Functions of thyroid hormone signaling in regulating melanophore, iridophore, erythrophore, and pigment pattern formation in spotted scat (Scatophagus argus)
Abstract Background Spotted scat, a marine aquaculture fish, has variable body color development stages during their ontogenesis. However, the regulatory mechanism of body color patterns formation was poorly understood. Thyroid hormones (TH) function as an important endocrine factor in regulating me...
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2025-01-01
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| Online Access: | https://doi.org/10.1186/s12864-025-11286-6 |
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| author | Yongguan Liao Tong Han Dongneng Jiang Chunhua Zhu Gang Shi GuangLi Li Hongjuan Shi |
| author_facet | Yongguan Liao Tong Han Dongneng Jiang Chunhua Zhu Gang Shi GuangLi Li Hongjuan Shi |
| author_sort | Yongguan Liao |
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| description | Abstract Background Spotted scat, a marine aquaculture fish, has variable body color development stages during their ontogenesis. However, the regulatory mechanism of body color patterns formation was poorly understood. Thyroid hormones (TH) function as an important endocrine factor in regulating metamorphosis. In this study, exogenous thyroid hormones 3,5,3′-L-triiodothyronine (T3) and its inhibitor thiourea (TU) were used to treat spotted scat juveniles during the metamorphosis stage (from 60 to 90 dpf). The function and molecular mechanism of thyroid hormone signaling in regulating body color patterns formation was revealed, using the micro-observation of pigments cells distribution, colorimetric evaluation and carotenoids concentration measurement by spectrophotometry, and comparative transcriptome analysis. Results Spotted scat body color patterns consisted of whole body black color, black bar, black and red spots, and its final pattern was formed through the metamorphosis. When spotted scat were treated with the inhibitor TU to disrupt thyroid hormone signaling, the levels of T3 and T4 were significantly decreased, the melanophores numbers were significantly increased, as well as the expression of genes involved in melanin synthesis and melanophore differentiation (tyr, tyrp1, dct, mitf, pmel, oca2, slc24a5, and erbb3) was significantly increased. Besides, the expression of genes associated with carotenoids and pteridine metabolism (apod, pnpla2, rdh12, stard10, xdh, abca1, retsat, scarb1, rgs2, and gch1) and carotenoids accumulation were stimulated, when thyroid hormone signaling was disrupted by TU. On the contrary, the levels of T3 and T4 were significantly elevated in spotted scat treated with T3, which could weaken the skin redness and reduce the number of black spots and melanophores, as well as the number and diameter of larval erythrophores. Notably, unlike melanophores and erythrophores, the differentiation of iridophore was promoted by thyroid hormones, gene related to iridophore differentiation (fhl2-l, fhl2, ltk, id2a, alx4) and guanine metabolism (gmps, hprt1, ppat, impdh1b) were up-regulated after T3 treatment, but they were down-regulated after TU treatment. Conclusions Above results showed that thyroid hormone signaling might play critical roles in regulation pigments synthesis and deposition, thereby affecting pigment cells (melanophores, iridophores and erythrophores) formation and body color patterns. The mechanisms of hyperthyroid and hypothyroid on different pigment cells development were different. Excess thyroid hormone might impact the rearrangement of melanophore by regulating cell cycle, resulting in the abnormalities of black spots in spotted scat. Meanwhile, the excessed thyroid hormone could reduce the number and diameter of larval erythrophores, as well as weaken the skin redness of juvenile erythrophores, but they were enhanced by the disruption of thyroid hormone. However, the formation of iridophore differentiation and guanine synthesis genes expression were stimulated by thyroid hormones. These findings provide new insights for exploring the formation of body color patterns in fish, and help to elucidate the molecular mechanism of thyroid hormone in regulating pigment cell development and body coloration, and may also contribute to selective breeding of ornamental fish. |
| format | Article |
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| institution | Kabale University |
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| spelling | doaj-art-15dcdfd9cf98475fab629c0efcb7713e2025-02-02T12:10:04ZengBMCBMC Genomics1471-21642025-01-0126111910.1186/s12864-025-11286-6Functions of thyroid hormone signaling in regulating melanophore, iridophore, erythrophore, and pigment pattern formation in spotted scat (Scatophagus argus)Yongguan Liao0Tong Han1Dongneng Jiang2Chunhua Zhu3Gang Shi4GuangLi Li5Hongjuan Shi6Guangdong Research Center On Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Guangdong Provincial Key Laboratory of Aquatic Animal Disease Control and Healthy Culture, Fisheries College, Guangdong Ocean UniversityGuangdong Research Center On Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Guangdong Provincial Key Laboratory of Aquatic Animal Disease Control and Healthy Culture, Fisheries College, Guangdong Ocean UniversityGuangdong Research Center On Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Guangdong Provincial Key Laboratory of Aquatic Animal Disease Control and Healthy Culture, Fisheries College, Guangdong Ocean UniversityGuangdong Research Center On Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Guangdong Provincial Key Laboratory of Aquatic Animal Disease Control and Healthy Culture, Fisheries College, Guangdong