Role of Halloween genes in ecdysteroids biosynthesis of the swimming crab (Portunus trituberculatus): Implications from RNA interference and eyestalk ablation

Xie, Xuewen; Liu, Zhiye; Liu, Mingxin; Tian, Tao; Shen, Xianhua; Zhu, Dongfa

doi:10.1016/j.cbpa.2016.06.001

Cited by 27 publications

(16 citation statements)

References 33 publications

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“…Expression of these genes was observed in other tissues such as the EG, thoracic ganglia complex, brain, and ovary. A similar pattern has been observed in P. trituberculatus [26], but further study of the localization and translation of mRNAs in these tissues is needed. Neverland and Spook have been identified in ovarian cells in other species such as the salmon louse, Lepoeophtheirus salmonis [64], the water flea, D. magna [65], the acari, Ornithodoros moubata [66], the mosquito, Anopheles gambiae [67], and the fruit fly, Drosophila melanogaster [68].…”

Section: Plos Onesupporting

confidence: 64%

“…Most Halloween genes are found among other arthropod species. For example, the water flea, Daphnia pulex has orthologs of all 5 of these genes [25] while four (cytochrome P450 (CYP), 307A1 (spook), CYP315A (shadow), and CYP306A1 (phantom)) are found in the swimming crab, Portunus terituberculatus [26] and the kuruma prawn, Marsupenaeus japonicus [6]. However, while spook and spookier have been detected in arthropods, potentially involved in the second step of the Ecd synthesis (transformation of 7-dehydrocholesterol (7dC) to Δ4-Diketol and Diketol), only a spook homolog has been identified in crustaceans [27].…”

Section: Introductionmentioning

confidence: 99%

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Understanding molt control switches: Transcriptomic and expression analysis of the genes involved in ecdysteroidogenesis and cholesterol uptake pathways in the Y-organ of the blue crab, Callinectes sapidus

et al. 2021

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The crustacean molting process is regulated by an interplay of hormones produced by the eyestalk ganglia and Y-organs (YO). Molt-inhibiting hormone and crustacean hyperglycemic hormone released by the sinus gland of the eyestalk ganglia (EG) inhibit the synthesis and secretion of ecdysteroid by the YO, hence regulating hemolymph levels during the molt cycle. The purpose of this study is to investigate the ecdysteroidogenesis pathway, specifically genes linked to changes in ecdysteroid levels occurring at early premolt (ePM). To this end, a reference transcriptome based on YO, EG, and hepatopancreas was de novo assembled. Two genes (cholesterol 7-desaturase Neverland and cytochrome p450 307a1-like Spook) involved in ecdysteroidogenesis were identified from the YO transcriptome using sequence comparisons and transcript abundance. Two other candidates, Hormone receptor 4 and probable cytochrome p450 49a1 potentially involved in ecdysteroidogenesis were also identified. Since cholesterol is the ecdysteroid precursor, a putative cholesterol carrier (Apolipoprotein D-like) was also examined to understand if cholesterol uptake coincided with the increase in the ecdysteroid levels at the ePM stage. The expression level changes of the five candidate genes in the YO were compared between intermolt (IM) and induced ePM (iePM) stages using transcriptomic analysis. Expression analysis using qPCR were carried out at IM, iePM, and normal ePM. The increase in Spook and Neverland expression in the YO at the ePM was accompanied by a concomitant rise in ecdysteroid levels. The data obtained from iePM stage were congruent with those obtained from the normal ePM stage of intact control animals. The present findings support the role of Halloween genes in the ecdysteroidogenesis and molt cycle in the blue crab, Callinectes sapidus.

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Section: Plos Onesupporting

confidence: 64%

Section: Introductionmentioning

confidence: 99%

Understanding molt control switches: Transcriptomic and expression analysis of the genes involved in ecdysteroidogenesis and cholesterol uptake pathways in the Y-organ of the blue crab, Callinectes sapidus

et al. 2021

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“…Interestingly, transcript levels of the spook gene, a class 1 monooxygenase involved in diketol synthesis from cholesterol, increased 25- to 35-fold relative to the other ecdysteroid pathway enzymes following entry into early premolt. qPCR studies in the swimming crab, Portunus trituberculatus , did not report an increase in spo transcripts on entering premolt 68 . In insects, however, a homolog of this gene, spookier , is subject to transcriptional up-regulation by the zinc finger transcription factor Ouija board ( ouib ), which is principally expressed in the ecdysteroidogenic prothoracic gland 69 , 70 .…”

