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Genome structural evolution in Brassica crops

Nature Plants volume 7, pages 757–765 (2021)Cite this article

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Abstract

The cultivated Brassica species include numerous vegetable and oil crops of global importance. Three genomes (designated A, B and C) share mesohexapolyploid ancestry and occur both singly and in each pairwise combination to define the Brassica species. With organizational errors (such as misplaced genome segments) corrected, we showed that the fundamental structure of each of the genomes is the same, irrespective of the species in which it occurs. This enabled us to clarify genome evolutionary pathways, including updating the Ancestral Crucifer Karyotype (ACK) block organization and providing support for the Brassica mesohexaploidy having occurred via a two-step process. We then constructed genus-wide pan-genomes, drawing from genes present in any species in which the respective genome occurs, which enabled us to provide a global gene nomenclature system for the cultivated Brassica species and develop a methodology to cost-effectively elucidate the genomic impacts of alien introgressions. Our advances not only underpin knowledge-based approaches to the more efficient breeding of Brassica crops but also provide an exemplar for the study of other polyploids.

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Fig. 1: GOGGs for the Brassica A, B and C genomes as represented in allotetraploid species.
Fig. 2: Collinearity of Brassica A, B and C genomes.
Fig. 3: Inferred structure of chromosomes in the nascent triplicated ancestral genome.
Fig. 4: Visualization of genomic impacts of alien introgression into allotetraploid Brassica species.

Data availability

The raw sequence reads of the R. sativus introgression samples can be found under NCBI BioProject accession ID PRJNA507350. The raw sequence reads of the B. fruticulosa introgression samples can be found under NCBI BioProject accession ID PRJNA673122. The raw genome resequencing reads for the B. carinata mapping population YWDH can be found under NCBI BioProject accession ID PRJNA722822. R-o-18 genome assembly information can be found under NCBI BioProject ID PRJNA649364.

Code availability

The R script Genome_Sequence_Reorganise has been deposited on GitHub (https://github.com/hezhesi/Genome_Sequence_Reorganise).

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Acknowledgements

This work was supported by UK Biotechnology and Biological Sciences Research Council grant nos. BB/L002124/1 and BB/R019819/1 to I.B.; National Natural Science Foundation of China grant no. 31972412 and Natural Science Foundation of Liaoning Province grant no. 2019-MS283 to R.J.; grant nos. 031B0890A from BMBF and SN14/22-1 from DFG to R.J.S. and H.T.L.; Australia Research Council Project grant no. LP160100030 to D.E.; National Natural Science Foundation of China grant no. 31970564 to J.Z.; and Indian Council of Agricultural Research grant no. F.No.27(5)/2007-HRD and Department of Biotechnology and Government of India grant no. BT/01/CEIB/12/I/03 to S.S.B.

Author information

Author notes

  1. Ruiqin Ji

    Present address: Department of Horticulture, Shenyang Agricultural University, Shenyang, China

Authors and Affiliations

  1. Department of Biology, University of York, York, UK

    Zhesi He, Ruiqin Ji, Lenka Havlickova, Lihong Wang, Yi Li & Ian Bancroft

  2. Department of Plant Breeding, Justus Liebig University of Giessen, Giessen, Germany

    Huey Tyng Lee & Rod J. Snowdon

  3. National Key Laboratory of Crop Genetic Improvement, College of Plant Science & Technology, Huazhong Agricultural University, Wuhan, China

    Jiaming Song, Jun Zou & Kede Liu

  4. Global Institute for Food Security (GIFS), University of Saskatchewan, Saskatoon, Saskatchewan, Canada

    Chushin Koh

  5. Department of Horticulture, College of Agriculture & Biotechnology, Zhejiang University, Hangzhou, China

    Jinghua Yang & Mingfang Zhang

  6. Agriculture and Agri-Food Canada, Saskatoon, Saskatchewan, Canada

    Isobel A. P. Parkin

  7. Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences (IVF, CAAS), Beijing, China

    Xiaowu Wang

  8. School of Biological Sciences and the Institute of Agriculture, Faculty of Science, The University of Western Australia, Crawley, Western Australia, Australia

