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Iron rescues glucose-mediated photosynthesis repression during lipid accumulation in the green alga Chromochloris zofingiensis

Author

Listed:
  • Tim L. Jeffers

    (University of California)

  • Samuel O. Purvine

    (Pacific Northwest National Laboratory)

  • Carrie D. Nicora

    (Pacific Northwest National Laboratory)

  • Ryan McCombs

    (University of California)

  • Shivani Upadhyaya

    (University of California)

  • Adrien Stroumza

    (University of California)

  • Ken Whang

    (University of California)

  • Sean D. Gallaher

    (University of California
    University of California)

  • Alice Dohnalkova

    (Pacific Northwest National Laboratory)

  • Sabeeha S. Merchant

    (University of California
    University of California
    University of California
    Lawrence Berkeley National Laboratory)

  • Mary Lipton

    (Pacific Northwest National Laboratory)

  • Krishna K. Niyogi

    (University of California
    University of California
    Lawrence Berkeley National Laboratory)

  • Melissa S. Roth

    (University of California)

Abstract

Energy status and nutrients regulate photosynthetic protein expression. The unicellular green alga Chromochloris zofingiensis switches off photosynthesis in the presence of exogenous glucose (+Glc) in a process that depends on hexokinase (HXK1). Here, we show that this response requires that cells lack sufficient iron (−Fe). Cells grown in −Fe+Glc accumulate triacylglycerol (TAG) while losing photosynthesis and thylakoid membranes. However, cells with an iron supplement (+Fe+Glc) maintain photosynthesis and thylakoids while still accumulating TAG. Proteomic analysis shows that known photosynthetic proteins are most depleted in heterotrophy, alongside hundreds of uncharacterized, conserved proteins. Photosynthesis repression is associated with enzyme and transporter regulation that redirects iron resources to (a) respiratory instead of photosynthetic complexes and (b) a ferredoxin-dependent desaturase pathway supporting TAG accumulation rather than thylakoid lipid synthesis. Combining insights from diverse organisms from green algae to vascular plants, we show how iron and trophic constraints on metabolism aid gene discovery for photosynthesis and biofuel production.

Suggested Citation

  • Tim L. Jeffers & Samuel O. Purvine & Carrie D. Nicora & Ryan McCombs & Shivani Upadhyaya & Adrien Stroumza & Ken Whang & Sean D. Gallaher & Alice Dohnalkova & Sabeeha S. Merchant & Mary Lipton & Krish, 2024. "Iron rescues glucose-mediated photosynthesis repression during lipid accumulation in the green alga Chromochloris zofingiensis," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50170-x
    DOI: 10.1038/s41467-024-50170-x
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    References listed on IDEAS

    as
    1. Alessandro Tagliabue & Andrew R. Bowie & Philip W. Boyd & Kristen N. Buck & Kenneth S. Johnson & Mak A. Saito, 2017. "The integral role of iron in ocean biogeochemistry," Nature, Nature, vol. 543(7643), pages 51-59, March.
    2. Khurram Bashir & Yasuhiro Ishimaru & Hugo Shimo & Seiji Nagasaka & Masaru Fujimoto & Hideki Takanashi & Nobuhiro Tsutsumi & Gynheung An & Hiromi Nakanishi & Naoko K. Nishizawa, 2011. "The rice mitochondrial iron transporter is essential for plant growth," Nature Communications, Nature, vol. 2(1), pages 1-7, September.
    3. Joseph Swift & Mark Adame & Daniel Tranchina & Amelia Henry & Gloria M. Coruzzi, 2019. "Water impacts nutrient dose responses genome-wide to affect crop production," Nature Communications, Nature, vol. 10(1), pages 1-9, December.
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