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Genome Sequence of the Cultivated Cotton Gossypium Arboreum

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Genome Sequence of the Cultivated Cotton Gossypium Arboreum ARTICLES OPEN Genome sequence of the cultivated cotton Gossypium arboreum Fuguang Li1,11, Guangyi Fan2,11, Kunbo Wang1,11, Fengming Sun2,11, Youlu Yuan1,11, Guoli Song1,11, Qin Li3,11, Zhiying Ma4,11, Cairui Lu1, Changsong Zou1, Wenbin Chen2, Xinming Liang2, Haihong Shang1, Weiqing Liu2, Chengcheng Shi2, Guanghui Xiao3, Caiyun Gou2, Wuwei Ye1, Xun Xu2, Xueyan Zhang1, Hengling Wei1, Zhifang Li1, Guiyin Zhang4, Junyi Wang2, Kun Liu1, Russell J Kohel5, Richard G Percy5, John Z Yu5, Yu-Xian Zhu3, Jun Wang2,6–10 & Shuxun Yu1 The complex allotetraploid nature of the cotton genome (AADD; 2n = 52) makes genetic, genomic and functional analyses extremely challenging. Here we sequenced and assembled the Gossypium arboreum (AA; 2n = 26) genome, a putative contributor of the A subgenome. A total of 193.6 Gb of clean sequence covering the genome by 112.6-fold was obtained by paired-end sequencing. We further anchored and oriented 90.4% of the assembly on 13 pseudochromosomes and found that 68.5% of the genome is occupied by repetitive DNA sequences. We predicted 41,330 protein-coding genes in G. arboreum. Two whole-genome duplications were shared by G. arboreum and Gossypium raimondii before speciation. Insertions of long terminal repeats in the past 5 million years are responsible for the twofold difference in the sizes of these genomes. Comparative transcriptome studies showed the key role of the nucleotide binding site (NBS)-encoding gene family in resistance to Verticillium dahliae and the involvement of ethylene in the development of cotton fiber cells. The genus Gossypium includes 46 diploid (2n = 2x = 26) and 5 well- evolution and species divergence. A highly homozygous single-seed established and 1 purported tetraploid (2n = 4x = 52) species1,2. It descendant, derived from 18 successive generations of self-fertilization, Nature America, Inc. All rights reserved. America, Inc. Nature 4 has been proposed that all diploid cotton species may have evolved of the cultivated diploid cotton Shixiya1 (SXY1) was used for DNA from a common ancestor that subsequently diversified to produce sequencing. Assembly of the G. arboreum genome and compara- 3 5,6 © 201 eight groups, including groups A–G and K . Allopolyploid cotton may tive studies with the genome of G. raimondii may provide new have appeared in the last 1–2 million years through hybridization and insights into the process of divergence among polyploid species7–9. subsequent polyploidization events between the A- and D-subgenome We believe that the G. arboreum genome offers a diploid reference for progenitors. All tetraploid cotton species came from interspecific the analysis of cotton agronomic traits, such as fiber quality10–13 and npg 14,15 hybridization between the A-genome species G. arboreum (A2) and disease resistance . 3 the D-genome species G. raimondii (D5) . The A-genome species are cultivated, whereas the D-genome species do not produce spinnable RESULTS fiber. Although G. arboreum (A2) and G. raimondii (D5) are the putative Genome sequencing and assembly donor species for the A and D chromosome groups, respectively, tetra- We sequenced and assembled the G. arboreum genome using the whole- ploid cotton species differ greatly with respect to plant morphology as genome shotgun approach. In brief, a total of 371.5 Gb of raw paired- well as economic characteristics, including fiber production, oil content end Illumina reads was generated by sequencing genome shotgun and disease resistance. Furthermore, G. arboreum (1,746 Mb/1C) has a libraries with different fragment lengths that ranged from 180 bp to genome size that is almost twice that of G. raimondii (885 Mb/1C)4. 40 kb (Supplementary Table 1). After filtering out low-quality reads, In the current study, assisted by a high-resolution genetic map, 193.6 Gb of high-quality sequence was obtained and used for the de novo we anchored and oriented 90.4% of the G. arboreum assembled assembly process (Supplementary Table 2). We next used 33,454 BAC scaffolds on 13 pseudochromosomes. This assembly was compared end sequences (16,727 pairs; approximately 1-fold physical coverage) to with that of G. raimondii to understand possible paths for genome improve the assembly. Over 90% of our BAC clones contained inserts of 1State Key Laboratory of Cotton Biology, Institute of Cotton Research of the Chinese Academy of Agricultural Sciences, Anyang, China. 2BGI-Shenzhen, Shenzhen, China. 3State Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China. 4Key Laboratory for Crop Germplasm Resources of Hebei, Agricultural University of Hebei, Baoding, China. 5Crop Germplasm Research Unit, Southern Plains Agricultural Research Center, US Department of Agriculture–Agricultural Research Service (USDA-ARS), College Station, Texas, USA. 6Department of Biology, University of Copenhagen, Copenhagen, Denmark. 