Comparing complete organelle genomes of holoparasitic Christisonia kwangtungensis (Orabanchaceae) with its close relatives: how different are they?

Background Orobanchaceae is the only flowering plant family with species from free-living nonparasite, hemi-parasite to holoparasite, making it an ideal system for studying the evolution of parasitism. However, both plastid and mitochondrial genome have been sequenced in only few parasitic species in Orobanchaceae. Therefore, further comparative study is wanted to investigate the impact of holoparasitism on organelle genomes evolution between close relatives. Here, we sequenced organelle genomes and transcriptome of holoparasitic Christisonia kwangtungensis and compared it with its closely related groups to analyze similarities and differences in adaption strategies to the holoparasitic lifestyle. Results The plastid genome of C. kwangtungensis has undergone extensive pseudogenization and gene loss, but its reduction pattern is different from that of Aeginetia indica, the close relative of C. kwangtungensis. Similarly, the gene expression detected in the photosynthetic pathway of these two genera is different. In Orobanchaceae, holoparasites in Buchnereae have more plastid gene loss than Rhinantheae, which reflects their longer history of holoparasitism. Distinct from severe degradation of the plastome, protein-coding genes in the mitochondrial genome of C. kwangtungensis are relatively conserved. Interestingly, besides intracellularly transferred genes which are still retained in its plastid genome, we also found several horizontally transferred genes of plastid origin from diverse donors other than their current hosts in the mitochondrial genome, which probably indicate historical hosts. Conclusion Even though C. kwangtungensis and A. indica are closely related and share severe degradation of plastome, they adapt organelle genomes to the parasitic lifestyle in different ways. The difference between their gene loss and gene expression shows they ultimately lost photosynthetic genes but through different pathways. Our study exemplifies how parasites part company after achieving holoparasitism.

Automated summary

This study investigates the adaptation strategies and evolution of organelle genomes in the holoparasitic plant Christisonia kwangtungensis. By comparing the plastid genome and transcriptome of C. kwangtungensis with its closely related species, the study reveals differences in gene loss and gene expression, indicating different pathways to the loss of photosynthetic genes in these species. The study also discovers horizontally transferred genes of plastid origin in the mitochondrial genome, which may indicate historical hosts. This research provides insights into the evolution of parasitism in Orobanchaceae.