Paramutation and related phenomena in diverse species

Key Points Paramutation describes the occurrence of meiotically heritable epigenetic changes in gene regulation and trans -inactivation behaviours. These behaviours are recognized by non-Mendelian inheritance patterns that are found independently of chromosome transmission ratio distortions and, at least in plants, in the absence of parent-of-origin effects. Genetic analyses implicate small RNAs (sRNAs) and RNA interference mechanisms in affecting paramutations operating in both plants and model metazoans. Species-specific elaborations of core RNA interference components provide unique strategies for establishing and maintaining self-reinforcing loops of transcriptional and post-transcriptional control based on sRNA biogenesis from either nascent or messenger RNA scaffolds. Specialized Pol II-related RNA polymerase complexes (exemplified in Zea mays ), histone readers and RNA-processing factors (found in Drosophila melanogaster ), nuclear Argonaute proteins (as elaborated in Caenorhabditis elegans ), and RNA-dependent RNA polymerases (found in both Z. mays and C. elegans ) are implicated in paramutation-type behaviours. Paramutations are associated with repeated sequences in Z. mays , D. melanogaster and possibly in mammals, and are recognized when changes occur at regulatory regions of specific genes affecting discernible traits. Gametic transmission of sRNAs themselves seems to be responsible for paramutation-type inheritance patterns in metazoans. In plants, the transmission of locus-specific episomes of sRNA biogenesis seems to be dependent on heritable features of DNA and/or chromatin structure. Paramutations exhibit dynamic behaviours based on allele histories, lead to non-Mendelian inheritance patterns that affect allele frequencies and can facilitate the inheritance of acquired characteristics. Although the biological roles of paramutation remain ill-defined, their deviations from the principle tenets of the modern synthesis represent little understood strategies for evolutionary change. In this Review, the author discusses current knowledge on the paramutations that occur in maize and contrasts these behaviours with potentially parallel examples in metazoans. He highlights the key role of small RNAs (sRNAs) in diverse paramutation mechanisms across eukaryotes and considers the evolutionary importance of these regulatory systems. Paramutation describes a process that results in heritable epigenetic changes of gene regulation and trans-homologue int