Periodic Reporting for period 4 - RHEA (Rotifers Highlight the Evolution of Asexuals: the mechanisms of genome evolution in the absence of meiosis)
Periodo di rendicontazione: 2022-04-01 al 2023-09-30
Using this high-quality assembly of A. vaga, the heterozygosity along chromosomes could be compared between different A.vaga lineages. Large-scale homozygous regions were detected in most samples suggesting that recombination between homologous chromosomes can occur. The homologous chromosomes found in A. vaga, with signatures of recombination, suggest the possibility of a modified meiosis as has been observed in several other asexual metazoans. However, the old founding studies of Hsu (1956a, 1956b) established that oogenesis in bdelloids is reduced to two maturation divisions analogous to somatic mitosis. We challenged this view within this ERC with a series of cytogenetic observations that allowed us to propose a model of automictic parthenogenesis in A. vaga where homologous chromosomes interact during a non-reductional meiosis I. Such a model would explain how diploidy and heterozygosity are maintained in A. vaga in the absence of sexual reproduction, while creating genetic variability through homologous recombination. This important finding changes the status of bdelloid rotifers to successful ancient automictic clade.
In addition to its importance in evolutionary biology, A. vaga is the ultimate model organism to study extreme resistance to desiccation and ionizing radiation and the associated DNA repair mechanisms. It has indeed an exceptional ability to reconstruct its genome following massive breakage. By studying the dynamics of DNA repair in somatic and germline cells in A. vaga following radiation, we observed that somatic nuclei repaired immediately the broken DNA while there was a delay in the germline cells with no repair activity occurring until the oocyte started its maturation through its modified meiosis. Moreover, the genome in the progeny of irradiated individuals was fully reconstituted except for some signatures of homologous recombination. DSB repair by inter-homolog recombination is a hallmark event of meiosis and we hypothesize that, in bdelloid rotifers, it would not only participate to the resolution of accidental genomic lesions undergone by the germ line, but it would also contribute to an allelic shuffling in these parthenogenetic species.
Finally, through a proteomic approach we detected a unique, horizontally acquired protein in A. vaga, ligase E, highly expressed upon irradiation. Its ligation function was studied in vitro and through heterologous expression in human cells. The expression of this AvLigase E in human cells significantly increased their radiotolerance, which will be studied further.
In the end, we aim to identify the key players involved in extreme stress resistance in the bdelloid rotifer species A. vaga. This is complementary to the European Space Agency project RISE (Rotifers in Space) in which Karine Van Doninck is the Principal Investigator.