Subgenome dominance shapes novel gene evolution in the decaploid pitcher plant Nepenthes gracilis
F. Saul, M. Scharmann, T. Wakatake, S. Rajaraman, A. Marques, M. Freund, G. Bringmann, L. Channon, D. Becker, E. Carroll, Y. Low, C. Lindqvist, K. Gilbert, T. Renner, S. Masuda, M. Richter, G. Vogg, K. Shirasu, T. Michael, R. Hedrich, V. Albert, and K. Fukushima. Nat Plants, (2023)Saul, Franziska
Scharmann, Mathias
Wakatake, Takanori
Rajaraman, Sitaram
Marques, Andre
Freund, Matthias
Bringmann, Gerhard
Channon, Louisa
Becker, Dirk
Carroll, Emily
Low, Yee Wen
Lindqvist, Charlotte
Gilbert, Kadeem J
Renner, Tanya
Masuda, Sachiko
Richter, Michaela
Vogg, Gerd
Shirasu, Ken
Michael, Todd P
Hedrich, Rainer
Albert, Victor A
Fukushima, Kenji
eng
Sofja Kovalevskaja programme 2018/Alexander von Humboldt-Stiftung (Alexander von Humboldt Foundation)/
RGY0082/2021/Human Frontier Science Program (HFSP)/
454506241/Deutsche Forschungsgemeinschaft (German Research Foundation)/
699/14-2/Deutsche Forschungsgemeinschaft (German Research Foundation)/
415282803/Deutsche Forschungsgemeinschaft (German Research Foundation)/
2019-67012-37587/U.S. Department of Agriculture ( Department of Agriculture)/
JP20H05909/MEXT | Japan Society for the Promotion of Science (JSPS)/
2030871/National Science Foundation (NSF)/
England
2023/11/24
Nat Plants. 2023 Nov 23. doi: 10.1038/s41477-023-01562-2..
DOI: 10.1038/s41477-023-01562-2
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.
Saul, Franziska
Scharmann, Mathias
Wakatake, Takanori
Rajaraman, Sitaram
Marques, Andre
Freund, Matthias
Bringmann, Gerhard
Channon, Louisa
Becker, Dirk
Carroll, Emily
Low, Yee Wen
Lindqvist, Charlotte
Gilbert, Kadeem J
Renner, Tanya
Masuda, Sachiko
Richter, Michaela
Vogg, Gerd
Shirasu, Ken
Michael, Todd P
Hedrich, Rainer
Albert, Victor A
Fukushima, Kenji
eng
Sofja Kovalevskaja programme 2018/Alexander von Humboldt-Stiftung (Alexander von Humboldt Foundation)/
RGY0082/2021/Human Frontier Science Program (HFSP)/
454506241/Deutsche Forschungsgemeinschaft (German Research Foundation)/
699/14-2/Deutsche Forschungsgemeinschaft (German Research Foundation)/
415282803/Deutsche Forschungsgemeinschaft (German Research Foundation)/
2019-67012-37587/U.S. Department of Agriculture ( Department of Agriculture)/
JP20H05909/MEXT | Japan Society for the Promotion of Science (JSPS)/
2030871/National Science Foundation (NSF)/
England
2023/11/24
Nat Plants. 2023 Nov 23. doi: 10.1038/s41477-023-01562-2.
%0 Journal Article
%1 saul2023subgenome
%A Saul, F.
%A Scharmann, M.
%A Wakatake, T.
%A Rajaraman, S.
%A Marques, A.
%A Freund, M.
%A Bringmann, G.
%A Channon, L.
%A Becker, D.
%A Carroll, E.
%A Low, Y. W.
%A Lindqvist, C.
%A Gilbert, K. J.
%A Renner, T.
%A Masuda, S.
%A Richter, M.
%A Vogg, G.
%A Shirasu, K.
%A Michael, T. P.
%A Hedrich, R.
%A Albert, V. A.
%A Fukushima, K.
%D 2023
%J Nat Plants
%K imported myOwn uni_network
%R 10.1038/s41477-023-01562-2
%T Subgenome dominance shapes novel gene evolution in the decaploid pitcher plant Nepenthes gracilis
%U https://www.ncbi.nlm.nih.gov/pubmed/37996654https://www.nature.com/articles/s41477-023-01562-2
%X 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.
@article{saul2023subgenome,
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.},
added-at = {2024-02-15T15:11:54.000+0100},
author = {Saul, F. and Scharmann, M. and Wakatake, T. and Rajaraman, S. and Marques, A. and Freund, M. and Bringmann, G. and Channon, L. and Becker, D. and Carroll, E. and Low, Y. W. and Lindqvist, C. and Gilbert, K. J. and Renner, T. and Masuda, S. and Richter, M. and Vogg, G. and Shirasu, K. and Michael, T. P. and Hedrich, R. and Albert, V. A. and Fukushima, K.},
biburl = {https://www.bibsonomy.org/bibtex/2fcb9860dd707ebd79234dfc871adb8cb/jvsi_all},
doi = {10.1038/s41477-023-01562-2},
interhash = {b3329376fd9a9fa9be1de05f00dad8d6},
intrahash = {fcb9860dd707ebd79234dfc871adb8cb},
issn = {2055-0278 (Electronic)
2055-0278 (Linking)},
journal = {Nat Plants},
keywords = {imported myOwn uni_network},
note = {Saul, Franziska
Scharmann, Mathias
Wakatake, Takanori
Rajaraman, Sitaram
Marques, Andre
Freund, Matthias
Bringmann, Gerhard
Channon, Louisa
Becker, Dirk
Carroll, Emily
Low, Yee Wen
Lindqvist, Charlotte
Gilbert, Kadeem J
Renner, Tanya
Masuda, Sachiko
Richter, Michaela
Vogg, Gerd
Shirasu, Ken
Michael, Todd P
Hedrich, Rainer
Albert, Victor A
Fukushima, Kenji
eng
Sofja Kovalevskaja programme 2018/Alexander von Humboldt-Stiftung (Alexander von Humboldt Foundation)/
RGY0082/2021/Human Frontier Science Program (HFSP)/
454506241/Deutsche Forschungsgemeinschaft (German Research Foundation)/
699/14-2/Deutsche Forschungsgemeinschaft (German Research Foundation)/
415282803/Deutsche Forschungsgemeinschaft (German Research Foundation)/
2019-67012-37587/U.S. Department of Agriculture ( Department of Agriculture)/
JP20H05909/MEXT | Japan Society for the Promotion of Science (JSPS)/
2030871/National Science Foundation (NSF)/
England
2023/11/24
Nat Plants. 2023 Nov 23. doi: 10.1038/s41477-023-01562-2.},
timestamp = {2024-02-15T15:11:54.000+0100},
title = {Subgenome dominance shapes novel gene evolution in the decaploid pitcher plant Nepenthes gracilis},
type = {Journal Article},
url = {https://www.ncbi.nlm.nih.gov/pubmed/37996654https://www.nature.com/articles/s41477-023-01562-2},
year = 2023
}