. 2014 May 23:5:3930.

doi: 10.1038/ncomms4930.

The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes

Shengyi Liu¹, Yumei Liu², Xinhua Yang³, Chaobo Tong¹, David Edwards⁴, Isobel A P Parkin⁵, Meixia Zhao⁶, Jianxin Ma⁷, Jingyin Yu⁸, Shunmou Huang⁸, Xiyin Wang⁹, Junyi Wang¹⁰, Kun Lu¹¹, Zhiyuan Fang¹², Ian Bancroft¹³, Tae-Jin Yang¹⁴, Qiong Hu⁸, Xinfa Wang⁸, Zhen Yue¹⁰, Haojie Li¹⁵, Linfeng Yang¹⁰, Jian Wu¹², Qing Zhou¹⁰, Wanxin Wang¹², Graham J King¹⁶, J Chris Pires¹⁷, Changxin Lu¹⁰, Zhangyan Wu¹⁰, Perumal Sampath¹⁴, Zhuo Wang¹⁰, Hui Guo¹⁸, Shengkai Pan¹⁰, Limei Yang¹², Jiumeng Min¹⁰, Dong Zhang¹⁸, Dianchuan Jin¹⁹, Wanshun Li¹⁰, Harry Belcram²⁰, Jinxing Tu²¹, Mei Guan²², Cunkou Qi²³, Dezhi Du²⁴, Jiana Li¹¹, Liangcai Jiang¹⁵, Jacqueline Batley²⁵, Andrew G Sharpe²⁶, Beom-Seok Park²⁷, Pradeep Ruperao²⁸, Feng Cheng¹², Nomar Espinosa Waminal²⁹, Yin Huang¹⁰, Caihua Dong⁸, Li Wang¹⁹, Jingping Li¹⁸, Zhiyong Hu⁸, Mu Zhuang¹², Yi Huang⁸, Junyan Huang⁸, Jiaqin Shi⁸, Desheng Mei⁸, Jing Liu⁸, Tae-Ho Lee¹⁸, Jinpeng Wang¹⁹, Huizhe Jin¹⁸, Zaiyun Li²¹, Xun Li²², Jiefu Zhang²³, Lu Xiao²⁴, Yongming Zhou²¹, Zhongsong Liu²², Xuequn Liu³⁰, Rui Qin³⁰, Xu Tang¹⁸, Wenbin Liu¹⁰, Yupeng Wang¹⁸, Yangyong Zhang¹², Jonghoon Lee¹⁴, Hyun Hee Kim³¹, France Denoeud³², Xun Xu¹⁰, Xinming Liang¹⁰, Wei Hua⁸, Xiaowu Wang¹², Jun Wang³³, Boulos Chalhoub²⁰, Andrew H Paterson¹⁸

