In Haliotis, NO means YES

Bishop, Cory D.; Biggers, William J.

doi:10.3389/fmars.2014.00051

Cited by 7 publications

(7 citation statements)

References 23 publications

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“…Together, these results indicate that NO signalling is necessary – and perhaps also sufficient – for the induction of settlement and initiation of metamorphosis of A. queenslandica larvae. The activating role of NO in A. queenslandica settlement and metamorphosis contrasts with observations in a range of bilaterian larvae where NO appears to play a repressive or inhibitory role202122232425262728, but is similar to other species where it appears to play an inductive or stimulatory role3031323334.…”

Section: Discussioncontrasting

confidence: 88%

“…7). NO typically represses the initiation of metamorphosis in multiple bilaterian marine invertebrates20212223242526272829, although there are other reported cases where NO acts as an activator of metamorphosis3031323334. The results presented here for the demosponge A. queenslandica phylogenetically extend the role of NO in animal metamorphosis beyond the bilaterians, thus raising the possibility that its action harks back to the last common animal ancestor, and that it has been able to switch between being an activator and repressor of life cycle transitions over the course of animal evolution.…”

Section: Discussionmentioning

confidence: 99%

“…In all of these bilaterian cases, a reduction in the level of endogenously synthesised NO appears sufficient to either alone initiate metamorphosis, or at least to enhance the response to an inductive exogenous cue. The phylogenetic diversity of taxa in which this has been experimentally observed has led to the proposition that NO maintains larvae in a prepared state for metamorphosis25 and that this role for NO may be a highly conserved feature of marine invertebrate settlement and metamorphosis2930. However, there are documented cases in ascidians and a gastropod of NO playing a positive role in regulating the initiation and rate of metamorphosis31323334, raising the possibility that differing roles of NO may be associated with different animal life histories and ecologies30.…”

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confidence: 99%

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An ancient role for nitric oxide in regulating the animal pelagobenthic life cycle: evidence from a marine sponge

Ueda

Richards

Degnan

et al. 2016

Sci Rep

111

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In many marine invertebrates, larval metamorphosis is induced by environmental cues that activate sensory receptors and signalling pathways. Nitric oxide (NO) is a gaseous signalling molecule that regulates metamorphosis in diverse bilaterians. In most cases NO inhibits or represses this process, although it functions as an activator in some species. Here we demonstrate that NO positively regulates metamorphosis in the poriferan Amphimedon queenslandica. High rates of A. queenslandica metamorphosis normally induced by a coralline alga are inhibited by an inhibitor of nitric oxide synthase (NOS) and by a NO scavenger. Consistent with this, an artificial donor of NO induces metamorphosis even in the absence of the alga. Inhibition of the ERK signalling pathway prevents metamorphosis in concert with, or downstream of, NO signalling; a NO donor cannot override the ERK inhibitor. NOS gene expression is activated late in embryogenesis and in larvae, and is enriched in specific epithelial and subepithelial cell types, including a putative sensory cell, the globular cell; DAF-FM staining supports these cells being primary sources of NO. Together, these results are consistent with NO playing an activating role in induction of A. queenslandica metamorphosis, evidence of its highly conserved regulatory role in metamorphosis throughout the Metazoa.

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Section: Discussioncontrasting

confidence: 88%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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An ancient role for nitric oxide in regulating the animal pelagobenthic life cycle: evidence from a marine sponge

Ueda

Richards

Degnan

et al. 2016

Sci Rep

111

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“…At this stage, the larva has the ontogenetic capacity to settle, but does not do so if simply provided with a local settlement cue. This situation may arise due to active inhibition of the sensory system by which the larva responds to local settlement cues (summarized in [ 87 ]), but this type of inhibition can be overcome by an appropriate environmental trigger (in the case of precompetent echinoid larvae, a brief exposure to turbulence) that modifies the reactivity of larvae to more localized chemical or tactile cues. — Phase 3: competent larva .…”

Section: Discussionmentioning

confidence: 99%

Rethinking competence in marine life cycles: ontogenetic changes in the settlement response of sand dollar larvae exposed to turbulence

