Wild emmer wheat, Triticum turgidum ssp. dicoccoides is the wild relative of Triticum turgidum, the progenitor of durum and bread wheat, and maintains a rich allelic diversity among its wild populations. The lack of adequate genetic and genomic resources, however, restricts its exploitation in wheat improvement. Here, we report next-generation sequencing of the flow-sorted chromosome 5B of T. dicoccoides to shed light into its genome structure, function and organization by exploring the repetitive elements, protein-encoding genes and putative microRNA and tRNA coding sequences. Comparative analyses with its counterparts in modern and wild wheats suggest clues into the B-genome evolution. Syntenic relationships of chromosome 5B with the model grasses can facilitate further efforts for fine-mapping of traits of interest. Mapping of 5B sequences onto the root transcriptomes of two additional T. dicoccoides genotypes, with contrasting drought tolerances, revealed several thousands of single nucleotide polymorphisms, of which 584 shared polymorphisms on 228 transcripts were specific to the drought-tolerant genotype. To our knowledge, this study presents the largest genomics resource currently available for T. dicoccoides, which, we believe, will encourage the exploitation of its genetic and genomic potential for wheat improvement to meet the increasing demand to feed the world.

] Sabanci University Nanotechnology Research and Application Centre Sabanci University Orhanlı 34956 Tuzla Istanbul Turkey [2] Faculty of Engineering and Natural Sciences Molecular Biology Genetics and Bioengineering Sabanci University Orhanlı 34956 Tuzla Istanbul Turkey

Institute of Experimental Botany Centre of the Region Haná for Biotechnological and Agricultural Research Slechtitelu 31 CZ 78371 Olomouc Czech Republic

Sabanci University Nanotechnology Research and Application Centre Sabanci University Orhanlı 34956 Tuzla Istanbul Turkey

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Feuillet C., Langridge P. & Waugh R. Cereal breeding takes a walk on the wild side. Trends Genet. 24, 24–32 (2008). PubMed

Nevo E. & Chen G. Drought and salt tolerances in wild relatives for wheat and barley improvement. Plant. Cell Environ. 33, 670–85 (2010). PubMed

Paux E., Sourdille P., Mackay I. & Feuillet C. Sequence-based marker development in wheat: advances and applications to breeding. Biotechnol. Adv. 30, 1071–88 (2012). PubMed

Marcussen T. et al. Ancient hybridizations among the ancestral genomes of bread wheat. Science 345, 1250092–1250092 (2014). PubMed

Hao M. et al. QTug.sau-3B is a major quantitative trait locus for wheat hexaploidization. G3 (Bethesda). 4, 1943–53 (2014). PubMed PMC

Budak H., Kantar M. & Kurtoglu K. Y. Drought tolerance in modern and wild wheat. ScientificWorld Journal. 2013, 548246 (2013). PubMed PMC

Xie W. & Nevo E. Wild emmer: genetic resources, gene mapping and potential for wheat improvement. Euphytica 164, 603–614 (2008).

Ergen N. Z. & Budak H. Sequencing over 13 000 expressed sequence tags from six subtractive cDNA libraries of wild and modern wheats following slow drought stress. Plant. Cell Environ. 32, 220–36 (2009). PubMed

Ergen N. Z., Thimmapuram J., Bohnert H. J. & Budak H. Transcriptome pathways unique to dehydration tolerant relatives of modern wheat. Funct. Integr. Genomics 9, 377–96 (2009). PubMed

Budak H., Akpinar B. A., Unver T. & Turktas M. Proteome changes in wild and modern wheat leaves upon drought stress by two-dimensional electrophoresis and nanoLC-ESI-MS/MS. Plant Mol. Biol. 83, 89–103 (2013). PubMed

Kubaláková M., Vrána J., Cíhalíková J., Simková H. & Dolezel J. Flow karyotyping and chromosome sorting in bread wheat (Triticum aestivum L.). Theor. Appl. Genet. 104, 1362–1372 (2002). PubMed

Safár J. et al. Development of chromosome-specific BAC resources for genomics of bread wheat. Cytogenet. Genome Res. 129, 211–23 (2010). PubMed

Vitulo N. et al. First survey of the wheat chromosome 5A composition through a next generation sequencing approach. PLoS One 6, e26421 (2011). PubMed PMC

Mayer K. F. X. et al. A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science. 345, 1251788–1251788 (2014). PubMed

Ling H.-Q. et al. Draft genome of the wheat A-genome progenitor Triticum urartu. Nature 496, 87–90 (2013). PubMed

Jia J. et al. Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 496, 91–5 (2013). PubMed

Venora G. et al. Chromatin organisation and computer aided karyotyping of Triticum durum Desf. cv. Timilia. Caryologia 55, 91–98 (2002).

