A dynamic architecture of life

Abstract

In recent decades, a profound conceptual transformation has occurred comprising different areas of biological research, leading to a novel understanding of life processes as much more dynamic and changeable. Discoveries in plants and animals, as well as novel experimental approaches, have prompted the research community to reconsider established concepts and paradigms. This development was taken as an incentive to organise a workshop in May 2014 at the Academia Nazionale dei Lincei in Rome. There, experts on epigenetics, regeneration, neuroplasticity, and computational biology, using different animal and plant models, presented their insights on important aspects of a dynamic architecture of life, which comprises all organisational levels of the organism. Their work demonstrates that a dynamic nature of life persists during the entire existence of the organism and permits animals and plants not only to fine-tune their response to particular environmental demands during development, but underlies their continuous capacity to do so. Here, a synthesis of the different findings and their relevance for biological thinking is presented.

Keywords: computational biology; development; limb regeneration; neuroplasticity; plant epigenetics; repair regeneration; tissue homeostasis.

Figure 1.. Homeostatic and developmental plasticity in Hydra.

The scheme represents the typical epithelial bilayered anatomy of Hydra polyps with interstitial stem cells (green dots) distributed along the central body column (framed box). By contrast cells at the apical and basal extremities are terminally differentiated. A highly dynamic homeostasis with continuous renewal of stem cells supports the fitness and the low senescence of Hydra. Animals survive long periods of starvation as well as the elimination of the nervous system if force-fed. After bisection at any level along the body column, the stump is able to reestablish an organizer centre and regenerate the missing part, either basal or apical. However, some Hydra oligactis strains show a very low level of plasticity: they do not adapt to the loss of neuronal progenitors induced by the transfer to cold temperature, they rapidly lose the ability to regenerate, undergo aging, and finally die in a couple of months.

Figure 2.. Critical period and the role of Otx2.

Sensory signals, for example eye opening at P14 in the mouse, triggers Perineuronal net (PNN) assembly at the surface of Parvalbumin neurons in layers III/IV of the visual cortex. PNN complex sugars specifically recognize Otx2 en route from extra-cortical sources and enhance its internalization by Parvalbumin neurons, thus triggering the maturation of this class of interneurons. Otx2 reaches a first intracellular concentration threshold that opens plasticity and accumulates until a second threshold closes plasticity. The maintenance of an adult non-plastic state requires the continuous import of Otx2 from extra-cortical sources and blocking the latter import reopens a window of plasticity in the adult.

Figure 3.. The plasticity of the target morphology in planarian worms.

The regenerating phenotype from an amputated planarian trunk piece can be locally and permanently altered by non-genetic perturbations, suggesting a linear encoding of the target morphology outside the genome. Experiments extracted from Planform ( Lobo et al., 2013a).