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

Abstract

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.