The genome of Thesium ramosoides (Santalales) reveals evolutionary dynamics associated with parasitism and alpine adaptation.

Abstract

Plant species adapting to complex environments experience contrasting selection pressures that drive the expansion and contraction of different gene families. However, few studies have investigated simultaneous genomic responses to such diverse selective forces. Here, we generate a high-quality genome assembly for the hemiparasitic plant Thesium ramosoides, the first for the largest genus in the Santalales, and explore the genomic basis underlying the evolution of parasitism and alpine adaptation. Unlike many other parasitic plants, the Thesium genome has not undergone additional rounds of whole-genome duplication, making it particularly tractable for studying gene family evolution. Our analyses reveal substantial loss of photosynthesis-related genes and contraction of biotic defense gene families, likely reflecting adaptation to a hemiparasitic lifestyle and reduced pathogen pressure at high altitudes. The absence of key root hair development genes correlates with the degenerate root hair phenotype observed in this species. Furthermore, hallmarks of high-altitude adaptation include the expansion of gene families involved in responses to hypoxia. Notably, expansion of gene families associated with meristem development is consistent with the presence of below-ground crown buds that enable rapid regeneration after mountain fires. Unexpectedly, we detected tandem duplication and diversification of the strigolactone receptor gene D14, which regulates secondary shoot formation, but not of its ancestral paralog KAI2, which mediates seed germination in response to the smoke-derived compound karrikin. This finding suggests divergent signaling mechanisms underlying fire adaptation across different parasitic plant lineages. By integrating time-series transcriptomic data, we propose a post-fire "defense first, repair later, recovery last" model, in which resources are reallocated from immediate defense to rapid repair and ultimately to long-term recovery, to explain the adaptation of T. ramosoides to fire-prone habitats. Our study provides critical insights into the complex and contrasting genomic dynamics that drive adaptation to multiple co-occurring selection pressures.