Responses of Nitrogen Metabolism Pathways to Low-Phosphorus Stress: Decrease in Nitrogen Accumulation and Alterations in Protein Metabolism in Soybeans
Abstract
1. Introduction
2. Materials and Methods
2.1. Plant Materials and Sampling
2.2. Measurement and Calculation Methods
2.3. Soluble Protein Content Detection
2.4. Real-Time Quantitative PCR Analysis
2.5. Metabolites Extraction
2.6. UHPLC-MS/MS Analysis
2.7. Precision and Accuracy
3. Results
3.1. Changes of Nitrogen Accumulation of Soybean Plants Under Low-P Stress
3.2. 15N Abundance of Soybean Plants Under Low-P Stress
3.3. Changes in Nodule Nitrogen Fixation Accumulation and Ratio of Nodule Nitrogen Fixation of Soybean Plants Under Low-P Stress
3.4. Effect of Low-P Stress on Soluble Protein Content of Soybean
3.5. Effect of Low-P Stress on PTs of Soybean
3.6. Effect of Low-P Stress on Amino Acid Metabolism in Soybean
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Treatments | Aboveground | Root | Nodule | ||||
---|---|---|---|---|---|---|---|
2022 | 2023 | 2022 | 2023 | 2022 | 2023 | ||
7 days | P1 | 23.98 ± 0.21 * | 31.78 ± 1.67 * | 9.53 ± 0.10 * | 9.54 ± 0.10 * | 1.22 ± 0.00 * | 1.19 ± 0.08 * |
P31 | 39.49 ± 0.47 | 66.90 ± 1.82 | 10.73 ± 0.16 | 10.73 ± 0.16 | 5.39 ± 0.12 | 8.82 ± 0.34 | |
14 days | P1 | 29.78 ± 0.49 * | 47.68 ± 1.02 * | 16.74 ± 0.01 * | 9.94 ± 0.24 * | 1.53 ± 0.00 * | 2.56 ± 0.05 * |
P31 | 90.78 ± 2.70 | 92.42 ± 1.97 | 19.60 ± 0.15 | 14.17 ± 0.13 | 11.20 ± 0.46 | 8.49 ± 0.06 | |
21 days | P1 | 48.26 ± 3.11 * | 46.48 ± 0.75 * | 18.96 ± 0.96 * | 17.09 ± 0.21 * | 1.23 ± 0.12 * | 2.67 ± 0.14 * |
P31 | 143.23 ± 7.02 | 225.48 ± 3.62 | 37.99 ± 0.08 | 44.90 ± 2.57 | 26.82 ± 0.21 | 24.64 ± 0.30 | |
28 days | P1 | 75.03 ± 2.98 * | 63.15 ± 0.12 * | 25.38 ± 1.12 * | 20.02 ± 1.04 * | 2.23 ± 0.04 * | 2.67 ± 0.17 * |
P31 | 248.56 ± 14.83 | 325.61 ± 8.05 | 66.41 ± 1.26 | 76.50 ± 2.38 | 33.59 ± 1.18 | 24.87 ± 1.04 | |
35 days | P1 | 102.52 ± 0.27 * | 97.70 ± 3.49 * | 41.52 ± 1.04 * | 22.74 ± 1.28 * | 3.65 ± 0.35 * | 2.69 ± 0.23 * |
P31 | 403.80 ± 14.93 | 476.66 ± 2.02 | 92.52 ± 2.31 | 90.20 ± 1.73 | 37.02 ± 0.39 | 36.22 ± 0.68 | |
42 days | P1 | 186.66 ± 0.59 * | 175.45 ± 1.29 * | 53.08 ± 1.68 * | 58.64 ± 0.16 * | 6.69 ± 0.04 * | 2.92 ± 0.21 * |
