Invited Review Beyond parasitic convergence: unravelling the evolution of the organellar genomes in holoparasites.

BACKGROUND: The molecular evolution of organellar genomes in angiosperms has been studied extensively, with some lineages, such as parasitic ones, displaying unique characteristics. Parasitism has emerged 12 times independently in angiosperm evolution. Holoparasitism is the most severe form of parasitism, and is found in ~10 % of parasitic angiosperms. Although a few holoparasitic species have been examined at the molecular level, most reports involve plastomes instead of mitogenomes. Parasitic plants establish vascular connections with their hosts through haustoria to obtain water and nutrients, which facilitates the exchange of genetic information, making them more susceptible to horizontal gene transfer (HGT). HGT is more prevalent in the mitochondria than in the chloroplast or nuclear compartments. SCOPE: This review summarizes current knowledge on the plastid and mitochondrial genomes of holoparasitic angiosperms, compares the genomic features across the different lineages, and discusses their convergent evolutionary trajectories and distinctive features. We focused on Balanophoraceae (Santalales), which exhibits extraordinary traits in both their organelles. CONCLUSIONS: Apart from morphological similarities, plastid genomes of holoparasitic plants also display other convergent features, such as rampant gene loss, biased nucleotide composition and accelerated evolutionary rates. In addition, the plastomes of Balanophoraceae have extremely low GC and gene content, and two unexpected changes in the genetic code. Limited data on the mitochondrial genomes of holoparasitic plants preclude thorough comparisons. Nonetheless, no obvious genomic features distinguish them from the mitochondria of free-living angiosperms, except for a higher incidence of HGT. HGT appears to be predominant in holoparasitic angiosperms with a long-lasting endophytic stage. Among the Balanophoraceae, mitochondrial genomes exhibit disparate evolutionary paths with notable levels of heteroplasmy in Rhopalocnemis and unprecedented levels of HGT in Lophophytum. Despite their differences, these Balanophoraceae share a multichromosomal mitogenome, a feature also found in a few free-living angiosperms.

Native and foreign mitochondrial and nuclear encoded proteins conform the OXPHOS complexes of a holoparasitic plant.

The intimate contact between the holoparasitic plant Lophophytum mirabile (Balanophoraceae) and its host plant (Fabaceae) facilitates the exchange of genetic information, increasing the frequency of horizontal gene transfer (HGT). Lophophytum stands out because it acquired a large number of mitochondrial genes (greater than 20) from its legume host that replaced the majority of the native homologs. These foreign genes code for proteins that form multisubunit enzyme complexes, such as those in the oxidative phosphorylation system (OXPHOS) and cytochrome c maturation (ccm) system, together with dozens of nuclear-encoded subunits. However, the existence and the origin of the nuclear subunits that form the major part of the OXPHOS and ccm system in Lophophytum remain unknown. It was proposed that nuclear-encoding genes whose products interact with foreign mitochondrial proteins are also foreign, minimizing the incompatibilities that could arise in the assembly and functioning of these multiprotein complexes. We identified a nearly complete set of OXPHOS and ccm system subunits evolving under selective constraints in the transcriptome of Lophophytum, indicating that OXPHOS is functional and resembles that of free-living angiosperms. Maximum Likelihood phylogenetic analyses revealed a single case of HGT in the nuclear genes, which results in mosaic OXPHOS and ccm system in Lophophytum. These observations raise new questions about the evolution and physiology of this parasitic plant. A putative case of cooperation between two foreign (one mitochondrial and one nuclear) genes is presented.