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Subgenome-dominant expression and alternative splicing in response to pathogen stress in polyploid Brassica napus and progenitors

ABSTRACT: Polyploidy has played an extensive role in the evolution of flowering plants. Allopolyploids, with subgenomes containing duplicated gene pairs called homeologs, can show rapid transcriptome changes including novel alternative splicing (AS) patterns. The extent to which abiotic stress modulates AS of homeologs is a nascent topic in polyploidy research. We subjected both natural and resynthesized lines of polyploid Brassica napus, along with the progenitors B. rapa and B. oleracea, to infection with the fungal pathogen Sclerotinia sclerotiorum. RNA-seq analyses revealed widespread divergence between polyploid subgenomes in both gene expression and AS patterns. Resynthesized B. napus displayed significantly more A and C subgenome biased homeologs under pathogen infection than during uninfected growth. Differential AS (DAS) in response to infection was highest in natural B. napus (12,709 DAS events) and lower in resynthesized Brassica napus (8,863 DAS events). Natural B. napus had more up-regulated events and fewer down-regulated events. There was a global expression bias towards the B. oleracea-derived (C) subgenome in both resynthesized and natural B. napus, enhanced by widespread non-parental downregulation of the B. rapa-derived (A) homeolog. In the resynthesized B. napus specifically, this resulted a disproportionate C subgenome contribution to pathogen defense response, characterized by biases in both transcript expression levels and the proportion of induced genes. Our results elucidate the complex ways in which Sclerotinia infection affects expression and AS of homeologous genes in natural and resynthesized B. napus, and indicate that abiotic stress can influence the evolution of homeologous genes in polyploids.

ORGANISM(S): Brassica rapa Brassica napus Brassica oleracea

PROVIDER: GSE201225 | GEO | 2023/02/04

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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Subgenome-dominant expression and alternative splicing in response to pathogen stress in polyploid Brassica napus and progenitors

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