P31 | 425.70 ± 2.87 | 464.67 ± 5.73 | 89.55 ± 6.04 | 140.15 ± 1.13 | 40.09 ± 0.65 | 30.95 ± 1.67 | |
49 days | P1 | 302.11 ± 0.88 * | 271.70 ± 5.51 * | 92.58 ± 0.19 * | 87.96 ± 4.19 * | 11.23 ± 0.07 * | 5.58 ± 0.23 * |
P31 | 446.68 ± 1.03 | 684.25 ± 7.95 | 117.42 ± 1.36 | 108.26 ± 2.85 | 46.79 ± 0.77 | 25.94 ± 1.39 |
Treatments | Aboveground | Root | Nodule | ||||
---|---|---|---|---|---|---|---|
2022 | 2023 | 2022 | 2023 | 2022 | 2023 | ||
7 days | P1 | 1.89 ± 0.01 | 1.91 ± 0.00 | 2.11 ± 0.04 * | 2.02 ± 0.01 | 0.91 ± 0.00 * | 1.02 ± 0.02 * |
P31 | 1.91 ± 0.02 | 1.94 ± 0.02 | 1.80 ± 0.00 | 1.81 ± 0.05 | 1.21 ± 0.01 | 0.78 ± 0.00 | |
14 days | P1 | 2.08 ± 0.00 * | 2.17 ± 0.02 | 2.22 ± 0.02 | 2.33 ± 0.05 | 1.00 ± 0.03 * | 1.18 ± 0.05 * |
P31 | 1.84 ± 0.01 | 2.00 ± 0.04 | 2.12 ± 0.04 | 2.13 ± 0.01 | 0.62 ± 0.00 | 0.78 ± 0.03 | |
21 days | P1 | 2.31 ± 0.00 * | 2.28 ± 0.04 * | 2.29 ± 0.03 * | 2.23 ± 0.03 * | 1.01 ± 0.04 * | 1.21 ± 0.00 * |
P31 | 1.33 ± 0.06 | 1.30 ± 0.03 | 1.71 ± 0.02 | 1.76 ± 0.01 | 0.51 ± 0.03 | 0.44 ± 0.00 | |
28 days | P1 | 2.42 ± 0.00 * | 2.31 ± 0.03 * | 2.40 ± 0.00 * | 2.35 ± 0.03 * | 1.28 ± 0.02 * | 1.06 ± 0.01 * |
P31 | 1.17 ± 0.02 | 1.55 ± 0.03 | 1.61 ± 0.01 | 2.00 ± 0.00 | 0.50 ± 0.00 | 0.53 ± 0.02 | |
35 days | P1 | 2.45 ± 0.02 * | 2.43 ± 0.01 * | 2.44 ± 0.01 * | 2.44 ± 0.03 * | 1.00 ± 0.03 * | 1.40 ± 0.01 * |
P31 | 1.20 ± 0.01 | 1.60 ± 0.00 | 1.75 ± 0.00 | 1.98 ± 0.03 | 0.57 ± 0.01 | 0.59 ± 0.04 | |
42 days | P1 | 2.27 ± 0.08 * | 2.58 ± 0.02 * | 2.47 ± 0.05 * | 2.63 ± 0.00 * | 0.80 ± 0.01 * | 1.08 ± 0.04 * |
P31 | 1.23 ± 0.00 | 1.72 ± 0.01 | 1.68 ± 0.00 | 2.07 ± 0.00 | 0.55 ± 0.00 | 0.53 ± 0.00 | |
49 days | P1 | 2.20 ± 0.05 * | 2.38 ± 0.06 * | 2.41 ± 0.03 * | 2.49 ± 0.04 * | 0.77 ± 0.03 * | 0.89 ± 0.08 * |
P31 | 1.18 ± 0.01 | 1.72 ± 0.06 | 1.66 ± 0.02 | 2.06 ± 0.06 | 0.46 ± 0.00 | 0.53 ± 0.03 |
Treatments | Aboveground | Root | Nodule | ||||
---|---|---|---|---|---|---|---|
2022 | 2023 | 2022 | 2023 | 2022 | 2023 | ||
7 days | P1 | 10.26 ± 0.17 * | 11.76 ± 0.00 * | 5.86 ± 0.11 | 3.18 ± 0.02 * | 0.89 ± 0.00 * | 0.79 ± 0.06 * |
P31 | 16.67 ± 0.51 | 24.11 ± 0.15 | 5.42 ± 0.02 | 4.33 ± 0.13 | 3.42 ± 0.06 | 6.54 ± 0.26 | |
