and for the alignable regions, average amino acid divergence was 40%, ranging 7%–56%. As expected, and unlike the
endonuclease (Goddard and Burt 1999
), none of the 14 sequences contained mutations disrupting the reading frame, as these would interrupt translation of the VMA1 gene. Also, there is no correlation between the presence of VDE and (G = 0.01, n = 20 species, P > 0.5) and thus no evidence that some species are particularly susceptible or resistant to HEGs in general.
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To test whether VDE occurs at other locations in the genome, DNA from the 22 species was probed with 7 of the 14 VDE sequences chosen to span the full range of VDE diversity, in two batches. The first batch included VDE probes from S. castellii, S. unisporus, K. lactis, and K. polysporus and gave hybridization signals from these four species plus S. exiguus and S. dairenensis. The second batch included probes from S. cerevisiae, Z. bailii, and T. pretoriensis and gave signals only from these three species. As control, the membrane was also probed separately with the VDE- sequences from S. kudriavzevii and K. thermotolerans, and all species gave a strong hybridization signal. The lack of crosshybridization for VDE is consistent with its high divergence among the species assayed. With the exception of S. exiguus, the position, number, and size of all VDE hybridization bands were as expected from the VDE- hybridizations and the presence of HaeIII restriction sites, i.e., either they were identical to the VDE- hybridization bands or their size was as expected by the presence of additional HaeIII sites inside the VDE sequences. These results indicate that VDE only exists inside the VMA1 gene, if at all. For S. exiguus, one extra band was obtained for both VMA1 and VDE hybridizations, though neither fragment included a HaeIII restriction site, perhaps indicating that the strain is heterozygous for a site beyond the fragments considered here or there has been a gene duplication not detected by PCR. Thus, VDE does not appear to exist at any location in the genome of these yeast species other than the VMA1 gene.
Horizontal Transmission
The distribution of VDE in the Saccharomycetaceae appears to be random, without significant clustering along specific clades, indicating multiple independent gains or losses (or both) (fig. 1 ). Significant clustering of states on the tree would have suggested that gains and losses are relatively infrequent events. The most parsimonious character reconstruction for the observed distribution of VDE on the host tree infers eight steps and is no shorter than the length obtained when presence/absence is randomized on the tree (P = 0.66, from 100 randomizations). We also failed to find significant clustering if gains or losses are modeled as irreversible (P = 0.94 and 0.59, from 100 randomizations, respectively). To estimate the rates of VDE gain and loss, we used a maximum likelihood approach, combining information from the observed distribution of VDE and the maximum parsimony host tree (fig. 1
; Pagel 1994
). Branch lengths were estimated by maximum likelihood while enforcing a molecular clock (Swofford 1999
) and were calibrated following Berbee and Taylor (1993)
. The fit of a two-parameter model, in which rates of gain and loss are allowed to differ, is not significantly better than the one-parameter model with equal rates (
lnL = 0.33, df = 1, NS [not significant]) but is significantly better than unidirectional models in which only gains or only losses are allowed (lnL = 19.46 and 16.62, respectively, df = 1, P < 0.001). Therefore, to estimate the rates of gain and loss we fitted a one-parameter model with equal rates. The estimate maximizing the likelihood of the data is 
(infinity), with a lower bound of 0.17 events per million years (from the 2-unit support limit, i.e., the value at which the lnL is 2 units less than the maximum, which is equivalent to the 95% confidence limit; Edwards 1992
; note that this does not take into account error in the phylogeny; fig. 1
). This is equivalent to a maximum average waiting time of 6 Myr for each transition. As the total time represented in the entire phylogeny is estimated to be 766 Myr, this implies at least 128 gains and losses in the ancestry of our 24 species. Note this last estimate is independent of the temporal calibration of the host tree. It indicates that VDE has been an extremely dynamic element, continuously moving in and out of species throughout its evolutionary history.
