Large-scale gene expression alterations introduced by structural variation drive morphotype diversification in Brassica oleracea

Xing Li; Yong Wang; Chengcheng Cai; Jialei Ji; Fengqing Han; Lei Zhang; Shumin Chen; Lingkui Zhang; Yinqing Yang; Qi Tang; Johan Bucher; Xuelin Wang; Limei Yang; Mu Zhuang; Kang Zhang; Honghao Lv; Guusje Bonnema; Yangyong Zhang; Feng Cheng

doi:10.1038/s41588-024-01655-4

Large-scale gene expression alterations introduced by structural variation drive morphotype diversification in Brassica oleracea

Xing Li, Yong Wang, Chengcheng Cai, Jialei Ji, Fengqing Han, Lei Zhang, Shumin Chen, Lingkui Zhang, Yinqing Yang, Qi Tang, Johan Bucher, Xuelin Wang, Limei Yang, Mu Zhuang, Kang Zhang^*, Honghao Lv^*, Guusje Bonnema^*, Yangyong Zhang^*, Feng Cheng^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

9 Citations (Scopus)

Abstract

Brassica oleracea, globally cultivated for its vegetable crops, consists of very diverse morphotypes, characterized by specialized enlarged organs as harvested products. This makes B. oleracea an ideal model for studying rapid evolution and domestication. We constructed a B. oleracea pan-genome from 27 high-quality genomes representing all morphotypes and their wild relatives. We identified structural variations (SVs) among these genomes and characterized these in 704 B. oleracea accessions using graph-based genome tools. We show that SVs exert bidirectional effects on the expression of numerous genes, either suppressing through DNA methylation or promoting probably by harboring transcription factor-binding elements. The following examples illustrate the role of SVs modulating gene expression: SVs promoting BoPNY and suppressing BoCKX3 in cauliflower/broccoli, suppressing BoKAN1 and BoACS4 in cabbage and promoting BoMYBtf in ornamental kale. These results provide solid evidence for the role of SVs as dosage regulators of gene expression, driving B. oleracea domestication and diversification.

Original language	English
Pages (from-to)	517-529
Journal	Nature Genetics
Volume	56
Issue number	3
Early online date	13 Feb 2024
DOIs	https://doi.org/10.1038/s41588-024-01655-4
Publication status	Published - 2024

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10.1038/s41588-024-01655-4Licence: CC BY

https://edepot.wur.nl/651241Licence: CC BY

Brassica oleracea Genome sequencing and assembly
Li, X. (Creator), Wang, Y. (Creator), Cai, C. (Creator), Ji, J. (Creator), Han, F. (Creator), Zhang, L. (Creator), Chen, S. (Creator), Zhang, L. (Creator), Yang, Y. (Creator), Tang, Q. (Creator), Bucher, J. (Creator), Wang, X. (Creator), Yang, L. (Creator), Zhuang, M. (Creator), Zhang, K. (Creator), Lv, H. (Creator), Bonnema, G. (Creator), Zhang, Y. (Creator) & Cheng, F. (Creator), Chinese Academy of Agricultural Sciences, 26 Dec 2023
https://www.ncbi.nlm.nih.gov/bioproject/1047966
Dataset

Cite this

Li, X., Wang, Y., Cai, C., Ji, J., Han, F., Zhang, L., Chen, S., Zhang, L., Yang, Y., Tang, Q., Bucher, J., Wang, X., Yang, L., Zhuang, M., Zhang, K., Lv, H., Bonnema, G., Zhang, Y., & Cheng, F. (2024). Large-scale gene expression alterations introduced by structural variation drive morphotype diversification in Brassica oleracea. Nature Genetics, 56(3), 517-529. https://doi.org/10.1038/s41588-024-01655-4

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title = "Large-scale gene expression alterations introduced by structural variation drive morphotype diversification in Brassica oleracea",

abstract = "Brassica oleracea, globally cultivated for its vegetable crops, consists of very diverse morphotypes, characterized by specialized enlarged organs as harvested products. This makes B. oleracea an ideal model for studying rapid evolution and domestication. We constructed a B. oleracea pan-genome from 27 high-quality genomes representing all morphotypes and their wild relatives. We identified structural variations (SVs) among these genomes and characterized these in 704 B. oleracea accessions using graph-based genome tools. We show that SVs exert bidirectional effects on the expression of numerous genes, either suppressing through DNA methylation or promoting probably by harboring transcription factor-binding elements. The following examples illustrate the role of SVs modulating gene expression: SVs promoting BoPNY and suppressing BoCKX3 in cauliflower/broccoli, suppressing BoKAN1 and BoACS4 in cabbage and promoting BoMYBtf in ornamental kale. These results provide solid evidence for the role of SVs as dosage regulators of gene expression, driving B. oleracea domestication and diversification.",

