Abstract:Most species of the class Holothuroidea are able to regenerate most of their internal organs following a typical evisceration process, which is a unique mechanism that allows sea cucumbers to survive in adverse environments. In this review, we compare autotomy among different type of sea cucumber and summarize the histocytological events that occur during the five stages of intestinal regeneration. Multiple cytological activities, such as apoptosis and dedifferentiation, take place during wound healing and anl… Show more
“…A series of studies performed differential gene expression analysis of A. japonicus subjected to environmental changes such as different light stimuli [ 90 ], different salinity conditions [ 173 ], and copper exposure [ 87 ]. Because sea cucumbers show the remarkable ability of quickly replacing injured organs, transcriptomes have been generated on H. glaberrima, E. fraudatrix , and A. japonic us during gut evisceration and regeneration [ 44 , 115 , 123 , 124 , 136 , 144 , 145 ], radial organ complex regeneration [ 109 ], and muscle regeneration [ 111 ]. Other studies explored gene expression during aestivation, a process that so far has been exclusively observed in sea sponges and sea cucumbers [ 159 , 174 – 176 ].…”
Section: Genomic-transcriptomic Information and Cellular And Molecula...mentioning
confidence: 99%
“…The consequence of sea cucumbers' increased economic value has led to their illegal and unsustainable fishing to fulfill the market [ 20 , 59 ], but also prompted many detailed studies for their rearing in animal farms. In fact, although most studies are performed on the adults (including ecotoxicological assessments, isolation of bioactive compounds from adult tissues, exploration of their regeneration capacities, reviewed in [ 23 , 108 , 144 , 145 ], there is significant growing interest in dissecting the factors that regulate and/or influence sea cucumbers’ embryonic and larval development, for both aquaculture and basic research purposes. Fig.…”
A challenge for evolutionary developmental (evo-devo) biology is to expand the breadth of research organisms used to investigate how animal diversity has evolved through changes in embryonic development. New experimental systems should couple a relevant phylogenetic position with available molecular tools and genomic resources. As a phylum of the sister group to chordates, echinoderms extensively contributed to our knowledge of embryonic patterning, organ development and cell-type evolution. Echinoderms display a variety of larval forms with diverse shapes, making them a suitable group to compare the evolution of embryonic developmental strategies. However, because of the laboratory accessibility and the already available techniques, most studies focus on sea urchins and sea stars mainly. As a comparative approach, the field would benefit from including information on other members of this group, like the sea cucumbers (holothuroids), for which little is known on the molecular basis of their development. Here, we review the spawning and culture methods, the available morphological and molecular information, and the current state of genomic and transcriptomic resources on sea cucumbers. With the goal of making this system accessible to the broader community, we discuss how sea cucumber embryos and larvae can be a powerful system to address the open questions in evo-devo, including understanding the origins of bilaterian structures.
“…A series of studies performed differential gene expression analysis of A. japonicus subjected to environmental changes such as different light stimuli [ 90 ], different salinity conditions [ 173 ], and copper exposure [ 87 ]. Because sea cucumbers show the remarkable ability of quickly replacing injured organs, transcriptomes have been generated on H. glaberrima, E. fraudatrix , and A. japonic us during gut evisceration and regeneration [ 44 , 115 , 123 , 124 , 136 , 144 , 145 ], radial organ complex regeneration [ 109 ], and muscle regeneration [ 111 ]. Other studies explored gene expression during aestivation, a process that so far has been exclusively observed in sea sponges and sea cucumbers [ 159 , 174 – 176 ].…”
Section: Genomic-transcriptomic Information and Cellular And Molecula...mentioning
confidence: 99%
“…The consequence of sea cucumbers' increased economic value has led to their illegal and unsustainable fishing to fulfill the market [ 20 , 59 ], but also prompted many detailed studies for their rearing in animal farms. In fact, although most studies are performed on the adults (including ecotoxicological assessments, isolation of bioactive compounds from adult tissues, exploration of their regeneration capacities, reviewed in [ 23 , 108 , 144 , 145 ], there is significant growing interest in dissecting the factors that regulate and/or influence sea cucumbers’ embryonic and larval development, for both aquaculture and basic research purposes. Fig.…”
A challenge for evolutionary developmental (evo-devo) biology is to expand the breadth of research organisms used to investigate how animal diversity has evolved through changes in embryonic development. New experimental systems should couple a relevant phylogenetic position with available molecular tools and genomic resources. As a phylum of the sister group to chordates, echinoderms extensively contributed to our knowledge of embryonic patterning, organ development and cell-type evolution. Echinoderms display a variety of larval forms with diverse shapes, making them a suitable group to compare the evolution of embryonic developmental strategies. However, because of the laboratory accessibility and the already available techniques, most studies focus on sea urchins and sea stars mainly. As a comparative approach, the field would benefit from including information on other members of this group, like the sea cucumbers (holothuroids), for which little is known on the molecular basis of their development. Here, we review the spawning and culture methods, the available morphological and molecular information, and the current state of genomic and transcriptomic resources on sea cucumbers. With the goal of making this system accessible to the broader community, we discuss how sea cucumber embryos and larvae can be a powerful system to address the open questions in evo-devo, including understanding the origins of bilaterian structures.
