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Foundational studies of chloroplast genome (plastome) evolution in parasitic plants have focused on broad trends across large clades, particularly among the Orobanchaceae, a species-rich and ecologically diverse family of root parasites. However, the extent to which such patterns and processes of plastome evolution, such as stepwise gene loss following the complete loss of photosynthesis (shift to holoparasitism), are detectable at shallow evolutionary time scale is largely unknown. We used genome skimming to assemble eight chloroplast genomes representing complete taxonomic sampling of Aphyllon sect. Aphyllon, a small clade within the Orobanchaceae that evolved approximately 6 Ma, long after the origin of holoparasitism. We show substantial plastome reduction occurred in the stem lineage, but subsequent change in plastome size, gene content, and structure has been relatively minimal, albeit detectable. This lends additional fine-grained support to existing models of stepwise plastome reduction in holoparasitic plants. Additionally, we report phylogenetic evidence based on an rbcL gene tree and assembled 60+ kb fragments of the Aphyllon epigalium mitochondrial genome indicating host-to-parasite horizontal gene transfers (hpHGT) of several genes originating from the plastome of an ancient Galium host into the mitochondrial genome of a recent common ancestor of A. epigalium. Ecologically, this evidence of hpHGT suggests that the host–parasite associations between Galium and A. epigalium have been stable at least since its subspecies diverged hundreds of thousands of years ago.

Main conclusionMost 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.

The distribution of Cuscuta subg. Grammica sect. Cleistogrammica (Cuscuta pentagona clade) is centered in North America (C. campestris, C. glabrior, C. harperi, C. pentagona, C. obtusiflora, C. plattensis, C. polygonorum, C. runyonii); however, long-distance dispersal was documented to Hawaii (C. sandwichiana), South America (C. gymnocarpa, C. stenolepis, and in part C. obtusiflora), Africa (C. bifurcata, C. schlechteri), Eurasia, and Australia (C. australis). Hybrid speciation has already been documented for some members of sect. Cleistogrammica (C. sandwichiana, C. bifurcata) but previous studies strongly suggested that the extent of reticulate evolution is underestimated in Cuscuta generally, and in this section in particular. Sequence data from the nuclear internal transcribed spacer (ITS) and the plastid trnL-F region were used to reconstruct the phylogeny and gain a better understanding of the evolutionary history within the clade. Additionally, a morphometric analysis was conducted to test the phenetic distinctiveness of a select number of species with taxonomic problems: C. campestris, C. glabrior, C. gymnocarpa, and C. pentagona. Discordances between phylogenies derived from plastid and nuclear data showed that C. campestris is a hybrid, likely involving the C. runyonii/glabrior lineage as a maternal progenitor and an undiscovered species as a paternal progenitor. This latter species, an extinct or unsampled lineage, was itself inferred to be a hybrid between C. pentagona / harperi and C. australis / obtusiflora / polygonorum lineages. Both the evolutionary and morphometric results clearly showed that C. campestris is a distinct species and the negative consequences of its amalgamation with C. pentagona during the last decades are discussed. Cuscuta gymnocarpa, an enigmatic species described from specimens collected by Darwin from the Galapagos, was inferred as conspecific with C. campestrisand proposed as a variety of the latter. Because C. gymnocarpa is only a form of C. campestris, the possible means of dispersal of the latter species to the Galapagos are discussed. Cuscuta modesta, a new species discovered while studying the systematics of the clade, is described and illustrated.

The genus Cuscuta (Convolvulaceae, the morning glory family) is one of the most intensely studied lineages of parasitic plants. Whole plastome sequencing of four Cuscuta species has demonstrated changes to both plastid gene content and structure. The presence of photosynthetic genes under purifying selection indicates that Cuscuta is cryptically photosynthetic. However, the tempo and mode of plastid genome evolution across the diversity of this group (~200 species) remain largely unknown. A comparative investigation of plastid genome content, grounded within a phylogenetic framework, was conducted using a slot-blot Southern hybridization approach. Cuscuta was extensively sampled (~56% of species), including groups previously suggested to possess more altered plastomes compared with other members of this genus. A total of 56 probes derived from all categories of protein-coding genes, typically found within the plastomes of flowering plants, were used. The results indicate that two clades within subgenus Grammica (clades ‘O’ and ‘K’) exhibit substantially more plastid gene loss relative to other members of Cuscuta. All surveyed members of the ‘O’ clade show extensive losses of plastid genes from every category of genes typically found in the plastome, including otherwise highly conserved small and large ribosomal subunits. The extent of plastid gene losses within this clade is similar in magnitude to that observed previously in some non-asterid holoparasites, in which the very presence of a plastome has been questioned. The ‘K’ clade also exhibits considerable loss of plastid genes. Unlike in the ‘O’ clade, in which all species seem to be affected, the losses in clade ‘K’ progress phylogenetically, following a pattern consistent with the Evolutionary Transition Series hypothesis. This clade presents an ideal opportunity to study the reduction of the plastome of parasites ‘in action’. The widespread plastid gene loss in these two clades is hypothesized to be a consequence of the complete loss of photosynthesis. Additionally, taxa that would be the best candidates for entire plastome sequencing are identified in order to investigate further the loss of photosynthesis and reduction of the plastome within Cuscuta.

Key messageAn 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.

