Circle-Mediated HGT shapes the multichromosomal mitochondrial genome of the endoparasite Mitrastemon yamamotoi

Abstract

Horizontal gene transfer (HGT), a well-established driver of genome evolution in prokaryotes, was historically considered rare in plants. However, accumulating genomic evidence supports its occurrence in angiosperms, impacting both nuclear and mitochondrial genomes, particularly in parasitic species that establish vascular connections with their hosts. Despite the increasing recognition of HGT in a few clades of parasitic plants (e.g., Balanophoraceae, Rafflesiaceae, and Cynomoriaceae), the underlying mechanisms and evolutionary consequences of these transfers are still not fully understood. Mitrastemon yamamotoi, a holoparasitic endoparasite in the order Ericales, invades the roots of host trees in the Fagaceae family, creating favorable conditions for HGT. In this study, we assembled for the first time the mtDNA of Mitrastemon, revealing a multipartite structure consisting of 51 circular-mapping chromosomes. Phylogenetic and comparative genomic analyses uncovered extensive HGT from Fagaceae hosts, affecting both coding and non-coding regions. Notably, more than 60% of the Mitrastemon mtDNA is of foreign origin, and seven chromosomes are entirely foreign, with structural signatures in the donor mtDNA consistent with the recently proposed circle-mediated HGT model. Additionally, we detected six protein-coding genes of foreign origin and one chimeric gene. Remarkably, a foreign atp1 gene has replaced the missing native copy and represents a rare event of functional HGT in plant mitochondria. These results position Mitrastemon as a valuable model for studying mtDNA evolution and deepening our understanding of the HGT process. Our findings expand the range of lineages in which circle-mediated HGT has been documented, suggesting it is a more widespread and fundamental mode of mitochondrial HGT in plants. Significant StatementParasitic plants form intimate connections with their hosts, but how these interactions influence genome evolution remains poorly understood. Our study shows that Mitrastemon yamamotoi has acquired over 60% of its mitochondrial DNA from its host through horizontal gene transfer, including entire foreign chromosomes. These findings provide strong support for a recently proposed mechanism, circle-mediated HGT, and suggest that this process may be a more widespread driver of mitochondrial genome evolution in flowering plants.