Next-generation sequencing of flow-sorted wheat chromosome 5D reveals lineage-specific translocations and widespread gene duplications

BMC Genomics

Hikmet Budak³  Jaroslav Doležel²  Marie Kubaláková²  Hana Šimková²  Bala Anı Akpınar¹  Stuart J Lucas³ 

[1] Faculty of Engineering and Natural Sciences, Sabanci University, Orhanlı, 34956 Tuzla, Istanbul, Turkey;Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany, Sokolovská 6, CZ-77200 Olomouc, Czech Republic;Sabanci University Nanotechnology Research and Application Centre (SUNUM), Sabanci University, Orhanlı, 34956 Tuzla, Istanbul, Turkey

关键词: Comparative grass genomics;    Chromosome arm shotgun;    Triticeae genome;    Genome zipper;    Triticum aestivum;    Chromosome sorting;    Wheat genome;   

Others  :  1127474
DOI  :  10.1186/1471-2164-15-1080

 received in 2014-08-29, accepted in 2014-11-26,  发布年份 2014

【 摘 要 】

Background

The ~17 Gb hexaploid bread wheat genome is a high priority and a major technical challenge for genomic studies. In particular, the D sub-genome is relatively lacking in genetic diversity, making it both difficult to map genetically, and a target for introgression of agriculturally useful traits. Elucidating its sequence and structure will therefore facilitate wheat breeding and crop improvement.

Results

We generated shotgun sequences from each arm of flow-sorted Triticum aestivum chromosome 5D using 454 FLX Titanium technology, giving 1.34× and 1.61× coverage of the short (5DS) and long (5DL) arms of the chromosome respectively. By a combination of sequence similarity and assembly-based methods, ~74% of the sequence reads were classified as repetitive elements, and coding sequence models of 1314 (5DS) and 2975 (5DL) genes were generated. The order of conserved genes in syntenic regions of previously sequenced grass genomes were integrated with physical and genetic map positions of 518 wheat markers to establish a virtual gene order for chromosome 5D.

Conclusions

The virtual gene order revealed a large-scale chromosomal rearrangement in the peri-centromeric region of 5DL, and a concentration of non-syntenic genes in the telomeric region of 5DS. Although our data support the large-scale conservation of Triticeae chromosome structure, they also suggest that some regions are evolving rapidly through frequent gene duplications and translocations.

