Paramutation at the maize pl1 locus is associated with RdDM activity at distal tandem repeats.

Exceptions to Mendelian inheritance often highlight novel chromosomal behaviors. The maize Pl1-Rhoades allele conferring plant pigmentation can display inheritance patterns deviating from Mendelian expectations in a behavior known as paramutation. However, the chromosome features mediating such exceptions remain unknown.

Locus-specific paramutation in Zea mays is maintained by a PICKLE-like chromodomain helicase DNA-binding 3 protein controlling development and male gametophyte function.

Paramutations represent directed and meiotically-heritable changes in gene regulation leading to apparent violations of Mendelian inheritance. Although the mechanism and evolutionary importance of paramutation behaviors remain largely unknown, genetic screens in maize (Zea mays) identify five components affecting 24 nucleotide RNA biogenesis as required to maintain repression of a paramutant purple plant1 (pl1) allele. Currently, the RNA polymerase IV largest subunit represents the only component also specifying proper development.

Paramutation and related phenomena in diverse species.

Paramutation describes a process that results in heritable epigenetic changes of gene regulation and trans-homologue interactions. Recent discoveries in model organisms have highlighted roles for the respective nuclear systems that regulate transposons via small RNA molecules both for paramutation and for defining transgenerational inheritance. Differences between plants and animals may influence specific transmission behaviours but the involvement of small RNA-based mechanisms identifies a unifying eukaryotic theme.

Paramutation in maize and related behaviors in metazoans.

Paramutation refers to both the process and results of trans-homolog interactions causing heritable changes in both gene regulation and silencing abilities. Originally described in plants, paramutation-like behaviors have now been reported in model metazoans. Here we detail our current understanding of the paramutation mechanism as defined in Zea mays and compare this paradigm to these metazoan examples.

Trans-Homolog Interactions Facilitating Paramutation in Maize.

Paramutations represent locus-specific trans-homolog interactions affecting the heritable silencing properties of endogenous alleles. Although examples of paramutation are well studied in maize (Zea mays), the responsible mechanisms remain unclear. Genetic analyses indicate roles for plant-specific DNA-dependent RNA polymerases that generate small RNAs, and current working models hypothesize that these small RNAs direct heritable changes at sequences often acting as transcriptional enhancers.

Nascent transcription affected by RNA polymerase IV in Zea mays.

All eukaryotes use three DNA-dependent RNA polymerases (RNAPs) to create cellular RNAs from DNA templates. Plants have additional RNAPs related to Pol II, but their evolutionary role(s) remain largely unknown. Zea mays (maize) RNA polymerase D1 (RPD1), the largest subunit of RNA polymerase IV (Pol IV), is required for normal plant development, paramutation, transcriptional repression of certain transposable elements (TEs), and transcriptional regulation of specific alleles.

Maize RNA polymerase IV defines trans-generational epigenetic variation.

The maize (Zea mays) RNA Polymerase IV (Pol IV) largest subunit, RNA Polymerase D1 (RPD1 or NRPD1), is required for facilitating paramutations, restricting expression patterns of genes required for normal development, and generating small interfering RNA (siRNAs). Despite this expanded role for maize Pol IV relative to Arabidopsis thaliana, neither the general characteristics of Pol IV-regulated haplotypes, nor their prevalence, are known. Here, we show that specific haplotypes of the purple plant1 locus, encoding an anthocyanin pigment regulator, acquire and retain an expanded expression domain following transmission from siRNA biogenesis mutants.

Paramutation: a trans-homolog interaction affecting heritable gene regulation.

Paramutation describes both the process and results of trans-sensing between chromosomes that causes specific heritable changes in gene regulation. RNA molecules are implicated in mediating similar events in maize, mouse, and Drosophila. Changes in both small RNA profiles and cytosine methylation patterns in Arabidopsis hybrids represent a potential molecular equivalent to the interactions responsible for paramutations.

required to maintain repression2 is a novel protein that facilitates locus-specific paramutation in maize.

Meiotically heritable epigenetic changes in gene regulation known as paramutations are facilitated by poorly understood trans-homolog interactions. Mutations affecting paramutations in maize (Zea mays) identify components required for the accumulation of 24-nucleotide RNAs. Some of these components have Arabidopsis thaliana orthologs that are part of an RNA-directed DNA methylation (RdDM) pathway.

Paramutation: a process for acquiring trans-generational regulatory states.

Basic tenets of Mendelian inheritance are violated by paramutations in which trans-homolog interactions lead to heritable changes in gene regulation and phenotype. First described in plants, similar behaviors have now been noted in diverse eukaryotes. Genetic and molecular studies of paramutations occurring in maize indicate that components of a small interfering RNA (siRNA) biogenesis pathway are required for the maintenance of meiotically heritable regulatory states.