A history of horizontal transmission should mean that the phylogenies of host and VDE are significantly different. Before testing this prediction, we first determined whether the self-splicing and endonuclease domains of VDE themselves have different phylogenetic histories (Dalgaard et al. 1997a
). Separate phylogenies for the two domains have no well-supported branches (i.e., with bootstrap values >70%) that are incompatible between trees (not shown), and the data sets do not differ by the partition homogeneity test (P = 0.11; Farris et al. 1995
). However, the host and VDE phylogenies are strikingly different (fig. 2
). First, each tree has well-supported branches that are incompatible with the other tree. Second, each of the two data sets fits its own tree significantly better than the alternative tree (winning sites test; 83 of 95 sites, P < 0.0001, and 63 of 71 sites, P < 0.0001, for host and VDE data sets, respectively; Swofford 1999
). Finally, the two data sets are significantly different by the partition-homogeneity test (P << 0.001; fig. 2
; Farris et al. 1995
; Swofford 1999
), despite having similar amounts of homoplasy (consistency index [CI] = Lmin/Lshortest: 0.73 = 475/649 and 0.78 = 472/605, for the host and VDE trees, respectively, with character changes distributed over 153 and 126 informative sites). These incompatibilities provide compelling evidence for horizontal transmission of VDE across yeast species. An absolute lower bound on the number of horizontal transmission events can be obtained by calculating how many branches of one tree have to be cut off and reconnected in a new position to transform it into the other tree (Hein 1993
). Starting with the better resolved VDE tree, it takes four such rearrangements to get the host tree or three rearrangements to get a tree that is not significantly worse than the best host tree (table 1
). However, such an approach is likely to substantially underestimate the actual number of rearrangements (Goddard and Burt 1999
).
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To test whether there is still an association remaining between the host and VDE phylogenies, despite the horizontal transmission events, we compared the length of the shortest tree fitted to the combined host-VDE data set to the length of trees fitted to data sets in which the host-VDE association was randomized (Koufopanou, Burt, and Taylor 1997
). The observed association gave significantly shorter tree lengths than the randomized associations (1,208 vs. 1,220–1,290 for the observed and 100 random associations, respectively; P < 0.01). One possible explanation for such an association is that transfers tend to be between close relatives. Consistent with this possibility, deep nodes in the host tree (leading to C. tropicalis and K. lactis) correspond to deep nodes in the VDE tree (fig. 2
). Moreover, TBLASTN searches of GenBank with our VDE sequences failed to retrieve any close homologue except the yeast mating-type switching (HO) gene, implying that transfers among yeasts are more common than transfers from the more distantly related taxa known to have intein-associated HEGs (bacteriophages, eubacteria, archaea, and algal chloroplasts; Dalgaard et al. 1997a
; Perler, Olsen, and Adam 1997
).
Adaptation for Horizontal Transfer
Three lines of evidence indicate that the recognition sequence of VDE is particularly well conserved. First, the host gene, VMA1, is unusually well conserved among yeasts. Complete or virtually complete genomes are now available for two yeasts, S. cerevisiae and C. albicans, and we used these to compute an average amino acid divergence of genes: 20 genes of known function were chosen randomly from the S. cerevisiae genome directory (Goffeau et al. 1997
) and used as queries to search the C. albicans genome data base (Stanford DNA sequencing and technology centre; http://www-sequence.Stanford.edu/group/candida). VMA1 is 12% divergent, significantly better conserved than random genes in the two species (one-tailed t-test on arcsine-transformed values, t = 2.76, P < 0.01; fig. 3a
). Second, an alignment of VMA1 genes from six ascomycete fungi shows that the 31-bp recognition sequence of VDE is significantly better conserved than random 31-bp regions within the gene (P = 0.03; fig. 3b
). This last result could be due in part to the homogenization of the recognition sequence, through coconversion of flanking regions during homing (Dujon 1989
; Cho et al. 1998
), though the high divergence of VDE among species suggests that this cannot be a strong effect. Finally, within VDEs 31-bp recognition sequence, there are nine sites which have been identified by site-directed mutagenesis as being critical for effective homing (Gimble and Wang 1996
). Our VMA1 sequences include the recognition site for all 24 species, and these nine sites are perfectly conserved in all 24 species and are significantly better conserved than the other 22 sites (G = 9.83, P < 0.005, fig. 3c
). These results indicate that VDE has evolved to use as its homing site a region that is very highly conserved and thus likely to be present in a large variety of species.
