Genomic Footprints of Multiple Host Lineages in the Mitochondrial and Nuclear Genomes of the Holoparasite Prosopanche americana

Abstract

Horizontal Gene Transfer (HGT) is a hallmark of the evolution of parasitic plants, facilitated by the haustorial connection. While mitochondrial HGT is widespread, the extent of nuclear HGT and the long-term retention of foreign genetic material in holoparasitic lineages remain poorly understood. This study explores the genomic architecture of Prosopanche americana (Hydnoraceae), a non-photosynthetic holoparasite currently specialized on Fabaceae. Through a comparative phylogenomic approach integrating draft mitochondrial genomes (mtDNA) and nuclear transcriptomes of P. americana, we identified a multi-layered landscape of foreign DNA. The mtDNA of P. americana contains 18 foreign regions (>500 bp) primarily derived from Solanales, Malvales, and Fabales. Notably, 13 of these regions are shared with P. panguanensis, indicating they were acquired in their common ancestor before speciation and ecological shift. In the nuclear genome, we identified 303 horizontally acquired transcripts (99 orthogroups) with high confidence. Functional analysis revealed an enrichment of foreign genes involved in metabolic pathways and plastid functions (e.g., photosystems and thylakoids) exclusively derived from the ancestral host order Solanales. Our results demonstrate that the genome of P. americana acts as a “molecular fossil,” preserving evidence of past ecological interactions with diverse host lineages. The disparity in HGT footprints between the current host (Fabaceae) and ancestral hosts suggests a period of high genomic plasticity followed by host specialization, providing new insights into the timing and dynamics of horizontal gene flow in holoparasitic Piperales.