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Ferric reduction by a CYBDOM protein counteracts increased iron availability in root meristems induced by phosphorus deficiency

Author

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  • Rodolfo A. Maniero

    (Leibniz Institute of Plant Genetics & Crop Plant Research (IPK) OT Gatersleben, Corrensstr 3)

  • Cristiana Picco

    (Institute of Biophysics, National Research Council)

  • Anja Hartmann

    (Leibniz Institute of Plant Genetics & Crop Plant Research (IPK) OT Gatersleben, Corrensstr 3)

  • Felipe Engelberger

    (Leipzig University)

  • Antonella Gradogna

    (Institute of Biophysics, National Research Council)

  • Joachim Scholz-Starke

    (Institute of Biophysics, National Research Council)

  • Michael Melzer

    (Leibniz Institute of Plant Genetics & Crop Plant Research (IPK) OT Gatersleben, Corrensstr 3)

  • Georg Künze

    (Leipzig University
    Leipzig University
    Leipzig University)

  • Armando Carpaneto

    (Institute of Biophysics, National Research Council
    University of Genoa)

  • Nicolaus Wirén

    (Leibniz Institute of Plant Genetics & Crop Plant Research (IPK) OT Gatersleben, Corrensstr 3)

  • Ricardo F. H. Giehl

    (Leibniz Institute of Plant Genetics & Crop Plant Research (IPK) OT Gatersleben, Corrensstr 3)

Abstract

To mobilize sparingly available phosphorus (P) in the rhizosphere, many plant species secrete malate to release P sorbed onto (hydr)oxides of aluminum and iron (Fe). In the presence of Fe, malate can provoke Fe over-accumulation in the root apoplast, triggering a series of events that inhibit root growth. Here, we identified HYPERSENSITIVE TO LOW P1 (HYP1), a CYBDOM protein constituted of a DOMON and a cytochrome b561 domain, as critical to maintain cell elongation and meristem integrity under low P. We demonstrate that HYP1 mediates ascorbate-dependent trans-plasma membrane electron transport and can reduce ferric and cupric substrates in Xenopus laevis oocytes and in planta. HYP1 expression is up-regulated in response to P deficiency in the proximal zone of the root apical meristem. Disruption of HYP1 leads to increased Fe and callose accumulation in the root meristem and causes significant transcriptional changes in roots. We further demonstrate that HYP1 activity overcomes malate-induced Fe accumulation, thereby preventing Fe-dependent root growth arrest in response to low P. Collectively, our results uncover an ascorbate-dependent metalloreductase that is critical to protect root meristems of P-deficient plants from increased Fe availability and provide insights into the physiological function of the yet poorly characterized but ubiquitous CYBDOM proteins.

Suggested Citation

  • Rodolfo A. Maniero & Cristiana Picco & Anja Hartmann & Felipe Engelberger & Antonella Gradogna & Joachim Scholz-Starke & Michael Melzer & Georg Künze & Armando Carpaneto & Nicolaus Wirén & Ricardo F. , 2024. "Ferric reduction by a CYBDOM protein counteracts increased iron availability in root meristems induced by phosphorus deficiency," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-43912-w
    DOI: 10.1038/s41467-023-43912-w
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    1. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    2. Smyth Gordon K, 2004. "Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 3(1), pages 1-28, February.
    3. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
    4. Keiji Nakajima & Giovanni Sena & Tal Nawy & Philip N. Benfey, 2001. "Intercellular movement of the putative transcription factor SHR in root patterning," Nature, Nature, vol. 413(6853), pages 307-311, September.
    5. Nigel J. Robinson & Catherine M. Procter & Erin L. Connolly & Mary Lou Guerinot, 1999. "A ferric-chelate reductase for iron uptake from soils," Nature, Nature, vol. 397(6721), pages 694-697, February.
    6. Coline Balzergue & Thibault Dartevelle & Christian Godon & Edith Laugier & Claudia Meisrimler & Jean-Marie Teulon & Audrey Creff & Marie Bissler & Corinne Brouchoud & Agnès Hagège & Jens Müller & Serg, 2017. "Low phosphate activates STOP1-ALMT1 to rapidly inhibit root cell elongation," Nature Communications, Nature, vol. 8(1), pages 1-16, August.
    7. Rahul Bhosale & Jitender Giri & Bipin K. Pandey & Ricardo F. H. Giehl & Anja Hartmann & Richard Traini & Jekaterina Truskina & Nicola Leftley & Meredith Hanlon & Kamal Swarup & Afaf Rashed & Ute Voß &, 2018. "A mechanistic framework for auxin dependent Arabidopsis root hair elongation to low external phosphate," Nature Communications, Nature, vol. 9(1), pages 1-9, December.
    8. Xing Xing Liu & Hai Hua Zhang & Qing Yang Zhu & Jia Yuan Ye & Ya Xin Zhu & Xiang Ting Jing & Wen Xin Du & Miao Zhou & Xian Yong Lin & Shao Jian Zheng & Chong Wei Jin, 2022. "Phloem iron remodels root development in response to ammonium as the major nitrogen source," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    9. Rahul Bhosale & Jitender Giri & Bipin K. Pandey & Ricardo F. H. Giehl & Anja Hartmann & Richard Traini & Jekaterina Truskina & Nicola Leftley & Meredith Hanlon & Kamal Swarup & Afaf Rashed & Ute Voß &, 2018. "Author Correction: A mechanistic framework for auxin dependent Arabidopsis root hair elongation to low external phosphate," Nature Communications, Nature, vol. 9(1), pages 1-1, December.
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