Effects of sewage sludge application on root growth and heavy metal uptake of Schefflera arboricola
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摘要:目的
分析表施和混施污泥对鹅掌藤Schefflera arboricola根系生长和重金属吸收的影响，深入认识污泥施用对园林植物根系生长的影响，为污泥在园林中安全利用提供借鉴。
方法采用根箱试验，观测不施、表施和混施10%(w)污泥对常见园林植物鹅掌藤的不同土层根系形态及土壤pH和电导率动态变化的影响，分析根组织密度、根密度和重金属含量，拟合土壤pH、电导率、根系重金属含量与根长的关系。
结果与不施污泥相比，混施污泥明显抑制鹅掌藤根长、根表面积和根密度增长；而表施污泥显著增加鹅掌藤0~20 cm土层的总根长、根体积和根密度。处理240 d后，混施污泥处理的0~20与20~40 cm土层总根长分别为不施污泥的66.37%和51.51%，而表施污泥处理分别为不施污泥的115.43%和98.66%。最大总根长、根体积和根密度均出现在表施污泥的0~20 cm土层，最大根干质量和根组织密度出现在表施污泥的污泥层。混施污泥显著提高了土壤pH和电导率以及植株重金属含量，不同土层根系Cd、Zn、Cu和Ni含量分别是不施污泥的2.32~11.70倍。线性回归拟合分析表明，不施和表施污泥处理的0~20 cm土层鹅掌藤原位扫描总根长均与原位测定土壤pH呈极显著正相关(P<0.001)，鹅掌藤总根长与根系Cd、Zn、Cu和Ni含量均呈极显著负相关(P<0.001)。
结论表施10%(w)污泥可以提高土壤pH并促进鹅掌藤根系生长。混施10%(w)污泥显著增加不同土层根系重金属含量，进而抑制鹅掌藤根系生长。
Abstract:ObjectiveThis study aimed to analyze the effect of sewage sludge (SS) surface and mixed application on Schefflera arboricola root growth and heavy metals uptake, to deeply understand the effect of SS application on landscape plant root growth, and to provide a reference for the safe use of SS in the landscape.
MethodWe conducted a root box experiment without SS (no SS) and with the surface application (surface SS) or the mixed application (mixed SS) of 10% SS, to analyze the dynamic changes of S. arboricola root morphology, soil pH, and conductivity in different soil layers. Root tissue density, root density, and heavy metal contents of plant were also analyzed. The relationships between soil pH, soil conductivity, root heavy metal contents, and root length were further established by the linear regression analysis.
ResultCompared with no SS, mixed SS treatment obviously inhibited the increment of root length, root surface area, and root density. Surface SS treatment significantly increased total root length, root volume, and root density in the 0−20 cm soil layer. After 240 days of treatment, total root length in 0−20 cm and 20−40 cm layers in mixed SS treatment were 66.37% and 51.51% of no SS, respectively. Those for surface SS treatment were 115.43% and 98.66% of no SS, respectively. The maximum root total length, root volume, and root density occurred in the 0−20 cm soil layer in surface SS treatment, while the maximum root dry weight and tissue density occurred in the SS layer in surface SS treatment. Mixed SS treatment significantly increased soil pH, soil conductivity, and heavy metal contents of S. arboricola. The contents of Cd, Zn, Cu, and Ni in roots of different soil layers in mixed SS treatment were 2.32 to 11.70 times higher than those in no SS treatment. The linear regression analysis showed that the in-situ scanning total root length of S. arboricola in 0−20 cm soil layers was significantly positively correlated with in-situ measured soil pH in no SS and surface SS treatment (P<0.001). Total root length of S. arboricola was significantly negatively correlated with the contents of Cd, Zn, Cu, and Ni in roots (P<0.001).
ConclusionSurface application of 10% SS increases soil pH and promotes S. arboricola root growth. Mixed application of 10% SS significantly increases root heavy metal uptake in different soil layers and inhibits root growth of S. arboricola.
