Origin and evolution of the bread wheat D genome.

Bread wheat (Triticum aestivum) is a globally dominant crop and major source of calories and proteins for the human diet. Compared with its wild ancestors, modern bread wheat shows lower genetic diversity, caused by polyploidisation, domestication and breeding bottlenecks1,2. Wild wheat relatives represent genetic reservoirs, and harbour diversity and beneficial alleles that have not been incorporated into bread wheat. Here we establish and analyse extensive genome resources for Tausch's goatgrass (Aegilops tauschii), the donor of the bread wheat D genome. Our analysis of 46 Ae. tauschii genomes enabled us to clone a disease resistance gene and perform haplotype analysis across a complex disease resistance locus, allowing us to discern alleles from paralogous gene copies. We also reveal the complex genetic composition and history of the bread wheat D genome, which involves contributions from genetically and geographically discrete Ae. tauschii subpopulations. Together, our results reveal the complex history of the bread wheat D genome and demonstrate the potential of wild relatives in crop improvement.

Wheat Ym2 originated from Aegilops sharonensis and confers resistance to soil-borne Wheat yellow mosaic virus infection to the roots.

Wheat yellow mosaic virus (WYMV) is a pathogen transmitted into its host's roots by the soil-borne vector Polymyxa graminis. Ym1 and Ym2 genes protect the host from the significant yield losses caused by the virus, but the mechanistic basis of these resistance genes remains poorly understood. Here, it has been shown that Ym1 and Ym2 act within the root either by hindering the initial movement of WYMV from the vector into the root and/or by suppressing viral multiplication. A mechanical inoculation experiment on the leaf revealed that the presence of Ym1 reduced viral infection incidence, rather than viral titer, while that of Ym2 was ineffective in the leaf. To understand the basis of the root specificity of the Ym2 product, the gene was isolated from bread wheat using a positional cloning approach. The candidate gene encodes a CC-NBS-LRR protein and it correlated allelic variation with respect to its sequence with the host's disease response. Ym2 (B37500) and its paralog (B35800) are found in the near-relatives, respectively, Aegilops sharonensis and Aegilops speltoides (a close relative of the donor of bread wheat's B genome), while both sequences, in a concatenated state, are present in several accessions of the latter species. Structural diversity in Ym2 has been generated via translocation and recombination between the two genes and enhanced by the formation of a chimeric gene resulting from an intralocus recombination event. The analysis has revealed how the Ym2 region has evolved during the polyploidization events leading to the creation of cultivated wheat.

Evolutionary genomics of two diploid goat grass species belonging to the section Sitopsis of Aegilops, Aegilops longissima, and Aegilops sharonensis.

Aegilops longissima and Ae. sharonensis, being classified into the Sitopsis section of genus Aegilops, are distinct species both taxonomically and ecologically. Nevertheless, earlier observations indicate that the two species are not reproductively isolated to full extent and can inter-bred upon secondary contact. However, the genomic underpinnings of the morpho-ecological differentiation between the two foci species remained unexplored. Here, we resequenced 31 representative accessions of the two species and conducted in-depth comparative genomic analyses. We demonstrate recurrent and ongoing natural hybridizations between Ae. longissima and Ae. sharonensis, and depict features of genome composition of the resultant hybrids at both individual and population levels. We also delineate genomic regions and candidate genes potentially underpinning the differential morphological and edaphic adaptations of the two species. Intriguingly, a binary morphology was observed in the hybrids, suggesting existence of highly diverged genomic regions that remain uneroded by the admixtures. Together, our results provide new insights into the molding effects of interspecific hybridization on genome composition and mechanisms preventing merge of the two species.

Ploidy variation induces butterfly effect on chromatin topology in wheat.

Polyploidy is a prominent driver of plant diversification, accompanied with dramatic chromosomal rearrangement and epigenetic changes that affect gene expression. How chromatin interactions within and between subgenomes adapt to ploidy transition remains poorly understood. We generate open chromatin interaction maps for natural hexaploid wheat (AABBDD), extracted tetraploid wheat (AABB), diploid wheat progenitor Aegilops tauschii (DD) and resynthesized hexaploid wheat (RHW, AABBDD). Thousands of intra- and interchromosomal loops are de novo established or disappeared in AB subgenomes after separation of D subgenome, in which 37-95% of novel loops are lost again in RHW after merger of D genome. Interestingly, more than half of novel loops are formed by cascade reactions that are triggered by disruption of chromatin interaction between AB and D subgenomes. The interaction repressed genes in RHW relative to DD are expression suppressed, resulting in more balanced expression of the three homoeologs in RHW. The interaction levels of cascade anchors are decreased step-by-step. Leading single nucleotide polymorphisms of yield- and plant architecture-related quantitative trait locus are significantly enriched in cascade anchors. The expression of 116 genes interacted with these anchors are significantly correlated with the corresponding traits. Our findings reveal trans-regulation of intrachromosomal loops by interchromosomal interactions during genome merger and separation in polyploid species.

Variation of TaMyb10 and their function on grain color and pre-harvest sprouting resistance of wheat.

