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Acta Agronomica Sinica ›› 2021, Vol. 47 ›› Issue (11): 2268-2277.doi: 10.3724/SP.J.1006.2021.04237

• TILLAGE & CULTIVATION·PHYSIOLOGY & BIOCHEMISTRY • Previous Articles     Next Articles

Effects of maize and soybean intercropping on nodule growth, nitrogen fixation of soybean under low phosphorus condition

QIN Xiao-Min1(), PAN Hao-Nan1, XIAO Jing-Xiu1, TANG Li1, ZHENG Yi1,2,*()   

  1. 1Yunnan Agricultural University, Kunming 650201, Yunnan, China
    2Yunnan Open University, Kunming 650599, Yunnan, China
  • Received:2020-10-31 Accepted:2021-03-19 Online:2021-11-12 Published:2021-04-13
  • Contact: ZHENG Yi E-mail:qinxiaomin89@163.com;zhengyi-64@163.com
  • Supported by:
    National Key Research and Development Program of China(2017YFD0200200/207);National Natural Science Foundation of China(31760615);National Natural Science Foundation of China(31760611);National Natural Science Foundation of China(32060718);Science and Technology Talent and Platform of Yunnan Province(2019IC026)

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Abstract:

To investigate the effects of maize and soybean intercropping on nitrogen and phosphorus uptake, nodule growth, and nitrogen fixation in soybean, a pot experiment was conducted with two phosphorus (P) rates (low P -P50 and sufficient P -P100). The results showed that, compared with monocropped soybean, intercropping of soybean and maize significantly increased the nodule number, nodule weight, leghemoglobin content, and nitrogenase activity of nodule, and promoted the growth and nitrogen (N) and phosphorus uptake of soybean under P50 and P100 rates. The concentrations of N, P, and the activities of acid phosphatase, phytase in nodules in intercropped soybean were significantly higher than those of monocropped soybean under P50 and P100 rates, and the activities of acid phosphatase and phytase showed the highest values under IS-P50 treatment. In addition, the P concentration in the nodules of intercropped soybean under P50 rate was significantly higher than that of monocropped soybean under P90 rate. so In summary, to maintain the larger phosphorus content for nitrogen fixation of soybean under phosphorus deficiency, the soybean and maize intercropping system increased the phosphorus concentration in the nodules mainly by enhancing the activities of acid phosphatase and phytase in the nodules, and thus promoted the growth and nitrogen uptake of soybean.

Key words: P rates, maize and soybean intercropping, nodule, nitrogen fixation, N and P uptake

Table 1

Effects of maize and soybean intercropping on soybean growth under different P rates (g plant-1)"

磷水平
P rates		 种植模式
Planting patterns		 叶
Leaf		 茎
Stem		 根
Root		 全株
Whole plant
P50 MS 4.09±0.20 c 4.05±0.32 c 1.16±0.11 d 9.44±0.13 c
IS 7.04±0.69 b 6.76±0.81 b 2.17±0.15 c 16.23±1.16 b
P100 MS 6.39±0.33 b 6.01±0.27 b 2.48±0.18 b 15.04±0.39 b
IS 8.75±0.44 a 8.27±0.63 a 3.52±0.15 a 20.85±0.76 a

Table 2

Effects of intercropping and P rates on growth and nitrogen fixation ability of soybean nodules"

磷水平
P rates		 种植模式
Planting patterns		 根瘤数
Nodule number		 根瘤干重
Nodule dry weight		 豆血红蛋白
Leghemoglobin		 固氮酶活性
Nitrogenase activity
P50 29.04 b 0.197 b 4.56 b 1.53 b
P100 42.88 a 0.245 a 5.74 a 2.02 a
MS 24.92 b 0.155 b 4.76 b 1.62 b
IS 47.00 a 0.287 a 5.55 a 1.92 a
磷水平 P rates (P) ** ** ** **
种植模式 Planting patterns (PP) ** ** ** **
P×PP * ns ns ns

Fig. 1

Effects of intercropping on growth, nitrogen fixation ability of soybean nodules under different P rates Abbreviations and treatments are the same as those given in Table 1. Different uppercase and lowercase letters mean significant difference between monocropping and intercropping at the 0.05 probability level under P50 and P100 rates, respectively."

