Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
, 26 (7), 2761-76

Evolution of the BBAA Component of Bread Wheat During Its History at the Allohexaploid Level

Affiliations

Evolution of the BBAA Component of Bread Wheat During Its History at the Allohexaploid Level

Huakun Zhang et al. Plant Cell.

Abstract

Subgenome integrity in bread wheat (Triticum aestivum; BBAADD) makes possible the extraction of its BBAA component to restitute a novel plant type. The availability of such a ploidy-reversed wheat (extracted tetraploid wheat [ETW]) provides a unique opportunity to address whether and to what extent the BBAA component of bread wheat has been modified in phenotype, karyotype, and gene expression during its evolutionary history at the allohexaploid level. We report here that ETW was anomalous in multiple phenotypic traits but maintained a stable karyotype. Microarray-based transcriptome profiling identified a large number of differentially expressed genes between ETW and natural tetraploid wheat (Triticum turgidum), and the ETW-downregulated genes were enriched for distinct Gene Ontology categories. Quantitative RT-PCR analysis showed that gene expression differences between ETW and a set of diverse durum wheat (T. turgidum subsp durum) cultivars were distinct from those characterizing tetraploid cultivars per se. Pyrosequencing revealed that the expression alterations may occur to either only one or both of the B and A homoeolog transcripts in ETW. A majority of the genes showed additive expression in a resynthesized allohexaploid wheat. Analysis of a synthetic allohexaploid wheat and diverse bread wheat cultivars revealed the rapid occurrence of expression changes to the BBAA subgenomes subsequent to allohexaploidization and their evolutionary persistence.

Figures

Figure 1.
Figure 1.
Schematic Representation of the Evolutionary History of Wheat (Triticum) and Related Aegilops Species and the Three Synthetic Polyploid Wheat Lines Used in This Study. Diagrammatic illustration of the divergent speciation of diploid progenitor species (containing A, S [≈B], or D genomes) of polyploid wheat, the evolutionary trajectories and/or domestication processes of natural tetraploid and hexaploid wheats, and the construction (dashed arrows) of the three synthetic polyploid wheat lines used in this study. The synthetic wheat lines (shaded) included an ETW containing the BBAA genomes of a bread wheat cultivar, a resynthesized allohexaploid (XX329) produced by crossing ETW and Ae. tauschii followed by WGD, and a newly synthesized allohexaploid (Allo960) produced by crossing T. turgidum and Ae. tauschii followed by WGD. The estimated evolution or domestication timing is according to Feldman et al. (1995), Huang et al. (2002), and Dvorak and Akhunov (2005). [See online article for color version of this figure.]
Figure 2.
Figure 2.
Description and Characterization of the ETW and Resynthesized Allohexaploid Wheat. (A) Diagrammatic illustration of the pedigree for the construction of ETW from allohexaploid bread wheat (cv Canthach; our designation is TAA10) by hybridization with a tetraploid line of subsp durum (cv Stewart; our designation is TTR13) and repeated backcrossing to the hexaploid parent and resynthesizing allohexaploid wheat (XX329). This is based on Kerber (1964) with additional backcrossing for two times and selfing for propagations. The same genomes in different colors denote intraspecific differentiation. (B) Karyotypes of bread wheat (cv Canthach; our designation is TAA10), ETW, Ae. tauschii (line TQ18), and XX329 based on sequential FISH using four hybridization probes to identify each chromosome pair. (C) Nearly complete euploidy and lack of gross structural rearrangements in both ETW and XX329 were evidenced by karyotyping 150 randomly chosen plant individuals from each line. (D) Typical phenotypes of the bread wheat donor (line TAA10) to ETW, Ae. tauschii (line TQ18), and the resynthesized allohexaploid wheat (XX329). Severely deteriorated phenotypes in spikes and whole plants are evident in ETW, which, however, are fully restored in the resynthesized allohexaploid wheat (XX329) by crossing ETW (maternal parent) and Ae. tauschii (paternal parent). Notably, although kernels of ETW do not show apparent deterioration, its seed-setting rate is conspicuously reduced to only approximately 20%, which is also fully restored in XX329.
Figure 3.
Figure 3.
Transcriptome Differences between or among the Four Allotetraploid Wheat Lines, ETW and T. turgidum subsp durum (cv TTR13), subsp carthlicum (cv Blackbird), and subsp dicoccoides (Line TD265), Based on Affymetrix Wheat Genome Array Analysis. (A) Hierarchical clustering of differentially expressed genes, based on the microarray data, between ETW and each of the three natural allotetraploid subspecies, durum, carthlicum, and dicoccoides, of T. turgidum. All three biological replicates of each line are shown. The color key is indicated at the bottom. (B) Histograms of the total numbers of differentially expressed genes in each of the three pairwise comparisons between ETW and three subspecies, durum, carthlicum, and dicoccoides, of T. turgidum and numbers of upregulated and downregulated genes (vermilion and blue bars, respectively) in each comparison. (C) Histograms of the total numbers of differentially expressed genes between any two and between common genes of durum and carthlicum versus dicoccoides and numbers and proportions of upregulated and downregulated genes (vermilion and blue bars, respectively) in each comparison. (D) Histograms of the total numbers of differentially expressed genes between ETW and any two or all three subspecies, durum, carthlicum, and dicoccoides, of T. turgidum and numbers and proportions of upregulated and downregulated genes (vermilion and blue bars, respectively) in each comparison.
Figure 4.
Figure 4.
Expression Level Differences between ETW and 21 durum Wheat Cultivars of Diverse Origins Based on qRT-PCR Assay in the Seedling Leaf Tissue. (A) Heat maps of expression of 111 genes (Supplemental Data Set 3) in ETW relative to each of 21 durum wheat cultivars of diverse origins based on qRT-PCR assay with three biological replicates. The color key is indicated. (B) A Fisher’s exact test was conducted to test whether the gene expression level difference between ETW and each durum cultivar versus that of normal gene expression divergence among the diverse durum cultivars was equal.
Figure 5.
Figure 5.
Difference in Homoeolog-Specific Expression between ETW and Natural Tetraploid Wheat, T. turgidum. Heat maps of equal or differential expression for each of 51 genes (Supplemental Data Set 2) in ETW relative to each of the three natural subspecies of T. turgidum, durum (cv TTR13) (A), carthlicum (cv Blackbird) (B), and dicoccoides (line TD265) (C), as collective transcripts for each gene based on the microarray data of three biological replicates (left panels) and the relative transcript contribution by the B and A subgenomes for each gene based on cDNA pyrosequencing data (right panels). Differential (top part of each panel) or equal (bottom part of each panel) expression between ETW and each of the three natural subspecies for each of the 51 analyzed genes were determined by statistically significant (FDR, P < 0.05) fold changes (FC) of the microarray data (three biological replications). The relative transcript contribution by the B and A subgenomes for each gene is calculated based on mean ratios of pyrosequencing data of three biological replicates using the same cDNAs as for the microarray analysis. Equal or preferential changes to the B and A subgenome transcripts were determined according to statistically insignificant (t test, P > 0.05) or significant (t test, P < 0.05) changes of the B versus A subgenome transcript ratios between the two partners of each pairwise comparison, which are marked by black and vermilion rectangles for the 51 analyzed genes, respectively. The color keys are indicated.

Similar articles

See all similar articles

Cited by 15 articles

See all "Cited by" articles

Publication types

MeSH terms

Associated data

LinkOut - more resources

Feedback