活性硅缓解植物重金属胁迫及其生物学机制研究进展

林翰志, 陈涛, 蒋少军, 周洋, 黄祖率, 肖贤明, 徐文彬, 晏波,*

活性硅缓解植物重金属胁迫及其生物学机制研究进展

林翰志1,3, 陈涛2, 蒋少军2, 周洋1,3, 黄祖率1,3, 肖贤明1, 徐文彬4, 晏波2,*

1. 中国科学院广州地球化学研究所, 有机地球化学国家重点实验室, 广州 510640 2. 华南师范大学环境学院, 广州 510006 3. 中国科学院大学, 北京 100049 4. 东江环保股份有限公司, 深圳 518057

土壤重金属污染可抑制植物的正常生长并增加其在食物链传播的风险。硅是重要的植物营养元素, 可通过多种途径调节植物生理、生化和代谢功能, 在缓解植物的重金属胁迫及促进植物生长方面发挥重要作用。论文从活性硅促进组织结构发育、调节基因表达、增强抗氧化防御系统及建立重金属内部隔离等方面进行分析, 阐述活性硅缓解植物重金属胁迫的生物学机制。建议针对硅材料的施加方式、自然条件下硅缓解复合重金属污染胁迫机制、硅材料在土壤中的老化机理等方面, 系统开展长期田间实验, 以阐明活性硅缓解植物重金属胁迫作用机制并应用于农田土壤重金属修复。

硅; 植物; 重金属胁迫; 缓解机制; 土壤

据报道, 世界范围内主要污染场地有1000多万个, 其中超过50%为重金属或类金属污染[1]。重金属污染具有毒性高、生物累积性强的特点, 是环境安全和人类健康的主要威胁之一[2–4]。研究表明, 重金属对植物生长、细胞膜通透性、抗氧化防御、光合作用和基因表达均具有很强的毒性和破坏性[5], 而重金属污染物通过食物链富集导致各种人类疾病的产生[6–9], 引起了世界各国政府及研究人员的持续关注。

硅在地壳中的丰度仅次于O, 是除N、P、K之外重要的植物生长营养元素, 在各种植物中发现其有益作用[10–11]。在重金属污染土壤条件下, 有效硅可通过吸附、络合等方式与重金属形成硅酸盐复合物改变土壤溶液中金属的状态, 降低重金属的生物有效性, 从而实现重金属的稳定[12–13]。其次, 硅可刺激植物根系分泌物的产生并与重金属螯合而减少根对重金属的吸收[14–15]。此外, 硅可以有效降低重金属对植物的毒害作用, 使植物在重金属胁迫下正常生长发育[16]。如图1所示, 论文从宏观和微观两个尺度阐述活性硅对植物生长的影响, 并从植物组织结构、基因表达、抗氧化防御能力以及重金属传输等方面阐述硅参与的缓解植物重金属胁迫的生物学机制。

1.1 促进植物宏观组织发育

重金属严重影响植物的正常生理生化过程, 出现生长缓慢、叶片泛黄、产量下降等生长异常现象[17–18]。植物根系在吸收、运输水分和营养上发挥着重要作用, 活性硅的加入明显改善重金属胁迫下根部的形态结构, 促进主根和侧根的发育[19], 增加了总根长、根表面积、平均根径和根系活力[14]。同时, 硅可增强重金属胁迫下植株节位、叶片木质部和韧皮部的完整性[20], 减少维管束异常, 并缓解叶片损伤和坏死[21–22]。此外, 根部内皮层的硅沉积降低了凯氏带的孔隙度, 减少了重金属通过根部维管束进行质外体运输, 降低了植物地上部位重金属的含量[23]。因此, 硅缓解植物重金属胁迫最终体现在其地上部、根系、穗部和籽粒干生物量的显著提高[24-25]。

图1 硅缓解植物重金属胁迫表现及其生物学机制

Figure 1 Silicon alleviates heavy metal stress in plants and its biological mechanism

1.2 促进植物细胞组织发育

从微观角度观察, 重金属使植物细胞发生超微结构障碍[26], 如光合作用及呼吸作用相关细胞器受损、细胞核破裂和消失等[27–28], 研究表明, 添加Si显著提高总蛋白含量和膜稳定性, 在植物细胞重金属解毒中起着关键作用[29]。Cui等[30]对水稻细胞的形态学研究显示, Cd胁迫下细胞器的完整性发生了严重的破坏, 而通过添加纳米硅, 即使在高浓度Cd情况下细胞也几乎保持完整。Guo等认为, Si对植物细胞结构的积极作用主要体现为恢复叶绿体的基粒片层和膜结构并增加线粒体嵴的数量[26,28]。此外, Si可提高细胞壁再生率、降低原生质体对重金属的吸收, 从而增加细胞原生质体再生能力和活力[31]。

可见, 硅可通过修复受损结构、增加根部营养吸收、抑制根部对重金属的吸收、改善植物细胞超微结构障碍, 促进受重金属胁迫植物正常生长发育, 有利于维持植物细胞和组织的构造的完整性。这些生理学、形态学和超微结构变化与硅参与植物体内多种调控和防御机制相关。

