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1.  The genetic study utility of a hexaploid wheat DH population with non-recombinant A- and B-genomes 
SpringerPlus  2013;2:131.
To study the D-genome of the wild wheat relative Aegilops tauschii Cosson at the hexaploid level, we developed a synthetic doubled-haploid (DH) hexaploid wheat population, SynDH3. This population was derived from the spontaneous chromosome doubling of triploid F1 hybrid plants obtained from a cross between Triticum turgidum ssp. dicoccon PI377655 and A. tauschii ssp. strangulata AS66 × ssp. tauschii AS87. SynDH3 is a diploidization-hexaploid DH population containing recombinant D chromosomes from two different A. tauschii genotypes, with A and B chromosomes from T. turgidum being homogenous across the entire population. Using this population, we constructed a genetic map. Of the 440 markers used to construct the map, 421 (96%) were assigned to 12 linkage groups; these included 346 Diversity Arrays Technology (DArT) and 75 simple sequence repeat (SSR) markers. The total map length of the seven D chromosomes spanned 916.27 cM, with an average length of 130.90 cM per chromosome and an average distance between markers of 3.47 cM. Seven segregation distortion regions were detected on seven linkage groups. Out of 50 markers shared with those on a common wheat map, 37 showed a consistent order. The utility of the diploidization-hexaploid DH population for mapping qualitative trait genes was confirmed using the dominant glaucousness-inhibiting gene W2I as an example.
Electronic supplementary material
The online version of this article (doi:10.1186/2193-1801-2-131) contains supplementary material, which is available to authorized users.
doi:10.1186/2193-1801-2-131
PMCID: PMC3618880  PMID: 23577301
Allopolyploid; Aegilops tauschii; Doubled-haploid; Segregation distortion
2.  QTug.sau-3B Is a Major Quantitative Trait Locus for Wheat Hexaploidization 
G3: Genes|Genomes|Genetics  2014;4(10):1943-1953.
Meiotic nonreduction resulting in unreduced gametes is thought to be the predominant mechanism underlying allopolyploid formation in plants. Until now, however, its genetic base was largely unknown. The allohexaploid crop common wheat (Triticum aestivum L.), which originated from hybrids of T. turgidum L. with Aegilops tauschii Cosson, provides a model to address this issue. Our observations of meiosis in pollen mother cells from T. turgidum×Ae. tauschii hybrids indicated that first division restitution, which exhibited prolonged cell division during meiosis I, was responsible for unreduced gamete formation. A major quantitative trait locus (QTL) for this trait, named QTug.sau-3B, was detected on chromosome 3B in two T. turgidum×Ae. tauschii haploid populations. This QTL is situated between markers Xgwm285 and Xcfp1012 and covered a genetic distance of 1 cM in one population. QTug.sau-3B is a haploid-dependent QTL because it was not detected in doubled haploid populations. Comparative genome analysis indicated that this QTL was close to Ttam-3B, a collinear homolog of tam in wheat. Although the relationship between QTug.sau-3B and Ttam requires further study, high frequencies of unreduced gametes may be related to reduced expression of Ttam in wheat.
doi:10.1534/g3.114.013078
PMCID: PMC4199700  PMID: 25128436
allopolyploidy; CYCA1;2/TAM; first division restitution; unreduced gametes; Triticum aestivum
3.  Nucleotide diversity maps reveal variation in diversity among wheat genomes and chromosomes 
BMC Genomics  2010;11:702.
Background
A genome-wide assessment of nucleotide diversity in a polyploid species must minimize the inclusion of homoeologous sequences into diversity estimates and reliably allocate individual haplotypes into their respective genomes. The same requirements complicate the development and deployment of single nucleotide polymorphism (SNP) markers in polyploid species. We report here a strategy that satisfies these requirements and deploy it in the sequencing of genes in cultivated hexaploid wheat (Triticum aestivum, genomes AABBDD) and wild tetraploid wheat (Triticum turgidum ssp. dicoccoides, genomes AABB) from the putative site of wheat domestication in Turkey. Data are used to assess the distribution of diversity among and within wheat genomes and to develop a panel of SNP markers for polyploid wheat.
Results
Nucleotide diversity was estimated in 2114 wheat genes and was similar between the A and B genomes and reduced in the D genome. Within a genome, diversity was diminished on some chromosomes. Low diversity was always accompanied by an excess of rare alleles. A total of 5,471 SNPs was discovered in 1791 wheat genes. Totals of 1,271, 1,218, and 2,203 SNPs were discovered in 488, 463, and 641 genes of wheat putative diploid ancestors, T. urartu, Aegilops speltoides, and Ae. tauschii, respectively. A public database containing genome-specific primers, SNPs, and other information was constructed. A total of 987 genes with nucleotide diversity estimated in one or more of the wheat genomes was placed on an Ae. tauschii genetic map, and the map was superimposed on wheat deletion-bin maps. The agreement between the maps was assessed.
