Evolution by whole genome duplication in Xenopus

Evolution by whole genome duplication in Xenopus

Soutenance de thèse
 26/09/2025
 13:00:00
 Zhen LI, EGCE
 IDEEV - Salle Rosalind Franklin

The thesis project was supervised by Nicolas Pollet, Directeur de Recherche.

KEYWORDS:

Whole genome duplication, Xenopus, Evolution, Subgenome dominance, Transposable element

SUMMARY:

Whole-genome duplications (WGDs) play a crucial role in the evolution of eukaryotic species by providing raw genetic material for adaptation to novel and changing environments. Despite their evolutionary significance, the long-term dynamics of polyploid genome evolution following WGD events remain poorly understood. The Xenopus genus, a known hotspot for WGD in animals, serves as an excellent model for studying polyploid genome evolution.

In this study, I generated a high-quality, subgenome-resolved genome assembly for Xenopus mellotropicalis, a tetraploid species within the Silurana subgenus, using Nanopore long-read sequencing and high-throughput chromosome conformation capture (Hi-C) data. Molecular clock analysis dated its most recent WGD event to less than 5.9 million years ago, much more recent than that of Xenopus laevis, a widely studied paleopolyploid species. By comparing the two subgenomes of X. mellotropicalis to the diploid genome of Xenopus tropicalis, I determined that one subgenome (subgenome B) was phylogenetically closer to X. tropicalis. Further analyses revealed that subgenome A retained significantly more genes and exhibited slightly higher expression levels of protein-coding genes compared to subgenome B, indicating the presence of subgenome dominance, with subgenome A being the dominant one. To explore potential mechanisms of the subgenome dominance, I investigated the distribution patterns of CpG methylation and transposable elements (TE). I found that subgenome A showed significantly lower levels of CpG methylation and TE abundance in gene body regions compared to subgenome B. These findings support the hypothesis that subgenome dominance may be influenced by epigenetic regulation.

Another focus of my Ph.D. thesis was on repetitive elements, particularly TEs, which play key roles in shaping polyploid genome evolution. However, due to their structural diversity and complexity, many TEs remain difficult to annotate, limiting our understanding of their biology and their impact on host genomes. In Xenopus genomes, I observed that two specific types of TEs, retrozymes and Helitrons, were especially poorly annotated.

Retrozymes are recently discovered retroelements that contain hammerhead ribozymes. In animals, they are typically found as tandem repeats, known as non-LTR retrozymes. I developed a bioinformatic pipeline to annotate them and discovered that their phylogenetic distribution closely mirrored that of Penelope-like elements (PLEs). Phylogenetic analysis further indicated that the pLTR region of PLEs was closely related to non-LTR retrozymes, supporting the hypothesis that non-LTR retrozymes might be non-autonomous derivatives of PLEs. Helitrons are widespread eukaryotic DNA transposons employing a rolling-circle transposition mechanism. To improve their annotation, I developed HELIANO, a software for annotating Helitron-like element sequences from whole genomes. HELIANO outperformed existing tools in both speed and accuracy, as demonstrated through benchmarking and application to 404 diverse eukaryotic genomes. In the genome of X. laevis, I found that one of the Helitron family, Heli1Xen1, was recurrently involved in capturing and shuffling X. laevis genes required in early embryonic development. Remarkably, Heli1Xen1 appeared to be transcriptionally active in X. laevis and has contributed to genomic polymorphisms within species. Furthermore, I identified highly similar Heli1Xen1 copies in the genomes of another 13 species from divergent vertebrate lineages. Phylogenetic analysis supported the hypothesis that Heli1Xen1 was recently horizontally transferred among these species.

In conclusion, my thesis provides new insights into the early-stage evolution of polyploid genomes in vertebrates, the molecular basis of subgenome dominance, and the underestimated role of TEs in genome remodelling and innovation.

JURY:

  • Matthias Stöck, PD Dr. rer. nat., Leibniz Institute of Freshwater Ecology and Inland Fisheries, Rapporteur & Examinateur
  • Anna-Sophie Fiston-Lavier, Professor, Université Montpellier, Rapporteur & Examinatrice
  • Olivier Lespinet, Professor, Université Paris-Saclay, Examinateur
  • Clémentine Vitte, Chargée de recherche CNRS, Examinatrice