2.1 转运基因表达

重金属胁迫下硅参与植物体内的多种调控, 硅的施用促进了Lsi1、Lsi2和Lsi6三个硅转运蛋白的表达[32], Lsi1和Lsi2主要定位在根部, 分别位于外胚层和内胚层细胞的远端和近端, 负责硅的吸收和外排; Lsi6主要位于木质部薄壁细胞, 参与硅的卸载[10,32]。此外, 在植物营养吸收上, 硅差异调控了与N、P、K运转利用相关的12个关键基因(NR、NIR、AMT、NR、GS、GOGAT、PT、PHT1、PHT2、APase、KAT1和HAK10), 提高了植物体内的常量和微量元素含量, 确保了植物正常生长[32,34]。

硅修饰的基因表达影响着植物体内多种转运蛋白活性, 在减少重金属吸收以及增强植物营养吸收等方面发挥重要作用[35–36]。研究表明, 重金属转运ATP酶(HMA)、低亲和力阳离子转运蛋白(LCT)和天然抗性相关巨噬细胞蛋白(Nramp)可调控多种植物体内重金属的吸收和转运, 且不同的金属转运蛋白在不同组织中的表达具有完全不同的意义[37–39]。Peng发现Nramp5主要在根部表达, 负责将Cd从土壤转运到根细胞[40], 而Nramp1定位于质膜上, 参与植物体内的Cd运输[38]。Greger等研究发现硅可通过抑制LCT1和HMA2基因的表达降低小麦吸收和转运Cd的能力[33]。与之相反, 硅增强拟南芥对铜超耐受性与转运蛋白SvHMA5I和SvHMA5II基因表达增强有关[41]。

2.2 植物螯合物合成与分泌

植物体内的螯合作用降低了游离重金属的含量。硅可促进植物螯合肽(PCs)和金属硫蛋白(MTs)两类不同的富含半胱氨酸的蛋白螯合剂的合成[28], 在重金属解毒的中起着重要作用。研究发现, 在As、Cd、Cu、Hg和Pb等重金属离子胁迫条件下, 还原型谷胱甘肽通过PC酶合成植物螯合肽[42–43], 并与重金属形成复合物, 然后通过腺苷三磷酸结合盒式转运蛋白运输到液泡或细胞外形成稳定螯合物[44-45]。MTs是重金属胁迫下诱导基因编码而成, 是一种富含硫的蛋白质, 在大多数被子植物中均有发现[43]。与PCs类似, MTs可与金属离子结合, 有助于降低细胞液环境的金属毒性[29]。

另一方面, 硅促进黄酮类(如, 槲皮素)、酚类化合物(如, 儿茶素)和有机酸(如, 柠檬酸、苹果酸和乌头酸)等螯合物的分泌, 限制了重金属的迁移[46-47]。多胺和氨基酸在隔离重金属方面也起着重要作用。Bosnic发现硅供给显著增加Cu暴露下黄瓜植株叶片中螯合物烟碱胺(NA)和组氨酸(His)的浓度, 使NA: Cu和His: Cu摩尔比超过了控制值, 增强了植株对铜的耐受性[48]。然而, 关于Si对这些蛋白质活性和丰度影响的信息还很缺乏, Si缓解重金属胁迫的机制在分子和遗传水平上还不清楚。需要更多的遗传实验来确定Si与重金属胁迫之间的连锁关系, 以研究金属和Si在不同植物中的运输、沉积和转运相关基因的表达水平。

3.1 抑制氧化应激产物的产生

植物在细胞器的光合作用和呼吸过程中可代谢产生了活性氧(ROS)[30,49], 而在重金属胁迫作用下, 线粒体、叶绿体和过氧化物酶体等细胞器代谢产生过量ROS, 包括单线态氧(1O2), 超氧阴离子(O2-), 过氧化氢(H2O2)和羟基自由基(·OH)等[19,50], 这些活性氧可对蛋白质、DNA和脂质造成严重的氧化损伤[51–52]。同时, 重金属胁迫造成丙二醛(MDA)、电解质渗漏(EL)等脂质过氧化物增加, 导致细胞内酶活性和氨基酸失调以及蛋白质氧化, 使植物生长受抑制[26,53–55]。研究显示, 硅降低了Cd、Pb、As、Al、Ni、Cu、Cr等重金属胁迫下小麦、水稻、玉米、芥菜、棉花等植物叶片和根系的ROS、MDA和EL等的含量, 在维持细胞结构完整以及光合气体交换上发挥重要作用[19,24,44,56–58]。

