Gene Expression Patterns during the Early Stages of Chemically Induced Larval Metamorphosis and Settlement of the Coral Acropora millepora

Siboni, Nachshon; Abrego, David; Motti, Cherie A.; Tebben, Jan; Harder, Tilmann

doi:10.1371/journal.pone.0091082

Cited by 22 publications

(22 citation statements)

References 26 publications

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“…) and during metamorphosis of coral larvae (Siboni et al . ). While analysing network interactions of c‐fos‐like and c‐jun, which together compose the primary activating form of AP1 (Eferl & Wagner ) and Egr1 on the background of Hg‐up‐regulated transcripts, the involvement of additional early response genes was revealed, including SRF that may activate c‐fos‐like and Egr1 genes by binding, together with Elk1, to their SREs (Thiel & Cibelli ; O'Donnell et al .…”

Section: Discussionmentioning

confidence: 97%

Early and late response of Nematostella vectensis transcriptome to heavy metals

et al. 2014

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Environmental contamination from heavy metals poses a global concern for the marine environment, as heavy metals are passed up the food chain and persist in the environment long after the pollution source is contained. Cnidarians play an important role in shaping marine ecosystems, but environmental pollution profoundly affects their vitality. Among the cnidarians, the sea anemone Nematostella vectensis is an advantageous model for addressing questions in molecular ecology and toxicology as it tolerates extreme environments and its genome has been published. Here, we employed a transcriptome-wide RNA-Seq approach to analyse N. vectensis molecular defence mechanisms against four heavy metals: Hg, Cu, Cd and Zn. Altogether, more than 4800 transcripts showed significant changes in gene expression. Hg had the greatest impact on up-regulating transcripts, followed by Cu, Zn and Cd. We identified, for the first time in Cnidaria, co-up-regulation of immediate-early transcription factors such as Egr1, AP1 and NF-κB. Time-course analysis of these genes revealed their early expression as rapidly as one hour after exposure to heavy metals, suggesting that they may complement or substitute for the roles of the metal-mediating Mtf1 transcription factor. We further characterized the regulation of a large array of stress-response gene families, including Hsp, ABC, CYP members and phytochelatin synthase, that may regulate synthesis of the metal-binding phytochelatins instead of the metallothioneins that are absent from Cnidaria genome. This study provides mechanistic insight into heavy metal toxicity in N. vectensis and sheds light on ancestral stress adaptations.

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Section: Discussionmentioning

confidence: 97%

Early and late response of Nematostella vectensis transcriptome to heavy metals

et al. 2014

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“…Alternatively, VWF domain-containing genes could be involved in cell adhesion during tissue remodeling (51). Hydroides larvae up-regulated MAPK signaling genes, which were previously implicated in modulating metamorphosis of other marine organisms including corals (28), ascidians (30), and barnacles (31). The transcriptional signature of metamorphosis in Hydroides therefore parallels developmental processes identified in other animal species.…”

Section: Discussionmentioning

confidence: 66%

“…Hydroides up-regulated SPI-encoding genes, which have potent bactericidal activity implicated in host innate immunity in Hydra (49) and black tiger shrimp (50). Similar differential expression of immunity genes during metamorphosis was observed in corals (25,28) and ascidians (14,27,61). VWF domain-encoding genes were up-regulated and might be important for tube building.…”

Section: Discussionmentioning

confidence: 74%

“…These systems include hormones (16)(17)(18), neurotransmitters (19)(20)(21), and nitric oxide (22)(23)(24). Additionally, diverse animals regulate metamorphosis at the transcriptional and posttranslational levels, such as differential expression of metamorphosis-associated genes (25)(26)(27) and MAPK signaling (28)(29)(30)(31), respectively. Although a number of signaling systems and regulatory networks orchestrate metamorphosis in animals from diverse taxa, comparatively little is known about how bacteria stimulate these systems and networks.…”

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confidence: 99%

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Stepwise metamorphosis of the tubeworm Hydroides elegans is mediated by a bacterial inducer and MAPK signaling