14 days | P1 | 10.99 ± 0.11 * | 13.54 ± 0.71 * | 5.50 ± 0.09 * | 2.31 ± 0.11 * | 1.07 ± 0.01 * | 1.57 ± 0.01 * |
P31 | 40.34 ± 1.59 | 31.33 ± 0.79 | 7.01 ± 0.22 | 4.22 ± 0.09 | 9.10 ± 0.37 | 6.32 ± 0.15 | |
21 days | P1 | 14.56 ± 0.79 * | 11.49 ± 0.50 * | 5.81 ± 0.11 * | 4.53 ± 0.11 * | 0.86 ± 0.10 * | 1.61 ± 0.08 * |
P31 | 85.36 ± 1.55 | 128.9 ± 0.50 | 18.31 ± 0.28 | 18.81 ± 0.86 | 22.70 ± 0.43 | 21.08 ± 0.19 | |
28 days | P1 | 20.06 ± 0.71 * | 15.03 ± 0.75 * | 6.94 ± 0.29 * | 4.50 ± 0.03 * | 1.37 ± 0.04 * | 1.73 ± 0.12 * |
P31 | 160.14 ± 7.94 | 159.62 ± 7.75 | 34.13 ± 0.87 | 26.14 ± 0.80 | 28.49 ± 0.97 | 20.55 ± 1.02 | |
35 days | P1 | 26.56 ± 0.75 * | 19.61 ± 1.10 * | 10.80 ± 0.82 * | 4.46 ± 0.02 * | 2.54 ± 0.21 * | 1.44 ± 0.11 * |
P31 | 256.88 ± 7.70 | 225.39 ± 2.39 | 43.48 ± 1.31 | 31.36 ± 1.50 | 30.63 ± 0.50 | 29.12 ± 0.02 | |
42 days | P1 | 58.44 ± 1.28 * | 26.11 ± 1.54 * | 13.38 ± 0.37 * | 7.83 ± 0.82 * | 5.07 ± 0.00 * | 1.88 ± 0.09 * |
P31 | 267.45 ± 1.61 | 200.22 ± 4.51 | 44.03 ± 1.14 | 44.77 ± 0.50 | 33.43 ± 0.59 | 25.55 ± 1.31 | |
49 days | P1 | 101.24 ± 4.32 * | 58.84 ± 6.80 * | 24.97 ± 1.04 * | 15.85 ± 0.32 * | 8.62 ± 0.05 * | 3.96 ± 0.31 * |
P31 | 287.07 ± 2.21 | 295.93 ± 11.39 | 58.63 ± 1.56 | 34.78 ± 1.55 | 40.28 ± 0.54 | 21.48 ± 1.43 |
Treatments | Aboveground | Root | Nodule | ||||
---|---|---|---|---|---|---|---|
2022 | 2023 | 2022 | 2023 | 2022 | 2023 | ||
7 days | P1 | 42.79 ± 0.32 | 37.01 ± 0.14 | 36.05 ± 1.49 * | 33.37 ± 0.56 * | 72.41 ± 0.16 * | 66.49 ± 0.56 * |
P31 | 42.18 ± 0.78 | 36.09 ± 0.74 | 45.57 ± 0.16 | 40.40 ± 1.88 | 63.53 ± 0.34 | 74.16 ± 0.08 | |
14 days | P1 | 36.93 ± 0.21 * | 28.35 ± 0.88 * | 32.85 ± 0.61 | 23.36 ± 1.77 * | 69.86 ± 1.05 * | 61.27 ± 1.67 * |
P31 | 44.42 ± 0.42 | 33.97 ± 1.59 | 35.80 ± 1.43 | 29.72 ± 0.25 | 81.29 ± 0.06 | 74.39 ± 1.30 | |
21 days | P1 | 30.20 ± 0.03 * | 24.76 ± 1.47 * | 30.76 ± 0.94 * | 26.54 ± 1.02 * | 69.54 ± 1.26 * | 60.23 ± 0.13 * |
P31 | 59.78 ± 1.87 | 57.20 ± 1.14 | 48.20 ± 0.84 | 41.95 ± 0.48 | 84.63 ± 0.93 | 85.57 ± 0.26 | |
28 days | P1 | 26.75 ± 0.11 * | 23.80 ± 1.15 * | 27.35 ± 0.05 * | 22.60 ± 1.02 * | 61.31 ± 0.77 * | 64.94 ± 0.61 * |
P31 | 64.50 ± 0.65 | 48.96 ± 1.16 | 51.38 ± 0.34 | 34.17 ± 0.01 | 84.83 ± 0.07 | 82.56 ± 0.67 | |
