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Transcriptomics reveals the molecular processes of light-induced rapid darkening of the non-obligate cave dweller Oreolalax rhodostigmatus (Megophryidae, Anura) and their genetic basis of pigmentation strategy.

ABSTRACT: BACKGROUND:Vertebrates use different pigmentation strategies to adapt to various environments. A large amount of research has been done on disclosing the mechanisms of pigmentation strategies in vertebrates either under light, or, living in constant darkness. However, less attention has been paid to non-obligate, darkness dwellers. Red-spotted toothed toads Oreolalax rhodostigmatus (Megophryidae; Anura) from the karst mountainous region of southwestern China are non-obligate cave dwellers. Most tadpoles of the species possess transparent skin as they inhabit the dark karst caves. But remarkably, the transparent tadpoles can darken just within 15 h once exposed to light. Obviously, it is very significant to reveal molecular mechanisms of the unexpected rapid-darkening phenomenon. RESULTS:We compared the transcriptomes of O. rhodostigmatus tadpoles with different durations of light exposure to investigate the cellular processes and potential regulation signals for their light-induced rapid darkening. Genes involved in melanogenesis (i.e. TYR, TYRP1 and DCT) and melanocyte proliferation, as well as their transcriptional factor (MITF), showed light-induced transcription, suggesting a dominating role of morphological color change (MCC) in this process. Transcription of genes related to growth factor, MAPK and PI3K-Akt pathways increased with time of light exposure, suggesting that light could induce significant growth signal, which might facilitate the rapid skin darkening. Most importantly, an in-frame deletion of four residues was identified in O. rhodostigmatus melanocortin-1 receptor (MC1R), a critical receptor in MCC. This deletion results in a more negatively charged ligand pocket with three stereo-tandem aspartate residues. Such structural changes likely decrease the constitutive activity of MC1R, but increase its ligands-dependent activity, thus coordinating pigment regression and rapid melanogenesis in the dark and light, respectively. CONCLUSION:Our study suggested that rapid MCC was responsible for the light-induced rapid darkening of O. rhodostigmatus tadpoles. Genetic mutations of MC1R in them could explain how these non-obligate cave dwellers coordinate pigment regression and robust melanogenesis in darkness and light, respectively. To our knowledge, this is the first study that reports the association between pigmentation phenotype adaptation and MC1R mutations in amphibians and/or in non-obligate cave dwellers.

SUBMITTER: Zhu W

PROVIDER: S-EPMC5984452 | biostudies-literature | 2018 May

REPOSITORIES: biostudies-literature

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Transcriptomics reveals the molecular processes of light-induced rapid darkening of the non-obligate cave dweller Oreolalax rhodostigmatus (Megophryidae, Anura) and their genetic basis of pigmentation strategy.

Zhu Wei W Liu Lusha L Wang Xungang X Gao Xinyu X Jiang Jianping J Wang Bin B

BMC genomics 20180531 1

<h4>Background</h4>Vertebrates use different pigmentation strategies to adapt to various environments. A large amount of research has been done on disclosing the mechanisms of pigmentation strategies in vertebrates either under light, or, living in constant darkness. However, less attention has been paid to non-obligate, darkness dwellers. Red-spotted toothed toads Oreolalax rhodostigmatus (Megophryidae; Anura) from the karst mountainous region of southwestern China are non-obligate cave dweller ...[more]

PMID: 29855256

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Project description:O. rhodostigmatus are non-obligative cave dwellers, whose tadpoles keep albinistic phenotype in caves but rapidly darken in light within 24 hours. Their coloration system is an excellent model for exploring the processes and mechanisms of light-induced pigmentation and revealing the genetic adaptation for non-obligative cave dwelling due to complicated life history. Using comparative transcriptomics, we found that melanocyte MCC (including melanogenesis and melanocytes proliferation) was responsible for the rapid skin darkening in was activated in O. rhodostigmatus. Light exposure induced robust activation of growth signals (including growth factor signals, MAPK signal pathways and PIK3-Akt signal pathways) at transcriptional levels, which were likely the upstream activation signals of melanocyte MCC in O. rhodostigmatus tadpoles. These results evidenced that amphibians and mammals likely share similar regulatory signals for light-induced melanocyte MCC. The conservation of pigmentation mechanisms across lower vertebrates and mammals imply that knowledge based on simpler models could also provide implications for causations and therapies of human pigmentation disorders and pigmented tumors. In aspect of genetic adaptation, an in-frame deletion of four amino acids in the membrane/extracellular junctions of the second and third transmembrane domains of O. rhodostigmatus MC1R, the receptor for melanogenesis signal, was identified. This mutation increases the negative charge of the ligand pocket of MC1R and results stereo-tandem of three aspartate residues aligning towards its ligand pocket. The ligand pocket of O. rhodostigmatus MC1R resembles a trap for positively charged ligands (α-MSH and ACTH) and likely increases the ligands-dependent activity of MC1R, providing an explanation for the rapid MCC of O. rhodostigmatus in light. Meanwhile, increased negative charge of ligand pocket likely decreased the constitutive activity of MC1R, in in supporting the albinistic phenotype of cave dwelling tadpoles. Therefore, genetic change of MC1R explains, at least to some extent, how the pigmentation system of O. rhodostigmatus coordinates the capacity of rapid melanogenesis (or other types of pigment production) and pigment regression, a couple of seemingly contradictory coloration requirements. To our knowledge, this is the first study reporting the association between pigmentation phenotype adaptation and MC1R mutations in amphibians or in non-obligative cave dwellers.

Dataset Information

Transcriptomics reveals the molecular processes of light-induced rapid darkening of the non-obligate cave dweller Oreolalax rhodostigmatus (Megophryidae, Anura) and their genetic basis of pigmentation strategy.

Publications

Transcriptomics reveals the molecular processes of light-induced rapid darkening of the non-obligate cave dweller Oreolalax rhodostigmatus (Megophryidae, Anura) and their genetic basis of pigmentation strategy.

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