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

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.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4790-y) contains supplementary material, which is available to authorized users.

Effects of photoperiod on growth performance and melanogenesis pathway for skin pigmentation of Malaysian red tilapia

“…In this study, the mRNA expression of sox 10 , tyr , slc7a11 and tyrp‐1 genes in red tilapia was directly affected by light duration, similar to results obtained in Oreolalax rhodostigmatus (Zhu et al, ). In the ventral skin of Malaysian red tilapia, sox 10 mRNA expression level was increased in prolonged darkness.…”

“…The colour phenotype of different organisms is influenced by the interaction between environmental factors and genetics (Hubbard, Uy, Hauber, Hoekstra, & Safran, ). Among the environmental factors, light condition is known to play a major role in pigmentation by affecting melanin concentration and distribution (Pavlidis, Karkana, Fanouraki, & Papandroulakis, ; Zhu et al, ). Two major types of melanin are known, the eumelanin (black/brown) and pheomelanin (red/yellow) (Bar, Kaddar, Velan, & David, ), which are the important determinants of colour variations in animals (Morgan, Lo, & Fisher, ).…”

Remarkable metabolic reorganization and altered metabolic requirements in frog metamorphic climax

“…Total RNA of each liver or tail sample (n = 3 for each stage or treatment group) was extracted using a TRIzol kit (Invitrogen, Carlsbad, CA, USA), following manufacturer instructions. After RNA quantification, quality assessment and purification, cDNA libraries were built following the methods described by Zhu et al [34]. After cluster generation, the libraries were sequenced on an Illumina HiSeq 2500 platform by Annoroad (Beijing, China), and paired-end reads were generated.…”

Plateau Grass and Greenhouse Flower? Distinct Genetic Basis of Closely Related Toad Tadpoles Respectively Adapted to High Altitude and Karst Caves

“…Thus, a series of typical phenotypes of cave adaptation in the toad tadpoles, such as small eyes, transparent bodies, and a long developmental cycle [17,18], might be derived from gene loss, pseudogenization or deletion [21], other than fast evolving or positive selection. For example, in O. rhodostigmatus tadpoles, in-frame deletion of four amino acids in the M/EJTD of MC1R supporting the transparent phenotype of the tadpoles [59], was not detected by our fast evolving and positively selective analyses. This indicated that further work on cave adaptation should focus on explorations of gene structure, multiple copy gene families, genomic architecture, etc.…”