3.2 增加酶类抗氧化剂的产生

酶类抗氧化剂是抵抗ROS的第一道防线。硅普遍增加了这些酶类抗氧化剂在植物体内的含量, 在降低膜脂过氧化, 保护植物细胞免受氧化损伤发挥着作用[51,59]。超氧化物歧化酶(SOD)能有效地清除叶绿体中的超氧阴离子自由基[49,60]; 过氧化氢酶(CAT)位于植物细胞的过氧化物酶体中, 其主要作用是催化SOD反应产生的H2O2[57,61–62]; 抗坏血酸过氧化物酶(APX)在多种细胞器以不同形式出现并发挥着作用, 在清除H2O2上发挥着作用[19,63]; 愈创木酚过氧化物酶(POD)主要对抗细胞壁中的自由基[64]; 而乙醛酶系统(GlyⅠ和GlyⅡ)酶参与者甲基乙二醛(MG)的解毒[65]。Geng等研究表明, 硅显著提高受有机砷污染的水稻植株SOD、CAT和POD活性, 暗示了硅积极参与活性氧的清除并缓解了有机砷的毒害[49]。

3.3 增加非酶类抗氧化剂的产生

非酶抗氧化剂是抵御ROS的第二道防线。抗坏血酸(ASA)是一种在线粒体中合成的水溶性抗氧化剂, 可以直接清除细胞内的ROS, 并作为APX的反应基质, 是植物细胞中最有效的抗氧化剂[32]; 谷胱甘肽(GSH)是另一种重要的水溶性抗氧化剂, 而类胡萝卜素是一类酚类化合物, 他们在清除叶绿体中的1O2和·OH方面发挥着重要作用[66–67]; 生育酚(TCP)最重要的作用是可以清除类囊体膜中产生的1O2、O2-和·OH[54]。研究发现, 硅的应用使植物组织及细胞中非酶抗氧化剂水平上升, 显著提高了Cd胁迫植物的生长发育、总蛋白含量和膜稳定性[49,54,68]。

3.4 硅介导酶/非酶抗氧化剂清除ROS机制

在重金属胁迫下, Si可抑制植物体内氧化应激物的产生, 并通过激活酶和非酶抗氧化系统来降低植物细胞氧化损伤, 其作用机制如图2所示。然而, 抗氧化酶活性与植物种类、年龄、硅调节时间和条件有关[69–71], 同时, Si促进抗氧化剂活性的增强只在温和的金属胁迫下起作用, 在较高的金属浓度下添加Si将导致SOD等酶活性显著降低[71]。

注: 酶类: 超氧化物歧化酶(SOD), 过氧化氢酶(CAT), 抗坏血酸过氧化物酶(APX), 脱氢抗坏血酸还原酶(DHAR), 谷胱甘肽过氧化物酶(GPX), 谷胱甘肽S-转移酶(GST), 单脱氢抗坏血酸还原酶(MDHAR), 谷胱甘肽还原酶(GR)。非酶类: 抗坏血酸(ASA), 脱氢抗坏血酸(DHA), 谷胱甘肽(GSH), 氧化型谷胱甘肽(GSSG), 生育酚(TCP), 类胡萝卜素。

Figure 2 Mechanism of silicon-mediated enzyme / non-enzyme antioxidant scavenging ROS

4.1 减少植物重金属向地上部位传输

植物根部通过截留重金属, 限制重金属向地上部位运输, 保证了植物的正常生长发育[24,44,73]。添加硅基改良剂后, 植物积累的As、Cr、Cd和Pb大部分保留在根中, 使根中重金属的生物浓缩因子(BCF值)明显高于枝条[74–75]。硅介导金属胁迫下植物根部内胚层的形成, 是减少重金属向地上部分迁移的重要机制之一[47]。Shi等[75]通过质外体荧光示踪剂PTS证明了植物根部内胚层附近的硅沉积部分地物理阻断了Cd通过根部质外体的旁路流动, 从而抑制了Cd通过质外体途径向上运输。

4.2 促进植物低代谢细胞器对重金属隔离

硅在细胞壁中沉积并与重金属结合[76–­77], 限制了重金属的运输, 是硅降低植物金属毒性的机制之一[79–80]。通过X射线显微和电感耦合等离子体质谱法分析, 发现Cd和Si主要在植物细胞的细胞壁中积累[30,81], 这是由于硅以有机硅化合物的形式积累在细胞壁中, 并与重金属结合, 减少了重金属向细胞质的迁移[82]。Ma等[83]发现当悬浮细胞的细胞壁中存在Si时, 植物细胞壁在Cd胁迫下表现出优先积累金属的位置, 主要是通过修饰壁多糖成分, 形成Si-半纤维素基质-Zn复合物来限制Cd的吸收, 减轻了Cd的细胞毒性。

液泡中含有各种类型的有机酸和蛋白质等能与重金属离子结合, 在重金属截留、钝化和解毒方面发挥着重要作用[29,44], 而硅能有效地促进了重金属从原生质体到液泡的转运[84]。在重金属胁迫下, 硅可促进液泡膜上H+-焦磷酸化酶(OVP)和ATPase酶(V-ATPase)的表达, 这两种酶提供了驱动金属离子和其他分子进入液泡的质子梯度[85-86]。类似的, 硅增强了重金属转运ATP酶3(HMA3)的表达, 使重金属转运进入液泡[30]。

