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Seasonal regulation of the lncRNA LDAIR modulates self-protective behaviours during the breeding season

Nature Ecology & Evolution volume 3, pages 845–852 (2019)Cite this article

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Abstract

To cope with seasonal environmental changes, animals adapt their physiology and behaviour in response to photoperiod. However, the molecular mechanisms underlying these adaptive changes are not completely understood. Here, using genome-wide expression analysis, we show that an uncharacterized long noncoding RNA (lncRNA), LDAIR, is strongly regulated by photoperiod in Japanese medaka fish (Oryzias latipes). Numerous transcripts and signalling pathways are activated during the transition from short- to long-day conditions; however, LDAIR is one of the first genes to be induced and its expression shows a robust daily rhythm under long-day conditions. Transcriptome analysis of LDAIR knockout fish reveals that the LDAIR locus regulates a gene neighbourhood, including corticotropin releasing hormone receptor 2, which is involved in the stress response. Behavioural analysis of LDAIR knockout fish demonstrates that LDAIR affects self-protective behaviours under long-day conditions. Therefore, we propose that photoperiodic regulation of corticotropin releasing hormone receptor 2 by LDAIR modulates adaptive behaviours to seasonal environmental changes.

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Fig. 1: Transcriptional landscape during the transition from short to long day.
Fig. 2: olvl28m13 is an lncRNA.
Fig. 3: The LDAIR locus regulates a gene neighbourhood.
Fig. 4: LDAIR knockout fish show decreased self-protective behaviours under long-day conditions.

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Data availability

The microarray and RNA-Seq data are available at the NCBI Gene Expression Omnibus (accession no. GSE119905). All other data are available from the authors upon request.

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Acknowledgements

We thank NBRP-Medaka (National Bio-Resource Project of MEXT, Japan) and the Data Integration and Analysis Facility for use of their facilities. We also thank M. Okubo, A. Akama, N. Baba and C. Kinoshita for technical assistance, and T.K. Tamai for comments on the manuscript. This work was supported in part by the JSPS KAKENHI Grant-in-Aid for Specially Promoted Research (grant no. 26000013), the Human Frontier Science Program (grant no. RGP0030/2015) and Grant-in-Aid for JSPS Fellows (grant no. 18J10936). The WPI-ITbM is supported by the World Premier International Research Center Initiative, MEXT, Japan.

Author information

Author notes

  1. Tsuyoshi Shimmura

    Present address: Department of Biological Production, Tokyo University of Agriculture and Technology, Fuchu, Tokyo, Japan

  2. Yusuke Takehana

    Present address: Department of Bio-Science, Nagahama Institute of Bio-Science and Technology, Nagahama, Japan

  3. These authors contributed equally: Tomoya Nakayama, Tsuyoshi Shimmura

Authors and Affiliations

  1. Division of Seasonal Biology, National Institute for Basic Biology, Okazaki, Japan

    Tomoya Nakayama, Tsuyoshi Shimmura, Ai Shinomiya, Takayuki Shimo, Takumi Senga, Mana Nakatsukasa & Takashi Yoshimura

  2. Laboratory of Animal Integrative Physiology, Nagoya University, Nagoya, Japan

    Tomoya Nakayama, Tsuyoshi Shimmura, Kousuke Okimura, Takayuki Shimo, Takumi Senga, Mana Nakatsukasa & Takashi Yoshimura

  3. Department of Basic Biology, The Graduate University for Advanced Studies (SOKENDAI), Miura, Japan

    Tsuyoshi Shimmura, Ai Shinomiya, Yusuke Takehana, Yasuhiro Kamei & Kiyoshi Naruse

  4. Institute of Transformative Bio-Molecules (WPI-ITbM), Nagoya University, Nagoya, Japan

    Kousuke Okimura, Yuko Furukawa & Takashi Yoshimura

  5. Laboratory of Bioresources, National Institute for Basic Biology, Okazaki, Japan

    Yusuke Takehana & Kiyoshi Naruse

  6. Division of Biological Science, Graduate School of Science, Nagoya University, Nagoya, Japan

    Toshiya Nishimura & Minoru Tanaka

  7. Department of Aquatic Bioscience, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo, Tokyo, Japan

    Kataaki Okubo

  8. Spectrography and Bioimaging Facility, National Institute for Basic Biology, Okazaki, Japan

    Yasuhiro Kamei

  9. Avian Bioscience Research Center, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan

    Takashi Yoshimura

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Contributions

T.Y. conceived the research. T. Nakayama, T. Shimmura and T.Y. designed the research. T. Shimmura, T. Shimo, T. Senga and T.Y. performed the microarray analysis for the short-day to long-day transition experiments. T. Nakayama, K. Okimura and T.Y. performed the IPA. T. Nakayama and Y.F. performed the strand-specific RNA-Seq. T. Nakayama performed the Ribo-Seq, qPCR analysis, cortisol measurement and behavioural assays. T. Nakayama, T. Shimmura, Y.T., T. Shimo and M.N. generated and genotyped LDAIR knockout medaka. T. Nakayama and A.S. performed the microarray analysis for the experiment using the LDAIR knockout fish. T. Nishimura and M.T. provided the medaka microarrays. Y.K., K.N. and K. Okubo provided new methods and materials. T. Nakayama and T.Y. wrote the manuscript. All authors discussed the results and commented on the manuscript.

Corresponding author

Correspondence to Takashi Yoshimura.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–6 and Supplementary Table 1

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Supplementary Data

Supplementary Data 1: List of photoperiodically-regulated transcripts. Supplementary Data 2: List of differentially expressed transcripts between wild type (WT) and LDAIR knockout (KO) medaka.

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Nakayama, T., Shimmura, T., Shinomiya, A. et al. Seasonal regulation of the lncRNA LDAIR modulates self-protective behaviours during the breeding season. Nat Ecol Evol 3, 845–852 (2019). https://doi.org/10.1038/s41559-019-0866-6

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