IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-48643-0.html
   My bibliography  Save this article

Two telomere-to-telomere gapless genomes reveal insights into Capsicum evolution and capsaicinoid biosynthesis

Author

Listed:
  • Weikai Chen

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang)

  • Xiangfeng Wang

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang)

  • Jie Sun

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang)

  • Xinrui Wang

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang)

  • Zhangsheng Zhu

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang
    South China Agricultural University)

  • Dilay Hazal Ayhan

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang)

  • Shu Yi

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang)

  • Ming Yan

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang)

  • Lili Zhang

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang
    Weifang Institute of Technology)

  • Tan Meng

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang)

  • Yu Mu

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang)

  • Jun Li

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang)

  • Dian Meng

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang)

  • Jianxin Bian

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang)

  • Ke Wang

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang
    Shandong Agricultural University)

  • Lu Wang

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang)

  • Shaoying Chen

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang)

  • Ruidong Chen

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang)

  • Jingyun Jin

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang)

  • Bosheng Li

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang)

  • Xingping Zhang

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang)

  • Xing Wang Deng

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang
    Peking University)

  • Hang He

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang
    Peking University)

  • Li Guo

    (Shandong Laboratory of Advanced Agricultural Sciences in Weifang)

Abstract

Chili pepper (Capsicum) is known for its unique fruit pungency due to the presence of capsaicinoids. The evolutionary history of capsaicinoid biosynthesis and the mechanism of their tissue specificity remain obscure due to the lack of high-quality Capsicum genomes. Here, we report two telomere-to-telomere (T2T) gap-free genomes of C. annuum and its wild nonpungent relative C. rhomboideum to investigate the evolution of fruit pungency in chili peppers. We precisely delineate Capsicum centromeres, which lack high-copy tandem repeats but are extensively invaded by CRM retrotransposons. Through phylogenomic analyses, we estimate the evolutionary timing of capsaicinoid biosynthesis. We reveal disrupted coding and regulatory regions of key biosynthesis genes in nonpungent species. We also find conserved placenta-specific accessible chromatin regions, which likely allow for tissue-specific biosynthetic gene coregulation and capsaicinoid accumulation. These T2T genomic resources will accelerate chili pepper genetic improvement and help to understand Capsicum genome evolution.

