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

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, Shaoying Chen, Ruidong Chen, Jingyun Jin, Bosheng Li, Xingping Zhang, Xing Wang Deng, Hang He () and Li Guo ()
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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
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
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
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
Hang He: Shandong Laboratory of Advanced Agricultural Sciences in Weifang
Li Guo: Shandong Laboratory of Advanced Agricultural Sciences in Weifang

Nature Communications, 2024, vol. 15, issue 1, 1-14

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-48643-0

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