A transcriptional time-course analysis of oral vs. aboral whole-body regeneration in the Sea anemone Nematostella vectensis

Abstract

BackgroundThe ability of regeneration is essential for the homeostasis of all animals as it allows the repair and renewal of tissues and body parts upon normal turnover or injury. The extent of this ability varies greatly in different animals with the sea anemone Nematostella vectensis, a basal cnidarian model animal, displaying remarkable whole-body regeneration competence.ResultsIn order to study this process in Nematostella we performed an RNA-Seq screen wherein we analyzed and compared the transcriptional response to bisection in the wound-proximal body parts undergoing oral (head) or aboral (tail) regeneration at several time points up to the initial restoration of the basic body shape. The transcriptional profiles of regeneration responsive genes were analyzed so as to define the temporal pattern of differential gene expression associated with the tissue-specific oral and aboral regeneration. The identified genes were characterized according to their GO (gene ontology) assignations revealing groups that were enriched in the regeneration process with particular attention to their affiliation to the major developmental signaling pathways. While some of the genes and gene groups thus analyzed were previously known to be active in regeneration, we have also revealed novel and surprising candidate genes such as cilia-associated genes that likely participate in this important developmental program.ConclusionsThis work highlighted the main groups of genes which showed polarization upon regeneration, notably the proteinases, multiple transcription factors and the Wnt pathway genes that were highly represented, all displaying an intricate temporal balance between the two sides. In addition, the evolutionary comparison performed between regeneration in different animal model systems may reveal the basic mechanisms playing a role in this fascinating process.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3027-1) contains supplementary material, which is available to authorized users.

The rapid regenerative response of a model sea anemone speciesExaiptasia pallidais characterised by tissue plasticity and highly coordinated cell communication

“…Key genes found by Schaffer et al (2016) to be differentially expressed in orally regenerating N. vectensis include multiple components of the Wnt pathway, multiple transcription factors and homeobox genes, consistent with results here for E. pallida and with an earlier study on N. vectensis (DuBuc et al 2014). The homeobox gene Otxc was not found in the present study, consistent with it being found to denote physa (foot) not oral regeneration in N.…”

“…This indicates that N. vectensis is not the most representative model species for anemone regeneration. Multiple recent studies have explored regeneration in N. vectensis from a transcriptional, morphological and cellular perspective (Amiel et al 2015;DuBuc et al 2014;Schaffer et al 2016) and some similarities and differences can be drawn between this species and E. pallida.…”

“…In contrast to N. vectensis, Notch pathway genes were not differentially expressed in this study (except for one notch1 gene DE at T1 vs T5, Supplementary Table S5g). There is no evidence that any of the DE E. pallida genes have either a chitin binding or synthesising protein domain (chitin genes were found highly enriched in N. vectensis (Schaffer et al 2016)), although the GO term associated with 'chitin binding' (GO:0008061) is found in several genes with carbohydrate binding domains, one of which is Chitotriosidase-1 (DE at T1 vs T2, Supplementary Table S5g). Other results for N. vectensis found by DuBuc et al (2014) are also consistently found in E. pallida, e.g., the MAPK cascade was proposed to be essential for would healing and is significantly enriched here and many metalloproteinases can be found throughout the timecourse.…”

Whole body regeneration deploys a rewired embryonic gene regulatory network logic

“…A long-standing question in the field of regeneration is whether and to what extent embryonic gene programs that are initially used to build an organism are re-used during regeneration (Morgan 1901). Several transcriptomic studies of regeneration have highlighted the importance of re-deployed developmental pathways in axolotl, anole, zebrafish and sea anemones (Bryant et al 2017) (Habermann et al 2004) (Hutchins et al 2014) (Mathew et al 2009) (Rodius et al 2016) (Gardiner et al 1995;Schaffer et al 2016). Many studies have directly compared embryonic and regenerative gene expression of single or groups of genes identifying i) genes that are specific to embryonic development (Binari et al 2013), ii) genes that are specifically expressed or required during regeneration (Millimaki et al 2010;Katz et al 2015), and iii) embryonic genes that are re-used during regeneration to some extent (Imokawa and Yoshizato 1997) (Carlson et al 2001) (Torok et al 1998) (Özpolat et al 2012) (Wang and Beck 2014).…”

“…Nematostella has long been used as a model system for embryonic development, the evolution of body patterning, and gene regulatory networks (Hand and Uhlinger 1992;Wikramanayake et al 2003;Hutchins et al 2014; Wang and Beck 2014). More recently, Nematostella has emerged as a powerful whole-body regeneration model as it capable of re-growing missing body parts in less than a week (Burton and Finnerty 2009;Trevino et al 2011;Passamaneck and Martindale 2012;Bossert et al 2013;Dubuc et al 2014;Amiel et al 2015;Schaffer et al 2016) Regeneration in Nematostella follows a dynamic but highly stereotypical morphological and cellular program involving tissue rearrangement and the de novo formation of body structures (Amiel et al 2015).…”