4.8 Article

The highest-elevation frog provides insights into mechanisms and evolution of defenses against high UV radiation

Publisher

NATL ACAD SCIENCES
DOI: 10.1073/pnas.2212406119

Keywords

UV defense; melanin production; gene substitution; expression shift

Funding

  1. Chinese Academy of Sciences [XDPB17, XDA20050201, 2017VBA0003, 2018VBA0039]
  2. Second Tibetan Plateau Scientific Expedition and Research Program [2019QZKK0501]
  3. Chinese Academy of Sciences, Animal Branch of the Germplasm Bank of Wild Species
  4. Yunnan Province in China, Spring City Plan: the high-level talent promotion and training project of Kunming
  5. Natural Science Foundation of China [31671326, 81760648]
  6. Yunnan Province in China [202101AV070009]
  7. State Key Laboratory of Genetic Resources and Evolution [GREKF20-02]
  8. National Sciences and Engineering Research Council of Canada [A3148]
  9. China Scholarship Council [201904910862]

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A study on Nanorana parkeri, the highest-elevation frog, revealed its superior defense against UV radiation compared to lower-elevation relatives. The frog showed less skin damage and more efficient antioxidant activity after UV exposure. Analysis of its genes, metabolomics, and large-scale transcripts indicated a time-dependent coordinated defense mechanism, as well as the presence of important regulatory microRNAs.
Defense against ultraviolet (UV) radiation exposure is essential for survival, especially in high-elevation species. Although some specific genes involved in UV response have been reported, the full view of UV defense mechanisms remains largely unexplored. Herein, we used integrated approaches to analyze UV responses in the highest-elevation frog, Nanorana parkeri. We show less damage and more efficient antioxidant activity in skin of this frog than those of its lower-elevation relatives after UV exposure. We also reveal genes related to UV defense and a corresponding temporal expression pattern in N. parkeri. Genomic and metabolomic analysis along with large-scale transcriptomic profiling revealed a time-dependent coordinated defense mechanism in N. parkeri. We also identified several microRNAs that play important regulatory roles, especially in decreasing the expression levels of cell cycle genes. Moreover, multiple defense genes (i.e., TYR for melanogenesis) exhibit positive selection with function-enhancing substitutions. Thus, both expression shifts and gene mutations contribute to UV adaptation in N. parkeri. Our work demonstrates a genetic framework for evolution of UV defense in a natural environment.

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