Conclusions
In a young polyploid, exemplified by T. aestivum, ancestral species are the primary source of genetic diversity. Low effective recombination due to self-pollination and a genetic mechanism precluding homoeologous chromosome pairing during polyploid meiosis can lead to the loss of diversity from large chromosomal regions. The net effect of these factors in T. aestivum is large variation in diversity among genomes and chromosomes, which impacts the development of SNP markers and their practical utility. Accumulation of new mutations in older polyploid species, such as wild emmer, results in increased diversity and its more uniform distribution across the genome.
doi:10.1186/1471-2164-11-702
PMCID: PMC3022916  PMID: 21156062
4.  Microsatellite Mutation Rate during Allohexaploidization of Newly Resynthesized Wheat 
Simple sequence repeats (SSRs, also known as microsatellites) are known to be mutational hotspots in genomes. DNA rearrangements have also been reported to accompany allopolyploidization. A study of the effect of allopolyploidization on SSR mutation is therefore important for understanding the origin and evolutionary dynamics of SSRs in allopolyploids. Three synthesized double haploid (SynDH) populations were made from 241 interspecific F1 haploid hybrids between Triticum turgidum L. and Aegilops tauschii (Coss.) through spontaneous chromosome doubling via unreduced gametes. Mutation events were studied at 160 SSR loci in the S1 generation (the first generation after chromosome doubling) of the three SynDH populations. Of the 148260 SSR alleles investigated in S1 generation, only one mutation (changed number of repeats) was confirmed with a mutation rate of 6.74 × 10−6. This mutation most likely occurred in the respective F1 hybrid. In comparison with previously reported data, our results suggested that allohexaploidization of wheat did not increase SSR mutation rate.
doi:10.3390/ijms131012533
PMCID: PMC3497285  PMID: 23202911
allopolyploidy; distant hybridization; microsatellite evolution; wheat
5.  A Novel Retrotransposon Inserted in the Dominant Vrn-B1 Allele Confers Spring Growth Habit in Tetraploid Wheat (Triticum turgidum L.) 
G3: Genes|Genomes|Genetics  2011;1(7):637-645.
Vernalization genes determine winter/spring growth habit in temperate cereals and play important roles in plant development and environmental adaptation. In wheat (Triticum L. sp.), it was previously shown that allelic variation in the vernalization gene VRN1 was due to deletions or insertions either in the promoter or in the first intron. Here, we report a novel Vrn-B1 allele that has a retrotransposon in its promoter conferring spring growth habit. The VRN-B1 gene was mapped in a doubled haploid population that segregated for winter-spring growth habit but was derived from two spring tetraploid wheat genotypes, the durum wheat (T. turgidum subsp. durum) variety ‘Lebsock’ and T. turgidum subsp. carthlicum accession PI 94749. Genetic analysis revealed that Lebsock carried the dominant Vrn-A1 and recessive vrn-B1 alleles, whereas PI 94749 had the recessive vrn-A1 and dominant Vrn-B1 alleles. The Vrn-A1 allele in Lebsock was the same as the Vrn-A1c allele previously reported in hexaploid wheat. No differences existed between the vrn-B1 and Vrn-B1 alleles, except that a 5463-bp insertion was detected in the 5′-UTR region of the Vrn-B1 allele. This insertion was a novel retrotransposon (designated as retrotrans_VRN), which was flanked by a 5-bp target site duplication and contained primer binding site and polypurine tract motifs, a 325-bp long terminal repeat, and an open reading frame encoding 1231 amino acids. The insertion of retrotrans_VRN resulted in expression of Vrn-B1 without vernalization. Retrotrans_VRN is prevalent among T. turgidum subsp. carthlicum accessions, less prevalent among T. turgidum subsp. dicoccum accessions, and rarely found in other tetraploid wheat subspecies.
doi:10.1534/g3.111.001131
PMCID: PMC3276170  PMID: 22384375
Triticum turgidum; tetraploid wheat; vernalization; Vrn-B1; retrotransposon
6.  AB-QTL analysis in winter wheat: II. Genetic analysis of seedling and field resistance against leaf rust in a wheat advanced backcross population 
The present study aimed to localize exotic quantitative trait locus (QTL) alleles for the improvement of leaf rust (P.triticina) resistance in an advanced backcross (AB) population, B22, which is derived from a cross between the winter wheat cultivar Batis (Triticumaestivum) and the synthetic wheat accession Syn022L. The latter was developed from hybridization of T.turgidum ssp. dicoccoides and T.tauschii. Altogether, 250 BC2F3 lines of B22 were assessed for seedling resistance against the leaf rust isolate 77WxR under controlled conditions. In addition, field resistance against leaf rust was evaluated by assessing symptom severity under natural infestation across multiple environments. Simultaneously, population B22 was genotyped with a total of 97 SSR markers, distributed over the wheat A, B and D genomes. The phenotype and genotype data were subjected to QTL analysis by applying a 3-factorial mixed model analysis of variance including the marker genotype as a fixed effect and the environments, the lines and the marker by environment interactions as random effects. The QTL analysis revealed six putative QTLs for seedling resistance and seven for field resistance. For seedling resistance, the effects of exotic QTL alleles improved resistance at all detected loci. The maximum decrease of disease symptoms (−46.3%) was associated with marker locus Xbarc149 on chromosome 1D. For field resistance, two loci had stable main effects across environments and five loci exhibited marker by environment interaction effects. The strongest effects were detected at marker locus Xbarc149 on chromosome 1D, at which the exotic allele decreased seedling symptoms by 46.3% and field symptoms by 43.6%, respectively. Some of the detected QTLs co-localized with known resistance genes, while others appear to be as novel resistance loci. Our findings indicate, that the exotic wheat accession Syn022L may be useful for the improvement of leaf rust resistance in cultivated wheat.
doi:10.1007/s00122-008-0738-y
PMCID: PMC2358941  PMID: 18338154
7.  Characterization of Ferredoxin-Dependent Glutamine-Oxoglutarate Amidotransferase (Fd-GOGAT) Genes and Their Relationship with Grain Protein Content QTL in Wheat 
PLoS ONE  2014;9(8):e103869.
