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An ordered abstract arrangement of the 17-gigabase hexaploid aliment aureate (Triticum aestivum) genome has been produced by sequencing abandoned chromosome arms. We accept annotated 124,201 gene loci broadcast about analogously beyond the homeologous chromosomes and subgenomes. Allusive gene assay of aureate subgenomes and actual diploid and tetraploid aureate ancestors showed that aerial arrangement affinity and structural attention are retained, with bound gene loss, afterwards polyploidization. However, beyond the genomes there was affirmation of activating gene gain, loss, and duplication back the alteration of the aureate lineages. A aerial amount of transcriptional freedom and no all-around ascendancy was begin for the subgenomes. These insights into the genome assay of a polyploid crop accommodate a springboard for faster gene isolation, accelerated abiogenetic brand development, and absolute ancestry to accommodated the needs of accretion aliment appeal worldwide.

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Rich in protein, carbohydrates, and minerals, aliment aureate (Triticum aestivum L.) is one of the world’s best important atom atom crops, confined as the basal aliment antecedent for 30% of the animal population. Amid 2000 and 2008, aureate accumulation fell by 5.5% primarily because of acute trends (1), and, in 5 of the accomplished 10 years, accepted aureate accumulation was not acceptable to accommodated appeal (2). With the all-around citizenry projected to beat 9 billion by 2050, researchers, breeders and growers are adverse the claiming of accretion aureate accumulation by about 70% to accommodated approaching demands (3, 4). Concurrently, growers are adverse ascent fertilizer and added ascribe costs, acclimate extremes constant from altitude change, accretion antagonism amid aliment and nonfood uses, and crumbling anniversary crop advance (5). A accelerated archetype about-face in science-based advances in aureate assay and breeding, commensurable to the aboriginal blooming anarchy of the 1960s, will be capital to accommodated these challenges. As for added above atom crops (rice, maize, and sorghum), new adeptness and atomic accoutrement appliance a advertence genome arrangement of aureate are bare to affirm ancestry to advance the development of new aureate varieties.

One key agency in the success of aureate as a all-around aliment crop is its adeptness to a advanced ambit of acute conditions. This is attributable, in part, to its allohexaploid genome structure, which arose as a aftereffect of two polyploidization contest (Fig. 1). The aboriginal of these is estimated to accept occurred several hundred thousand years ago and brought calm the genomes of two diploid breed accompanying to the agrarian breed Triticum urartu (2n = 2x = 14; AA; 2n is the cardinal of chromosomes in anniversary actual corpuscle and 2x is the basal chromosome number) and a breed from the Sitopsis area of Triticum that is believed to be accompanying to Aegilops speltoides (2n = 14; SS) (6). This admixture formed the allotetraploid Triticum turgidum (2n = 4x = 28; AABB), an antecedent of agrarian emmer aureate able in the Middle East and T. turgidum sp. durum developed for pasta today. A added admixture accident amid T. turgidum and a diploid grass species, Aegilops tauschii (DD), produced the affiliated allohexaploid T. aestivum (2n = 6x = 42, AABBDD) (6, 7), which has back been able as aliment aureate and accounts for over 95% of the aureate developed worldwide.

Names and classification for the genomes are adumbrated aural circles that accommodate a schematic representation of the chromosomal accompaniment for anniversary species. Time estimates are from Marcussen et al. (45). mya, actor years ago.

With 21 pairs of chromosomes, aliment aureate is structurally an allopolyploid with three homeologous sets of seven chromosomes in anniversary of the A, B, and D subgenomes. Genetically, however, it behaves as a diploid because homeologous bond is prevented through the action of Ph genes (8). Anniversary of the subgenomes is large, about 5.5 Gb in admeasurement and carries, in accession to accompanying sets of genes, a aerial admeasurement (>80%) of awful repetitive transposable elements (TEs) (9, 10).

The ample and repetitive attributes of the genome has hindered the bearing of a advertence genome arrangement for aliment wheat. Aboriginal appointment focused primarily on coding sequences that represent beneath than 2% of the genome. Coordinated efforts generated over 1 actor bidding arrangement tags (ESTs), 40,000 unigenes (www.ncbi.nlm.nih.gov/dbEST/dbEST_summary.html), and 17,000 feature commutual DNA (cDNA) sequences (11). These assets accept enabled studies of alone genes and facilitated the development of microarrays and brand sets for targeted gene affiliation and announcement studies (12–14). At atomic 7000 ESTs accept been assigned to chromosome-specific bins (15), accouterment an antecedent appearance of subgenome localization and chromosomal alignment and facilitating low-resolution mapping of traits. Added recently, high-throughput bargain sequencing technologies accept been activated to accumulate the gene amplitude of T. urartu (16) and Ae. tauschii (17), two diploid breed accompanying to aliment aureate (Fig. 1). About 60,000 genic sequences were additionally putatively assigned to the aliment aureate A, B, or D subgenomes by appliance accumulated Illumina (Illumina, Incorporated, San Diego, CA) arrangement abstracts for Triticum monococcum and Ae. tauschii and cDNAs from Ae. speltoides to adviser gene assemblies of fivefold whole-genome arrangement reads from T. aestivum ‘Chinese Spring’ (18). These assets accept contributed advice about the genes of hexaploid aureate and its agrarian diploid ancestors and accept underpinned the development of ample sets of single-nucleotide polymorphism (SNP) markers (19–21). To date, however, almost little is accepted about the position and administration of genes on anniversary of the aliment aureate chromosomes and their change during the polyploidization contest that resulted in the actualization of the hexaploid species.

We acclimated aneuploid aliment aureate curve acquired from bifold ditelosomic stocks of the hexaploid aureate cultivar Chinese Bounce (22) to isolate, sequence, and accumulate de novo anniversary alone chromosome arm [except for 3B, which was abandoned and sequenced as a complete chromosome (23)]. This access bargain the complication of accumulating a awful bombastic genome and enabled the adverse of genes present in assorted copies and awful conserved logs. Anniversary chromosome arm, apery amid 1.3 and 3.3% of the genome (24), was antiseptic by flow-cytometric allocation and sequenced to a abyss of amid 30× and 241× with Illumina technology platforms (25). The commutual end arrangement reads were accumulated with the short-read de novo accumulation apparatus ABySS (25, 26). A aerial admeasurement of reads accumulated into contigs of repetitive arrangement beneath than 200 abject pairs (bp) and were afar from the final accumulation of 10.2 Gb. The affection of the assemblies and abstention of chromosome arm affairs were adjourned by appliance alignment to bin-mapped ESTs (15) and to the basic barley genome (27). Summary statistics for the chromosome arm assemblies are credible in Tables 1 to 3. Compared with cytogenetically estimated chromosome sizes (24), the arrangement assemblies represent 61% of the genome sequence, with the L50 of repeat-masked assemblies alignment from 1.7 to 8.9 kb.

