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Parasitic plants have evolved to have reduced or completely lost ability to conduct photosynthesis and are usually characterized by sweeping morphological, physiological and genomic changes. The plastid genome (or plastome) is highly conserved in autotrophic plants and houses many key photosynthesis genes. This molecule is thus a useful system for documenting the genomic effects of a loss of autotrophy. Cuscuta (dodders) represents one of 12 independent transitions to a parasitic lifestyle in angiosperms. This near-cosmopolitan genus contains > 200 obligate parasitic species circumscribed in four subgenera: Grammica, Pachystigma, Cuscuta and Monogynella. With respect to photosynthesis, Cuscuta is a heterogeneous group, containing both hemi- and holoparasitic members that are, respectively, partially or entirely reliant on parasitism to meet their carbon budget. Plastomes in this genus have been reported to show a substantial degree of diversification in terms of length and gene composition. Considered together with well-understood phylogenetic relationships, this genus presents an opportunity for fine-scale comparisons among closely related species of heterotrophic plants. This research documents changes in sequence composition and structure that occurred as these plants evolved along the trophic spectrum by using multiple whole-plastome assemblies from each of the four subgenera. By ‘triangulating’ the positions of genomic changes, we construct a step-by-s’tep model of plastome evolution across the phylogenetic backbone of Cuscuta and highlight the remarkable retention of most photosynthetic genes in these parasitic plants.

The Lennoaceae, a small monophyletic plant family of root parasites endemic to the Americas, are one of the last remaining independently evolved lineages of parasitic angiosperms lacking a published plastome. In this study, we present the assembled and annotated plastomes of two species spanning the crown node of Lennoaceae, Lennoa madreporoides and Pholisma arenarium, as well as their close autotrophic relative from the sister family Ehretiaceae, Tiquilia plicata. We find that the plastomes of L. madreporoides and P. arenarium are similar in size and gene content, and substantially reduced compared to T. plicata, consistent with trends seen in other holoparasitic lineages. In particular, most plastid genes involved in photosynthesis function have been lost, whereas housekeeping genes (ribosomal protein-coding genes, rRNAs, and tRNAs) are retained. One notable exception is the persistence of a rbcL open reading frame in P. arenarium but not L. madreporoides suggesting a nonphotosynthetic function for this gene. Of the retained coding genes, dN/dS ratios indicate that some remain under purifying selection, whereas others show relaxed selection. Overall, this study supports the mounting evidence for convergent plastome evolution in flowering plants following the shift to heterotrophy.

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 non-functional. 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 above. 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.

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