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.

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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转录组学揭示了非专性穴居动物 Oreolalax rhodostigmatus(Megophryidae,Anura)光诱导快速变黑的分子过程及其色素沉着策略的遗传基础

DOI:
10.1186/s12864-018-4790-y
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发表时间:
2018-05-31
期刊:
影响因子:
4.4
通讯作者:
Wang B
Wang B
中科院分区:
生物学2区
文献类型:
--
作者:
Zhu W;Liu L;Wang X;Gao X;Jiang J;Wang B

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背景脊椎动物使用不同的着色策略来适应不同的环境。在揭示脊椎动物无论是在光照下还是在持续黑暗中生活的着色策略的机制方面,已经进行了大量的研究。然而,对非强制性、黑暗居民的关注较少。产于中国西南部喀斯特山区的红斑齿蛙Oreolalax rodostigmatus是一种非专性穴居动物。该物种的大多数蝌蚪都有透明的皮肤,因为它们生活在黑暗的喀斯特洞穴中。但值得注意的是,这些透明的蝌蚪一旦暴露在阳光下,就会在15小时内变暗。显然,揭示这种意外快速变暗现象的分子机制具有非常重要的意义。结果我们比较了不同光照时间的罗氏田鼠蝌蚪的转录本,研究了它们在光诱导快速变暗过程中的细胞过程和潜在的调控信号。参与黑素合成和黑素细胞增殖的基因(TYR、TYRP1和DCT)以及它们的转录因子(MITF)显示出光诱导的转录,表明形态颜色变化(MCC)在这一过程中起主导作用。生长因子、MAPK和PI3K-Akt通路相关基因的转录随着光照时间的延长而增加,提示光照可以诱导显著的生长信号,这可能有助于皮肤的快速变暗。最重要的是,在MCC中的关键受体-黑素皮质素-1受体(MC1R)中发现了四个残基的框内缺失。这种缺失导致带有三个立体串联天冬氨酸残基的更负电荷的配体口袋。这种结构变化可能降低了MC1R的构成活性,但增加了其配体依赖的活性,从而分别在黑暗和光照下协调了色素退化和快速黑素合成。结论快速MCC可能是光诱导罗氏田鼠蝌蚪快速变暗的原因。它们中MC1R的基因突变可以解释这些非专性洞穴居民如何分别在黑暗和光线下协调色素退化和强大的黑素生成。据我们所知,这是第一次报道两栖动物和/或非独居洞穴居民的色素沉着表型适应和MC1R突变之间的关联。
BackgroundVertebrates 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.ResultsWe 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.ConclusionOur 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.
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