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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.
PMCID: PMC3618880  PMID: 23577301
Allopolyploid; Aegilops tauschii; Doubled-haploid; Segregation distortion
2.  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.
PMCID: PMC3497285  PMID: 23202911
allopolyploidy; distant hybridization; microsatellite evolution; wheat
3.  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.
PMCID: PMC3182498  PMID: 21427754
Triticum aestivum; Triticum turgidum; pentaploid crosses; DArTs
4.  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.
PMCID: PMC3276170  PMID: 22384375
Triticum turgidum; tetraploid wheat; vernalization; Vrn-B1; retrotransposon
5.  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.
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.
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.
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.
PMCID: PMC2900270  PMID: 20553621
6.  Hypersensitive Response-Like Reaction Is Associated with Hybrid Necrosis in Interspecific Crosses between Tetraploid Wheat and Aegilops tauschii Coss 
PLoS ONE  2010;5(6):e11326.
Hybrid speciation is classified into homoploid and polyploid based on ploidy level. Common wheat is an allohexaploid species that originated from a naturally occurring interploidy cross between tetraploid wheat and diploid wild wheat Aegilops tauschii Coss. Aegilops tauschii provides wide naturally occurring genetic variation. Sometimes its triploid hybrids with tetraploid wheat show the following four types of hybrid growth abnormalities: types II and III hybrid necrosis, hybrid chlorosis, and severe growth abortion. The growth abnormalities in the triploid hybrids could act as postzygotic hybridization barriers to prevent formation of hexaploid wheat.
Methodology/Principal Findings
Here, we report on the geographical and phylogenetic distribution of Ae. tauschii accessions inducing the hybrid growth abnormalities and showed that they are widely distributed across growth habitats in Ae. tauschii. Molecular and cytological characterization of the type III necrosis phenotype was performed. The hybrid abnormality causing accessions were widely distributed across growth habitats in Ae. tauschii. Transcriptome analysis showed that a number of defense-related genes such as pathogenesis-related genes were highly up-regulated in the type III necrosis lines. Transmission electron microscope observation revealed that cell death occurred accompanied by generation of reactive oxygen species in leaves undergoing type III necrosis. The reduction of photosynthetic activity occurred prior to the appearance of necrotic symptoms on the leaves exhibiting hybrid necrosis.
Taking these results together strongly suggests that an autoimmune response might be triggered by intergenomic incompatibility between the tetraploid wheat and Ae. tauschii genomes in type III necrosis, and that genetically programmed cell death could be regarded as a hypersensitive response-like cell death similar to that observed in Arabidopsis intraspecific and Nicotiana interspecific hybrids. Only Ae. tauschii accessions without such inhibiting factors could be candidates for the D-genome donor for the present hexaploid wheat.
PMCID: PMC2892878  PMID: 20593003
7.  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.
PMCID: PMC3738567  PMID: 23950867
8.  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.
PMCID: PMC3405951  PMID: 23136512
Aegilops tauschii; Triticum aestivum; synthetic wheat; DArT markers; drought tolerance
9.  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.
PMCID: PMC3859354  PMID: 24399915
allopolyploidization; grain shape; quantitative trait locus; synthetic wheat
10.  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.
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.
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.
PMCID: PMC2710895  PMID: 19491089
Triticum; wheat; inflorescence; spikelet; floret; meristem; heterochrony; heterochronic development; knotted1; polyploidy
11.  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.
PMCID: PMC3276138  PMID: 22384332
association mapping; durum wheat; Fusarium head blight; QTL analysis; suppressor of resistance
12.  Characterization of HMW-GS and evaluation of their diversity in morphologically elite synthetic hexaploid wheats 
Breeding Science  2012;62(4):365-370.