Smith D. B. & Flavell R. B. Characterisation of the wheat genome by renaturation kinetics. Chromosoma 50, 223–242 (1975).

Lucas S. J. et al. Next-generation sequencing of flow-sorted wheat chromosome 5D reveals lineage-specific translocations and widespread gene duplications. BMC Genomics 15, 1080 (2014). PubMed PMC

Akpinar B. A., Lucas S. J., Vrána J., Doležel J. & Budak H. Sequencing chromosome 5D of Aegilops tauschii and comparison with its allopolyploid descendant bread wheat (Triticum aestivum). Plant Biotechnol. J. doi:10.1111/pbi.12302 (2014). PubMed

Choulet F. et al. Structural and functional partitioning of bread wheat chromosome 3B. Science 345, 1249721–1249721 (2014). PubMed

Senerchia N., Felber F. & Parisod C. Contrasting evolutionary trajectories of multiple retrotransposons following independent allopolyploidy in wild wheats. New Phytol. 202, 975–985 (2014). PubMed

International Brachypodium Initiative. Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463, 763–8 (2010). PubMed

Tanaka T. et al. The Rice Annotation Project Database (RAP-DB): 2008 update. Nucleic Acids Res. 36, D1028–D1033 (2008). PubMed PMC

Paterson A. H. et al. The Sorghum bicolor genome and the diversification of grasses. Nature 457, 551–6 (2009). PubMed

Mayer K. F. X. et al. A physical, genetic and functional sequence assembly of the barley genome. Nature 491, 711–6 (2012). PubMed

Wicker T. et al. Frequent Gene Movement and Pseudogene Evolution Is Common to the Large and Complex Genomes of Wheat, Barley, and Their Relatives. Plant Cell 23, 1706–1718 (2011). PubMed PMC

Wicker T., Buchmann J. P. & Keller B. Patching gaps in plant genomes results in gene movement and erosion of colinearity. Genome Res. 20, 1229–37 (2010). PubMed PMC

Tanaka T. et al. Next-generation survey sequencing and the molecular organization of wheat chromosome 6B. DNA Res. 21, 103–14 (2014). PubMed PMC

Kojima K. K. & Jurka J. A superfamily of DNA transposons targeting multicopy small RNA genes. PLoS One 8, e68260 (2013). PubMed PMC

Budak H., Khan Z. & Kantar M. History and current status of wheat miRNAs using next-generation sequencing and their roles in development and stress. Brief. Funct. Genomics doi:10.1093/bfgp/elu021 (2014). PubMed

Kantar M., Unver T. & Budak H. Regulation of barley miRNAs upon dehydration stress correlated with target gene expression. Funct. Integr. Genomics 10, 493–507 (2010). PubMed

Pfeifer M. et al. Genome interplay in the grain transcriptome of hexaploid bread wheat. Science 345, 1250091–1250091 (2014). PubMed

You F. M. et al. Annotation-based genome-wide SNP discovery in the large and complex Aegilops tauschii genome using next-generation sequencing without a reference genome sequence. BMC Genomics 12, 59 (2011). PubMed PMC

Zhang H. et al. Genetic and comparative genomics mapping reveals that a powdery mildew resistance gene Ml3D232 originating from wild emmer co-segregates with an NBS-LRR analog in common wheat (Triticum aestivum L.). Theor. Appl. Genet. 121, 1613–21 (2010). PubMed

Xue F., Ji W., Wang C., Zhang H. & Yang B. High-density mapping and marker development for the powdery mildew resistance gene PmAS846 derived from wild emmer wheat (Triticum turgidum var. dicoccoides). Theor. Appl. Genet. 124, 1549–60 (2012). PubMed

Abdollahi Mandoulakani B. et al. Development of IRAP- and REMAP-derived SCAR markers for marker-assisted selection of the stripe rust resistance gene Yr15 derived from wild emmer wheat. Theor. Appl. Genet. doi:10.1007/s00122-014-2422-8 (2014). PubMed