Sequence accessions

EBI European Nucleotide Archive, Study no. ERP002330

【 授权许可】

   
2014 Lucas et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Gill BS, Appels R, Botha-Oberholster A-M, Buell CR, Bennetzen JL, Chalhoub B, Chumley F, Dvorák J, Iwanaga M, Keller B, Li W, McCombie WR, Ogihara Y, Quetier F, Sasaki T: A workshop report on wheat genome sequencing: ınternational genome research on wheat consortium. Genetics 2004, 168:1087-1096.
• [2]Peng JH, Sun D, Nevo E: Domestication evolution, genetics and genomics in wheat. Mol Breed 2011, 28:281-301.
• [3]Feuillet C, Leach JE, Rogers J, Schnable PS, Eversole K: Crop genome sequencing: lessons and rationales. Trends Plant Sci 2011, 16:77-88.
• [4]Kubaláková M, Vrána J, Číhalíková J, Šimková H, Doležel J: Flow karyotyping and chromosome sorting in bread wheat (Triticum aestivum L.). Theor Appl Genet 2002, 104:1362-1372.
• [5]Šafář J, Šimková H, Kubaláková M, Číhalíková J, Suchánková P, Bartoš J, Doležel J: Development of chromosome-specific BAC resources for genomics of bread wheat. Cytogenet Genome Res 2010, 129:211-223.
• [6]Paux E, Roger D, Badaeva E, Gay G, Bernard M, Sourdille P, Feuillet C: Characterizing the composition and evolution of homoeologous genomes in hexaploid wheat through BAC-end sequencing on chromosome 3B. Plant J 2006, 48:463-474.
• [7]Lucas SJ, Šimková H, Šafář J, Jurman I, Cattonaro F, Vautrin S, Bellec A, Berges H, Doležel J, Budak H: Functional features of a single chromosome arm in wheat (1AL) determined from its structure. Funct Integr Genomics 2012, 12:173-82.
• [8]Mayer KFX, Taudien S, Martis M, Simková H, Suchánková P, Gundlach H, Wicker T, Petzold A, Felder M, Steuernagel B, Scholz U, Graner A, Platzer M, Dolezel J, Stein N: Gene content and virtual gene order of barley chromosome 1H. Plant Physiol 2009, 151:496-505.
• [9]Mayer KFX, Martis M, Hedley PE, Simková H, Liu H, Morris JA, Steuernagel B, Taudien S, Roessner S, Gundlach H, Kubaláková M, Suchánková P, Murat F, Felder M, Nussbaumer T, Graner A, Salse J, Endo T, Sakai H, Tanaka T, Itoh T, Sato K, Platzer M, Matsumoto T, Scholz U, Dolezel J, Waugh R, Stein N: Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell 2011, 23:1249-1263.
• [10]Vitulo N, Albiero A, Forcato C, Campagna D, Dal Pero F, Bagnaresi P, Colaiacovo M, Faccioli P, Lamontanara A, Šimková H, Kubaláková M, Perrotta G, Facella P, Lopez L, Pietrella M, Gianese G, Doležel J, Giuliano G, Cattivelli L, Valle G, Stanca AM: First survey of the wheat chromosome 5A composition through a next generation sequencing approach. PLoS One 2011, 6:e26421.
• [11]Wicker T, Mayer KFX, Gundlach H, Martis M, Steuernagel B, Scholz U, Simková H, Kubaláková M, Choulet F, Taudien S, Platzer M, Feuillet C, Fahima T, Budak H, Dolezel J, Keller B, Stein N: Frequent gene movement and pseudogene evolution is common to the large and complex genomes of wheat, barley, and their relatives. Plant Cell 2011, 23:1706-1718.
• [12]Berkman PJ, Skarshewski A, Manoli S, Lorenc MT, Stiller J, Smits L, Lai K, Campbell E, Kubaláková M, Šimková H, Batley J, Dolezel J, Hernandez P, Edwards D: Sequencing wheat chromosome arm 7BS delimits the 7BS/4AL translocation and reveals homoeologous gene conservation. Theor Appl Genet 2012, 124:423-432.
• [13]Hernandez P, Martis M, Dorado G, Pfeifer M, Gálvez S, Schaaf S, Jouve N, Šimková H, Valárik M, Doležel J, Mayer KFX: Next-generation sequencing and syntenic integration of flow-sorted arms of wheat chromosome 4A exposes the chromosome structure and gene content. Plant J 2012, 69:377-386.
• [14]Tanaka T, Kobayashi F, Joshi GP, Onuki R, Sakai H, Kanamori H, Wu J, Šimková H, Nasuda S, Endo TR, Hayakawa K, Doležel J, Ogihara Y, Itoh T, Matsumoto T, Handa H: Next-generation survey sequencing and the molecular organization of wheat chromosome 6B. DNA Res 2014, 21:103-114.