Background
In higher plants, inorganic nitrogen is assimilated via the glutamate synthase cycle or GS-GOGAT pathway. GOGAT enzyme occurs in two distinct forms that use NADH (NADH-GOGAT) or Fd (Fd-GOGAT) as electron carriers. The goal of the present study was to characterize wheat Fd-GOGAT genes and to assess the linkage with grain protein content (GPC), an important quantitative trait controlled by multiple genes.
Results
We report the complete genomic sequences of the three homoeologous A, B and D Fd-GOGAT genes from hexaploid wheat (Triticum aestivum) and their localization and characterization. The gene is comprised of 33 exons and 32 introns for all the three homoeologues genes. The three genes show the same exon/intron number and size, with the only exception of a series of indels in intronic regions. The partial sequence of the Fd-GOGAT gene located on A genome was determined in two durum wheat (Triticum turgidum ssp. durum) cvs Ciccio and Svevo, characterized by different grain protein content. Genomic differences allowed the gene mapping in the centromeric region of chromosome 2A. QTL analysis was conducted in the Svevo×Ciccio RIL mapping population, previously evaluated in 5 different environments. The study co-localized the Fd-GOGAT-A gene with the marker GWM-339, identifying a significant major QTL for GPC.
Conclusions
The wheat Fd-GOGAT genes are highly conserved; both among the three homoeologous hexaploid wheat genes and in comparison with other plants. In durum wheat, an association was shown between the Fd-GOGAT allele of cv Svevo with increasing GPC - potentially useful in breeding programs.
doi:10.1371/journal.pone.0103869
PMCID: PMC4123923  PMID: 25099972
8.  Radiation hybrid maps of the D-genome of Aegilops tauschii and their application in sequence assembly of large and complex plant genomes 
BMC Genomics  2015;16:800.
Background
The large and complex genome of bread wheat (Triticum aestivum L., ~17 Gb) requires high resolution genome maps with saturated marker scaffolds to anchor and orient BAC contigs/ sequence scaffolds for whole genome assembly. Radiation hybrid (RH) mapping has proven to be an excellent tool for the development of such maps for it offers much higher and more uniform marker resolution across the length of the chromosome compared to genetic mapping and does not require marker polymorphism per se, as it is based on presence (retention) vs. absence (deletion) marker assay.
Methods
In this study, a 178 line RH panel was genotyped with SSRs and DArT markers to develop the first high resolution RH maps of the entire D-genome of Ae. tauschii accession AL8/78. To confirm map order accuracy, the AL8/78-RH maps were compared with:1) a DArT consensus genetic map constructed using more than 100 bi-parental populations, 2) a RH map of the D-genome of reference hexaploid wheat ’Chinese Spring’, and 3) two SNP-based genetic maps, one with anchored D-genome BAC contigs and another with anchored D-genome sequence scaffolds. Using marker sequences, the RH maps were also anchored with a BAC contig based physical map and draft sequence of the D-genome of Ae. tauschii.
Results
A total of 609 markers were mapped to 503 unique positions on the seven D-genome chromosomes, with a total map length of 14,706.7 cR. The average distance between any two marker loci was 29.2 cR which corresponds to 2.1 cM or 9.8 Mb. The average mapping resolution across the D-genome was estimated to be 0.34 Mb (Mb/cR) or 0.07 cM (cM/cR). The RH maps showed almost perfect agreement with several published maps with regard to chromosome assignments of markers. The mean rank correlations between the position of markers on AL8/78 maps and the four published maps, ranged from 0.75 to 0.92, suggesting a good agreement in marker order. With 609 mapped markers, a total of 2481 deletions for the whole D-genome were detected with an average deletion size of 42.0 Mb. A total of 520 markers were anchored to 216 Ae. tauschii sequence scaffolds, 116 of which were not anchored earlier to the D-genome.
Conclusion
This study reports the development of first high resolution RH maps for the D-genome of Ae. tauschii accession AL8/78, which were then used for the anchoring of unassigned sequence scaffolds. This study demonstrates how RH mapping, which offered high and uniform resolution across the length of the chromosome, can facilitate the complete sequence assembly of the large and complex plant genomes.
Electronic supplementary material
The online version of this article (doi:10.1186/s12864-015-2030-2) contains supplementary material, which is available to authorized users.
doi:10.1186/s12864-015-2030-2
PMCID: PMC4609151  PMID: 26475137
Aegilops tauschii; Deletion; Physical mapping; Radiation hybrid mapping; Sequence assembly; Wheat
9.  Retention of D genome chromosomes in pentaploid wheat crosses 
Heredity  2011;107(4):315-319.
The transfer of genes between Triticum aestivum (hexaploid bread wheat) and T. turgidum (tetraploid durum wheat) holds considerable potential for genetic improvement of both these closely related species. Five different T. aestivum/T. turgidum ssp. durum crosses were investigated using Diversity Arrays Technology (DArT) markers to determine the inheritance of parental A, B and D genome material in subsequent generations derived from these crosses. The proportions of A, B and D chromosomal segments inherited from the hexaploid parent were found to vary significantly among individual crosses. F2 populations retained widely varying quantities of D genome material, ranging from 99% to none. The relative inheritance of bread wheat and durum alleles in the A and B genomes of derived lines also varied among the crosses. Within any one cross, progeny without D chromosomes in general had significantly more A and B genome durum alleles than lines retaining D chromosomes. The ability to select for and manipulate this non-random segregation in bread wheat/durum crosses will assist in efficient backcrossing of selected characters into the recurrent durum or hexaploid genotype of choice. This study illustrates the utility of DArT markers in the study of inter-specific crosses to commercial crop species.
doi:10.1038/hdy.2011.17
PMCID: PMC3182498  PMID: 21427754
Triticum aestivum; Triticum turgidum; pentaploid crosses; DArTs
10.  The cuticular wax inhibitor locus Iw2 in wild diploid wheat Aegilops tauschii: phenotypic survey, genetic analysis, and implications for the evolution of common wheat 
BMC Plant Biology  2014;14:246.
