Transcriptomics and molecular evolutionary rate analysis of the Bladderwort (Utricularia), a Carnivorous Plant with a Minimal Genome

Background The carnivorous plant Utricularia gibba (bladderwort) is remarkable in having a minute genome, which at ca. 80 megabases is approximately half that of Arabidopsis. Bladderworts show an incredible diversity of forms surrounding a defined theme: tiny, bladder-like suction traps on terrestrial, epiphytic, or aquatic plants with a diversity of unusual vegetative formats. Utricularia plants, which are rootless, are also anomalous in physiological features (respiration and carbon distribution) and in preliminary data that suggests highly enhanced molecular evolutionary rates. Despite great interest in the genus, no genomic resources exist for Utricularia, and the substitution rate increase has not received further study. Results We describe the sequencing and analysis of the Utricularia gibba transcriptome. Three different plant parts were surveyed, the traps, the vegetative shoot bodies, and the inflorescence stems. We also examined the bladderwort transcriptome under diverse stress conditions. We detail aspects of functional classification, tissue similarity, nitrogen and phosphorus metabolism, respiration, DNA repair, and detoxification of reactive oxygen species (ROS). Long contigs of chloroplast and mitochondrial genomes were compared with those of other plants to better establish information on molecular evolutionary rates. Conclusion The Utricularia transcriptome provides a detailed genomic window into processes occurring in carnivorous plants. It contains a deep representation of the complex metabolic pathways that characterize a putative minimal plant genome, permitting its use as a source of genomic information to explore the structural, functional, and evolutionary diversity of the genus. Vegetative shoots and traps are the most similar organs by functional classification of their transcriptome, the traps expressing hydrolytic enzymes for prey digestion that were previously thought to be encoded by bacteria. Supporting physiological data, global gene expression analysis shows that traps significantly over-express genes involved in respiration and that phosphate uptake might occur mainly in trap, whereas nitrogen uptake could in part take place in vegetative parts. Expression of DNA repair and ROS detoxification enzymes may be indicative of response to increased respiration. Finally, evidence from the bladderwort transcriptome, direct measurement of ROS in situ, and cross-species comparisons of chloroplast and mitochondrial genomes supports a hypothesis that increased nucleotide substitution rates may be due to the mutagenic action of amplified ROS production.