Pre-harvest sprouting (PHS) is a significant threat to global food security due to its association with losses in both yield and quality. Among the genes involved in PHS resistance in wheat, PHS-3D (TaMyb10-D) plays a crucial role. Here, we characterized the sequence variations of TaMyb10 genes in 416 bread wheat and 302 Aegilops tauschii accessions. Within TaMyb10-A sequences, we identified a deletion ranging from 214 to 305 bp in the signal and amino acid coding region, present in 61.3% of the accessions. Similarly, 79.3% of the TaMyb10-B sequences within the third exon region exhibited a 19 bp deletion. Additionally, 40.8% of the accessions lacked the 2.4 Mb fragment (in/del mutations) on Chr3D, where TaMyb10-D/PHS-3D was located. Interestingly, the geographical distribution of accessions showed little correlation with the divergence of TaMyb10. TaMyb10-A-IIIDele, TaMyb10-B-IVDele, and TaMyb10-D-VDele genotypes were prevalent in wheat populations across continents. Despite their structural variations, the five distinct protein types exhibited comparable ability to bind the promoters of downstream genes in the flavonoid and ABA pathways, such as CHS, DFR, and NCED. Furthermore, the combination of TaMyb10 homologs was significantly associated with grain color and germination percentages. Accessions exclusively harboring TaMyb10-D displayed red seed color and reduced germination percentages, indicating the predominant role of TaMyb10-D compared to TaMyb10-A and TaMyb10-B. This comprehensive investigation enhances our understanding of the structural variations and functional divergence of TaMyb10, providing valuable insights and resources for improving PHS resistance in wheat.

Aegilops tauschii presents a genetic roadmap for hexaploid wheat improvement.

Modern wheat shows phenomenal evolutional success and adaptability to a range of environments owing to polyploidization; however, during its hybridization process a major genetic gain has been overlooked. Recently, Gaurav et al. emphasized harnessing genetic diversity from wheat wild progenitor Aegilops tauschii for the improvement of hexaploid wheat through introgression or transgenesis.

Evolutionary trajectory of organelle-derived nuclear DNAs in the Triticum/Aegilops complex species.

Organelle-derived nuclear DNAs, nuclear plastid DNAs (NUPTs), and nuclear mitochondrial DNAs (NUMTs) have been identified in plants. Most, if not all, genes residing in NUPTs/NUMTs (NUPGs/NUMGs) are known to be inactivated and pseudogenized. However, the role of epigenetic control in silencing NUPGs/NUMGs and the dynamic evolution of NUPTs/NUMTs with respect to organismal phylogeny remain barely explored. Based on the available nuclear and organellar genomic resources of wheat (genus Triticum) and goat grass (genus Aegilops) within Triticum/Aegilops complex species, we investigated the evolutionary fates of NUPTs/NUMTs in terms of their epigenetic silencing and their dynamic occurrence rates in the nuclear diploid genomes and allopolyploid subgenomes. NUPTs and NUMTs possessed similar genomic atlas, including (i) predominantly located in intergenic regions and preferential integration to gene regulation regions and (ii) generating sequence variations in the nuclear genome. Unlike nuclear indigenous genes, the alien NUPGs/NUMGs were associated with repressive epigenetic signals, namely high levels of DNA methylation and low levels of active histone modifications. Phylogenomic analyses suggested that the species-specific and gradual accumulation of NUPTs/NUMTs accompanied the speciation processes. Moreover, based on further pan-genomic analyses, we found significant subgenomic asymmetry in the NUPT/NUMT occurrence, which accumulated during allopolyploid wheat evolution. Our findings provide insight into the dynamic evolutionary fates of organelle-derived nuclear DNA in plants.

Post-hybridization introgression and natural selection promoted genomic divergence of Aegilops speltoides and the four S*-genome diploid species.

Understanding how different driving forces have promoted biological divergence and speciation is one of the central issues in evolutionary biology. The Triticum/Aegilops species complex contains 13 diploid species belonging to the A-, B- and D-lineages and offers an ideal system to address the evolutionary dynamics of lineage fusion and splitting. Here, we sequenced the whole genomes of one S-genome species (Aegilops speltoides) of the B-lineage and four S*-genome diploid species (Aegilops bicornis, Aegilops longissima, Aegilops sharonensis and Aegilops searsii) of the D-lineage at the population level. We performed detailed comparisons of the five species and with the other four representative A-, B- and D-lineage species. Our estimates identified frequent genetic introgressions from A- and B-lineages to the D-lineage species. A remarkable observation is the contrasting distributions of putative introgressed loci by the A- and B-lineages along all the seven chromosomes to the extant D-lineage species. These genetic introgressions resulted in high levels of genetic divergence at centromeric regions between Ae. speltoides (B-lineage) and the other four S*-genome diploid species (D-lineage), while natural selection is a potential contributor to divergence among the four S*-genome species at telomeric regions. Our study provides a genome-wide view on how genetic introgression and natural selection acted together yet chromosome-regionally divided to promote genomic divergence among the five S- and S*-genome diploid species, which provides new and nuanced insights into the evolutionary history of the Triticum/Aegilops species complex.

