Developmental and molecular biology of annelid regeneration: a comparative review of recent studies

Özpolat, B. Duygu; Bely, Alexandra E.

doi:10.1016/j.gde.2016.07.010

Cited by 85 publications

(117 citation statements)

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“…Morgan proposed what has proven to be a resilient distinction between epimorphic regeneration, in which the replacement tissue is produced via cellular proliferation, and morphallactic regeneration, in which the tissue proximal to the wound is remodeled into a smaller version of the complete body part without proliferation at the wound site (Morgan 1901). Despite the breadth of taxon sampling that informed Morgan’s understanding of regeneration (Sunderland 2010), the categorization has not always been found to hold strictly true; many species that engage in epimorphosis also engage either simultaneously or sequentially in morphallactic remodeling (Özpolat and Bely 2016), whereas other regenerative mechanisms defy categorization when examined with modern tools. There are also substantial differences in the cellular mechanisms underlying examples of each type of regeneration (e.g., the wide variety of replacement tissue origins, [Tiozzo and Copley 2015]).…”

Section: Introductionmentioning

confidence: 99%

“…2016; Özpolat and Bely 2016; Boilly et al. 2017), and are proving extremely beneficial for bilaterian-wide comparisons of a number of biological processes (Christodoulou et al.…”

Section: Introductionmentioning

confidence: 99%

“…2009, 2012; Ferrier 2012). Recent studies of annelid regeneration focus almost exclusively on antero-posterior segmental regeneration, which follows a stereotyped morphological sequence of wound healing, blastema formation, blastema patterning, differentiation, and growth (Bely 2014; Özpolat and Bely 2016). However, there are clear differences, notably with regards to the presence/absence of morphallactic processes occurring proximally to the dissection plane, even between closely related species (Licciano et al.…”

Section: Introductionmentioning

confidence: 99%

“…2008) in nereids and Capitella teleta . Hox expression in the regenerative blastema seems to be ancestral to the annelids (Özpolat and Bely 2016). They do not exhibit spatial or temporal collinearity of regenerative expression, indicating that they are not recapitulating embryogenic roles.…”

Section: Introductionmentioning

confidence: 99%

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A Revised Spiralian Homeobox Gene Classification Incorporating New Polychaete Transcriptomes Reveals a Diverse TALE Class and a Divergent Hox Gene

Barton-Owen

Szabó

Somorjai

et al. 2018

Genome Biology and Evolution

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The diversity of mechanisms and capacity for regeneration across the Metazoa present an intriguing challenge in evolutionary biology, impacting on the burgeoning field of regenerative medicine. Broad taxonomic sampling is essential to improve our understanding of regeneration, and studies outside of the traditional model organisms have proved extremely informative. Within the historically understudied Spiralia, the Annelida have an impressive variety of tractable regenerative systems. The biomeralizing, blastema-less regeneration of the head appendage (operculum) of the serpulid polychaete keelworm Spirobranchus (formerly Pomatoceros) lamarcki is one such system. To profile potential regulatory mechanisms, we classified the homeobox gene content of opercular regeneration transcriptomes. As a result of retrieving several difficult-to-classify homeobox sequences, we performed an extensive search and phylogenetic analysis of the TALE and PRD-class homeobox gene content of a broad selection of lophotrochozoan genomes. These analyses contribute to our increasing understanding of the diversity, taxonomic extent, rapid evolution, and radical flexibility of these recently discovered homeobox gene radiations. Our expansion and integration of previous nomenclature systems helps to clarify their cryptic orthology. We also describe an unusual divergent S. lamarcki Antp gene, a previously unclassified lophotrochozoan orphan gene family (Lopx), and a number of novel Nk class orphan genes. The expression and potential involvement of many of these lineage- and clade-restricted homeobox genes in S. lamarcki operculum regeneration provides an example of diversity in regenerative mechanisms, as well as significantly improving our understanding of homeobox gene evolution.