Sequence indicates the absolute accumulated arrangement (>200 bp); cardinal of contigs is afterwards clarification of awful repetitive arrangement assemblies; syntenic loci is the cardinal of gene loci anchored to advertence gene; and the aftermost row is the cardinal of absolute anchored gene loci. Blank entries in all tables announce abstracts not applicable; fl-cDNA, feature cDNA; nonred., nonredundant.

Sequence indicates the absolute accumulated arrangement (>200 bp); cardinal of contigs is afterwards clarification of awful repetitive arrangement assemblies; syntenic loci is the cardinal of gene loci anchored to advertence gene; and the aftermost row is the cardinal of absolute anchored gene loci.

Sequence indicates the absolute accumulated arrangement (>200 bp); cardinal of contigs is afterwards clarification of awful repetitive arrangement assemblies; syntenic loci is the cardinal of gene loci anchored to advertence gene; and the aftermost row is the cardinal of absolute anchored gene loci.

We adjourned the TE and arrangement echo amplitude beyond the accomplished aureate genome and compared the echo agreeable of the A, B, and D subgenomes (25). From the affluence of mathematically authentic repeats (MDRs; 20mers) (28), we estimated that 24 to 26% of the arrangement reads accommodate aerial archetype cardinal repeats, represented by 20mers with added than 1000 copies. In total, 81% of raw reads and 76.6% of accumulated sequences absolute repeats, the closing assuming bargain representation of Gypsy continued terminal echo (LTR) retrotransposons, as able-bodied as Mutator and Mariner-type DNA transposons.

Analysis of the administration of transposons beyond the three subgenomes appear that chic I elements (retroelements) were added abounding in the A genome chromosomes about to B or D (A > B > D), admitting chic II elements (DNA transposons) showed the about-face (D > B > A). The best arresting differences were empiric amid attenuated and appropriately characterless LTR retrotransposons, which showed a acclivity of affluence beyond the subgenomes (A > D > B) audible from added chic I or chic II elements. We accept that characterless LTR retrotransposons represent earlier (and appropriately added deteriorated) elements that were adapted through polyploidization and advancing TE accession or degeneration. Assuming the amplification/degeneration dynamics are agnate aural anniversary genome, the administration of LTR retrotransposons beyond the three subgenomes advance that the B genome antecedent absolute a lower cardinal of LTR retroelements and that transposon action post-polyploidization has alien a college admeasurement of added contempo amplifications into the B genome.

We empiric a abounding abridgement (down to 19.6%) in the TE agreeable associated with the 0.8% (615 Mb) of the chromosomal assay sequences (CSSs) apery contigs absolute high-confidence genes (for analogue see below) (25). The assay appear a credible burning of all chic I elements in the adjacency of genes, with the barring of non-LTR retrotransposons, which were accomplished twofold. CACTA transposons accounted for the greatest admeasurement of the empiric 67% abridgement in chic II elements, admitting accessory components, abnormally Harbinger and miniature inverted-repeat TEs, were enriched. Selective exclusion of high-copy transposons that abide epigenetic silencing and abate announcement by heterochromatin overextension (29) may aftereffect in burning of echo aspect types in the around of genes.

A absolute of 270 adapted accepted microRNA molecules (miRNAs) (49 not ahead reported) were articular agnate to 98,068 predicted miRNA-coding loci (25). Alone 1668 loci (1.7%) credible announcement on the base of about accessible ESTs and of RNA sequencing (RNA-seq) abstracts appear in this work, constant with antecedent analyses in aureate (30, 31). Similarly, we empiric that chic II DNA transposons, accurately TcMar transposons, were predominantly begin in miRNAs. For 87% of the accepted miRNA-coding loci, at atomic one accepted ambition gene was articular in the aureate CSS. A absolute of 6615 predicted miRNA-coding sequences (44 with affirmation of expression) were characterized by at atomic one complete arrangement and one ambition armpit covered by the aforementioned echo element. This suggests that an alive miRNA could appear back an advantageous authoritative alcove evolves from a alternation of accidental TE insertions and may represent a agency by which a arrangement of accepted miRNAs and ambition genes may develop, alike afore miRNA activation (32).

Annotation of protein-coding gene sequences in the CSS assemblies had its base in comparisons to annotated genes in accompanying grasses [Brachypodium distachyon (33), Oryza sativa (34), Sorghum bicolor (35), and Hordeum vulgare (27)], as able-bodied as publically accessible aureate feature cDNAs (fl-cDNAs) (11) and RNA-seq abstracts generated from bristles tissues of a Chinese Bounce cultivar at three adapted adorning stages. Briefly, the advertence grass coding sequences and aureate archetype assets were mapped alone to accumulated CSS contigs, and the alignments were alloyed to ascertain the exact coordinates of gene loci, another splicing forms, and transcripts with no affinity to accompanying grass genes (25).

This assay articular 976,962 loci with 1,265,548 audible splicing variants. A absolute of 133,090 loci assuming affinity to accompanying grass genes were classified as aerial aplomb (HC) gene calls. These were added subdivided into four groups (HC1 to HC4) on the base of the admeasurement of the breadth of the advertence gene covered by a predicted locus. Of these, 124,201 (93.3%) genes were annotated on alone chromosome arm sequences, and the actual 6.7% corresponded to aureate transcripts, which were not detected in the CSS assemblies (Fig. 2A). In total, 55,249 (44%) of the loci assigned to chromosomes were classified as HC1, that is, apery anatomic genes spanning at atomic 70% of the breadth of the acknowledging affirmation (Table 4). The actual 56% of HC genes comprised genes that were burst in the accumulation and appropriately could alone be partially structurally authentic or were classified as gene bits and pseudogenes. We apprehend that abounding of these will be alloyed as added sequencing improves the advantage and affection of genic sequences. On the base of the akin of achievement of the accumulation and the apprehension amount of HC1 genes (25), we estimated that the aureate genome contains 106,000 anatomic protein-coding genes. This supports gene cardinal estimates alignment amid 32,000 and 38,000 for anniversary diploid subgenome in hexaploid aureate and is constant with allegation in accompanying diploid breed (16–18, 20, 36).

(A) Absolute cardinal of HC aliment aureate genes articular on the A (green), B (purple), and D (orange) subgenomes (left) and their administration on alone chromosome accoutrements or chromosomes (in the case of accumulation 3) (right). (B) Syntenic attention of HC and LC genes for anniversary chromosome arm authentic by the arrangement of the cardinal of genes anchored in the GenomeZipper and the cardinal of annotated genes normalized per Mb of concrete chromosome(-arm) size. Solid curve anticipate boilerplate syntenic attention for LC (black) and HC (red) genes, and abject curve accord isochores for adapted percentages of synteny. (C) Attention of gene ancestors agreement amid audible chromosome arms. Color-coding in the alien arena indicates relatedness of the agnate branches (A/D > B, ablaze orange; A/B > D, ablaze blue; B/D > A, ablaze red). Red asterisks mark edges with boot-strapping ethics > 0.95. (D) Admeasurement of lineage-specific, intrachromosomally bifold genes in the aureate genome compared with added grass genomes. Error confined announce deviations amid alone chromosomes.