Affiliations

¹ 1] The Key Laboratory of Biology and Genetic Improvement of Oil Crops, The Ministry of Agriculture of PRC, Oil Crops Research Institute, Chinese Academy of Agricultural Sciences, Wuhan 430062, China [2].
² 1] The Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, The Ministry of Agriculture, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 10081, China [2].
³ 1] Beijing Genome Institute-Shenzhen, Shenzhen 518083, China [2].
⁴ 1] Australian Centre for Plant Functional Genomics, School of Agriculture and Food Sciences, University of Queensland, Brisbane, Queensland 4072, Australia [2].
⁵ 1] Agriculture and Agri-Food Canada, Saskatoon, Saskatchewan, Canada S7N OX2 [2].
⁶ 1] The Key Laboratory of Biology and Genetic Improvement of Oil Crops, The Ministry of Agriculture of PRC, Oil Crops Research Institute, Chinese Academy of Agricultural Sciences, Wuhan 430062, China [2] Department of Agronomy, Purdue University, WSLR Building B018, West Lafayette, Indiana 47907, USA.
⁷ Department of Agronomy, Purdue University, WSLR Building B018, West Lafayette, Indiana 47907, USA.
⁸ The Key Laboratory of Biology and Genetic Improvement of Oil Crops, The Ministry of Agriculture of PRC, Oil Crops Research Institute, Chinese Academy of Agricultural Sciences, Wuhan 430062, China.
⁹ 1] Plant Genome Mapping Laboratory, University of Georgia, Athens, Georgia 30605, USA [2] Center for Genomics and Computational Biology, School of Life Sciences, and School of Sciences, Hebei United University, Tangshan 063000, China.
¹⁰ Beijing Genome Institute-Shenzhen, Shenzhen 518083, China.
¹¹ College of Agronomy and Biotechnology, Southwest University, BeiBei District, Chongqing 400715, China.
¹² The Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, The Ministry of Agriculture, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 10081, China.
¹³ Centre for Novel Agricultural Products (CNAP), Department of Biology, University of York, Wentworth Way, Heslington, York YO10 5DD, UK.
¹⁴ Department of Plant Sciences, Plant Genomics and Breeding Institute and Research Institute for Agriculture and Life Sciences, College of Agriculture & Life Sciences, Seoul National University, Seoul 151-921, Republic of Korea.
¹⁵ Sichuan Academy of Agricultural Sciences, Chengdu 610066, China.
¹⁶ Southern Cross Plant Science, Southern Cross University, Lismore, New South Wales 2480, Australia.
¹⁷ Bond Life Sciences Center, University of Missouri, Columbia, Missouri 65211-7310, USA.
¹⁸ Plant Genome Mapping Laboratory, University of Georgia, Athens, Georgia 30605, USA.
¹⁹ Center for Genomics and Computational Biology, School of Life Sciences, and School of Sciences, Hebei United University, Tangshan 063000, China.
²⁰ Organization and Evolution of Plant Genomes, Unité de Recherche en Génomique Végétale, Unité Mixte de Recherche 1165 (Institut National de Recherche Agronomique, Centre National de la Recherche Scientifique, Université Evry Val d'Essonne), Evry 91057, France.
²¹ National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan 430070, China.
²² College of Agronomy, Hunan Agricultural University, Changsha 410128, China.
²³ Jiangsu Academy of Agricultural Sciences, Nanjing 210014, China.
²⁴ Qinghai Academy of Agriculture and Forestry Sciences, National Key Laboratory Breeding Base for Innovation and Utilization of Plateau Crop Germplasm, Xining 810016, China.
²⁵ Australian Research Council Centre of Excellence for Integrative Legume Research, University of Queensland, Brisbane, Queensland 4072, Australia.
²⁶ National Research Council Canada, Saskatoon, Saskatchewan, Canada S7N 0W9.
²⁷ The Agricultural Genome Center, National Academy of Agricultural Science, RDA, 126 Suin-Ro, Suwon 441-707, Republic of Korea.
²⁸ Australian Centre for Plant Functional Genomics, School of Agriculture and Food Sciences, University of Queensland, Brisbane, Queensland 4072, Australia.
²⁹ 1] Department of Plant Sciences, Plant Genomics and Breeding Institute and Research Institute for Agriculture and Life Sciences, College of Agriculture & Life Sciences, Seoul National University, Seoul 151-921, Republic of Korea [2] Department of Life Science, Plant Biotechnology Institute, Sahmyook University, Seoul 139-742, Republic of Korea.
³⁰ School of Life Sciences, South-Central University for Nationality, Wuhan 430074, China.
³¹ Department of Life Science, Plant Biotechnology Institute, Sahmyook University, Seoul 139-742, Republic of Korea.
³² 1] Commissariat à l'Energie Atomique (CEA), Genoscope, Institut de Génomique, BP5706 Evry 91057, France [2] Centre National de Recherche Scientifique (CNRS), Université d'Evry, UMR 8030, CP5706, Evry 91057, France.
³³ 1] Beijing Genome Institute-Shenzhen, Shenzhen 518083, China [2] Department of Biology, University of Copenhagen, Ole Maaløes Vej 5, 2200, Copenhagen, Denmark [3] King Abdulaziz University, Jeddah, 21589, Saudi Arabia [4] Department of Medicine and State Key Laboratory of Pharmaceutical Biotechnology, University of Hong Kong, 21 Sassoon Road, Hong Kong.

PMID: 24852848
PMCID: PMC4279128
DOI: 10.1038/ncomms4930

Free PMC article

The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes

Shengyi Liu et al. Nat Commun. 2014.

Free PMC article

. 2014 May 23:5:3930.

doi: 10.1038/ncomms4930.

