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Twenty-four–nucleotide siRNAs produce heritable trans-chromosomal methylation in F1 Arabidopsis hybrids

We show that the changes in DNA methylation that occur in F1 hybrids of Arabidopsis are mostly dependent on the presence of 24-nt siRNAs at the locus. The methylation change at a locus results in the two alleles becoming similar to each other in methylation pattern. The methylation changes occur through the processes of trans-chromosomal methylation and trans-chromosomal demethylation.

Ian K. Greaves, Steven R. Eichten, Michael Groszmann, Aihua Wang, Hua Ying, W. James Peacock, and Elizabeth S. Dennis

Significance

We show that the changes in DNA methylation that occur in F1 hybrids of Arabidopsis are mostly dependent on the presence of 24-nt siRNAs at the locus. The methylation change at a locus results in the two alleles becoming similar to each other in methylation pattern. The methylation changes occur through the processes of trans-chromosomal methylation and trans-chromosomal demethylation. These altered methylation states can be inherited in the F2 generation and can be associated with changes in levels of gene activity, which may contribute to the phenotypic heterogeneity in the F2.

Abstract

Hybrid Arabidopsis plants undergo epigenetic reprogramming producing decreased levels of 24-nt siRNAs and altered patterns of DNA methylation that can affect gene expression. Driving the changes in methylation are the processes trans-chromosomal methylation (TCM) and trans-chromosomal demethylation (TCdM). In TCM/TCdM the methylation state of one allele is altered to resemble the other allele. We show that Pol IV-dependent sRNAs are required to establish TCM events. The changes in DNA methylation and the associated changes in sRNA levels in the F1 hybrid can be maintained in subsequent generations and affect hundreds of regions in the F2 epigenome. The inheritance of these altered epigenetic states varies in F2 individuals, resulting in individuals with genetically identical loci displaying different epigenetic states and gene expression profiles. The change in methylation at these regions is associated with the presence of sRNAs. Loci without any sRNA activity can have altered methylation states, suggesting that a sRNA-independent mechanism may also contribute to the altered methylation state of the F1 and F2 generations.

 

See: http://www.pnas.org/content/113/44/E6895.abstract.html?etoc

PNAS November 8 2016; vol.113; no.44: E6895–E6902

 

Fig. 4.

Role of sRNAs in altered mC states. (A) sRNA levels correlate with altered mC states in the F2 populations. Dotted green line represents median mC level of the two parents. The black line represents the median sRNA level in the parental accessions. (B) Enzymes involved in maintaining mC at the F2-inherited windows. n = the number of inherited windows that had coverage and were methylated in Col (21).

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