Mitochondrial phylogenomics of Cuscuta (Convolvulaceae) reveals a potentially functional horizontal gene transfer from the host.

Abstract

Horizontal gene transfers (HGTs) from host or other organisms have been reported in mitochondrial genomes of parasitic plants. Genes transferred in this fashion have usually been found nonfunctional. Several examples of HGT from the mitochondrial genome of parasitic Cuscuta (Convolvulaceae) to its hosts have been reported, but not vice versa. Here we used 31 protein-coding mitochondrial genes to infer the phylogeny of Cuscuta, and compared it with previous nuclear and plastid phylogenetic estimates. We also investigated the presence of HGTs within these lineages. Unlike in plastid genomes, we did not find extensive gene loss in their mitochondrial counterparts. Our results reveal the first example of organellar HGT from host to Cuscuta. Mitochondrial atp1 genes of South African subgenus Pachystigma were inferred to be transferred from Lamiales, with high support. Moreover, the horizontally transferred atp1 gene has functionally replaced the native, vertically transmitted copy, has an intact open reading frame, and is under strong purifying selection, all of which suggests that this xenolog remains functional. The mitochondrial phylogeny of Cuscuta is generally consistent with previous plastid and nuclear phylogenies, except for the misplacement of Pachystigma when atp1 is included. This incongruence may be caused by the HGT mentioned earlier. No example of HGT was found within mitochondrial genes of three other, independently evolved parasitic lineages we sampled: Cassytha/Laurales, Krameria/Zygophyllales, and Lennooideae/Boraginales.