Authors

Affiliations

¹ 1] The Key Laboratory of Biology and Genetic Improvement of Oil Crops, The Ministry of Agriculture of PRC, Oil Crops Research Institute, Chinese Academy of Agricultural Sciences, Wuhan 430062, China [2].
² 1] The Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, The Ministry of Agriculture, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 10081, China [2].
³ 1] Beijing Genome Institute-Shenzhen, Shenzhen 518083, China [2].
⁴ 1] Australian Centre for Plant Functional Genomics, School of Agriculture and Food Sciences, University of Queensland, Brisbane, Queensland 4072, Australia [2].
⁵ 1] Agriculture and Agri-Food Canada, Saskatoon, Saskatchewan, Canada S7N OX2 [2].
⁶ 1] The Key Laboratory of Biology and Genetic Improvement of Oil Crops, The Ministry of Agriculture of PRC, Oil Crops Research Institute, Chinese Academy of Agricultural Sciences, Wuhan 430062, China [2] Department of Agronomy, Purdue University, WSLR Building B018, West Lafayette, Indiana 47907, USA.
⁷ Department of Agronomy, Purdue University, WSLR Building B018, West Lafayette, Indiana 47907, USA.
⁸ The Key Laboratory of Biology and Genetic Improvement of Oil Crops, The Ministry of Agriculture of PRC, Oil Crops Research Institute, Chinese Academy of Agricultural Sciences, Wuhan 430062, China.
⁹ 1] Plant Genome Mapping Laboratory, University of Georgia, Athens, Georgia 30605, USA [2] Center for Genomics and Computational Biology, School of Life Sciences, and School of Sciences, Hebei United University, Tangshan 063000, China.
¹⁰ Beijing Genome Institute-Shenzhen, Shenzhen 518083, China.
¹¹ College of Agronomy and Biotechnology, Southwest University, BeiBei District, Chongqing 400715, China.
¹² The Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, The Ministry of Agriculture, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 10081, China.
¹³ Centre for Novel Agricultural Products (CNAP), Department of Biology, University of York, Wentworth Way, Heslington, York YO10 5DD, UK.
¹⁴ Department of Plant Sciences, Plant Genomics and Breeding Institute and Research Institute for Agriculture and Life Sciences, College of Agriculture & Life Sciences, Seoul National University, Seoul 151-921, Republic of Korea.
¹⁵ Sichuan Academy of Agricultural Sciences, Chengdu 610066, China.
¹⁶ Southern Cross Plant Science, Southern Cross University, Lismore, New South Wales 2480, Australia.
¹⁷ Bond Life Sciences Center, University of Missouri, Columbia, Missouri 65211-7310, USA.
¹⁸ Plant Genome Mapping Laboratory, University of Georgia, Athens, Georgia 30605, USA.
¹⁹ Center for Genomics and Computational Biology, School of Life Sciences, and School of Sciences, Hebei United University, Tangshan 063000, China.
²⁰ Organization and Evolution of Plant Genomes, Unité de Recherche en Génomique Végétale, Unité Mixte de Recherche 1165 (Institut National de Recherche Agronomique, Centre National de la Recherche Scientifique, Université Evry Val d'Essonne), Evry 91057, France.
²¹ National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan 430070, China.
²² College of Agronomy, Hunan Agricultural University, Changsha 410128, China.
²³ Jiangsu Academy of Agricultural Sciences, Nanjing 210014, China.
²⁴ Qinghai Academy of Agriculture and Forestry Sciences, National Key Laboratory Breeding Base for Innovation and Utilization of Plateau Crop Germplasm, Xining 810016, China.
²⁵ Australian Research Council Centre of Excellence for Integrative Legume Research, University of Queensland, Brisbane, Queensland 4072, Australia.
²⁶ National Research Council Canada, Saskatoon, Saskatchewan, Canada S7N 0W9.
²⁷ The Agricultural Genome Center, National Academy of Agricultural Science, RDA, 126 Suin-Ro, Suwon 441-707, Republic of Korea.
²⁸ Australian Centre for Plant Functional Genomics, School of Agriculture and Food Sciences, University of Queensland, Brisbane, Queensland 4072, Australia.
²⁹ 1] Department of Plant Sciences, Plant Genomics and Breeding Institute and Research Institute for Agriculture and Life Sciences, College of Agriculture & Life Sciences, Seoul National University, Seoul 151-921, Republic of Korea [2] Department of Life Science, Plant Biotechnology Institute, Sahmyook University, Seoul 139-742, Republic of Korea.
³⁰ School of Life Sciences, South-Central University for Nationality, Wuhan 430074, China.
³¹ Department of Life Science, Plant Biotechnology Institute, Sahmyook University, Seoul 139-742, Republic of Korea.
³² 1] Commissariat à l'Energie Atomique (CEA), Genoscope, Institut de Génomique, BP5706 Evry 91057, France [2] Centre National de Recherche Scientifique (CNRS), Université d'Evry, UMR 8030, CP5706, Evry 91057, France.
³³ 1] Beijing Genome Institute-Shenzhen, Shenzhen 518083, China [2] Department of Biology, University of Copenhagen, Ole Maaløes Vej 5, 2200, Copenhagen, Denmark [3] King Abdulaziz University, Jeddah, 21589, Saudi Arabia [4] Department of Medicine and State Key Laboratory of Pharmaceutical Biotechnology, University of Hong Kong, 21 Sassoon Road, Hong Kong.

