Long-read sequencing uncovers the adaptive topography of a carnivorous plant genome

Tianying Lan, Tanya Renner, Enrique Ibarra-Laclette, Kimberly M. Farr, Tien Hao Chang, Sergio Alan Cervantes-Pérez, Chunfang Zheng, David Sankoff, Haibao Tang, Rikky W. Purbojati, Alexander Putra, Daniela I. Drautz-Moses, Stephan C. Schuster, Luis Herrera-Estrella, Victor A. Albert

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Abstract

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 trapspecific 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 brokendown 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.

Original languageEnglish (US)
Pages (from-to)E4435-E4441
JournalProceedings of the National Academy of Sciences of the United States of America
Volume114
Issue number22
DOIs
StatePublished - May 30 2017

All Science Journal Classification (ASJC) codes

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    Lan, T., Renner, T., Ibarra-Laclette, E., Farr, K. M., Chang, T. H., Cervantes-Pérez, S. A., Zheng, C., Sankoff, D., Tang, H., Purbojati, R. W., Putra, A., Drautz-Moses, D. I., Schuster, S. C., Herrera-Estrella, L., & Albert, V. A. (2017). Long-read sequencing uncovers the adaptive topography of a carnivorous plant genome. Proceedings of the National Academy of Sciences of the United States of America, 114(22), E4435-E4441. https://doi.org/10.1073/pnas.1702072114