Exogenous addition of nitrate nitrogen regulates the uptake and translocation of lead (Pb) by Iris lacteal Pall. var. chinensis (Fisch.) Koidz.
SUN Mengjie1, GUO Shiwen2, XIONG Chunlian3, LI Pinfang1,*()
1College of Land Science and Technology, China Agricultural University, Beijing 100193, China 2College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, China 3Yibin Ecological Environment Monitoring Center, Sichuan 644099, China
Since Pb is a non-biodegradable inorganic pollutant and a non-essential metal, its long-term presence in soil poses a great threat to the environment. Iris lactea Pall. var. chinensis (Fisch.) Koidz., a perennial dense bush herb with high resistance of Pb and wide adaptability, was used in pot experiments to study the effects of exogenous nitrate N (NO−3−N) on the absorption and transportation of Pb and plant growth under different Pb concentrations. Then, the mechanism of NO−3−N affecting Pb and nutrient uptake and transport was explored. The concentration of Pb in the experiment ranged from 0 to 1600 mg/kg, and the added concentration of NO−3−N was 0.0-0.3 g/kg. The results showed that I. lactea was highly tolerant to Pb, and the shoot fraction was more sensitive to varied Pb concentrations in the soil than the root fraction. This protective function became more pronounced under the condition of raised Pb concentration in the soil. When the concentration of Pb in the soil reached 800 mg/kg, the highest Pb content of I. lactea was found under the condition of 0.1 g/kg of NO−3−N addition. When Pb concentration in the soil increased to 1600 mg/kg, the increase in NO−3−N addition promoted Pb uptake by the root. To ensure the well growth of I. lactea and the effect of remediation of Pb-contaminated soil, the recommended concentration of NO−3−N in the soil is 0.1 g/kg. This result provides a theoretical basis for exogenous N regulation of phytoremediation of Pb-contaminated soil.
SUN Mengjie, GUO Shiwen, XIONG Chunlian, LI Pinfang. Exogenous addition of nitrate nitrogen regulates the uptake and translocation of lead (Pb) by Iris lacteal Pall. var. chinensis (Fisch.) Koidz.. Journal of Arid Land, 2023, 15(2): 218-230.
Taking 1 g of air dried soil into a 100-mL centrifuge tube, adding 40 mL of 0.11 mol/L HOAc, shaking at 22°C (±5°C) for 16 h, centrifuging for 20 min at 3000 r/min, and then transferring the supernatant to a polyethylene bottle.
2
Reducible
Adding 40 mL of 0.5 mol/L NH2OH•HCl (pH 1.5) solution containing 25 mL HNO3 to the solid residue in step 1, shaking at 22°C (±5°C) for 16 h, centrifuging for 20 min at 3000 r/min, and then transferring the supernatant to a polyethylene bottle.
3
Oxidizable
Adding 10 mL of 8.8 mol/L H2O2 (pH 2-3) to the solid residue in step 2, keeping at room temperature for 1 h, and water bathing at 85°C (±2°C) for 1 h. When heated to a volume less than 3 mL, adding another 10 mL of H2O2, then water bathing at 85°C (±2°C) for 1 h. When heating to a volume less than 1 mL, adding 50 mL of 1 mol/L NH4OAc (pH 2), centrifuging for 20 min at 3000 r/min, and then transferring the supernatant to a polyethylene bottle.
4
Residual
Differential subtraction method.
Table 3 BCR (Bureau of Reference, European Community) three-step sequential extraction procedure
Fig. 1Biomass of Iris lactea in lead (Pb)-contaminated soil with exogenous nitrate nitrogen (NO−3−N). CK, 0.0 g/kg Pb and N; N0, 0.0 g/kg; N1, 0.1 g/kg, N2, 0.2 g/kg; N3, 0.3 g/kg; Pb0, 0 mg/kg; Pb1, 800 mg/kg; Pb2, 1600 mg/kg. (a), Pb0 treatment; (b), Pb1 treatment; (c), Pb2 treatment. The detailed treatment of Pb and N is shown in Table 2. Different lowercase letters within the same Pb treatment indicate significant differences among different N treatments in root or shoot at P<0.05 level according to Tukey's test. Bars are standard errors.
Fig. 2pH value varied in Pb-contaminated soil with exogenous nitrate nitrogen (NO−3−N). CK, 0.0 g/kg Pb and N; N0, 0.0 mg/kg; N1, 0.1 g/kg, N2, 0.2 g/kg; N3, 0.3 g/kg; Pb0, 0 mg/kg; Pb1, 800 mg/kg; Pb2, 1600 mg/kg. The detailed treatment is shown in Table 2. Different lowercase letters within the same Pb treatment denote significant differences among different N treatments at P<0.05 level according to Tukey's test. Bars are standard errors.
