Subgenome-specific usage of transposable element-derived promoters and enhancers in bread wheat development
Ontology highlight
ABSTRACT:
ORGANISM(S): Triticum urartu Triticum aestivum
PROVIDER: GSE198284 | GEO | 2023/10/12
REPOSITORIES: GEO
Similar Datasets
Project description:Common wheat (T. aestivum) converged three subgenomes adapted to different environments. The combinatorial interaction between transcription factors (TFs) and regulatory elements (REs) defines a regulatory circuit that underlies subgenome convergence and divergence. Compared to the relatively conserved gene composition across subgenomes, the intergenic regions with abundant REs is drastically diversified by almost complete TE turnovers, raising major questions regarding how subgenome convergent and divergent regulation is encoded in the highly diversified intergenic regions, and the impact of TE evolution on regulatory conservation and innovation. In the present study, we created genome-wide TF binding catalog to assemble an extensive wheat regulatory network comprising connections among 182 TFs. The different effects of ancient and recent TE insertions on regulatory specificity were observed. Subgenome asymmetric TE expansion is an important source of subgenome divergent TFBS, which help explain the vast occupancy difference across subgenomes. Interestingly, the ancient expansion of RLC_famc1.4-derived TFBS occurred in more than 25% triads promoters. A significant fraction of these TE-derived TFBS subjected to region-specific evolutionary selections, resulting in subgenome-balanced TF binding but unbalanced degeneration of flanking TE sequences. These TE-derived subgenome convergent and divergent regulation linked to subgenome conserved and diversified pathways, suggesting that TEs are an important regulatory driving force contributed to polyploid evolution. Overall, this study demonstrated the impact of TEs on shaping the plasticity and adaptation of common wheat, enriched the theories of TE-promoted transcriptional innovation from the evolutionary aspects of polyploid regulation since first reported by McClintock.
2022-10-08 | GSE192815 | GEO
Project description:Polyploidization and introgression are major events driving plant genome evolution and influencing crop breeding. However, the mechanisms underlying the higher-order chromatin organization of subgenomes and alien chromosomes are largely unknown. We probe the three-dimensional chromatin architecture of Aikang 58 (AK58), a widely-cultivated allohexaploid wheat variety carrying the 1RS/1BL translocation chromosome. The regions involved in inter-chromosomal interactions, both within and between subgenomes, have highly similar sequences. Subgenome-specific territories tend to be connected by subgenome-dominant homologous transposable elements (TEs). The alien 1RS chromosomal arm, which was introgressed from rye and differs from its wheat counterpart, has relatively few inter-chromosome interactions with wheat chromosomes. An analysis of local chromatin structures reveals topologically associating domain (TAD)-like regions covering 52% of the AK58 genome, the boundaries of which are enriched with active genes, zinc-finger factor-binding motifs, CHH methylation, and 24-nt small RNAs. The chromatin loops are mostly localized around TAD boundaries, and the number of gene loops is positively associated with gene activity. The present study reveals the impact of the genetic sequence context on the higher-order chromatin structure and subgenome stability in hexaploid wheat. Specifically, we characterized the sequence homology-mediated inter-chromosome interactions and the non-canonical role of subgenome-biased TEs. Our findings may have profound implications for future investigations of the interplay between genetic sequences and higher-order structures and their consequences on polyploid genome evolution and introgression-based breeding of crop plants.
2020-11-30 | GSE139020 | GEO
Project description:Subgenome-specific usage of transposable element-derived promoters and enhancers in bread wheat development
| PRJNA814385 | ENA
Project description:High plasticity of common wheat is attributed to the captured and polyploidization-promoted diversity. However, uncontrolled subgenome diversification can lead to hybrid conflict and dysgenesis, resulting in decreased diversity. How genomic diversity is maintained and interpreted to increase plasticity is unclear. By data-mining from the binding of 193 genome-wide trans-factors and genetic perturbations in common wheat, we identified LHP1 as a major regulator of subgenome-diversified defense genes, enhancer RNAs, and metabolite synthesis-related gene clusters via H3K27me3. Stripe rust infection leads to a global decrease in LHP1-mediated H3K27me3, deprivation of which enhances common wheat stripe rust resistance. We also revealed the consistency between subgenome diversity and population diversity, potentially promoted by LHP1, implying the recent diversification preferentially occurred in the captured subgenome-diversified regions regulated by LHP1. Thus, common wheat benefitted from multi-faced role of LHP1 in promoting sequence diversity and repressing subgenome-diversified defenses; this constraint is eliminated by pathogen infections, enabling timely release and fixation of favorable variations, conferring the evolutionary advantage and high plasticity of common wheat.
