Sub genome anchored physical frameworks of the allotetraploid Upland cotton (Gossypium hirsutum L.) genome, and an approach toward reference-grade assemblies of polyploids

Saski, Christopher A.; Scheffler, Brian E.; Hulse-Kemp, Amanda M.; Liu, Bo; Song, Qingxin; Ando, Atsumi; Stelly, David M.; Scheffler, Jodi A.; Grimwood, Jane; Jones, Don C.; Peterson, Daniel G.; Schmutz, Jeremy; Chen, Z. Jeffery

doi:10.1038/s41598-017-14885-w

Title: Sub genome anchored physical frameworks of the allotetraploid Upland cotton (Gossypium hirsutum L.) genome, and an approach toward reference-grade assemblies of polyploids

Journal Article · Fri Nov 10 00:00:00 EST 2017 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-017-14885-w· OSTI ID:1543775

Saski, Christopher A. ^[1];

^[2]; Hulse-Kemp, Amanda M. ^[3]; Liu, Bo ^[3]; Song, Qingxin ^[4]; Ando, Atsumi ^[4];

^[3]; Scheffler, Jodi A. ^[5]; Grimwood, Jane ^[6]; Jones, Don C. ^[7]; Peterson, Daniel G. ^[8]; Schmutz, Jeremy ^[6];

^[4]

Clemson Univ., SC (United States)
US Dept. of Agriculture-Agricultural Research Service (USDA-ARS), Stoneville, MS (United States). Genomics and Bioinformatics Research Unit
Texas A & M Univ., College Station, TX (United States)
Univ. of Texas, Austin, TX (United States)
US Dept. of Agriculture-Agricultural Research Service (USDA-ARS), Stoneville, MS (United States). Crop Genetics Research Unit
HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States)
Cotton Inc., Cary, NC (United States). Agriculture and Environmental Research
Mississippi State Univ., Mississippi State, MS (United States)

Like those of many agricultural crops, the cultivated cotton is an allotetraploid and has a large genome (~2.5 gigabase pairs). The two sub genomes, A and D, are highly similar but unequally sized and repeat-rich, which pose significant challenges for accurate genome reconstruction using standard approaches. Here we report the development of BAC libraries, sub genome specific physical maps, and a new-generation sequencing approach that will lead to a reference-grade genome assembly for Upland cotton. Three BAC libraries were constructed, fingerprinted, and integrated with BAC-end sequences (BES) to produce a de novo whole-genome physical map. The BAC map was partitioned by sub genomes through alignment to the diploid progenitor D-genome reference sequence with densely spaced BES anchor points and computational filtering. The physical maps were validated with FISH and genetic mapping of SNP markers derived from BES. Two pairs of homeologous chromosomes, A11/D11 and A12/D12, were used to assess multiplex sequencing approaches for completeness and scalability. The results represent the first sub genome anchored physical maps of Upland cotton, and a new-generation approach to the whole-genome sequencing, which will lead to the reference-grade assembly of allopolyploid cotton and serve as a general strategy for sequencing other polyploid species.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Organization:: USDOE Office of Science (SC); National Science Foundation (NSF)

OSTI ID:: 1543775

Journal Information:: Scientific Reports, Vol. 7, Issue 1; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 18 works

Citation information provided by
Web of Science

References (58)