Fig. 3Transformation of lead (Pb) and proportions in different forms with exogenous nitrate nitrogen (NO−3−N). N0, 0.0 mg/kg; N1, 0.1 g/kg, N2, 0.2 g/kg; N3, 0.3 g/kg; Pb1, 800 mg/kg; Pb2, 1600 mg/kg. (a), Pb1 treatment; (b), Pb2 treatment. The detailed treatment is shown in Table 2. Different lowercase letters within the same Pb treatment denote significant differences among different forms of Pb at P<0.05 level according to Tukey's test. Bars are standard errors.
Fig. 4Lead (Pb) content of Iris lactea in Pb-contaminated soil with exogenous nitrate nitrogen (NO−3−N). N0, 0.0 mg/kg; N1, 0.1 g/kg, N2, 0.2 g/kg; N3, 0.3 g/kg; Pb1, 800 mg/kg; Pb2, 1600 mg/kg. (a), Pb1 treatment; (b), Pb2 treatment. The detailed treatment is shown in Table 2. Different lowercase letters within the same Pb treatment denote significant differences among different N treatments at P<0.05 level according to Tukey's test. Bars are standard errors.
Fig. 5Lead (Pb) accumulation content of Iris lactea in Pb-contaminated soil with exogenous nitrate nitrogen (NO−3−N). N0, 0.0 mg/kg; N1, 0.1 g/kg, N2, 0.2 g/kg; N3, 0.3 g/kg; Pb1, 800 mg/kg; Pb2, 1600 mg/kg. (a), Pb1 treatment; (b) Pb2 treatment. The detailed treatment is shown in Table 2. Different lowercase letters within the same Pb treatment denote significant differences among different N treatments at P<0.05 level according to Tukey's test. Bars are standard errors.
Fig. 6Correlations of Iris lactea growth with absorption and transport of Pb. *, P<0.05 level.
NO−3−N treatment
Pb0
Pb1
Pb2
N0
0.4988
0.5093
0.5202
N1
0.5221
0.4553
0.5300
N2
0.5485
0.4874
0.5584
N3
0.5889
0.4887
0.5672
Table S1 Effect of NO−3−N on root/shoot ratio of Iris lactea in Pb-contaminated soil
Nutrient element
Nitrate nitrogen treatment
Content in shoot (g/kg)
Content in root (g/kg)
Pb0
Pb1
Pb2
Pb0
Pb1
Pb2
N
N0
20.82±1.52c
20.49±1.36b
15.60±1.34b
9.57±1.02a
10.46±0.33b
8.60±1.33b
N1
23.89±0.89a
21.12±0.90b
18.15±1.42a
9.55±1.14 a
10.69±0.31b
9.55±1.89a
N2
22.77±0.33ab
24.61±0.75a
17.52±0.57ab
10.55±1.02a
13.70±0.20 a
9.96±1.00ab
N3
22.12±1.47ab
16.36±0.91c
17.12±0.01ab
11.24±0.51a
13.54±3.06 c
10.17±0.70ab
P
N0
6.19±0.45a
4.65±0.16b
10.71±3.62ab
10.28±1.16ab
7.53±0.47a
8.58±2.23a
N1
6.27±0.29a
6.72±0.69b
8.79±0.26ab
17.32±7.66a
8.29±0.91a
6.37±0.39a
N2
6.19±0.07a
6.81±1.02b
13.47±3.43a
2.82±0.38b
8.69±0.68a
6.73±0.48a
N3
6.46±0.06a
12.77±1.70a
4.47±0.04b
7.56±0.15b
8.64±0.54a
8.38±0.52a
K
N0
31.33±0.18a
34.97±1.07a
32.94±0.59a
10.58±0.13b
12.70±0.76ab
12.48±1.37b
N1
31.85±0.79a
30.38±0.90b
31.79±1.56a
15.47±1.99a
11.51±0.64b
13.43±1.41ab
N2
28.85±0.53b
28.97±0.29c
28.42±0.28b
14.17±1.66a
11.20±0.99b
15.40±1.14a
N3
28.46±1.06b
28.61±0.40c
24.88±1.06c
13.00±0.16ab
13.54±0.86a
12.46±1.18b
Table S2 Effect of NO−3−N on N, P, and K uptake and transportation of Iris lactea in Pb-contaminated soil
Nutrient element
Nitrate nitrogen treatment
Accumulation in shoot
Accumulation in root
(mg/plant)
(mg/plant)
Pb0
Pb1
Pb2
Pb0
Pb1
Pb2
N
N0
1.50±0.06ab
1.74±0.10a
1.16±0.12a
0.42±0.05a
0.46±0.05a
0.33±0.08a
N1
1.94±0.17a
1.84±0.12a
1.15±0.15 a