Background
Cuticular wax production on plant surfaces confers a glaucous appearance and plays important roles in plant stress tolerance. Most common wheat cultivars, which are hexaploid, and most tetraploid wheat cultivars are glaucous; in contrast, a wild wheat progenitor, Aegilops tauschii, can be glaucous or non-glaucous. A dominant non-glaucous allele, Iw2, resides on the short arm of chromosome 2D, which was inherited from Ae. tauschii through polyploidization. Iw2 is one of the major causal genes related to variation in glaucousness among hexaploid wheat. Detailed genetic and phylogeographic knowledge of the Iw2 locus in Ae. tauschii may provide important information and lead to a better understanding of the evolution of common wheat.
Results
Glaucous Ae. tauschii accessions were collected from a broad area ranging from Armenia to the southwestern coastal part of the Caspian Sea. Linkage analyses with five mapping populations showed that the glaucous versus non-glaucous difference was mainly controlled by the Iw2 locus in Ae. tauschii. Comparative genomic analysis of barley and Ae. tauschii was then used to develop molecular markers tightly linked with Ae. tauschii Iw2. Chromosomal synteny around the orthologous Iw2 regions indicated that some chromosomal rearrangement had occurred during the genetic divergence leading to Ae. tauschii, barley, and Brachypodium. Genetic associations between specific Iw2-linked markers and respective glaucous phenotypes in Ae. tauschii indicated that at least two non-glaucous accessions might carry other glaucousness-determining loci outside of the Iw2 locus.
Conclusion
Allelic differences at the Iw2 locus were the main contributors to the phenotypic difference between the glaucous and non-glaucous accessions of Ae. tauschii. Our results supported the previous assumption that the D-genome donor of common wheat could have been any Ae. tauschii variant that carried the recessive iw2 allele.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-014-0246-y) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-014-0246-y
PMCID: PMC4172845  PMID: 25224598
Allopolyploid speciation; Cuticluar wax inhibitor; Synthetic wheat; Wheat evolution
11.  Physical mapping of a large plant genome using global high-information-content-fingerprinting: the distal region of the wheat ancestor Aegilops tauschii chromosome 3DS 
BMC Genomics  2010;11:382.
Background
Physical maps employing libraries of bacterial artificial chromosome (BAC) clones are essential for comparative genomics and sequencing of large and repetitive genomes such as those of the hexaploid bread wheat. The diploid ancestor of the D-genome of hexaploid wheat (Triticum aestivum), Aegilops tauschii, is used as a resource for wheat genomics. The barley diploid genome also provides a good model for the Triticeae and T. aestivum since it is only slightly larger than the ancestor wheat D genome. Gene co-linearity between the grasses can be exploited by extrapolating from rice and Brachypodium distachyon to Ae. tauschii or barley, and then to wheat.
Results
We report the use of Ae. tauschii for the construction of the physical map of a large distal region of chromosome arm 3DS. A physical map of 25.4 Mb was constructed by anchoring BAC clones of Ae. tauschii with 85 EST on the Ae. tauschii and barley genetic maps. The 24 contigs were aligned to the rice and B. distachyon genomic sequences and a high density SNP genetic map of barley. As expected, the mapped region is highly collinear to the orthologous chromosome 1 in rice, chromosome 2 in B. distachyon and chromosome 3H in barley. However, the chromosome scale of the comparative maps presented provides new insights into grass genome organization. The disruptions of the Ae. tauschii-rice and Ae. tauschii-Brachypodium syntenies were identical. We observed chromosomal rearrangements between Ae. tauschii and barley. The comparison of Ae. tauschii physical and genetic maps showed that the recombination rate across the region dropped from 2.19 cM/Mb in the distal region to 0.09 cM/Mb in the proximal region. The size of the gaps between contigs was evaluated by comparing the recombination rate along the map with the local recombination rates calculated on single contigs.
Conclusions
The physical map reported here is the first physical map using fingerprinting of a complete Triticeae genome. This study demonstrates that global fingerprinting of the large plant genomes is a viable strategy for generating physical maps. Physical maps allow the description of the co-linearity between wheat and grass genomes and provide a powerful tool for positional cloning of new genes.
doi:10.1186/1471-2164-11-382
PMCID: PMC2900270  PMID: 20553621
12.  Identification of quantitative trait loci controlling grain size and shape in the D genome of synthetic hexaploid wheat lines 
Breeding Science  2013;63(4):423-429.
Synthetic hexaploid wheat is an effective genetic resource for transferring agronomically important genes from Aegilops tauschii to common wheat. Wide variation in grain size and shape, one of the main targets for wheat breeding, has been observed among Ae. tauschii accessions. To identify the quantitative trait loci (QTLs) responsible for grain size and shape variation in the wheat D genome under a hexaploid genetic background, six parameters related to grain size and shape were measured using SmartGrain digital image software and QTL analysis was conducted using four F2 mapping populations of wheat synthetic hexaploids. In total, 18 QTLs for the six parameters were found on five of the seven D-genome chromosomes. The identified QTLs significantly contributed to the variation in grain size and shape among the synthetic wheat lines, implying that the D-genome QTLs might be at least partly functional in hexaploid wheat. Thus, synthetic wheat lines with diverse D genomes from Ae. tauschii are useful resources for the identification of agronomically important loci that function in hexaploid wheat.
doi:10.1270/jsbbs.63.423
PMCID: PMC3859354  PMID: 24399915
allopolyploidization; grain shape; quantitative trait locus; synthetic wheat
13.  Genetic Diversity and Population Structure of Tetraploid Wheats (Triticum turgidum L.) Estimated by SSR, DArT and Pedigree Data 
PLoS ONE  2013;8(6):e67280.
