Bicarbonate-Dependent Detoxification by Mitigating Ammonium-Induced Hypoxic Stress in <i>Triticum aestivum</i> Root
Ammonium (NH<sub>4</sub><sup>+</sup>) toxicity is ubiquitous in plants. To investigate the underlying mechanisms of this toxicity and bicarbonate (HCO<sub>3</sub><sup>−</sup>)-dependent alleviation, wheat plants were hydroponically cultivated in half-s...
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MDPI AG
2024-02-01
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| author | Xiao Liu Yunxiu Zhang Chengming Tang Huawei Li Haiyong Xia Shoujin Fan Lingan Kong |
| author_facet | Xiao Liu Yunxiu Zhang Chengming Tang Huawei Li Haiyong Xia Shoujin Fan Lingan Kong |
| author_sort | Xiao Liu |
| collection | DOAJ |
| description | Ammonium (NH<sub>4</sub><sup>+</sup>) toxicity is ubiquitous in plants. To investigate the underlying mechanisms of this toxicity and bicarbonate (HCO<sub>3</sub><sup>−</sup>)-dependent alleviation, wheat plants were hydroponically cultivated in half-strength Hoagland nutrient solution containing 7.5 mM NO<sub>3</sub><sup>−</sup> (CK), 7.5 mM NH<sub>4</sub><sup>+</sup> (SA), or 7.5 mM NH<sub>4</sub><sup>+</sup> + 3 mM HCO<sub>3</sub><sup>−</sup> (AC). Transcriptomic analysis revealed that compared to CK, SA treatment at 48 h significantly upregulated the expression of genes encoding fermentation enzymes (pyruvate decarboxylase (PDC), alcohol dehydrogenase (ADH), and lactate dehydrogenase (LDH)) and oxygen consumption enzymes (respiratory burst oxidase homologs, dioxygenases, and alternative oxidases), downregulated the expression of genes encoding oxygen transporters (PIP-type aquaporins, non-symbiotic hemoglobins), and those involved in energy metabolism, including tricarboxylic acid (TCA) cycle enzymes and ATP synthases, but upregulated the glycolytic enzymes in the roots and downregulated the expression of genes involved in the cell cycle and elongation. The physiological assay showed that SA treatment significantly increased PDC, ADH, and LDH activity by 36.69%, 43.66%, and 61.60%, respectively; root ethanol concentration by 62.95%; and lactate efflux by 23.20%, and significantly decreased the concentrations of pyruvate and most TCA cycle intermediates, the complex V activity, ATP content, and ATP/ADP ratio. As a consequence, SA significantly inhibited root growth. AC treatment reversed the changes caused by SA and alleviated the inhibition of root growth. In conclusion, NH<sub>4</sub><sup>+</sup> treatment alone may cause hypoxic stress in the roots, inhibit energy generation, suppress cell division and elongation, and ultimately inhibit root growth, and adding HCO<sub>3</sub><sup>−</sup> remarkably alleviates the NH<sub>4</sub><sup>+</sup>-induced inhibitory effects on root growth largely by attenuating the hypoxic stress. |
| first_indexed | 2024-03-07T22:41:55Z |
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| issn | 2079-7737 |
| language | English |
| last_indexed | 2024-03-07T22:41:55Z |
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| spelling | doaj.art-a9914e76bac447a2a5499ba1f3cb35ac2024-02-23T15:08:11ZengMDPI AGBiology2079-77372024-02-0113210110.3390/biology13020101Bicarbonate-Dependent Detoxification by Mitigating Ammonium-Induced Hypoxic Stress in <i>Triticum aestivum</i> RootXiao Liu0Yunxiu Zhang1Chengming Tang2Huawei Li3Haiyong Xia4Shoujin Fan5Lingan Kong6Crop Research Institute, Shandong Academy of Agricultural Sciences, Jinan 250100, ChinaCrop Research Institute, Shandong Academy of Agricultural Sciences, Jinan 250100, ChinaCrop Research Institute, Shandong Academy of Agricultural Sciences, Jinan 250100, ChinaCrop Research Institute, Shandong