The Olfactory Transcriptome and Progression of Sexual Maturation in Homing Chum Salmon Oncorhynchus keta

Palstra, Arjan P.; Fukaya, Kosuke; Chiba, Hiroaki; Dirks, Ron P.; Planas, Josep V.; Ueda, Hiroshi

doi:10.1371/journal.pone.0137404

Cited by 18 publications

(13 citation statements)

References 40 publications

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“…Furthermore, they analyzed soig mRNA levels but found no difference between life stages. Palstra et al () compared by RNAseq expression profiles of 75 known and 27 unknown olfactory genes in coastal adult chum salmon with prespawning individuals caught 75 km upstream in the river. Seven MOR genes, n24 , asor , and two ependymin ‐ like genes were significantly upregulated (1.5–2.5×), and olfc13.1 and O51F2 HUMAN —a novel salmonid gene—were downregulated (0.7–0.5×) in prespawning individuals.…”

Section: Discussionmentioning

confidence: 99%

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Differential expression of olfactory genes in Atlantic salmon (Salmo salar) during the parr–smolt transformation

Madsen

Winther

Bollinger

et al. 2019

Ecology and Evolution

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The anadromous salmon life cycle includes two migratory events, downstream smolt migration and adult homing migration, during which they must navigate with high precision. During homing migration, olfactory cues are used for navigation in coastal and freshwater areas, and studies have suggested that the parr–smolt transformation has a sensitive period for imprinting. Accordingly, we hypothesized that there would be significant changes in gene expression in the olfactory epithelium specifically related to smoltification and sampled olfactory rosettes from hatchery‐reared upper growth modal juvenile Atlantic salmon at 3‐week intervals from January to June, using lower growth modal nonsmolting siblings as controls. A suite of olfactory receptors and receptor‐specific proteins involved in functional aspects of olfaction and peripheral odor memorization was analyzed by qPCR. Gene expression in juveniles was compared with mature adult salmon of the same genetic strain caught in the river Gudenaa. All mRNAs displayed significant variation over time in both modal groups. Furthermore, five receptor genes (olfc13.1, olfc15.1, sorb, ora2, and asor1) and four olfactory‐specific genes (soig, ependymin, gst, and omp2) were differentially regulated between modal groups, suggesting altered olfactory function during smoltification. Several genes were differentially regulated in mature salmon compared with juveniles, suggesting that homing and odor recollection involve a different set of genes than during imprinting. Thyroid hormone receptors thrα and thrβ mRNAs were elevated during smolting, suggesting increased sensitivity to thyroid hormones. Treatment of presmolts with triiodothyronine in vivo and ex vivo had, however, only subtle effects on the investigated olfactory targets, questioning the hypothesis that thyroid hormones directly regulate gene expression in the olfactory epithelium.

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Section: Discussionmentioning

confidence: 99%

“…analyzed soig mRNA levels but found no difference between life stages Palstra et al (2015). compared by RNAseq expression profiles of 75 known and 27 unknown olfactory genes in coastal adult chum salmon with prespawning individuals caught 75 km upstream in the river.…”

mentioning

confidence: 99%

Differential expression of olfactory genes in Atlantic salmon (Salmo salar) during the parr–smolt transformation

Madsen

Winther

Bollinger

et al. 2019

Ecology and Evolution

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“…Validation using RT-qPCR on the same RNA samples as assayed in the RNA-seq analysis only validates the technology, it does not validate the conclusion about the treatments or conditions ( Fang and Cui, 2011 ). Moreover, RNAseq represents a high-throughput transcriptomic approach, specifically useful when analysing on the level of physiological processes (e.g., Palstra et al, 2015 ; Rurangwa et al, 2015 ) which was also the main aim of this study. This paper is aimed to be a first step toward a project on the immune modulating effects of seaweeds in which this study can be followed up by dedicated RT-qPCR studies to validate the results obtained on a new and larger set of samples.…”