Table 3

Effects of maize and soybean intercropping on N uptake of soybean different organs under different P rates (mg plant-1)"

磷水平
P rates		 种植模式
Planting patterns		 叶
Leaves		 茎
Stems		 根
Roots		 根瘤
Nodules		 全株
Whole plant
P50 MS 13.76±1.51 a 11.61±1.78 a 1.24±0.09 a 1.22±0.01 a 27.83±1.07 a
IS 25.05±2.46 a 17.31±0.36 a 2.80±0.32 a 2.72±0.19 a 47.88±2.87 a
P100 MS 24.03±1.58 a 21.36±0.61 a 3.41±0.15 a 1.81±0.20 a 50.60±0.97 a
IS 34.63±1.86 a 26.67±2.20 a 5.53±0.24 a 3.59±0.32 a 70.43±3.52 a
施磷量 P rates
P50 19.41 b 14.46 b 2.02 b 1.97 b 37.86 b
P100 29.33 a 24.02 a 4.47 a 2.70 a 60.51 a
种植模式 Planting pattern
MS 18.90 b 16.48 b 2.32 b 1.51 b 39.22 b
IS 29.84 a 21.99 a 4.17 a 3.16 a 59.15 a
显著性 Significance
磷水平 P rates (P) ** ** ** ** **
种植模式 Planting patterns (PP) ** ** ** ** **
P×PP ns ns ns ns ns

Table 4

Effects of maize and soybean intercropping on P uptake of soybean different organs under different P rates (mg plant-1)"

磷水平
P rates		 种植模式
Planting patterns		 叶
Leaves		 茎
Stems		 根
Roots		 根瘤
Nodules		 全株
Whole plant
P50 MS 12.13±0.56 a 7.66±0.78 a 1.75±0.25 a 1.55±0.07 a 23.09±0.61 a
IS 26.39±2.15 a 15.35±1.91 a 4.46±0.47 a 3.55±0.33 a 49.75±0.57 a
P100 MS 23.74±2.18 a 14.41±0.94 a 5.39±0.67 a 2.17±0.24 a 45.71±3.27 a
IS 37.16±1.54 a 22.36±1.79 a 9.32±0.15 a 4.60±0.22 a 73.45±0.43 a
施磷量 P rates
P50 19.26 b 11.50 b 3.11 b 2.55 b 36.42 b
P100 30.45 a 18.39 a 7.36 a 3.38 a 59.58 a
种植模式 Planting pattern
MS 17.93 b 11.04 b 3.57 b 1.88 b 34.40 b
IS 31.78 a 18.85 a 6.89 a 4.08 a 61.60 a
显著性Significance
磷水平 P rates (P) ** ** ** ** **
种植模式 Planting patterns (PP) ** ** ** ** **
P×PP ns ns * ns ns

Table 5

Effects of intercropping and P rates on N and P concentrations of soybean organs"

磷水平
P rates		 种植模式
Planting patterns		 氮素浓度N concentrations 磷素浓度P concentrations
叶Leaf 根系Root 根瘤Nodule 叶Leaf 根系Root 根瘤Nodule
P50 34.58 b 11.86 b 98.07 b 3.36 b 1.78 b 12.63 a
P100 38.58 a 14.73 a 107.98 a 3.98 a 2.41 a 13.43 a
MS 35.57 b 12.28 b 96.75 b 3.34 b 1.84 b 11.93 b
IS 37.59 a 14.31 a 109.30 a 4.01 a 2.35 a 14.14 a
磷水平 P rates (P) ** ** * ** ** ns
种植模式 Planting patterns (PP) * * * ** ** **
P×PP ns ns ns ns ns ns

Fig. 2

Effects of maize and soybean intercropping on N concentration of soybean organs Abbreviations and treatments are the same as those given in Table 1. Different uppercase and lowercase letters mean the significant difference between monocropping and intercropping at the 0.05 probability level under P50 and P100 rates, respectively."

