Diverging repeatomes in holoparasitic Hydnoraceae uncover a playground of genome evolution

Abstract

O_LIThe nuclear genomes of parasitic plants have undergone unique evolutionary trajectories to adapt to the heterotrophic lifestyle. These adaptations often involve large genomic alterations, potentially driven by repetitive DNAs. Despite the recognized role of repetitive DNAs for shaping plant genomes, their contribution to parasitic plant genome evolution remains largely unexplored. This study presents the first analysis of repetitive DNAs in eleven genomes of Hydnoraceae, a holoparasitic plant family. C_LIO_LIThe repetitive DNAs were identified and annotated de novo. Patterns of abundance and presence-absence were aligned with the phylogenetic relationships, geographical distribution, and host shifts, suggesting repetitive DNAs key role in shaping Hydnoraceae genomes. C_LIO_LIThe two Hydnoraceae genera, Hydnora and Prosopanche, exhibit distinct profiles. Eight Hydnora genomes are largely populated by long terminal repeat retrotransposons, while three Prosopanche genomes vary greatly in repetitive DNA composition, including P. bonacinae with massive amplifications of a single DNA transposon and P. panguanensis with over 15% 5S rDNA, compared to <0.1% in some Hydnoraceae. Both extremely low and very high abundance of 5S rDNA challenges our current understanding on chromosomal stabilization and rDNA transcription. C_LIO_LIThese genome dynamics, while inviting for further investigations, suggest rapidly evolving repeat profiles, potentially accelerated by the adaptation to the parasitic lifestyle. C_LI