PMID: 24852848
PMCID: PMC4279128
DOI: 10.1038/ncomms4930

Abstract

Polyploidization has provided much genetic variation for plant adaptive evolution, but the mechanisms by which the molecular evolution of polyploid genomes establishes genetic architecture underlying species differentiation are unclear. Brassica is an ideal model to increase knowledge of polyploid evolution. Here we describe a draft genome sequence of Brassica oleracea, comparing it with that of its sister species B. rapa to reveal numerous chromosome rearrangements and asymmetrical gene loss in duplicated genomic blocks, asymmetrical amplification of transposable elements, differential gene co-retention for specific pathways and variation in gene expression, including alternative splicing, among a large number of paralogous and orthologous genes. Genes related to the production of anticancer phytochemicals and morphological variations illustrate consequences of genome duplication and gene divergence, imparting biochemical and morphological variation to B. oleracea. This study provides insights into Brassica genome evolution and will underpin research into the many important crops in this genus.

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Figures

**Figure 1. Genomic structure and gene retention rates in syntenic regions of *B. oleracea* and *B. rapa*.**
(a) Segmental colinearity of the genomes of *B. oleracea*, *B. rapa* and *A. thaliana*. Syntenic blocks are defined and labelled from A to X (coloured) previously reported in *A. thaliana*. (b) Time estimate of WGD and subsequent two *Brassica* species divergence. (c) Pattern of retention/loss of orthologous genes on each set of three subgenomic (LF, MF1 and MF2) blocks of *B. oleracea* and *B. rapa* corresponding to *A. thaliana* A to X blocks. The x axis denotes the physical position of each *A. thaliana* gene locus. The y axis denotes the proportion of orthologous genes retained in the *B. oleracea* and *B. rapa* subgenomic blocks around each *A. thaliana* gene, where 500 genes flanking each side of a certain gene locus were analysed, giving a total window size of 1,001 genes.

Figure 2. TE comparison analyses in *B. oleracea* and *B. rapa.*
(a) TE copy number and total length in each assembly and *B. oleracea–B. rapa* syntenic blocks. (b) The number of intact LTR (*Copia*-like and *Gypsy*-like) birthed at different times (million years ago, MYA) in the syntenic regions of *B. oleracea* and *B. rapa*. (c) The comparison of TE distribution and composition in *B. oleracea–B. rapa* syntenic blocks along *B. oleracea* chromosomes. We divided *B. oleracea–B. rapa* syntenic region into non-overlapping sliding 200 kb windows to compare TE contents. For each window, the ratio log₁₀(*B. oleracea/B. rapa*) was calculated for total syntenic block length (blue line), LTR length (purple line), gene length (yellow point), exons length (red point) and intron length (green point). If *B. oleracea* > *B. rapa* in absolute length of TE composition in a compared window, the dot or line is above the line y=0. The corresponding *B. rapa* chromosome segments along *B. oleracea* C08 were indicated by coloured bars. All other *B. oleracea* chromosomes are showed in Supplementary Fig. 31. (d) Phylogeny of the Copia-like elements as an example of LTR-RTs of the syntenic regions in *B. rapa* and *B. oleracea*. The neighbor-joining (NJ) trees were generated based on the conserved RT domain nucleotide sequences using the Kimura two-parameter method in MEGA4 (ref. 69).

