Deeply Altered Genome Architecture in the Endoparasitic Flowering Plant Sapria himalayana Griff. (Rafflesiaceae)

Despite more than 2,000-fold variation in genome size, key features of genome architecture are largely conserved across angiosperms. Parasitic plants have elucidated the many ways in which genomes can be modified, yet we still lack comprehensive genome data for species that represent the most extreme form of parasitism. Here, we present the highly modified genome of the iconic endophytic parasite Sapria himalayana Griff. (Rafflesiaceae), which lacks a typical plant body. First, 44% of the genes conserved in eurosids are lost in Sapria, dwarfing previously reported levels of gene loss in vascular plants. These losses demonstrate remarkable functional convergence with other parasitic plants, suggesting a common genetic roadmap underlying the evolution of plant parasitism. Second, we identified extreme disparity in intron size among retained genes. This includes a category of genes with introns longer than any so far observed in angiosperms, nearing 100 kb in some cases, and a second category of genes with exceptionally short or absent introns. Finally, at least 1.2% of the Sapria genome, including both genic and intergenic content, is inferred to be derived from host-to-parasite horizontal gene transfers (HGTs) and includes genes potentially adaptive for parasitism. Focused phylogenomic reconstruction of HGTs reveals a hidden history of former host-parasite associations involving close relatives of Sapria’s modern hosts in the grapevine family. Our findings offer a unique perspective into how deeply angiosperm genomes can be altered to fit an extreme form of plant parasitism and demonstrate the value of HGTs as DNA fossils to investigate extinct symbioses. •Sapria lost 44% of conserved plant genes•Patterns of gene loss in Sapria are convergent with other parasitic plants•Most genes are highly streamlined, but others contain exceptionally long introns•Extinct host associations are revealed from numerous horizontally transferred genes Cai et al. report the first genome of the endoparasitic plant Sapria, representing the most extreme form of plant parasitism. Alongside the loss of vegetative features, Sapria has lost 44% of conserved plant genes. The genome also demonstrates widespread evidence of horizontal transfer, revealing a dynamic history of former host associations.