7King Abdulaziz University, Jeddah, Saudi Arabia. 8Macau University of Science and Technology, Macau, China. 9Department of Medicine, University of Hong Kong, Hong Kong. 10State Key Laboratory of Pharmaceutical Biotechnology, University of Hong Kong, Hong Kong. 11These authors contributed equally to this work. Correspondence should be addressed to Y.-X.Z. ([email protected]), S.Y. ([email protected]) or Jun Wang ([email protected]). Received 17 June 2013; accepted 24 April 2014; published online 18 May 2014; doi:10.1038/ng.2987 NATURE GENETICS VOLUME 46 | NUMBER 6 | JUNE 2014 567 ARTICLES Table 1 Global statistics of G. arboreum genome assembly and Genome annotation annotation We performed genome annotation by combining results obtained from N50 Longest Size Percent of the ab initio prediction, homology search and transcriptome alignment. Category Number (kb) (Mb) (Mb) assembly As much as 68.5% of the G. arboreum genome was composed of vari- Total contigs 40,381 72.0 0.8 1,561 NA ous types of repeat sequences (Fig. 1a, Table 1 and Supplementary Total scaffolds 7,914 665.8 5.9 1,694 100 Table 7). We believe that this genome has the greatest amount of Anchored and oriented 3,740 790 5.9 1,532 90.4 repeat-containing sequences among sequenced eudicots19–24. Long scaffolds terminal repeat (LTR) retrotransposons accounted for 95.12% of all Genes annotated 41,330 105 6.2 repeat sequences. In comparison with the G. raimondii genome5, the miRNAs 431 0.05 <0.01 G. arboreum genome had noticeable proliferation of Gorge elements, rRNAs 10,464 1.2 0.07 tRNAs 2,289 0.2 0.01 whereas LTR Copia elements tended to accumulate in the G. raimondii 25 snRNAs 7,619 0.8 0.04 genome (Supplementary Table 8), as has been suggested previously . Repeat sequences NA 1,160 68.5 LTR retrotransposons in G. arboreum appeared to have inserted NA, not applicable or not analyzed. randomly along each chromosome (Fig. 1a), in a pattern substantially different from the ones observed for their insertion sites in soybean and potato, in which LTRs are clustered near the centromere and are ≥50,000 bp in length (Supplementary Fig. 1). In-depth analysis showed found less frequently near telomeres20,21. that all scaffolds were supported by multiple (>80) paired-end linkages A total of 41,330 protein-coding genes were identified in the (Supplementary Fig. 2). The number of scaffolds decreased in libraries G. arboreum genome, with an average transcript size of 2,533 bp (as with increasing insert size (>2,000 bp). Using K-mer distribution analysis, determined by GLEAN) and a mean of 4.6 exons per gene (Fig. 1b, the genome size was estimated to be 1,724 Mb (Supplementary Fig. 3), Table 1 and Supplementary Table 9). The genome encoded 431 micro- which is consistent with a previous report4. RNAs (miRNAs), 10,464 rRNAs, 2,289 tRNAs and 7,619 small nuclear Our final assembly, performed with SOAPdenovo16,17, showed RNAs (snRNAs) (Table 1). Among the annotated genes, 85.64% that the G. arboreum genome is 1,694 Mb in total length (Table 1). encoded proteins that showed homology to proteins in the TrEMBL Ninety percent of the assembly fell into 2,724 superscaffolds that database, and 68.71% were identified in InterPro (Supplementary were >148 kb in length, with the largest scaffold being 5.9 Mb. N50 Table 10). Over 96% of predicted coding sequences were supported by (the size above which 50% of the total length of the sequence assem- transcriptome sequencing data (Fig. 1c and Supplementary Table 9), bly can be found) for the contigs and scaffolds was 72 kb and 666 kb, which indicated high accuracy of G. arboreum gene predictions from respectively. Data quality was assessed by comparison with Sanger the genome sequence. Orthologous clustering of the G. arboreum sequencing–derived G. arboreum sequences and by mapping available proteome with 3 closely related plant genomes identified 11,699 gene ESTs to the assembly. Nineteen of the twenty completely sequenced families in common, with 739 gene families that were present specifi- G. arboreum BAC clones available from GenBank were recovered in cally in G. arboreum (Supplementary Fig. 7). our assembly, with >98% sequence identity (Supplementary Table 3). 120 Nature America, Inc. All rights reserved. America, Inc. Nature Of the 55,894 Sanger sequencing–derived G. arboreum ESTs (>200 bp Mb Chr. 1 4 80 Chr. 13 0 40 in length) available from NCBI, 96.37% were detected in our assembly 40 a 80 (Supplementary Table 4). Using a restriction site–associated DNA 120 0 © 201 (RAD) linkage map that we constructed during the current study 120 b 0 Chr. 2 40 based on 24,569 codominant SNP markers, 1,532 Mb or 90.4% of 80 c Chr. 12 d 80 the assembled genome was anchored and oriented on 13 pseudo- 40 0 npg e chromosomes (Fig. 1, Supplementary Fig. 4 and Supplementary Chr.
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