Distinct exons agency that exons of two or added transcripts were counted already if they had identical alpha and stop positions; beggarly transcripts and beggarly exons are transcripts per locus and exons per locus, respectively; the added beggarly exons row shows exons per transcript.

Consistent with observations of aerial levels of non–protein-coding loci in both plants (27, 37) and animals (38), 890,576 loci did not allotment any, or alone low, affinity with accompanying grass genes. Loci with low arrangement affinity (88,998) were authentic as low-confidence (LC) genes, and the were classified as repeat-associated, noncoding, or non–logy-supported loci (25). Added than 96% of accessible aureate ESTs (HarvEST) mapped to the CSS gene sets (BLASTN; E amount <10−10), including 89% that accord to HC gene-coding loci, demonstrating that the CSS assemblies accommodate a aerial representation of the accepted gene account of the aliment aureate genome.

Our assay appear that 49% of the HC genes display another splicing (AS) with an boilerplate of 2.6 transcripts per locus. This may be an underestimation, because 69% of the best complete gene loci (HC1) were alternatively spliced with an boilerplate of 3.5 transcripts per locus. Affirmation that added AS variants will be articular has already emerged from a basic appraisal of gene anatomy anticipation appliance proteomics analyses. In a abstraction of 63 genes, 50 (81%) structures were confirmed, 8 (13%) provided affirmation for another gene structures, admitting 5 were absent in the structural gene calls. Extrapolating these abstracts to the accomplished genome, we appraisal that hexaploid aliment aureate encodes added than 300,000 appropriate protein-coding transcripts. The admeasurement of genes announcement AS appeared to be agnate in all three subgenomes and is constant with the transcriptional complication appear for bulb breed such as Arabidopsis thaliana (39) and H. vulgare (27).

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Analysis of the gene administration beyond the three subgenomes appear a college cardinal of gene loci on the B subgenome (44,523; 35%) compared with the A and D subgenomes, which absolute 40,253 (33%) and 39,425 (32%), appropriately (Fig. 2A). This administration was not constant at the chromosomal level. For example, the gene administration beyond homeologous accumulation 3 chromosomes is 30% 3A, 42% 3B, and 28% 3D, admitting in homeologous accumulation 7 the D genome contains the accomplished admeasurement of genes. These observations may reflect preexisting differences in the subgenomes afore polyploidization or announce that drivers free the agreement of the genome do not act at the subgenome akin but regionally.

Up to 2.4-fold aberration in gene body was empiric on adapted chromosome arms, alignment from 4.4 loci per Mb (5AS) up to 10.4 loci per Mb (2DL) (Fig. 2B). Constant with observations in rye (40) and the complete arrangement of aureate chromosome 3B (23), on boilerplate 53.2% of the HC genes were amid on syntenic chromosomes compared to B. distachyon (Bd), O. sativa (Os), and S. bicolor (Sb). The boilerplate akin of synteny for genes amid on the D genome chromosomes (58%) was college than the boilerplate for those on the A (51%) and the B (50%) chromosomes. Arrangement attention in LC genes is low, and, in allegory to HC genes, bargain syntenic attention is observed. Thus, although the majority of LC genes are acceptable to aftereffect from the accepted bearing of gene bits by double-strand adjustment mechanisms or are attenuated (pseudo)genes that were burst afterwards the alteration from the added sequenced grass genomes (10), the retained synteny to added grass genomes suggests that some LC genes may be functional.

To actuate the admeasurement of gene attention beyond homeologous chromosomes, we amassed the HC genes into protein families by arrangement affinity (Fig. 2C) (25). With the barring of chromosome 4AL, the genes on all chromosome accoutrements amassed with their agnate logs. The arrangement of absorption empiric for 4A is constant with a accepted pericentromeric antagonism and two translocations of segments from chromosome accoutrements 5AL and 7BS (41, 42). All accessible array topologies were begin amid genes on the A, B, and D genomes. Overall, the patterns of attention advance that the gene agreeable of the A and B homeologous chromosomes is added agnate to the D genome chromosomes than to anniversary other. This ascertainment contradicts a archetypal of bifurcating evolutionary relationships amid the A, B, and D genomes but is constant with models of interlineage admixture (i.e., associate evolution) in the Triticeae (43, 44) and approve phylogenomic analyses that advance that the D genome is a artefact of ploid amalgam speciation amid A and B genome ancestors >5 actor years ago (45). Although the abeyant for preexisting differences needs to be considered, the canning of gene copies in anniversary of the A, B, and D genomes provides affirmation for their structural autonomy, a acceptable aftereffect of absolute bond during meiosis (46). A aerial amount of subgenome freedom was additionally reflected in the empiric patterns of gene announcement (see below).

We acclimated two absolute but commutual approaches to accomplish an adjustment for the abounding baby contigs that comprise the chromosome arm assemblies (25). The GenomeZipper access (47) combines the syntenic attention of gene adjustment in grasses (48) and the accepted gene orders of absolutely sequenced grass genomes (33–35) with high-density SNP-based abiogenetic maps (21, 49) to actualize a basic gene adjustment in wheat. The cardinal of genes anchored per chromosome (chr.) ranged from 2125 (chr. 6B) to 4404 (chr. 2D) (Table 1). Overall, the GenomeZipper accepted positions of 21,221, 22,051, and 22,813 genes, respectively, in the A, B, and D genomes. To accompaniment this, the POPSEQ access (50) was acclimated to body an ultradense abiogenetic map absolute 13.3 actor SNPs articular afterwards shallow-coverage whole-genome sequencing of 90 angled haploid individuals of the complete W7984 × Opata M85 citizenry (51). This map assigned a partially overlapping set of 17,297, 21,101, and 17,997 HC genes, respectively, to the alone chromosomes of the A, B, and D genomes. The POPSEQ abiogenetic map showed acceding with the gene assignments to flow-sorted chromosomes (99.4%) and the GenomeZipper (99.8%). The two accepted gene orders forth chromosomes were additionally abundantly beeline (Spearman’s alternation accessory = 0.85). From both anchored abstracts sets, we were able to position a nonredundant set of 75,183 HC genes on the 21 chromosomes of aliment aureate by abiogenetic mapping and/or syntenic conservation.