• [15]Brenchley R, Spannagl M, Pfeifer M, Barker GL, D’Amore R, Allen AM, McKenzie N, Kramer M, Kerhornou A, Bolser D, Kay S, Waite D, Trick M, Bancroft I, Gu Y, Huo N, Luo M-C, Sehgal S, Gill B, Kianian S, Anderson O, Kersey P, Dvorak J, McCombie WR, Hall A, Mayer KFX, Edwards KJ, Bevan MW, Hall N: Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 2012, 491:705-10.
• [16]International Wheat Genome Sequencing Consortium: A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 2014, 345(80):1250092-1250092.
• [17]Choulet F, Alberti A, Theil S, Glover N, Barbe V, Daron J, Pingault L, Sourdille P, Couloux A, Paux E, Leroy P, Mangenot S, Guilhot N, Le Gouis J, Balfourier F, Alaux M, Jamilloux V, Poulain J, Durand C, Bellec A, Gaspin C, Safar J, Dolezel J, Rogers J, Vandepoele K, Aury J-M, Mayer K, Berges H, Quesneville H, Wincker P, et al.: Structural and functional partitioning of bread wheat chromosome 3B. Science 2014, 345(80):1249721-1249721.
• [18]Marcussen T, Sandve SR, Heier L, Spannagl M, Pfeifer M, Jakobsen KS, Wulff BBH, Steuernagel B, Mayer KFX, Olsen O, International Wheat Genome Sequencing Consortium: Ancient hybridizations among the ancestral genomes of bread wheat. Science 2014, 345(80):1250092. 1–1250092:4
• [19]Dubcovsky J, Dvorak J: Genome plasticity a key factor in the success of polyploid wheat under domestication. Science 2007, 316:1862-1866.
• [20]Linkiewicz AM, Qi LL, Gill BS, Ratnasiri A, Echalier B, Chao S, Lazo GR, Hummel DD, Anderson OD, Akhunov ED, Dvorák J, Pathan MS, Nguyen HT, Peng JH, Lapitan NLV, Miftahudin , Gustafson JP, La Rota CM, Sorrells ME, Hossain KG, Kalavacharla V, Kianian SF, Sandhu D, Bondareva SN, Gill KS, Conley EJ, Anderson JA, Fenton RD, Close TJ, McGuire PE, et al.: A 2500-locus bin map of wheat homoeologous group 5 provides insights on gene distribution and colinearity with rice. Genetics 2004, 168:665-676.
• [21]Morris CF: Puroindolines: the molecular genetic basis of wheat grain hardness. Plant Mol Biol 2002, 48:633-647.
• [22]Yoshida T, Nishida H, Zhu J, Nitcher R, Distelfeld A, Akashi Y, Kato K, Dubcovsky J: Vrn-D4 is a vernalization gene located on the centromeric region of chromosome 5D in hexaploid wheat. Theor Appl Genet 2010, 120:543-552.
• [23]Zhang J, Wang Y, Wu S, Yang J, Liu H, Zhou Y: A single nucleotide polymorphism at the Vrn-D1 promoter region in common wheat is associated with vernalization response. Theor Appl Genet 2012, 125:1697-1704.
• [24]Cloutier S, McCallum BD, Loutre C, Banks TW, Wicker T, Feuillet C, Keller B, Jordan MC: Leaf rust resistance gene Lr1, isolated from bread wheat (Triticum aestivum L.) is a member of the large psr567 gene family. Plant Mol Biol 2007, 65:93-106.
• [25]Pont C, Murat F, Guizard S, Flores R, Foucrier S, Bidet Y, Quraishi UM, Alaux M, Doležel J, Fahima T, Budak H, Keller B, Salvi S, Maccaferri M, Steinbach D, Feuillet C, Quesneville H, Salse J: Wheat syntenome unveils new evidences of contrasted evolutionary plasticity between paleo- and neoduplicated subgenomes. Plant J 2013, 76:1030-1044.
• [26]Nelson JC, Sorrells ME, Van Deynze AE, Lu YH, Atkinson M, Bernard M, Leroy P, Faris JD, Anderson JA: Molecular mapping of wheat: major genes and rearrangements in homoeologous groups 4, 5, and 7. Genetics 1995, 141:721-731.
• [27]Wicker T, Buchmann JP, Keller B: Patching gaps in plant genomes results in gene movement and erosion of colinearity. Genome Res 2010, 20:1229-1237.
• [28]Schreiber AW, Hayden MJ, Forrest KL, Kong SL, Langridge P, Baumann U: Transcriptome-scale homoeolog-specific transcript assemblies of bread wheat. BMC Genomics 2012, 13:492. BioMed Central Full Text
• [29]Mayer KFX, Waugh R, Brown JWS, Schulman A, Langridge P, Platzer M, Fincher GB, Muehlbauer GJ, Sato K, Close TJ, Wise RP, Stein N: A physical, genetic and functional sequence assembly of the barley genome. Nature 2012, 491:711-6.