Suggested Citation

  • Weikai Chen & Xiangfeng Wang & Jie Sun & Xinrui Wang & Zhangsheng Zhu & Dilay Hazal Ayhan & Shu Yi & Ming Yan & Lili Zhang & Tan Meng & Yu Mu & Jun Li & Dian Meng & Jianxin Bian & Ke Wang & Lu Wang & , 2024. "Two telomere-to-telomere gapless genomes reveal insights into Capsicum evolution and capsaicinoid biosynthesis," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48643-0
    DOI: 10.1038/s41467-024-48643-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-48643-0
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-48643-0?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Hanin Ibrahim Ahmed & Matthias Heuberger & Adam Schoen & Dal-Hoe Koo & Jesus Quiroz-Chavez & Laxman Adhikari & John Raupp & Stéphane Cauet & Nathalie Rodde & Charlotte Cravero & Caroline Callot & Gera, 2023. "Einkorn genomics sheds light on history of the oldest domesticated wheat," Nature, Nature, vol. 620(7975), pages 830-838, August.
    2. Piotr Wlodzimierz & Fernando A. Rabanal & Robin Burns & Matthew Naish & Elias Primetis & Alison Scott & Terezie Mandáková & Nicola Gorringe & Andrew J. Tock & Daniel Holland & Katrin Fritschi & Anette, 2023. "Cycles of satellite and transposon evolution in Arabidopsis centromeres," Nature, Nature, vol. 618(7965), pages 557-565, June.
    3. Ryan S. Nett & Warren Lau & Elizabeth S. Sattely, 2020. "Discovery and engineering of colchicine alkaloid biosynthesis," Nature, Nature, vol. 584(7819), pages 148-153, August.
    4. Yi Liao & Juntao Wang & Zhangsheng Zhu & Yuanlong Liu & Jinfeng Chen & Yongfeng Zhou & Feng Liu & Jianjun Lei & Brandon S. Gaut & Bihao Cao & J. J. Emerson & Changming Chen, 2022. "The 3D architecture of the pepper genome and its relationship to function and evolution," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    5. Feng Liu & Jiantao Zhao & Honghe Sun & Cheng Xiong & Xuepeng Sun & Xin Wang & Zhongyi Wang & Robert Jarret & Jin Wang & Bingqian Tang & Hao Xu & Bowen Hu & Huan Suo & Bozhi Yang & Lijun Ou & Xuefeng L, 2023. "Genomes of cultivated and wild Capsicum species provide insights into pepper domestication and population differentiation," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    6. Ryan S. Nett & Warren Lau & Elizabeth S. Sattely, 2020. "Publisher Correction: Discovery and engineering of colchicine alkaloid biosynthesis," Nature, Nature, vol. 584(7821), pages 35-35, August.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Radin Sadre & Thilani M. Anthony & Josh M. Grabar & Matthew A. Bedewitz & A. Daniel Jones & Cornelius S. Barry, 2022. "Metabolomics-guided discovery of cytochrome P450s involved in pseudotropine-dependent biosynthesis of modified tropane alkaloids," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. Xiaofei Yang & Shenghan Gao & Li Guo & Bo Wang & Yanyan Jia & Jian Zhou & Yizhuo Che & Peng Jia & Jiadong Lin & Tun Xu & Jianyong Sun & Kai Ye, 2021. "Three chromosome-scale Papaver genomes reveal punctuated patchwork evolution of the morphinan and noscapine biosynthesis pathway," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    3. Hao-Tian Wang & Zi-Long Wang & Kuan Chen & Ming-Ju Yao & Meng Zhang & Rong-Shen Wang & Jia-He Zhang & Hans Ågren & Fu-Dong Li & Junhao Li & Xue Qiao & Min Ye, 2023. "Insights into the missing apiosylation step in flavonoid apiosides biosynthesis of Leguminosae plants," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Ruiqi Yan & Binghan Xie & Kebo Xie & Qi Liu & Songyang Sui & Shuqi Wang & Dawei Chen & Jimei Liu & Ridao Chen & Jungui Dai & Lin Yang, 2024. "Unravelling and reconstructing the biosynthetic pathway of bergenin," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    5. Dong Zheng & Yunlong Zheng & Junjie Tan & Zhenjie Zhang & He Huang & Yao Chen, 2024. "Co-immobilization of whole cells and enzymes by covalent organic framework for biocatalysis process intensification," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    6. Yue Gao & Fei Li & Zhengshan Luo & Zhiwei Deng & Yan Zhang & Zhenbo Yuan & Changmei Liu & Yijian Rao, 2024. "Modular assembly of an artificially concise biocatalytic cascade for the manufacture of phenethylisoquinoline alkaloids," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    7. Christopher J. Vavricka & Shunsuke Takahashi & Naoki Watanabe & Musashi Takenaka & Mami Matsuda & Takanobu Yoshida & Ryo Suzuki & Hiromasa Kiyota & Jianyong Li & Hiromichi Minami & Jun Ishii & Kenji T, 2022. "Machine learning discovery of missing links that mediate alternative branches to plant alkaloids," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    8. Yuanwei Gou & Dongfang Li & Minghui Zhao & Mengxin Li & Jiaojiao Zhang & Yilian Zhou & Feng Xiao & Gaofei Liu & Haote Ding & Chenfan Sun & Cuifang Ye & Chang Dong & Jucan Gao & Di Gao & Zehua Bao & Le, 2024. "Intein-mediated temperature control for complete biosynthesis of sanguinarine and its halogenated derivatives in yeast," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    9. Feng Liu & Jiantao Zhao & Honghe Sun & Cheng Xiong & Xuepeng Sun & Xin Wang & Zhongyi Wang & Robert Jarret & Jin Wang & Bingqian Tang & Hao Xu & Bowen Hu & Huan Suo & Bozhi Yang & Lijun Ou & Xuefeng L, 2023. "Genomes of cultivated and wild Capsicum species provide insights into pepper domestication and population differentiation," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48643-0. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.