A genetically anchored physical framework for Theobroma cacao cv. Matina 1-6 Saski, Christopher A.; Feltus, Frank A.; Staton, Margaret E. BMC Genomics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2164-12-413	journal	August 2011
Microscopy and Bioinformatic Analyses of Lipid Metabolism Implicate a Sporophytic Signaling Network Supporting Pollen Development in Arabidopsis Wang, Yixing; Wu, Hong; Yang, Ming Molecular Plant, Vol. 1, Issue 4 https://doi.org/10.1093/mp/ssn027	journal	July 2008
Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome Chalhoub, B.; Denoeud, F.; Liu, S. Science, Vol. 345, Issue 6199 https://doi.org/10.1126/science.1253435	journal	August 2014
Development of a 63K SNP Array for Cotton and High-Density Mapping of Intraspecific and Interspecific Populations of Gossypium spp. Hulse-Kemp, A. M.; Lemm, J.; Plieske, J. G3: Genes\|Genomes\|Genetics, Vol. 5, Issue 6 https://doi.org/10.1534/g3.115.018416	journal	April 2015
Five-Color-Based High-Information-Content Fingerprinting of Bacterial Artificial Chromosome Clones Using Type IIS Restriction Endonucleases Ding, Y.; Johnson, M. D.; Chen, W. Q. Genomics, Vol. 74, Issue 2 https://doi.org/10.1006/geno.2001.6547	journal	June 2001
Duplicate gene evolution, homoeologous recombination, and transcriptome characterization in allopolyploid cotton Flagel, Lex E.; Wendel, Jonathan F.; Udall, Joshua A. BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-302	journal	January 2012
A comprehensive meta QTL analysis for fiber quality, yield, yield related and morphological traits, drought tolerance, and disease resistance in tetraploid cotton Said, Joseph I.; Lin, Zhongxu; Zhang, Xianlong BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-776	journal	January 2013
The B73 Maize Genome: Complexity, Diversity, and Dynamics Schnable, P. S.; Ware, D.; Fulton, R. S. Science, Vol. 326, Issue 5956, p. 1112-1115 https://doi.org/10.1126/science.1178534	journal	November 2009
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
BAC Sequencing Using Pooled Methods Saski, Christopher A.; Feltus, F. Alex; Parida, Laxmi Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-1652-8_3	book	September 2014
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
An Improved Approach for Construction of Bacterial Artificial Chromosome Libraries Osoegawa, Kazutoyo; Woon, Peng Yeong; Zhao, Baohui Genomics, Vol. 52, Issue 1 https://doi.org/10.1006/geno.1998.5423	journal	August 1998
A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome Mayer, K. F. X.; Rogers, J.; Dole el, J. Science, Vol. 345, Issue 6194 https://doi.org/10.1126/science.1251788	journal	July 2014
Chromosome structural changes in diploid and tetraploid A genomes of Gossypium Desai, Aparna; Chee, Peng W.; Rong, Junkang Genome, Vol. 49, Issue 4 https://doi.org/10.1139/g05-116	journal	April 2006
Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres Paterson, Andrew H.; Wendel, Jonathan F.; Gundlach, Heidrun Nature, Vol. 492, Issue 7429 https://doi.org/10.1038/nature11798	journal	December 2012
Estimation of the Nuclear DNA Content of Gossypium Species Hendrix, B. Annals of Botany, Vol. 95, Issue 5 https://doi.org/10.1093/aob/mci078	journal	February 2005
The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution Verde, Ignazio; Abbott, Albert G.; Scalabrin, Simone Nature Genetics, Vol. 45, Issue 5 https://doi.org/10.1038/ng.2586	journal	March 2013
De novo assembly of human genomes with massively parallel short read sequencing Li, R.; Zhu, H.; Ruan, J. Genome Research, Vol. 20, Issue 2 https://doi.org/10.1101/gr.097261.109	journal	December 2009
The genome sequence of Sea-Island cotton (Gossypium barbadense) provides insights into the allopolyploidization and development of superior spinnable fibres Yuan, Daojun; Tang, Zhonghui; Wang, Maojun Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep17662	journal	December 2015
Construction and Identification of Bacterial Artificial Chromosome Library for 0-613-2R in Upland Cotton Yin, Jian-Mei; Guo, Wang-Zhen; Zhang, Tian-Zhen Journal of Integrative Plant Biology, Vol. 48, Issue 2 https://doi.org/10.1111/j.1744-7909.2006.00169.x-i1	journal	February 2006
