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Interdependent iron and phosphorus availability controls photosynthesis through retrograde signaling

Author

Listed:
  • Hye-In Nam

    (Carnegie Institution for Science)

  • Zaigham Shahzad

    (John Innes Centre)

  • Yanniv Dorone

    (Carnegie Institution for Science
    Stanford University)

  • Sophie Clowez

    (Carnegie Institution for Science)

  • Kangmei Zhao

    (Carnegie Institution for Science)

  • Nadia Bouain

    (Stanford University)

  • Katerina S. Lay-Pruitt

    (Michigan State University
    Michigan State University)

  • Huikyong Cho

    (Stanford University)

  • Seung Y. Rhee

    (Carnegie Institution for Science)

  • Hatem Rouached

    (Michigan State University
    Michigan State University
    BPMP, Univ Montpellier, CNRS, INRAE, Montpellier SupAgro)

Abstract

Iron deficiency hampers photosynthesis and is associated with chlorosis. We recently showed that iron deficiency-induced chlorosis depends on phosphorus availability. How plants integrate these cues to control chlorophyll accumulation is unknown. Here, we show that iron limitation downregulates photosynthesis genes in a phosphorus-dependent manner. Using transcriptomics and genome-wide association analysis, we identify two genes, PHT4;4 encoding a chloroplastic ascorbate transporter and bZIP58, encoding a nuclear transcription factor, which prevent the downregulation of photosynthesis genes leading to the stay-green phenotype under iron-phosphorus deficiency. Joint limitation of these nutrients induces ascorbate accumulation by activating expression of an ascorbate biosynthesis gene, VTC4, which requires bZIP58. Furthermore, we demonstrate that chloroplastic ascorbate transport prevents the downregulation of photosynthesis genes under iron-phosphorus combined deficiency through modulation of ROS homeostasis. Our study uncovers a ROS-mediated chloroplastic retrograde signaling pathway to adapt photosynthesis to nutrient availability.

Suggested Citation

  • Hye-In Nam & Zaigham Shahzad & Yanniv Dorone & Sophie Clowez & Kangmei Zhao & Nadia Bouain & Katerina S. Lay-Pruitt & Huikyong Cho & Seung Y. Rhee & Hatem Rouached, 2021. "Interdependent iron and phosphorus availability controls photosynthesis through retrograde signaling," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27548-2
    DOI: 10.1038/s41467-021-27548-2
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    References listed on IDEAS

    as
    1. Roland Lill, 2009. "Function and biogenesis of iron–sulphur proteins," Nature, Nature, vol. 460(7257), pages 831-838, August.
    2. Takaaki Miyaji & Takashi Kuromori & Yu Takeuchi & Naoki Yamaji & Kengo Yokosho & Atsushi Shimazawa & Eriko Sugimoto & Hiroshi Omote & Jian Feng Ma & Kazuo Shinozaki & Yoshinori Moriyama, 2015. "AtPHT4;4 is a chloroplast-localized ascorbate transporter in Arabidopsis," Nature Communications, Nature, vol. 6(1), pages 1-11, May.
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    Cited by:

    1. Guo-Wei Qiu & Wen-Can Zheng & Hao-Ming Yang & Yu-Ying Wang & Xing Qi & Da Huang & Guo-Zheng Dai & Huazhong Shi & Neil M. Price & Bao-Sheng Qiu, 2024. "Phosphorus deficiency alleviates iron limitation in Synechocystis cyanobacteria through direct PhoB-mediated gene regulation," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Chen, Lingyun & Hu, Ziyi & Chen, Wenhui & Xu, Ziwei & Hao, Can & Lakshmanan, Prakash & Liu, Dunyi & Chen, Xinping, 2023. "Comparative study of the effectiveness of nano-sized iron-containing particles as a foliar top-dressing of peanut in rainy conditions," Agricultural Water Management, Elsevier, vol. 286(C).

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