Evidence, mechanisms and models for the inheritance of acquired characters

doi:10.1016/S0022-5193(05)80722-2

Journal of Theoretical Biology

Volume 158, Issue 2, 21 September 1992, Pages 245-268

https://doi.org/10.1016/S0022-5193(05)80722-2 Get rights and content

Several different types of epigenetic inheritance system enable alternative functional states to be maintained in cell lineages that have identical DNA sequences. Both random and guided (directed) epigenetic variations can be transmitted by these systems, and lead to heritable modifications in cell structure and function. Although it is usually assumed that epigenetic inheritance does not occur between generations, both old and new experimental evidence suggest, and in some cases show explicitly, that epigenetic variations can be transmitted from parents to progeny. Simple models of epigenetic inheritance in asexual and sexual organisms are presented. These show that in populations of asexual unicellular organisms, the distinctive properties of induced epigenetic variations mean that the variations may be retained for many generations after the inducing stimulus is removed, even in the absence of selection. The models also show that the epigenetic systems enable some types of acquired character to be inherited in sexual, as well as asexual, organisms. The importance of epigenetic inheritance systems in the evolution of multicellularity is discussed.

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A model in which decoherence is localized to intercompartmental boundaries suggests a strong and potentially testable prediction: that internal, bulk states of daughter cells may remain entangled for macroscopic times following cell division. While long-lasting mirror symmetry of cytoskeletal components and hence motion patterns as well as cell-cycle correlation of sister cells has been observed (Albrecht-Buehler, 1977) and numerous examples of epigenetic inheritance (Jablonka et al., 1992; Cunliffe, 2015), including epigenetic inheritance of organism-scale bioelectric state (Durant et al., 2017, 2019) are now known, Bell-type experiments that directly test for state entanglement in recently-separated sister cells have not, to our knowledge, yet been performed. If coherence is preserved as the above analysis suggests, perturbations of bulk biochemical state, e.g. targeting intermediate components of signal transduction pathways, in one daughter cell may be expected to affect the behavior of the other, biochemically and bioelectrically isolated, daughter cell.
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Evidence, mechanisms and models for the inheritance of acquired characters

Cell

Progr. Brain Res.

Cell

Cell

J. theor. Biol.

Int. J. Insect Morphol. Embryol.

J. theor. Biol.

Cell

Trends Genet.

Cell

Cell

Cell

Daughter 3T3 cells: are they mirror images of each other?

J. cell Biol.

The Genetics of Paramecium aurelia

The Lansing effect and age-mediated changes in genetic parameters

Genetica

Cytoplasmic inheritance of the organization of the cell cortex in Paramecium aurelia

Effect of hydrocortisone on the phenotypic expression and inheritance of the fused gene in mice

Theor. appl. Genet.

Inheritance of alternative states of the fused gene in mice

J. Hered.

Phase change in higher plants and somatic cell heredity

Q. Rev. Biol.

Paramutation

A. Rev. Genet.

The Evolution of Individuality

The origin of mutants

Nature, Lond.

DNA modification of a maize transposable element correlates with loss of activity

Inactivation of the maize transposable element Activator (Ac) is associated with its DNA modification

EMBO J.

Chromatin structure and gene expression

DNA methylation of maize transposable elements is correlated with activity

Phil. Trans. R. Soc. Lond. B

Molecular genetic analysis of the maize Suppressormutator element's epigenetic developmental regulatory mechanism

Genome

Mutations, epimutations, and the developmental programming of the maize Suppressor-mutator transposable element

BioEssays

Variation and inheritance of cytosine methylation patterns in wheat at the high molecular weight glutenin and ribosomal RNA gene loci

Development

Heritable nature of colchicine induced variation in diploid Lolium perenne

Heredity

Maternal inhibition of hepatitis B surface antigen gene expression in transgenic mice correlates with de novo methylation

Nature, Lond.

Inheritance of DNA methylation in microinjected eggs of Xenopus laevis

Phenotypic changes in cell culture

Transmission of phenotypic variability within a pure line

Nature, Lond.

Temperature-induced variability in peas

Am. J. Bot.