Ferric reduction by a CYBDOM protein counteracts increased iron availability in root meristems induced by phosphorus deficiency
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 inhib...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2024-01-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-43912-w |
| _version_ | 1827382055930953728 |
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| author | Rodolfo A. Maniero Cristiana Picco Anja Hartmann Felipe Engelberger Antonella Gradogna Joachim Scholz-Starke Michael Melzer Georg Künze Armando Carpaneto Nicolaus von Wirén Ricardo F. H. Giehl |
| author_facet | Rodolfo A. Maniero Cristiana Picco Anja Hartmann Felipe Engelberger Antonella Gradogna Joachim Scholz-Starke Michael Melzer Georg Künze Armando Carpaneto Nicolaus von Wirén Ricardo F. H. Giehl |
| author_sort | Rodolfo A. Maniero |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-03-08T14:13:58Z |
| format | Article |
| id | doaj.art-40d1c4e9872b4f48835bb5b28de24f9d |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-08T14:13:58Z |
| publishDate | 2024-01-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-40d1c4e9872b4f48835bb5b28de24f9d2024-01-14T12:29:20ZengNature PortfolioNature Communications2041-17232024-01-0115111810.1038/s41467-023-43912-wFerric reduction by a CYBDOM protein counteracts increased iron availability in root meristems induced by phosphorus deficiencyRodolfo A. Maniero0Cristiana Picco1Anja Hartmann2Felipe Engelberger3Antonella Gradogna4Joachim Scholz-Starke5Michael Melzer6Georg Künze7Armando Carpaneto8Nicolaus von Wirén9Ricardo F. H. Giehl10Leibniz Institute of Plant Genetics & Crop Plant Research (IPK) OT Gatersleben, Corrensstr 3Institute of Biophysics, National Research CouncilLeibniz Institute of Plant Genetics & Crop Plant Research (IPK) OT Gatersleben, Corrensstr 3Institute for Drug Discovery, Leipzig UniversityInstitute of Biophysics, National Research CouncilInstitute of Biophysics, National Research CouncilLeibniz Institute of Plant Genetics & Crop Plant Research (IPK) OT Gatersleben, Corrensstr 3Institute for Drug Discovery, Leipzig UniversityInstitute of Biophysics, National Research CouncilLeibniz Institute of Plant Genetics & Crop Plant Research (IPK) OT Gatersleben, Corrensstr 3Leibniz Institute of Plant Genetics & Crop Plant Research (IPK) OT Gatersleben, Corrensstr 3Abstract 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.https://doi.org/10.1038/s41467-023-43912-w |
| spellingShingle | Rodolfo A. Maniero Cristiana Picco Anja Hartmann Felipe Engelberger Antonella Gradogna Joachim Scholz-Starke Michael Melzer Georg Künze Armando Carpaneto Nicolaus von Wirén Ricardo F. H. Giehl Ferric reduction by a CYBDOM protein counteracts increased iron availability in root meristems induced by phosphorus deficiency Nature Communications |
| title | Ferric reduction by a CYBDOM protein counteracts increased iron availability in root meristems induced by phosphorus deficiency |
| title_full | Ferric reduction by a CYBDOM protein counteracts increased iron availability in root meristems induced by phosphorus deficiency |
| title_fullStr | Ferric reduction by a CYBDOM protein counteracts increased iron availability in root meristems induced by phosphorus deficiency |
| title_full_unstemmed | Ferric reduction by a CYBDOM protein counteracts increased iron availability in root meristems induced by phosphorus deficiency |
| title_short | Ferric reduction by a CYBDOM protein counteracts increased iron availability in root meristems induced by phosphorus deficiency |
| title_sort | ferric reduction by a cybdom protein counteracts increased iron availability in root meristems induced by phosphorus deficiency |
| url | https://doi.org/10.1038/s41467-023-43912-w |
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