Subgenome parallel selection is associated with morphotype diversification and convergent crop domestication in Brassica rapa and Brassica oleracea

Journal name:
Nature Genetics
Volume:
48,
Pages:
1218–1224
Year published:
DOI:
doi:10.1038/ng.3634
Received
Accepted
Published online

Abstract

Brassica species, including crops such as cabbage, turnip and oilseed, display enormous phenotypic variation. Brassica genomes have all undergone a whole-genome triplication (WGT) event with unknown effects on phenotype diversification. We resequenced 199 Brassica rapa and 119 Brassica oleracea accessions representing various morphotypes and identified signals of selection at the mesohexaploid subgenome level. For cabbage morphotypes with their typical leaf-heading trait, we identified four subgenome loci that show signs of parallel selection among subgenomes within B. rapa, as well as four such loci within B. oleracea. Fifteen subgenome loci are under selection and are shared by these two species. We also detected strong subgenome parallel selection linked to the domestication of the tuberous morphotypes, turnip (B. rapa) and kohlrabi (B. oleracea). Overall, we demonstrated that the mesohexaploidization of the two Brassica genomes contributed to their diversification into heading and tuber-forming morphotypes through convergent subgenome parallel selection of paralogous genes.

At a glance

Figures

  1. Phylogenetic tree of 199 B. rapa and 119 B. oleracea accessions.
    Figure 1: Phylogenetic tree of 199 B. rapa and 119 B. oleracea accessions.

    The tree was constructed using 6,707 SNP loci selected from gene pairs that were syntenic in the B. rapa and B. oleracea genomes. Different branches of the tree are highlighted by different colors. For B. rapa accessions (left), colors correspond to groups as follows: light blue, turnip; dark blue, sarson; pink, turnip rape; yellow, Japanese group; green, pak choi, wutacai, caixin, zicaitai and taicai; red, late-diverging Chinese cabbage (heading B. rapa, BrH group). For B. oleracea accessions (right), colors correspond to groups as follows: black, wild B. oleracea; blue, kohlrabi; yellow, Chinese kale; light green, cauliflower; green, broccoli; light green, Brussels sprouts; purple, kale; red, heading cabbage (heading B. oleracea, BoH group). Pictures placed beside each clade show typical morphotypes for the corresponding groups.

  2. Genomic signatures of selection in genomes of Chinese cabbage and cabbage.
    Figure 2: Genomic signatures of selection in genomes of Chinese cabbage and cabbage.

    (a) ROD and PiHS values were normalized as z scores for B. rapa. A 200-kb sliding window with an increment of 5 kb was used to calculate these values; each point represents a value in a 200-kb window. The horizontal dashed lines show the empirical threshold of α = 0.01 (z = 2.33). (b) The distributions of normalized values for ROD, π and PiHS. The rightward tails of z (ROD) and z (PiHS) indicate the existence of highly differentiated regions in the BrH genome as compared to the BrNH genome that have been positively selected. The leftward tail of z (π) reflects the existence of genomic regions with low diversity in the BrH group. μ, mean; σ, sigma. (c) A Venn diagram showing unique and shared outlier regions detected by ROD, π and PiHS for B. rapa. (d) Normalized ROD and PiHS z scores for B. oleracea. (e) The distributions of normalized ROD, π and PiHS values for B. oleracea, with the same interpretations as in b. (f) A Venn diagram of the outlier regions detected by ROD, π and PiHS for B. oleracea.

  3. Parallel subgenomic selection among subgenomes from leaf-heading morphotypes of B. rapa and B. oleracea.
    Figure 3: Parallel subgenomic selection among subgenomes from leaf-heading morphotypes of B. rapa and B. oleracea.

    The LF, MF1 and MF2 subgenomes were constructed using diploid chromosomes from the Brassica ancestor tPCK9. The z scores of PiHS values were then plotted against the six B. rapa and B. oleracea subgenomes. The red vertical lines show the empirical threshold of α = 0.01 (z = 2.33). The red horizontal lines encompass regions of subgenomic parallel selection among the six subgenomes, and the light blue horizontal lines encompass loci that harbor candidate genes for the leaf-heading trait on one of the subgenomes. Blue arrows indicate subgenomic parallel selection among the three B. rapa (left) or B. oleracea (right) subgenomes, and green arrows indicate parallel or convergent selection between the B. rapa and B. oleracea subgenomes. The light blue circles show the location of retained candidate paralogs, and circles with red crosses denote gene copies lost in the corresponding subgenomes. Numerical suffixes to the gene names denote the location of the gene on the LF (1), MF1 (2) or MF2 (3) subgenome, respectively.

