Uncoupling Aluminum Toxicity From Aluminum Signals in the STOP1 Pathway
Aluminum (Al) is a major limiting factor for crop production on acidic soils, inhibiting root growth and plant development. At acidic pH (pH < 5.5), Al3+ ions are the main form of Al present in the media. Al3+ ions have an increased solubility at pH < 5.5 and result in plant toxicity....
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-05-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2022.785791/full |
| _version_ | 1818572073363046400 |
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| author | Léa Le Poder Caroline Mercier Caroline Mercier Laureline Février Nathalie Duong Pascale David Sylvain Pluchon Laurent Nussaume Thierry Desnos |
| author_facet | Léa Le Poder Caroline Mercier Caroline Mercier Laureline Février Nathalie Duong Pascale David Sylvain Pluchon Laurent Nussaume Thierry Desnos |
| author_sort | Léa Le Poder |
| collection | DOAJ |
| description | Aluminum (Al) is a major limiting factor for crop production on acidic soils, inhibiting root growth and plant development. At acidic pH (pH < 5.5), Al3+ ions are the main form of Al present in the media. Al3+ ions have an increased solubility at pH < 5.5 and result in plant toxicity. At higher pH, the free Al3+ fraction decreases in the media, but whether plants can detect Al at these pHs remain unknown. To cope with Al stress, the SENSITIVE TO PROTON RHIZOTOXICITY1 (STOP1) transcription factor induces AL-ACTIVATED MALATE TRANSPORTER1 (ALMT1), a malate-exuding transporter as a strategy to chelate the toxic ions in the rhizosphere. Here, we uncoupled the Al signalling pathway that controls STOP1 from Al toxicity using wild type (WT) and two stop1 mutants carrying the pALMT1:GUS construct with an agar powder naturally containing low amounts of phosphate, iron (Fe), and Al. We combined gene expression [real-time PCR (RT-PCR) and the pALMT1:GUS reporter], confocal microscopy (pSTOP1:GFP-STOP1 reporter), and root growth measurement to assess the effects of Al and Fe on the STOP1-ALMT1 pathway in roots. Our results show that Al triggers STOP1 signaling at a concentration as little as 2 μM and can be detected at a pH above 6.0. We observed that at pH 5.7, 20 μM AlCl3 induces ALMT1 in WT but does not inhibit root growth in stop1 Al-hypersensitive mutants. Increasing AlCl3 concentration (>50 μM) at pH 5.7 results in the inhibition of the stop1 mutants primary root. Using the green fluorescent protein (GFP)-STOP1 and ALMT1 reporters, we show that the Al signal pathway can be uncoupled from the Al toxicity on the root. Furthermore, we observe that Al strengthens the Fe-mediated inhibition of primary root growth in WT, suggesting an interaction between Fe and Al on the STOP1-ALMT1 pathway. |
| first_indexed | 2024-12-14T18:52:32Z |
| format | Article |
| id | doaj.art-58e396247aa44028a7a785a33699f844 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-14T18:52:32Z |
| publishDate | 2022-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-58e396247aa44028a7a785a33699f8442022-12-21T22:51:11ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-05-011310.3389/fpls.2022.785791785791Uncoupling Aluminum Toxicity From Aluminum Signals in the STOP1 PathwayLéa Le Poder0Caroline Mercier1Caroline Mercier2Laureline Février3Nathalie Duong4Pascale David5Sylvain Pluchon6Laurent Nussaume7Thierry Desnos8Aix Marseille Université, CEA, CNRS, BIAM, UMR 7265, SAVE, Saint Paul-lez-Durance, FranceAix Marseille Université, CEA, CNRS, BIAM, UMR 7265, SAVE, Saint