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Section: Introductionmentioning

confidence: 99%

“…2016; Özpolat and Bely 2016; Boilly et al. 2017), and are proving extremely beneficial for bilaterian-wide comparisons of a number of biological processes (Christodoulou et al.…”

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

A Revised Spiralian Homeobox Gene Classification Incorporating New Polychaete Transcriptomes Reveals a Diverse TALE Class and a Divergent Hox Gene

Barton-Owen

Szabó

Somorjai

et al. 2018

Genome Biology and Evolution

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“…The primary function of these photosensitive structures, and those more recently documented in ark clams, is likely to be shadow detection [6], but so far research into the underlying molecular mechanisms of the shadow reflex has been limited due to the dearth of molecular tools available in these model organisms. Platynereis dumerilii, a molecularly slowly evolving [8, 9], morphologically archetypical marine nereidid [10], and distant annelid relative of sabellid fan worms [11–13], with its expansive genetic toolkit [14] and observable, well-characterised shadow reflex [15], represents a useful model to understand the molecular mechanisms and evolution of this behaviour. Platynereis dumerilii is a predominantly nocturnal animal, but the animals also exhibit movement and exploratory behaviour during the day, anchoring their trunks inside protective tubes whilst occasionally reaching out with their heads, likely to survey the environment and to feed [16].…”

Section: Introductionmentioning

confidence: 99%

A Go-type opsin mediates the shadow reflex in the annelid Platynereis dumerilii

et al. 2018

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BackgroundThe presence of photoreceptive molecules outside the eye is widespread among animals, yet their functions in the periphery are less well understood. Marine organisms, such as annelid worms, exhibit a ‘shadow reflex’, a defensive withdrawal behaviour triggered by a decrease in illumination. Herein, we examine the cellular and molecular underpinnings of this response, identifying a role for a photoreceptor molecule of the Go-opsin class in the shadow response of the marine bristle worm Platynereis dumerilii.ResultsWe found Pdu-Go-opsin1 expression in single specialised cells located in adult Platynereis head and trunk appendages, known as cirri. Using gene knock-out technology and ablation approaches, we show that the presence of Go-opsin1 and the cirri is necessary for the shadow reflex. Consistently, quantification of the shadow reflex reveals a chromatic dependence upon light of approximately 500 nm in wavelength, matching the photoexcitation characteristics of the Platynereis Go-opsin1. However, the loss of Go-opsin1 does not abolish the shadow reflex completely, suggesting the existence of a compensatory mechanism, possibly acting through a ciliary-type opsin, Pdu-c-opsin2, with a Lambdamax of approximately 490 nm.ConclusionsWe show that a Go-opsin is necessary for the shadow reflex in a marine annelid, describing a functional example for a peripherally expressed photoreceptor, and suggesting that, in different species, distinct opsins contribute to varying degrees to the shadow reflex.Electronic supplementary materialThe online version of this article (10.1186/s12915-018-0505-8) contains supplementary material, which is available to authorized users.

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Circalunar clocks—Old experiments for a new era

Kaiser

Neumann

2021

BioEssays

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Circalunar clocks, which allow organisms to time reproduction to lunar phase, have been experimentally proven but are still not understood at the molecular level. Currently, a new generation of researchers with new tools is setting out to fill this gap. Our essay provides an overview of classic experiments on circalunar clocks. From the unpublished work of the late D. Neumann we also present a novel phase response curve for a circalunar clock. These experiments highlight avenues for molecular work and call for rigor in setting up and analyzing the logistically complex experiments on circalunar clocks. Re-evaluating classic experiments, we propose that (1) circalunar clocks in different organisms will have divergent mechanisms and physiological bases, (2) they may have properties very different from the well-studied circadian clocks and (3) they may have close mechanistic and molecular relations to seasonal rhythms and diapause.

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Developmental and molecular biology of annelid regeneration: a comparative review of recent studies

Cited by 85 publications

References 74 publications

A Revised Spiralian Homeobox Gene Classification Incorporating New Polychaete Transcriptomes Reveals a Diverse TALE Class and a Divergent Hox Gene

A Revised Spiralian Homeobox Gene Classification Incorporating New Polychaete Transcriptomes Reveals a Diverse TALE Class and a Divergent Hox Gene

A Go-type opsin mediates the shadow reflex in the annelid Platynereis dumerilii

Circalunar clocks—Old experiments for a new era

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