Development of molecular markers for genetic male sterility in Gossypium hirsutum Feng, Xuehui; Keim, Don; Wanjugi, Humphrey Molecular Breeding, Vol. 35, Issue 6 https://doi.org/10.1007/s11032-015-0336-z	journal	June 2015
Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement Zhang, Tianzhen; Hu, Yan; Jiang, Wenkai Nature Biotechnology, Vol. 33, Issue 5 https://doi.org/10.1038/nbt.3207	journal	April 2015
The tobacco genome sequence and its comparison with those of tomato and potato Sierro, Nicolas; Battey, James N. D.; Ouadi, Sonia Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4833	journal	May 2014
Genome sequence of the cultivated cotton Gossypium arboreum Li, Fuguang; Fan, Guangyi; Wang, Kunbo Nature Genetics, Vol. 46, Issue 6 https://doi.org/10.1038/ng.2987	journal	May 2014
Genome sequence of the palaeopolyploid soybean Schmutz, Jeremy; Cannon, Steven B.; Schlueter, Jessica Nature, Vol. 463, Issue 7278 https://doi.org/10.1038/nature08670	journal	January 2010
Cytochrome b5 Reductase Encoded by CBR1 Is Essential for a Functional Male Gametophyte in Arabidopsis Wayne, Laura L.; Wallis, James G.; Kumar, Rajesh The Plant Cell, Vol. 25, Issue 8 https://doi.org/10.1105/tpc.113.113324	journal	August 2013
Assembly algorithms for next-generation sequencing data Miller, Jason R.; Koren, Sergey; Sutton, Granger Genomics, Vol. 95, Issue 6 https://doi.org/10.1016/j.ygeno.2010.03.001	journal	June 2010
Genome sequence of cultivated Upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution Li, Fuguang; Fan, Guangyi; Lu, Cairui Nature Biotechnology, Vol. 33, Issue 5 https://doi.org/10.1038/nbt.3208	journal	April 2015
Construction of a bacterial artificial chromosome library for Gossypium herbaceum var. africanum Gao, HaiYan; Wang, XingFen; Liu, Fang Chinese Science Bulletin, Vol. 58, Issue 26 https://doi.org/10.1007/s11434-013-5864-5	journal	June 2013
Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss Schnable, J. C.; Springer, N. M.; Freeling, M. Proceedings of the National Academy of Sciences, Vol. 108, Issue 10 https://doi.org/10.1073/pnas.1101368108	journal	February 2011
Allele-Specific, Bidirectional Silencing of an Alcohol Dehydrogenase Gene in Different Organs of Interspecific Diploid Cotton Hybrids Adams, Keith L.; Wendel, Jonathan F. Genetics, Vol. 171, Issue 4 https://doi.org/10.1534/genetics.105.047357	journal	September 2005
Molecular mapping of genic male-sterile genes ms ₁₅ , ms ₅ and ms ₆ in tetraploid cotton Chen, D.; Ding, Y.; Guo, W. Plant Breeding, Vol. 128, Issue 2 https://doi.org/10.1111/j.1439-0523.2008.01562.x	journal	April 2009
The draft genome of a diploid cotton Gossypium raimondii Wang, Kunbo; Wang, Zhiwen; Li, Fuguang Nature Genetics, Vol. 44, Issue 10 https://doi.org/10.1038/ng.2371	journal	August 2012
Functional analysis of Hsp70 superfamily proteins of rice (Oryza sativa) Sarkar, Neelam K.; Kundnani, Preeti; Grover, Anil Cell Stress and Chaperones, Vol. 18, Issue 4 https://doi.org/10.1007/s12192-012-0395-6	journal	December 2012
Serine/threonine protein phosphatases: Multi-purpose enzymes in control of defense mechanisms Bajsa, Joanna; Pan, Zhiqiang; Duke, Stephen O. Plant Signaling & Behavior, Vol. 6, Issue 12 https://doi.org/10.4161/psb.6.12.18146	journal	December 2011
Genetic Diversity in Gossypium hirsutum and the Origin of Upland Cotton Wendel, Jonathan F.; Brubaker, Curt L.; Percival, A. Edward American Journal of Botany, Vol. 79, Issue 11 https://doi.org/10.2307/2445058	journal	November 1992
Dissecting the genome of the polyploid crop oilseed rape by transcriptome sequencing Bancroft, Ian; Morgan, Colin; Fraser, Fiona Nature Biotechnology, Vol. 29, Issue 8 https://doi.org/10.1038/nbt.1926	journal	July 2011
Consed: A Graphical Tool for Sequence Finishing Gordon, David; Abajian, Chris; Green, Phil Genome Research, Vol. 8, Issue 3 https://doi.org/10.1101/gr.8.3.195	journal	March 1998
Plant disease resistance genes: Current status and future directions Gururani, Mayank Anand; Venkatesh, Jelli; Upadhyaya, Chandrama Prakash Physiological and Molecular Plant Pathology, Vol. 78 https://doi.org/10.1016/j.pmpp.2012.01.002	journal	April 2012
