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

ABSTRACT: 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. Cis-linked features of Pl1-Rhoades responsible for these trans-sensing behaviors remain unknown. Here, genetic tests of a pl1 allelic series identify two potentially separate cis-linked features: one facilitating repression of Pl-Rh and another stabilizing Pl' in trans. Neither function is affected in ethyl-methanesulfonate-induced Pl1-Rhoades derivatives that produce truncated PL1 peptides, indicating that PL1 is unlikely to mediate trans interactions. Both functions, however, are impaired in a spontaneous Pl1-Rhoades derivative that fails to produce detectable pl1 RNA. Pl'-like states can also repress expression of a pl1-W22 allele, but this repression is not meiotically heritable. As the Pl' state is not associated with unique small RNA species representing the pl1-coding region, the available data suggest that interactions between elements required for transcription underlie Pl1-Rhoades epigenetic behaviors.

SUBMITTER: Gross SM

PROVIDER: S-EPMC1894611 | biostudies-literature | 2007 Jun

REPOSITORIES: biostudies-literature

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

Gross Stephen M SM Hollick Jay B JB

Genetics 20070415 2

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 absenc ...[more]

PMID: 17435245

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Project description:Epigenetic variation describes heritable differences that are not attributable to changes in DNA sequence. There is the potential for pure epigenetic variation that occurs in the absence of any genetic change or for more complex situations that involve both genetic and epigenetic differences. Methylation of cytosine residues provides one mechanism for the inheritance of epigenetic information. A genome-wide profiling of DNA methylation in two different genotypes of Zea mays (ssp. mays), an organism with a complex genome of interspersed genes and repetitive elements, allowed the identification and characterization of examples of natural epigenetic variation. The distribution of DNA methylation was profiled using immunoprecipitation of methylated DNA followed by hybridization to a high-density tiling microarray. The comparison of the DNA methylation levels in the two genotypes, B73 and Mo17, allowed for the identification of approximately 700 differentially methylated regions (DMRs). Several of these DMRs occur in genomic regions that are apparently identical by descent in B73 and Mo17 suggesting that they may be examples of pure epigenetic variation. The methylation levels of the DMRs were further studied in a panel of near-isogenic lines to evaluate the stable inheritance of the methylation levels and to assess the contribution of cis- and trans- acting information to natural epigenetic variation. The majority of DMRs that occur in genomic regions without genetic variation are controlled by cis-acting differences and exhibit relatively stable inheritance. This study provides evidence for naturally occurring epigenetic variation in maize, including examples of pure epigenetic variation that is not conditioned by genetic differences. The epigenetic differences are variable within maize populations and exhibit relatively stable trans-generational inheritance. The detected examples of epigenetic variation, including some without tightly linked genetic variation, may contribute to complex trait variation.

Project description:How genetic and phenotypic variation are maintained has long been one of the fundamental questions in population and quantitative genetics. A variety of factors have been implicated to explain the maintenance of genetic variation in some contexts (e.g. balancing selection), but the potential role of epigenetic regulation to influence population dynamics has been understudied. It is well recognized that epigenetic regulation, including histone methylation, small RNA expression, and DNA methylation, helps to define differences between cell types and facilitate phenotypic plasticity. In recent years, empirical studies have shown the potential for epigenetic regulation to also be heritable for at least a few generations without selection, raising the possibility that differences in epigenetic regulation can act alongside genetic variation to shape evolutionary trajectories. Heritable differences in epigenetic regulation that arise spontaneously are termed "epimutations." Epimutations differ from genetic mutations in 2 key ways-they occur at a higher rate and the loci at which they occur often revert back to their original state within a few generations. Here, we present an extension of the standard population genetic model with selection to incorporate epigenetic variation arising via epimutation. Our model assumes a diploid, sexually reproducing population with random mating. In addition to spontaneous genetic mutation, we included parameters for spontaneous epimutation and back-epimutation, allowing for 4 potential epialleles at a single locus (2 genetic alleles, each with 2 epigenetic states), each of which affect fitness. We then analyzed the conditions under which stable epialleles were maintained. Our results show that highly reversible epialleles can be maintained in long-term equilibrium under neutral conditions in a manner that depends on the epimutation and back-epimutation rates, which we term epimutation-back-epimutation equilibrium. On the other hand, epialleles that compensate for deleterious mutations cause deviations from the expectations of mutation-selection balance by a simple factor that depends on the epimutation and back-epimutation rates. We also numerically analyze several sets of fitness parameters for which large deviations from mutation-selection balance occur. Together, these results demonstrate that transient epigenetic regulation may be an important factor in the maintenance of both epigenetic and genetic variation in populations.

Dataset Information

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

Publications

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

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