  4. Selection signals detected in the BrARF3.1 gene.
    Figure 4: Selection signals detected in the BrARF3.1 gene.

    (a) PiHS analysis identifies recent positive selection for the haplotype harboring BrARF3.1; the red star denotes the location of a core SNP in the genic region of BrARF3.1. (b) High FST and ROD values and low π values around the BrARF3.1 gene. Measures were calculated for individual SNPs located in the genomic region between the two vertical dashed lines in a. (c) Haplotypes extending from the core SNP located in the BrARF3.1 gene region for the B. rapa accessions. (d) Extent of haplotype conservation in the BrH and BrNH groups of B. rapa. EHH denotes extended haplotype homozygosity21. (e) BrARF3.1 gene model. A nonsynonymous mutation (G>C) was detected in coding exon 9, which causes an amino acid change from glutamine to histidine. (f) In a larger B. rapa collection of 806 accessions, the C genotype at the core SNP referred to in e strongly associates with the BrH trait.

Accession codes

Primary accessions

BioProject

Sequence Read Archive

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Author information

  1. These authors contributed equally to this work.

    • Feng Cheng,
    • Rifei Sun,
    • Xilin Hou,
    • Hongkun Zheng &
    • Fenglan Zhang

Affiliations

  1. Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Key Laboratory of Biology and Genetic Improvement of Horticultural Crops of the Ministry of Agriculture, Sino-Dutch Joint Laboratory of Horticultural Genomics, Beijing, China.

    • Feng Cheng,
    • Rifei Sun,
    • Yangyong Zhang,
    • Bo Liu,
    • Jianli Liang,
    • Mu Zhuang,
    • Yunxia Liu,
    • Xiaobo Wang,
    • Pingxia Li,
    • Yumei Liu,
    • Yan Wang,
    • Hui Wang,
    • Jie Deng,
    • Yongcui Liao,
    • Keyun Wei,
    • Xueming Zhang,
    • Lixia Fu,
    • Yunyan Hu,
    • Jisheng Liu,
    • Chengcheng Cai,
    • Shujiang Zhang,
    • Shifan Zhang,
    • Fei Li,
    • Hui Zhang,
    • Jifang Zhang,
    • Ning Guo,
    • Zhiyuan Liu,
    • Jin Liu,
    • Chao Sun,
    • Yuan Ma,
    • Haijiao Zhang,
    • Yang Cui,
    • Guusje Bonnema,
    • Jian Wu &
    • Xiaowu Wang
  2. State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Weigang, Nanjing, China.

    • Xilin Hou
  3. Biomarker Technologies Corporation, Beijing, China.

    • Hongkun Zheng &
    • Dongyuan Liu
  4. Beijing Academy of Agriculture and Forestry Science (BAAFS), Beijing Vegetable Research Center (BVRC), Beijing, China.

    • Fenglan Zhang
  5. Wageningen UR Plant Breeding, Wageningen University and Research Centre, Wageningen, the Netherlands.

    • Ke Lin,
    • Johan Bucher,
    • Ningwen Zhang,
    • Theo Borm &
    • Guusje Bonnema
  6. Department of Plant and Microbial Biology, University of California, Berkeley, Berkley, California, USA.

    • Micheal R Freeling

Contributions

Xiaowu Wang, F.C., G.B. and J.W. conceived and designed the experiments. J.W., G.B., Y.Z., M.Z., Yunxia Liu, Yumei Liu, T.B., X.Z., L.F., Y.H., Shujiang Zhang, Shifan Zhang, F.L., Hui Zhang, J.Z., N.G., Z.L., Jin Liu, Y.M., Haijiao Zhang, J.B. and Y.C. contributed materials. Y.W., H.W., N.Z., J.D., Y. Liao and K.W. contributed to phenotyping. N.Z. performed QTL analysis for the RIL populations. R.S., G.B., T.B., H. Zheng, X.H., F.Z., K.L., B.L., D.L., Xiaobo Wang, Jisheng Liu and C.S. contributed to resequencing. F.C., B.L., C.C. and T.B. analyzed the data and performed statistical analysis. P.L., J. Liang and L.F. performed the experiments. F.C. and Xiaowu Wang wrote the manuscript, with help from J. Liang, M.R.F., J.W., G.B., T.B. and P.L.

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The authors declare no competing financial interests.

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