IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-023-43912-w.html
   My bibliography  Save this article

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

Author

Listed:
  • 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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43912-w
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-43912-w?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. María Pérez-Burgos & Marco Herfurth & Andreas Kaczmarczyk & Andrea Harms & Katrin Huber & Urs Jenal & Timo Glatter & Lotte Søgaard-Andersen, 2024. "A deterministic, c-di-GMP-dependent program ensures the generation of phenotypically similar, symmetric daughter cells during cytokinesis," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    2. Joaquín Clúa & Jonatan Montpetit & Pedro Jimenez-Sandoval & Christin Naumann & Julia Santiago & Yves Poirier, 2024. "A CYBDOM protein impacts iron homeostasis and primary root growth under phosphate deficiency in Arabidopsis," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    3. Ye Yuan & Lei Chen & Kexu Song & Miaomiao Cheng & Ling Fang & Lingfei Kong & Lanlan Yu & Ruonan Wang & Zhendong Fu & Minmin Sun & Qian Wang & Chengjun Cui & Haojue Wang & Jiuyang He & Xiaonan Wang & Y, 2024. "Stable peptide-assembled nanozyme mimicking dual antifungal actions," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Ivica Odorčić & Mohamed Belal Hamed & Sam Lismont & Lucía Chávez-Gutiérrez & Rouslan G. Efremov, 2024. "Apo and Aβ46-bound γ-secretase structures provide insights into amyloid-β processing by the APH-1B isoform," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. Stella Vitt & Simone Prinz & Martin Eisinger & Ulrich Ermler & Wolfgang Buckel, 2022. "Purification and structural characterization of the Na+-translocating ferredoxin: NAD+ reductase (Rnf) complex of Clostridium tetanomorphum," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    6. Pierre Azoulay & Joshua Krieger & Abhishek Nagaraj, 2024. "Old Moats for New Models: Openness, Control, and Competition in Generative AI," NBER Chapters, in: Entrepreneurship and Innovation Policy and the Economy, volume 4, National Bureau of Economic Research, Inc.
    7. Riya Shah & Thomas C. Panagiotou & Gregory B. Cole & Trevor F. Moraes & Brigitte D. Lavoie & Christopher A. McCulloch & Andrew Wilde, 2024. "The DIAPH3 linker specifies a β-actin network that maintains RhoA and Myosin-II at the cytokinetic furrow," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    8. Yashan Yang & Qianqian Shao & Mingcheng Guo & Lin Han & Xinyue Zhao & Aohan Wang & Xiangyun Li & Bo Wang & Ji-An Pan & Zhenguo Chen & Andrei Fokine & Lei Sun & Qianglin Fang, 2024. "Capsid structure of bacteriophage ΦKZ provides insights into assembly and stabilization of jumbo phages," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    9. Bret M. Boyd & Ian James & Kevin P. Johnson & Robert B. Weiss & Sarah E. Bush & Dale H. Clayton & Colin Dale, 2024. "Stochasticity, determinism, and contingency shape genome evolution of endosymbiotic bacteria," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    10. Jun-Yu Si & Yuan-Mei Chen & Ye-Hui Sun & Meng-Xue Gu & Mei-Ling Huang & Lu-Lu Shi & Xiao Yu & Xiao Yang & Qing Xiong & Cheng-Bao Ma & Peng Liu & Zheng-Li Shi & Huan Yan, 2024. "Sarbecovirus RBD indels and specific residues dictating multi-species ACE2 adaptiveness," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    11. Deyun Qiu & Jinxin V. Pei & James E. O. Rosling & Vandana Thathy & Dongdi Li & Yi Xue & John D. Tanner & Jocelyn Sietsma Penington & Yi Tong Vincent Aw & Jessica Yi Han Aw & Guoyue Xu & Abhai K. Tripa, 2022. "A G358S mutation in the Plasmodium falciparum Na+ pump PfATP4 confers clinically-relevant resistance to cipargamin," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    12. Shuo-Shuo Liu & Tian-Xia Jiang & Fan Bu & Ji-Lan Zhao & Guang-Fei Wang & Guo-Heng Yang & Jie-Yan Kong & Yun-Fan Qie & Pei Wen & Li-Bin Fan & Ning-Ning Li & Ning Gao & Xiao-Bo Qiu, 2024. "Molecular mechanisms underlying the BIRC6-mediated regulation of apoptosis and autophagy," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    13. Justin N. Vaughn & Sandra E. Branham & Brian Abernathy & Amanda M. Hulse-Kemp & Adam R. Rivers & Amnon Levi & William P. Wechter, 2022. "Graph-based pangenomics maximizes genotyping density and reveals structural impacts on fungal resistance in melon," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    14. Eliza S. Nieweglowska & Axel F. Brilot & Melissa Méndez-Moran & Claire Kokontis & Minkyung Baek & Junrui Li & Yifan Cheng & David Baker & Joseph Bondy-Denomy & David A. Agard, 2023. "The ϕPA3 phage nucleus is enclosed by a self-assembling 2D crystalline lattice," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    15. Sash Lopaticki & Robyn McConville & Alan John & Niall Geoghegan & Shihab Deen Mohamed & Lisa Verzier & Ryan W. J. Steel & Cindy Evelyn & Matthew T. O’Neill & Niccolay Madiedo Soler & Nichollas E. Scot, 2022. "Tryptophan C-mannosylation is critical for Plasmodium falciparum transmission," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    16. Radoslaw Pluta & Eric Aragón & Nicholas A. Prescott & Lidia Ruiz & Rebeca A. Mees & Blazej Baginski & Julia R. Flood & Pau Martin-Malpartida & Joan Massagué & Yael David & Maria J. Macias, 2022. "Molecular basis for DNA recognition by the maternal pioneer transcription factor FoxH1," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    17. Xinheng He & Lifen Zhao & Yinping Tian & Rui Li & Qinyu Chu & Zhiyong Gu & Mingyue Zheng & Yusong Wang & Shaoning Li & Hualiang Jiang & Yi Jiang & Liuqing Wen & Dingyan Wang & Xi Cheng, 2024. "Highly accurate carbohydrate-binding site prediction with DeepGlycanSite," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    18. Xiaoke Yang & Mingqi Zhu & Xue Lu & Yuxin Wang & Junyu Xiao, 2024. "Architecture and activation of human muscle phosphorylase kinase," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    19. Efren Garcia-Maldonado & Andrew D. Huber & Sergio C. Chai & Stanley Nithianantham & Yongtao Li & Jing Wu & Shyaron Poudel & Darcie J. Miller & Jayaraman Seetharaman & Taosheng Chen, 2024. "Chemical manipulation of an activation/inhibition switch in the nuclear receptor PXR," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    20. Mindaugas Margelevičius, 2024. "GTalign: spatial index-driven protein structure alignment, superposition, and search," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-43912-w. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.