Diversity of Pol IV function is defined by mutations at the maize rmr7 locus.

Mutations affecting the heritable maintenance of epigenetic states in maize identify multiple small RNA biogenesis factors including NRPD1, the largest subunit of the presumed maize Pol IV holoenzyme. Here we show that mutations defining the required to maintain repression7 locus identify a second RNA polymerase subunit related to Arabidopsis NRPD2a, the sole second largest subunit shared between Arabidopsis Pol IV and Pol V. A phylogenetic analysis shows that, in contrast to representative eudicots, grasses have retained duplicate loci capable of producing functional NRPD2-like proteins, which is indicative of increased RNA polymerase diversity in grasses relative to eudicots.

Production and processing of siRNA precursor transcripts from the highly repetitive maize genome.

Mutations affecting the maintenance of heritable epigenetic states in maize identify multiple RNA-directed DNA methylation (RdDM) factors including RMR1, a novel member of a plant-specific clade of Snf2-related proteins. Here we show that RMR1 is necessary for the accumulation of a majority of 24 nt small RNAs, including those derived from Long-Terminal Repeat (LTR) retrotransposons, the most common repetitive feature in the maize genome. A genetic analysis of DNA transposon repression indicates that RMR1 acts upstream of the RNA-dependent RNA polymerase, RDR2 (MOP1).

Paramutation and development.

Paramutation describes a heritable change of gene expression that is brought about through interactions between homologous chromosomes. Genetic analyses in plants and, more recently, in mouse indicate that genomic sequences related to transcriptional control and molecules related to small RNA biology are necessary for specific examples of paramutation. Some of the molecules identified in maize are also required for normal plant development.

RNA polymerase IV functions in paramutation in Zea mays.

Plants have distinct RNA polymerase complexes (Pol IV and Pol V) with largely unknown roles in maintaining small RNA-associated gene silencing. Curiously, the eudicot Arabidopsis thaliana is not affected when either function is lost. By use of mutation selection and positional cloning, we showed that the largest subunit of the presumed maize Pol IV is involved in paramutation, an inherited epigenetic change facilitated by an interaction between two alleles, as well as normal maize development.

Sensing the epigenome.

Recent studies of plant development and environmental stress responses have converged on the roles of RNA and its metabolism as primary regulators of gene action. This RNA-based system appears to represent a versatile platform both for maintaining epigenetic memory and for reprogramming gene control in response to external signals. The fast-paced research reviewed here highlights exciting new trends in plant research relating to mechanisms and roles of the RNA-dependent epigenome in both development and evolution.

A novel Snf2 protein maintains trans-generational regulatory states established by paramutation in maize.

Paramutations represent heritable epigenetic alterations that cause departures from Mendelian inheritance. While the mechanism responsible is largely unknown, recent results in both mouse and maize suggest paramutations are correlated with RNA molecules capable of affecting changes in gene expression patterns. In maize, multiple required to maintain repression (rmr) loci stabilize these paramutant states.

Maize sex determination and abaxial leaf fates are canalized by a factor that maintains repressed epigenetic states.

In maize (Zea mays ssp. mays), the meiotically heritable maintenance of specific transcriptionally repressed epigenetic states is facilitated by a putative RNA-dependent RNA polymerase encoded by mediator of paramutation1 (mop1) and an unknown factor encoded by the required to maintain repression6 (rmr6) locus. These so-called "paramutant" states occur at certain alleles of loci encoding regulators of anthocyanin pigment biosynthesis.

Multiple trans-sensing interactions affect meiotically heritable epigenetic states at the maize pl1 locus.

Interactions between specific maize purple plant1 (pl1) alleles result in heritable changes of gene regulation that are manifested as differences in anthocyanin pigmentation. Transcriptionally repressed states of Pl1-Rhoades alleles (termed Pl') are remarkably stable and invariably facilitate heritable changes of highly expressed states (termed Pl-Rh) in Pl'/Pl-Rh plants. However, Pl' can revert to Pl-Rh when hemizygous, when heterozygous with pl1 alleles other than Pl1-Rhoades, or in the absence of trans-acting factors required to maintain repressed states.

Rmr6 maintains meiotic inheritance of paramutant states in Zea mays.

Paramutation generates heritable changes affecting regulation of specific alleles found at several Zea mays (maize) loci that encode transcriptional regulators of anthocyanin biosynthetic genes. Although the direction and extent of paramutation is influenced by poorly understood allelic interactions occurring in diploid sporophytes, two required to maintain repression loci (rmr1 and rmr2), as well as mediator of paramutation1 (mop1), affect this process at the purple plant1 (pl1) locus. Here we show that the rmr6 locus is required for faithful transmission of weakly expressed paramutant states previously established at both pl1 and red1 (r1) loci.