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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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.
The R script Genome_Sequence_Reorganise has been deposited on GitHub (https://github.com/hezhesi/Genome_Sequence_Reorganise).
USDA Oilseeds: World Markets and Trade (USDA-FAS, 2020).
Murat, F. et al. Understanding Brassicaceae evolution through ancestral genome reconstruction. Genome Biol. 16, 262 (2015).
Nagaharu, U. Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Jpn J. Bot. 7, 389–452 (1935).
Wang, X. et al. The genome of the mesopolyploid crop species Brassica rapa. Nat. Genet. 43, 1035–1039 (2011).
Liu, S. et al. The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat. Commun. 5, 3930 (2014).
Parkin, I. et al. Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea. Genome Biol. 15, R77 (2014).
Chalhoub, B. et al. Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345, 950–953 (2014).
Yang, J. et al. The genome sequence of allopolyploid Brassica juncea and analysis of differential homoeolog gene expression influencing selection. Nat. Genet. 48, 1225–1232 (2016).
Lagercrantz, U. & Lydiate, D. J. Comparative genome mapping in Brassica. Genetics 144, 1903–1910 (1996).
O’Neill, C. M. & Bancroft, I. Comparative physical mapping of segments of the genome of Brassica oleracea var. alboglabra that are homoeologous to sequenced regions of chromosomes 4 and 5 of Arabidopsis thaliana. Plant J. 23, 233–243 (2000).
Yang, T.-J. et al. Sequence-level analysis of the diploidization process in the triplicated FLOWERING LOCUS C region of Brassica rapa. Plant Cell 18, 1339–1347 (2006).
Town, C. D. et al. Comparative genomics of Brassica oleracea and Arabidopsis thaliana reveal gene loss, fragmentation, and dispersal after polyploidy. Plant Cell 18, 1348–1359 (2006).
Parkin, I. A., Sharpe, A. G., Keith, D. J. & Lydiate, D. J. Identification of the A and C genomes of amphidiploid Brassica napus (oilseed rape). Genome 38, 1122–1131 (1995).
Rana, D. et al. Conservation of the microstructure of genome segments in Brassica napus and its diploid relatives. Plant J. 40, 725–733 (2004).
Cheung, F. et al. Comparative analysis between homoeologous genome segments of Brassica napus and its progenitor species reveals extensive sequence-level divergence. Plant Cell 21, 1912–1928 (2009).
Trick, M., Long, Y., Meng, J. & Bancroft, I. Single nucleotide polymorphism (SNP) discovery in the polyploid Brassica napus using Solexa transcriptome sequencing. Plant Biotechnol. J. 7, 334–346 (2009).
Bancroft, I. et al. Dissecting the genome of the polyploid crop oilseed rape by transcriptome sequencing. Nat. Biotechnol. 29, 762–766 (2011).
He, Z. & Bancroft, I. Organization of the genome sequence of the polyploid crop species Brassica juncea. Nat. Genet. 50, 1496–1497 (2018).
Vernikos, G., Medini, D., Riley, D. R. & Tettelin, H. Ten years of pan-genome analyses. Curr. Opin. Microbiol. 23, 148–154 (2015).
Golicz, A. A. et al. The pangenome of an agronomically important crop plant Brassica oleracea. Nat. Commun. 7, 13390 (2016).
Dolatabadian, A. et al. Characterization of disease resistance genes in the Brassica napus pangenome reveals significant structural variation. Plant Biotechnol. J. 18, 969–982 (2019).
Mallet, J. Hybridization as an invasion of the genome. Trends Ecol. Evol. 20, 229–237 (2005).
Arnold, M. L. Transfer and origin of adaptations through natural hybridization: were Anderson and Stebbins right? Plant Cell 16, 562–570 (2004).
Zamir, D. Improving plant breeding with exotic genetic libraries. Nat. Rev. Genet. 2, 983–989 (2001).
Delourme, R., Horvais, R., Vallée, P. & Renard, M. Double low restored F1 hybrids can be produced with the Ogu-INRA CMS in rapeseed. In Proc. 10th International Rapeseed Congress 26–29 (ACT, 1999).
Brown, G. G. et al. The radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats. Plant J. 35, 262–272 (2003).
Hu, X. et al. Mapping of the Ogura fertility restorer gene Rfo and development of Rfo allele-specific markers in canola (Brassica napus L.). Mol. Breed. 22, 663–674 (2008).
Feng, J. et al. Physical localization and genetic mapping of the fertility restoration gene Rfo in canola (Brassica napus L.). Genome 52, 401–407 (2009).
Yang, J., Ji, C., Liu, D., Wang, X. & Zhang, M. Reply to: ‘Organization of the genome sequence of the polyploid crop species Brassica juncea’. Nat. Genet. 50, 1497–1498 (2018).
He, Z. et al. Extensive homoeologous genome exchanges in allopolyploid crops revealed by mRNAseq-based visualization. Plant Biotechnol. J. 15, 594–604 (2017).
Crown, K. N., Miller, D. E., Sekelsky, J. & Hawley, R. S. Local inversion heterozygosity alters recombination throughout the genome. Curr. Biol. 28, 2984–2990.e3 (2018).
Bancroft, I., Fraser, F., Morgan, C. & Trick, M. Collinearity analysis of Brassica A and C genomes based on an updated inferred unigene order. Data Brief 3, 51–55 (2015).
Schranz, M., Lysak, M. & Mitchell-Olds, T. The ABC’s of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci. 11, 535–542 (2006).
Lysak, M. A., Mandáková, T. & Schranz, M. E. Comparative paleogenomics of crucifers: ancestral genomic blocks revisited. Curr. Opin. Plant Biol. 30, 108–115 (2016).
Cheng, F. et al. Deciphering the diploid ancestral genome of the mesohexaploid Brassica rapa. Plant Cell 25, 1541–1554 (2013).
Belser, C. et al. Chromosome-scale assemblies of plant genomes using nanopore long reads and optical maps. Nat. Plants 4, 879–887 (2018).
Perumal, S. et al. A high-contiguity Brassica nigra genome localizes active centromeres and defines the ancestral Brassica genome. Nat. Plants 6, 929–941 (2020).
Higgins, J., Magusin, A., Trick, M., Fraser, F. & Bancroft, I. Use of mRNA-seq to discriminate contributions to the transcriptome from the constituent genomes of the polyploid crop species Brassica napus. BMC Genom. 13, 247 (2012).
Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinform. 10, 421 (2009).
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
Zhang, L. et al. Improved Brassica rapa reference genome by single-molecule sequencing and chromosome conformation capture technologies. Hortic. Res. 5, 50 (2018).
Zou, J. et al. Genome-wide selection footprints and deleterious variations in young Asian allotetraploid rapeseed. Plant Biotechnol. J. 17, 1998–2010 (2019).
Song, J.-M. et al. Eight high-quality genomes reveal pan-genome architecture and ecotype differentiation of Brassica napus. Nat. Plants 6, 34–45 (2020).
Lee, H. et al. Chromosome-scale assembly of winter oilseed rape Brassica napus. Front. Plant Sci. 11, 496 (2020).
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.
The authors declare no competing interests.
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 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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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