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

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. 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. 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. The online version contains supplementary material available at 10.1186/s12870-022-03814-3.

列当科是唯一包含从自由生活的非寄生植物、半寄生植物到全寄生植物的开花植物科，这使其成为研究寄生现象进化的理想体系。然而，列当科中只有少数寄生植物的质体和线粒体基因组已被测序。因此，需要进一步的比较研究来探究全寄生现象对近缘物种细胞器基因组进化的影响。在此，我们对全寄生植物广东假野菰的细胞器基因组和转录组进行了测序，并将其与近缘类群进行比较，以分析对全寄生生活方式适应策略的异同。 广东假野菰的质体基因组经历了广泛的假基因化和基因丢失，但其减少模式与广东假野菰的近缘植物野菰不同。同样，在这两个属的光合途径中检测到的基因表达也不同。在列当科中，来江藤族的全寄生植物比鼻花族的全寄生植物质体基因丢失更多，这反映了它们更长的全寄生历史。与质体基因组的严重退化不同，广东假野菰线粒体基因组中的蛋白质编码基因相对保守。有趣的是，除了其质体基因组中仍然保留的细胞内转移基因外，我们还在线粒体基因组中发现了几个来自不同供体（而非其当前宿主）的质体来源的水平转移基因，这可能暗示了其历史宿主。 尽管广东假野菰和野菰亲缘关系密切且质体基因组都严重退化，但它们以不同的方式使细胞器基因组适应寄生生活方式。它们基因丢失和基因表达的差异表明，它们最终都丢失了光合基因，但途径不同。我们的研究例证了全寄生植物在实现全寄生后是如何分化的。 网络版包含补充材料，可在10.1186/s12870 - 022 - 03814 - 3获取。