Disruption of DNA methylation induces genome-specific changes in gene expression in Arabidopsis allotetraploids

Abstract

Allopolyploids are formed by the combination of evolutionarily-diverged genomes, the union of which leads to dynamic changes in gene expression and genome organization. Expression patterns of orthologous genes are rapidly and stochastically established in newly created allotetraploids, where gene silencing is maintained by microRNAs, DNA methylation, and other chromatin modifications. Among them, DNA methylation has been known as an important mechanism of epigenetic regulation of gene expression and chromatin structure. However, it is unclear how DNA methylation affects genome-wide expression of homoeologous genes in the natural polyploid Arabidopsis suecica that contains genome of both A. thaliana and A. arenosa. To understand the role that DNA methylation plays in the polyploidization process, a comparative analysis was performed comparing up- or down-regulated genes in met1-RNAi A. suecica lines with the non-additively expressed genes in the synthetic allotetraploids, i.e., different from the mid-parent value. The previous studies indicated that decreased DNA methylation in A. suecica induces A. arenosa-specific demethylation in centromere regions and differentially alters expression of >200 genes encoding many transposons, unknown proteins and some other functional proteins that are located along chromosomes, whereas >1,300 non-additively expressed genes in the synthetic allotetraploids are distributed randomly along the chromosomes and encode various proteins in metabolism, energy, cellular biogenesis, cell defense and aging, and hormonal regulation. The origins of the progenitors of the genes whose expressions are altered in both met1-RNAi A. suecica and resynthesized allotetraploid were analyzed with single strand conformation polymorphism (SSCP) analysis. Reactivated genes in met1-RNAi A. suecica lines were predominately derived from the A. thaliana genome in euchromatic regions, whereas the suppressed genes were mainly derived from the A. Arenosa genome, indicating that changes in DNA methylation are genome-sensitive. The data suggest that allotetraploids incidentally display chromosome-specific changes and genomedependent regulation of homoeologous genes in response to DNA methylation perturbations.