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Keywords:
- Sewage sludge /
- Landscape application /
- Landscape plant /
- Root morphology /
- Heavy metal /
- pH /
- Schefflera arboricola
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作为哺乳动物的泌乳器官，良好的发育是乳腺充分发挥泌乳功能的前提，对动物子代的生长发育及畜牧业生产具有重要影响。因此，研究影响乳腺发育的因素及其机制对提高动物泌乳性能及畜牧业生产提质增效具有重要意义。
哺乳动物乳腺发育期包括初情期、妊娠期和泌乳期等不同阶段[1]。猪乳腺发育有3个关键阶段，分别是90日龄到性成熟期间、妊娠期后三分之一阶段和哺乳期[2]。乳腺的发育受到遗传、激素、营养和环境等不同因素的影响[1-3]，其中营养对乳腺的发育起着非常重要的作用[3-4]。前期研究发现，高脂日粮会抑制初情期小鼠乳腺的发育[5-6]；相反，限饲或者过瘦也会影响乳腺的发育，例如：母猪90日龄至性成熟期间，25%的限饲可显著降低乳腺实质质量、乳腺组织DNA和RNA含量[7]。此外，一定程度的能量限制是预防乳腺癌的潜在策略[8]，但是过量限饲也会抑制乳腺的正常发育。目前，对于限饲调控初情期哺乳动物乳腺发育的机制尚不清楚。
本试验以初情期小鼠为对象，在研究限饲对初情期小鼠乳腺导管发育的基础上，进一步探索限饲对初情期小鼠血清中胰岛素样生长因子1(Insulin-like growth factor 1,IGF-1)和雌二醇(Estradiol, E2)水平及乳腺组织中增殖相关蛋白增殖细胞核抗原(Proliferating cell nuclear antigen, PCNA)表达的影响，旨在揭示限饲对初情期小鼠乳腺发育的影响及其机制，为动物乳腺发育的营养调控提供科学依据。
1. 材料与方法
1.1 试验动物与试验设计
选用24只4周龄的C57BL/6J雌性小鼠(购于广东省医学实验动物中心)，预饲喂正常日粮3 d后，根据体质量随机分为2组：对照组(自由采食日粮)和限饲组(每天饲喂对照组小鼠前一天平均采食量的70%)，每组12只。将小鼠同室分笼饲养，自由采食饮水；每天光照与黑暗各12 h，环境温度控制在(25±1) ℃，湿度(60±5)%。每周进行小鼠采食量、饮水量和体质量的测定，采样前对小鼠进行体成像和体组成检测，饲养4周后，眼球采血静置离心分离得到血清，并对血清IGF-1和E2水平进行检测；通过颈部脱臼方式处死小鼠，采集小鼠乳腺组织、褐色脂肪和内脏脂肪组织并称质量，同时对乳腺进行染色和蛋白表达等检测。
1.2 试验材料
小鼠日粮购于广东省医学实验动物中心；百里酚、胭脂红和硫酸铝钾购于成都艾科达化学试剂有限公司；轻型小动物成分分析仪(上海纽迈电子科技有限公司)用于对小鼠进行体成像和体成分测定；IGF-1放射免疫试剂盒购于天津九鼎医学生物工程有限公司；PCNA抗体购于Cell Signaling Technology。
1.3 测定指标及方法
乳腺采集和Whole-mount染色：切下右侧乳腺腹腺体(第4对乳腺)并称质量，涂在玻璃载玻片上，进行Whole-mount染色[5]，显微镜下观察初情期小鼠乳腺组织结构，统计乳腺组织终末乳芽(Terminal end bud，TEB)数量和导管分支数量。
PCNA蛋白的免疫荧光染色：步骤为组织脱水、包埋、切片、抗原修复、血清封闭、孵一抗过夜、孵二抗、DAPI复染细胞核、封片，之后在免疫荧光显微镜下观察初情期小鼠乳腺组织荧光强弱并分析。
1.4 数据分析
数据结果用平均值±标准误表示，统计分析采用SigmaPlot 12.5软件分析，采用t检验比较对照组和限饲组的统计差异。
2. 结果与分析
2.1 限饲对初情期小鼠生长性状的影响
如图1a所示，限饲组小鼠的第1周体质量显著低于对照组(P<0.05)，从第2周开始，限饲组小鼠的体质量极显著低于对照组(P<0.001)；每周限饲组小鼠的体增质量均极显著低于对照组(图1b)；另外，限饲组小鼠平均日采食量和平均日能量摄入均极显著低于对照组(图1c、1d)；然而，限饲组小鼠平均日饮水量极显著高于对照组(图1e)。
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图 1 限饲对初情期小鼠生长性状的影响“*”、“**”和“***”分别表示与对照组相比差异达0.05、0.01、0.001的显著水平(t检验)Figure 1. Effects of feed restriction on growth traits of pubertal mice“*”,“**” and “***” indicate the difference with control group reaches 0.05, 0.01 and 0.001 significance levels respectively (t test)2.2 限饲对初情期小鼠体组成及不同部位脂肪的影响
体成像和体组成检测结果(图2、图3)表明，与对照组相比，限饲不会显著改变初情期小鼠的整体肌肉含量和脂肪含量。
