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

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.

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Figure 1: Phylogenetic tree of 199 B. rapa and 119 B. oleracea accessions.
Figure 2: Genomic signatures of selection in genomes of Chinese cabbage and cabbage.
Figure 3: Parallel subgenomic selection among subgenomes from leaf-heading morphotypes of B. rapa and B. oleracea.
Figure 4: Selection signals detected in the BrARF3.1 gene.

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Acknowledgements

This study was funded by National Program on Key Basic Research Projects (973 Program: 2012CB113900 to Xiaowu Wang and F.C. and 2013CB127000 to Xiaowu Wang), the National High-Technology R&D Program of China (2012AA100201 to J.W.), a National Program on Key Research Project (2016YFD0100307) and the National Natural Science Foundation of China (NSFC grants 31301771 to F.C., 31272179 to J.W. and 31301784 to J. Liang). Research was supported by the Program for Strategic Scientific Alliances between China and the Netherlands, the Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, the Ministry of Agriculture, China, and the Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences. The authors gratefully acknowledge funding from the European Community under the Seventh Framework Programme for Research, Technological Development and Demonstration Activities, for Integrated Project NUE-CROPS FP7-CP-IP 222645. B. oleracea resequencing data and analyses were funded by a grant from the Technological Top Institute (TTI) Green Genetics, Rijk Zwaan and Bejo Zaden.

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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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Correspondence to Guusje Bonnema, Jian Wu or Xiaowu Wang.

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Cheng, F., Sun, R., Hou, X. et al. Subgenome parallel selection is associated with morphotype diversification and convergent crop domestication in Brassica rapa and Brassica oleracea. Nat Genet 48, 1218–1224 (2016). https://doi.org/10.1038/ng.3634

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