Section: Discussionmentioning

confidence: 99%

Immunomodulatory Effects of Dietary Seaweeds in LPS Challenged Atlantic Salmon Salmo salar as Determined by Deep RNA Sequencing of the Head Kidney Transcriptome

et al. 2018

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Seaweeds may represent immuno-stimulants that could be used as health-promoting fish feed components. This study was performed to gain insights into the immunomodulatory effects of dietary seaweeds in Atlantic salmon. Specifically tested were 10% inclusion levels of Laminaria digitata (SW1) and a commercial blend of seaweeds (Oceanfeed®) (SW2) against a fishmeal based control diet (FMC). Differences between groups were assessed in growth, feed conversion ratio and blood parameters hematocrit and hemoglobin. After a LPS challenge of fish representing each of the three groups, RNAseq was performed on the head kidney as major immune organ to determine transcriptomic differences in response to the immune activation. Atlantic salmon fed with dietary seaweeds did not show major differences in performance in comparison with fishmeal fed fish. RNAseq resulted in ∼154 million reads which were mapped against a NCBI Salmo salar reference and against a de novo assembled S. salar reference for analyses of expression of immune genes and ontology of immune processes among the 87,600 cDNA contigs. The dietary seaweeds provoked a more efficient immune response which involved more efficient identification of the infection site, and processing and presentation of antigens. More specifically, chemotaxis and the chemokine-mediated signaling were improved and therewith the defense response to Gram-positive bacterium reduced. Specific Laminaria digitata effects included reduction of the interferon-gamma-mediated signaling. Highly upregulated and specific for this diet was the expression of major histocompatibility complex class I-related gene protein. The commercial blend of seaweeds caused more differential expression than Laminaria digitata and improved immune processes such as receptor-mediated endocytosis and cell adhesion, and increased the expression of genes involved in response to lipopolysaccharide and inflammatory response. Particularly, expression of many important immune receptors was up-regulated illustrating increased responsiveness. NF-kappa-B inhibitor alpha is an important gene that marked the difference between both seaweed diets as Laminaria digitata inhibits the expression for this cytokine while the blend of seaweeds stimulates it. It can be concluded that the inclusion of seaweeds such as Laminaria digitata can have important modulatory effects on the immune capacity of Atlantic salmon resulting in a more efficient immune response.

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“…Faster migration can be accomplished by more directed movements, which could be afforded by a higher sensitivity to imprinted natal odours. Portage Creek sockeye salmon are more mature than salmon from Gates Creek when they pass through the Seton River (Middleton et al, ), and maturation level is linked to olfactory homing (Palstra et al, ). It is possible that their more advance state of maturity may improve their ability to discriminate imprinted odours (Ueda et al, ).…”

Section: Discussionmentioning

confidence: 99%

Effects of natal water dilution on the migration of Pacific salmon in a regulated river

Bett

Hinch

Casselman

2018

River Research & Apps

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Adult salmon are guided by chemical cues from their natal water during the spawning migration. Consequently, hydroelectric activities can have negative effects on adult salmon navigation if they alter the chemical properties of the homing environment.We conducted riverside experiments to examine the effects of natal water dilution resulting from hydroelectric operations on upstream navigation in a British Columbia river and the efficacy of current dilution management in providing clear migratory cues for two local populations of sockeye salmon (Oncorhynchus nerka) and a population of pink salmon (Oncorhynchus gorbuscha). We found that both sockeye populations exhibited behavioural preferences for pure natal water when compared with various levels of diluted natal water, whereas pink salmon, which spawn throughout the system and exhibit lower levels of natal site fidelity, appeared unaffected by natal water dilution. Our findings confirmed that current management operations were appropriate for ensuring timely migration to spawning grounds and highlight the potential effects of alterations to water odour properties on salmon migrations.

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The Olfactory Transcriptome and Progression of Sexual Maturation in Homing Chum Salmon Oncorhynchus keta

Cited by 18 publications

References 40 publications

Differential expression of olfactory genes in Atlantic salmon (Salmo salar) during the parr–smolt transformation

Differential expression of olfactory genes in Atlantic salmon (Salmo salar) during the parr–smolt transformation

Immunomodulatory Effects of Dietary Seaweeds in LPS Challenged Atlantic Salmon Salmo salar as Determined by Deep RNA Sequencing of the Head Kidney Transcriptome

Effects of natal water dilution on the migration of Pacific salmon in a regulated river

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