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HOT3/eIF5B1 confers Kozak motif-dependent translational control of photosynthesis-associated nuclear genes for chloroplast biogenesis

Author

Listed:
  • Runlai Hang

    (Peking University)

  • Hao Li

    (Peking University)

  • Wenjing Liu

    (Peking University)

  • Runyu Wang

    (Peking University)

  • Hao Hu

    (Peking University)

  • Meng Chen

    (Riverside)

  • Chenjiang You

    (Guangzhou
    Guangzhou)

  • Xuemei Chen

    (Peking University)

Abstract

Photosynthesis requires chloroplasts, in which most proteins are nucleus-encoded and produced via cytoplasmic translation. The translation initiation factor eIF5B gates the transition from initiation (I) to elongation (E), and the Kozak motif is associated with translation efficiency, but their relationship is previously unknown. Here, with ribosome profiling, we determined the genome-wide I-E transition efficiencies. We discovered that the most prevalent Kozak motif is associated with high I-E transition efficiency in Arabidopsis, rice, and wheat, thus implicating the potential of the Kozak motif in facilitating the I-E transition. Indeed, the effects of Kozak motifs in promoting translation depend on HOT3/eIF5B1 in Arabidopsis. HOT3 preferentially promotes the translation of photosynthesis-associated nuclear genes in a Kozak motif-dependent manner, which explains the chloroplast defects and reduced photosynthesis activity of hot3 mutants. Our study linked the Kozak motif to eIF5B-mediated I-E transition during translation and uncovered the function of HOT3 in the cytoplasmic translational control of chloroplast biogenesis and photosynthesis.

Suggested Citation

  • Runlai Hang & Hao Li & Wenjing Liu & Runyu Wang & Hao Hu & Meng Chen & Chenjiang You & Xuemei Chen, 2024. "HOT3/eIF5B1 confers Kozak motif-dependent translational control of photosynthesis-associated nuclear genes for chloroplast biogenesis," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54194-1
    DOI: 10.1038/s41467-024-54194-1
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    References listed on IDEAS

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    1. Yezi Xiang & Wenze Huang & Lianmei Tan & Tianyuan Chen & Yang He & Patrick S. Irving & Kevin M. Weeks & Qiangfeng Cliff Zhang & Xinnian Dong, 2023. "Pervasive downstream RNA hairpins dynamically dictate start-codon selection," Nature, Nature, vol. 621(7978), pages 423-430, September.
    2. Jinfan Wang & Alex G. Johnson & Christopher P. Lapointe & Junhong Choi & Arjun Prabhakar & Dong-Hua Chen & Alexey N. Petrov & Joseph D. Puglisi, 2019. "eIF5B gates the transition from translation initiation to elongation," Nature, Nature, vol. 573(7775), pages 605-608, September.
    3. Christopher P. Lapointe & Rosslyn Grosely & Masaaki Sokabe & Carlos Alvarado & Jinfan Wang & Elizabeth Montabana & Nancy Villa & Byung-Sik Shin & Thomas E. Dever & Christopher S. Fraser & Israel S. Fe, 2022. "eIF5B and eIF1A reorient initiator tRNA to allow ribosomal subunit joining," Nature, Nature, vol. 607(7917), pages 185-190, July.
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    5. Youra Hwang & Soeun Han & Chan Yul Yoo & Liu Hong & Chenjiang You & Brandon H. Le & Hui Shi & Shangwei Zhong & Ute Hoecker & Xuemei Chen & Meng Chen, 2022. "Anterograde signaling controls plastid transcription via sigma factors separately from nuclear photosynthesis genes," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    6. Jinfan Wang & Jing Wang & Byung-Sik Shin & Joo-Ran Kim & Thomas E. Dever & Joseph D. Puglisi & Israel S. Fernández, 2020. "Structural basis for the transition from translation initiation to elongation by an 80S-eIF5B complex," Nature Communications, Nature, vol. 11(1), pages 1-8, December.
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