Shikuma

Antoshechkin

Medeiros

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Diverse animal taxa metamorphose between larval and juvenile phases in response to bacteria. Although bacteria-induced metamorphosis is widespread among metazoans, little is known about the molecular changes that occur in the animal upon stimulation by bacteria. Larvae of the tubeworm Hydroides elegans metamorphose in response to surface-bound Pseudoalteromonas luteoviolacea bacteria, producing ordered arrays of phage tail-like metamorphosis-associated contractile structures (MACs). Sequencing the Hydroides genome and transcripts during five developmental stages revealed that MACs induce the regulation of groups of genes important for tissue remodeling, innate immunity, and mitogen-activated protein kinase (MAPK) signaling. Using two MAC mutations that block P. luteoviolacea from inducing settlement or metamorphosis and three MAPK inhibitors, we established a sequence of bacteria-induced metamorphic events: MACs induce larval settlement; then, particular properties of MACs encoded by a specific locus in P. luteoviolacea initiate cilia loss and activate metamorphosis-associated transcription; finally, signaling through p38 and c-Jun N-terminal kinase (JNK) MAPK pathways alters gene expression and leads to morphological changes upon initiation of metamorphosis. Our results reveal that the intricate interaction between Hydroides and P. luteoviolacea can be dissected using genomic, genetic, and pharmacological tools. Hydroides' dependency on bacteria for metamorphosis highlights the importance of external stimuli to orchestrate animal development. The conservation of Hydroides genome content with distantly related deuterostomes (urchins, sea squirts, and humans) suggests that mechanisms of bacteria-induced metamorphosis in Hydroides may have conserved features in diverse animals. As a major biofouling agent, insight into the triggers of Hydroides metamorphosis might lead to practical strategies for fouling control.genome | phage | symbiosis | biofouling | development

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“…Among our findings, we have identified rapid activation of several immediate-early response genes such as the transcription factors early growth response1 ( egr1 ) and fos . Furthermore, fos transcript was shown to be up-regulated by injury in Nematostella [26], during head regeneration in Hydra and during metamorphosis of coral larvae [27-29]. …”

Section: Introductionmentioning

confidence: 99%

Regulation of AP-1 by MAPK Signaling in Metal-Stressed Sea Anemone

Agron

Brekhman

Morgenstern

et al. 2017

Cell Physiol Biochem

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Background/Aims: AP-1 transcription factor plays a conserved role in the immediate response to stress. Activation of AP-1 members jun and fos is mediated by complex signaling cascades to control cell proliferation and survival. To understand the evolution of this broadly-shared pathway, we studied AP-1 regulation by MAPK signaling in a basal metazoan. Methods: Metal- stressed cnidarian Nematostella vectensis anemones were tested with kinase inhibitors and analyzed for gene expression levels and protein phosphorylation. Results: We show that in cnidarian, AP-1 is regulated differently than in bilaterian models. ERK2 and ERK5, the main MAPK drivers of AP-1 activation in Bilateria, down-regulated fos1 and jun1 transcription in anemones exposed to metal stress, whereas p38 MAPK, triggered transcription of jun1 but not fos1. Furthermore, our results reveal that GSK3-β is the main driver of the immediate stress response in Nematostella. GSK3-β triggered transcription of AP-1 and two other stress-related genes, egr1 and hsp70. Finally, phylogenetic analysis and protein characterization show that while MAPKs and GSK3-β are evolutionarily conserved, Fos and Jun proteins in Nematostella and other cnidarians lack important regulatory and phosphorylation sites found in Bilateria. Conclusion: These findings reveal alternative network interactions of conserved signaling kinases, providing insight into the evolutionary plasticity of immediate stress response mechanisms.

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Gene Expression Patterns during the Early Stages of Chemically Induced Larval Metamorphosis and Settlement of the Coral Acropora millepora

Cited by 22 publications

References 26 publications

Early and late response of Nematostella vectensis transcriptome to heavy metals

Early and late response of Nematostella vectensis transcriptome to heavy metals

Stepwise metamorphosis of the tubeworm Hydroides elegans is mediated by a bacterial inducer and MAPK signaling

Regulation of AP-1 by MAPK Signaling in Metal-Stressed Sea Anemone

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