Repeat competition and ecological shifts drive the evolution of the mobilome in Rhynchospora Vahl. (Cyperaceae), the holocentric beaksedges

Background and aims: Genomic changes triggered by polyploidy, chromosomal rearrangements, and/ or environmental stress are among factors that affect the activity of mobile elements, particularly Long Terminal Repeats Retrotransposons (LTR-RTs) and DNA transposons. Because these elements can proliferate and move throughout host genomes, altering the genetic, epigenetic and nucleotypic landscape, they have been recognized as a relevant evolutionary force. Beaksedges (Rhynchospora) stand out for their wide cosmopolitan distribution, high diversity (~400 spp.) and holocentric chromosomes related to high karyotypic diversity and a centromere-specific satDNA Tyba. This makes the genus an interesting model to investigate the interactions between repetitive elements, phylogenetic relationships, and ecological variables.

Methods: Here, we used comparative phylogenetic methods to investigate the forces driving the evolution of the entire set of mobile elements (mobilome) in the holocentric genus Rhynchospora. We statistically tested the impact of phylogenetic relationships, abundance of holocentromeric satDNA Tyba, diversity of repeatome composition, ecological variables, and chromosome number in mobile element diversification.

Key results: Tyba abundance was found to be inversely correlated with LTR-RT content. Decrease of LTR abundance and diversity was also related to increase in chromosome number (likely due to fission events), and colonization of dry environments in the northern hemisphere. In contrast, we found constant LTR insertions throughout time in species with lower chromosome numbers in rainier environments in South America. A multivariate model showed that different traits drive LTR abundance, especially repeat diversity and Tyba abundance. Other mobile elements, such as non-LTR RTs and DNA transposons had insufficient abundance to be included in our models.

Conclusions: Our findings suggest that LTR evolution is strongly impacted by the holocentric characteristics of Rhynchospora chromosomes, correlating with species diversification and biome shifts, and supporting a holokinetic drive model of evolution and a competitive scenario with Tyba. Altogether, our results present evidence of multi-trait influence on LTR-RT dynamics and provide a broader understanding of TE evolution in a macroevolutionary context.