Paul-lez-Durance, FranceLaboratoire de Nutrition Végétale, Agroinnovation International – TIMAC AGRO, Saint-Malo, FranceIRSN/PSE-ENV/SRTE/LR2T, Saint Paul-lez-Durance, FranceAix Marseille Université, CEA, CNRS, BIAM, UMR 7265, SAVE, Saint Paul-lez-Durance, FranceAix Marseille Université, CEA, CNRS, BIAM, UMR 7265, SAVE, Saint Paul-lez-Durance, FranceLaboratoire de Nutrition Végétale, Agroinnovation International – TIMAC AGRO, Saint-Malo, FranceAix Marseille Université, CEA, CNRS, BIAM, UMR 7265, SAVE, Saint Paul-lez-Durance, FranceAix Marseille Université, CEA, CNRS, BIAM, UMR 7265, SAVE, Saint Paul-lez-Durance, FranceAluminum (Al) is a major limiting factor for crop production on acidic soils, inhibiting root growth and plant development. At acidic pH (pH < 5.5), Al3+ ions are the main form of Al present in the media. Al3+ ions have an increased solubility at pH < 5.5 and result in plant toxicity. At higher pH, the free Al3+ fraction decreases in the media, but whether plants can detect Al at these pHs remain unknown. To cope with Al stress, the SENSITIVE TO PROTON RHIZOTOXICITY1 (STOP1) transcription factor induces AL-ACTIVATED MALATE TRANSPORTER1 (ALMT1), a malate-exuding transporter as a strategy to chelate the toxic ions in the rhizosphere. Here, we uncoupled the Al signalling pathway that controls STOP1 from Al toxicity using wild type (WT) and two stop1 mutants carrying the pALMT1:GUS construct with an agar powder naturally containing low amounts of phosphate, iron (Fe), and Al. We combined gene expression [real-time PCR (RT-PCR) and the pALMT1:GUS reporter], confocal microscopy (pSTOP1:GFP-STOP1 reporter), and root growth measurement to assess the effects of Al and Fe on the STOP1-ALMT1 pathway in roots. Our results show that Al triggers STOP1 signaling at a concentration as little as 2 μM and can be detected at a pH above 6.0. We observed that at pH 5.7, 20 μM AlCl3 induces ALMT1 in WT but does not inhibit root growth in stop1 Al-hypersensitive mutants. Increasing AlCl3 concentration (>50 μM) at pH 5.7 results in the inhibition of the stop1 mutants primary root. Using the green fluorescent protein (GFP)-STOP1 and ALMT1 reporters, we show that the Al signal pathway can be uncoupled from the Al toxicity on the root. Furthermore, we observe that Al strengthens the Fe-mediated inhibition of primary root growth in WT, suggesting an interaction between Fe and Al on the STOP1-ALMT1 pathway.https://www.frontiersin.org/articles/10.3389/fpls.2022.785791/fullaluminumironphosphatepHSTOP1ALMT1 |
| spellingShingle | Léa Le Poder Caroline Mercier Caroline Mercier Laureline Février Nathalie Duong Pascale David Sylvain Pluchon Laurent Nussaume Thierry Desnos Uncoupling Aluminum Toxicity From Aluminum Signals in the STOP1 Pathway Frontiers in Plant Science aluminum iron phosphate pH STOP1 ALMT1 |
| title | Uncoupling Aluminum Toxicity From Aluminum Signals in the STOP1 Pathway |
| title_full | Uncoupling Aluminum Toxicity From Aluminum Signals in the STOP1 Pathway |
| title_fullStr | Uncoupling Aluminum Toxicity From Aluminum Signals in the STOP1 Pathway |
| title_full_unstemmed | Uncoupling Aluminum Toxicity From Aluminum Signals in the STOP1 Pathway |
| title_short | Uncoupling Aluminum Toxicity From Aluminum Signals in the STOP1 Pathway |
| title_sort | uncoupling aluminum toxicity from aluminum signals in the stop1 pathway |
| topic | aluminum iron phosphate pH STOP1 ALMT1 |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2022.785791/full |
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