可见, 通过限制植物体内重金属迁移和金属在组织、器官区域化影响是Si促进植物缓解重金属胁迫的重要机制。然而, 这一机制因植物种类、基因类型和重金属种类不同而存在较大差异[87]。

硅通过单个或多个机制的联合作用调控植物生长发育, 在缓解植物重金属胁迫上发挥着重要作用。其生物学机制体现在减少重金属吸收及增强植物重金属耐受能力两方面, 通过调控基因表达、增强植物抗氧化能力及建立重金属屏障等促使植物恢复正常细胞结构和生长状态。然而, 这些机制可能与植物种类、基因类型、重金属种类、生长条件、胁迫时间等因素有关, 其作用机制极为复杂, 需重点开展的研究工作主要包括: (1)多金属复合污染自然土壤环境下活性硅缓解植物重金属胁迫的协同机制; (2)活性硅在土壤中的老化机理及其对植物重金属胁迫缓解的长效机制; (3)新型活性硅材料的研制、施加工艺与修复效应。

[1] KHALID S, SHAHID M, NIAZI N K, et al. A comparison of technologies for remediation of heavy metal conta­minated soils[J]. Journal of Geochemical Exploration, 2017, 182: 247–268.

[2] KHANAM R, KUMAR A, NAYAK A K, et al. Metal(loid)s (As, Hg, Se, Pb and Cd) in paddy soil: Bioavailability and potential risk to human health[J]. Science of the Total Environment, 2020, 699: 134330.

[3] ZHENG Zhongjie, LIN Mengying, CHIUEH P T, et al. Framework for determining optimal strategy for sustainable remediation of contaminated sediment: A case study in Northern Taiwan[J]. Science of the Total Environment, 2019, 654: 822–831.

[4] YIN Kun, WANG Qiaoning, LV Min, et al. Microorganism remediation strategies towards heavy metals[J]. Chemical Engineering Journal, 2019, 360: 1553–1563.

[5] WU Jiawen, SHI Yu, ZHU Yongxing, et al. Mechanisms of enhanced heavy metal tolerance in plants by silicon: A review[J]. Pedosphere, 2013, 23(6): 815–825.

[6] RAI P K, LEE S S, ZHANG Ming, et al. Heavy metals in food crops: Health risks, fate, mechanisms, and manage­ment[J]. Environment International, 2019, 125: 365–385.

[7] CHEN Bo, WANG Meng, DUAN Mingxiao, et al. In search of key: Protecting human health and the ecosystem from water pollution in China[J]. Journal of Cleaner Production, 2019, 228: 101–111.

[8] AL-BOGHDADY A A, HASSANEIN K M A. Chemical analysis and environmental impact of heavy metals in soil of Wadi Jazan area, southwest of Saudi Arabia[J]. Applied Ecology and Environmental Research, 2019, 17(3): 7067– 7084.

[9] MAHAR A, WANG Ping, ALI A, et al. Challenges and opportunities in the phytoremediation of heavy metals contaminated soils: A review[J]. Ecotoxicology and Environmental Safety, 2016, 126: 111–121.

[10] YAN Guochao, NIKOLIC M, YE Mujun, et al. Silicon acquisition and accumulation in plant and its significance for agriculture[J]. Journal of Integrative Agriculture, 2018, 17(10): 2138–2150.

[11] ARTYSZAK A. Effect of silicon fertilization on crop yield quantity and quality-a literature review in Europe[J]. Plants, 2018, doi: 10.3390/plants7030054.

[12] SUI Fengfeng, WANG Jingbo, ZUO Jing, et al. Effect of amendment of biochar supplemented with Si on Cd mobility and rice uptake over three rice growing seasons in an acidic Cd-tainted paddy from central South China[J]. Science of the Total Environment, 2020, 709: 136101.

[13] 颜奕华, 郑子成, 李廷轩, 等. 硅对土壤-烟草系统中铅迁移及形态分布的影响[J]. 应用生态学报, 2014, 25(10): 2991–2998.

[14] FAN Xueying, WEN Xiaohui, HUANG Fei, et al. Effects of silicon on morphology, ultrastructure and exudates of rice root under heavy metal stress[J]. Acta Physiologiae Plantarum, 2016, 38(8): 197.

[15] SHIM J, SHEA P J, OH B T. Stabilization of heavy metals in mining site soil with silica extracted from corn cob[J]. Water, Air, & Soil Pollution, 2014, 225(10): 2152.

[16] REHMAN M Z U, RIZWAN M, RAUF A, et al. Split application of silicon in cadmium (Cd) spiked alkaline soil plays a vital role in decreasing Cd accumulation in rice (L.) grains[J]. Chemosphere, 2019, 226: 454– 462.

[17] PEREIRA T S, PEREIRA T S, SOUZA C L F D, et al. Silicon deposition in roots minimizes the cadmium accumulation and oxidative stress in leaves of cowpea plants[J]. Physiology and Molecular Biology of Plants, 2018, 24(1): 99–114.