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图 2 限饲对初情期小鼠体成像的影响红色部分代表脂肪Figure 2. Effect of feed restriction on the body imaging of pubertal miceRed part represents fat![]()
图 3 限饲对初情期小鼠体组成的影响Figure 3. Effects of feed restriction on the body composition of pubertal mice采样褐色脂肪和内脏脂肪的结果表明，与对照组相比，限饲对初情期小鼠的褐色脂肪指数(褐色脂肪质量占体质量百分比)无显著影响(图4A)，但可极显著降低内脏脂肪指数(内脏脂肪质量占体质量百分比)(图4B)。
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图 4 限饲对初情期小鼠褐色脂肪和内脏脂肪的影响“***”表示与对照组相比差异达0.001的显著水平(t检验)Figure 4. Effects of feed restriction on the brown adipose tissue and visceral adipose tissue of pubertal mice“***” indicates the difference with control group reaches 0.001 significance level (t test)2.3 限饲对初情期小鼠乳腺发育的影响
小鼠乳腺Whole-mount染色如图5所示，与对照组小鼠相比，限饲组小鼠的乳腺组织在乳腺导管的密度和数量上有明显的降低；此外，与对照组小鼠相比，限饲组小鼠的乳腺质量显著降低29%，同时限饲组小鼠乳腺导管分支数量显著降低，导管的TEB数量极显著降低(表1)。
表 1 限饲对初情期小鼠乳腺(第4对右侧)发育性状的影响1)Table 1. Effects of feed restriction on developmental traits of mammary gland (the right one of the fourth pair) of pubertal mice处理
Treatment乳腺质量/g
Mammary gland weight乳腺指数/%
Mammary gland index终末乳芽数量
TEB number导管分支数量
Duct branch number对照 Control 0.059 5±0.004 7 0.298 1±0.023 7 38.666 7±0.666 7 27.666 7±1.201 9 限饲 Feed restriction 0.042 2±0.003 7* 0.258 5±0.019 2 21.666 7±0.666 7*** 21.666 7±1.201 9* 1) “*”和“***”分别表示与对照组相比差异达0.05和0.001的显著水平(t检验)
1)“*” and “***” indicate the difference with control group reaches 0.05 and 0.001 significance levels respectively (t test)![]()
图 5 限饲对初情期小鼠乳腺形态和导管发育的影响a、b分别为Whole-mount染色后对照组和限饲组小鼠乳腺组织的低倍显微镜照片；c、d分别为Whole-mount染色后对照组和限饲组小鼠乳腺组织的高倍显微镜照片；TEB：终末乳芽Figure 5. Effects of feed restriction on mammary gland morphology and duct development of pubertal micea and b are low-power microscope pictures of the breast tissue from mice in the control group and feed restriction group after whole-mount staining, respectively; c and d are high-power microscope pictures of the breast tissue from mice of the control group and feed restriction group after whole-mount staining, respectively; TEB: Terminal end bud2.4 限饲对初情期小鼠血清中IGF-1和E2水平的影响
如图6所示，与对照组相比，限饲可以使初情期小鼠血清中IGF-1水平降低34%，但是对小鼠血清中E2水平没有显著影响。
