苯并[α]芘对不同修复潜力羊茅属植物的根系分泌物中几种低分子量有机物的影响

doi:10.17521/cjpe.2015.0426

摘要/Abstract

摘要：

根系分泌物是植物与土壤间进行物质交换和信息传递的重要载体, 是植物响应外界胁迫的重要途径, 也是构成根际微生态特征的关键因素。根系分泌物与有机污染物的植物修复密切相关, 研究胁迫条件下不同修复潜力植物间根系分泌物的释放特征有助于揭示植物修复的内在机制。该文借助根际袋土培试验研究了苯并[α]芘(BaP)胁迫下5种羊茅属(Festuca)植物根系不同生长期(30-70天)几种低分子量有机物的分泌特征。结果表明: 1) BaP浓度在10.25-161.74 mg·kg^-1范围内时, 待试植物能有效地促进土壤中BaP的去除, 其修复潜力依次为苇状羊茅(F. arundinacea) > 草原羊茅(F. chelungkiangnica) ≥ 毛稃羊茅(F. rubra subsp. arctica) ≥ 贫芒羊茅(F. sinomutica) > 细芒羊茅(F. stapfii)。2) BaP胁迫增强了植物根系对可溶性糖的分泌: 随着胁迫强度的增大、胁迫期的延长, 其分泌量变化呈“先升后降”趋势。3) BaP胁迫促进了植物根系低分子量有机酸的释放, 植物的修复潜力越大, 有机酸高峰值出现时的胁迫浓度越高; 组成成分较稳定, 草酸、乙酸、乳酸和苹果酸为主要组分(>97.34%), 在修复潜力较强植物的根系分泌物中检测出微量的反丁烯二酸。4) BaP胁迫对氨基酸种类影响不大, 但对分泌量影响较大。其中, 苏氨酸、丝氨酸、甘氨酸、丙氨酸的分泌量随BaP胁迫强度的增强而剧增; 脯氨酸、羟脯氨酸和天冬氨酸近乎以加和效应甚至协同效应的形式参与植物对BaP胁迫的应激反应: 参与应激组分的分泌量随胁迫强度的增强而剧增, 植物的修复潜力越强, 参与的组分越多。可见BaP胁迫下, 5种羊茅属植物根系分泌物中几种低分子量有机物的释放特征与植物自身的修复潜力有关: 修复潜力越强, 释放量越多且成分也越复杂, 并呈现出较强的环境适应性及生理可塑性。

关键词: 苯并[α]芘, 羊茅属植物, 根系分泌物, 低分子量有机物, 种间差异

Abstract:

Aims Root exudates have specialized roles in nutrient cycling and signal transduction between a root system and soil, as well as in plant responses to environmental stresses. They are the key regulators in the rhizosphere communications and can modify the biological and physical interactions between roots and soil organisms. Phytoremediation is an important measure to remove organic pollutants from contaminated soil, and root exudates are considered to be closely related to the mechanisms in the phytoremediation of soils contaminated by organic pollutants．This study was designed to determine the characteristics of root exudates in five Festuca species under the stress of benzo [α] pyrene (BaP) and to identify the effects of BaP on the organic compounds of low molecule weight in root exudates.Methods Five Festuca species, which had been tested to be tolerant to the BaP stress, were used in this study. A soil-cultivating test, with rhizobag technique, was conducted to investigate the effect of BaP concentration on the organic compounds of low molecule weight in root exudates at different growth stages (30-70 days). The BaP concentrations in the contaminated soils were set for 10.25 mg·kg^-1, 20.37 mg·kg^-1, 40.45 mg·kg^-1, 80.24 mg·kg^-1, and 161.74 mg·kg^-1(denoted by T₁, T₂, T₃, T₄ and T₅, respectively).Important findings The presence of vegetation enhanced the dissipation of BaP in soils. This effect was especially marked in treatment with F. arundinacea, followed sequentially by that of F. chelungkiangnica, F. rubra subsp. arctica and F. sinomutica; the dissipation of BaP in treatment with F. stapfiwas lowest during the entire experiment. The contents of soluble sugars, organic acids, and amino acids in root exudates were all increased by the BaP treatments. The contents of soluble sugars in root exudates increased notably at relatively low BaP levels (T₁-T₃) or in earlier stress stages (30-40 days), and declined at relatively high BaP levels (T₄-T₅) or in later stress stages (40-70 days), with highest values always occurring in the T₃ treatments on day 50 of the experiments. In the five Festuca species, oxlic acid, acetic acid, lactic acid and malic acid are the main constituents of organic acids in root exudates, at greater than 97.34% in total in all treatments. However, there are traces of fumaric acid in the root exudates of Festuca species with stronger remediation potentials. When the contents of organic acids in root exudates reached the peak, the stronger the remediation potentials of plants were, the higher the concentrations of BaP would be to induce stress. Nineteen types of common amino acids were found in root exudates of Festuca and the proportion of total amino acids in root exudates remain stable under all the BaP stress treatments, albeit varying contents of the 19 types of amino acids under different BaP concentrations. The contents of all amino acid in root exudates increased with increasing BaP concentrations; especially, the contents of secreted threonine, serine, glycine and alanine increased significantly among the 19 types of amino acids and the differences were significant among all treatments with different BaP concentrations (p< 0.05). However, proline, hydroxyproline, and aspartic acid participated in the stress responses of plants almost in the form of additive or synergistic effects, and their contents in root exudates increased markedly with increasing BaP concentrations in soils; the differences among different treatments were significant (p< 0.05). The more constituents of amino acids there were in stress responses, the stronger the remediation potentials of plants would be. All these illustrate that the characteristics of root exudates in Festuca were closely related to their remediation potential under the BaP stress. The greater the remediation potentials were, the more organic compounds of low molecular weight there were and the more complex those compounds would be. Moreover, they also showed a stronger environment adaptability and physiological plasticity.

