Post-metamorphic skeletal growth in the sea urchin Paracentrotus lividus and implications for body plan evolution

Thompson, Jeffrey R.; Paganos, Periklis; Benvenuto, Giovanna; Arnone, Maria Ina; Oliveri, Paola

doi:10.1186/s13227-021-00174-1

Cited by 21 publications

(13 citation statements)

References 43 publications

(36 reference statements)

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“…Immunostaining and assays of cell proliferation followed procedures reported by Thompson et al (2021) . For each developmental time point of interest, 4,000–7,000 embryos or larvae were fixed in 4% PFA, permeabilized in ice-cold methanol, and stored in blocking buffer (BB).…”

Section: Methodsmentioning

confidence: 99%

The Development and Neuronal Complexity of Bipinnaria Larvae of the Sea Star Asterias rubens

Carter

Thompson

Elphick

et al. 2021

Integrative and Comparative Biology

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Free-swimming planktonic larvae are a key stage in the development of many marine phyla, and studies of these organisms have contributed to our understanding of major genetic and evolutionary processes. Although transitory, these larvae often attain a remarkable degree of tissue complexity, with well-defined musculature and nervous systems. Amongst the best studied are larvae belonging to the phylum Echinodermata, but with work largely focused on the pleuteus larvae of sea urchins (class Echinoidea). The greatest diversity of larval strategies amongst echinoderms is found in the class Asteroidea (sea-stars), organisms that are rapidly emerging as experimental systems for genetic and developmental studies. However, the bipinnaria larvae of sea stars have only been studied in detail in a small number of species and although they have been relatively well described neuro-anatomically, they are poorly understood neuro-chemically. Here we have analysed embryonic development and bipinnaria larval anatomy in the common North Atlantic sea-star Asterias rubens, employing use of a variety of staining methods in combination with confocal microscopy. Importantly, the chemical complexity of the nervous system of bipinnaria larvae was revealed with a diverse set of antibodies, with identification of at least three centres with different neuro-chemical signature within the previously described nervous system: the anterior apical organ, oral region and ciliary bands. Furthermore, the anatomy of the musculature and sites of cell division in bipinnaria larvae were analysed. Comparisons of developmental progression and molecular anatomy across the Echinodermata provided a basis for hypotheses on the shared evolutionary and developmental processes that have shaped this group of animals. We conclude that bipinnaria larvae appear to be remarkably conserved across ∼200 million years of evolutionary time and may represent a strong evolutionary and/or developmental constraint for species utilizing this larval strategy.

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Section: Methodsmentioning

confidence: 99%

The Development and Neuronal Complexity of Bipinnaria Larvae of the Sea Star Asterias rubens

Carter

Thompson

Elphick

et al. 2021

Integrative and Comparative Biology

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“…Based on the morphology of Yorkicystis, with its calcified axial and uncalcified extraxial skeletons, we hypothesize that functional knockout of transcription factors or signalling genes towards the top of the skeletal gene regulatory network hierarchy, such as Alx1 or VegfR, in the extraxial regions of growing adult echinoderms will result in a distinct loss of skeleton in those regions. Developments in functional perturbations, paired with recent advances in localizing skeletal gene expression in post-metamorphic echinoderms [51], make testing this hypothesis possible.…”

Section: Discussionmentioning

confidence: 99%

Cambrian edrioasteroid reveals new mechanism for secondary reduction of the skeleton in echinoderms

et al. 2022

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Echinoderms are characterized by a distinctive high-magnesium calcite endoskeleton as adults, but elements of this have been drastically reduced in some groups. Herein, we describe a new pentaradial echinoderm, Yorkicystis haefneri n. gen. n. sp., which provides, to our knowledge, the oldest evidence of secondary non-mineralization of the echinoderm skeleton. This material was collected from the Cambrian Kinzers Formation in York (Pennsylvania, USA) and is dated as ca 510 Ma. Detailed morphological observations demonstrate that the ambulacra (i.e. axial region) are composed of flooring and cover plates, but the rest of the body (i.e. extraxial region) is preserved as a dark film and lacks any evidence of skeletal plating. Moreover, X-ray fluorescence analysis reveals that the axial region is elevated in iron. Based on our morphological and chemical data and on taphonomic comparisons with other fossils from the Kinzers Formation, we infer that the axial region was originally calcified, while the extraxial region was non-mineralized. Phylogenetic analyses recover Yorkicystis as an edrioasteroid, indicating that this partial absence of skeleton resulted from a secondary reduction. We hypothesize that skeletal reduction resulted from lack of expression of the skeletogenic gene regulatory network in the extraxial body wall during development. Secondary reduction of the skeleton in Yorkicystis might have allowed for greater flexibility of the body wall.

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“…For immunostaining, the specimens were fixed in 4% paraformaldehyde (PFA) in 0.1 M phosphate-buffered saline (PBS) for 15 min at room temperature (RT) and were washed four times in PBS. The animals were dehydrated through a graded methanol series and then transferred into ice-cold methanol and stored at −20 °C until use [ 2 , 65 ]. For qRT-PCR analysis, the filtered samples (six biological replicates) were frozen in liquid nitrogen and stored at −80 °C for use.…”

Section: Methodsmentioning

confidence: 99%

Nervous System Development and Neuropeptides Characterization in Embryo and Larva: Insights from a Non-Chordate Deuterostome, the Sea Cucumber Apostichopus japonicus

Zheng

Cong

Liu

et al. 2022

Biology

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Here, we described the complex nervous system at five early developmental stages (blastula, gastrula, auricularia, doliolaria and pentactula) of a holothurian species with highly economic value, Apostichopus japonicus. The results revealed that the nervous system of embryos and larvae is mainly distributed in the anterior apical region, ciliary bands or rings, and the feeding and attachment organs, and that serotonergic immunoreactivity was not observed until the embryo developed into the late gastrula; these are evolutionarily conserved features of echinoderm, hemichordate and protostome larvae. Furthermore, based on available transcriptome data, we reported the neuropeptide precursors profile at different embryonic and larval developmental stages. This analysis showed that 40 neuropeptide precursors present in adult sea cucumbers were also identified at different developmental stages of embryos and larvae, and only four neuropeptide precursors (SWYG precursor 2, GYWKDLDNYVKAHKT precursor, Neuropeptide precursor 14-like precursor, GLRFAmprecursor-like precursor) predicted in adults were absent in embryos and larvae. Combining the quantitative expression of ten specific neuropeptide precursor genes (NPs) by qRT-PCR, we revealed the potential important roles of neuropeptides in embryo development, feeding and attachment in A. japonicus larvae. In conclusion, this work provides novel perspectives on the diverse physiological functions of neuropeptides and contributes to understanding the evolution of neuropeptidergic systems in echinoderm embryos and larvae.

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Post-metamorphic skeletal growth in the sea urchin Paracentrotus lividus and implications for body plan evolution

Cited by 21 publications

References 43 publications

The Development and Neuronal Complexity of Bipinnaria Larvae of the Sea Star Asterias rubens

The Development and Neuronal Complexity of Bipinnaria Larvae of the Sea Star Asterias rubens

Cambrian edrioasteroid reveals new mechanism for secondary reduction of the skeleton in echinoderms

Nervous System Development and Neuropeptides Characterization in Embryo and Larva: Insights from a Non-Chordate Deuterostome, the Sea Cucumber Apostichopus japonicus

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