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

Plant species adapting to complex environments will 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 selection. 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 experienced additional rounds of whole genome duplication, making it particularly tractable for studying gene family evolution. Our analyses reveal the significant loss of photosynthesis-related genes and the contraction of biotic defense gene families, likely reflecting adaptation to a hemiparasitic lifestyle and to 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, expansions of gene families associated with meristem development are consistent with the presence of below-ground crown buds that can enable rapid regeneration after mountain fires. Unexpectedly, we detected tandem duplication and diversification in the strigolactone receptor gene D14 that regulates secondary shoot formation, but not in its ancestral paralog KAI2 that mediates seed germination stimulated by the smoke-derived compound karrikin. This indicates divergent mechanisms of signaling for fire adaptation across different parasitic plant lineages. By analyzing time-series transcriptomic data, we propose a post-fire "defense-first, repair-later, recovery-last" model, where resources are reallocated from immediate defense to rapid repair and finally 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 driving adaptation to multiple co-occurring selection pressures.