[18] AFSHAN S, ALI S, BHARWANA S A, et al. Citric acid enhances the phytoextraction of chromium, plant growth, and photosynthesis by alleviating the oxidative damages in Brassica napus L[J]. Environmental Science and Pollution Research, 2015, 22(15): 11679–11689.

[19] PANDEY C, KHAN E, PANTHRI M, et al. Impact of silicon on Indian mustard (L.) root traits by regulating growth parameters, cellular antioxidants and stress modulators under arsenic stress[J]. Plant Physiology and Biochemistry, 2016, 104: 216–225.

[20] MAJUMDAR A, UPADHYAY M K, KUMAR J S, et al. Ultra-structure alteration via enhanced silicon uptake in arsenic stressed rice cultivars under intermittent irrigation practices in Bengal delta basin[J]. Ecotoxicology and Environmental Safety, 2019, 180: 770–779.

[21] TRIPATHI D K, SINGH V P, KUMAR D, et al. Rice seedlings under cadmium stress: effect of silicon on growth, cadmium uptake, oxidative stress, antioxidant capacity and root and leaf structures[J]. Chemistry and Ecology, 2012, 28(3): 281–291.

[22] KIM Y H, KHAN A L, KIM D H, et al. Silicon mitigates heavy metal stress by regulating P-type heavy metal ATPases,silicon genes, and endogenous phytohormones[J]. BMC Plant Biology, 2014, 14(1): 13.

[23] RIZWAN M, MEUNIER J D, DAVIDIAN J C, et al. Silicon alleviates Cd stress of wheat seedlings (L. cv. Claudio) grown in hydroponics[J]. Environ­mental Science and Pollution Research, 2016, 23(2): 1414– 1427.

[24] ALI S, RIZWAN M, HUSSAIN A, et al. Silicon nanoparticles enhanced the growth and reduced the cadmium accumulation in grains of wheat (L.)[J]. Plant Physiology and Biochemistry, 2019, 140: 1–8.

[25] 邓腾灏博, 谷海红, 仇荣亮. 钢渣施用对多金属复合污染土壤的改良效果及水稻吸收重金属的影响[J]. 农业环境科学学报, 2011, 30(3): 455–460.

[26] GUO Lei, CHEN Aiting, HE Na, et al. Exogenous silicon alleviates cadmium toxicity in rice seedlings in relation to Cd distribution and ultrastructure changes[J]. Journal of Soils and Sediments, 2018, 18(4): 1691–1700.

[27] ALI S, FAROOQ M A, YASMEEN T, et al. The influence of silicon on barley growth, photosynthesis and ultra- structure under chromium stress[J]. Ecotoxicology and Environmental Safety, 2013, 89: 66–72.

[28] LI Tianzhe, CHEN Aiting, LI Cai, et al. Effects of silicon on growth and physiological responses of rice seedlings under cadmium stress[J]. Journal of Agro-Environment Science, 2018, 37(6): 1072–1078.

[29] RAHMAN M F, GHOSAL A, ALAM M F, et al. Remediation of cadmium toxicity in field peas (L.) through exogenous silicon[J]. Ecotoxicology and Environmental Safety, 2017, 135: 165–172.

[30] CUI Jianghu, LIU Tongxu, LI Fangbai, et al. Silica nanoparticles alleviate cadmium toxicity in rice cells: Mechanisms and size effects[J]. Environmental Pollution, 2017, 228: 363–369.

[31] KOLLAROVA K, KUSA Z, VATEHOVA-VIVODOVA Z, et al. The response of maize protoplasts to cadmium stress mitigated by silicon[J]. Ecotoxicology and Environmental Safety, 2019, 170: 488–494.

[32] KHAN E, GUPTA M. Arsenic-silicon priming of rice (L.) seeds influence mineral nutrient uptake and biochemical responses through modulation of Lsi-1, Lsi-2, Lsi-6 and nutrient transporter genes[J]. Scientific Reports, 2018, 8(1): 10301.

[33] GREGER M, KABIR A H, LANDBERG T, et al. Silicate reduces cadmium uptake into cells of wheat[J]. Environ­mental Pollution, 2016, 211: 90–97.

[34] PATI S, PAL B, BADOLE S, et al. Effect of silicon fertilization on growth, yield, and nutrient uptake of rice[J]. Communications in Soil Science and Plant Analysis, 2016, 47(3): 284–290.

[35] MARMIROLI M, MUSSI F, IMPERIALE D, et al. Target proteins reprogrammed by As and As plus Si treatments inL. fruit[J]. Bmc Plant Biology, 2017, 17: 210.

[36] CARNEIRO J M T, CHACON-MADRID K, GALAZZI R M, et al. Evaluation of silicon influence on the mitigation of cadmium-stress in the development ofthrough total metal content, proteomic and enzymatic approaches[J]. Journal of Trace Elements in Medicine and Biology, 2017, 44: 50–58.

[37] LIU Songmei, JIANG Jie, LIU Yang, et al. Characterization and evaluation of OsLCT1 and OsNramp5 mutants generated through CRISPR/Cas9-mediated mutagenesis for breeding low Cd rice[J]. Rice Science, 2019, 26(2): 88–97.