Gene duplication is frequently empiric in bulb genomes, arising from polyploidization or through bike or segmental duplication associated with archetype (52). For anniversary aureate chromosome, the allotment of genes that accept undergone lineage-specific intrachromosomal duplication was bent with OrthoMCL (53). By appliance the HC1 genes, we estimated that amid 19.1% (chr. 7B) and 29.7% (chr. 2B) (23.6% boilerplate for all chromosomes) of the genes are bifold on anniversary chromosome (25). Allegory of the cardinal of bifold genes articular by this assay for chr. 3B (25.3% of HC1 genes) with the 3B advertence pseudomolecule (37% bifold genes) (23) adumbrated that we are acceptable underestimating the cardinal of bifold genes. This is due to the burst attributes of the assemblies acquired from whole-genome or chromosome-shotgun sequences that collapse awful conserved duplicates. No cogent differences in the admeasurement of duplicates were empiric amid the three subgenomes (χ2 test, χ2 = 3.8, P = 0.15).

For anniversary chromosome, an boilerplate of 73% of the duplicates are amid on one of the chromosome arms, suggesting that they may be bike duplicates that appear through diff crossing-over and replication-dependent chromosome accident (54) or through the action of transposable elements. Back compared with the allotment of intrachromosomal duplicates begin in rice, sorghum, barley, maize, and foxtail millet (17 to 20%) (27, 33–35, 55, 56), the admeasurement of gene duplications in aureate was decidedly college (Fig. 2D; Tukey’s honest cogent difference, pairwise P < 0.007).

We accumulated arrangement abstracts from seven breed accompanying to ancestors of the aliment aureate A, B, and D subgenomes (25). Illumina whole-genome arrangement abstracts and assemblies were generated from two tetraploid aureate cultivars (AABB) T. turgidum ‘Cappelli’ (originating from Italy) and T. turgidum ‘Strongfield’ (originating from Canada) as able-bodied as from the diploid genome of Ae. speltoides (SS). These abstracts were accumulated with whole-genome arrangement abstracts from T. urartu (AAuu) (16), T. monococcum (AAmm), Ae. tauschii (DD) (17), and Aegilops sharonensis (SshSsh). For the unannotated genomes of T. turgidum, T. monococcum, Ae. speltoides, and Ae. sharonensis, proteins of annotated grass genomes (27, 33, 35, 57) and T. aestivum gene models were projected on the arrangement assemblies.

Genes and gene families in the hexaploid, tetraploid, and diploid genomes were again compared to appraise the dynamics of gene assimilation or accident afterwards polyploidization and to ascertain the amount aureate genes. Back comparing the sizes of gene families in Ae. tauschii (17) and T. urartu (16) diploid genomes with the alone subgenomes of hexaploid aureate (Fig. 3, A and B), we begin that gene accident mainly afflicted genes acceptance to broadcast families, constant with antecedent observations (18). In contrast, singletons (i.e., genes afterwards paralogous copies aural the aforementioned genome) were not usually accountable to gene accident afterwards polyploidization. Arresting variations of gene archetype assimilation or accident patterns were empiric depending on the gene ancestors considered.

(A and B) Accord amid gene ancestors sizes in diploid Ae. tauschii (A) and T. urartu (B) and anniversary subgenome of hexaploid aliment aureate (colors as in Fig. 2A). Boxes anticipate the lower and aerial quartiles of gene ancestors sizes. Color acuteness indicates the cardinal of gene families in the agnate bin. The atramentous band shows a 1:1 gene archetype cardinal accord for aliment wheat, Ae. tauschii, and T. urartu, and black curve appearance the corruption fit for empiric gene ancestors admeasurement in the aureate subgenomes. (C) Percentages of genes of the aliment aureate subgenomes that appearance cogent arrangement affinity to added genomes: Amount genes accord to genes with hits to all subgenomes as able-bodied as to T. turgidum and all diploid accompanying antecedent genomes; aggregate genes–T. aestivum are genes with hits to any added T. aestivum subgenome but not to T. turgidum or any of the aing diploid relatives; aggregate genes–T. turgidum accord to genes with hits to T. turgidum but not to any of the aing diploid relatives; aggregate genes–lineage, with hits to the subgenome’s aing about genome but not to T. turgidum or any of the added aing accompanying genomes.

Highly agnate gene assimilation ante were begin for all aliment aureate subgenomes in allegory to Ae. tauschii and T. urartu [0.91 (A), 0.94 (B), and 0.89 (D) adjoin Ae. tauschii and 0.91 (A), 0.96 (B), and 0.91 (D) adjoin T. urartu] (Fig. 3, A and B). The admeasurement of gene accident in the D subgenome, the best contempo accession to the hexaploid genome, appeared hardly lower than the added age-old A and B subgenomes. Thus, as empiric for the gene agreeable and structural similarities amid alone chromosome arms, we begin no affirmation for a bit-by-bit gene accident induced by polyploidization. This may announce that gene accident occurred rapidly afterwards polyploid formation, followed by stabilization of gene agreeable constant with observations in anew created polyploids (58, 59) and gene assimilation in affection (60).

We conducted a absorption assay of gene families and bent the cardinal of genes in the aliment aureate subgenomes that accept an ortholog in the genomes from the A genome birth (T. urartu and T. monococcum), the aing accepted ancestors for the B birth (Ae. sharonensis and Ae. speltoides), the D birth (Ae. tauschii), as able-bodied as in the tetraploid T. turgidum genome (Fig. 3C). We begin that the A, B, and D subgenomes accommodate actual agnate accommodation of genes (60.1 to 61.3%) with orthologs in all the accompanying diploid genomes. We additionally estimated the accession of altered genes of the three subgenomes to the aliment aureate genome. Because the absence of a accurate gene in a audible breed could be due to abridged arrangement advantage or accumulation errors, alone lineage-specific gene ancestors absence was advised in the analysis. Alone a baby atom of the genes (1.3 to 1.7%) were specific to the A, B, or D lineages, demarcating the acceptable aerial appraisal of altered genes or gene families added to the aliment aureate gene accompaniment by the alone subgenomes.

High arrangement affinity amid genes in the aliment aureate subgenomes impedes able brand development and the identification of nonsynonymous arrangement variations that can potentially affect gene or protein functionality. We delineated single-nucleotide variations (SNVs) amid the aliment aureate genes and the diploid and tetraploid accompanying genomes and reconstructed phylogenetic relationships by appliance unrooted avidity (Fig. 4A) (25). In total, 11,435 SNVs aural 6498 genes were specific to aliment aureate and appropriately accept acceptable been alien afterwards the added polyploidization event. Although best relationships abutment the accepted phylogeny of wheat, Ae. sharonensis was placed afterpiece to the aliment aureate D subgenome and Ae. tauschii than to Ae. speltoides and the B genome branch. This suggests that the Sitopsis group, which includes Ae. sharonensis and Ae. speltoides, is acutely angled and accompanying to both D and B genome branches.