High molecular weight glutenin subunit composition and variation in 95 Elite-1 synthetic hexaploid (SH) wheats (Triticum turgidum/Aegilops tauschii; 2n = 6× = 42; AABBDD) were determined by sodium dodecyl sulphate polyacrylamide gel electrophoresis method (SDS-PAGE). Twenty two different alleles at Glu-1 loci in SHs were observed. Forty four different patterns of HMW-GS in synthetics were found. This higher HMW glutenin composition was due to higher proportion of D-genome encoded subunits in these SHs. 8% urea/SDS-PAGE better discriminated subunit 2* than 12% gels. However 12% urea/SDS-PAGE allowed differentiated mobility of Glu-Dt1 subunits. Genetic variability at Glu-Dt1 locus was greater than Glu-A1 and Glu-B1 loci. The relative high frequency of superior alleles, Glu-B1b and Glu-Dt1d indicated the superior bread making quality attributes embedded in these synthetic hexaploid wheats. Of the 95 Elite-1 SHs 27.1% possessed superior alleles at Glu-A1 and 51% had superior alleles at Glu-B1 locus. At Glu-Dt1 frequency of inferior allele 1Dx2 + 1Dy12 was very low (5.26%) and nine different rare alleles along with the higher frequency (22.1%) of D-genome encoded subunit, 1Dx5 + 1Dy10, were observed. These superior alleles shall form the priority selective sieve for their usage in wheat improvement efforts.
PMCID: PMC3528335  PMID: 23341752
synthetic hexaploid wheats; bread making quality; HMW-GS; Aegilops tauschii
13.  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.
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.
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.
PMCID: PMC3478059  PMID: 22984164
Wheat; Triticum aestivum ssp. spelta; molecular characterization; phylogeny; spelt origin; waxy genes
14.  Structural Analysis of the Wheat Genes Encoding NADH-Dependent Glutamine-2-oxoglutarate Amidotransferases and Correlation with Grain Protein Content 
PLoS ONE  2013;8(9):e73751.
Nitrogen uptake and the efficient absorption and metabolism of nitrogen are essential elements in attempts to breed improved cereal cultivars for grain or silage production. One of the enzymes related to nitrogen metabolism is glutamine-2-oxoglutarate amidotransferase (GOGAT). Together with glutamine synthetase (GS), GOGAT maintains the flow of nitrogen from NH4+ into glutamine and glutamate, which are then used for several aminotransferase reactions during amino acid synthesis.
The aim of the present work was to identify and analyse the structure of wheat NADH-GOGAT genomic sequences, and study the expression in two durum wheat cultivars characterized by low and high kernel protein content. The genomic sequences of the three homoeologous A, B and D NADH-GOGAT genes were obtained for hexaploid Triticum aestivum and the tetraploid A and B genes of Triticum turgidum ssp. durum. Analysis of the gene sequences indicates that all wheat NADH-GOGAT genes are composed of 22 exons and 21 introns. The three hexaploid wheat homoeologous genes have high conservation of sequence except intron 13 which shows differences in both length and sequence. A comparative analysis of sequences among di- and mono-cotyledonous plants shows both regions of high conservation and of divergence. qRT-PCR performed with the two durum wheat cvs Svevo and Ciccio (characterized by high and low protein content, respectively) indicates different expression levels of the two NADH-GOGAT-3A and NADH-GOGAT-3B genes.
The three hexaploid wheat homoeologous NADH-GOGAT gene sequences are highly conserved – consistent with the key metabolic role of this gene. However, the dicot and monocot amino acid sequences show distinctive patterns, particularly in the transit peptide, the exon 16–17 junction, and the C-terminus. The lack of conservation in the transit peptide may indicate subcellular differences between the two plant divisions - while the sequence conservation within enzyme functional domains remains high. Higher expression levels of NADH-GOGAT are associated with higher grain protein content in two durum wheats.