[38] PENG Fan, WANG Chao, ZHU Jianshu, et al. Expression of TpNRAMP5, a metal transporter from Polish wheat (L.), enhances the accumulation of Cd, Co and Mn in transgenic Arabidopsis plants[J]. Planta, 2018, 247(6): 1395–1406.

[39] LI Nannan, XIAO Hua, SUN Juanjuan, et al. Genome-wide analysis and expression profiling of the HMA gene family inunder cd stress[J]. Plant and Soil, 2018, 426(1-2): 365–381.

[40] WU Dezhi, YAMAJI N, YAMANE M, et al. The HvNramp5 transporter mediates uptake of cadmium and manganese, but not iron[J]. Plant Physiology, 2016, 172(3): 1899–1910.

[41] LI Yanbang, IQBAL M, ZHANG Qianqian,et al. Two Silene vulgaris copper transporters residing in different cellular compartments confer copper hypertolerance by distinct mechanisms when expressed in Arabidopsis thaliana[J]. New Phytologist, 2017, 215(3): 1102–1114.

[42] WANG Lei, ZHENG Bei, YUAN Yong, et al. Transcrip­tome profiling ofleaves in response to lead stress[J]. Bmc Plant Biology, 2020, 20(1): 1–14.

[43] COBBETT C, GOLDSBROUGH P. Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis[J]. Annual Review of Plant Biology, 2002, 53(1): 159–182.

[44] HUDA A, HAQUE M A, ZAMAN R, et al. Silicon ameliorates chromium toxicity through phytochelatin- mediated vacuolar sequestration in the roots of(L.)[J]. International Journal of Phytoremediation, 2017, 19(3): 246–253.

[45] JASINSKI M, DUCOS E, MARTINOIA E, et al. The ATP-binding cassette transporters: structure, function, and gene family comparison between rice and Arabidopsis[J]. Plant Physiology, 2003, 131(3): 1169–1177.

[46] ADREES M, ALI S, RIZWAN M, et al. Mechanisms of silicon-mediated alleviation of heavy metal toxicity in plants: A review[J]. Ecotoxicology and Environmental Safety, 2015, 119: 186–197.

[47] RIZWAN M, MEUNIER J D, MICHE H, et al. Effect of silicon on wheat seedlings (L.) grown in hydroponics and exposed to 0 to 30 µM Cu[J]. Planta, 2015, 241(4): 847–860.

[48] BOSNIC D, BOSNIC P, NIKOLIC D, et al. Silicon and iron differently alleviate copper toxicity in cucumber leaves[J]. Plants, 2019, 8(12): 554.

[49] GENG Anjing, WANG Xu, WU Lishu, et al. Silicon improves growth and alleviates oxidative stress in rice seedlings (L.) by strengthening antioxidant defense and enhancing protein metabolism under arsanilic acid exposure[J]. Ecotoxicology and Environmental Safety, 2018, 158: 266–273.

[50] KHAN Z S, RIZWAN M, HAFEEZ M, et al. Effects of silicon nanoparticles on growth and physiology of wheat in cadmium contaminated soil under different soil moisture levels[J]. Environmental Science and Pollution Research, 2020, 27(5): 4958–4968.

[51] HUANG Hengliang, RIZWAN M, LI Mei, et al. Comparative efficacy of organic and inorganic silicon fertilizers on antioxidant response, Cd/Pb accumulation and health risk assessment in wheat (L.)[J]. Environmental Pollution, 2019, 255(Pt 1): 113146.

[52] LI P, ZHAO C Z, ZHAND Y Q, et al. Silicon enhances the tolerance of Poa annua to cadmium by inhibiting its absorption and oxidative stress[J]. Biologia Plantarum, 2017, 61(4): 741–750.

[53] SHI Zhenya, YANG Suqin, HAN Dan, et al. Silicon alleviates cadmium toxicity in wheat seedlings (L.) by reducing cadmium ion uptake and enhancing antioxidative capacity[J]. Environmental Science and Pollution Research, 2018, 25(8): 7638–7646.

[54] SOUSA A D, SALEH A M, HABEEB T H, et al. Silicon dioxide nanoparticles ameliorate the phytotoxic hazards of aluminum in maize grown on acidic soil[J]. Science of the Total Environment, 2019, 693: 133636.

[55] LU Yingang, MA Jun, TENG Ying, et al. Effect of silicon on growth, physiology, and cadmium translocation of tobacco (L.) in cadmium-contaminated soil[J]. Pedosphere, 2018, 28(4): 680–689.

[56] HOWLADAR S M, AL-ROBAI S A, AL-ZAHRANI F S, et al. Silicon and its application method effects on modulation of cadmium stress responses in(L.) through improving the antioxidative defense system and polyamine gene expression[J]. Ecotoxicology and Environmental Safety, 2018, 159: 143–152.