Fig. 3

Effects of maize and soybean intercropping on P concentration of soybean organs under different P rates Abbreviations and treatments are the same as those given in Table 1. Different uppercase and lowercase letters mean the significant difference between monocropping and intercropping at the 0.05 probability level under P50 and P100 rates, respectively."

Table 6

Effects of intercropping and P rates on enzyme activities of soybean organs"

磷水平
P rates		 种植模式
Planting patterns		 酸性磷酸酶Acid phosphatase 植酸酶Phytase
叶Leaf 根系Root 根瘤Nodule 叶Leaf 根系Root 根瘤Nodule
P50 21.19 a 7.74 a 28.89 a 37.17 a 10.00 a 52.84 a
P100 18.37 b 6.38 b 25.35 b 26.67 b 7.80 b 40.56 b
MS 18.48 b 6.22 b 25.60 b 29.45 b 8.18 b 43.67 b
IS 21.07 a 7.90 a 28.64 a 34.40 a 9.62 a 49.73 a
磷水平 P rates (P) ** ** ** ** ** **
种植模式 Planting patterns (PP) ** ** ** ** ** **
P×PP ns ns ns ns ns ns

Fig. 4

Effects of maize and soybean intercropping on enzyme activities of soybean organs under different P rates Abbreviations and treatments are the same as those given in Table 1. Different uppercase and lowercase letters mean significant difference between monocropping and intercropping at the 0.05 probability level under P50 and P100 rates, respectively."