Multi-omic analysis reveals the effects of interspecific hybridization on the synthesis of seed reserve polymers in a Triticum turgidum ssp. durum × Aegilops sharonensis amphidiploid.

BACKGROUND: Wheat grain endosperm is mainly composed of proteins and starch. The contents and the overall composition of seed storage proteins (SSP) markedly affect the processing quality of wheat flour. Polyploidization results in duplicated chromosomes, and the genomes are often unstable and may result in a large number of gene losses and gene rearrangements. However, the instability of the genome itself, as well as the large number of duplicated genes generated during polyploidy, is an important driving force for genetic innovation. In this study, we compared the differences in starch and SSP, and analyzed the transcriptome and metabolome among Aegilops sharonensis (R7), durum wheat (Z636) and amphidiploid (Z636×R7) to reveal the effects of polyploidization on the synthesis of seed reserve polymers. RESULTS: The total starch and amylose content of Z636×R7 was significantly higher than R7 and lower than Z636. The gliadin and glutenin contents of Z636×R7 were higher than those in Z636 and R7. Through transcriptome analysis, there were 21,037, 2197, 15,090 differentially expressed genes (DEGs) in the three comparison groups of R7 vs Z636, Z636 vs Z636×R7, and Z636×R7 vs R7, respectively, which were mainly enriched in carbon metabolism and amino acid biosynthesis pathways. Transcriptome data and qRT-PCR were combined to analyze the expression levels of genes related to storage polymers. It was found that the expression levels of some starch synthase genes, namely AGP-L, AGP-S and GBSSI in Z636×R7 were higher than in R7 and among the 17 DEGs related to storage proteins, the expression levels of 14 genes in R7 were lower than those in Z636 and Z636×R7. According to the classification analysis of all differential metabolites, most belonged to carboxylic acids and derivatives, and fatty acyls were enriched in the biosynthesis of unsaturated fatty acids, niacin and nicotinamide metabolism, one-carbon pool by folate, etc. CONCLUSION: After allopolyploidization, the expression of genes related to starch synthesis was down-regulated in Z636×R7, and the process of starch synthesis was inhibited, resulting in delayed starch accumulation and prolongation of the seed development process. Therefore, at the same development time point, the starch accumulation of Z636×R7 lagged behind that of Z636. In this study, the expression of the GSe2 gene in Z636×R7 was higher than that of the two parents, which was beneficial to protein synthesis, and increased the protein content. These results eventually led to changes in the synthesis of seed reserve polymers. The current study provided a basis for a greater in-depth understanding of the mechanism of wheat allopolyploid formation and its stable preservation, and also promoted the effective exploitation of high-value alleles.

Chromosome stability of synthetic Triticum turgidum-Aegilops umbellulata hybrids.

BACKGROUND: Unreduced gamete formation during meiosis plays a critical role in natural polyploidization. However, the unreduced gamete formation mechanisms in Triticum turgidum-Aegilops umbellulata triploid F1 hybrid crosses and the chromsome numbers and compostions in T. turgidum-Ae. umbellulata F2 still not known. RESULTS: In this study, 11 T.turgidum-Ae. umbellulata triploid F1 hybrid crosses were produced by distant hybridization. All of the triploid F1 hybrids had 21 chromosomes and two basic pathways of meiotic restitution, namely first-division restitution (FDR) and single-division meiosis (SDM). Only FDR was found in six of the 11 crosses, while both FDR and SDM occurred in the remaining five crosses. The chromosome numbers in the 127 selfed F2 seeds from the triploid F1 hybrid plants of 10 crosses (no F2 seeds for STU 16) varied from 35 to 43, and the proportions of euploid and aneuploid F2 plants were 49.61% and 50.39%, respectively. In the aneuploid F2 plants, the frequency of chromosome loss/gain varied among genomes. The chromosome loss of the U genome was the highest (26.77%) among the three genomes, followed by that of the B (22.83%) and A (11.81%) genomes, and the chromosome gain for the A, B, and U genomes was 3.94%, 3.94%, and 1.57%, respectively. Of the 21 chromosomes, 7U (16.54%), 5 A (3.94%), and 1B (9.45%) had the highest loss frequency among the U, A, and B genomes. In addition to chromosome loss, seven chromosomes, namely 1 A, 3 A, 5 A, 6 A, 1B, 1U, and 6U, were gained in the aneuploids. CONCLUSION: In the aneuploid F2 plants, the frequency of chromosome loss/gain varied among genomes, chromsomes, and crosses. In addition to variations in chromosome numbers, three types of chromosome translocations including 3UL·2AS, 6UL·1AL, and 4US·6AL were identified in the F2 plants. Furthermore, polymorphic fluorescence in situ hybridization karyotypes for all the U chromosomes were also identified in the F2 plants when compared with the Ae. umbellulata parents. These results provide useful information for our understanding the naturally occurred T. turgidum-Ae. umbellulata amphidiploids.