Key words: benzo [α] pyrene, Festuca, root exudates, organic compounds of low molecule weight, interspecies difference

潘声旺, 袁馨, 刘灿, 李亚阑, 杨婷, 唐海云. 苯并[α]芘对不同修复潜力羊茅属植物的根系分泌物中几种低分子量有机物的影响. 植物生态学报, 2016, 40(6): 604-614. DOI: 10.17521/cjpe.2015.0426

Sheng-Wang PAN, Xin YUAN, Can LIU, Yan-Lan LI, Ting YANG, Hai-Yuan TANG. Effects of benzo [α] pyrene on the organic compounds of low molecule weight excreted by root systems in five Festuca species with different remediation potentials. Chinese Journal of Plant Ecology, 2016, 40(6): 604-614. DOI: 10.17521/cjpe.2015.0426

导出引用管理器 EndNote|Ris|BibTeX

链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2015.0426

https://www.plant-ecology.com/CN/Y2016/V40/I6/604

图/表 6

图1 苯并[α]芘(BaP)胁迫对5种羊茅属植物生物量、根冠比的影响(平均值±标准误差)。CK、T1、T2、T3、T4、T5, BaP的初始含量分别为0、10.25、20.37、40.45、80.24和161.74 mg·kg-1。不同小写字母表示相同胁迫条件下差异显著(p < 0.05)。

Fig. 1 Biomass and root: shoot ratio of plants in five Festuca species growing in soils contaminated with different concentrations of benzo [α] pyrene (BaP) (mean ± SE). CK, T1, T2, T3, T4, and T5 designate the treatments with initial concentrations of BaP at 0, 10.25, 20.37, 40.45, 80.24 and 161.74 mg·kg-1, respectively. Fa, F. arundinacea; Fc, F. chelungkiangnica; Fr, F. rubra subsp. arctica; Fm, F. sinomutica; Fs, F. stapfii. Different lowercase letters indicate significant differences (p < 0.05) under the same stress conditions.

图2 待试植物对BaP污染土壤修复潜力的种间差异(平均值±标准误差)。T1、T2、T3、T4、T5, BaP的初始含量分别为10.25、20.37、40.45、80.24和161.74 mg·kg-1。数据源右侧的不同小写字母表示相同胁迫条件下差异显著(p < 0.05)。

Fig. 2 Differences in phytoremediation potentials of benzo [α] pyrene (BaP)-contaminated soils among five Festuca species (mean ± SE). T1, T2, T3, T4, and T5 designate the treatments with initial concentrations of BaP at 10.25, 20.37, 40.45, 80.24 and 161.74 mg·kg-1, respectively. Fa, F. arundinacea; Fc, F. chelungkiangnica; Fr, F. rubra subsp. arctica; Fm, F. sinomutica; Fs, F. stapfii. Different lowercase letters next to the right of data points indicate significant differences (p < 0.05) under the same stress conditions.