    David Edwards

  9. Southern Cross Plant Science, Southern Cross University, Lismore, New South Wales, Australia

    Graham J. King

  10. Department of Plant Breeding and Genetics, Punjab Agricultural University, Ludhiana, India

    Surinder S. Banga

  11. Selgen, a.s., Plant breeding station, Chlumec nad Cidlinou, Czech Republic

    Ivana Machackova

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Contributions

I.B. conceived the work. Z.H., R.J., L.H., I.M. and I.B. designed the experiments. Z.H., R.J., L.H., L.W., Y.L., H.T.L., J.S., C.K., J.Y., M.Z., I.A.P.P., X.W., D.E., G.J.K., J.Z., K.L., R.J.S. and S.S.B. acquired, analysed and/or interpreted the data. Z.H. and I.B. drafted the manuscript.

Corresponding author

Correspondence to Ian Bancroft.

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The authors declare no competing interests.

Additional information

Peer review information Nature Plants thanks Jue Ruan, Yongfeng Zhou and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Visualization of genomic impacts of alien introgression into allotetraploid Brassica species: using an assembled genome for the donor species.

Genome Display Tile Plots were generated based on the relative abundance of genome sequence reads mapping to three reference genome assemblies. Quantification is represented in CMYK colour space for orthologous gene triplets. The cyan component represents abundance of the Brassica A genome orthologue, the yellow component that of the Brassica C genome orthologue and the magenta component that of the radish (R) genome orthologue. Controls are included, comprising parental species and in silico combinations to render a diagnostic colour key. Three plants representing the male sterile (CMS) plants of the hybrid system (no introgression) and three plants containing the radish introgression harbouring the restorer (Rfo) gene are illustrated. (a) Plots ordered by Brassica C genome. (b) Plots ordered by radish (R) genome.

Extended Data Fig. 2 Visualization of genomic impacts of alien introgression into allotetraploid Brassica species: use of mRNAseq.

Transcriptome Display Tile Plots were generated based on the relative abundance of mRNAseq sequence reads mapping to CDS gene models from three reference genome sequence assemblies. Quantification is represented in CMYK colour space for orthologous gene triplets. The cyan component represents abundance of the Brassica A genome orthologue, the yellow component that of the Brassica C genome orthologue and the magenta component that of the radish (R) genome orthologue. The triplets are plotted in Brassica C genome order, along with controls comprising parental species and in silico combinations to render a diagnostic colour key. Four plants representing the male sterile (CMS) plants of the hybrid system (no introgression) and four plants containing the radish introgression harbouring the restorer (Rfo) gene are illustrated.

Extended Data Fig. 3 Genome-ordered graphical genotypes for the Brassica A, B and C genomes as represented in allotetraploid species: before editing of genome sequences.

Graphical genotypes are shown for transcriptome or genome SNP markers scored across three doubled haploid (DH) linkage mapping populations: (1) 119 lines of the Varuna x Heera (VHDH) mapping population for A genome B. juncea and B genome B. juncea (Heera alleles in coral, Varuna alleles in blue and missing scores in white). (2) 45 lines of the Tapidor x Ningyou 7 (TNDH) mapping population for A genome B. napus and C genome B. napus (Ningyou 7 alleles in coral, Tapidor alleles in blue and missing scores in white). (3) 93 lines of the Yellowcross x Whiteban (YWDH) mapping population for B genome B. carinata and C genome B. carinata (Whiteban alleles in coral, Yellowcross alleles in blue and missing scores in white). The multi-coloured bars are colour-coded by the top BLAST sequence similarity match to the chromosomes in Arabidopsis thaliana (left bar) and Thellungiella parvula (right bar) of the Brassica gene model in which each respective SNP is scored (light blue = chromosome 1, orange = chromosome 2, dark blue = chromosome 3, green = chromosome 4, red = chromosome 5, salmon = chromosome 6, yellow = chromosome 7, light grey = no BLAST hit with E-value < 1e-30). Red arrows indicate the positions of anomalous genome segments for confirmation and editing into a new position. Clusters of 2 or 3 red arrows indicate unanchored scaffolds originally presented at the end of the respective genome sequence.

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Supplementary data workbook containing spreadsheets of 15 supplementary datasets and their legends.

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He, Z., Ji, R., Havlickova, L. et al. Genome structural evolution in Brassica crops. Nat. Plants 7, 757–765 (2021). https://doi.org/10.1038/s41477-021-00928-8

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