Structural Plastome Evolution in Holoparasitic Hydnoraceae with Special Focus on Inverted and Direct Repeats

Abstract

Plastome condensation during adaptation to a heterotrophic lifestyle is generally well understood and lineage-independent models have been derived. However, understanding the evolutionary trajectories of comparatively old heterotrophic lineages, that are on the cusp of a minimal plastomes, is essential to complement and expand current knowledge. We study Hydnoraceae, one of the oldest and least investigated parasitic angiosperm lineages. Plastome comparative genomics, using seven out of eight known species of the genus Hydnora and three species of Prosopanche, reveal a high degree of structural similarity and shared gene content; contrasted by striking dissimilarities with respect to repeat content (inverted and direct repeats). We identified varying IR content and positions, likely resulting from multiple, independent evolutionary events and a direct repeat gain in Prosopanche. Considering different evolutionary trajectories and based on a fully resolved and supported species-level phylogenetic hypothesis, we describe three possible, distinct models to explain the Hydnoraceae plastome states. For comparative purposes we also report the first plastid genomes for the closely related autotrophic genera Lactoris (Lactoridaceae) and Thottea (Aristolochiaceae).

A taxonomic revision of the genusHydnora(Hydnoraceae)

“…The copyright holder for this this version posted October 17, 2022. ; https://doi.org/10.1101/2022.10.13.512068 doi: bioRxiv preprint these taxonomic decisions, although they already comply with existing phylogenetic trees for the genus (Bolin et al, 2009b;Jost et al, 2022).…”

“…According to the most recent phylogeny for the genus (Jost et al, 2022), a shift has occurred from the parasitism of CAM-photosynthesising Euphorbia (Malpighiales) to C3-photosynthesising Fabaceae (Fabales). Whether there is any significance in the difference in photosynthetic metabolism between these two groups is unknown.…”

“…Whether there is any significance in the difference in photosynthetic metabolism between these two groups is unknown. The identity of the ancestral host family remains uncertain, although the phylogeny suggests that the ancestral Hydnora parasitised Fabaceae (Bolin, 2009b; Jost et al, 2022). Therefore, a transition must presumably also have been made from Fabaceae to Commiphora (Burseraceae) in H. sinandevu .…”

“…We follow the infrageneric sections of Decaisne (1873), added to by Harms (1935), but we make modifications to accommodate new taxa, in line with the existing phylogenetic data for the genus (Bolin et al, 2009b; Jost et al, 2022). The revised subgeneric classification is presented summarised in Table 2.…”

“…On the basis that H. sinandevu lacks both setae and an apical osmophore, and parasitises Commiphora (Burseraceae) rather than Fabaceae, thus conflicting considerably with the criteria for subgenus Dorhyna , it is moved from subgenus Dorhyna to its own new section, subgenus Sineseta (translating to ‘without setae’ in Latin). A widely sampled molecular phylogeny will be required to confirm these taxonomic decisions, although they already comply with existing phylogenetic trees for the genus (Bolin et al, 2009b; Jost et al, 2022).…”