The Cuscuta umbellata complex is one of the 15 major clades recently circumscribed in C. subg. Grammica. Most of its members occur in North America and the Caribbean (C. desmouliniana, C. lacerata, C. leptantha, C. liliputana, C. odontolepis, C. polyanthemos, C. tuberculata, C. umbellata), but three species (C. acuta, C. membranacea, C. umbellata) grow in South America, and one (C. hyalina) is found as a native species in India, Pakistan and Eastern to South Africa. Basic morphology, scanning electron microscopy and sequence data from the nuclear internal transcribed spacer (ITS) and the plastid trnL-F region were used to reconstruct the phylogeny, gain a better understanding of the evolutionary history, and determine species boundaries. Our results show that in its currently accepted delimitation C. umbellata is polyphyletic. Discordances between phylogenies derived from plastid and nuclear data strongly suggest that at least four independent hybridization events have occurred in the evolution of this species group, rendering relationships among its members more complex than previously thought. One of these reticulation events involves C. umbellata var. reflexa, a taxon that has been considered synonymous to C. umbellata var. umbellata in the last decades. This hybrid is morphologically intermediate but distinct from its putative parents, C. odontolepis or C. acuta on the maternal side, and C. umbellata (var. umbellata) on the paternal side, which supports its treatment as a new species, C. legitima. Cuscuta umbellata is further redefined to exclude C. umbellata var. dubia, which is merged into C. desmouliniana. A new classification is provided, together with an identification key, descriptions, illustrations, and geographical distributions for the twelve species of the clade.

Ericaceae (the heather family) is a large and diverse group of plants that forms elaborate symbiotic relationships with mycorrhizal fungi, and includes several nonphotosynthetic lineages. Using an extensive sample of fully mycoheterotrophic (MH) species, we explored interand intraspecific variation as well as selective constraints acting on the plastomes of these unusual plants. The plastomes of seven MH genera were analysed in a phylogenetic context with two geographically disparate individuals sequenced for Allotropa, Monotropa, and Pityopus. The plastomes of nonphotosynthetic Ericaceae are highly reduced in size (c. 33–41 kbp) and content, having lost all photosynthesis-related genes, and are reduced to encoding housekeeping genes as well as a protease subunit (clpP)-like and acetyl-CoA carboxylase subunit D (accD)-like open reading frames. Despite an increase in the rate of their nucleotide substitutions, the remaining protein-coding genes are typically under purifying selection in full MHs. We also identified ribosomal proteins under relaxed or neutral selection. These plastomes also exhibit striking structural rearrangements. Intraspecific variation within MH Ericaceae ranges from a few differences (Allotropa) to extensive population divergences (Monotropa, Hypopitys), which indicates that cryptic speciation may be occurring in several lineages. The pattern of gene loss within fully MH Ericaceae plastomes suggests an advanced state of degradation.

Premise of research. Understanding how various organisms respond to previous changes in climate could provide insight into how they may respond or adapt to the current changes. Conopholis americana has a broad distribution across eastern North America, covering both previously glaciated and unglaciated regions. In this study, we investigated the postglacial history and phylogeographic structure of this parasitic plant species to characterize its genetic variation and structure and to identify the number and locations of refugia. Methodology. Molecular data from 10 microsatellite markers and DNA sequences from the plastid gene/introns (clpP) were obtained for 281 individuals sampled from 75 populations spanning the current range of the species in eastern North America and analyzed using a variety of phylogeographic methods. Distribution modeling was carried out to determine regions with relatively suitable climate niches for populations at the Last Glacial Maximum (LGM) and present. Pivotal results. We inferred the persistence of a minimum of two glacial refugia for C. americana at the LGM, one in north-central Florida and southern Alabama and another in the Appalachian Mountains near the southern tip of the Blue Ridge Mountains. High levels of genetic diversity were observed across the southern Appalachian Mountains, the region where populations from two refugia come together following recolonization northward. Conclusions. The genetic and geographic patterns revealed by our results provide further evidence of the dynamic nature and phylogeographical history of eastern North American taxa. The discovery of a distinct southern lineage is in agreement with the location of a previously proposed southern glacial refugium spanning across Florida, southern Georgia and Alabama, and the Lower Mississippi Valley. The second lineage is dominant across the present northern range of the species and is hypothesized to have been located in the southern extent of the Blue Ridge mountain range of the Appalachian Mountains at the LGM.

PREMISE OF THE STUDY: Dispersal of parasitic Cuscuta species (dodders) worldwide has been assumed to be largely anthropomorphic because their seeds do not match any previously known dispersal syndrome and no natural dispersal vectors have been reliably documented. However, the genus has a subcosmopolitan distribution and recent phylogeographic results have indicated that at least 18 historical cases of long-distance dispersal (LDD) have occurred during its evolution. The objective of this study is to report the first LDD biological vector for Cuscuta seeds. METHODS: Twelve northern pintails (Anas acuta) were collected from Suisun Marsh, California and the contents of their lowest part of the large intestine (rectum) were extracted and analyzed. Seed identification was done both morphologically and using a molecular approach. Extracted seeds were tested for germination and compared to seeds not subjected to gut passage to determine the extent of structural changes caused to the seed coat by passing through the digestive tract. KEY RESULTS: Four hundred and twenty dodder seeds were found in the rectum of four northern pintails. From these, 411 seeds were identified as Cuscuta campestris and nine as most likely C.pacifica. The germination rate of campestris seeds after gut passage was 55%. Structural changes caused by the gut passage in both species were similar to those caused by an acid scarification. CONCLUSIONS: Endozoochory by waterbirds may explain the historical LDD cases in the evolution of Cuscuta. This also suggests that current border quarantine measures may be insufficient to stopping spreading of dodder pests along migratory flyways.

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.