Hodin

Ferner

et al. 2015

R. Soc. open sci.

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Complex life cycles have evolved independently numerous times in marine animals as well as in disparate algae. Such life histories typically involve a dispersive immature stage followed by settlement and metamorphosis to an adult stage on the sea floor. One commonality among animals exhibiting transitions of this type is that their larvae pass through a ‘precompetent’ period in which they do not respond to localized settlement cues, before entering a ‘competent’ period, during which cues can induce settlement. Despite the widespread existence of these two phases, relatively little is known about how larvae transition between them. Moreover, recent studies have blurred the distinction between the phases by demonstrating that fluid turbulence can spark precocious activation of competence. Here, we further investigate this phenomenon by exploring how larval interactions with turbulence change across ontogeny, focusing on offspring of the sand dollar Dendraster excentricus (Eschscholtz). Our data indicate that larvae exhibit increased responsiveness to turbulence as they get older. We also demonstrate a likely cost to precocious competence: the resulting juveniles are smaller. Based upon these findings, we outline a new, testable conception of competence that has the potential to reshape our understanding of larval dispersal and connectivity among marine populations.

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“…Inhibition of the NO pathway by exogenous NO scavengers or inhibitors to NOS has successfully induced metamorphosis in these species. However, interestingly for some gastropod, ascidian and sponge species, NO had a positive regulatory effect on metamorphosis instead (27)(28)(29)(30)(31), suggesting some species-speci c adaptation in response to NO (32). Nevertheless, NO biosynthesis by NOS is a conserved pathway, found in all types of living organisms from prokaryotes, plants to metazoans with a remarkable conservation of animal NOS despite several duplication events in invertebrates and vertebrates (33)(34)(35).…”

Section: Introductionmentioning

confidence: 99%

Bivalves are NO Different: Nitric Oxide as Negative Regulator of Metamorphosis in the Pacific Oyster, Crassostrea Gigas.

Vogeler

Carboni

et al. 2020

Preprint

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Background Nitric oxide (NO) is a presumed regulator of metamorphosis in many invertebrate species, and although NO pathways have been comparatively well-investigated in gastropods, annelids and crustaceans, there has been very limited research on the effects of NO on metamorphosis in bivalve shellfish.Results In this paper, we investigate the effects of NO pathway inhibitors and NO donors on metamorphosis induction in larvae of the Pacific oyster, Crassostrea gigas, demonstrating that the nitric oxides synthase (NOS) inhibitors s-methylisothiourea hemisulfate salt (SMIS), aminoguanidine hemisulfate salt (AGH) and 7-nitroindazole (7-NI) induce metamorphosis in a concentration-dependent manner ranging from 75%, 76–83% respectively. Additional induction resulted from exposures to 1H-[1, 2, 4]Oxadiazole[4,3-a]quinoxalin-1-one (ODQ), an inhibitor of soluble guanylyl cyclase, with which NO interacts to catalyse the synthesis of cyclic guanosine monophosphate (cGMP). Conversely, high concentrations of the NO donor sodium nitroprusside dihydrate in combination with metamorphosis inducers epinephrine, MK-801 or SMIS, significantly decreased metamorphosis. Expression of CgNOS also decreased in larvae after metamorphosis regardless of the inducers used, but intensified again post-metamorphosis in spat. Fluorescent detection of NO in competent larvae with DAF-FM diacetate and localisation of the oyster nitric oxide synthase CgNOS expression by in-situ hybridisation showed that NO occurs primarily in two key larval structures, the velum and foot. cGMP was also detected in the foot using immunofluorescent assays, and is potentially involved in the foot’s smooth muscle relaxation.Conclusion Together, these results suggest that NO is a negative regulator of metamorphosis in Pacific oyster larvae, and that NO reduction induces metamorphosis by inhibiting swimming or crawling behaviour, in conjunction with a cascade of additional neuroendocrine downstream responses.

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In Haliotis, NO means YES

Cited by 7 publications

References 23 publications

An ancient role for nitric oxide in regulating the animal pelagobenthic life cycle: evidence from a marine sponge

An ancient role for nitric oxide in regulating the animal pelagobenthic life cycle: evidence from a marine sponge

Rethinking competence in marine life cycles: ontogenetic changes in the settlement response of sand dollar larvae exposed to turbulence

Bivalves are NO Different: Nitric Oxide as Negative Regulator of Metamorphosis in the Pacific Oyster, Crassostrea Gigas.

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