Abstract
Subgenome dominance after whole-genome duplication generates distinction in gene number and expression at the level of chromosome sets, but it remains unclear how this process may be involved in evolutionary novelty. Here we generated a chromosome-scale genome assembly of the Asian pitcher plant Nepenthes gracilis to analyse how its novel traits (dioecy and carnivorous pitcher leaves) are linked to genomic evolution. We found a decaploid karyotype and a clear indication of subgenome dominance. A male-linked and pericentromerically located region on the putative sex chromosome was identified in a recessive subgenome and was found to harbour three transcription factors involved in flower and pollen development, including a likely neofunctionalized LEAFY duplicate. Transcriptomic and syntenic analyses of carnivory-related genes suggested that the paleopolyploidization events seeded genes that subsequently formed tandem clusters in recessive subgenomes with specific expression in the digestive zone of the pitcher, where specialized cells digest prey and absorb derived nutrients. A genome-scale analysis suggested that subgenome dominance likely contributed to evolutionary innovation by permitting recessive subgenomes to diversify functions of novel tissue-specific duplicates. Our results provide insight into how polyploidy can give rise to novel traits in divergent and successful high-ploidy lineages.
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Data availability
Raw data and results are available at Dryad (https://doi.org/10.5061/dryad.xsj3tx9mj). The N. gracilis genome assembly and gene models are available from the DNA Data Bank of Japan (DDBJ) with the accession numbers BSYO01000001 to BSYO01000176. The N. gracilis genome assemblies are also available on CoGe (https://genomevolution.org/coge/) (genome ID: male assembly, 61566; female Hi-C assembly, 61892; female syntenic path assembly, 61931) and Dryad (https://doi.org/10.5061/dryad.xsj3tx9mj). DNA and mRNA sequencing reads were deposited to DDBJ (PRJDB15224, PRJDB15738, PRJDB15742 and PRJDB15737) and EBI (PRJEB20488), and the accession numbers are shown in Supplementary Tables 1 and 4. In this study, data were sourced from the following publicly accessible databases: DDBJ (https://www.ddbj.nig.ac.jp/index-e.html), JASPAR (https://jaspar.genereg.net/), NCBI (https://www.ncbi.nlm.nih.gov/), OrthoDB (https://www.orthodb.org/), Pfam (https://www.ebi.ac.uk/interpro/) and UniProt (https://www.uniprot.org/).
Code availability
Scripts used in this study are available at Dryad (https://doi.org/10.5061/dryad.xsj3tx9mj).
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Acknowledgements
We acknowledge the following sources for funding: the Sofja Kovalevskaja programme of the Alexander von Humboldt Foundation (to K.F.), a Human Frontier Science Program Young Investigators grant RGY0082/2021 (to K.F. and T.R.), Deutsche Forschungsgemeinschaft research grants (454506241 to K.F., 415282803 to R.H. and 699/14-2 to G.B.), JSPS KAKENHI JP20H05909 (to K.S.), United States National Science Foundation grants (1442190 to V.A.A. and 2030871 to T.R. and V.A.A.), United States Department of Agriculture-National Institutes of Food and Agriculture grant 2019-67012-37587 (to K.J.G.) and research-leave funding from the School of Biological Sciences, Nanyang Technological University, to V.A.A. and C.L. that supported N. gracilis collecting and sequencing. M. Niissalo, J. H. Ang, Q. Y. Tan and G. Khew (Singapore Botanic Gardens, National Parks Board, Singapore) are thanked for their assistance with collecting and processing the N. gracilis material for long-read DNA sequencing. We thank J. Danz, H. Doi and L. Steffen for providing additional plant materials of Nepenthes, T. Winkelmann for propagating in vitro cultures of T. peltatum and J. Rothenhöfer for plant cultivation. Computations were partially performed on the National Institute of Genetics supercomputer, the Data Integration and Analysis Facility at the National Institute for Basic Biology, the Erlangen National High Performance Computing Center, the University at Buffalo Center for Computational Research and the High-Performance Computing Clusters at the University of Würzburg.
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V.A.A. and K.F. conceptualized the project. F.S., G.V., G.B., Y.W.L., C.L., V.A.A. and K.F. acquired materials. Y.W.L., C.L., T.P.M., S.M. and K.S. conducted and/or oversaw DNA extraction and sequencing. F.S., E.C., T.P.M., V.A.A. and K.F. conducted genome assembly. F.S., L.C., M.F., T.W. and K.F. conducted RNA extraction. S.R. conducted gene model prediction. F.S., A.M., M.R., M.S., V.A.A. and K.F. analysed the results. F.S., M.S., V.A.A. and K.F. wrote the manuscript with input from all authors. K.J.G. and T.R. contributed to improving the manuscript. D.B., R.H., V.A.A. and K.F. supervised the project and coordinated collaborations. All authors reviewed the final manuscript.
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Saul, F., Scharmann, M., Wakatake, T. et al. Subgenome dominance shapes novel gene evolution in the decaploid pitcher plant Nepenthes gracilis. Nat. Plants 9, 2000–2015 (2023). https://doi.org/10.1038/s41477-023-01562-2
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DOI: https://doi.org/10.1038/s41477-023-01562-2