Section: Discussionmentioning

confidence: 93%

Transcriptomic analysis of crustacean molting gland (Y-organ) regulation via the mTOR signaling pathway

Shyamal

Das

Guruacharya

et al. 2018

Sci Rep

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The intermolt crustacean Y-organ (YO) maintains a basal state mediated by pulsatile release of molt inhibiting hormone (MIH), a neuropeptide produced in the eyestalk ganglia, inhibiting YO ecdysteroidogenesis. Reduction of MIH results in YO activation and the animal enters premolt. In the crab, Gecarcinus lateralis, molting was induced by eyestalk ablation (ESA). ESA animals were injected with either rapamycin, an mTOR inhibitor, or DMSO vehicle at Day 0. YOs were harvested at 1, 3, and 7 days post-ESA and processed for high throughput RNA sequencing. ESA-induced increases in mRNA levels of mTOR signaling genes (e.g., mTOR, Rheb, TSC1/2, Raptor, Akt, and S6 kinase) declined following rapamycin treatment. In concert with mTOR inhibition, mRNA levels of ecdysteroid biosynthesis genes (e.g., Nvd, Spo, Sad, Dib, and Phm) were decreased and accompanied by a decrease in hemolymph ecdysteroid titer. By contrast, rapamycin increased the mRNA level of FKBP12, the rapamycin-binding protein, as well as the mRNA levels of genes associated with Wnt and insulin-like growth factor signaling pathways. Many MIH and transforming growth factor-β signaling genes were down regulated in ESA animals. These results indicate that mTOR activity either directly or indirectly controls transcription of genes that drive activation of the YO.

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“…They were called "Halloween Family Gene" and play significant role in the synthesis of ecdysone (Nusslein-Volhard, 1980). In crustaceans, Xie et al (2016) successfully cloned the disembodied (dib), spook (spo), and shadow (sad) genes from Portunus trituberculatus (Liu et al, 2015), and Chang and O'Connor (1977) found that the expression level of these genes in Y-organ was significantly higher than that of other tissues, which was consistent with the conclusion that the Y-organ is the primary secretory organ of crustacean synthetic ecdysone.…”

Section: Function Analysis Overview and Analysis Of Main Metabolic Pamentioning

confidence: 99%

Reconstruction of Eriocheir sinensis Y-organ Genome-Scale Metabolic Network and Differential Analysis After Eyestalk Ablation

et al. 2020

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Genome-scale metabolic network (GSMN) has been proven to be a useful tool for the system analysis of organism metabolism and applied to deeply explore the metabolic functions or mechanisms in many organisms, including model or non-model organisms. However, the systematic studies on the metabolisms of aquatic animals are seldom reported, especially the aquatic crustaceans. In this work, we reconstructed an Eriocheir sinensis Y-organ GSMN based on the transcriptome sequencing of Y-organ, which includes 1,645 reactions, 1,885 unigenes, and 1,524 metabolites distributed in 100 pathways and 11 subsystems. Functional module and centrality analysis of the GSMN show the main metabolic functions of Y-organ. Further analysis of the differentially expressed unigenes in Y-organ after eyestalk ablation reveals that 191 genes in the network were up-regulated and 283 were down-regulated. The unigenes associated with the ecdysone synthetic pathway were all up-regulated, which is consistent with the report on the increasing secretion of ecdysone after eyestalk ablation. Besides, we compared the Y-organ GSMN with that of E. sinensis eyestalk and hepatopancreas, and we analyzed the specific metabolisms in each organ. The specific metabolisms and pathways of these three networks are closely related to their corresponding metabolic functions. The GSMN reconstructed in this work provides a new method and many novel clues for further understanding the physiological function of Y-organ. It also supplies a new platform for the investigation of the interactions among different organs in the growth process of E. sinensis.

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Role of Halloween genes in ecdysteroids biosynthesis of the swimming crab (Portunus trituberculatus): Implications from RNA interference and eyestalk ablation

Cited by 27 publications

References 33 publications

Understanding molt control switches: Transcriptomic and expression analysis of the genes involved in ecdysteroidogenesis and cholesterol uptake pathways in the Y-organ of the blue crab, Callinectes sapidus

Understanding molt control switches: Transcriptomic and expression analysis of the genes involved in ecdysteroidogenesis and cholesterol uptake pathways in the Y-organ of the blue crab, Callinectes sapidus

Transcriptomic analysis of crustacean molting gland (Y-organ) regulation via the mTOR signaling pathway

Reconstruction of Eriocheir sinensis Y-organ Genome-Scale Metabolic Network and Differential Analysis After Eyestalk Ablation

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