Ouyang S. et al. Fine physical and genetic mapping of powdery mildew resistance gene MlIW172 originating from wild emmer (Triticum dicoccoides). PLoS One 9, e100160 (2014). PubMed PMC

Wang Z. et al. Comparative genetic mapping and genomic region collinearity analysis of the powdery mildew resistance gene Pm41. Theor. Appl. Genet. 127, 1741–51 (2014). PubMed

Blanco A. et al. Molecular mapping of the novel powdery mildew resistance gene Pm36 introgressed from Triticum turgidum var. dicoccoides in durum wheat. Theor. Appl. Genet. 117, 135–42 (2008). PubMed

Qi L., Friebe B. & Gill B. S. Meiotic metaphase I pairing behavior of a 5BL recombinant isochromosome in wheat. Chromosome Res. 8, 671–6 (2000). PubMed

Griffiths S. et al. Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat. Nature 439, 749–52 (2006). PubMed

Bhullar R. et al. Silencing of a metaphase I-specific gene results in a phenotype similar to that of the Pairing homeologous 1 (Ph1) gene mutations. Proc. Natl. Acad. Sci. USA 111, 14187–92 (2014). PubMed PMC

Sergeeva E. M. et al. Common Wheat Chromosome 5B Composition Analysis Using Low-Coverage 454 Sequencing. Plant Genome 7, 1–16 (2013).

Renny-Byfield S. et al. Diploidization and genome size change in allopolyploids is associated with differential dynamics of low- and high-copy sequences. Plant J. 74, 829–39 (2013). PubMed

Wu H. et al. Comparative high-resolution mapping of the wax inhibitors Iw1 and Iw2 in hexaploid wheat. PLoS One 8, e84691 (2013). PubMed PMC

Kurtoglu K. Y., Kantar M., Lucas S. J. & Budak H. Unique and conserved microRNAs in wheat chromosome 5D revealed by next-generation sequencing. PLoS One 8, e69801 (2013). PubMed PMC

Luan M. et al. Family-wide survey of miR169s and NF-YAs and their expression profiles response to abiotic stress in maize roots. PLoS One 9, e91369 (2014). PubMed PMC

Shivaprasad P. V et al. A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24, 859–74 (2012). PubMed PMC

Brenchley R. et al. Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491, 705–10 (2012). PubMed PMC

Sela H. et al. Linkage disequilibrium and association analysis of stripe rust resistance in wild emmer wheat (Triticum turgidum ssp. dicoccoides) population in Israel. Theor. Appl. Genet. 127, 2453–63 (2014). PubMed

Trick M. et al. Combining SNP discovery from next-generation sequencing data with bulked segregant analysis (BSA) to fine-map genes in polyploid wheat. BMC Plant Biol. 12, 14 (2012). PubMed PMC

Giorgi D. et al. FISHIS: fluorescence in situ hybridization in suspension and chromosome flow sorting made easy. PLoS One 8, e57994 (2013). PubMed PMC

Kubaláková M. et al. Analysis and sorting of rye (Secale cereale L.) chromosomes using flow cytometry. Genome 46, 893–905 (2003). PubMed

Simková H. et al. Coupling amplified DNA from flow-sorted chromosomes to high-density SNP mapping in barley. BMC Genomics 9, 294 (2008). PubMed PMC

Nussbaumer T. et al. MIPS PlantsDB: a database framework for comparative plant genome research. Nucleic Acids Res. 41, D1144–51 (2013). PubMed PMC

Camacho C. et al. BLAST+: architecture and applications. BMC Bioinformatics 10, 421 (2009). PubMed PMC

Krzywinski M. et al. Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639–1645 (2009). PubMed PMC

Conesa A. & Götz S. Blast2GO: A comprehensive suite for functional analysis in plant genomics. Int. J. Plant Genomics 2008, 619832 (2008). PubMed PMC

Lowe T. M. & Eddy S. R. tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence. Nucleic Acids Res. 25, 0955–964 (1997). PubMed PMC

Flow karyotyping of wheat-Aegilops additions facilitate dissecting the genomes of Ae. biuncialis and Ae. geniculata into individual chromosomes

Chromosome analysis and sorting

Hotspots in the genomic architecture of field drought responses in wheat as breeding targets

Chromosome-based survey sequencing reveals the genome organization of wild wheat progenitor Triticum dicoccoides