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.
Description
Subgenome dominance shapes novel gene evolution in the decaploid pitcher plant Nepenthes gracilis | Nature Plants
%0 Journal Article
%1 Saul2023
%A Saul, Franziska
%A Scharmann, Mathias
%A Wakatake, Takanori
%A Rajaraman, Sitaram
%A Marques, André
%A Freund, Matthias
%A Bringmann, Gerhard
%A Channon, Louisa
%A Becker, Dirk
%A Carroll, Emily
%A Low, Yee Wen
%A Lindqvist, Charlotte
%A Gilbert, Kadeem J.
%A Renner, Tanya
%A Masuda, Sachiko
%A Richter, Michaela
%A Vogg, Gerd
%A Shirasu, Ken
%A Michael, Todd P.
%A Hedrich, Rainer
%A Albert, Victor A.
%A Fukushima, Kenji
%D 2023
%J Nature Plants
%K myown
%N 12
%P 2000--2015
%R 10.1038/s41477-023-01562-2
%T Subgenome dominance shapes novel gene evolution in the decaploid pitcher plant Nepenthes gracilis
%U https://doi.org/10.1038/s41477-023-01562-2
%V 9
%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{Saul2023,
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 = {2024-01-17T23:49:33.000+0100},
author = {Saul, Franziska and Scharmann, Mathias and Wakatake, Takanori and Rajaraman, Sitaram and Marques, Andr{\'e} and Freund, Matthias and Bringmann, Gerhard and Channon, Louisa and Becker, Dirk and Carroll, Emily and Low, Yee Wen and Lindqvist, Charlotte and Gilbert, Kadeem J. and Renner, Tanya and Masuda, Sachiko and Richter, Michaela and Vogg, Gerd and Shirasu, Ken and Michael, Todd P. and Hedrich, Rainer and Albert, Victor A. and Fukushima, Kenji},
biburl = {https://www.bibsonomy.org/bibtex/237aafa3e0bc98d1ddcf52c3a6f975585/kfuku},
day = 01,
description = {Subgenome dominance shapes novel gene evolution in the decaploid pitcher plant Nepenthes gracilis | Nature Plants},
doi = {10.1038/s41477-023-01562-2},
interhash = {b3329376fd9a9fa9be1de05f00dad8d6},
intrahash = {37aafa3e0bc98d1ddcf52c3a6f975585},
issn = {2055-0278},
journal = {Nature Plants},
keywords = {myown},
month = dec,
number = 12,
pages = {2000--2015},
timestamp = {2024-01-17T23:49:33.000+0100},
title = {Subgenome dominance shapes novel gene evolution in the decaploid pitcher plant Nepenthes gracilis},
url = {https://doi.org/10.1038/s41477-023-01562-2},
volume = 9,
year = 2023
}