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The diatom-derived aldehyde decadienal affects life cycle transition in the ascidian Ciona intestinalis through nitric oxide/ERK signalling.

Castellano I, Ercolesi E, Romano G, Ianora A, Palumbo A - Open Biol (2015)

Bottom Line: PUAs, including 2,4-trans-decadienal (DD), induce deleterious effects on embryonic and larval development of several planktonic and benthic organisms.DD affects redox balance by reducing total glutathione and NO levels.By biochemical and quantitative gene expression analysis, we identify the NO-signalling network affected by DD, including the upregulation of ERK phosphatase mkp1 and consequent reduction of ERK phosphorylation, with final changes in the expression of downstream ERK target genes.

View Article: PubMed Central - PubMed

Affiliation: Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy.

ABSTRACT
Polyunsaturated aldehydes (PUAs) are fatty-acid-derived metabolites produced by some microalgae, including different diatom species. PUAs are mainly produced as a wound-activated defence mechanism against microalgal predators or released from senescent cells at the end of a bloom. PUAs, including 2,4-trans-decadienal (DD), induce deleterious effects on embryonic and larval development of several planktonic and benthic organisms. Here, we report on the effects of DD on larval development and metamorphosis of the ascidian Ciona intestinalis. Ciona larval development is regulated by the cross-talking of different molecular events, including nitric oxide (NO) production, ERK activation and caspase 3-dependent apoptosis. We report that treatment with DD at the competence larval stage results in a delay in metamorphosis. DD affects redox balance by reducing total glutathione and NO levels. By biochemical and quantitative gene expression analysis, we identify the NO-signalling network affected by DD, including the upregulation of ERK phosphatase mkp1 and consequent reduction of ERK phosphorylation, with final changes in the expression of downstream ERK target genes. Overall, these results give new insights into the molecular pathways induced in marine organisms after exposure to PUAs during larval development, demonstrating that this aldehyde affects key checkpoints of larval transition from the vegetative to the reproductive life stage.

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Decadienal (DD) induces a delay in metamorphosis at the time of competence. (a) Early, middle and late stage larvae were treated with 0.5 µg ml−1 DD. (b) Middle-late stage larvae were treated with different concentrations of DD (0.125, 0.25, 0.5, 0.9, 1.35 µg ml−1). After 24 h of treatment, the number of late larvae, larvae during tail regression (white bars) and juveniles (grey bars) were counted and reported as percentage of the total. Results are representative of 7 (a) and 10 (b) independent experiments. Data, expressed as means ± s.e.m., were assessed by unpaired t-test. Asterisks represent significant differences with respect to the control: **p < 0.01, ***p < 0.001. (c) Left panel shows untreated control juvenile and right panel shows abnormal juvenile after 72 h of incubation with 0.5 µg ml−1 DD. (d) Larva treated with 1.35 µg ml−1 DD after 24 h of treatment (toxic effect).
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RSOB140182F1: Decadienal (DD) induces a delay in metamorphosis at the time of competence. (a) Early, middle and late stage larvae were treated with 0.5 µg ml−1 DD. (b) Middle-late stage larvae were treated with different concentrations of DD (0.125, 0.25, 0.5, 0.9, 1.35 µg ml−1). After 24 h of treatment, the number of late larvae, larvae during tail regression (white bars) and juveniles (grey bars) were counted and reported as percentage of the total. Results are representative of 7 (a) and 10 (b) independent experiments. Data, expressed as means ± s.e.m., were assessed by unpaired t-test. Asterisks represent significant differences with respect to the control: **p < 0.01, ***p < 0.001. (c) Left panel shows untreated control juvenile and right panel shows abnormal juvenile after 72 h of incubation with 0.5 µg ml−1 DD. (d) Larva treated with 1.35 µg ml−1 DD after 24 h of treatment (toxic effect).

Mentions: To investigate the effect of DD on C. intestinalis larval settlement and subsequent metamorphosis, larvae were treated at different times from hatching, corresponding to early, middle and late larval stages. Larvae were morphologically analysed after 24 h treatment. DD did not significantly affect the rate of metamorphosis when added at the early stage, whereas middle and late larvae treated with 0.5 µg ml−1 DD encountered a significant delay in metamorphosis with respect to controls in which the majority of larvae had completely metamorphosed into juveniles. Indeed, one day after exposure, late larvae treated with DD did not completely metamorphose, as shown by an increase in the percentage of late larvae or larvae during tail regression to 72% with respect to 20% in controls and a concomitant decrease of juveniles to 22% with respect to 78% in controls (figure 1a). Late larvae (2–4 h post-hatching) were also treated with different concentrations of DD (0.125, 0.25, 0.5, 0.9, 1.35 µg ml−1 corresponding to 0.8, 1.6, 3.2, 5.9, 8.9 µM, respectively) and examined for the rate of metamorphosis (figure 1b). At lower concentrations, DD did not significantly affect the rate of metamorphosis, whereas at 0.5 µg ml−1, we observed a significant delay in metamorphosis at 24 h post-treatment, as assessed by the drastic reduction in the number of juveniles with respect to the control. After 3 days, 72 h post-treatment, larvae treated with 0.5 µg ml−1 DD were weakly attached to the substrate, had not completely retracted their tail, whereas head reorganization proceeded normally (figure 1c). At 0.9 µg ml−1, DD had completely blocked metamorphosis, with 97% of late larvae and only 3% of juveniles with respect to the control. At higher concentrations (1.35 µg ml−1), the effect was toxic for larvae, with DD hampering larval development and tail retraction (figure 1d).Figure 1.