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图 6 限饲对初情期小鼠血清中IGF-1和E2水平的影响“*”表示与对照组相比差异达0.05的显著水平(t检验)Figure 6. Effects of feed restriction on the serum levels of IGF-1 and E2 of pubertal mice“*”indicates the difference with control group reaches 0.05 significance level (t test)2.5 限饲对初情期小鼠乳腺组织中增殖相关蛋白PCNA表达的影响
如图7所示，对照组乳腺组织导管免疫荧光染色(红色箭头部分)明亮清晰，而限饲组乳腺组织导管却暗淡模糊，由此得知，限饲可以显著降低乳腺导管增殖相关蛋白PCNA的表达。
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图 7 限饲对初情期小鼠乳腺组织中PCNA蛋白表达的影响图中DAPI表示4′,6−二脒基−2−苯基吲哚荧光染色图片；PCNA表示增殖细胞核抗原荧光染色图片，红色箭头处为乳腺导管；Merge表示DAPI荧光染色和PCNA荧光染色合并图片；White light表示光学显微镜拍摄图片Figure 7. Effect of feed restriction on PCNA protein expression in mammary gland of pubertal miceIn the figure, DAPI represents 4′,6-diamidino-2-phenylindole fluorescence staining picture, red arrow points at mammary duct; PCNA represents the fluorescence staining image of PCNA; Merge represents the combined image of DAPI fluorescence staining and PCNA fluorescence staining; White light represents the image taken by an optical microscope3. 讨论与结论
3.1 限饲对初情期小鼠生长和体组成的影响
周期性能量限制能显著降低羔羊的生长性能[9]，对鸡和鹅的研究也观察到类似情况。叶耀辉等[10]的研究表明，限饲对猪胴体蛋白质日沉积量无显著影响，但能引起胴体脂肪沉积的减少，从而达到胴体瘦肉比例相对增加的目的。本研究发现，限饲同样也能显著降低小鼠的生长性能，体质量、体增质量、平均日采食量和平均日能量摄入均显著降低，但是平均日饮水量却显著升高，这可能是因为限饲组小鼠能量供给不足，代偿性通过增加饮水量来弥补能量的缺失。另外，限饲也能显著降低初情期小鼠内脏脂肪指数，但是对褐色脂肪指数、脂肪含量和肌肉含量均无显著影响。
3.2 限饲对初情期小鼠乳腺发育的影响
许多研究表明，青春期，妊娠期和哺乳期的乳腺快速增生期间，母猪的营养会影响乳腺发育。母猪90日龄至性成熟，相对于正常采食量25%的限饲可以显著降低乳腺实质质量、乳腺组织DNA和RNA含量，但是，在断奶后至90日龄对母猪进行34%的限饲不会影响乳腺的发育[7]。在本试验中，whole-mount染色结果表明，限饲可显著降低乳腺组织导管分支数量以及TEB的数量，提示限饲可显著抑制初情期小鼠乳腺的发育。Park等[11]的研究也发现，能量限制延迟了大鼠青春期的开始并延缓了母代和后代的生长，减少了乳腺中的脂肪沉积，但它并没有影响乳腺细胞性质。但是泌乳母猪饲料限制不会对乳汁组成和窝产仔数产生不利影响[12]。可见，不同阶段的限饲造成的影响也不相同。
3.3 限饲对初情期小鼠血清IGF-1和E2水平及乳腺组织中PCNA蛋白表达的影响
IGF-1是动物出生后生长调节的重要因子，有研究报道，IGF-1能增加乳腺上皮细胞存活率并刺激乳腺上皮细胞的增殖，还促进乳腺肿瘤发生[13]。Clemmons[14]的研究结果表明，血清中IGF- 1能够提高动物体内能量和蛋白的沉积，加快生长速度。E2是卵巢卵泡颗粒细胞分泌的一种自然雌激素，能增进和调节雌性器官及副性征的正常发育。有研究表明，17β−雌二醇能显著促进人乳腺癌细胞系MCF-7细胞的增殖[15]。本研究发现，限饲能显著降低初情期小鼠血清中IGF-1水平，这可能是导致限饲组小鼠生长发育受阻的重要原因。但是，限饲对初情期小鼠血清中E2水平无显著影响。
研究发现，IGF-1在初情期小鼠优先激活PI3K/Akt通路，增加细胞周期蛋白D1(Cyclin D1)表达[13]。本研究中乳腺组织的免疫荧光结果表明，限饲可以显著降低乳腺组织增殖相关蛋白PCNA的表达，提示限饲可能抑制血清IGF-1水平，从而降低乳腺组织增殖相关蛋白PCNA的表达来抑制乳腺发育。
综上所述，限饲可抑制初情期小鼠乳腺发育，其乳腺导管分支数量和TEB数量显著减少。限饲对初情期小鼠乳腺发育的抑制作用可能与其抑制增殖相关蛋白PCNA的表达和降低血清中IGF-1水平有关。本论文研究结果为动物和人类乳腺健康发育的营养调控提供了科学的参考依据。
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图 1 原位扫描鹅掌藤总根长、根表面积和根体积变化