0.40±0.05ab
0.45±0.10b
0.32±0.10a
N2
1.40±0.03bc
1.88±0.03a
0.94±0.12ab
0.36±0.04b
0.48±0.01a
0.30±0.04a
N3
1.24±0.10c
1.15±0.04b
0.83±0.02b
0.35±0.03b
0.44±0.11b
0.28±0.07a
P
N0
0.52±0.08a
0.41±0.02c
0.80±0.33ab
0.37±0.04ab
0.33±0.03 a
0.33±0.07a
N1
0.52±0.01a
0.60±0.01b
0.52±0.10ab
0.74±0.41a
0.34±0.06a
0.21±0.07ab
N2
0.38±0.01b
0.49±0.02c
0.76±0.29a
0.09±0.01b
0.30±0.02a
0.19±0.03b
N3
0.36±0.03b
0.88±0.06a
0.22±0.00b
0.24±0.02b
0.30±0.05a
0.22±0.04ab
K
N0
2.44±0.24a
2.98±0.30a
2.45±0.12 a
0.43±0.10b
0.57±0.10a
0.48±0.07 a
N1
2.58±0.24a
2.64±0.11a
2.01±0.37b
0.64±0.00 a
0.48±0.12a
0.45±0.10ab
N2
1.78±0.02b
2.12±0.16b
1.52±0.19c
0.49±0.10ab
0.40±0.05a
0.46±0.08ab
N3
1.52±0.08b
2.02±0.13b
1.10±0.13c
0.41±0.05b
0.48±0.09a
0.30±0.00b
Table S3 Effect of NO−3−N on N, P, and K accumulation of Iris lactea in Pb-contaminated soil
NO−3−N treatment
N
P
K
Pb0
Pb1
Pb2
Pb0
Pb1
Pb2
Pb0
Pb1
Pb2
N0
2.18
1.96
1.81
0.60
0.62
1.25
2.96
2.75
2.64
N1
2.50
1.98
1.90
0.36
0.81
1.38
2.06
2.64
2.38
N2
2.16
1.80
1.76
2.20
0.78
2.00
2.05
2.59
1.85
N3
1.97
1.21
1.68
0.85
1.48
0.53
2.19
2.11
2.00
Table S4 Effect of NO−3−N on transfer coefficients of N, P, and K of Iris lactea in Pb-contaminated soil
NO−3−N treatment
Pb treatment
Pb1
Pb2
N0
0.08
0.10
N1
0.06
0.08
N2
0.08
0.06
N3
0.08
0.05
Table S5 Effect of NO−3−N on transfer coefficients of Pb of Iris lactea in Pb-contaminated soil
Index
Acid soluble state
Reducible state
Oxidizable state
Residual state
Pb content in root
0.972**
0.946**
0.889**
0.897**
Pb content in shoot
0.900**
0.877**
0.859**
0.875**
Table S6 Correlation between Pb forms in soil and contents of Pb in shoot and root of Iris lactea
[1]
Amari T, Ghnaya T, Abdelly C. 2017. Nickel, cadmium and lead phytotoxicity and potential of halophytic plants in heavy metal extraction. South African Journal of Botany, 111: 99-110.
doi: 10.1016/j.sajb.2017.03.011
[2]
Ayyasamy P M, Lee S. 2009. Redox transformation and biogeochemical interaction of heavy metals in Korean soil using different treatment columns in the presence of Shewanella sp. Chemosphere, 77(4): 501-509.
doi: 10.1016/j.chemosphere.2009.07.052
[3]
Bai W B, Li P F, Li B G, et al. 2008. Some physiological responses of Chinese Iris lactea to salt stress. Pedosphere, 18(4): 454-463.
doi: 10.1016/S1002-0160(08)60036-3
[4]
Bao S D. 2000. Agrochemical Analysis of Soil. Beijing: China Agriculture Press, 370-375. (in Chinese)
[5]
Boi M E, Cappai G, De Giudici G, et al. 2021. Ex situ phytoremediation trial of Sardinian mine waste using a pioneer plant species. Environmental Science and Pollution Research, 28 (39): 1-18.
doi: 10.1007/s11356-020-11060-z
[6]
Chandana C, Joseph G R. 2019. Lead accumulation, growth responses and biochemical changes of three plant species exposed to soil amended with different concentrations of lead nitrate. Ecotoxicology and Environmental Safety, 171: 26-36.
doi: S0147-6513(18)31355-1
pmid: 30594754
[7]
Chaney R L, Angle J S, Mcintosh M S, et al. 2005. Using hyperaccumulator plants to phytoextract soil Ni and Cd. Zeitschrift für Naturforschung C, 60(3-4): 190-198.
