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Subgenome dominance shapes novel gene evolution in the decaploid pitcher plant Nepenthes gracilis

Nature Plants volume 9, pages 2000–2015 (2023)Cite this article

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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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Fig. 1: Evolution of novel traits in Nepenthes.
Fig. 2: Subgenome dominance in the decaploid Nepenthes genome.
Fig. 3: The male-specific chromosomal region harbours transcriptional regulators of flower development.
Fig. 4: Tissue-specific gene expression in trapping pitcher leaves.
Fig. 5: Differential contributions of subgenomes to the evolution of novel genes.

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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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Author notes

  1. These authors contributed equally: Franziska Saul, Mathias Scharmann.

Authors and Affiliations

  1. Institute for Molecular Plant Physiology and Biophysics, University of Würzburg, Würzburg, Germany

    Franziska Saul, Takanori Wakatake, Matthias Freund, Louisa Channon, Dirk Becker, Rainer Hedrich & Kenji Fukushima

  2. Institute for Biochemistry and Biology (IBB), University of Potsdam, Potsdam, Germany

    Mathias Scharmann

  3. School of Biological Sciences, Nanyang Technological University, Singapore, Singapore

    Sitaram Rajaraman

  4. Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland

    Sitaram Rajaraman

  5. Department of Chromosome Biology, Max Planck Institute for Plant Breeding Research, Cologne, Germany

    André Marques

  6. Institute of Organic Chemistry, University of Würzburg, Am Hubland, Würzburg, Germany

    Gerhard Bringmann

  7. Department of Biological Sciences, University at Buffalo, Buffalo, NY, USA

    Emily Carroll, Charlotte Lindqvist, Michaela Richter & Victor A. Albert

  8. Singapore Botanic Gardens, National Parks Board, Singapore, Singapore

    Yee Wen Low

  9. Department of Plant Biology & W.K. Kellogg Biological Station & Program in Ecology, Evolution, and Behavior, Michigan State University, Hickory Corners, MI, USA

    Kadeem J. Gilbert

  10. Department of Entomology, The Pennsylvania State University, University Park, PA, USA

    Tanya Renner

  11. Riken Center for Sustainable Resource Science, Yokohama, Japan

    Sachiko Masuda & Ken Shirasu

  12. Botanical Garden, University of Würzburg, Würzburg, Germany

    Gerd Vogg

  13. Plant Molecular and Cellular Biology Laboratory, The Salk Institute for Biological Studies, La Jolla, CA, USA

    Todd P. Michael

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  1. Franziska Saul
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Contributions

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.

Corresponding authors

Correspondence to Victor A. Albert or Kenji Fukushima.

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Nature Plants thanks Takashi Akagi, Andrej Pavlovic and Feng Cheng for their contribution to the peer review of this work.

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Supplementary Methods, Texts 1–7, Figs. 1–29 and references.

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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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