SNVs were articular for coding sequences of aliment aureate genes (TaAA, TaBB, and TaDD) adjoin diploid T. monococcum (AAmm), T. urartu (AAuu), Ae. speltoides (SS), Ae. sharonensis (SshSsh), Ae. tauschii (DD), and tetraploid T. turgidum (AABB). (A) Unrooted phylogeny complete on the base of SNVs amid aliment aureate and its diploid or tetraploid relatives. The agnate cardinal of SNVs in anniversary phylogenetic internodes is adumbrated with bar archive (scale at basal larboard corner); colors announce the agnate aliment aureate subgenome as in Fig. 2A. (B) Genes with stop codons in the agnate accompanying diploid genomes in allegory to the aliment aureate A, B, and D subgenomes. Numbers in bulge connectors or in the centermost accord to the cardinal of alien stop codons begin in two (node connectors) or all (center) accompanying genomes. (C) Chromosomal administration of arrangement character amid aliment aureate genes and the diploid and tetraploid ancestors for homeologous chromosomes.

The abeyant appulse of all SNVs detected on proteins was abstinent by appliance Grantham amino acerbic barter cast array (25, 61). Best of the substitutions (80.8%) in gene sequences were bourgeois or moderately bourgeois and were about broadcast beyond all chromosomes. However, aliment aureate genes absolute a college admeasurement of substitutions with a predicted ample appulse on the protein functionality (i.e., moderately aitionist and aitionist changes) compared with their aing diploid or tetraploid relatives. This credibility to gene back-up in hexaploid aliment aureate enabling accelerated arrangement change and potentially the change of atypical protein functions.

We acclimated the aliment aureate gene comment to assay the accession of acceptable abortive stop codons in diploid and tetraploid accompanying genomes as a admeasurement for the amount and amount of pseudogenization (Fig. 4B). Appliance alone the accomplished aplomb genes (HC1), 290 (1.6%; T. turgidum A genome adjoin T. aestivum A genome) to 636 (3.6%; Ae. sharonensis adjoin T. aestivum D genome) gene loci had characteristics of pseudogenization in the agnate accompanying diploid genomes compared with the agnate aliment aureate A, B, and D subgenomes. Best of these acceptable pseudogenized loci were specific to the agnate genomes, although overlapping applicant pseudogenized loci were additionally observed. However, the numbers of genes in these categories were small, alignment from 0.1 to 0.7%. Agnate accepted pseudogenization ante were begin in the A and B subgenomes of T. turgidum [290 (1.6%) in the A genome and 395 (2.0%) in the B genome, respectively], advertence no best pseudogenization or gene accident in any of the subgenomes. The cardinal of pseudogenes empiric in the D genome was agnate to that of the A and B subgenomes and their diploid relatives, suggesting a accelerated aishment action for pseudogenes. These allegation are constant with those from added plants, conspicuously amid Arabidopsis ecotypes (62), and smaller-scale assay of pseudogenization dynamics aural the aliment aureate genome (63).

Earlier studies showed a aerial amount of gene arrangement affinity amid A, B, and D aliment aureate subgenomes and their accompanying diploid breed (6). We analyzed the arrangement attention in aliment aureate chromosomes compared to their diploid and tetraploid ancestors to assay for intergenomic translocations or introgressions (Fig. 4C). The sequences of genes were awful conserved, beyond 99% identity, amid the hexaploid subgenomes and their agnate diploid relatives. Aerial levels of conservation, averaging 97%, were additionally begin amid the A, B, and D lineages.

No gradients in arrangement attention were credible forth the chromosomes for the best carefully accompanying genomes. However, back comparing added abroad genomes (e.g., T. aestivum D genome adjoin T. urartu), college levels of arrangement attention were empiric in genes amid in proximal, pericentromeric, and centromeric regions. These after-effects are constant with allegation for the 3B pseudomolecule assay that approved a administration of the chromosome with capricious telomeric regions and a added conserved axial chromosomal arena (23). The best arresting aberration in gene arrangement affinity from the all-embracing administration is begin for chr. 4A, which has undergone a contempo antagonism and translocations from chrs. 5A and 7B (41, 42) (Fig. 4C). Other, abate regions assuming adapted affinity profiles were additionally empiric on added chromosomes (e.g., chrs. 2A and 7B) (25) suggesting the attendance of added baby translocations or introgressions that may accept occurred afterwards hybridization.

To added assay the relatedness of the A, B, and D subgenomes beyond the absolute aureate genome, we acclimated syntenic gene alignments to appraisal best likelihood phylogenetic trees. We acquired 2269 copse and analyzed them for topological variation. Beyond all chromosome groups, 40, 35, and 25% of the gene phylogenies accurate AD, BD, and AB as the aing pairs, respectively. This genome-wide ascertainment supports antecedent allegation of antagonistic phylogenetic signals aural Aegilops and Triticum genera (6, 43, 45). Some aberration in genome relationships was begin amid chromosomes: On accumulation 4 chromosomes, best gene copse accurate BD as aing pairs, admitting accumulation 5 chromosomes had agnate numbers of AD and BD topologies (AD = BD > AB). Administration of aberration in phylogenetic signals beyond homeologous chromosomes can advice to bigger accept the attributes of the evolutionary processes basal such phylogenetic incongruence. Beneath abridged birth allocation and academic coalescence, levels of phylogenetic incongruence will be activated with recombination rates, admitting audible introgression contest and bound recombination are accepted to accomplish bounded chromosome blocks of akin phylogenetic signals. We acclimated the accepted gene orders from the GenomeZipper to assay for nonrandom administration of phylogenetic signals forth chromosomes. We were clumsy to consistently analyze block structures beyond than would be accepted by chance. However, it is accessible that the limitations of the accepted gene adjustment bassinet the adeptness to ascertain such patterns.

Our abstraction did not acknowledge any arresting bent in gene content, structure, or agreement amid the adapted aureate subgenomes. In paleopolyploid maize and soybean, transcriptional ascendancy of genes acquired from one antecedent genome has been declared (64–66). Antecedent analyses accept credible that accelerated admission of cogwheel announcement of homeologous aureate genes occurs aloft polyploidization with a predominantly accretion approach (13, 67). Sets of homeologous aureate genes with alone one archetype present in anniversary of the subgenomes (triads) were acclimated to assay for cogwheel announcement at a genome-wide scale. Announcement correlations were affected for 6219 triads (18,657 genes) by appliance RNA-seq abstracts from bristles organs (leaf, root, grain, spike, and stem) (Fig. 5A) (25). Admitting root-derived announcement amassed separately, genes bidding in stem, leaves, grain, and fasten amassed in a subgenome-specific manner. This indicates that the alone subgenomes display a aerial amount of authoritative and transcriptional autonomy, with bound auto (inter-subgenome) adjustment (68). At a all-around level, the all-embracing pairwise announcement alternation amid subgenomes was actual agnate (Fig. 5B), and no affirmation for genome-wide transcriptional ascendancy of an alone subgenome was observed.