图3 苯并[α]芘(BaP)的胁迫强度(A)、T3处理下胁迫期(B)对5种羊茅属植物根系分泌物中可溶性糖含量的影响(平均值±标准误差)。CK、T1、T2、T3、T4、T5, BaP的初始含量分别为0、10.25、20.37、40.45、80.24和161.74 mg·kg-1。不同小写字母表示相同胁迫条件下差异显著(p < 0.05)。

Fig. 3 The effects of benzo [α] pyrene (BaP) stress level (A) and stress stage under T3 treatment (B) on the total amount of soluble sugars in root exudates of five Festuca species (mean ± SE) . CK, T1, T2, T3, T4, and T5 designate the treatments with initial concentrations of BaP at 0, 10.25, 20.37, 40.45, 80.24 and 161.74 mg·kg-1, respectively. Fa, F. arundinacea; Fc, F. chelungkiangnica; Fr, F. rubra subsp. arctica; Fm, F. sinomutica; Fs, F. stapfii. Different lowercase letters indicate significant differences (p < 0.05) under the same stress conditions.

图4 苯并[α]芘(BaP)的胁迫强度(A)、T3处理下胁迫期(B)对5种羊茅属植物根系分泌物中有机酸总量的影响(平均值±标准误差)。CK、T1、T2、T3、T4、T5, BaP的初始含量分别为0、10.25、20.37、40.45、80.24和161.74 mg·kg-1。不同小写字母表示相同胁迫条件下差异显著(p < 0.05)。

Fig. 4 The effects of benzo [α] pyrene (BaP) stress level (A) and stress stage under T3 treatment (B) on the total amount of organic acids in root exudates of five Festuca species (mean ± SE) . CK, T1, T2, T3, T4, and T5 designate the treatments with initial concentrations of BaP at 0, 10.25, 20.37, 40.45, 80.24 and 161.74 mg·kg-1, respectively. Fa, F. arundinacea; Fc, F. chelungkiangnica; Fr, F. rubra subsp. arctica; Fm, F. sinomutica; Fs, F. stapfii. Different lowercase letters indicate significant differences (p < 0.05) under the same stress conditions.

图5 苯并[α]芘(BaP)的胁迫强度(A)、T3处理下胁迫期(B)对5种羊茅属植物根系分泌物中氨基酸总量的影响(平均值±标准误差)。CK、T1、T2、T3、T4、T5, BaP的初始含量分别为0、10.25、20.37、40.45、80.24和161.74 mg·kg-1。不同小写字母表示相同胁迫条件下差异显著(p < 0.05)。

Fig. 5 The effects of benzo [α] pyrene (BaP) stress level (A) and stress stage under T3 treatment (B) on the total amount of amino acids in root exudates of five Festuca species (mean ± SE) . CK, T1, T2, T3, T4, and T5 designate the treatments with initial concentrations of BaP at 0, 10.25, 20.37, 40.45, 80.24 and 161.74 mg·kg-1, respectively. Fa, F. arundinacea; Fc, F. chelungkiangnica; Fr, F. rubra subsp. arctica; Fm, F. sinomutica; Fs, F. stapfii. Different lowercase letters indicate significant differences (p < 0.05) under the same stress conditions.

表1 苯并[α]芘(BaP)胁迫50天时5种羊茅属植物根系分泌物中7种氨基酸释放量(mg·kg-1)

Table 1 Amount of seven amino acids released in root exudates of five Festuca species tested on day 50 under benzo [α] pyrene (BaP) stress (mg·kg-1)

