Trans-acting small RNA determines dominance relationships in Brassica self-incompatibility

Abstract

A diploid organism has two copies of each gene, one inherited from each parent. The expression of two inherited alleles is sometimes biased by the effects known as dominant/recessive relationships, which determine the final phenotype of the organism. To explore the mechanisms underlying these relationships, we have examined the monoallelic expression of S-locus protein 11 genes (SP11), which encode the male determinants of self-incompatibility in Brassica. We previously reported that SP11 expression was monoallelic in some S heterozygotes, and that the promoter regions of recessive SP11 alleles were specifically methylated in the anther tapetum. Here we show that this methylation is controlled by trans-acting small non-coding RNA (sRNA). We identified inverted genomic sequences that were similar to the recessive SP11 promoters in the flanking regions of dominant SP11 alleles. These sequences were specifically expressed in the anther tapetum and processed into 24-nucleotide sRNA, named SP11 methylation inducer (Smi). Introduction of the Smi genomic region into the recessive S homozygotes triggered the methylation of the promoter of recessive SP11 alleles and repressed their transcription. This is an example showing sRNA encoded in the flanking region of a dominant allele acts in trans to induce transcriptional silencing of the recessive allele. Our finding may provide new insights into the widespread monoallelic gene expression systems.

Epigenetic Variation, Inheritance, and Selection in Plant Populations

“…In the case of SP11, a precursor RNA is produced from the Smi locus of selected S alleles and is processed into a small RNA that can direct methylation of the SP11 promoter of some S alleles in trans. Thus, epigenetic silencing results in dominance of the SP11 allele of the S locus that transcribes the Smi gene, but silencing is only observed as long as the particular S-allele combination is present in the same cell (Tarutani et al 2010). In contrast, a silenced FOLT1 epiallele, whose silencing was induced by small RNAs produced from a truncated paralogous locus in trans, can be segregated away from the inducing locus and remains silent (Durand et al 2012).…”

“…Further examples of naturally occurring epialleles are the Colorless nonripening (Cnr) locus in tomato (Manning et al 2006), the transcription factor CmWIP controlling sex determination in melon (Martin et al 2009), the FLOWERING WAGENINGEN (FWA) (Kakutani 1997;Soppe et al 2000;Fujimoto et al 2008Fujimoto et al , 2011 and FOLT1 loci (Durand et al 2012) in Arabidopsis thaliana, and selected SP11 alleles at the complex S locus responsible for self-incompatibility in Brassica rapa (Shiba et al 2006;Tarutani et al 2010). Although no changes in the underlying DNA sequence of the Lcyc and Cnr region have been observed, the epigenetic variants at CmWIP, FWA, FOLT1, and SP11 originate from structural genetic variation.…”

Achievement of genetics in plant reproduction research: the past decade for the coming decade

“…Repression of recessive SP11 allele is a result of tapetum-specific de novo cytosine methylation in its promoter region, and small RNA produced from SP11-methylation inducing region (Smi), which is located in the flanking region of a dominant SP11 allele, controls this monoallelic gene silencing (Tarutani et al, 2010).…”

“…Their details are available in recent publications (Franklin-Tong, 2008;Suzuki, 2009). The latest topics in SI research, in addition to the publication of the above articles, are identification of the trans-acting small RNA controlling dominance/recessive relationship in the Brassica pollen SI factor (Tarutani et al, 2010), the evolution of self-compatibility (SC) in Arabidopsis (Tsuchimatsu et al, 2010), and collaborative non-self recognition system in S-RNase-based SI .…”

DNA methylation polymorphism and stability in Chinese indica hybrid rice

“…In hybrids, interactions between allelic variants are thought to be involved in vigor [3638]. The recessive allele of Brassica S-locus protein 11 genes (SP11) is methylated in trans by RdDM, which is guided by siRNAs produced from the Smi gene on the dominant SP11-allele, resulting in the expression repression of recessive allele [39]. These alteration modes of DNA methylation and expression have also been documented in a genome-wide study of Arabidopsis parental lines and their hybrids [35].…”