[1] Cordell D, White S. Life’s bottleneck: sustaining the world’s phosphorus for a food secure future. Annu Rev Environ Resour, 2014, 39: 161-188.
doi: 10.1146/annurev-environ-010213-113300
[2] Zhang Z L, Liao H, Lucas W J. Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants. J Integr Plant Biol, 2014, 56: 192-220.
doi: 10.1111/jipb.12163
[3] 李杰, 石元亮, 陈智文. 我国南方红壤磷素研究概况. 土壤通报, 2011, 42: 763-768.
Li J, Shi Y L, Chen Z W. Research on phosphorus in southern red soils in China. Chin J Soil Sci, 2011, 42: 763-768 (in Chinese with English abstract).
[4] 苗淑杰, 乔云发, 韩晓增, 王树起, 李海波. 缺磷对已结瘤大豆生长和固氮功能的影响. 作物学报, 2009, 35: 1344-1349.
Miao S J, Qiao Y F, Han X Z, Wang S Q, Li H B. Effects of phosphorus deficiency on growth and nitrogen fixation of soybean after nodule formation. Acta Agron Sin, 2009, 35: 1344-1349 (in Chinese with English abstract).
[5] Vardien W, Mesjasz-Przybylowicz J, Przybylowicz W, Wang Y D, Steenkamp E T, Valentine A J. Nodules from Fynbos legume Virgilia divaricata have high functional plasticity under variable P supply levels. J Plant Physiol, 2014, 171: 1732-1739.
doi: 10.1016/j.jplph.2014.08.005
[6] Valentine A J, Kleinert A, Benedito V A. Adaptive strategies for nitrogen metabolism in phosphate deficient legume nodules. Plant Sci, 2017, 256: 46-52.
doi: S0168-9452(16)30891-3 pmid: 28167037
[7] Wen Z H, Li H B, Tang X M, Xiong C Y, Li H G, Pang J Y, Ryan M H, Lambers H, Shen J B. Trade-offs among root morphology, exudation and mycorrhizal symbioses for phosphorus-acquisition strategies of 16 crop species. New Phytol, 2019, 223: 882-895.
doi: 10.1111/nph.2019.223.issue-2
[8] 张丽梅, 郭再华, 张琳, 贺立源. 缺磷对不同耐低磷玉米基因型酸性磷酸酶活性的影响. 植物营养与肥料学报, 2015, 21: 898-910.
Zhang L M, Guo Z H, Zhang L, He L Y. Effects of phosphate deficiency on acid phosphatase activities of different maize genotypes tolerant to low P stress. J Plant Nutr Fert, 2015, 21: 898-910 (in Chinese with English abstract).
[9] Magadlela A, Kleinert A, Dreyer L L, Valentine A. Low-phosphorus conditions affect the nitrogen nutrition and associated carbon costs of two legume tree species from a Mediterranean-type ecosystem. Aust J Bot, 2014, 62: 1-9.
doi: 10.1071/BT13264
[10] Magadlela A, Beukes C, Venter F, Steenkamp E, Valentine A. Does P deficiency affect nodule bacterial composition and N source utilization in a legume from nutrient-poor Mediterranean-type ecosystems? Soil Biol Biochem, 2017, 104: 164-174.
doi: 10.1016/j.soilbio.2016.10.021
[11] Thuynsma R, Valentine A, Kleinert A. Phosphorus deficiency affects the allocation of below-ground resources to combined cluster roots and nodules in Lupinus albus. J Plant Physiol, 2013, 173: 1-7.
[12] Lazali M, Bargaz A, Carlsson G, Ounane S M, Drevon J J. Discrimination against 15N among recombinant inbred lines of Phaseolus vulgaris L. contrasting in phosphorus use efficiency for nitrogen fixation. J Plant Physiol, 2014, 171: 199-204.
doi: 10.1016/j.jplph.2013.07.009
[13] Ahmed A, Aftab S, Hussain S, Cheema H N, Liu W G, Yang F, Yang W Y. Nutrient accumulation and distribution assessment in response to potassium application under maize-soybean intercropping system. Agronomy, 2020, 10: 725-731.
doi: 10.3390/agronomy10050725
[14] Li B, Li Y Y, Wu H M, Zhang F F, Li C J, Li X X, Lambers H, Li L. Root exudates drive interspecific facilitation by enhancing nodulation and N2 fixation. Proc Natl Acad Sci USA, 2016, 113: 6496-6501.
doi: 10.1073/pnas.1523580113
[15] Zhang D, Zhang C, Tang X, Li H G, Zhang F S, Rengel Z, Whalley W R, Davies W J, Shen J B. Increased soil phosphorus availability induced by faba bean root exudation stimulates root growth and phosphorus uptake in neighbouring maize. New Phytol, 2016, 209: 823-831.
doi: 10.1111/nph.2016.209.issue-2
[16] 左元梅, 刘永秀, 张福锁. 与玉米混作改善花生铁营养对其根瘤形态结构及豆血红蛋白含量的影响. 植物生理与分子生物学学报, 2003, 29: 33-38.
Zuo Y M, Liu Y X, Zhang F S. Effects of improvement of iron nutrition by mixed cropping with maize on nodule microstructure and leghemoglobin content of peanut. J Plant Physiol Mol Biol, 2003, 29: 33-38 (in Chinese with English abstract).