SS：污泥；柱子上方的不同小写字母表示不同时间的同一处理同一土层的数值差异显著(P<0.05，0~20 cm土层使用Duncan’s法，不施污泥层与20~40 cm土层使用t检验)；柱子上方的不同大写字母表示不同处理的同一时间同一土层的数值差异显著(P<0.05，Duncan’s法)
Figure 1. Changes of total root length, root surface area and root volume
in Schefflera arboricola by in-situ scanning SS: Sewage sludge; Different lowercase letters on the bars indicate significant differences among the same treatment at different times for the same soil layer (P<0.05, Duncan’s method was used for 0−20 cm soil layer, and t test was used for no SS layer and 20−40 cm soil layer); Different capital letters on the bars indicate significant differences among different treatments at the same time for the same soil layer (P<0.05, Duncan’s method)
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图 2 原位测定土壤pH和电导率(σ)变化
相同时间的不同小写字母表示不同处理间差异显著(P<0.05，Duncan’s法)
Figure 2. Changes of soil pH and electrical conductivity (σ) by in-situ measurement
Different lowercase letters in the same time indicate significant differences among different treatments (P<0.05, Duncan’s method)
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图 3 原位测定土壤pH和原位扫描总根长线性回归拟合
Figure 3. Linearization regression analysis between in-situ measured soil pH and in-situ scanned total root length
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图 4 原位测定土壤电导率和原位扫描总根长线性回归拟合
Figure 4. Linearization regression analysis between in-situ measured soil electrical conductivity value and in-situ scanned total root length
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图 5 根系重金属含量和总根长线性回归拟合
Figure 5. Linearization regression analysis between root heavy metal contents and total root length
表 1 土壤及堆肥污泥的基本性质
Table 1 Basic properties of soil and composted sludge
试验材料
Testing
materialpH σ/
(mS·cm−1)w(有机质)/
(g·kg−1)
Organic matter
contentw/(mg·kg−1) 碱解氮
Available
N有效磷
Available
P速效钾
Available
KCd Ni Cu Zn 土壤 Soil 4.68 0.05 2.48 67.26 4.56 47.65 0.12 9.77 20.58 37.93 污泥 Sewage sludge 7.86 3.35 178.35 1 496.48 695.67 498.37 2.39 47.96 419.50 1070.37 
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表 2 收获后根系干质量及相关指标1)
Table 2 Root dry weight and other indexes after harvest
处理
Treatment土层/ cm
Soil layer根干质量/g
Root dry weight总根长/cm
Total root length根体积/cm3
Root volume比根长/(cm∙g−1)
Specific root length根组织密度/(g∙cm−3)
Root tissue density根密度/(cm∙cm−3)
Root density不施污泥