氨基酸 Acids	苇状羊茅 Fa	草原羊茅 Fc	毛稃羊茅 Fr	贫芒羊茅 Fm	细芒羊茅 Fs
苏氨酸 Thr	7.28, 21.29 (10.31-31.53)^↑*	6.74, 16.81 (8.42-26.35)^↑*	7.12, 17.36 (9.24-26.39)^↑*	6.52, 18.81 (8.78-29.03)^↑*	4.55, 12.18 (6.36-20.95)^↑*
丝氨酸 Ser	29.36, 79.94 (40.95-116.42)^↑*	22.24, 60.12 (34.25-81.27)^↑*	22.07,65.74 (38.42-76.05)^↑*	19.08, 42.11 (27.24-64.31)^↑*	19.60, 44.27 (25.63-62.48)^↑*
甘氨酸 Gly	3.72, 11.62 (5.43-18.11)^↑*	3.17, 8.84 (4.47-15.91)^↑*	2.62, 9.56 (3.93-16.07)^↑*	2.72, 9.51 (4.11-16.42)^↑*	2.12, 6.75 (3.35-12.67)^↑*
丙氨酸 Ala	5.63, 17.09 (8.16-26.14)^↑*	4.57, 14.79 (6.94-24.07)^↑*	4.09, 14.91 (5.81-21.47)^↑*	3.95, 10.17 (5.74-22.41)^↑*	3.42, 10.98 (5.14-19.35)^↑*
脯氨酸 Pro	10.73, 31.45 (16.73-47.24)^↑*	8.56, 25.33 (12.12-39.56)^↑*	6.64, 21.37 (8.42-33.07)^↑*	7.82, 18.17 (8.57-28.44)^↑	6.90, 12.78 (4.28-20.07)^↑↓
羟脯氨酸 Hyp	12.50, 35.42 (17.87-52.94)^↑*	11.06, 11.57 (11.34-11.72)^↑	8.16, 27.08 (12.84-46.87)^↑*	9.21, 16.74 (9.91-31.17)^↑	8.10, 15.97 (7.49-20.12)^↑↓
天冬氨酸 Asp	14.20, 39.36 (20.08-58.62)^↑*	9.86, 18.87 (12.07-31.48)^↑*	8.77, 9.65 (9.02-10.13)^↑	8.15, 24.32 (11.47-38.25)^↑*	9.27, 17.07 (8.24-26.17)^↑↓