[17] Hu F, Zhao C, Feng F C, Chai Q, Mu Y P, Zhang Y. Improving N management through intercropping alleviates the inhibitory effect of mineral N on nodulation in pea. Plant Soil, 2017, 412: 235-251.
doi: 10.1007/s11104-016-3063-2
[18] Liu Y C, Yin X H, Xiao J X, Tang L, Zheng Y. Interactive influences of intercropping by nitrogen on flavonoid exudation and nodulation in faba bean. Sci Rep, 2019, 9: 1-11.
[19] Li B, Li Y Y, Wu H M, Zhang F F, Li L. Root exudates drive interspecific facilitation by enhancing nodulation and N2 fixation. Proc Natl Acad Sci USA, 2016, 113: 6496-6501.
doi: 10.1073/pnas.1523580113
[20] Liu Y C, Qin X M, Xiao J X, Tang L, Wei C Z, Wei J J, Zheng Y. Intercropping influences component and content change of flavonoids in root exudates and nodulation of Faba bean. J Plant Interact, 2017, 12: 187-192.
doi: 10.1080/17429145.2017.1308569
[21] 赵雅姣, 刘晓静, 童长春, 吴勇. 紫花苜蓿/玉米间作对紫花苜蓿结瘤固氮特性的影响. 草业学报, 2020, 29(1):95-105.
Zhao Y J, Liu X J, Tong C C, Wu Y. Factors influencing nodulation and N fixation ability of alfalfa in a simulated alfalfa/maize intercropping system. Acta Pratac Sin, 2020, 29(1):95-105 (in Chinese with English abstract).
[22] Esfahani M N, Kusano M, Nguyen K H, Watanabe Y, Ha C V, Saito K, Sulieman S, Herrera-Estrella L, Tran L S P. Adaptation of the symbiotic Mesorhizobium-chickpea relationship to phosphate deficiency relies on reprogramming of whole-plant metabolism. Proc Natl Acad Sci USA, 2016, 22: 4610-4619.
[23] Chen Z J, Cui Q Q, Liang C Y, Sun L L, Tian J, Liao H. Identification of differentially expressed proteins in soybean nodules under phosphorus deficiency through proteomic analysis. Proteomics, 2011, 11: 4648-4659.
doi: 10.1002/pmic.v11.24
[24] 齐敏兴, 刘晓静, 张晓磊, 刘艳楠. 不同磷水平对紫花苜蓿光合作用和根瘤固氮特性的影响. 草地学报, 2013, 21: 512-516.
Qi M X, Liu X J, Zhang X L, Liu Y N. Effects of different phosphorus levels on photosynthesis and root nodule nitrogen-fixing characteristic of alfalfa. Acta Agrest Sin, 2013, 21: 512-516 (in Chinese with English abstract).
[25] Sulieman S, Tran L S P. Phosphorus homeostasis in legume nodules as an adaptive strategy to phosphorus deficiency. Plant Sci, 2015, 221: 1-8.
[26] Sulieman S, Van Ha C, Schulze J, Tran L S P. Growth and nodulation of symbiotic Medicago truncatula at different levels of phosphorus availability. J Exp Bot, 2013, 64: 2701-2712.
doi: 10.1093/jxb/ert122 pmid: 23682114
[27] Schulze J, Temple G, Temple S J, Beschow H, Vance C P. Nitrogen fixation by white lupin under phosphorus deficiency. Ann Bot, 2006, 98: 731-740.
doi: 10.1093/aob/mcl154
[28] Lu M Y, Cheng Z Y, Zhang X M, Huang P H, Fan C M, Yu G L, Chen F L, Xu K, Chen Q S, Miao Y C, Han Y Z, Feng X Z, Liu L Y, Fu Y F. Spatial divergence of PHR-PHT1 modules maintains phosphorus homeostasis in soybean nodules. Plant Physiol, 2020, 10: 1-19.
[29] Bargaz A, Faghire M, Abdi N, Farissi M, Sifi B, Drevon J J, Ikbal M C, Ghoulam C. Low soil phosphorus availability increases acid phosphatases activities and affects P partitioning in nodules, seeds and rhizosphere of Phaseolus vulgaris. Agriculture, 2012, 2: 139-153.
doi: 10.3390/agriculture2020139
[30] Lazali M, Drevon J J. Role of acid phosphatase in the tolerance of the rhizobial symbiosis with legumes to phosphorus deficiency. Symbiosis, 2018, 76: 221-228.
doi: 10.1007/s13199-018-0552-5
[31] Araújo A P, Plassard C, Drevon J J. Phosphatase and phytase activities in nodules of common bean genotypes at different levels of phosphorus supply. Plant Soil, 2008, 312: 129-138.
doi: 10.1007/s11104-008-9595-3
[32] Lazali M, Zaman-Allah M, Amenc L, Ounane G, Abadie J, Drevon J J. A phytase gene is overexpressed in root nodules cortex of Phaseolus vulgaris-rhizobia symbiosis under phosphorus deficiency. Planta, 2013, 238: 317-324.
doi: 10.1007/s00425-013-1893-1
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