No SS0~20 6.55±0.74ab 1 140.39±31.00b 2.83±0.09b 177.56±16.38a 2.33±0.33a 0.19±0.01b 20~40 3.02±0.08ab 1 152.36±33.32a 3.18±0.29a 381.99±18.64a 0.96±0.0.07a 0.19±0.01a 表施污泥
Surface SS污泥层SS 13.28±0.59A 430.92±25.68C 1.51±0.26B 32.59±2.38C 9.30±1.38A 0.14±0.01B 0~20 8.54±0.94aB 1 316.34±33.77aA 3.71±0.27aA 158.14±18.07aB 2.36±0.39aB 0.22±0.01aA 20~40 4.10±0.72aC 1 136.90±71.77aB 3.31±0.30aA 297.68±58.97aA 1.27±0.29aB 0.19±0.01aA 混施污泥
Mixed SS0~20 4.53±0.79b 756.92±33.66c 2.21±0.10c 182.20±43.92a 2.07±0.39a 0.13±0.01c 20~40 1.75±0.33b 593.57±13.14b 2.39±0.17b 369.57±83.47a 0.74±0.16b 0.10±0.00b 1)表中数据为平均值±标准误，n=3；同列数据后的不同小写字母表示同一土层的不同处理间差异显著(P<0.05，Duncan’s法)；同列数据后的不同大写字母表示表施污泥处理不同土层间差异显著(P<0.05，Duncan’s法)
1)Values in table are means±SE, n=3; Different lowercase letters after the data in the same column indicate significant differences in the same soil layer among different treatments (P<0.05, Duncan’s method); Different capital letters after the data in the same column indicate significant differences among different soil layers treated with surface sewage sludge (P<0.05, Duncan’s method)
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表 3 鹅掌藤根系重金属含量1)
Table 3 Heavy metal contents in root of Schefflera arboricola
处理
Treatment土层/cm
Soil layerw/(mg∙kg−1) Cd Zn Cu Ni 不施污泥
No SS0~20 0.23±0.02b 13.61±2.74c 15.39±6.38b 2.34±0.24b 20~40 0.35±0.07b 14.16±2.17b 19.51±3.80b 1.99±0.06b 表施污泥
Surface SS污泥层SS 1.43±0.31A 83.88±1.75A 48.64±2.25A 18.11±0.35A 0~20 1.14±0.21bA 27.38±6.02bB 24.51±8.42bB 2.76±0.96bB 20~40 0.95±0.10bA 18.94±2.60bB 11.28±0.41bB 2.84±0.60bB 混施污泥
Mixed SS0~20 2.69±0.50a 54.69±1.39a 46.74±1.96a 12.53±1.87a 20~40 2.32±0.47a 50.49±1.49a 45.26±1.94a 13.24±0.59a 1) 表中数据为平均值±标准误，n=3；同列数据后的不同小写字母表示同一土层的不同处理间差异显著(P<0.05，Duncan’s法)；同列数据后的不同大写字母表示表施污泥处理不同土层间差异显著(P<0.05，Duncan’s法)
1) Values in table are means ± SE, n=3; Different lowercase letters after the data in the same column indicate significant differences in the same soil layer among different treatments (P<0.05, Duncan’s method); Different capital letters after the data in the same column indicate significant differences among different soil layers treated with surface sewage sludge (P<0.05, Duncan’s method)
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