The floral ABCs of Hydnora, one of the most bizarre parasitic plants in the world, and its autotrophic relatives of the order Piperales

Hydnora (Hydnoraceae) comprises a few parasitic species exceptional among the autotrophic members of the perianth-bearing Piperales. Flowers in the genus are thick, fleshy, sapromyophilous, and develop into massive, polyspermous fruits. They are formed directly along underground rhizomes that parasitize species of Euphorbiaceae and Fabaceae. Due to its peculiar floral morphology and lack of leaves, Hydnora is often dubbed 'the strangest plant in the world'. Here we generated the first transcriptomes of Hydnora visseri from the dissected rhizome, perianth, osmophore, stamen, carpel, and fruit. Our results suggest that Hydnora possesses one of the simplest developmental genetic toolkits for flowering and floral organ identity among angiosperms, further emphasizing its uniqueness. We detected that most of the photoperiodic flowering integrators are expressed. In contrast, regulators of the autonomous pathway and circadian clock were notably absent from the transcriptomes. Conversely, we identified an intact genetic toolkit linked to floral organ identity and fruit development in Hydnora. Through positional homology and gene expression data, we inferred that the perianth of Hydnora corresponds to the calyx, and that the osmophores are late sepal elaborations. Additionally, the expression patterns of genes responsible for stamen, carpel, and ovule identity align with the canonical ABCDE model. Finally, we recorded large-scale duplications in putative perianth identity genes prior to the diversification of all perianth-bearing Piperales. This study serves as an additional comparative point for assessing the evolutionary onset of holoparasitic plants, as Hydnora and its sister genus Prosopanche are likely the earliest branching representatives of this lifestyle across angiosperms.