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The phosphorylation of carboxyl-terminal eIF2α by SPA kinases contributes to enhanced translation efficiency during photomorphogenesis

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  • Hui-Hsien Chang

    (National Taiwan University)

  • Lin-Chen Huang

    (National Taiwan University)

  • Karen S. Browning

    (University of Texas at Austin)

  • Enamul Huq

    (University of Texas at Austin)

  • Mei-Chun Cheng

    (National Taiwan University)

Abstract

Light triggers an enhancement of global translation during photomorphogenesis in Arabidopsis, but little is known about the underlying mechanisms. The phosphorylation of the α-subunit of eukaryotic initiation factor 2 (eIF2α) at a conserved serine residue in the N-terminus has been shown as an important mechanism for the regulation of protein synthesis in mammalian and yeast cells. However, whether the phosphorylation of this residue in plant eIF2α plays a role in regulation of translation remains elusive. Here, we show that the quadruple mutant of SUPPRESSOR OF PHYA-105 family members (SPA1-SPA4) display repressed translation efficiency after light illumination. Moreover, SPA1 directly phosphorylates the eIF2α C-terminus under light conditions. The C-term-phosphorylated eIF2α promotes translation efficiency and photomorphogenesis, whereas the C-term-unphosphorylated eIF2α results in a decreased translation efficiency. We also demonstrate that the phosphorylated eIF2α enhances ternary complex assembly by promoting its affinity to eIF2β and eIF2γ. This study reveals a unique mechanism by which light promotes translation via SPA1-mediated phosphorylation of the C-terminus of eIF2α in plants.

Suggested Citation

  • Hui-Hsien Chang & Lin-Chen Huang & Karen S. Browning & Enamul Huq & Mei-Chun Cheng, 2024. "The phosphorylation of carboxyl-terminal eIF2α by SPA kinases contributes to enhanced translation efficiency during photomorphogenesis," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47848-7
    DOI: 10.1038/s41467-024-47848-7
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    References listed on IDEAS

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    1. Martin D. Jennings & Graham D. Pavitt, 2010. "Erratum: eIF5 has GDI activity necessary for translational control by eIF2 phosphorylation," Nature, Nature, vol. 468(7320), pages 122-122, November.
    2. Inyup Paik & Fulu Chen & Vinh Ngoc Pham & Ling Zhu & Jeong-Il Kim & Enamul Huq, 2019. "A phyB-PIF1-SPA1 kinase regulatory complex promotes photomorphogenesis in Arabidopsis," Nature Communications, Nature, vol. 10(1), pages 1-17, December.
    3. Martin D. Jennings & Graham D. Pavitt, 2010. "eIF5 has GDI activity necessary for translational control by eIF2 phosphorylation," Nature, Nature, vol. 465(7296), pages 378-381, May.
    4. Ling Zhu & Qingyun Bu & Xiaosa Xu & Inyup Paik & Xi Huang & Ute Hoecker & Xing Wang Deng & Enamul Huq, 2015. "CUL4 forms an E3 ligase with COP1 and SPA to promote light-induced degradation of PIF1," Nature Communications, Nature, vol. 6(1), pages 1-10, November.
    5. Sanghwa Lee & Wenli Wang & Enamul Huq, 2021. "Spatial regulation of thermomorphogenesis by HY5 and PIF4 in Arabidopsis," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
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