参考文献 44

[1]	Abhilash PC, Powell JR, Singh HB, Singh BK (2012). Plant- microbe interactions: Novel applications for exploitation in multipurpose remediation technologies.Cell, 30, 416-420.
[2]	Bertin C, Yang X (2003). The role of root exudates and allelochemicals in the rhizosphere.The Plant Soil, 256, 67-83.
[3]	Chen SC, Liao CM (2006). Health risk assessment on human exposed to environmental polycyclic aromatic hydrocar- bons pollution sources.Science of the Total Environment, 366, 112-123.
[4]	Chen SJ, Zhu XL, Feng XZ, Huang LQ, Mei YQ (2012). Effect of polycyclic aromatic hydrocarbons (PAHs) on plant. Bulletin of Biology, 45(2), 9-11. (in Chinese)[陈世军, 祝贤凌, 冯秀珍, 黄烈琴, 梅运群 (2012). 多环芳烃对植物的影响. 生物学通报, 45(2), 9-11.]
[5]	D’Orazio V, Ghanem A, Senesi N (2013). Phytoremediation of pyrene contaminated soils by different plant species.Clean-Soil, Air, Water, 41, 377-382.
[6]	Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Jonathan AE, Sundaresan V (2015). Structure, variation, and assembly of the root-associated microbiomes of rice.Proceedings of the National Academy of Sciences of the United States of America, 112, 911-920.
[7]	Gao YZ, Ling WT, Wong MH (2006). Plant-accelerated dissipation of phenanthrene and pyrene from water in the presence of a nonionic-surfactant.Chemosphere, 63, 1560-1567.
[8]	Gao YZ, Ren LL, Ling WT, Gong SS, Sun BQ, Zhang Y (2010). Desorption of phenanthrene and pyrene in soils by root exudates.Bioresource Technology, 101, 1159-1165.
[9]	Howsam M, Jones KC, Ineson P (2000). PAHs associated with the leaves of three decidous tree species. I–Concentration and profile.Environmental Pollution, 108, 413-424.
[10]	Hunter PJ, Teakle GR, Bending GD (2014). Root traits and microbial community interactions in relation to phosphorus availability and acquisition, with particular reference to Brassica.Frontiers Plant Science, 2, 352-361.
[11]	Jennifer AK, Nina MG, Frank G (2015). Plant-soil interactions in metal contaminated soils.Soil Biology & Biochemistry, 80, 232-236.
[12]	Joner EJ, Leyval C (2003). Rhizosphere gradients of polycyclic aromatic hydrocarbon (PAH) dissipation in two industrial soils and the impact of arbuscular mycorrhiza.Environm- ental Science & Technology, 37, 2371-2375.
[13]	Kim YB, Park KY, Chung Y, Buchanan BB (2004). Phytorem- ediation of anthracene contaminated soils by different plant species.Journal of Plant Biology, 47, 174-178.
[14]	Kirk JL, Klironomos JN, Lee H, Trevors JT (2005). The effects of perennial ryegrass and alfalfa on microbial abundance and diversity in petroleum contaminated soil.Environmental Pollution, 133, 455-465.
[15]	Lakshmanan V, Selvaraj G, Bais HP (2014). Functional soil microbiome: Belowground solutions to an aboveground problem.Plant Physiology, 166, 689-700.
[16]	Li XH, Ma LL, Liu XF, Fu S, Cheng HX, Xu XB (2006). Polycyclic aromatic hydrocarbon in urban soil from Beijing, China.Journal of Environmental Sciences, 18, 944-950.
[17]	Line ES, Paul HK, Torben N, Christian K, Jørgen S (2003). Toxicity of eight polycyclic aromatic compounds to red clover (Trifolium pratense), ryegrass (Lolium perenne) and mustard (Sinapsis alba).Chemosphere, 53, 993-1003.
[18]	Liu H, Ye YB, Cui B, Zheng LM, Huang YH, Wang ZH (2008). Responses of Arabidopsis thaliana to oxidative stress induced by polycyclic aromatic hydrocarbon fluoranthene.Chinese Journal of Applied Ecology, 19, 413-418. (in Chinese with English abstract)[刘泓, 叶媛蓓, 崔波, 郑荔敏, 黄炎和, 王宗华 (2008). 多环芳烃荧蒽诱导拟南芥氧化胁迫. 应用生态学报, 19, 413-418.]
[19]	Liu J, Zhou ML, Zhang N, Chen GP, Zhao RR, Gao X, Shi FC (2015). Effects of polycyclic aromatic hydrocarbons (phenanthrene and pyrene) on the growth and physiological cheracteristics ofSpartina atterniflora. Acta Scientialiu Universitatis Nankaiensis, 48(1), 14-20. (in Chinese with English abstract)[刘静, 周美利, 张楠, 陈国平, 赵瑞瑞, 高鑫, 石福臣 (2015). 多环芳烃菲和芘对互花米草生长和生理特征的影响. 南开大学学报(自然科学版), 48(1), 14-20.]
[20]	Liu Y, Zhou LL (2011). Comparative studies on absorption of benzo (a) pyrene (BaP) in city atmosphere by leaves of 8 street plants. Urban Environment & Urban Ecology, 24(4), 5-8. (in Chinese with English abstract)[刘玉, 周璐璐 (2011). 8种植物叶片对城市大气苯并(a)芘(BaP)的吸收比较. 城市环境与城市生态, 24(4), 5-8.]
[21]	Luo L, Zhang SZ, Shan XQ, Zhu YG (2006). Oxalate and root exudates enhance the desorption of p,p′-DDT from soils.Chemosphere, 63, 1273-1279.
[22]	Maliszewska-Kordybach B, Smreczak B (2000). Ecotoxico- logical activity of soils polluted with polycyclic aromatic hydrocarbons (PAHs)—Effect on plants.Environmental Technology, 21, 1099-1110.
[23]	Marschner P, Crowley D, Yang CH (2004). Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type.The Plant Soil, 261, 199-208.
