A structural solution to functional HGT: Gene chimerism bypasses mitochondrial expression barriers in parasitic plants

ABSTRACT Horizontal Gene Transfer (HGT) in plant mitochondria is frequent, yet acquired genes are rarely functional due to expression barriers. The holoparasitic plant Lophophytum mirabile (Balanophoraceae) is an exceptional case, having functionally replaced numerous native mitochondrial genes with host-derived xenologs. This system provides a unique opportunity to investigate the mechanisms of functional HGT assimilation. Here, we assembled mitochondrial genomes of the sister species L. pyramidale and their mimosoid hosts and analyzed expression data from both holoparasites. We show that this extensive functional integration occurred without the co-transfer of nuclear regulatory factors; Lophophytum relies entirely on its pre-existing, native machinery. Our results demonstrate that the primary mechanism enabling Lophophytum to overcome the transcription barrier is structural: most functional xenologs are chimeric and retain native 5′ regions that likely place foreign coding sequences under the control of a recognizable native promoter. This structural solution is complemented by post-transcriptional flexibility, as the RNA editing machinery efficiently processes novel host-specific sites. However, functional replacement appears biased towards genes with inherently low editing requirements and no introns, highlighting a strong selective filter. Taken together, our results show that functional integration is driven by a combination of structural integration and the flexibility of the native regulatory system.