Levels of genetic diversity and population genetic structure of a collection of 230 accessions of seven tetraploid Triticum turgidum L. subspecies were investigated using six morphological, nine seed storage protein loci, 26 SSRs and 970 DArT markers. The genetic diversity of the morphological traits and seed storage proteins was always lower in the durum wheat compared to the wild and domesticated emmer. Using Bayesian clustering (K = 2), both of the sets of molecular markers distinguished the durum wheat cultivars from the other tetraploid subspecies, and two distinct subgroups were detected within the durum wheat subspecies, which is in agreement with their origin and year of release. The genetic diversity of morphological traits and seed storage proteins was always lower in the improved durum cultivars registered after 1990, than in the intermediate and older ones. This marked effect on diversity was not observed for molecular markers, where there was only a weak reduction. At K >2, the SSR markers showed a greater degree of resolution than for DArT, with their identification of a greater number of groups within each subspecies. Analysis of DArT marker differentiation between the wheat subspecies indicated outlier loci that are potentially linked to genes controlling some important agronomic traits. Among the 211 loci identified under selection, 109 markers were recently mapped, and some of these markers were clustered into specific regions on chromosome arms 2BL, 3BS and 4AL, where several genes/quantitative trait loci (QTLs) are involved in the domestication of tetraploid wheats, such as the tenacious glumes (Tg) and brittle rachis (Br) characteristics. On the basis of these results, it can be assumed that the population structure of the tetraploid wheat collection partially reflects the evolutionary history of Triticum turgidum L. subspecies and the genetic potential of landraces and wild accessions for the detection of unexplored alleles.
doi:10.1371/journal.pone.0067280
PMCID: PMC3694930  PMID: 23826256
14.  Heterochronic development of the floret meristem determines grain number per spikelet in diploid, tetraploid and hexaploid wheats 
Annals of Botany  2009;104(2):243-251.
Background and Aims
The inflorescence of grass species such as wheat, rice and maize consists of a unique reproductive structure called the spikelet, which is comprised of one, a few, or several florets (individual flowers). When reproductive growth is initiated, the inflorescence meristem differentiates a spikelet meristem as a lateral branch; the spikelet meristem then produces a floret meristem as a lateral branch. Interestingly, in wheat, the number of fertile florets per spikelet is associated with ploidy level: one or two florets in diploid, two or three in tetraploid, and more than three in hexaploid wheats. The objective of this study was to identify the mechanisms that regulate the architecture of the inflorescence in wheat and its relationship to ploidy level.
Methods
The floral anatomy of diploid (Triticum monococcum), tetraploid (T. turgidum ssp. durum) and hexaploid (T. aestivum) wheat species were investigated by light and scanning electron microscopy to describe floret development and to clarify the timing of the initiation of the floret primordia. In situ hybridization analysis using Wknox1, a wheat knotted1 orthologue, was performed to determine the patterning of meristem formation in the inflorescence.
Key Results
The recessive natural mutation of tetraploid (T. turgidum ssp. turgidum) wheat, branching head (bh), which produces branched inflorescences, was used to demonstrate the utility of Wknox1 as a molecular marker for meristematic tissue. Then an analysis of Wknox1 expression was performed in diploid, tetraploid and hexaploid wheats and heterochronic development of the floret meristems was found among these wheat species.
Conclusions
It is shown that the difference in the number of floret primordia in diploid, tetraploid and hexaploid wheats is caused by the heterochronic initiation of floret meristem development from the spikelet meristem.
doi:10.1093/aob/mcp129
PMCID: PMC2710895  PMID: 19491089
Triticum; wheat; inflorescence; spikelet; floret; meristem; heterochrony; heterochronic development; knotted1; polyploidy
15.  Genetic Basis for Spontaneous Hybrid Genome Doubling during Allopolyploid Speciation of Common Wheat Shown by Natural Variation Analyses of the Paternal Species 
PLoS ONE  2013;8(8):e68310.
The complex process of allopolyploid speciation includes various mechanisms ranging from species crosses and hybrid genome doubling to genome alterations and the establishment of new allopolyploids as persisting natural entities. Currently, little is known about the genetic mechanisms that underlie hybrid genome doubling, despite the fact that natural allopolyploid formation is highly dependent on this phenomenon. We examined the genetic basis for the spontaneous genome doubling of triploid F1 hybrids between the direct ancestors of allohexaploid common wheat (Triticum aestivum L., AABBDD genome), namely Triticumturgidum L. (AABB genome) and Aegilopstauschii Coss. (DD genome). An Ae. tauschii intraspecific lineage that is closely related to the D genome of common wheat was identified by population-based analysis. Two representative accessions, one that produces a high-genome-doubling-frequency hybrid when crossed with a T. turgidum cultivar and the other that produces a low-genome-doubling-frequency hybrid with the same cultivar, were chosen from that lineage for further analyses. A series of investigations including fertility analysis, immunostaining, and quantitative trait locus (QTL) analysis showed that (1) production of functional unreduced gametes through nonreductional meiosis is an early step key to successful hybrid genome doubling, (2) first division restitution is one of the cytological mechanisms that cause meiotic nonreduction during the production of functional male unreduced gametes, and (3) six QTLs in the Ae. tauschii genome, most of which likely regulate nonreductional meiosis and its subsequent gamete production processes, are involved in hybrid genome doubling. Interlineage comparisons of Ae. tauschii’s ability to cause hybrid genome doubling suggested an evolutionary model for the natural variation pattern of the trait in which non-deleterious mutations in six QTLs may have important roles. The findings of this study demonstrated that the genetic mechanisms for hybrid genome doubling could be studied based on the intrinsic natural variation that exists in the parental species.