[24]	Mueller KE, Shann JR (2006). PAH dissipation in spiked soil: Impacts of bioavailability, microbial activity, and trees.Chemosphere, 64, 1006-1014.
[25]	Pan SW, Wei SQ, Yuan X, Cao SX (2008). The removal and remediation of phenanthrene and pyrene in soil by mixed cropping of alfalfa and rape.Agricultural Sciences in China, 7, 1355-1364.
[26]	Phillipsa LA, Greerb CW, Farrella RE, Germidaa JJ (2012). Plant root exudates impact the hydrocarbon degradation potential of a weathered-hydrocarbon contaminated soil.Applied Soil Ecology, 52, 56-64.
[27]	Ramos R, Garcia E (2007). Induction of mixed-function oxygenase system and antioxidant enzymes in the coral Montastraea faveolata on acute exposure to benzo (a) pyrene. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 144, 348-355.
[28]	Shahzad T, Chenu C, Genet P, Barot S, Perveen N, Mougin C, Fontaine S (2015). Contribution of exudates, arbuscular mycorrhizal fungi and litter depositions to the rhizosphere priming effect induced by grassland species.Soil Biology & Biochemistry, 80, 146-155.
[29]	Shen H, Yan XL, Zheng SL, Wang XR (2002). Exudation and accumulation of citric acid in common bean in response to Al toxicity stress.Chinese Journal of Applied Ecology, 13, 307-310. (in Chinese with English abstract)[沈宏, 严小龙, 郑少玲, 王秀荣 (2002). 铝毒胁迫诱导菜豆柠檬酸的分泌与累积. 应用生态学报, 13, 307-310.]
[30]	Sumia K, Muhammad A, Samina I, Qaiser K (2013). Plant- bacteria partnerships for the remediation of hydrocarbon contaminated soils.Chemosphere, 90, 1317-1332.
[31]	Sun TR, Cang L, Wang QY, Zhou DM, Cheng JM, Xu H (2010). Roles of abiotic losses, microbes, plant roots, and root exudateson phytoremediation of PAHs in a barren soil.Journal of Hazardous Materials, 176, 919-925.
[32]	Susarla S, Medina VF, McCutcheon SC (2002). Phytoremedia- tion: An ecological solution to organic chemical contamination.Ecological Engineering, 18, 647-658.
[33]	Tao S, Cui YH, Xu FL, Li BG, Cao J, Liu WX, Schmitt G, Wang XJ, Shen WR, Qing BP, Sun R (2004). Polycyclic aromatic hydrocarbons (PAHs) in agricultural soil and vegetable from Tianjin.Science of the Total Environment, 320, 11-24.
[34]	Tejeda-Agredano MC, Gallego S, Vila J, Grifoll M, Ortega-Calvo JJ, Cantos M (2013). Influence of the sunflower rhizosphere on the biodegradation of PAHs in soil.Soil Biology & Biochemistry, 57, 2065-2076.
[35]	Tian XX, Zhou GY, Peng PA (2008). Concentrations and influence factors of polycyclic aromatic hydrocarbons in leaves of dominant species in the Pearl River Delta, South China.Environmental Science, 29, 849–854. (in Chinese with English abstract)[田晓雪, 周国逸, 彭平安 (2008). 珠江三角洲地区主要树种叶片多环芳烃含量特征及影响因素分析. 环境科学, 2008, 29, 849-854.]
[36]	Tu SX, Ma L, Thomas L (2004). Root exudates and arsenic accumulation in arsenic hyperaccumulating Pteris vittata and non-hyperaccumulating Nephrolepis exaltata.Plant and Soil, 258, 9-19.
[37]	Wang HC, Hu LL, Li M, Chen WF, Wang Y, Zhou JJ (2013). Growth effects and accumulations of polycyclic aromatic hydrocarbons (PAHs) in rape.Chinese Journal of Plant Ecology, 37, 1123-1131. (in Chinese with English abstract)[王海翠, 胡林林, 李敏, 陈为峰, 王莹, 周佳佳 (2013). 多环芳烃(PAHs)对油菜生长的影响及其积累效应. 植物生态学报, 37, 1123-1131.]
[38]	Wei SQ, Pan SW (2010). Phytoremediation for soils contami- nated by phenanthrene and pyrene with multiple plant species. Journal of Soils and Sediments, 10, 886-894.
[39]	Wu LK, Lin XM, Lin WX (2014). Advances and perspective in research on plant-soil-microbe interactions mediated by root exudates. Chinese Journal of Plant Ecology, 38, 298-310. (in Chinese with English abstract)[吴林坤, 林向民, 林文雄 (2014). 根系分泌物介导下植物-土壤-微生物互作关系研究进展与展望. 植物生态学报, 38, 298-310.]
[40]	Xie XM, Liao M, Yang J (2011).Effects of pyrene on low molecule weight organic compounds in the root exudates of ryegrass (Lolium perenne L).Acta Ecologica Sinica, 31, 7564-7570. (in Chinese with English abstract)[谢晓梅, 廖敏, 杨静 (2011). 芘对黑麦草根系几种低分子量有机分泌物的影响. 生态学报, 31, 7564-7570.]
[41]	Xie XM, Liao M, Yang J, Chai JJ, Fang S, Wang RH (2012). Influence of root-exudates concentration on pyrene degradation and soil microbial characteristics in pyrene contaminated soil. Chemosphere, 88, 1190-1195.
[42]	Xu C, Lin XF, Xia BC (2010). Response of root exudates of maize seedlings (Zea mays L.) to pyrene contamination.Acta Ecologica Sinica, 30, 3280-3288. (in Chinese with English abstract)[许超, 林小方, 夏北成 (2010). 玉米幼苗根系分泌物对芘污染的响应. 生态学报, 30, 3280-3288.]
[43]	Yi H, Crowley DE (2007). Biostimulation of PAH degradation with plants containing high concentrations of linoleic acid.Environmental Science & Technology, 41, 4382-4388.
[44]	Zhu YH, Zhang SZ, Huang HL, Wen B (2009). Effects of maize root exudates and organic acids on the desorption of phenanthrene from soils. Journal of Environmental Sci- ences, 21, 920-926.