A “poly-matter network” conception of biological inheritance

Abstract

Here we intend to shift the “DNA- and information-centric” conception of biological inheritance, with the accompanying exclusion of any non-DNA matter, to a “poly-matter network” framework which, in addition to DNA, considers the action of other cellular membranous constituents. These cellular structures, in particular organelles and plasma membranes, express “landscapes” of specific topologies at their surfaces, which may become altered in response to certain environmental factors. These so-called “membranous environmental landscapes” (MELs), which replicate by self-organization / autopoiesis rather than self-assembly, are transferred from donor to acceptor cells by various – vesicular and non-vesicular – mechanisms and exert novel features in the acceptor cells. The “DNA-centric” conception may be certainly explanatorily sufficient for the transfer of heritable phenotype variation to acceptor cells following the copying of DNA in donor cells and thereby for the phenomenon of biological inheritance of traits. However, it is not causally sufficient. With the observation of phenotype variation, as initially manifested during bacterial transformation, the impact of environmental factors, such as nutrition and stress, in the differential regulation of gene expression has been widely accepted and resulted in intense efforts to resolve the underlying epigenetic mechanisms. However, these are explained under a conceptual frame where the DNA (and associated proteins) are the only matter of inheritance. In contrast, it is our argumentation that inheritance can only be adequately understood as the transfer of DNA in concert with non-DNA matter in a “poly-matter network” conception. The adequate inclusion of the transfer of non-DNA matter is still a desideratum of future genetic research, which may pave the way for the experimental elucidation not only of how DNA and membrane matter act in concert to enable the inheritance of innate traits, but also whether they interact for that of acquired biological traits. Moreover, the “poly-matter network” conception may open new perspectives for an understanding of the pathogenesis of “common complex” diseases.