The diatom-derived aldehyde decadienal affects life cycle transition in the ascidian Ciona intestinalis through nitric oxide/ERK signalling.

Castellano I, Ercolesi E, Romano G, Ianora A, Palumbo A - Open Biol (2015)

Decadienal (DD) induces a delay in metamorphosis at the time of competence. (a) Early, middle and late stage larvae were treated with 0.5 µg ml−1 DD. (b) Middle-late stage larvae were treated with different concentrations of DD (0.125, 0.25, 0.5, 0.9, 1.35 µg ml−1). After 24 h of treatment, the number of late larvae, larvae during tail regression (white bars) and juveniles (grey bars) were counted and reported as percentage of the total. Results are representative of 7 (a) and 10 (b) independent experiments. Data, expressed as means ± s.e.m., were assessed by unpaired t-test. Asterisks represent significant differences with respect to the control: **p < 0.01, ***p < 0.001. (c) Left panel shows untreated control juvenile and right panel shows abnormal juvenile after 72 h of incubation with 0.5 µg ml−1 DD. (d) Larva treated with 1.35 µg ml−1 DD after 24 h of treatment (toxic effect).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4389792&req=5

RSOB140182F1: Decadienal (DD) induces a delay in metamorphosis at the time of competence. (a) Early, middle and late stage larvae were treated with 0.5 µg ml−1 DD. (b) Middle-late stage larvae were treated with different concentrations of DD (0.125, 0.25, 0.5, 0.9, 1.35 µg ml−1). After 24 h of treatment, the number of late larvae, larvae during tail regression (white bars) and juveniles (grey bars) were counted and reported as percentage of the total. Results are representative of 7 (a) and 10 (b) independent experiments. Data, expressed as means ± s.e.m., were assessed by unpaired t-test. Asterisks represent significant differences with respect to the control: **p < 0.01, ***p < 0.001. (c) Left panel shows untreated control juvenile and right panel shows abnormal juvenile after 72 h of incubation with 0.5 µg ml−1 DD. (d) Larva treated with 1.35 µg ml−1 DD after 24 h of treatment (toxic effect).
Mentions: To investigate the effect of DD on C. intestinalis larval settlement and subsequent metamorphosis, larvae were treated at different times from hatching, corresponding to early, middle and late larval stages. Larvae were morphologically analysed after 24 h treatment. DD did not significantly affect the rate of metamorphosis when added at the early stage, whereas middle and late larvae treated with 0.5 µg ml−1 DD encountered a significant delay in metamorphosis with respect to controls in which the majority of larvae had completely metamorphosed into juveniles. Indeed, one day after exposure, late larvae treated with DD did not completely metamorphose, as shown by an increase in the percentage of late larvae or larvae during tail regression to 72% with respect to 20% in controls and a concomitant decrease of juveniles to 22% with respect to 78% in controls (figure 1a). Late larvae (2–4 h post-hatching) were also treated with different concentrations of DD (0.125, 0.25, 0.5, 0.9, 1.35 µg ml−1 corresponding to 0.8, 1.6, 3.2, 5.9, 8.9 µM, respectively) and examined for the rate of metamorphosis (figure 1b). At lower concentrations, DD did not significantly affect the rate of metamorphosis, whereas at 0.5 µg ml−1, we observed a significant delay in metamorphosis at 24 h post-treatment, as assessed by the drastic reduction in the number of juveniles with respect to the control. After 3 days, 72 h post-treatment, larvae treated with 0.5 µg ml−1 DD were weakly attached to the substrate, had not completely retracted their tail, whereas head reorganization proceeded normally (figure 1c). At 0.9 µg ml−1, DD had completely blocked metamorphosis, with 97% of late larvae and only 3% of juveniles with respect to the control. At higher concentrations (1.35 µg ml−1), the effect was toxic for larvae, with DD hampering larval development and tail retraction (figure 1d).Figure 1.

Bottom Line: PUAs, including 2,4-trans-decadienal (DD), induce deleterious effects on embryonic and larval development of several planktonic and benthic organisms.DD affects redox balance by reducing total glutathione and NO levels.By biochemical and quantitative gene expression analysis, we identify the NO-signalling network affected by DD, including the upregulation of ERK phosphatase mkp1 and consequent reduction of ERK phosphorylation, with final changes in the expression of downstream ERK target genes.

View Article: PubMed Central - PubMed

Affiliation: Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy.

ABSTRACT
Polyunsaturated aldehydes (PUAs) are fatty-acid-derived metabolites produced by some microalgae, including different diatom species. PUAs are mainly produced as a wound-activated defence mechanism against microalgal predators or released from senescent cells at the end of a bloom. PUAs, including 2,4-trans-decadienal (DD), induce deleterious effects on embryonic and larval development of several planktonic and benthic organisms. Here, we report on the effects of DD on larval development and metamorphosis of the ascidian Ciona intestinalis. Ciona larval development is regulated by the cross-talking of different molecular events, including nitric oxide (NO) production, ERK activation and caspase 3-dependent apoptosis. We report that treatment with DD at the competence larval stage results in a delay in metamorphosis. DD affects redox balance by reducing total glutathione and NO levels. By biochemical and quantitative gene expression analysis, we identify the NO-signalling network affected by DD, including the upregulation of ERK phosphatase mkp1 and consequent reduction of ERK phosphorylation, with final changes in the expression of downstream ERK target genes. Overall, these results give new insights into the molecular pathways induced in marine organisms after exposure to PUAs during larval development, demonstrating that this aldehyde affects key checkpoints of larval transition from the vegetative to the reproductive life stage.

Show MeSH
Related in: MedlinePlus