A microarray-based transcriptomic time-course of hyper- and hypo-osmotic stress signaling events in the euryhaline fish<i>Gillichthys mirabilis</i>:osmosensors to effectors

Evans, Tyler G.; Somero, George N.

doi:10.1242/jeb.022160

Cited by 101 publications

(125 citation statements)

References 91 publications

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“…Comparatively little is known about the mechanisms comprising the immediate-early responses of cells to osmotic stress relative to the mechanisms of downstream effectors of osmotic acclimation (43,44). However, immediate-early transcriptional responses are highly correlated with the pattern of population variation in transcriptional trajectories during acclimation (Fig.…”

Section: Resultsmentioning

confidence: 99%

Genomic mechanisms of evolved physiological plasticity in killifish distributed along an environmental salinity gradient

Whitehead

Roach

Zhang

et al. 2011

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

195

224

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Adaptive variation tends to emerge clinally along environmental gradients or discretely among habitats with limited connectivity. However, in Atlantic killifish (Fundulus heteroclitus), a population genetic discontinuity appears in the absence of obvious barriers to gene flow along parallel salinity clines and coincides with a physiologically stressful salinity. We show that populations resident on either side of this discontinuity differ in their abilities to compensate for osmotic shock and illustrate the physiological and functional genomic basis of population variation in hypoosmotic tolerance. A population native to a freshwater habitat, upstream of the genetic discontinuity, exhibits tolerance to extreme hypoosmotic challenge, whereas populations native to brackish or marine habitats downstream of the discontinuity lose osmotic homeostasis more severely and take longer to recover. Comparative transcriptomics reveals a core transcriptional response associated with acute and acclimatory responses to hypoosmotic shock and posits unique mechanisms that enable extreme osmotic tolerance. Of the genes that vary in expression among populations, those that are putatively involved in physiological acclimation are more likely to exhibit nonneutral patterns of divergence between freshwater and brackish populations. It is not the well-known effectors of osmotic acclimation, but rather the lesser-known immediateearly responses, that appear important in contributing to population differences.adaptive acclimation | ecological genomics | microarray A tlantic killifish (Fundulus heteroclitus) occupy an extremely wide osmotic niche from freshwater to marine, and populations are distributed along steep salinity gradients in Atlantic coast estuaries. In the Chesapeake Bay, salinity gradients are distributed across hundreds of kilometers, although no obvious barriers to gene flow exist across this continuum of osmotic habitats. Because salinity is arguably the most important single physical environmental variable that delimits aquatic species distributions in nature (including Fundulus species; ref. 1), we exploit F. heteroclitus distributed along Chesapeake Bay salinity gradients as a model to discover genes and pathways that enable extreme physiological plasticity and to explore the physiological and functional genomic basis of adaptive microevolution in alternative osmotic environments.Results and Discussion Population Genetic Divergence. We characterized the genetic structure of killifish distributed along two parallel salinity gradients in Chesapeake Bay: one along the Potomac River and the other along the James River (Fig. 1A). Steep clines in allele frequency for both mitochondrial and nuclear markers were centered at nearly identical salinities along the parallel gradients (Fig. 1B). Genotype frequency clines bounded the tidal freshwater transition region (<0.5 ppt) of both rivers, where sites upstream are freshwater year-round according to 20 y of data logged from fixed monitoring stations (www.chesapeakebay.net/ data_...

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Section: Resultsmentioning

confidence: 99%

Genomic mechanisms of evolved physiological plasticity in killifish distributed along an environmental salinity gradient

Whitehead

Roach

Zhang

et al. 2011

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

195

224

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“…The MIB pathway utilizes two enzymes, myo-inositol phosphate synthase (MIPS) and inositol monophosphatase (IMPA), to generate myo-inositol endogenously from glucose-6-phosphate (G-6-P) in a two-step reaction (Geiger and Jin, 2006). The study by Fiol et al (Fiol et al, 2006b) was the first to identify upregulation of MIPS mRNA in response to acute hyperosmotic challenge in tilapia gill, and since then, several studies have confirmed induction of the MIB pathway in other euryhaline species exposed to salinity challenge (Evans and Somero, 2008;Kalujnaia et al, 2009;Kalujnaia et al, 2010;Kalujnaia et al, 2013). In mammals, IMPA has at least two isoforms, originating from different genes (Ohnishi et al, 2007;Shamir et al, 2001), while MIPS can have alternative splice variants (Seelan et al, 2009) derived from the same gene.…”

Section: Introductionmentioning

confidence: 99%

Tilapia (Oreochromis mossambicus) brain cells respond to hyperosmotic challenge by inducingmyo-inositol biosynthesis