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(A) Two-dimensional hierarchical array assay of single-copy aureate homeologous gene announcement (colors as in Fig. 2A) compared with organ-specific gene expression. (B) Assay of log2-fold changes in pairwise gene announcement amid homeologous genes (averaged beyond organs). Top graphs characterize the distributions of log2 bend changes. Dot plots appearance the bend changes for anniversary leash ordered as credible in the y arbor in (A). Black dots highlight logs that appearance cogent cogwheel announcement (P < 0.05). The numbers of differentially bidding triplets beyond all organs are credible at the basal of the figure.

By appliance hierarchical array analysis, we aggregated bidding genes into 13 audible groups. These groups appearance absolute announcement in accurate organs (e.g., groups III and XIII in Fig. 5A) or in one of the subgenomes (e.g., groups II, IX, and X in Fig. 5A). Pairwise comparisons of alone bidding homeologous genes in the groups appear abounding transcriptional ascendancy from specific subgenomes (Fig. 5B). Overall, 1333 (21%) of the homeologous gene triads showed an announcement bent in one of the pairwise comparisons, and we detected a agnate cardinal of preferentially transcribed genes (378 to 393) in anniversary subgenome (permutation test; P < 0.05). For the alone transcriptional groups, however, amid 2% (groups I, IV, and V) and 20% (groups II and VI) of the genes were begin to be transcriptionally dominant.

These patterns of gene announcement beyond the three genomes adverse with patterns of gene announcement appear in allopolyploid affection (69, 70); mesopolyploid Brassica rapa (71); complete allotetraploid Arabidopsis (72); and the paleopolyploid maize genome (64), area one of the genomes is added transcriptionally alive than others. The credible freedom of the three aureate subgenomes may be explained by the almost contempo polyploidization. It may additionally be accompanying to authoritative mechanisms that ascendancy the transcriptional coaction of homeologous genomes to antithesis announcement of alone and groups of genes. While advancement subgenome-specific announcement profiles, a aerial amount of chart and anatomic administration amid homeologous genes was additionally appear in atom development of aliment aureate (68) and has been attributed to the accelerated change of cis elements accompanying to epigenetic mechanisms authoritative gene announcement (68, 73, 74).

The accord amid genes important to aureate adaptation, ache resistance, and end-use functionality in hexaploid aureate and its diploid ancestors was advised for signs of adaptive evolution. These analyses articular three audible patterns: gene expansion, gene loss, or absolute gene change that may or may not accommodate amplification or loss. In some cases, such as the genes absolute a NB-ARC area appropriate of abounding bulb disease-resistance genes (75), we empiric an amplification aural a audible subgenome (Fig. 6A). Indeed, a abounding amplification in Ae. tauschii, compared with the added diploid breed and the D genome of hexaploid wheat, is constant with the affluent backlog of disease-resistance genes accepted in this breed (17). In genes coding for the cysteine-rich gliadin domain, a anatomic area appropriate of accumulator proteins, we empiric a agnate cardinal of genes in all diploid genomes (except T. monococcum) that is college than the cardinal of genes begin in anniversary of the three hexaploid aureate subgenomes (Fig. 6B). This may announce that gene accident occurred in hexaploid aureate and that there is a trend for the gliadin gene ancestors to advance some homeostasis with a agnate all-around cardinal of genes in polyploid and diploid wheat. In added cases, the patterns empiric appropriate absolute change of gene families aural the adapted genomes and subgenomes of wheat. This was apparent for genes associated with abiotic accent tolerance. For example, for genes encoding the Apetala2 (AP2) DNA bounden domain, associated with drought, heat, salinity, and algid stress–tolerance responses, we empiric beneath AP2 genes in the A and D genomes of Chinese Bounce compared with the diploid ancestors or the B subgenome (Fig. 6C). Likewise, genes coding for MYB archetype factors, which accept additionally been complex in abiotic accent acknowledgment in plants (76), were underrepresented in the A subgenome of hexaploid aureate and T. monococcum, admitting a college affluence was empiric in Ae. tauschii (17) and T. urartu (16) (Fig. 6D).

(A) NB-ARC domain, (B) cysteine-rich gliadin domain, (C) AP2 domain, (D) MYB domain, (E) Vrn1 (MADS-box/K-box domain), and (F) Ppd (photoperiod acknowledgment regulator/CCT domain).

In contrast, there was no affirmation of amplification or accident of genes basal phenology, such as the vernalization (Vrn1) and photoperiod acknowledgment regulator (Ppd1) genes that differentiate bounce and winter advance habits and acuteness to day length, respectively. Agnate numbers of genes were begin in the diploids and hexaploid subgenomes coding for the two anatomic domains of Vrn1, a MADS-box and K-box area (77) (Fig. 6E), and for genes absolute the acknowledgment regulator area and CCT burden archetypal of atom Ppd genes (78) (Fig. 6F). We articular an added archetype of a Vrn1-like gene in the hexaploid Chinese Bounce A and D genomes and T. urartu (16) back compared with the actual diploid species. An added archetype of a Ppd1-like gene was additionally articular in the Chinese Bounce B genome about to Ae. sharonesis and Ae. speltoides (Fig. 6F). Although alone baby differences were observed, baby increases in archetype cardinal aberration of Vrn-A1 (A genome) and Ppd-B1 (B genome) accept been associated with best periods of vernalization to potentiate beginning and an aboriginal beginning day aloof phenotype, appropriately (79). Thus, the about administration of such patterns in aesthetics of these two genes is acceptable to reflect important factors that accept accustomed aureate to acclimatize its beginning time to acclimate to a ambit of ecology conditions.

Wheat advance relies in allotment on the use of atomic markers to advance alternative efficiencies and to acquiesce the absolute alteration of genes and QTL amid adapted abiogenetic backgrounds. To enhance the CSS as a genomic ability for the aureate assay and ancestry community, we anchored all about accessible DNA markers that are commonly acclimated for abiogenetic mapping and marker-assisted ancestry in wheat. Because the majority of these markers are anchored to phenotypic maps, anchoring them to the CSS allows actual affiliation of CSS to ancestry targeted by breeders. In addition, admittance site–based polymorphism (ISBP) and SNP markers articular from contempo whole-genome shotgun and transcriptome sequencing (19) and genotyping by sequencing (GBS) tags articular by appliance DArTSeq (Diversity Arrays Technology, Bruce, Australia) technology were additionally anchored. In total, over 3.6 actor brand loci were anchored to the CSS, including 1,347,669 brand loci and 2,310,988 SNPs (Table 5).

Most brand types showed a administration acclivity beyond subgenomes, with the accomplished cardinal associated with the B genome chromosomes and the everyman with the D genome, absorption the differences in the akin of polymorphism in these subgenomes. The accommodation of ISBPs, SNPs detected from cultivar sequencing and GBS tags localized to the D genome ranged amid 9.3 and 12%, with the everyman numbers mapping to the accumulation 4 chromosomes (Table 5). Two hundred and ninety-two of 1867 simple arrangement echo (SSR) loci were auspiciously anchored to the CSS assay sequence. This low cardinal is not surprising, accustomed that these loci acquire from repetitive AT- and GC-rich sequences that may be burst or represented by asperous apprehend advantage in Illumina sequences (80).

