Paramutation-like features of multiple natural epialleles in tomato.
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ABSTRACT: Freakish and rare or the tip of the iceberg? Both phrases have been used to refer to paramutation, an epigenetic drive that contravenes Mendel's first law of segregation. Although its underlying mechanisms are beginning to unravel, its understanding relies only on a few examples that may involve transgenes or artificially generated epialleles.By using DNA methylation of introgression lines as an indication of past paramutation, we reveal that the paramutation-like properties of the H06 locus in hybrids of Solanum lycopersicum and a range of tomato relatives and cultivars depend on the timing of sRNA production and conform to an RNA-directed mechanism. In addition, by scanning the methylomes of tomato introgression lines for shared regions of differential methylation that are absent in the S. lycopersicum parent, we identify thousands of candidate regions for paramutation-like behaviour. The methylation patterns for a subset of these regions segregate with non Mendelian ratios, consistent with secondary paramutation-like interactions to variable extents depending on the locus.Together these results demonstrate that paramutation-like epigenetic interactions are common for natural epialleles in tomato, but vary in timing and penetrance.
<h4>Background</h4>Freakish and rare or the tip of the iceberg? Both phrases have been used to refer to paramutation, an epigenetic drive that contravenes Mendel's first law of segregation. Although its underlying mechanisms are beginning to unravel, its understanding relies only on a few examples that may involve transgenes or artificially generated epialleles.<h4>Results</h4>By using DNA methylation of introgression lines as an indication of past paramutation, we reveal that the paramutation-l ...[more]
Project description:By using DNA methylation of introgression lines as a marker of past paramutation, we characterise in details the paramutation of the \textit{H06} locus in crosses between Solanum lycopersicum and a range of tomato relatives and cultivars. Paramutation of H06 depends on the timing of sRNA production and conforms to the RNA-directed model of paramutation. By scanning the methylomes of tomato introgression lines for shared regions of differential methylation, thousands of candidate regions for paramutation are identified. Analysing the segregation of the methylation patterns for a subset of these regions shows variations in the penetrance of paramutation-like interactions.
Project description:By using DNA methylation of introgression lines as a marker of past paramutation, we characterise in details the paramutation of the \textit{H06} locus in crosses between Solanum lycopersicum and a range of tomato relatives and cultivars. Paramutation of H06 depends on the timing of sRNA production and conforms to the RNA-directed model of paramutation. By scanning the methylomes of tomato introgression lines for shared regions of differential methylation, thousands of candidate regions for paramutation are identified. Analysing the segregation of the methylation patterns for a subset of these regions shows variations in the penetrance of paramutation-like interactions.
Project description:Analogous to genetically distinct alleles, epialleles represent heritable states of different gene expression from sequence-identical genes. Alleles and epialleles both contribute to phenotypic heterogeneity. While alleles originate from mutation and recombination, the source of epialleles is less well understood. We analyze active and inactive epialleles that were found at a transgenic insert with a selectable marker gene in Arabidopsis. Both converse expression states are stably transmitted to progeny. The silent epiallele was previously shown to change its state upon loss-of-function of trans-acting regulators and drug treatments. We analyzed the composition of the epialleles, their chromatin features, their nuclear localization, transcripts, and homologous small RNA. After mutagenesis by T-DNA transformation of plants carrying the silent epiallele, we found new active alleles. These switches were associated with different, larger or smaller, and non-overlapping deletions or rearrangements in the 3' regions of the epiallele. These cis-mutations caused different degrees of gene expression stability depending on the nature of the sequence alteration, the consequences for transcription and transcripts, and the resulting chromatin organization upstream. This illustrates a tight dependence of epigenetic regulation on local structures and indicates that sequence alterations can cause epigenetic changes at some distance in regions not directly affected by the mutation. Similar effects may also be involved in gene expression and chromatin changes in the vicinity of transposon insertions or excisions, recombination events, or DNA repair processes and could contribute to the origin of new epialleles.
Project description:Epimutations are heritable changes in gene function due to loss or gain of DNA cytosine methylation or chromatin modifications without changes in the DNA sequence. Only a few natural epimutations displaying discernible phenotypes are documented in plants. Here, we report natural epimutations in the cadastral gene, SUPERMAN(SUP), showing striking phenotypes despite normal transcription, discovered in a natural tetraploid, and subsequently in eleven diploid Arabidopsis genetic accessions. This natural lois lane(lol) epialleles behave as recessive mendelian alleles displaying a spectrum of silent to strong superwoman phenotypes affecting only the carpel whorl, in contrast to semi-dominant superman or supersex features manifested by induced epialleles which affect both stamen and carpel whorls. Despite its unknown origin, natural lol epialleles are subjected to the same epigenetic regulation as induced clk epialleles. The existence of superwoman epialleles in diverse wild populations is interpreted in the light of the evolution of unisexuality in plants.
Project description:DNA methylation in plants is depleted from cis-regulatory elements in and near genes but is present in some gene bodies, including exons. Methylation in exons solely in the CG context is called gene body methylation (gbM). Methylation in exons in both CG and non-CG contexts is called TE-like methylation (teM). Assigning functions to both forms of methylation in genes has proven to be challenging. Toward that end, we utilized recent genome assemblies, gene annotations, transcription data, and methylome data to quantify common patterns of gene methylation and their relations to gene expression in maize. We found that gbM genes exist in a continuum of CG methylation levels without a clear demarcation between unmethylated genes and gbM genes. Analysis of expression levels across diverse maize stocks and tissues revealed a weak but highly significant positive correlation between gbM and gene expression except in endosperm. gbM epialleles were associated with an approximately 3% increase in steady-state expression level relative to unmethylated epialleles. In contrast to gbM genes, which were conserved and were broadly expressed across tissues, we found that teM genes, which make up about 12% of genes, are mainly silent, are poorly conserved, and exhibit evidence of annotation errors. We used these data to flag teM genes in the 26 NAM founder genome assemblies. While some teM genes are likely functional, these data suggest that the majority are not, and their inclusion can confound the interpretation of whole-genome studies.
Project description:Detected and quantified siRNAs targeting VTE3(1) loci in ripe fruits of S. lycopersicum (cv. M82), S. pennellii (LA716) and IL9-2-6-1