doi:10.1371/journal.pone.0068310
PMCID: PMC3738567  PMID: 23950867
16.  Registration of wheat lines carrying the partial stripe rust resistance gene Yr36 without the Gpc-B1 high grain protein content allele 
Journal of plant registrations  2012;7(1):108-112.
While the high-temperature adult plant resistance gene Yr36 represents a promising source of quantitative and potentially race non-specific resistance to wheat stripe rust (causal organism Puccinia striiformis Westend. f. sp. tritici), its tight linkage (0.3 cM) with the high-grain protein content gene Gpc-B1 may hinder its introgression in certain cases, such as in soft wheat varieties requiring low grain protein content or in lines where the Gpc-B1 allele may be associated with a yield penalty. The development and registration of two donor lines, one tetraploid (Triticum turgidum L. ssp. durum; PI 656793) and one hexaploid (T. aestivum L. ssp. aestivum; PI 664549), each carrying the resistant wild emmer (T. turgidum ssp. dicoccoides) allele for Yr36 linked with the non-functional Gpc-B1 allele, are intended to overcome this potential limitation. Meiotic recombination events breaking the linkage between these two genes were discovered during the systematic screening of a population of 4,500 F2 durum plants (cv. Langdon background) used to fine map Yr36. One of the critical recombination events was selected for fixation by self-pollination and transferred to a California adapted spring hexaploid background (breeding line UC11105+10) through five generations of backcrossing. Genotypic and phenotypic data confirm the presence of Yr36 and the non-functional Gpc-B1 allele in both registered lines.
doi:10.3198/jpr2012.03.0150crg
PMCID: PMC4780365  PMID: 26962384
17.  Mapping of Ppd-B1, a Major Candidate Gene for Late Heading on Wild Emmer Chromosome Arm 2BS and Assessment of Its Interactions with Early Heading QTLs on 3AL 
PLoS ONE  2016;11(2):e0147377.
Wheat heading date is an important agronomic trait determining maturation time and yield. A set of common wheat (Triticum aestivum var. Chinese Spring; CS)-wild emmer (T. turgidum L. subsp. dicoccoides (TDIC)) chromosome arm substitution lines (CASLs) was used to identify and allocate QTLs conferring late or early spike emergence by examining heading date. Genetic loci accelerating heading were found on TDIC chromosome arms 3AL and 7BS, while loci delaying heading were located on 4AL and 2BS. To map QTLs conferring late heading on 2BS, F2 populations derived from two cross combinations of CASL2BS × CS and CASL3AL × CASL2BS were developed and each planted at two times, constituting four F2 mapping populations. Heading date varied continuously among individuals of these four populations, suggesting quantitative characteristics. A genetic map of 2BS, consisting of 23 SSR and one single-stranded conformation polymorphism (SSCP) marker(s), was constructed using these F2 populations. This map spanned a genetic length of 53.2 cM with average marker density of 2.3 cM. The photoperiod-sensitivity gene Ppd-B1 was mapped to chromosome arm 2BS as a SSCP molecular marker, and was validated as tightly linked to a major QTL governing late heading of CASL2BS in all mapping populations. A significant dominance by additive effect of Ppd-B1 with the LUX gene located on 3AL was also detected. CS had more copies of Ppd-B1 than CASL2BS, implying that increased copy number could elevate the expression of Ppd-1 in CS, also increasing expression of LUX and FT genes and causing CS to have an earlier heading date than CASL2BS in long days.
doi:10.1371/journal.pone.0147377
PMCID: PMC4743932  PMID: 26848576
18.  Mixed Model Association Mapping for Fusarium Head Blight Resistance in Tunisian-Derived Durum Wheat Populations 
G3: Genes|Genomes|Genetics  2011;1(3):209-218.
Sources of resistance to Fusarium head blight (FHB) in wheat are mostly restricted to Chinese hexaploid genotypes. The effort to incorporate the resistance from hexaploid wheat or wild relatives to cultivated durum wheat (Triticum turgidum L. var. durum Desf.) have not been successful in providing resistance to the level of the donor parents. In this study, we used 171 BC1F6 and 169 BC1F7 lines derived from crossing of four Tunisian tetraploid sources of resistance (Tun7, Tun18, Tun34, Tun36) with durum cultivars ‘Ben,’ ‘Maier,’ ‘Lebsock,’ and ‘Mountrail’ for association studies. The Tun18 and Tun7 FHB resistances were found to be comparable to the best hexaploid wheat sources. A new significant QTL for FHB resistance was identified on the long arm of chromosome 5B (Qfhs.ndsu-5BL) with both association and classical QTL mapping analysis. Linkage disequilibrium (LD) blocks extending up to 40 cM were evident in these populations. The linear mixed model considering the structure (Q or P) and the kinship matrix (KT) estimated by restricted maximum likelihood (REML) was identified as the best for association studies in a mixture of wheat populations from a breeding program. The results of association mapping analysis also demonstrated a region on the short arm of chromosome 3B as potentially linked to FHB resistance. This region is in proximity of major FHB resistance gene fhb1 reported in hexaploid wheat. A possibility of having susceptibility or suppressor of resistance gene(s) on durum wheat chromosome 2A was further confirmed in this material, explaining the problem in developing resistant genotypes without counter selection against this region.