2023-10-12 | GSE218538 | GEO
Project description:Wheat (Triticum aestivum) has a large allohexaploid genome. Subgenome-divergent regulation contributed to genome plasticity and the domestication of polyploid wheat. However, the specificity encoded in the wheat genome determining subgenome-divergent spatio-temporal regulation has been largely unexplored. The considerable size and complexity of the genome are major obstacles to dissecting the regulatory specificity. Here, we compared the epigenomes and transcriptomes from a large set of samples under diverse developmental and environmental conditions. Thousands of distal epigenetic regulatory elements (distal-epiREs) were specifically linked to their target promoters with coordinated epigenomic changes. We revealed that subgenome-divergent activity of homologous regulatory elements are affected by specific epigenetic signatures. Subgenome-divergent epiRE regulation of tissue specificity is associated with dynamic modulation of H3K27me3 mediated by Polycomb complex and demethylases. Furthermore, quantitative epigenomic approaches detected key stress responsive cis- and trans-acting factors validated by DNA Affinity Purification and sequencing (DAP-seq), and demonstrated the coordinated interplay between epiRE sequence contexts, epigenetic factors, and transcription factors in regulating subgenome divergent transcriptional responses to external changes. Thus, this study provides a wealth of resources for elucidating the epiRE regulomics and subgenome-divergent regulation in hexaploid wheat, and gives new clues for interpreting genetic and epigenetic interplay in regulating the benefits of polyploid wheat.
2021-02-04 | GSE139019 | GEO
Project description:Expression divergence caused by genetic variation and crosstalks among subgenomes of the allohexaploid bread wheat (Triticum aestivum. L., BBAADD) is hypothesized to increase its adaptability and/or plasticity. However, the molecular basis of expression divergence remains unclear. Squamosa promoter-binding protein-like (SPL) transcription factors are critical for a wide array of biological processes. In this study, we constructed expression regulatory networks by combining DAP-seq for 40 SPLs, ATAC-seq, and RNA-seq. Our findings indicate that a group of low-affinity SPL binding regions (SBRs) were targeted by diverse SPLs and caused different sequence preferences around the core GTAC motif. The SBRs including the low-affinity ones are evolutionarily conserved, enriched GWAS signals related to important agricultural traits. However, those SBRs are highly diversified among the cis-regulatory regions (CREs) of syntenic genes, with less than 8% SBRs coexisting in triad genes, suggesting that CRE variations are critical for subgenome differentiations. Knocking out of TaSPL7A/B/D and TaSPL15A/B/D subfamily further proved that both high- and low-affinity SBRs played critical roles in the differential expression of genes regulating tiller number and spike sizes. Our results have provided baseline data for downstream networks of SPLs and wheat improvements and revealed that CRE variations are critical sources for subgenome divergence in the allohexaploid wheat.
2022-11-28 | GSE188699 | GEO
Project description:Expression divergence caused by genetic variation and crosstalks among subgenomes of the allohexaploid bread wheat (Triticum aestivum. L., BBAADD) is hypothesized to increase its adaptability and/or plasticity. However, the molecular basis of expression divergence remains unclear. Squamosa promoter-binding protein-like (SPL) transcription factors are critical for a wide array of biological processes. In this study, we constructed expression regulatory networks by combining DAP-seq for 40 SPLs, ATAC-seq, and RNA-seq. Our findings indicate that a group of low-affinity SPL binding regions (SBRs) were targeted by diverse SPLs and caused different sequence preferences around the core GTAC motif. The SBRs including the low-affinity ones are evolutionarily conserved, enriched GWAS signals related to important agricultural traits. However, those SBRs are highly diversified among the cis-regulatory regions (CREs) of syntenic genes, with less than 8% SBRs coexisting in triad genes, suggesting that CRE variations are critical for subgenome differentiations. Knocking out of TaSPL7A/B/D and TaSPL15A/B/D subfamily further proved that both high- and low-affinity SBRs played critical roles in the differential expression of genes regulating tiller number and spike sizes. Our results have provided baseline data for downstream networks of SPLs and wheat improvements and revealed that CRE variations are critical sources for subgenome divergence in the allohexaploid wheat.
