Assembled Plastid and Mitochondrial Genomes, as well as Nuclear Genes, Place the Parasite Family Cynomoriaceae in the Saxifragales

Abstract

Cynomoriaceae, one of the last unplaced families of flowering plants, comprise one or two species or subspecies of root parasites that occur from the Mediterranean to the Gobi Desert. Using Illumina sequencing, we assembled the mitochondrial and plastid genomes as well as some nuclear genes of a Cynomorium specimen from Italy. Selected genes were also obtained by Sanger sequencing from individuals collected in China and Iran, resulting in matrices of 33 mitochondrial, 6 nuclear, and 14 plastid genes and rDNAs enlarged to include a representative angiosperm taxon sampling based on data available in GenBank. We also compiled a new geographic map to discern possible discontinuities in the parasites’ occurrence. Cynomorium has large genomes of 13.70–13.61 (Italy) to 13.95–13.76 pg (China). Its mitochondrial genome consists of up to 49 circular subgenomes and has an overall gene content similar to that of photosynthetic angiosperms, while its plastome retains only 27 of the normally 116 genes. Nuclear, plastid and mitochondrial phylogenies place Cynomoriaceae in Saxifragales, and we found evidence for several horizontal gene transfers from different hosts, as well as intracellular gene transfers.

Horizontal gene transfer is more frequent with increased heterotrophy and contributes to parasite adaptation

“…The hypothesis of increased HGT frequency in endoparasites compared with exoparasites was proposed in studies of HGT in the parasitic plants Rafflesia (20,25) and Cynomorium (22). Our study revealed increased numbers of HGT among related species with increased heterotrophic dependence, a pattern that could be corroborated with rigorous HGT identification in a much larger sampling of parasitic taxa from Orobanchaceae and other parasitic lineages (65) of varying ages and degrees of nutritional dependence.…”

“…A second apparent concentration of horizontally acquired sequences in plant genomes is associated with parasitic plants, where both mitochondrial (14,(17)(18)(19)(20)(21)(22)(23) and nuclear horizontal transfers (24)(25)(26)(27)(28)(29) have been identified. Repeated horizontal acquisitions of mitochondrial atpI by parasitic flowering plants occurred in four extreme parasite lineages where the parasite lives inside the host for much of its lifespan (14).…”

Limited mitogenomic degradation in response to a parasitic lifestyle in Orobanchaceae

“…Plastomes in the holoparasitic species of Orobanchaceae are also heavily degraded2391011, most extensively in Conopholis americana whose plastome is only 46 kb in size with just 21 intact protein-coding genes. Similar levels of degradation were found in the plastomes of other holoparasites in Cynomoriaceae and Hydnoraceae1213. Even greater genomic reduction was reported in Pilostyles (Apodanthaceae), whose plastomes are reduced to just 11–15 kb and may contain only five or six functional genes14.…”

“…In addition to the Orobanchaceae data reported here, large-scale mitogenomic data from a parasitic plant is available from four hemiparasitic mistletoes1617, four holoparasitic members of Rafflesiaceae1537, and a holoparasite in Cynomoriaceae13. As in the Orobanchaceae parasites described here, the Cynomoriaceae and Rafflesiaceae holoparasites contain a nearly complete set of the expected mitochondrial genes, although a substantial fraction were reported to have been acquired horizontally1337.…”

“…In contrast, the draft mitogenome from the holoparasite R. lagascae has a typical size (estimated at > 300 kb) for an angiosperm and contains a nearly complete set of protein-coding genes, including at least seven of nine nad genes15. The draft mitogenome of Cynomorium coccineum is even larger (>1 Mb) and also contains a nearly complete set of mitochondrial genes13. Thus, the effect of a plant parasitic lifestyle on the mitogenome is still unclear, requiring the analysis of mitogenomes from additional parasitic lineages.…”