[57] ABD ALLAH E F, HASHEM A, ALAM P, et al. Silicon alleviates nickel-induced oxidative stress by regulating antioxidant defense and glyoxalase systems in mustard Plants[J]. Journal of Plant Growth Regulation, 2019, 38(4): 1260–1273.

[58] ALI S, RIZWAN M, ULLAH N, et al. Physiological and biochemical mechanisms of silicon-induced copper stress tolerance in cotton (L.)[J]. Acta Physiologiae Plantarum, 2016, 38(11): 262.

[59] 张志雯, 秦素平, 陈于和, 等. 硅对铬、铜胁迫下小麦幼苗生理生化指标的影响[J]. 华北农学报, 2014, 29(S1): 229–233.

[60] WU Zhichao, LIU Shuai, ZHAO Jie, et al. Comparative responses to silicon and selenium in relation to antioxidant enzyme system and the glutathione-ascorbate cycle in flowering Chinese cabbage (L. sspvar.) under cadmium stress[J]. Environ­mental and Experimental Botany, 2017, 133: 1–11.

[61] ROSTAMI M, MOHAMMADI H, MULLER T, et al. Silicon application affects cadmium translocation and physiological traits ofunder cadmium stress[J]. Journal of Plant Nutrition, 2020, 43(5): 753–761.

[62] SHAN Shiping, GUO Zhaohui, LEI Ping, et al. Impacts of a compound amendment on Cd immobilization, enzyme activities and crop uptake in acidic Cd-contaminated paddy soils[J]. Bulletin of Environmental Contamination and Toxicology, 2018, 101(2): 243–249.

[63] KHODARAHMI S, KHOSHGOFTARMANESH A H. The effect of cadmium toxicity and silicon supplementation on the activity of antioxidative enzymes and the concentration of zinc and iron in hydroponically grown cucumber[J]. Communications in Soil Science and Plant Analysis, 2017, 48(1): 51–62.

[64] PEREIRA A S, DORNELES A O S, BERNARDY K, et al. Selenium and silicon reduce cadmium uptake and mitigate cadmium toxicity in(Spreng.) Pedersen plants by activation antioxidant enzyme system[J]. Environmental Science and Pollution Research, 2018, 25(19): 18548–18558.

[65] HASANUZZAMAN M, NAHAR K, ANEE T I, et al. Exogenous silicon attenuates cadmium-induced oxidative stress inL. by modulating AsA-GSH pathway and glyoxalase system[J]. Frontiers in Plant Science, 2017, 8: 1061.

[66] SHARMA P, JHA A B, DUBEY R S, et al. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions[J]. Journal of Botany, 2012, 2012: 1–26.

[67] ASHFAQUE F, INAM A, INAM A, et al. Response of silicon on metal accumulation, photosynthetic inhibition and oxidative stress in chromium-induced mustard (L.)[J]. South African Journal of Botany, 2017, 111: 153–160.

[68] 贾茜茹, 刘奋武, 樊文华, 等. 硅在Cd胁迫下对黄瓜产量和品质的影响[J]. 土壤通报, 2019, 50(1): 171–176.

[69] HUSSAIN I, ASHRAF M A, RASHEED R, et al. Exogenous application of silicon at the boot stage decreases accumulation of cadmium in wheat (L.) grains[J]. Brazilian Journal of Botany, 2015, 38(2): 223– 234.

[70] YANG Wenjia, WANG Qingya, SUN Jianyun. Alleviation mechanism of exogenous silicon in cabbages under cadmium stress[J]. Acta Botanica Boreali-Occidentalia Sinica, 2018, 38(6): 1088–1098.

[71] LABIDI S, FIRMIN S, VERDIN A, et al. Nature of fly ash amendments differently influences oxidative stress alleviation in four forest tree species and metal trace element phytostabilization in aged contaminated soil: A long-term field experiment[J]. Ecotoxicology and Environ­mental Safety, 2017, 138: 190–198.

[72] LIU Jinguang, ZHANG Hongmei, ZHANG Yuxiu, et al. Silicon attenuates cadmium toxicity inL. by reducing cadmium uptake and oxidative stress[J]. Plant Physiology and Biochemistry, 2013, 68: 1–7.

[73] ZHAO Mingliu, TANG Shouyin, DONG Haixia, et al. Effects of sodium silicate on soil properties and Cd, Pb and Zn absorption by rice plant[J]. Journal of Agro-Environ­ment Science, 2016, 35(9): 1653–1659.

[74] MU Jing, HU Zhengyi, HUANG Lijuan, et al. Influence of alkaline silicon-based amendment and incorporated with biochar on the growth and heavy metal translocation and accumulation of vetiver grass (V) grown in multi-metal-contaminated soils[J]. Journal of Soils and Sediments, 2019, 19(5): 2277–2289.

[75] WU Zhichao, WANG Fuhua, LIU Shuai, et al. Comparative responses to silicon and selenium in relation to cadmium uptake, compartmentation in roots, and xylem transport in flowering Chinese cabbage (L. sspvar.) under cadmium stress[J]. Environ­mental and Experimental Botany, 2016, 131: 173–180.