PMCID: PMC3775782  PMID: 24069228
15.  Variation in Dehydration Tolerance, ABA Sensitivity and Related Gene Expression Patterns in D-Genome Progenitor and Synthetic Hexaploid Wheat Lines 
The wild wheat Aegilops tauschii Coss. has extensive natural variation available for breeding of common wheat. Drought stress tolerance is closely related to abscisic acid (ABA) sensitivity. In this study, 17 synthetic hexaploid wheat lines, produced by crossing the tetraploid wheat cultivar Langdon with 17 accessions of Ae. tauschii, were used for comparative analysis of natural variation in drought tolerance and ABA sensitivity. Ae. tauschii showed wide natural variation, with weak association between the traits. Drought-sensitive accessions of Ae. tauschii exhibited significantly less ABA sensitivity. D-genome variations observed at the diploid genome level were not necessarily reflected in synthetic wheats. However, synthetic wheats derived from the parental Ae. tauschii accessions with high drought tolerance were significantly more tolerant to drought stress than those from drought-sensitive accessions. Moreover, synthetic wheats with high drought tolerance showed significantly higher ABA sensitivity than drought-sensitive synthetic lines. In the hexaploid genetic background, therefore, weak association of ABA sensitivity with drought tolerance was observed. To study differences in gene expression patterns between stress-tolerant and -sensitive lines, levels of two Cor/Lea and three transcription factor gene transcripts were compared. The more tolerant accession of Ae. tauschii tended to accumulate more abundant transcripts of the examined genes than the sensitive accession under stress conditions. The expression patterns in the synthetic wheats seemed to be additive for parental lines exposed to drought and ABA treatments. However, the transcript levels of transcription factor genes in the synthetic wheats did not necessarily correspond to the postulated levels based on expression in parental lines. Allopolyploidization altered the expression levels of the stress-responsive genes in synthetic wheats.
PMCID: PMC2705513  PMID: 19582226
abscisic acid; allopolyploidization; drought stress; natural variation; synthetic wheat
16.  Nucleotide diversity maps reveal variation in diversity among wheat genomes and chromosomes 
BMC Genomics  2010;11:702.
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.
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.
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.
PMCID: PMC3022916  PMID: 21156062
17.  Introgression and Characterization of a Goatgrass Gene for a High Level of Resistance to Ug99 Stem Rust in Tetraploid Wheat 
G3: Genes|Genomes|Genetics  2012;2(6):665-673.
The transfer of alien genes to crop plants using chromosome engineering has been attempted infrequently in tetraploid durum wheat (Triticum turgidum L. subsp. durum). Here, we report a highly efficient approach for the transfer of two genes conferring resistance to stem rust race Pgt-TTKSK (Ug99) from goatgrass (Aegilops speltoides) to tetraploid wheat. The durum line DAS15, carrying the stem rust resistance gene Sr47 derived from Ae. speltoides, was crossed, and backcrossed, to durum 5D(5B) aneuploids to induce homeologous pairing. After a final cross to ‘Rusty’ durum, allosyndetic recombinants were recovered. The Ae. speltoides chromosomal segment carrying Sr47 was found to have two stem rust resistance genes. One gene conditioning an infection type (IT) 2 was located in the same chromosomal region of 2BS as Sr39 and was assigned the temporary gene symbol SrAes7t. Based on ITs observed on a diverse set of rust races, SrAes7t may be the same as Sr39. The second gene conditioned an IT 0; and was located on chromosome arm 2BL. This gene retained the symbol Sr47 because it had a different IT and map location from other stem rust resistance genes derived from Ae. speltoides. Allosyndetic recombinant lines carrying each gene on minimal alien chromosomal segments were identified as were molecular markers distinguishing each alien segment. This study demonstrated that chromosome engineering of Ae. speltoides segments is feasible in tetraploid wheat. The Sr47 gene confers high-level and broad spectrum resistance to stem rust and should be very useful in efforts to control TTKSK.
PMCID: PMC3362296  PMID: 22690376
wheat; Ug99; Sr47; Aegilops speltoides; chromosome engineering
18.  Global transgenerational gene expression dynamics in two newly synthesized allohexaploid wheat (Triticum aestivum) lines 
BMC Biology  2012;10:3.