[8]
Duzgoren-Aydin N S. 2007. Sources and characteristics of lead pollution in the urban environment of Guangzhou. Science of the Total Environment, 385(1-3): 182-195.
pmid: 17692900
[9]
Gerhardt K E, Gerwing P D, Greenberg B M. 2017. Opinion: Taking phytoremediation from proven technology to accepted practice. Plant Science, 256: 170-185.
doi: S0168-9452(16)30812-3
pmid: 28167031
[10]
Hamlin R L, Barker A V. 2006. Influence of ammonium and nitrate nutrition on plant growth and zinc accumulation by Indian mustard. Journal of Plant Nutrition, 29(8): 1523-1541.
doi: 10.1080/01904160600837709
[11]
Han Y L, Huang S Z, Gu J G, et al. 2008. Tolerance and accumulation of lead by species of Iris L. Ecotoxicology, 17(8): 853-859.
doi: 10.1007/s10646-008-0248-3
[12]
Han Y L, Huang S Z, Yuan H Y, et al. 2013. Organic acids on the growth, anatomical structure, biochemical parameters and heavy metal accumulation of Iris lactea var. chinensis seedling growing in Pb mine tailings. Ecotoxicology, 22(6): 1033-1042.
doi: 10.1007/s10646-013-1089-2
pmid: 23771790
[13]
He M J, Shen H R, Li Z T, et al. 2019. Ten-year regional monitoring of soil-rice grain contamination by heavy metals with implications for target remediation and food safety. Environmental Pollution, 244: 431-439.
doi: S0269-7491(18)33875-2
pmid: 30359925
[14]
Kastl E M, Schloter-H B, Buegger F, et al. 2015. Impact of fertilization on the abundance of nitrifiers and denitrifiers at the root-soil interface of plants with different uptake strategies for nitrogen. Biology & Fertility of Soils, 51(1): 57-64.
[15]
Lee P K, Choi B Y, Kang M J. 2015. Assessment of mobility and bio-availability of heavy metals in dry depositions of Asian dust and implications for environmental risk. Chemosphere, 119: 1411-1421.
doi: 10.1016/j.chemosphere.2014.10.028
[16]
Liu L, Wei L, Song W, et al. 2018. Remediation techniques for heavy metal-contaminated soils: Principles and applicability. Science of the Total Environment, 633: 206-219.
doi: 10.1016/j.scitotenv.2018.03.161
[17]
Lou Y L, Zhang Y S, Lin X Y, et al. 2005. Effects of forms of nitrogen fertilizer on the bioavailability of heavy metals in the soils amended with biosolids and their uptake by corn plant. Journal of Zhejiang University, 31(4): 392-398. (in Chinese)
[18]
Monsant A C, Tang C, Baker A. 2008. The effect of nitrogen form on rhizosphere soil pH and zinc phytoextraction by Thlaspi caerulescens. Chemosphere, 73(5): 635-642.
doi: 10.1016/j.chemosphere.2008.07.034
pmid: 18752830
[19]
Monsant A C, Wang Y, Tang C. 2010. Nitrate nutrition enhances zinc hyperaccumulation in Noccaea caerulescens (Prayon). Plant and Soil, 336(1-2): 391-404.
doi: 10.1007/s11104-010-0490-3
[20]
Park B, Son Y. 2017. Ultrasonic and mechanical soil washing processes for the removal of heavy metals from soils. Ultrasonics Sonochemistry, 35: 640-645.
doi: S1350-4177(16)30042-6
pmid: 26867953
[21]
Rauret G, López-Sánchez J F, Sahuquillo A, et al. 1999. Improvement of the BCR three step sequential extraction procedure prior to the certification of new sediment and soil reference materials. Journal of Environmental Monitoring, 1: 57-61.
pmid: 11529080
[22]
Rosik-Dulewska C, Karwaczyńska U. 2004. Effect of a landfill site operation on quantitative and qualitative changes of the heavy metal (Pb, Cd, Ni, Co) content in soil profiles. Ecological Chemistry and Engineering S, 11(11): 1203-1214.