“…Stichopus horrens). Sea cucumbers that have autotomized their viscera can rapidly regenerate their internal organs, some in as little as two weeks [138][139][140][141]. While studies show that sea cucumbers that have their viscera manually removed re-grow their organs at a similar rate than those that eviscerate via autotomy [133], other metrics of wellbeing (e.g.…”
Section: Potential Applications Of Autotomymentioning
Autotomy refers to self-amputation where the loss of a limb or organ is generally said to be (1) in response to stressful external stimuli; (2) voluntary and nervously mediated; (3) supported by adaptive features that increase efficiency and simultaneously mediate the cost; and (4) morphologically delineated by a predictable breakage plane. It is estimated that this phenomenon has evolved independently nine different times across the animal kingdom, appearing in many different taxa, including vertebrate and invertebrate as well as aquatic and terrestrial animals. Marine invertebrates use this behaviour in a diversity of manners that have yet to be globally reviewed and critically examined. Here, published data from marine invertebrate taxa were used to explore instances of injury as an evolutionary driver of autotomy. Findings suggest that phyla (e.g. Echinodermata and Arthropoda) possibly experiencing high rates of injury (tissue damage or loss) are more likely to be able to perform autotomy. Additionally, this review looks at various morphological, physiological and environmental conditions that have either driven the evolution or maintained the behaviour of autotomy in marine invertebrates. Finally, the use of autotomic abilities in the development of more sustainable and less ecologically invasive fisheries is explored.
“…This extraordinary ability makes them a valuable model for studying regeneration in complex organisms. The regeneration of the digestive system in holothurians, in particular, has garnered significant interest (Dolmatov, 2021; Mashanov et al, 2014; Medina-Feliciano and García-Arrarás, 2021; Quispe-Parra et al, 2021; Su et al, 2022). Upon evisceration, the holothurian intestine, which constitutes nearly their entire digestive tract, begins to regenerate from the mesentery, a supportive tissue layer where the original intestine was attached (García-Arrarás et al, 1998).…”
In holothurians, the regenerative process following evisceration involves the development of a “rudiment” or “anlage” at the injured end of the mesentery. This regenerating anlage plays a pivotal role in the formation of a new intestine. Despite its significance, our understanding of the molecular characteristics inherent to the constituent cells of this structure has remained limited. To address this gap, we employed state-of-the-art scRNA-seq and HCR-FISH analyses to discern the distinct cellular populations associated with the regeneration anlage. Through this approach, we successfully identified thirteen distinct cell clusters. Among these, two clusters exhibit characteristics consistent with putative mesenchymal cells, while another four show features akin to coelomocyte cell populations. The remaining seven cell clusters collectively form a large group encompassing the coelomic epithelium of the regenerating anlage and mesentery. Within this large group of clusters, we recognized previously documented cell populations such as muscle precursors, neuroepithelial cells and actively proliferating cells. Strikingly, our analysis provides data for identifying at least four other cellular populations that we define as the precursor cells of the growing anlage. Consequently, our findings strengthen the hypothesis that the coelomic epithelium of the anlage is a pluripotent tissue that gives rise to diverse cell types of the regenerating intestinal organ. Moreover, our results provide the initial view into the transcriptomic analysis of cell populations responsible for the amazing regenerative capabilities of echinoderms.
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