Alteration in gene expression resulting from allopolyploidization is a prominent feature in plants, but its spectrum and extent are not fully known. Common wheat (Triticum aestivum) was formed via allohexaploidization about 10,000 years ago, and became the most important crop plant. To gain further insights into the genome-wide transcriptional dynamics associated with the onset of common wheat formation, we conducted microarray-based genome-wide gene expression analysis on two newly synthesized allohexaploid wheat lines with chromosomal stability and a genome constitution analogous to that of the present-day common wheat.
Multi-color GISH (genomic in situ hybridization) was used to identify individual plants from two nascent allohexaploid wheat lines between Triticum turgidum (2n = 4x = 28; genome BBAA) and Aegilops tauschii (2n = 2x = 14; genome DD), which had a stable chromosomal constitution analogous to that of common wheat (2n = 6x = 42; genome BBAADD). Genome-wide analysis of gene expression was performed for these allohexaploid lines along with their parental plants from T. turgidum and Ae. tauschii, using the Affymetrix Gene Chip Wheat Genome-Array. Comparison with the parental plants coupled with inclusion of empirical mid-parent values (MPVs) revealed that whereas the great majority of genes showed the expected parental additivity, two major patterns of alteration in gene expression in the allohexaploid lines were identified: parental dominance expression and non-additive expression. Genes involved in each of the two altered expression patterns could be classified into three distinct groups, stochastic, heritable and persistent, based on their transgenerational heritability and inter-line conservation. Strikingly, whereas both altered patterns of gene expression showed a propensity of inheritance, identity of the involved genes was highly stochastic, consistent with the involvement of diverse Gene Ontology (GO) terms. Nonetheless, those genes showing non-additive expression exhibited a significant enrichment for vesicle-function.
Our results show that two patterns of global alteration in gene expression are conditioned by allohexaploidization in wheat, that is, parental dominance expression and non-additive expression. Both altered patterns of gene expression but not the identity of the genes involved are likely to play functional roles in stabilization and establishment of the newly formed allohexaploid plants, and hence, relevant to speciation and evolution of T. aestivum.
PMCID: PMC3313882  PMID: 22277161
19.  Applicability of Aegilops tauschii drought tolerance traits to breeding of hexaploid wheat 
Breeding Science  2011;61(4):347-357.
Few genes are available to develop drought-tolerant bread wheat (Triticum aestivum L.) cultivars. One way to enhance bread wheat’s genetic diversity would be to take advantage of the diversity of wild species by creating synthetic hexaploid wheat (SW) with the genomic constitution of bread wheat. In this study, we compared the expression of traits encoded at different ploidy levels and evaluated the applicability of Aegilops tauschii drought-related traits using 33 Ae. tauschii accessions along with their corresponding SW lines under well-watered and drought conditions. We found wide variation in Ae. tauschii, and even wider variation in the SW lines. Some SW lines were more drought-tolerant than the standard cultivar Cham 6. Aegilops tauschii from some regions gave better performing SW lines. The traits of Ae. tauschii were not significantly correlated with their corresponding SW lines, indicating that the traits expressed in wild diploid relatives of wheat may not predict the traits that will be expressed in SW lines derived from them. We suggest that, regardless of the adaptability and performance of the Ae. tauschii under drought, production of SW could probably result in genotypes with enhanced trait expression due to gene interactions, and that the traits of the synthetic should be evaluated in hexaploid level.
PMCID: PMC3406773  PMID: 23136471
wheat; Aegilops tauschii; synthetic hexaploid wheat; wild relatives of wheat
20.  Metabolite Profiling of a Diverse Collection of Wheat Lines Using Ultraperformance Liquid Chromatography Coupled with Time-of-Flight Mass Spectrometry 
PLoS ONE  2012;7(8):e44179.