[23]
Salazar M J, Pignata M L. 2014. Lead accumulation in plants grown in polluted soils: Screening of native species for phytoremediation. Journal of Geochemical Exploration, 137: 29-36.
doi: 10.1016/j.gexplo.2013.11.003
[24]
Salazar M J, Rodriguez J H, Cid C V, et al. 2016. Soil variables that determine lead accumulation in Bidens pilosa L. and Tagetes minuta L. growing in polluted soils. Geoderma, 279: 97-108.
doi: 10.1016/j.geoderma.2016.06.011
[25]
Schwartz C, Echevarria G, Morel J L, et al. 2003. Phytoextraction of cadmium with Thlaspi caerulescens. Plant and Soil, 249: 27-35.
doi: 10.1023/A:1022584220411
[26]
Shen Z G, Li X D, Wang C, et al. 2002. Lead phytoextraction from contaminated soil with high-biomass plant species. Journal of Environmental Quality, 31(6): 1893-1900.
doi: 10.2134/jeq2002.1893
[27]
Sinha P, Dube B K, Srivastava P, et al. 2006. Alteration in uptake and translocation of essential nutrients in cabbage by excess lead. Chemosphere, 65(4): 651-656.
pmid: 16545426
[28]
Stanisław J, Mos M, Buckby S, et al. 2017. Establishment, growth, and yield potential of the perennial grass Miscanthus×giganteus on degraded coal mine soils. Frontiers in Plant Science, 8: 726, doi: 10.3389/fpls.2017.00726.
doi: 10.3389/fpls.2017.00726
pmid: 28659931
[29]
Vassil A D, Kapulnik Y, Salt R D E. 1998. The role of EDTA in lead transport and accumulation by Indian mustard. Plant Physiology, 117(2): 447-453.
pmid: 9625697
[30]
Wallace A. 1979. Excess trace metal effects on calcium distribution in plants. Communications in Soil Science and Plant Analysis, 10(1-2): 473-479.
doi: 10.1080/00103627909366909
[31]
Wang J, Xue S, Hartley W, et al. 2016. The physiological response of Mirabilis jalapa Linn. to lead stress and accumulation. International Biodeterioration & Biodegradation, 128: 11-14.
[32]
Williams D E, Vlamis J, Pukite A H. 1987. Metal movement in sludge-amended soils: A nine-year study. Soil Science, 143(2): 124-131.
doi: 10.1097/00010694-198702000-00007
[33]
Wu W H, Xie Z M, Xu J M. 2013. Immobilization of trace metals by phosphates in contaminated soil near lead/zinc mine tailings evaluated by sequential extraction and TCLP. Journals of Soils and Sediments, 13(8): 1386-1395.
[34]
Xie Y, Jiang R F, Zhang F S, et al. 2009. Effect of nitrogen form on the rhizosphere dynamics and uptake of cadmium and zinc by the hyperaccumulator Thlaspi caerulescens. Plant and Soil, 318: 205-215.
doi: 10.1007/s11104-008-9830-y
[35]
Xu F, Zhu J, Zhang B, et al. 2019. Sorption and immobilization of Cu and Pb in a red soil (Ultisol) after different long-term fertilizations. Environmental Science and Pollution Research, 26(2): 1716-1722.
doi: 10.1007/s11356-018-3714-3
[36]
Yuan H Y, Huang S Z, Guo Z, et al. 2015. Role of the non-protein thiols in accumulation, translocation and tolerance of lead in Iris lactea var. chinensis. Fresenius Environmental Bulletin, 24(3): 959-969.
[37]
Yuan H Y, Guo Z, Liu Q, et al. 2018. Exogenous glutathione increased lead uptake and accumulation in Iris lactea var. chinensis exposed to excess lead. International Journal of Phytoremediation, 20(11): 1136-1143.
doi: 10.1080/15226514.2018.1460307
[38]
Zeng X Y, Zou D S, Wang A D, et al. 2020. Remediation of cadmium-contaminated soils using Brassica napus: Effect of nitrogen fertilizers. Journal of Environmental Management, 255(1): 109885, doi: 10.1016/j.jenvman.2019.109885.
doi: 10.1016/j.jenvman.2019.109885
[39]
Zhuang J, Yu G R, Liu X Y. 2000. Characteristics of lead sorption on clay minerals in relation to metal oxides. Pedosphere, 10(1): 11-20.