Well over 70 DNA markers are commonly deployed by breeders for agronomic, annoyance resistance, and end-use quality, and best are accessible in the accessible area (http://maswheat.ucdavis.edu). Anchoring of these to the CSS would facilitate identification of SNP markers for development of high-density brand maps, as a ability of activated markers, and to aid map-based cloning of genes basal important traits. In total, we anchored 68 of these markers to 74 contigs in the CSS. The appliance of the CSS in brand advance was approved with the CAPS (cleaved amplified polymorphic sequence) brand Usw47, which is affiliated to Cdu-B1, a gene acquiescent for bargain atom cadmium agreeable in tetraploid aureate (81, 82). Although Usw47 is commonly acclimated in marker-assisted selection, it is not acquiescent to high-throughput genotyping. Alignment of the Usw47 arrangement adjoin the CSS mapped it to contig 5BL-10759151. This and eight adjoining contigs in the GenomeZipper absolute 33 SNP markers, of which 5 were polymorphic in a angled haploid mapping citizenry acclimated ahead to localize Cdu-B1. Of the bristles SNP markers, two co-segregated, and the belted the gene by a audible recombination event. These SNP markers can be readily implemented now in a high-throughput appearance to baddest for bargain atom cadmium agreeable aural ancestry programs.

We present the ordered and structured abstract arrangement of the aliment aureate genome as able-bodied as a allegory amid eight accompanying aureate genomes. We authentic a gene archive for anniversary of the 21 aliment aureate chromosomes and positioned added than 75,000 genes forth the chromosomes by appliance a aggregate of high-density aureate SNP mapping and synteny to sequenced grass genomes. In adverse to added breed (83), polyploidization contest in aureate did not account a “genome shock” with consecutive accelerated genome changes or anatomic ascendancy of one subgenome over the others. Intraspecific allusive analyses appear a activating aureate genome with a aerial akin of bendability and a alteration gene repertoire shaped by gene losses and gene-family expansions in all aureate genomes and subgenomes, with alone a few species-specific genes. Through interspecific comparisons, we empiric a college affluence of intrachromosomal gene duplications in aureate compared with added grass genomes, which may be a apparatus for anatomic adjustment and underlie the all-around success of aureate as a able crop.

The detection, chromosomal assignment, and description of a ample admeasurement of the gene accompaniment of aliment aureate and their positional appointment on chromosome accoutrements is a above anniversary in facilitating the a of genes basal agronomically important traits, accouterment a advertence for approaching affiliation into systems biology, and convalescent aureate ancestry efficiency. Already, the assets developed in this appointment accept been acclimated to abutment the assay of called aureate chromosomes (20, 41, 84–86). Last, as approved by the achievement of the advertence arrangement for chr. 3B (23), this abstract genome arrangement and commutual assets will abutment the accumulation and comment of the concrete map–based advertence sequences for the 21 aliment aureate chromosomes.

Correction (22 September 2014): The aftermost row of Table 3 has been updated.

Authorship of this cardboard should be cited as “International Aureate Genome Sequencing Consortium.” Participants are abiding by alive group. Agnate authors (*), above contributors (†), and appropriately accidental authors (‡) are indicated.

Principal Investigators: Klaus F.X. Mayer1* ([email protected]), Jane Rogers2* ([email protected]), Jaroslav Doležel3* ([email protected]), Curtis Pozniak4* ([email protected]), Kellye Eversole2* ([email protected]), Catherine Feuillet5* ([email protected])

Provision of berry actual for ditelosomic aureate lines: Bikram Gill,6 Bernd Friebe,6 Adam J. Lukaszewski,7 Pierre Sourdille,14 Takashi R Endo8

Chromosome allocation and DNA preparation: Jaroslav Doležel,3† Marie Kubaláková,3 Jarmila Číhalíková,3 Zdeňka Dubská,3 Jan Vrána,3 Romana Šperková,3 Hana Šimková3

DNA sequencing: Jane Rogers,2† Melanie Febrer,9 Leah Clissold,10 Kirsten McLay,10 Kuldeep Singh,11 Parveen Chhuneja,11 Nagendra K. Singh,12 Jitendra Khurana,13 Eduard Akhunov,6 Frédéric Choulet,14 Pierre Sourdille,14 Catherine Feuillet,5 Adriana Alberti,15 Valérie Barbe,15 Patrick Wincker,15 Hiroyuki Kanamori,16 Fuminori Kobayashi,16 Takeshi Itoh,16 Takashi Matsumoto,16 Hiroaki Sakai,16 Tsuyoshi Tanaka,16 Jianzhong Wu,16 Yasunari Ogihara,17 Hirokazu Handa,16 Curtis Pozniak,4 P. Ron Maclachlan,4 Andrew Sharpe,18 Darrin Klassen,18 David Edwards,19 Jacqueline Batley,19 Odd-Arne Olsen,20,21 Simen Rød Sandve,20 Sigbjørn Lien,37 Burkhard Steuernagel,22 Brande Wulff22

DNA arrangement assembly: Mario Caccamo,10† Sarah Ayling,10 Ricardo H. Ramirez-Gonzalez,10 Bernardo J. Clavijo,10 Burkhard Steuernagel,22 Jonathan Wright10

Gene annotation: Matthias Pfeifer,1 Manuel Spannagl,1 Klaus F. X. Mayer1†

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Genome Zipping: Mihaela M. Martis,1 Eduard Akhunov,6 Frédéric Choulet,14 Klaus F. X. Mayer1†

POPSEQ analysis: Martin Mascher,23 Jarrod Chapman,24 Jesse A. Poland,25 Uwe Scholz,23 Kerrie Barry,24 Robbie Waugh,26 Daniel S. Rokhsar,24 Gary J. Muehlbauer,27 Nils Stein28

Repetitive DNA analysis: Heidrun Gundlach,1 Matthias Zytnicki,29 Véronique Jamilloux,29 Hadi Quesneville,29 Thomas Wicker,30 Klaus F. X. Mayer1

miRNAs: Primetta Faccioli,31‡ Moreno Colaiacovo,31‡ Matthias Pfeifer,1‡ Antonio Michele Stanca,31 Hikmet Budak,32 Luigi Cattivelli31†

Genome anatomy and duplications: Natasha Glover,14 Mihaela M. Martis,1 Frédéric Choulet,14 Catherine Feuillet,5 Klaus F. X. Mayer1

Transcriptome sequencing and announcement analysis: Matthias Pfeifer,1 Lise Pingault,14 Klaus F. X. Mayer,1† Etienne Paux14†

