A Phylogenomic Inventory of Meiotic GenesEvidence for Sex in Giardia and an Early Eukaryotic Origin of Meiosis

Abstract

homologs of well-known meiotic genes. The direct implications are that Giardia is, or was recently, capable of sexual reproduction and, thus, does not represent an ancient eukaryotic lineage that diverged before meiosis arose. Instead, the origin of meiosis predates the diver- plemental Data), all indicate that these genes are comOne possible interpretation of these observations is that plete, bona fide homologs of meiotic genes. diplomonads such as Giardia represent an "intermedi- Table 2 shows that the Giardia genome encodes hoate" (i.e., premeiotic) stage in eukaryotic evolution [35]. mologs of key genes required for meiosis. Homologs of We have evaluated this compelling hypothesis and can five meiosis-specific genes are present in Giardia: now reject it.Dmc1, Spo11, Mnd1, Hop1, and Hop2. Proteins encoded by these genes are not known to function outside of meiosis among AFP species. Of meiosis-specific Genes and Their Functions at the Core of Meiosis We used a phylogenomic approach [36] to identify and genes surveyed, Giardia does not appear to encode mutS homologs Msh4 and Msh5. Whether this is due to validate a core group of meiotic genes as indicators for the presence or absence of meiosis. Our selection of the loss of these genes or later evolutionary origins is unclear; the sparse distribution of Msh4/5 genes indimeiotic genes was based on previous studies in eukaryotic model systems-mostly AFP. We chose genes havcates some losses. Five meiosis-specific genes in Giardia in conjunction with other known meiotic genes proing major meiotic functions in AFP and conservation in sequence and function [2]. Gene products with similar vide strong evolutionary evidence for meiosis in the putatively asexual diplomonads. The presence of meiimportant roles in meiosis among known models have the greatest potential as meiotic indicators in diverse otic genes in Giardia and in the other protists surveyed (see below) extends the diversity of eukaryotes known to eukaryotes. Readily detectable protein sequence conservation among these genes ‫%51ف(‬ amino acid idencontain these genes. The collective presence of multiple genes that work together in meiotic recombination tity) was needed to identify potential homologs in evolutionarily distant species. We included some "meiosis strongly suggests that Giardia has or very recently had the capacity to undergo meiosis and, thus, sexual reprospecific" genes-null mutations in all of these genes (in S. cerevisiae, at least) are defective only in meiosis, and duction. The possibility that Giardia undergoes meiosis warrants further investigation; experiments will be remost genes do not function outside of meiosis, with some possible exceptions in mammals (Hop2 processes, present either from the loss of meiosis (despecific gene present in Giardia requires independent loss or gain of meiotic functions in all other eukaryotes rived asexuality) or prior to its invention (ancestral asexuality). As the numbers of meiotic genes mount, these known. The strong inference of meiosis being present...

Interactions between Mei4, Rec114, and other proteins required for meiotic DNA double-strand break formation in Saccharomyces cerevisiae

“…Perhaps because of this divergence, we have been unable to identify clear homologs of these proteins in most organisms other than those related to S. cerevisiae. Similar divergence is seen for the other meiosis-regulated DSB proteins Jiao et al 2002;Henderson et al 2006;Keeney 2007), but this feature is not unique to the DSB proteins, as it has been observed that meiotic recombination proteins in general tend to be among the most rapidly diverging groups of proteins in the cell (see Ramesh et al 2005;Richard et al 2005). …”

Transcription of meiotic-like-pathway genes in Giardia intestinalis

“…Nuclei fusion has been physically observed through transmission electron micrographs (Poxleitner et al 2008), and the presence of meiotic recombinant genes has been detected in phylogenomic studies (Ramesh et al 2005). In this report we have shown that three of the eukaryotic meiotic-like recombination core genes, dmc1, spo11 and hop1 are present not only in the Giardia genome but are also being differentially transcribed during its life cycle suggesting a critical function in Giardia's differentiation process.…”

“…Although direct observation of sexual reproduction has not been described for Giardia, it has been proposed that this parasite might undergo rare meiotic-like events in the wild (Birky 2005, Cooper et al 2007 or might undergo a parasexual phenomenon, a process where two cell nuclei merge without any sexual process, which unlike meiosis, is not accompanied by genome reduction and subsequent fusion of gametes from the same parent (Poxleitner et al 2008). Parasexuality is supported by the observations of nuclei fusion in the Giardia cyst (karyogamy) together with a phylogenomic analysis of the Giardia sequenced genome that revealed genes associated with homologous recombination (Ramesh et al 2005). Homologues recombination is one of the most important consequences of meiosis and has been rated by some authors as the essence of sex (Villenueve & Hillers 2001).…”

“…The gene labelled as dmc1B has the same sequence as another gene reported in the GenBank as Rad51, a gene whose product is involved in DNA repair during mitosis and meiosis. Phylogenomic studies (Ramesh et al 2005) suggested that dmc1B belongs to the dmc1 family and not to that of rad51. This interpretation points to a probable divergence between the two families later during the evolutionary process and, therefore suggests that Giardia does not possess a homologue of Rad51.…”

The Entamoeba histolytica genome: something old, something new, something borrowed and sex too?

“…A fascinating recent discovery from mining the genome project is that E. histolytica possesses an essentially complete complement of the genes known to be required for meiosis [14]. E. histolytica trophozoites reproduce by binary fission and, although the existence of genetic recombination has been proposed on at least one occasion [15], there have been no confirmed sightings of amebic sex.…”