ABySS: A parallel assembler for short read sequence data Simpson, J. T.; Wong, K.; Jackman, S. D. Genome Research, Vol. 19, Issue 6 https://doi.org/10.1101/gr.089532.108	journal	February 2009
The coffee genome provides insight into the convergent evolution of caffeine biosynthesis Denoeud, F.; Carretero-Paulet, L.; Dereeper, A. Science, Vol. 345, Issue 6201 https://doi.org/10.1126/science.1255274	journal	September 2014
Analysis of the genome sequence of the flowering plant Arabidopsis thaliana Nature, Vol. 408, Issue 6814, p. 796-815 https://doi.org/10.1038/35048692	journal	December 2000
The Origin of American Tetraploid Gossypium Species Beasley, J. O. The American Naturalist, Vol. 74, Issue 752 https://doi.org/10.1086/280895	journal	May 1940
Gene Expression Changes and Early Events in Cotton Fibre Development Lee, J. J.; Woodward, A. W.; Chen, Z. J. Annals of Botany, Vol. 100, Issue 7 https://doi.org/10.1093/aob/mcm232	journal	September 2007
Construction of a plant-transformation-competent BIBAC library and genome sequence analysis of polyploid Upland cotton (Gossypium hirsutum L.) Lee, Mi-Kyung; Zhang, Yang; Zhang, Meiping BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-208	journal	January 2013
A cysteine-rich receptor-like kinase NCRK and a pathogen-induced protein kinase RBK1 are Rop GTPase interactors: Rop GTPases interacting with protein kinases Molendijk, Arthur J.; Ruperti, Benedetto; Singh, Manoj K. The Plant Journal, Vol. 53, Issue 6 https://doi.org/10.1111/j.1365-313X.2007.03384.x	journal	December 2007
Construction and characterization of a bacterial artificial chromosome library for the allotetraploid Gossypium tomentosum Liu, F.; Wang, Y. H.; Gao, H. Y. Genetics and Molecular Research, Vol. 14, Issue 4 https://doi.org/10.4238/2015.december.15.3	journal	January 2015
The wondrous cycles of polyploidy in plants Wendel, Jonathan F. American Journal of Botany, Vol. 102, Issue 11 https://doi.org/10.3732/ajb.1500320	journal	October 2015
Cytological studies in cotton: IV. Chromosome conjugation in interspecific hybrids Skovsted, A. Journal of Genetics, Vol. 34, Issue 1 https://doi.org/10.1007/bf02982258	journal	February 1937
Toward Sequencing Cotton ( Gossypium ) Genomes: Figure 1. Chen, Z. Jeffrey; Scheffler, Brian E.; Dennis, Elizabeth Plant Physiology, Vol. 145, Issue 4 https://doi.org/10.1104/pp.107.107672	journal	December 2007
Prospecting for Genes involved in transcriptional regulation of plant defenses, a bioinformatics approach van Verk, Marcel C.; Bol, John F.; Linthorst, Huub JM BMC Plant Biology, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2229-11-88	journal	January 2011
Comparative development of fiber in wild and cultivated cotton Applequist, Wendy L.; Cronn, Richard; Wendel, Jonathan F. Evolution and Development, Vol. 3, Issue 1 https://doi.org/10.1046/j.1525-142x.2001.00079.x	journal	January 2001
A Draft Sequence of the Rice Genome (Oryza sativa L. ssp. japonica) Goff, S. A. Science, Vol. 296, Issue 5565 https://doi.org/10.1126/science.1068275	journal	April 2002
Roles for mannitol and mannitol dehydrogenase in active oxygen-mediated plant defense Jennings, D. B.; Ehrenshaft, M.; Pharr, D. M. Proceedings of the National Academy of Sciences, Vol. 95, Issue 25 https://doi.org/10.1073/pnas.95.25.15129	journal	December 1998
Contigs Built with Fingerprints, Markers, and FPC V4.7 Soderlund, C. Genome Research, Vol. 10, Issue 11 https://doi.org/10.1101/gr.gr-1375r	journal	November 2000
BAC-End Sequence-Based SNP Mining in Allotetraploid Cotton (Gossypium) Utilizing Resequencing Data, Phylogenetic Inferences, and Perspectives for Genetic Mapping Hulse-Kemp, A. M.; Ashrafi, H.; Stoffel, K. G3: Genes\|Genomes\|Genetics, Vol. 5, Issue 6 https://doi.org/10.1534/g3.115.017749	journal	April 2015
Construction of integrated genetic linkage maps by means of a new computer package: Join Map Stam, Piet The Plant Journal, Vol. 3, Issue 5 https://doi.org/10.1111/j.1365-313X.1993.00739.x	journal	May 1993
Cotton: Origin, History, Technology, and Production Brown, D. Clayton Agricultural History, Vol. 74, Issue 4 https://doi.org/10.1215/00021482-74.4.823	journal	October 2000