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Conclusions |
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TOPAbstractIntroductionMaterials and MethodsResults and DiscussionConclusionsAcknowledgementsReferences |
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Simple evolutionary reasoning suggests that HEGs may be unable to persist over long time spans without regular movement, either by transposition to a new location in the genome or by horizontal transmission to a new species. Similar logic has also been applied to other selfish genetic elements (Hurst, Hurst, and Majerus 1992
; Lohe et al. 1995
; Hurst and McVean 1996
). Motivated by this idea, we surveyed 24 species of yeasts for VDE and found it to be widespread, present in 14 species. Various phylogenetic analyses give strong evidence for regular horizontal transmission, with some suggestion that it is more common between more closely related species; transposition to new sites was not detected. A specific reliance on horizontal transmission might also plausibly explain the absence of HEGs in animals (except in the mitochondrion of the sea anemone Metridium senile; Beagley, Okada, and Wolstenholme 1996
), where access to the germ line is more difficult.
If horizontal transmission is critical in determining the distribution of HEGs, then within taxa there ought to be selection among HEGs for those that are better able to transfer successfully, which in turn would produce adaptation for horizontal transmission. For transfer to be successful (i.e., the transferred gene spreads through the recipient population), the recipient population must contain the HEG recognition site. Therefore, HEGs with highly conserved recognition sequences should transfer successfully more frequently and become more widespread. This line of reasoning suggests that extant HEGs should target unusually well-conserved regions of the genome. The fact that VDE is in a gene instead of free standing in noncoding DNA supports this idea, but our analyses go further, indicating that VDE is in an unusually well-conserved region of an unusually well-conserved gene. This positioning presumably reflects selection among HEGs targeting different regions of the genome. Such selection probably also explains why HEGs are typically found in functionally important parts of genes (Garret et al. 1991
; Dalgaard et al. 1997b
; Edgell, Belfort, and Shub 2000
). Moreover, within the recognition site, VDE targets particularly well-conserved base pairs, and presumably this adaptation arose and is maintained by selection among variant VDEs at the same site, favoring those with increased binding affinity for highly-conserved nonsynonymous sites. These features of VDE biology we take to be adaptations for successful horizontal transmission and evidence that horizontal transmission is a key parameter in the distribution of these selfish genes. There are no adaptations for horizontal transmission, of which we are aware, other than the operon structure of prokaryotic genomes (Lawrence and Roth 1996
).
The mechanism of horizontal transfer is unclear as infectious viruses and plasmids appear to be absent from yeasts. Possibilities include interspecific hybridization (Marinoni et al. 1999
), vectoring by predacious yeasts (Lachance and Pang 1997
), and uptake of naked DNA from the environment (Nevoigt, Fassbender, and Stahl 2000)
. Once inside the cell, fragments of DNA are readily integrated into the yeast genome by homologous recombination. Note that this last step could also select for HEGs in well-conserved regions of the genome. Also unclear is the mechanism of intein loss, as imprecise deletions would disrupt the host gene and be highly deleterious.
More generally, the results also show that horizontal transmission in yeasts is not restricted to mitochondrial DNA but that nuclear DNA is also transferred intact from one species to another. HEGs have no extrachromosomal phase in their life cycle (unlike, say, transposable elements), and therefore normal host-benefiting genes probably also get transferred occasionally. The extent to which these show evidence of past horizontal transmission should then be determined by selection, rather than opportunity. Some degree of horizontal transmission of nuclear genes has been shown for filamentous fungi (Rosewich and Kistler 2000)
. For yeasts we are not yet aware of any compelling examples, but interestingly some ecologically contingent genes occur in clusters, for example, those involved in biotin synthesis (Phalip et al. 1999
), galactose metabolism (Greger and Proudfoot 1998
), and arsenic tolerance (Bobrowicz et al. 1997
). By analogy with prokaryotes, these would be excellent candidates for horizontal transmission.
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Acknowledgements |
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TOPAbstractIntroductionMaterials and MethodsResults and DiscussionConclusionsAcknowledgementsReferences |
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We thank C. Godfray for useful comments on the manuscript. This work was supported by NERC grant GR3/10626.
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Richard Thomas, Reviewing Editor
Abbreviations: VDE, VMA1-derived endonuclease; HEG, homing endonuclease gene; VMA1, vacuolar membrane H+-ATPase. 
Keywords: horizontal (lateral) transfer (transmission)
homing endonuclease
adaptation
yeast
selfish gene
VDE
distribution
Address for correspondence and reprints: Vassiliki Koufopanou, Department of Biology, Imperial College, Silwood Park, Ascot, Berkshire SL5 7PY, UK. v.koufopanou{at}ic.ac.uk
.
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TOPAbstractIntroductionMaterials and MethodsResults and DiscussionConclusionsAcknowledgementsReferences |
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