35 days | P1 | 25.90 ± 0.70 * | 20.04 ± 0.41 * | 26.13 ± 0.56 * | 19.75 ± 1.02 * | 69.88 ± 0.93 * | 53.78 ± 0.57 * |
P31 | 63.65 ± 0.44 | 47.44 ± 0.31 | 46.98 ± 0.24 | 34.72 ± 0.99 | 82.73 ± 0.48 | 80.45 ± 1.45 | |
42 days | P1 | 31.32 ± 0.24 * | 14.87 ± 0.77 * | 25.31 ± 1.51 * | 13.35 ± 0.07 * | 75.71 ± 0.46 * | 64.44 ± 1.51 * |
P31 | 62.83 ± 0.04 | 43.17 ± 0.44 | 49.14 ± 0.19 | 31.94 ± 0.09 | 83.37 ± 0.12 | 82.56 ± 0.21 | |
49 days | P1 | 33.52 ± 1.51 * | 21.57 ± 2.00 * | 26.97 ± 1.08 * | 17.88 ± 1.47 * | 76.73 ± 0.96 * | 70.75 ± 2.67 * |
P31 | 64.27 ± 0.34 | 43.30 ± 2.16 | 49.91 ± 0.75 | 32.25 ± 2.28 | 86.09 ± 0.27 | 82.67 ± 1.09 |
Pathway | Compounds | Upregulated | Downregulated | |
---|---|---|---|---|
P1_Leaf_7d-P31_Leaf_7d | 37 | 26 | 15 | 11 |
P1_Leaf_14d-P31_Leaf_14d | 37 | 26 | 17 | 9 |
P1_Leaf_21d-P31_Leaf_21d | 37 | 26 | 19 | 7 |
P1_Root_7d-P31_Root_7d | 37 | 26 | 18 | 8 |
P1_Root_14d-P31_Root_14d | 37 | 26 | 14 | 12 |
P1_Root_21d-P31_Root_21d | 37 | 26 | 13 | 13 |
P1_Nodule_7d-P31_Nodule_7d | 37 | 26 | 18 | 8 |
P1_Nodule_14d-P31_Nodule_14d | 37 | 26 | 19 | 7 |
P1_Nodule_21d-P31_Nodule_21d | 37 | 26 | 12 | 14 |
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Yao, Y.; Liu, X. Responses of Nitrogen Metabolism Pathways to Low-Phosphorus Stress: Decrease in Nitrogen Accumulation and Alterations in Protein Metabolism in Soybeans. Agronomy 2025, 15, 836. https://doi.org/10.3390/agronomy15040836
Yao Y, Liu X. Responses of Nitrogen Metabolism Pathways to Low-Phosphorus Stress: Decrease in Nitrogen Accumulation and Alterations in Protein Metabolism in Soybeans. Agronomy. 2025; 15(4):836. https://doi.org/10.3390/agronomy15040836
Chicago/Turabian StyleYao, Yubo, and Xinlei Liu. 2025. "Responses of Nitrogen Metabolism Pathways to Low-Phosphorus Stress: Decrease in Nitrogen Accumulation and Alterations in Protein Metabolism in Soybeans" Agronomy 15, no. 4: 836. https://doi.org/10.3390/agronomy15040836
APA StyleYao, Y., & Liu, X. (2025). Responses of Nitrogen Metabolism Pathways to Low-Phosphorus Stress: Decrease in Nitrogen Accumulation and Alterations in Protein Metabolism in Soybeans. Agronomy, 15(4), 836. https://doi.org/10.3390/agronomy15040836