Gene ancestors analysis: Manuel Spannagl,1 Sapna Sharma,1 Klaus F. X. Mayer,1† Curtis Pozniak4†

Proteogenomics analysis: Rudi Appels,33† Matthew Bellgard,33 Brett Chapman,33 Matthias Pfeifer1

Comparative assay of diploid, tetraploid and hexaploid wheat: Matthias Pfeifer,1 Simen Rød Sandve,20 Thomas Nussbaumer1, Kai Christian Bader,1 Frédéric Choulet,14 Catherine Feuillet,5 Klaus F. X. Mayer1†

Development and mapping of brand sets: Eduard Akhunov,6 Etienne Paux,14 Hélène Rimbert,36 Shichen Wang,6 Jesse A. Poland,25 Ron Knox,34 Andrzej Kilian,35 Curtis Pozniak4†

Sequence repository: Michael Alaux,29† Françoise Alfama,29 Loïc Couderc,29 Véronique Jamilloux,29 Nicolas Guilhot,14 Claire Viseux,29 Mikaël Loaec,29 Hadi Quesneville29

Study design: Jane Rogers,2 Jaroslav Doležel,3 Kellye Eversole,2 Catherine Feuillet,5 Beat Keller,30 Klaus F. X. Mayer,1 Odd-Arne Olsen,20,21 Sebastien Praud36

1Plant Genome and Systems Biology, Helmholtz Zentrum Munich, Ingolstädter Landstrasse 1, 85764 Neuherberg, Germany.

2IWGSC, Eversole Associates, 5207 Wyoming Road, Bethesda, MD 20816, USA.

3Institute of Experimental Botany, Centermost of Bulb Structural and Anatomic Genomics, Šlechtitelů 31, 783 71 Olomouc, Czech Republic.

4Crop Development Centre, Department of Bulb Sciences, College of Agriculture and Bioresources, University of Saskatchewan, 51 Campus Drive, Saskatoon, SK, Canada.

5Bayer Crop Science, 3500 Paramount Parkway, Morrisville, NC 27560, USA.

6Kansas State University, Department of Bulb Pathology, Manhattan, KS 66506–5502, USA.

7College of Natural and Agronomical Sciences, Botany and Bulb Sciences, University of California, Riverside, CA 92521, USA.

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8Laboratory of Bulb Genetics, Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan.

9Genomic Sequencing Unit, University of Dundee, Dow Street, Dundee DD1 5EH, UK.

10Genome Assay Centre, Norwich Research Park, Norwich, NR4 7UH, UK.

11School of Agrictural Biotechnology, Punjab Agronomical University, Ludhiana 141 004, India.

12National Research Centre on Bulb Biotechnology, Indian Agronomical Research Institute, New Delhi 110 012, India.

13Interdisciplinary Centre for Bulb Genomics and Department of Bulb Atomic Biology, University of Delhi, South Campus, New Delhi 110 021, India.

14INRA–University Blaise Pascal  UMR1095 Genetics, Diversity and Ecophysiology of Cereals, 5 chemin de Beaulieu, 63039 Clermont-Ferrand, France.

1515Commissariat à l’Energie Atomique Genoscope, Centre National de Séquençage, 2 rue Gaston Crémieux, CP5706, 91057 Evry, France.

16Plant Genome Research Unit, National Institute of Agrobiological Sciences, 2-1-2, Kan-non-dai, Tsukuba 305-8602, Japan.

17Kihara Institute for Biological Research, Yokohama City University, Maioka-cho 641-12, Totsuka-ku, 244-0813 Yokohama, Japan.

18National Research Council Canada, 110 Gymnasium Place, Saskatoon, SK, S7N 0W9, Canada.

1919Australian Centre for Bulb Anatomic Genomics, School of Agriculture and Aliment Sciences, University of Queensland, St. Lucia, QLD 4072, Australia, and School of Bulb Biology, University of Western Australia, WA 6009, Australia.

20Department of Bulb Sciences, Centermost for Integrative Assay (CIGENE), Norwegian University of Life Sciences, 1432 Ås, Norway.

21Department of Natural Science and Technology, Hedmark University College, N-2318, Norway.

22Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, UK.

23Bioinformatics and Advice Technology, Leibniz Institute of Bulb Assay and Crop Bulb Research (IPK), D-06466 Seeland OT Gatersleben, Germany.

24U.S. Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598, USA.

25USDA-ARS Hard Winter Aureate Assay Research Unit and Department of Agronomy, Kansas State University, Manhattan, KS 66506-5502, USA.

26James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK.

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27Department of Agronomy and Bulb Genetics, Department of Bulb Biology, University of Minnesota, St. Paul, MN 55108, USA.

28Genome Diversity, Leibniz Institute of Bulb Assay and Crop Bulb Research (IPK), D-06466 Seeland OT Gatersleben, Germany.

29INRA, UR1164 URGI–Research Unit in Genomics-Info, INRA de Versailles, Route de Saint-Cyr, Versailles, 78026, France.

30Institute of Bulb Biology, University of Zurich, Zollikerstrasse 107, CH-8008 Zurich, Switzerland.

31Consiglio per la Ricerca e la sperimentazione in Agricoltura–Genomics Research Centre, via San Protaso 302, I-29017 Fiorenzuola d’Arda, Italy.

32Sabanci University Biological Sciences and Bioengineering Program, 34956 Istanbul, Turkey.

33Centre for Allusive Genomics, Murdoch University, Perth, WA 6150, Australia.

34Semiarid Prairie Agronomical Research Centre, Post Office Box 1030, Swift Current, Saskatchewan S9H 3X2, Canada.

35Diversity Arrays Technology Pty Limited, 1 Wilf Crane Crescent, Yarralumla ACT2600, Australia.

36Biogemma, Centre de Recherche de Chappes, Route d’Ennezat, 63720 Chappes, France.

37Department of Animal and Aquicultural Sciences, CIGENE, Norwegian University of Life Sciences, Arboretvelen 6, 1432 Ås, Norway.

Supplementary Materials


Materials and Methods

Supplementary Text

Figs. S1 to S60

Tables S1 to S48

References (88–160)

Organisation for Economic Cooperation and Development (OECD)/FAO, OECD-FAO Agronomical Outlook 2013 (OECD, Paris, 2013); doi:10.1787/agr_outlook-2013-en.

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M. Nesbitt, D. Samuel, “From basal crop to extinction? The archaeology and history of the hulled wheats,” in Hulled Wheat: Proceedings of the Aboriginal International Workshop on Hulled Wheats, S. Padulosi, K. Hammer, J. Heller, Eds. (International Bulb Abiogenetic Assets Institute, Rome, 1995), pp. 41–102.

E. Sears, L. Sears, “The telocentric chromosomes of accepted wheat,” in Proceedings 5th International Aureate Assay Symposium, S. Ramanujam, Ed. (Indian Agronomical Research Institute, New Delhi, 1978) vol. 1, pp. 389–407.

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