doi:10.1534/g3.111.000489
PMCID: PMC3276138  PMID: 22384332
association mapping; durum wheat; Fusarium head blight; QTL analysis; suppressor of resistance
19.  Ancestral QTL Alleles from Wild Emmer Wheat Improve Drought Resistance and Productivity in Modern Wheat Cultivars 
Wild emmer wheat (Triticum turgidum ssp. dicoccoides) is considered a promising source for improving stress resistances in domesticated wheat. Here we explored the potential of selected quantitative trait loci (QTLs) from wild emmer wheat, introgressed via marker-assisted selection, to enhance drought resistance in elite durum (T. turgidum ssp. durum) and bread (T. aestivum) wheat cultivars. The resultant near-isogenic lines (BC3F3 and BC3F4) were genotyped using SNP array to confirm the introgressed genomic regions and evaluated in two consecutive years under well-watered (690–710 mm) and water-limited (290–320 mm) conditions. Three of the introgressed QTLs were successfully validated, two in the background of durum wheat cv. Uzan (on chromosomes 1BL and 2BS), and one in the background of bread wheat cvs. Bar Nir and Zahir (chromosome 7AS). In most cases, the QTL x environment interaction was validated in terms of improved grain yield and biomass—specifically under drought (7AS QTL in cv. Bar Nir background), under both treatments (2BS QTL), and a greater stability across treatments (1BL QTL). The results provide a first demonstration that introgression of wild emmer QTL alleles can enhance productivity and yield stability across environments in domesticated wheat, thereby enriching the modern gene pool with essential diversity for the improvement of drought resistance.
doi:10.3389/fpls.2016.00452
PMCID: PMC4832586  PMID: 27148287
interspecific introgression; marker-assisted selection; near-isogenic line; Triticum turgidum ssp. dicoccoides; quantitative trait locus; water stress; wheat; yield
20.  Identification and mapping of leaf, stem and stripe rust resistance quantitative trait loci and their interactions in durum wheat 
Molecular Breeding  2012;31(2):405-418.
Leaf rust (Puccinia triticina Eriks.), stripe rust (Puccinia striiformis f. tritici Eriks.) and stem rust (Puccinia graminis f. sp. tritici) cause major production losses in durum wheat (Triticum turgidum L. var. durum). The objective of this research was to identify and map leaf, stripe and stem rust resistance loci from the French cultivar Sachem and Canadian cultivar Strongfield. A doubled haploid population from Sachem/Strongfield and parents were phenotyped for seedling reaction to leaf rust races BBG/BN and BBG/BP and adult plant response was determined in three field rust nurseries near El Batan, Obregon and Toluca, Mexico. Stripe rust response was recorded in 2009 and 2011 nurseries near Toluca and near Njoro, Kenya in 2010. Response to stem rust was recorded in field nurseries near Njoro, Kenya, in 2010 and 2011. Sachem was resistant to leaf, stripe and stem rust. A major leaf rust quantitative trait locus (QTL) was identified on chromosome 7B at Xgwm146 in Sachem. In the same region on 7B, a stripe rust QTL was identified in Strongfield. Leaf and stripe rust QTL around DArT marker wPt3451 were identified on chromosome 1B. On chromosome 2B, a significant leaf rust QTL was detected conferred by Strongfield, and at the same QTL, a Yr gene derived from Sachem conferred resistance. Significant stem rust resistance QTL were detected on chromosome 4B. Consistent interactions among loci for resistance to each rust type across nurseries were detected, especially for leaf rust QTL on 7B. Sachem and Strongfield offer useful sources of rust resistance genes for durum rust breeding.
doi:10.1007/s11032-012-9798-4
PMCID: PMC3565083  PMID: 23396999
Durum; Leaf; Stem; Stripe; Rust; QTL
21.  Development of diversity array technology (DArT) markers for assessment of population structure and diversity in Aegilops tauschii 
Breeding Science  2012;62(1):38-45.
Aegilops tauschii Coss. is the D-genome donor to hexaploid bread wheat (Triticum aestivum) and is the most promising wild species as a genetic resource for wheat breeding. To study the population structure and diversity of 81 Ae. tauschii accessions collected from various regions of its geographical distribution, the genomic representation of these lines were used to develop a diversity array technology (DArT) marker array. This Ae. tauschii array and a previously developed DArT wheat array were used to scan the genomes of the 81 accessions. Out of 7500 markers (5500 wheat and 2000 Ae. tauschii), 4449 were polymorphic (3776 wheat and 673 Ae. tauschii). Phylogenetic and population structure studies revealed that the accessions could be divided into three groups. The two Ae. tauschii subspecies could also be separately clustered, suggesting that the current taxonomy might be valid. DArT markers are effective to detect very small polymorphisms. The information obtained about Ae. tauschii in the current study could be useful for wheat breeding. In addition, the new DArT array from this Ae. tauschii population is expected to be an effective tool for hexaploid wheat studies.
doi:10.1270/jsbbs.62.38
PMCID: PMC3405951  PMID: 23136512
Aegilops tauschii; Triticum aestivum; synthetic wheat; DArT markers; drought tolerance
22.  Application of Population Sequencing (POPSEQ) for Ordering and Imputing Genotyping-by-Sequencing Markers in Hexaploid Wheat 
G3: Genes|Genomes|Genetics  2015;5(12):2547-2553.