Gardell

Yang

Sacchi

et al. 2013

Journal of Experimental Biology

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SUMMARYThis study aimed to determine the regulation of the de novo myo-inositol biosynthetic (MIB) pathway in Mozambique tilapia (Oreochromis mossambicus) brain following acute (25 ppt) and chronic (30, 60 and 90 ppt) salinity acclimations. The MIB pathway plays an important role in accumulating the compatible osmolyte, myo-inositol, in cells in response to hyperosmotic challenge and consists of two enzymes, myo-inositol phosphate synthase and inositol monophosphatase. In tilapia brain, MIB enzyme transcriptional regulation was found to robustly increase in a time (acute acclimation) or dose (chronic acclimation) dependent manner. Blood plasma osmolality and Na + and Cl -concentrations were also measured and significantly increased in response to both acute and chronic salinity challenges. Interestingly, highly significant positive correlations were found between MIB enzyme mRNA and blood plasma osmolality in both acute and chronic salinity acclimations. Additionally, a mass spectrometry assay was established and used to quantify total myo-inositol concentration in tilapia brain, which closely mirrored the hyperosmotic MIB pathway induction. Thus, myo-inositol is a major compatible osmolyte that is accumulated in brain cells when exposed to acute and chronic hyperosmotic challenge. These data show that the MIB pathway is highly induced in response to environmental salinity challenge in tilapia brain and that this induction is likely prompted by increases in blood plasma osmolality. Because the MIB pathway uses glucose-6-phosphate as a substrate and large amounts of myo-inositol are being synthesized, our data also illustrate that the MIB pathway likely contributes to the high energetic demand posed by salinity challenge.

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“…Induction of these two genes is also evident in other euryhaline fish exposed to acute salinity stress. For instance, elevated salinity increases MIPS abundance in O. niloticus and Anguilla anguilla (52) and IMPA1.1 abundance in Gillichthys mirabilis and A. anguilla (53)(54)(55)(56). The MIB pathway promotes the accumulation of high concentrations of the compatible osmolyte myo-inositol, which protects cells from salinity-induced damage (44,48,57).…”

Section: Discussionmentioning

confidence: 99%

Osmolality/salinity-responsive enhancers (OSREs) control induction of osmoprotective genes in euryhaline fish

Wang

Kültz

2017

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

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Fish respond to salinity stress by transcriptional induction of many genes, but the mechanism of their osmotic regulation is unknown. We developed a reporter assay using cells derived from the brain of the tilapia Oreochromis mossambicus (OmB cells) to identify osmolality/salinity-responsive enhancers (OSREs) in the genes of O. mossambicus. Genomic DNA comprising the regulatory regions of two strongly salinity-induced genes, inositol monophosphatase 1 (IMPA1.1) and myo-inositol phosphate synthase (MIPS), was isolated and analyzed with dual luciferase enhancer trap reporter assays. We identified five sequences (two in IMPA1.1 and three in MIPS) that share a common consensus element (DDKGGAAWWDWWYDNRB), which we named "OSRE1." Additional OSREs that were less effective in conferring salinity-induced trans-activation and do not match the OSRE1 consensus also were identified in both MIPS and IMPA1.1. Although OSRE1 shares homology with the mammalian osmotic-response element/tonicity-responsive enhancer (ORE/TonE) enhancer, the latter is insufficient to confer osmotic induction in fish. Like other enhancers, OSRE1 trans-activates genes independent of orientation. We conclude that OSRE1 is a cis-regulatory element (CRE) that enhances the hyperosmotic induction of osmoregulated genes in fish. Our study also shows that tailored reporter assays developed for OmB cells facilitate the identification of CREs in fish genomes. Knowledge of the OSRE1 motif allows affinity-purification of the corresponding transcription factor and computational approaches for enhancer screening of fish genomes. Moreover, our study enables targeted inactivation of OSRE1 enhancers, a method superior to gene knockout for functional characterization because it confines impairment of gene function to a specific context (salinity stress) and eliminates pitfalls of constitutive gene knockouts (embryonic lethality, developmental compensation). biochemical evolution | compatible osmolytes | osmotic stress signaling | enhancer | CRE

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A microarray-based transcriptomic time-course of hyper- and hypo-osmotic stress signaling events in the euryhaline fishGillichthys mirabilis:osmosensors to effectors

Cited by 101 publications

References 91 publications

Genomic mechanisms of evolved physiological plasticity in killifish distributed along an environmental salinity gradient

Genomic mechanisms of evolved physiological plasticity in killifish distributed along an environmental salinity gradient

Tilapia (Oreochromis mossambicus) brain cells respond to hyperosmotic challenge by inducingmyo-inositol biosynthesis

Osmolality/salinity-responsive enhancers (OSREs) control induction of osmoprotective genes in euryhaline fish

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