Hydra, a fruitful model system for 270 years

Abstract

The discovery of Hydra regeneration by Abraham Trembley in 1744 promoted much scientific curiosity thanks to his clever design of experimental strategies away from the natural environment. Since then, this little freshwater cnidarian polyp flourished as a potent and fruitful model system. Here, we review some general biological questions that benefitted from Hydra research, such as the nature of embryogenesis, neurogenesis, induction by organizers, sex reversal, symbiosis, aging, feeding behavior, light regulation, multipotency of somatic stem cells, temperature-induced cell death, neuronal transdifferentiation, to cite only a few. To understand how phenotypes arise, theoricists also chose Hydra to model patterning and morphogenetic events, providing helpful concepts such as reaction-diffusion, positional information, and autocatalysis combined with lateral inhibition. Indeed, throughout these past 270 years, scientists used transplantation and grafting experiments, together with tissue, cell and molecular labelings, as well as biochemical procedures, in order to establish the solid foundations of cell and developmental biology. Nowadays, thanks to transgenic, genomic and proteomic tools, Hydra remains a promising model for these fields, but also for addressing novel questions such as evolutionary mechanisms, maintenance of dynamic homeostasis, regulation of stemness, functions of autophagy, cell death, stress response, innate immunity, bioactive compounds in ecosystems, ecotoxicant sensing and science communication. KEY WORDS: historical perspective, transplantation, modeling, developmental reactivation, Hydra regeneration, multipotency, stemness, symbiosis, environmentThe heuristic value of the Hydra model systemIn the early 18th century the word biology was not yet in use but the nature of living organisms and their evolutionary relationships was the focus of interest for philosophers and naturalists, as evidenced by their pioneering efforts to develop new tools such as microscopes that would allow finer observation (Palm, 1996). The microscopic observation of organisms taken in the field undoubtedly helped develop morphological keys to sort between the animal and vegetal kingdoms and to group them into phyla (Linnaeus, 1758). Among the ambiguous species that could not be easily classified were the seawater corals that looked like flowers (Watson, 1753;McConnell, 1990) and the freshwater Hydra polyp that was considered to exhibit both animal and vegetal features. For example, Hydra easily reproduces asexually through budding, a trait frequently assigned to plants or fungi.Having observed some Hydra polyps in a pond, Abraham Trembley (1710-1784) (who had received a PhD in mathematics from the University of Geneva (Switzerland) and was now educating the children of the Count of Bentick in the Netherlands) decided Int. J. Dev. Biol. 56: 411-423 (2012) to solve that problem by testing their capacity to regenerate, assuming that if Hydra regenerates, then it should be considered a plant, but if it does...

Evolutionary history of the mammalian synaptonemal complex

“…The second hypothesis seems to be most probable as very distantly related orthologues of SYCP1, SYCE2 and likely SYCP2 could be identified in the ecdysozoan phylum of Crustacea. Indeed, ecdysozoans have ostensibly lost many gene families which are otherwise conserved from Hydra to human (Galliot 2012). Thus, the SC components are not the first case in which Drosophila and C. elegans hold a rather exceptional role.…”

“…Additionally it will be discussed which methods are practicable to study the SC and its function in this organism. Hydra has been a model organism for biological research for more than 250 years (Galliot 2012). It belongs to the very old phylum of Cnidaria which is a sister group to the Bilateria (see also Figure 6-1).…”

Trithorax regulates systemic signaling duringDrosophilaimaginal disc regeneration

“…Although planarian flatworms and freshwater Hydra are capable of replacing a complete organism (Elliott and Sánchez Alvarado, 2013;Galliot, 2012) and urodele amphibians and teleost fish can replace whole appendages (Gemberling et al, 2013;McCusker and Gardiner, 2011), the regenerative capacity of mammals is restricted and decreases significantly with maturity and age. Therefore, understanding the regulatory mechanisms that permit and promote regeneration in model organisms is of great importance to the field of regenerative medicine, which seeks to enhance the regenerative capacity of human tissues.…”

Invertebrates as Model Organisms for Research on Aging Biology ∗

“…However, higher bilaterians, including humans seem to have traded immortality for greater complexity and safeguards against unregulated cell growth. Several recent papers review the utility of Hydra as a model for aging studies (Galliot 2012;Martinez & Bridge 2012;Boehm et al 2013;Schaible & Sussman 2013), and reviews by Galliot and by Bellantuono et al (laboratory of Martinez) in this volume highlight their recent work on these organisms.…”