Ocean UniversityGuangdong Research Center On Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Guangdong Provincial Key Laboratory of Aquatic Animal Disease Control and Healthy Culture, Fisheries College, Guangdong Ocean UniversityGuangdong Research Center On Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Guangdong Provincial Key Laboratory of Aquatic Animal Disease Control and Healthy Culture, Fisheries College, Guangdong Ocean UniversityGuangdong Research Center On Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Guangdong Provincial Key Laboratory of Aquatic Animal Disease Control and Healthy Culture, Fisheries College, Guangdong Ocean UniversityAbstract Background Spotted scat, a marine aquaculture fish, has variable body color development stages during their ontogenesis. However, the regulatory mechanism of body color patterns formation was poorly understood. Thyroid hormones (TH) function as an important endocrine factor in regulating metamorphosis. In this study, exogenous thyroid hormones 3,5,3′-L-triiodothyronine (T3) and its inhibitor thiourea (TU) were used to treat spotted scat juveniles during the metamorphosis stage (from 60 to 90 dpf). The function and molecular mechanism of thyroid hormone signaling in regulating body color patterns formation was revealed, using the micro-observation of pigments cells distribution, colorimetric evaluation and carotenoids concentration measurement by spectrophotometry, and comparative transcriptome analysis. Results Spotted scat body color patterns consisted of whole body black color, black bar, black and red spots, and its final pattern was formed through the metamorphosis. When spotted scat were treated with the inhibitor TU to disrupt thyroid hormone signaling, the levels of T3 and T4 were significantly decreased, the melanophores numbers were significantly increased, as well as the expression of genes involved in melanin synthesis and melanophore differentiation (tyr, tyrp1, dct, mitf, pmel, oca2, slc24a5, and erbb3) was significantly increased. Besides, the expression of genes associated with carotenoids and pteridine metabolism (apod, pnpla2, rdh12, stard10, xdh, abca1, retsat, scarb1, rgs2, and gch1) and carotenoids accumulation were stimulated, when thyroid hormone signaling was disrupted by TU. On the contrary, the levels of T3 and T4 were significantly elevated in spotted scat treated with T3, which could weaken the skin redness and reduce the number of black spots and melanophores, as well as the number and diameter of larval erythrophores. Notably, unlike melanophores and erythrophores, the differentiation of iridophore was promoted by thyroid hormones, gene related to iridophore differentiation (fhl2-l, fhl2, ltk, id2a, alx4) and guanine metabolism (gmps, hprt1, ppat, impdh1b) were up-regulated after T3 treatment, but they were down-regulated after TU treatment. Conclusions Above results showed that thyroid hormone signaling might play critical roles in regulation pigments synthesis and deposition, thereby affecting pigment cells (melanophores, iridophores and erythrophores) formation and body color patterns. The mechanisms of hyperthyroid and hypothyroid on different pigment cells development were different. Excess thyroid hormone might impact the rearrangement of melanophore by regulating cell cycle, resulting in the abnormalities of black spots in spotted scat. Meanwhile, the excessed thyroid hormone could reduce the number and diameter of larval erythrophores, as well as weaken the skin redness of juvenile erythrophores, but they were enhanced by the disruption of thyroid hormone. However, the formation of iridophore differentiation and guanine synthesis genes expression were stimulated by thyroid hormones. These findings provide new insights for exploring the formation of body color patterns in fish, and help to elucidate the molecular mechanism of thyroid hormone in regulating pigment cell development and body coloration, and may also contribute to selective breeding of ornamental fish.https://doi.org/10.1186/s12864-025-11286-6Spotted scatThyroid hormonesErythrophorePigment patternGene expression |
| spellingShingle | Yongguan Liao Tong Han Dongneng Jiang Chunhua Zhu Gang Shi GuangLi Li Hongjuan Shi Functions of thyroid hormone signaling in regulating melanophore, iridophore, erythrophore, and pigment pattern formation in spotted scat (Scatophagus argus) BMC Genomics Spotted scat Thyroid hormones Erythrophore Pigment pattern Gene expression |
| title | Functions of thyroid hormone signaling in regulating melanophore, iridophore, erythrophore, and pigment pattern formation in spotted scat (Scatophagus argus) |
| title_full | Functions of thyroid hormone signaling in regulating melanophore, iridophore, erythrophore, and pigment pattern formation in spotted scat (Scatophagus argus) |
| title_fullStr | Functions of thyroid hormone signaling in regulating melanophore, iridophore, erythrophore, and pigment pattern formation in spotted scat (Scatophagus argus) |
| title_full_unstemmed | Functions of thyroid hormone signaling in regulating melanophore, iridophore, erythrophore, and pigment pattern formation in spotted scat (Scatophagus argus) |
| title_short | Functions of thyroid hormone signaling in regulating melanophore, iridophore, erythrophore, and pigment pattern formation in spotted scat (Scatophagus argus) |
| title_sort | functions of thyroid hormone signaling in regulating melanophore iridophore erythrophore and pigment pattern formation in spotted scat scatophagus argus |
| topic | Spotted scat Thyroid hormones Erythrophore Pigment pattern Gene expression |
| url | https://doi.org/10.1186/s12864-025-11286-6 |
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