author = "Xing Li and Yong Wang and Chengcheng Cai and Jialei Ji and Fengqing Han and Lei Zhang and Shumin Chen and Lingkui Zhang and Yinqing Yang and Qi Tang and Johan Bucher and Xuelin Wang and Limei Yang and Mu Zhuang and Kang Zhang and Honghao Lv and Guusje Bonnema and Yangyong Zhang and Feng Cheng",

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doi = "10.1038/s41588-024-01655-4",

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journal = "Nature Genetics",

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Li, X, Wang, Y, Cai, C, Ji, J, Han, F, Zhang, L, Chen, S, Zhang, L, Yang, Y, Tang, Q, Bucher, J, Wang, X, Yang, L, Zhuang, M, Zhang, K, Lv, H, Bonnema, G, Zhang, Y & Cheng, F 2024, 'Large-scale gene expression alterations introduced by structural variation drive morphotype diversification in Brassica oleracea', Nature Genetics, vol. 56, no. 3, pp. 517-529. https://doi.org/10.1038/s41588-024-01655-4

TY - JOUR

T1 - Large-scale gene expression alterations introduced by structural variation drive morphotype diversification in Brassica oleracea

AU - Li, Xing

AU - Wang, Yong

AU - Cai, Chengcheng

AU - Ji, Jialei

AU - Han, Fengqing

AU - Zhang, Lei

AU - Chen, Shumin

AU - Zhang, Lingkui

AU - Yang, Yinqing

AU - Tang, Qi

AU - Bucher, Johan

AU - Wang, Xuelin

AU - Yang, Limei

AU - Zhuang, Mu

AU - Zhang, Kang

AU - Lv, Honghao

AU - Bonnema, Guusje

AU - Zhang, Yangyong

AU - Cheng, Feng

PY - 2024

Y1 - 2024

N2 - Brassica oleracea, globally cultivated for its vegetable crops, consists of very diverse morphotypes, characterized by specialized enlarged organs as harvested products. This makes B. oleracea an ideal model for studying rapid evolution and domestication. We constructed a B. oleracea pan-genome from 27 high-quality genomes representing all morphotypes and their wild relatives. We identified structural variations (SVs) among these genomes and characterized these in 704 B. oleracea accessions using graph-based genome tools. We show that SVs exert bidirectional effects on the expression of numerous genes, either suppressing through DNA methylation or promoting probably by harboring transcription factor-binding elements. The following examples illustrate the role of SVs modulating gene expression: SVs promoting BoPNY and suppressing BoCKX3 in cauliflower/broccoli, suppressing BoKAN1 and BoACS4 in cabbage and promoting BoMYBtf in ornamental kale. These results provide solid evidence for the role of SVs as dosage regulators of gene expression, driving B. oleracea domestication and diversification.

AB - Brassica oleracea, globally cultivated for its vegetable crops, consists of very diverse morphotypes, characterized by specialized enlarged organs as harvested products. This makes B. oleracea an ideal model for studying rapid evolution and domestication. We constructed a B. oleracea pan-genome from 27 high-quality genomes representing all morphotypes and their wild relatives. We identified structural variations (SVs) among these genomes and characterized these in 704 B. oleracea accessions using graph-based genome tools. We show that SVs exert bidirectional effects on the expression of numerous genes, either suppressing through DNA methylation or promoting probably by harboring transcription factor-binding elements. The following examples illustrate the role of SVs modulating gene expression: SVs promoting BoPNY and suppressing BoCKX3 in cauliflower/broccoli, suppressing BoKAN1 and BoACS4 in cabbage and promoting BoMYBtf in ornamental kale. These results provide solid evidence for the role of SVs as dosage regulators of gene expression, driving B. oleracea domestication and diversification.

U2 - 10.1038/s41588-024-01655-4

DO - 10.1038/s41588-024-01655-4

M3 - Article

C2 - 38351383

AN - SCOPUS:85185145934

SN - 1061-4036

VL - 56

SP - 517

EP - 529

JO - Nature Genetics

JF - Nature Genetics

IS - 3

ER -

Large-scale gene expression alterations introduced by structural variation drive morphotype diversification in Brassica oleracea

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Datasets

Brassica oleracea Genome sequencing and assembly

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