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Homology-mediated inter-chromosomal interactions in hexaploid wheat lead to specific subgenome territories following polyploidization and introgression

ABSTRACT: 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.

ORGANISM(S): Triticum aestivum

PROVIDER: GSE139020 | GEO | 2020/11/30

REPOSITORIES: GEO

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Project description:The three subgenomes (B, A and D) of common wheat (2n=6x=42) are largely intact, which makes extraction of the BBAA subgenomes as organismally independent genomes possible. Availability of such novel extracted tetraploid wheat (Extracted-tetra) provides a unique opportunity to study whether and to what extent the BBAA subgenomes of common wheat have been irreversibly modified, as well as its attendant biological consequences, during their evolutionary trajectory as allohexaploidy. We report here that the extracted-tetra is stable in karyotype but with severely deteriorated phenotypes. Microarray-based transcriptome analysis revealed a substantial portion of differentially expressed genes (down- or up-regulation) between extracted and natural tetraploid wheat, Triticum turgidum, which exceeded the transcriptome divergence at tetraploid level, implying reinforced effects of allopolyploidization and domestication at the allohexaploid level. Great majority of the differentially expressed genes showed additive expression in a resynthesized allohexaploid wheat (parented by Extracted-tetra), indicating transcriptome modifications to the BBAA subgenomes are largely irreversible. Analysis of a newly synthesized allohexaploid wheat (parented by T. turgidum) suggests that whereas most of the modified genes are accrued evolutionary changes, some showed immediate regulation post-allohexaploidization and evolutionary perseverance. Homeologue-specific pyrosequencing of 44 genes revealed either concordant or independent expression changes to the B and A homeologues. The Extracted-tetra vs.T. turgidum down-regulated genes showed enrichment for distinct GO categories. Structurally, the three constituent subgenomes of common wheat, BB, AA and DD, are largely intact with only a few inter-subgenomic translocations. Because of these unique attributes, it is feasible to extract the BBAA subgenomes from the common wheat BBAADD genome by hybridization to a durum line and repeated back-crossing to the hexaploid parent, restituting a novel type of extracted tetraploid wheat, namely Extracted-tetr, with a genome constitution BBAA, virtually identical to the subgenomes BBAA of its common wheat donor. Availability of the extracted-tetra, the resynthesized allohexaploid wheat parented by the extracted-tetra, and newly synthesized allohexaploid wheat parented by natural tetraploid wheat, T. turgidum, provides an excellent system to address the issues of whether and to what extent transcriptome modifications to the BBAA subgenomes of common wheat have occurred since its formation ca. 10,000 years ago, timing of the modifications, and their biological consequences. Here, we have addressed these issues by microarray-based transcriptome analysis.

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Homology-mediated inter-chromosomal interactions in hexaploid wheat lead to specific subgenome territories following polyploidization and introgression

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