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The maze of paramutation: a rough guide to the puzzling epigenetics of paramutation

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Abstract Epigenetic mechanisms maintain gene expression states through mitotic and sometimes meiotic cell divisions. Paramutation is an extreme example of epigenetic processes. Not only an established expression state is transmitted through meiosis to the following generations but also an information transfer occurs between alleles and leads to heritable changes in expression state. As a consequence the expression states can rapidly propagate in population, violating Mendelian genetics. Recent findings unraveled an essential role for siRNA‐dependent processes in paramutation. Despite significant progress, the overall picture is still puzzling and many important questions remain to be answered. WIREs RNA 2011 2 863–874 DOI: 10.1002/wrna.97 Regulatory RNAs/RNAi/Riboswitches > RNAi: Mechanisms of Action RNA in Disease and Development > RNA in Disease RNA in Disease and Development > RNA in Development

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Principle of paramutation at the maize b1 locus. (a) Paramutation induced by paramutagenic epiallele. B‐I epiallele has high transcription rate and confers dark purple pigmentation phenotype. Expression from B′ epiallele is about 20 times lower and results in light plant pigmentation. When the two epialleles are brought together by genetic crossing, B‐I is always changed (paramutated) to B′ in resulting heterozygotes. The newly established B′ epiallele continues to issue instructions that paramutate naïve B‐I epialleles in succeeding generations. (b) Spontaneous paramutation. In the progeny of B‐I homozygotes, B′ epialleles appear spontaneously with 1–10% frequency.

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Hypothetical models for CBBP role in b1 paramutation. (a) CBBP binds to the b1 repeats in a sequence‐specific manner. Multimerization of CBBP molecules bound to the distinct repeat units in B′ nuclei induce a specific chromatin structure that is susceptible to siRNA‐dependent silencing. In B‐I plants CBBP is not detectable and presumably other proteins bind to b1 repeats. (b) Multimerization of CBBP molecules bound to distinct b1 alleles in B′ nuclei leads to physical interaction of alleles. In B‐I nuclei these interactions do not occur, as CBBP is not detectable in B‐I plants. When genetic crossing brings B′ and B‐I together, CBBP molecules contributed by B′ parent induce physical allelic interactions that in turn leads to the transfer of epigenetic information from B′ to B‐I.

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Mechanistic models of paramutation at the maize b1 locus. (a) Model 1: in B‐I nuclei the repeats act as an enhancer driving high b1 expression. Chromatin status at the repeats prevents silencing by siRNAs in B‐I. In B′ nuclei chromatin is susceptible to the siRNA‐dependent silencing resulting in low b1 expression. In heterozygotes epigenetic information transfer occurs in trans between alleles inducing siRNA‐susceptible chromatin state at the paramutable B‐I. Currently, it is not clear how the information transfer occurs. (b) Model 2: in B′ nuclei the repeats are bound by chromatin modifying or remodeling enzymes. In heterozygotes physical interaction of the alleles induces modification of chromatin status at the B‐I epiallele by the enzyme molecules associated with B′. (c) Model 3: in B′ nuclei b1 locus resides inside nuclear bodies where siRNA‐dependent silencing occurs. In B‐I nuclei b1 locus is located outside of those nuclear bodies and does not undergo silencing. In heterozygotes physical interactions between alleles lead to translocation of B‐I into nuclear foci where it is subjected to siRNA‐dependent silencing.

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Paramutation phenotypes in maize. High expression from paramutable epialleles of b1, pl1, and p1 loci leads to pigment accumulation in respective tissues (left column). Lowered expression from paramutagenic epialleles leads to light pigmentation (right column).

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Regulatory RNAs/RNAi/Riboswitches > RNAi: Mechanisms of Action
RNA in Disease and Development > RNA in Development
RNA in Disease and Development > RNA in Disease

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