• [30]Choulet F, Wicker T, Rustenholz C, Paux E, Salse J, Leroy P, Schlub S, Le Paslier M-C, Magdelenat G, Gonthier C, Couloux A, Budak H, Breen J, Pumphrey M, Liu S, Kong X, Jia J, Gut M, Brunel D, Anderson JA, Gill BS, Appels R, Keller B, Feuillet C: Megabase level sequencing reveals contrasted organization and evolution patterns of the wheat gene and transposable element spaces. Plant Cell 2010, 22:1686-1701.
• [31]Shemesh R, Novik A, Cohen Y: Follow the leader: preference for specific amino acids directly following the ınitial methionine in proteins of different organisms. Genomics Proteomics Bioinformatics 2010, 8:180-189.
• [32]Frenkel-Morgenstern M, Danon T, Christian T, Igarashi T, Cohen L, Hou Y-M, Jensen LJ: Genes adopt non-optimal codon usage to generate cell cycle-dependent oscillations in protein levels. Mol Syst Biol 2012, 8:572.
• [33]International Brachypodium Initiative: Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 2010, 463:763-768.
• [34]Vrána J, Kubaláková M, Simková H, Cíhalíková J, Lysák MA, Dolezel J: Flow sorting of mitotic chromosomes in common wheat (Triticum aestivum L.). Genetics 2000, 156:2033-2041.
• [35]Simková H, Svensson JT, Condamine P, Hribová E, Suchánková P, Bhat PR, Bartos J, Safár J, Close TJ, Dolezel J: Coupling amplified DNA from flow-sorted chromosomes to high-density SNP mapping in barley. BMC Genomics 2008, 9:294. BioMed Central Full Text
• [36]Institute for Systems Biology: RepeatMasker. [http://www.repeatmasker.org/ webcite]
• [37]TREP: The Triticeae Repeat Sequence Database. [http://wheat.pw.usda.gov/ITMI/Repeats webcite]
• [38]Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J: Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 2005, 110:462-467.
• [39]Repbase. [http://www.girinst.org/repbase/index.html webcite]
• [40]Ouyang S, Buell CR: The TIGR Plant Repeat Databases: a collective resource for the identification of repetitive sequences in plants. Nucleic Acids Res 2004, 32:D360-D363.
• [41]Plant Repeat Databases. [http://plantrepeats.plantbiology.msu.edu/index.html webcite]
• [42]PlantsDB. [http://mips.helmholtz-muenchen.de/plant/genomes.jsp webcite]
• [43]Tanaka T, Antonio BA, Kikuchi S, Matsumoto T, Nagamura Y, Numa H, Sakai H, Wu J, Itoh T, Sasaki T, Aono R, Fujii Y, Habara T, Harada E, Kanno M, Kawahara Y, Kawashima H, Kubooka H, Matsuya A, Nakaoka H, Saichi N, Sanbonmatsu R, Sato Y, Shinso Y, Suzuki M, Takeda J, Tanino M, Todokoro F, Yamaguchi K, Yamamoto N, et al.: The Rice Annotation Project Database (RAP-DB): 2008 update. Nucleic Acids Res 2008, 36:D1028-D1033.
• [44]The Rice Annotation Project Database. [http://rapdb.dna.affrc.go.jp/download/irgsp1.html webcite]
• [45]Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, et al.: The Sorghum bicolor genome and the diversification of grasses. Nature 2009, 457:551-556.
• [46]URGI Genetic and Genomic Information System. [http://urgi.versailles.inra.fr/GnpMap/mapping/id.do?action=MAP&id=59 webcite]
• [47]GrainGenes wEST. [http://wheat.pw.usda.gov/wEST/ webcite]
• [48]UniGene Repository. [ftp://ftp.ncbi.nih.gov/repository/UniGene/ webcite]
• [49]The Uniprot Consortium: Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res 2012, 40:D71-5.
• [50]CerealsDB. [http://www.cerealsdb.uk.net/cerealgenomics/CerealsDB/copyright.php webcite]
• [51]URGI Sequence Repository. [https://urgi.versailles.inra.fr/download/iwgsc/ webcite]
• [52]Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL: BLAST+: architecture and applications. BMC Bioinformatics 2009, 10:421. BioMed Central Full Text
• [53]Lowe Lab tRNAscan-SE search server. [http://lowelab.ucsc.edu/tRNAscan-SE/ webcite]
• [54]Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA: Circos: an information aesthetic for comparative genomics. Genome Res 2009, 19:1639-1645.
• [55]Bayer M, Milne I, Stephen G, Shaw P, Cardle L, Wright F, Marshall D: Comparative visualization of genetic and physical maps with strudel. Bioinformatics 2011, 27:1307-1308.
• [56]Conesa A, Götz S: Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008, 2008:619832.