Genomic Insights into the Evolution of Carnivory in the Giant Butterwort, Pinguicula gigantea: Chromosome-Level Assembly and Phylogenomic Analysis

Abstract

Carnivorous plants provide a powerful system for studying plant morphological and physiological evolution. These plants capture and digest prey for nutrients and this rare trait has evolved independently at least eleven times in thirteen families within six orders. Among these are the butterworts in the genus Pinguicula. This group of plants captures prey on a basal rosette of sticky leaves where the prey is broken down and digested. Here we present the chromosome-level reference assembly of the carnivorous giant butterwort, Pinguicula gigantea. An additional two assemblies were generated for this study, primarily from long-read sequencing data. In this study, we focus on the genome evolution of Pinguicula, including confirming at least two whole genome duplications since the gamma hexaploidy event at the base of the core eudicots. We provide evidence from full-genome data that the carnivorous family that Pinguicula belongs to, the Lentibulariaceae, is most closely related to the Acanthaceae. We also report multiple tandem duplications of candidate digestive enzyme genes, including a putative tandem duplication of cysteine proteases that is syntenic with two cysteine protease tandem duplication in Utricularia gibba that contain genes with trap specific expression. We also show evidence that these tandem duplications evolved independently in both Pinguicula and Utricularia gibbaUtricularia gibba and were potentially facilitated by different repeat element families.