2022-11-28 | GSE188723 | GEO
Project description:Expression divergence caused by genetic variation and crosstalks among subgenomes of the allohexaploid bread wheat (Triticum aestivum. L., BBAADD) is hypothesized to increase its adaptability and/or plasticity. However, the molecular basis of expression divergence remains unclear. Squamosa promoter-binding protein-like (SPL) transcription factors are critical for a wide array of biological processes. In this study, we constructed expression regulatory networks by combining DAP-seq for 40 SPLs, ATAC-seq, and RNA-seq. Our findings indicate that a group of low-affinity SPL binding regions (SBRs) were targeted by diverse SPLs and caused different sequence preferences around the core GTAC motif. The SBRs including the low-affinity ones are evolutionarily conserved, enriched GWAS signals related to important agricultural traits. However, those SBRs are highly diversified among the cis-regulatory regions (CREs) of syntenic genes, with less than 8% SBRs coexisting in triad genes, suggesting that CRE variations are critical for subgenome differentiations. Knocking out of TaSPL7A/B/D and TaSPL15A/B/D subfamily further proved that both high- and low-affinity SBRs played critical roles in the differential expression of genes regulating tiller number and spike sizes. Our results have provided baseline data for downstream networks of SPLs and wheat improvements and revealed that CRE variations are critical sources for subgenome divergence in the allohexaploid wheat.
2022-11-28 | GSE188696 | GEO
Project description:Bread wheat is the major staple food of the world with a complex hexaploidy genome. The precise spatiotemporal gene expression is orchestrated by enhancers, which lack general sequence features and thus are difficult to be located, especially in large genomes. Epigenomic architecture, including chromatin openness and active chromatin marks, has been widely used to characterize enhancers. However, an active chromatin environment does not necessarily mean an active enhancer. Recently, enhancer RNAs (eRNAs), the hallmark for active enhancers, have been detected by nascent RNA sequencing in both Drosophila and mammalian. In order to answer whether plant enhancers could be transcribed, we investigated the transcriptome of bread wheat via two nascent RNA sequencing methods, GRO-seq and pNET-seq combining with epigenome profiling. Our study demonstrates the presence and wide distribution of transcription at intergenic enhancers, which accurately reflects high enhancer activity, shedding light on the complex gene expression regulation across subgenomes in bread wheat.
2022-04-06 | GSE178276 | GEO
Project description:The importance and applications of polyploidy have long been recognized, from shaping the evolutionary success of flowering plants to improving agricultural productivity. Recent studies have shown that one of the parental subgenomes in ancient polyploids is generally more dominant - having both retained more genes and being more highly expressed - a phenomenon termed subgenome dominance. How quickly one subgenome dominates within a newly formed polyploid, if immediate or after millions of years, and the genomic features that determine which genome dominates remain poorly understood. To investigate the rate of subgenome dominance emergence, we examined gene expression, gene methylation, and transposable element (TE) methylation in a natural less than 140 year old allopolyploid (Mimulus peregrinus), a resynthesized interspecies triploid hybrid (M. robertsii), a resynthesized allopolyploid (M. peregrinus), and diploid progenitors (M. guttatus and M. luteus). We show that subgenome expression dominance occurs instantly following the hybridization of two divergent genomes and that subgenome expression dominance significantly increases over generations. Additionally, CHH methylation levels are significantly reduced in regions near genes and within transposons in the first generation hybrid, intermediate in the resynthesized allopolyploid, and are repatterned differently between the dominant and submissive subgenomes in the natural allopolyploid. Our analyses reveal that the subgenome differences in levels of TE methylation mirror the increase in expression bias observed over the generations following the hybridization. These findings not only provide important insights into genomic and epigenomic shock that occurs following hybridization and polyploid events, but may also contribute to uncovering the mechanistic basis of heterosis and subgenomic dominance.
2018-05-23 | GSE95799 | GEO