[76] SHI Xinhui, ZHANG Chaochun, WANG He, et al. Effect of Si on the distribution of Cd in rice seedlings[J]. Plant and Soil, 2005, 272(1-2): 53–60.

[77] ZHANG Chaochun, WANG Lijun, NIE Qing, et al. Long-term effects of exogenous silicon on cadmium translocation and toxicity in rice (L.)[J]. Environmental and Experimental Botany, 2008, 62(3): 300–307.

[78] 潘智立, 李军. 硫, 硅对水稻体内NPT含量及镉亚细胞分布的影响[J]. 土壤通报, 2016(5): 1253–1258.

[79] GU Haihong, ZHAn Shuhhun, WANG Shizhong, et al. Silicon-mediated amelioration of zinc toxicity in rice (L.) seedlings[J]. Plant and Soil, 2012, 350(1): 193–204.

[80] YE Juan, YAN Chongling, LIU Jingchun, et al. Effects of silicon on the distribution of cadmium compartmentation in root tips of(S., L.) Yong[J]. Environ­mental Pollution, 2012, 162: 369–373.

[81] HORST W J, WANG YUNXIA, ETICHA D. The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: a review[J]. Annals of botany, 2010, 106(1): 185–197.

[82] HE Congwu, WANG Lijun, LIU Jian, et al. Evidence for ‘silicon’within the cell walls of suspension-cultured rice cells[J]. New Phytologist, 2013, 200(3): 700–709.

[83] MA Jie, ZHANG Xiuqing, WANG Lijun. Synergistic effects between Si-hemicellulose matrix ligands and Zn ions in inhibiting Cd ion uptake in rice () cells[J]. Planta, 2017, 245(5): 965–976.

[84] EMAMVERDIAN A, DING Yulong, XIE Yinfeng, et al. Silicon mechanisms to ameliorate heavy metal stress in plants[J]. Biomed Research International, 2018, 2018: 8492898.

[85] SHARMA S S., DIETZ K J, MIMURA T. Vacuolar compartmentalization as indispensable component of heavy metal detoxification in plants[J]. Plant, Cell & Environment, 2016, 39(5): 1112–1126.

[86] CAO Fangbin, DAI Huaxin, HAO Pengfei, et al. Silicon regulates the expression of vacuolar H+-pyrophosphatase 1 and decreases cadmium accumulation in rice (L.)[J]. Chemosphere, 2020, 240: 124907.

[87]DRESLER S, WÓJCIK M, BEDNAREK W, et al. The effect of silicon on maize growth under cadmium stress[J]. Russian Journal of Plant Physiology, 2015, 62(1): 86–92.

Research progress on biological mechanism of active silicon alleviating heavy metal stress in plants

LIN Hanzhi1,3, CHEN Tao2, JIANGShaojun2, ZHOU Yang1,3, HUANG Zulv1,3, XIAO Xianming1, XU Wenbin4, YAN Bo2,*

1. State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China 2. College of Environment, South China Normal University, Guangzhou 510006, China 3. University of Chinese Academy of Sciences, Beijing 100082, China 4. Dongjiang Environmental Company Limited, Shenzhen 518057, China

Heavy metal pollution in soil can inhibit the normal growth of plants and increase the risk of their transmission in the food chain. Silicon is an important plant nutrient element, which can regulate plant physiological, biochemical and metabolic functions in various ways. And it plays an important role in alleviating heavy metal stress and promoting plant growth. This paper expounds the biological mechanism of active silicon in alleviating heavy metal stress in plants from the following aspects: promoting tissue structure development, regulating gene expression, strengthening antioxidant defense system, establishing internal isolation of heavy metals and so on. In order to clarify the mechanism of active silicon in alleviating heavy metal stress in plants and applied to heavy metal remediation in farmland soil. It is suggested that long-term field experiments should be carried out systematically in the aspects of application mode of silicon material, the mechanism of silicon alleviating compound heavy metal pollution stress under natural conditions, and the aging mechanism of silicon materials in soil.

silicon; plants; heavy metal stress; mitigation mechanism; soil

林翰志, 陈涛, 蒋少军, 等. 活性硅缓解植物重金属胁迫及其生物学机制研究进展[J]. 生态科学, 2022, 41(5): 243–251.

LIN Hanzhi, CHEN Tao, JIANGShaojun, et al. Research progress on biological mechanism of active silicon alleviating heavy metal stress in plants[J]. Ecological Science, 2022, 41(5): 243–251.

10.14108/j.cnki.1008-8873.2022.05.028

X53

A

1008-8873(2022)05-243-09

2020-08-28;

2020-10-18

国家重点研发计划项目(2018YFC1802803); NSFC-广东省联合基金(U1901218)

林翰志(1993—), 男, 广东阳江人, 博士研究生, 主要从事土壤重金属污染修复研究, E-mail: xtulhz@126.com

晏波, 男, 博士, 教授, 主要从事资源综合利用, 水污染控制, 土壤重金属污染修复研究, E-mail: bo.yan@m.scnu.edu.cn