Genetic differences among major types of wheat are well characterized; however, little is known about how these distinctions affect the small molecule profile of the wheat seed. Ethanol/water (65% v/v) extracts of seed from 45 wheat lines representing 3 genetically distinct classes, tetraploid durum (Triticum turgidum subspecies durum) (DW) and hexaploid hard and soft bread wheat (T. aestivum subspecies aestivum) (BW) were subjected to ultraperformance liquid chromatography coupled with time-of-flight mass spectrometry (UPLC-TOF-MS). Discriminant analyses distinguished DW from BW with 100% accuracy due to differences in expression of nonpolar and polar ions, with differences attributed to sterol lipids/fatty acids and phospholipids/glycerolipids, respectively. Hard versus soft BW was distinguished with 100% accuracy by polar ions, with differences attributed to heterocyclic amines and polyketides versus phospholipid ions, respectively. This work provides a foundation for identification of metabolite profiles associated with desirable agronomic and human health traits and for assessing how environmental factors impact these characteristics.
PMCID: PMC3431305  PMID: 22957002
21.  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.
PMCID: PMC2358941  PMID: 18338154
22.  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.
PMCID: PMC3565083  PMID: 23396999
Durum; Leaf; Stem; Stripe; Rust; QTL
23.  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.
PMCID: PMC3694930  PMID: 23826256
24.  Rapid Genome Mapping in Nanochannel Arrays for Highly Complete and Accurate De Novo Sequence Assembly of the Complex Aegilops tauschii Genome 
PLoS ONE  2013;8(2):e55864.
Next-generation sequencing (NGS) technologies have enabled high-throughput and low-cost generation of sequence data; however, de novo genome assembly remains a great challenge, particularly for large genomes. NGS short reads are often insufficient to create large contigs that span repeat sequences and to facilitate unambiguous assembly. Plant genomes are notorious for containing high quantities of repetitive elements, which combined with huge genome sizes, makes accurate assembly of these large and complex genomes intractable thus far. Using two-color genome mapping of tiling bacterial artificial chromosomes (BAC) clones on nanochannel arrays, we completed high-confidence assembly of a 2.1-Mb, highly repetitive region in the large and complex genome of Aegilops tauschii, the D-genome donor of hexaploid wheat (Triticum aestivum). Genome mapping is based on direct visualization of sequence motifs on single DNA molecules hundreds of kilobases in length. With the genome map as a scaffold, we anchored unplaced sequence contigs, validated the initial draft assembly, and resolved instances of misassembly, some involving contigs <2 kb long, to dramatically improve the assembly from 75% to 95% complete.
PMCID: PMC3566107  PMID: 23405223
25.  Low temperature-induced necrosis shows phenotypic plasticity in wheat triploid hybrids 
Plant Signaling & Behavior  2011;6(10):1431-1433.
Hybrid necrosis sometimes appears in triploid hybrids between tetraploid wheat and Aegilops tauschii Coss. Two types of hybrid necrosis (type II and type III ) were observed when cultivar Langdon was used as female parent for hybrid production. Type II necrosis symptoms occurred only under low temperature conditions, whereas bushy and dwarf phenotypes were observed under normal temperature conditions. The developmental plasticity might be related to a temperature-responsive alteration of meristematic activity at the crown tissue of triploid hybrids. Epistatic interaction between the AB and D genomes induced not only upregulation of a number of defense-related genes, but also extensive changes in plant architecture in the type II necrosis hybrids. Such phenotypic plasticity was also observed in other cross combinations between cultivated tetraploid wheat and type II necrosis-induced Ae. tauschii accessions. Wild tetraploid wheat, Triticum turgidum subspecies dicoccoides, did not induce type II necrosis in the triploid hybrids, indicating the possibility of identifying the chromosomal location of a causal gene for type II necrosis in the AB genome.
PMCID: PMC3256362  PMID: 21897130
autoimmune response; allopolyploid speciation; common wheat; epistatic interaction; hybrid necrosis; post-zygotic hybridization barrier

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