Abstract
Carnivorous plants capture and digest animal prey for nutrition. In addition to being carnivorous, the humped bladderwort plant,
Utricularia gibba
, has the smallest reliably assembled flowering plant genome. We generated an updated genome assembly based on single-molecule sequencing to address questions regarding the bladderwort’s genome adaptive landscape. Among encoded genes, we segregated those that could be confidently distinguished as having derived from small-scale versus whole-genome duplication processes and showed that conspicuous expansions of gene families useful for prey trapping and processing derived mainly from localized duplication events. Such small-scale, tandem duplicates are therefore revealed as essential elements in the bladderwort’s carnivorous adaptation.
Utricularia gibba
, the humped bladderwort, is a carnivorous plant that retains a tiny nuclear genome despite at least two rounds of whole genome duplication (WGD) since common ancestry with grapevine and other species. We used a third-generation genome assembly with several complete chromosomes to reconstruct the two most recent lineage-specific ancestral genomes that led to the modern
U. gibba
genome structure. Patterns of subgenome dominance in the most recent WGD, both architectural and transcriptional, are suggestive of allopolyploidization, which may have generated genomic novelty and led to instantaneous speciation. Syntenic duplicates retained in polyploid blocks are enriched for transcription factor functions, whereas gene copies derived from ongoing tandem duplication events are enriched in metabolic functions potentially important for a carnivorous plant. Among these are tandem arrays of cysteine protease genes with trap-specific expression that evolved within a protein family known to be useful in the digestion of animal prey. Further enriched functions among tandem duplicates (also with trap-enhanced expression) include peptide transport (intercellular movement of broken-down prey proteins), ATPase activities (bladder-trap acidification and transmembrane nutrient transport), hydrolase and chitinase activities (breakdown of prey polysaccharides), and cell-wall dynamic components possibly associated with active bladder movements. Whereas independently polyploid
Arabidopsis
syntenic gene duplicates are similarly enriched for transcriptional regulatory activities,
Arabidopsis
tandems are distinct from those of
U. gibba
, while still metabolic and likely reflecting unique adaptations of that species. Taken together, these findings highlight the special importance of tandem duplications in the adaptive landscapes of a carnivorous plant genome.