**Figure 3. The duplicated genes derived from tandem duplication and whole-genome duplications in *Brassica* genomes.**
(a) A Venn diagram showing shared and specific tandem duplication events in *A. thaliana*, *B. rapa* and *B. oleracea*. (b,c) Distribution of tandem genes and WGT/WGD-derived paralogues in the KEGG pathway maps in *B. oleracea* (bol), *B. rapa* (bra) and *A. thaliana* (ath). For each KEGG pathway map, the proportion of the number of duplicated genes or paralogues to the total genes was calculated (x axis) and the number of maps whose tandem gene proportion fell in a range was shown on the y axis. (d) Oxidative phosphorylation pathway enriched by WGT-derived paralogous genes in the *Brassica* genomes. The gene copy number for each KO enzyme in *B. oleracea*, *B. rapa* and *A. thaliana* were shown (dash-connected) under the KO enzyme number.

**Figure 4. Divergence of *Brassica* paralogous and orthologous genes in *B. oleracea* and *B. rapa*.**
(a) Genome-wide gene conversion in *B. oleracea*. The conversion in *B. rapa* is showed in Supplementary Fig. 64. (b) The ratio of differentially expressed duplicated gene pairs derived from different duplications: alpha whole-genome duplication (α-WGD), *Brassiceae*-lineage WGT, tandem duplication (TD). Bol, *B. oleracea*; Bra, *B. rapa*. C: callus; R: root; St: stem; L: leaf; F: flower; Si: silique. The differentially expressed duplicated gene pairs were defined as fold change >2 and false discovery rate (FDR) <0.05 or gene pair where expression was detected for only one gene within gene pairs (FDR <0.05). (c) Box and whisker plots for differentiated expression for three subgenomes (LF, MF1 and MF2) in flower tissue of *B. oleracea* and *B. rapa*. For the other tissues, see Supplementary Fig. 67. (d) The duplicated gene pairs belonging to transcription factors (TFs) and its related GO terms contain a significantly lower ratio of differentially expressed duplicated gene pairs than the average at the genome-wide level in leaf (values given) and other tissues (values not presented) (Supplementary Table 45). (e) The GO terms (left) in which the duplicated gene pairs contain a significantly higher ratio of differentially expressed duplicated gene pairs than the average ratio at the genome-wide level in leaf and other tissues (Supplementary Table 46). Values from one tissue were presented and the other tissues were indicated with abbreviated letters to the right if expression in these tissues is significantly higher. (f) Expression variation caused by divergence (either different variants or differential expression of the same variants) of alternative splicing (AS) variants in WGT paralogous gene pairs with identical numbers of exons and in Bol–Bra orthologous gene pairs. IRES denotes types of intron retention and exon skipping.

**Figure 5. Whole-genome-wide comparison of genes involved in glucosinolate metabolism pathways in *B. oleracea* and its relatives.**
(a) Aliphatic and indolic GSL biosynthesis and catabolism pathways in *A. thaliana*, *B. oleracea* and *B. rapa*. The copy number of GSL biosynthetic genes in *A. thaliana*, *B. rapa* and *B. oleracea* are listed in square brackets, respectively. Potential anticancer substances/precursors are highlighted in blue bold. Two important amino acid chain elongation and side-chain modification loci *MAMs* and *AOP2* are highlighted in red bold, within the number in the green bracket representing the number of non-functional genes. (b,c) The neighbour-joining (NJ) trees of MAM and AOP genes were generated based on the aligned coding sequences and 100 bootstrap repeats. The silenced genes are indicated by red hollow circle, expressed functional genes are represented by red solid disc and green rectangle. In *A. thaliana* ecotype Columbia there are just MAM1 and MAM3. (d) Three *B. oleracea AOP2* loci among which are one functional *AOP2* and two mutated *AOP2*. 1MOI3M: 1-methoxyindol-3-ylmethyl GSL; 1OHI3M: 1-hydroxyindol-3-ylmethyl GSL; 3MSOP: 3-methylsulfinylpropyl GSL; 3MTP: 3-methylthiopropyl GSL; 3PREY: 2-Propenyl GSL; 4BTEY: 3-butenyl GSL; 4MOI3M: 4-methoxyindol-3-ylmethyl GSL; 4OHB, 4-hydroxybutyl GSL; 4OHI3M: 4-hydroxyindol-3-ylmethyl GSL; 4MSOB: 4-methylsulfinylbutyl GSL; 4MTB, 4-methylthiobutyl GSL; AITC: allyl isothiocyanate; I3C: indole-3-carbinol; I3M: indolyl-3-methyl GSL; DIM: 3,3′-diindolymethane; MAM: methylthioalkylmalate; AOP: 2-oxoglutarate-dependent dioxygenase.

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References

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The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes

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The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes

Authors

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Abstract

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