Cited By (6)

Cotton CENTRORADIALIS/TERMINAL FLOWER 1/SELF-PRUNING genes functionally diverged to differentially impact plant architecture Prewitt, Sarah F.; Ayre, Brian G.; McGarry, Roisin C. Journal of Experimental Botany https://doi.org/10.1093/jxb/ery324	journal	September 2018
Impact of Chromosomal Rearrangements on the Interpretation of Lupin Karyotype Evolution Susek, Karolina; Bielski, Wojciech; Czyż, Katarzyna B. Genes, Vol. 10, Issue 4 https://doi.org/10.3390/genes10040259	journal	April 2019
Unraveling cis and trans regulatory evolution during cotton domestication Bao, Ying; Hu, Guanjing; Grover, Corrinne E. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13386-w	journal	November 2019
Functional divergence of cellulose synthase orthologs in between wild Gossypium raimondii and domesticated G. arboreum diploid cotton species Kim, Hee Jin; Thyssen, Gregory N.; Song, Xianliang Cellulose, Vol. 26, Issue 18 https://doi.org/10.1007/s10570-019-02744-y	journal	September 2019
Genetic Analysis of the Transition from Wild to Domesticated Cotton ( Gossypium hirsutum L.) Grover, Corrinne E.; Yoo, Mi-Jeong; Lin, Meng G3 Genes\|Genomes\|Genetics, Vol. 10, Issue 2 https://doi.org/10.1534/g3.119.400909	journal	February 2020
Identification of cotton MOTHER OF FT AND TFL1 homologs, GhMFT1 and GhMFT2, involved in seed germination Yu, Xiuli; Liu, Hui; Sang, Na PLOS ONE, Vol. 14, Issue 4 https://doi.org/10.1371/journal.pone.0215771	journal	April 2019

Similar Records

Re-annotation of the physical map of Glycine max for polyploid-like regions by BAC end sequence driven whole genome shotgun read assembly

Journal Article · Mon Jul 07 00:00:00 EDT 2008 · BMC Genomics · OSTI ID:1543775

Saini, Navinder; Shultz, Jeffry; Lightfoot, David A.

CMD: a Cotton Microsatellite Database resource for Gossypium genomics

Journal Article · Wed May 31 00:00:00 EDT 2006 · BMC Genomics · OSTI ID:1543775

Blenda, Anna; Scheffler, Jodi; Scheffler, Brian; +22 more

Genomic diversifications of five Gossypium allopolyploid species and their impact on cotton improvement

Journal Article · Mon Apr 20 00:00:00 EDT 2020 · Nature Genetics · OSTI ID:1543775

Chen, Z. Jeffrey; Sreedasyam, Avinash; Ando, Atsumi; +30 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Sub genome anchored physical frameworks of the allotetraploid Upland cotton (Gossypium hirsutum L.) genome, and an approach toward reference-grade assemblies of polyploids

Citation Formats

References (58)

Cited By (6)

Similar Records

Related Subjects