Academy of Agricultural Sciences, Jinan 250100, ChinaCrop Research Institute, Shandong Academy of Agricultural Sciences, Jinan 250100, ChinaCollege of Life Science, Shandong Normal University, Jinan 250014, ChinaCrop Research Institute, Shandong Academy of Agricultural Sciences, Jinan 250100, ChinaAmmonium (NH<sub>4</sub><sup>+</sup>) toxicity is ubiquitous in plants. To investigate the underlying mechanisms of this toxicity and bicarbonate (HCO<sub>3</sub><sup>−</sup>)-dependent alleviation, wheat plants were hydroponically cultivated in half-strength Hoagland nutrient solution containing 7.5 mM NO<sub>3</sub><sup>−</sup> (CK), 7.5 mM NH<sub>4</sub><sup>+</sup> (SA), or 7.5 mM NH<sub>4</sub><sup>+</sup> + 3 mM HCO<sub>3</sub><sup>−</sup> (AC). Transcriptomic analysis revealed that compared to CK, SA treatment at 48 h significantly upregulated the expression of genes encoding fermentation enzymes (pyruvate decarboxylase (PDC), alcohol dehydrogenase (ADH), and lactate dehydrogenase (LDH)) and oxygen consumption enzymes (respiratory burst oxidase homologs, dioxygenases, and alternative oxidases), downregulated the expression of genes encoding oxygen transporters (PIP-type aquaporins, non-symbiotic hemoglobins), and those involved in energy metabolism, including tricarboxylic acid (TCA) cycle enzymes and ATP synthases, but upregulated the glycolytic enzymes in the roots and downregulated the expression of genes involved in the cell cycle and elongation. The physiological assay showed that SA treatment significantly increased PDC, ADH, and LDH activity by 36.69%, 43.66%, and 61.60%, respectively; root ethanol concentration by 62.95%; and lactate efflux by 23.20%, and significantly decreased the concentrations of pyruvate and most TCA cycle intermediates, the complex V activity, ATP content, and ATP/ADP ratio. As a consequence, SA significantly inhibited root growth. AC treatment reversed the changes caused by SA and alleviated the inhibition of root growth. In conclusion, NH<sub>4</sub><sup>+</sup> treatment alone may cause hypoxic stress in the roots, inhibit energy generation, suppress cell division and elongation, and ultimately inhibit root growth, and adding HCO<sub>3</sub><sup>−</sup> remarkably alleviates the NH<sub>4</sub><sup>+</sup>-induced inhibitory effects on root growth largely by attenuating the hypoxic stress.https://www.mdpi.com/2079-7737/13/2/101dioxygenasefermentationrootTCA cyclewheat |
| spellingShingle | Xiao Liu Yunxiu Zhang Chengming Tang Huawei Li Haiyong Xia Shoujin Fan Lingan Kong Bicarbonate-Dependent Detoxification by Mitigating Ammonium-Induced Hypoxic Stress in <i>Triticum aestivum</i> Root Biology dioxygenase fermentation root TCA cycle wheat |
| title | Bicarbonate-Dependent Detoxification by Mitigating Ammonium-Induced Hypoxic Stress in <i>Triticum aestivum</i> Root |
| title_full | Bicarbonate-Dependent Detoxification by Mitigating Ammonium-Induced Hypoxic Stress in <i>Triticum aestivum</i> Root |
| title_fullStr | Bicarbonate-Dependent Detoxification by Mitigating Ammonium-Induced Hypoxic Stress in <i>Triticum aestivum</i> Root |
| title_full_unstemmed | Bicarbonate-Dependent Detoxification by Mitigating Ammonium-Induced Hypoxic Stress in <i>Triticum aestivum</i> Root |
| title_short | Bicarbonate-Dependent Detoxification by Mitigating Ammonium-Induced Hypoxic Stress in <i>Triticum aestivum</i> Root |
| title_sort | bicarbonate dependent detoxification by mitigating ammonium induced hypoxic stress in i triticum aestivum i root |
| topic | dioxygenase fermentation root TCA cycle wheat |
| url | https://www.mdpi.com/2079-7737/13/2/101 |
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