Genome-Wide Analysis of Adaptive Molecular Evolution in the Carnivorous Plant Utricularia gibba

The genome of Utricularia gibba provides an unparalleled opportunity to uncover the adaptive landscape of an aquatic carnivorous plant that has evolved unique phenotypic features such as absence of roots, development of water-filled suction bladders and a highly ramified branching pattern. Despite its tiny size (only 82 Mb) the U. gibba genome accommodates a number of genes similar to grape or Arabidopsis. Using the U. gibba genome and those of 4 other eudicot species, we i) classified species-specific gene family expansions and contractions through estimation of birth and death rates, and ii) made a preliminary scan for signatures of lineage-specific protein functional specialization, including positive Darwinian selection (PS). Selected genes identified in the latter were later manually curated for evidence of positive selection. One important finding from the expansions/contractions analysis was that the U. gibba gene death rate is considerably higher than in the other species, which may explain why the number of genes encoded by its genome is similar to that of other plant genomes such as Arabidopsis, grape, and papaya, despite it having undergone three independent rounds of whole genome duplication since divergence from these other species. This high death rate is consistent with our published model of intense fractionation of the Utricularia genome via an enhanced DNA deletion bias. We examined the distributions of gene ontology terms enriched among expanded gene families, or showing possible adaptive functional specialization, to identify gene functions that may have played a prominent role during U. gibba evolution. One example is tryptophan and auxin metabolism as well as auxin signal transduction, which has a major impact on root architecture and stem elongation. We also identified several enzymatic functions among expanded families that might be related to metabolic adaptations to carnivory, e.g., hydrolase activity (mostly corresponding to proteases and phosphatases). Interestingly, the term “protein metabolic process” clustered 30 genes. Also either expanded or possibly under PS were several gene expression regulators involved in different developmental processes, including the transition between vegetative and reproductive state, likely relevant for U. gibba’s highly specialized body plan.