The advancement of next-generation sequencing technologies in conjunction with new bioinformatics tools enabled fine-tuning of sequence-based, high-resolution mapping strategies for complex genomes. Although genotyping-by-sequencing (GBS) provides a large number of markers, its application for association mapping and genomics-assisted breeding is limited by a large proportion of missing data per marker. For species with a reference genomic sequence, markers can be ordered on the physical map. However, in the absence of reference marker order, the use and imputation of GBS markers is challenging. Here, we demonstrate how the population sequencing (POPSEQ) approach can be used to provide marker context for GBS in wheat. The utility of a POPSEQ-based genetic map as a reference map to create genetically ordered markers on a chromosome for hexaploid wheat was validated by constructing an independent de novo linkage map of GBS markers from a Synthetic W7984 × Opata M85 recombinant inbred line (SynOpRIL) population. The results indicated that there is strong agreement between the independent de novo linkage map and the POPSEQ mapping approach in mapping and ordering GBS markers for hexaploid wheat. After ordering, a large number of GBS markers were imputed, thus providing a high-quality reference map that can be used for QTL mapping for different traits. The POPSEQ-based reference map and whole-genome sequence assemblies are valuable resources that can be used to order GBS markers and enable the application of highly accurate imputation methods to leverage the application GBS markers in wheat.
doi:10.1534/g3.115.020362
PMCID: PMC4683627  PMID: 26530417
GBS; WGS; POPSEQ; linkage map; imputation
23.  Waxy genes from spelt wheat: new alleles for modern wheat breeding and new phylogenetic inferences about the origin of this species 
Annals of Botany  2012;110(6):1161-1171.
Background and Aims
Waxy proteins are responsible for amylose synthesis in wheat seeds, being encoded by three waxy genes (Wx-A1, Wx-B1 and Wx-D1) in hexaploid wheat. In addition to their role in starch quality, waxy loci have been used to study the phylogeny of wheat. The origin of European spelt (Triticum aestivum ssp. spelta) is not clear. This study compared waxy gene sequences of a Spanish spelt collection with their homologous genes in emmer (T. turgidum ssp. dicoccum), durum (T. turgidum ssp. durum) and common wheat (T. aestivum ssp. aestivum), together with other Asian and European spelt that could be used to determine the origin of European spelt.
Methods
waxy genes were amplified and sequenced. Geneious Pro software, DNAsp and MEGA5 were used for sequence, nucleotide diversity and phylogenetic analysis, respectively.
Key Results
Three, four and three new alleles were described for the Wx-A1, Wx-B1 and Wx-D1 loci, respectively. Spelt accessions were classified into two groups based on the variation in Wx-B1, which suggests that there were two different origins for the emmer wheat that has been found to be part of the spelt genetic make-up. One of these groups was only detected in Iberian material. No differences were found between the rest of the European spelt and the Asiatic spelt, which suggested that the Iberian material had a different origin from the other spelt sources.
Conclusions
The results suggested that the waxy gene variability present in wheat is undervalued. The evaluation of this variability has permitted the detection of ten new waxy alleles that could affect starch quality and thus could be used in modern wheat breeding. In addition, two different classes of Wx-B1 were detected that could be used for evaluating the phylogenetic relationships and the origins of different types of wheat.
doi:10.1093/aob/mcs201
PMCID: PMC3478059  PMID: 22984164
Wheat; Triticum aestivum ssp. spelta; molecular characterization; phylogeny; spelt origin; waxy genes
24.  Mapping of QTL for Fusarium head blight resistance and morphological and developmental traits in three backcross populations derived from Triticum dicoccum × Triticum durum 
Breeding for resistance to Fusarium head blight (FHB) in durum wheat continues to be hindered by the lack of effective resistance sources. Only limited information is available on resistance QTL for FHB in tetraploid wheat. In this study, resistance to FHB of a Triticum dicoccum line in the background of three Austrian T. durum cultivars was genetically characterized. Three populations of BC1F4-derived RILs were developed from crosses between the resistant donor line T. dicoccum-161 and the Austrian T. durum recipient varieties DS-131621, Floradur and Helidur. About 130 BC1F4-derived lines per population were evaluated for FHB response using artificial spray inoculation in four field experiments during two seasons. Lines were genetically fingerprinted using SSR and AFLP markers. Genomic regions on chromosomes 3B, 4B, 6A, 6B and 7B were significantly associated with FHB severity. FHB resistance QTL on 6B and 7B were identified in two populations and a resistance QTL on 4B appeared in three populations. The alleles that enhanced FHB resistance were derived from the T. dicoccum parent, except for the QTL on chromosome 3B. All QTL except the QTL on 6A mapped to genomic regions where QTL for FHB have previously been reported in hexaploid wheat. QTL on 3B and 6B coincided with Fhb1 and Fhb2, respectively. This implies that tetraploid and hexaploid wheat share common genomic regions associated with FHB resistance. QTL for FHB resistance on 4B co-located with a major QTL for plant height and mapped at the position of the Rht-B1 gene, while QTL on 7B overlapped with QTL for flowering time.
Electronic supplementary material
The online version of this article (doi:10.1007/s00122-012-1951-2) contains supplementary material, which is available to authorized users.
doi:10.1007/s00122-012-1951-2
PMCID: PMC3493669  PMID: 22926291
25.  Molecular organization and comparative analysis of chromosome 5B of the wild wheat ancestor Triticum dicoccoides 
Scientific Reports  2015;5:10763.
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.
doi:10.1038/srep10763
PMCID: PMC4471722  PMID: 26084265

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