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Introns are mediators of cell response to starvation

Author

Listed:
  • Julie Parenteau

    (Université de Sherbrooke, Sherbrooke)

  • Laurine Maignon

    (Université de Sherbrooke, Sherbrooke)

  • Mélodie Berthoumieux

    (Université de Sherbrooke)

  • Mathieu Catala

    (Université de Sherbrooke, Sherbrooke)

  • Vanessa Gagnon

    (Université de Sherbrooke, Sherbrooke)

  • Sherif Abou Elela

    (Université de Sherbrooke, Sherbrooke)

Abstract

Introns are ubiquitous features of all eukaryotic cells. Introns need to be removed from nascent messenger RNA through the process of splicing to produce functional proteins. Here we show that the physical presence of introns in the genome promotes cell survival under starvation conditions. A systematic deletion set of all known introns in budding yeast genes indicates that, in most cases, cells with an intron deletion are impaired when nutrients are depleted. This effect of introns on growth is not linked to the expression of the host gene, and was reproduced even when translation of the host mRNA was blocked. Transcriptomic and genetic analyses indicate that introns promote resistance to starvation by enhancing the repression of ribosomal protein genes that are downstream of the nutrient-sensing TORC1 and PKA pathways. Our results reveal functions of introns that may help to explain their evolutionary preservation in genes, and uncover regulatory mechanisms of cell adaptations to starvation.

Suggested Citation

  • Julie Parenteau & Laurine Maignon & Mélodie Berthoumieux & Mathieu Catala & Vanessa Gagnon & Sherif Abou Elela, 2019. "Introns are mediators of cell response to starvation," Nature, Nature, vol. 565(7741), pages 612-617, January.
    • Handle: RePEc:nat:nature:v:565:y:2019:i:7741:d:10.1038_s41586-018-0859-7
    DOI: 10.1038/s41586-018-0859-7
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    Cited by:

    1. Tomoyuki Ohno & Taichi Akase & Shunya Kono & Hikaru Kurasawa & Takuto Takashima & Shinya Kaneko & Yasunori Aizawa, 2022. "Biallelic and gene-wide genomic substitution for endogenous intron and retroelement mutagenesis in human cells," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. Chengyun Wu & Xingsong Wang & Yan Li & Weibo Zhen & Chunfei Wang & Xiaoqing Wang & Zhouli Xie & Xiumei Xu & Siyi Guo & José Ramón Botella & Binglian Zheng & Wei Wang & Chun-Peng Song & Zhubing Hu, 2024. "Sequestration of DBR1 to stress granules promotes lariat intronic RNAs accumulation for heat-stress tolerance," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Yongheng Fan & Xianming Wu & Sufang Han & Qi Zhang & Zheng Sun & Bing Chen & Xiaoyu Xue & Haipeng Zhang & Zhenni Chen & Man Yin & Zhifeng Xiao & Yannan Zhao & Jianwu Dai, 2023. "Single-cell analysis reveals region-heterogeneous responses in rhesus monkey spinal cord with complete injury," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    4. Nicholas C. Gervais & Rebecca S. Shapiro, 2024. "Discovering the hidden function in fungal genomes," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    5. Annabel Qi En Ng & Seow Neng Chan & Jun Wei Pek, 2024. "Nutrient-dependent regulation of a stable intron modulates germline mitochondrial quality control," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    6. Shurong Liu & Junhong Huang & Jie Zhou & Siyan Chen & Wujian Zheng & Chang Liu & Qiao Lin & Ping Zhang & Di Wu & Simeng He & Jiayi Ye & Shun Liu & Keren Zhou & Bin Li & Lianghu Qu & Jianhua Yang, 2024. "NAP-seq reveals multiple classes of structured noncoding RNAs with regulatory functions," Nature Communications, Nature, vol. 15(1), pages 1-21, December.

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