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

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.H ybrid vigor, heterosis, is important in agriculture due to the increased performance of hybrid plants over parental lines. The increase in performance is attributable to changes in gene expression (1, 2) but how these changes result in the increased performance of the hybrid is still not known. The level of hybrid vigor is believed to correlate with the genetic distance between parental lines; however, hybrid vigor can occur in progeny derived from crosses of genetically similar parents. An example is found in intraspecific crosses between Arabidopsis thaliana accessions. In crosses between C24 and Landsberg erecta (Ler), up to a 100% increase in plant biomass and seed yield is observed (3). The different epigenomes of the two parental accessions could provide the diversity required to initiate gene expression changes and vigor-related characteristics. A number of laboratories have investigated whether there are epigenetic changes in Arabidopsis hybrids, whether they affect gene expression, and whether they contribute to the hybrid vigor phenotype (1, 3-6).We have previously established that F1 hybrids between Arabidopsis accessions undergo some epigenetic reprogramming. We found that the abundance of 24-nt siRNAs is reduced in F1 hybrids and that a second epigenetic system, DNA methylation ( m C), is also altered in the hybrid genome (1, 3, 5). The altered m C patterns in the hybrids involve the processes trans-chromosomal methylation (TCM) and trans-chromosomal demethylation (TCdM), where the m C state of one parental allele is altered to resemble the other allele (reviewed in ref. 7). Due to the presence of siRNAs at regions that undergo TCM/TCdM, we have suggested that siRNAs are the initiating molecules that establish these TCM/TCdM events (reviewed in ref. 8). In the hybrid nucleus, the complement of 24-nt siRNAs can interact with homologous sequences from either parent.The TCM and TCdM...

Paramutation-like features of multiple natural epialleles in tomato

“…These hypotheses are not mutually exclusive because both RdDM and meiotic silencing of unpaired DNA are dependent on an RNA-dependent RNA polymerase [ 27 , 25 ]. The involvement of RdDM is supported by several lines of evidence that link small RNAs and in particular 24-nt sRNAs with paramutation-like events in tomato in addition to the findings from other species [ 11 , 5 , 12 , 13 ]. At H06 , for example, the timing of the paramutation-like process correlates with the timing or sRNA production (Fig.…”

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