A comparative study across the parasitic plants of Cuscuta subgenus Grammica (Convolvulaceae) reveals a possible loss of the plastid genome in its section Subulatae.

MAIN CONCLUSION: Most species in Cuscuta subgenus Grammica retain many photosynthesis-related plastid genes, generally under purifying selection. A group of holoparasitic species in section Subulatae may have lost their plastid genomes entirely. The c. 153 species of plants belonging to Cuscuta subgenus Grammica are all obligate stem parasites. However, some have completely lost the ability to conduct photosynthesis while others retain photosynthetic machinery and genes. The plastid genome that primarily encodes key photosynthesis genes functions as a bellwether for how reliant plants are on primary production. This research assembles and analyses 17 plastomes across Cuscuta subgenus Grammica with the aim of characterizing the state of the plastome in each of its sections. By comparing the structure and content of plastid genomes across the subgenus, as well as by quantifying the selection acting upon each gene, we reconstructed the patterns of plastome change within the phylogenetic context for this group. We found that species in 13 of the 15 sections that comprise Grammica retain the bulk of plastid photosynthesis genes and are thus hemiparasitic. The complete loss of photosynthesis can be traced to two clades: the entire section Subulatae and a complex of three species within section Ceratophorae. We were unable to recover any significant plastome sequences from section Subulatae, suggesting that plastomes in these species are either drastically reduced or lost entirely.

Correction to: Caught in action: fine-scale plastome evolution in the parasitic plants of Cuscuta section Ceratophorae (Convolvulaceae).

Regrettably, an in-text citation wasn't listed in the reference section of the above mentioned publication. The citation reads Schneider et al. (2018) and the correct reference is published here.

Caught in action: fine-scale plastome evolution in the parasitic plants of Cuscuta section Ceratophorae (Convolvulaceae).

KEY MESSAGE: An exhaustive analysis of a group of closely related parasitic plants shows a predominantly gradual reduction in plastid genome composition and provides the most reduced plastomes in the genus Cuscuta. Parasitic plants have a diminished to completely absent reliance on photosynthesis, and are characterized by sweeping morphological, physiological, and genomic changes. The plastid genome (plastome) is highly conserved in autotrophic plants but is often reduced in parasites, and provides a useful system for documenting the genomic effects of a loss of photosynthesis. Previous studies have shown a substantial degree of heterogeneity in plastome length and composition across the species of the genus Cuscuta. Specifically, species in Cuscuta sect. Ceratophorae were suspected to exhibit even more dynamic plastome evolution than the rest of the genus. This complex of eight closely related species was exhaustively sampled here, and one accession per species was sequenced via a high-throughput approach. Complete plastid genomes were assembled and annotated for each of these species and were found to be 61-87 kbp in length, representing a 45-60% reduction relative to autotrophic Convolvulaceae. The most reduced plastomes on this spectrum have lost the bulk of their photosynthetic genes and are the first fully holoparasitic plastomes described for Cuscuta. The fine-scale nature of the system introduced here allowed us to phylogenetically triangulate the locations of gene loss and pseudogenization events precisely, and to construct a step-by-step model of plastome evolution in these plants. This model reveals an intense burst of gene loss along the branch leading to the most reduced plastomes, and a few idiosyncratic changes elsewhere, allowing us to conclude that the tempo of plastid evolution in sect. Ceratophorae is a blend of gradual and punctuated mode.

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

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.

Convergent Plastome Evolution and Gene Loss in Holoparasitic Lennoaceae.

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.