活性硅緩解植物重金屬脅迫及其生物學機制研究進展

林翰志, 陳濤, 蔣少軍, 周洋, 黃祖率, 肖賢明, 徐文彬, 晏波,*

活性硅緩解植物重金屬脅迫及其生物學機制研究進展

林翰志1,3, 陳濤2, 蔣少軍2, 周洋1,3, 黃祖率1,3, 肖賢明1, 徐文彬4, 晏波2,*

1. 中國科學院廣州地球化學研究所, 有機地球化學國家重點實驗室, 廣州 510640 2. 華南師范大學環(huán)境學院, 廣州 510006 3. 中國科學院大學, 北京 100049 4. 東江環(huán)保股份有限公司, 深圳 518057

土壤重金屬污染可抑制植物的正常生長并增加其在食物鏈傳播的風險。硅是重要的植物營養(yǎng)元素, 可通過多種途徑調節(jié)植物生理、生化和代謝功能, 在緩解植物的重金屬脅迫及促進植物生長方面發(fā)揮重要作用。論文從活性硅促進組織結構發(fā)育、調節(jié)基因表達、增強抗氧化防御系統(tǒng)及建立重金屬內部隔離等方面進行分析, 闡述活性硅緩解植物重金屬脅迫的生物學機制。建議針對硅材料的施加方式、自然條件下硅緩解復合重金屬污染脅迫機制、硅材料在土壤中的老化機理等方面, 系統(tǒng)開展長期田間實驗, 以闡明活性硅緩解植物重金屬脅迫作用機制并應用于農田土壤重金屬修復。

硅; 植物; 重金屬脅迫; 緩解機制; 土壤

0 前言

據報道, 世界范圍內主要污染場地有1000多萬個, 其中超過50%為重金屬或類金屬污染[1]。重金屬污染具有毒性高、生物累積性強的特點, 是環(huán)境安全和人類健康的主要威脅之一[2–4]。研究表明, 重金屬對植物生長、細胞膜通透性、抗氧化防御、光合作用和基因表達均具有很強的毒性和破壞性[5], 而重金屬污染物通過食物鏈富集導致各種人類疾病的產生[6–9], 引起了世界各國政府及研究人員的持續(xù)關注。

硅在地殼中的豐度僅次于O, 是除N、P、K之外重要的植物生長營養(yǎng)元素, 在各種植物中發(fā)現(xiàn)其有益作用[10–11]。在重金屬污染土壤條件下, 有效硅可通過吸附、絡合等方式與重金屬形成硅酸鹽復合物改變土壤溶液中金屬的狀態(tài), 降低重金屬的生物有效性, 從而實現(xiàn)重金屬的穩(wěn)定[12–13]。其次, 硅可刺激植物根系分泌物的產生并與重金屬螯合而減少根對重金屬的吸收[14–15]。此外, 硅可以有效降低重金屬對植物的毒害作用, 使植物在重金屬脅迫下正常生長發(fā)育[16]。如圖1所示, 論文從宏觀和微觀兩個尺度闡述活性硅對植物生長的影響, 并從植物組織結構、基因表達、抗氧化防御能力以及重金屬傳輸?shù)确矫骊U述硅參與的緩解植物重金屬脅迫的生物學機制。

1 促進植物組織結構發(fā)育

1.1 促進植物宏觀組織發(fā)育

重金屬嚴重影響植物的正常生理生化過程, 出現(xiàn)生長緩慢、葉片泛黃、產量下降等生長異?，F(xiàn)象[17–18]。植物根系在吸收、運輸水分和營養(yǎng)上發(fā)揮著重要作用, 活性硅的加入明顯改善重金屬脅迫下根部的形態(tài)結構, 促進主根和側根的發(fā)育[19], 增加了總根長、根表面積、平均根徑和根系活力[14]。同時, 硅可增強重金屬脅迫下植株節(jié)位、葉片木質部和韌皮部的完整性[20], 減少維管束異常, 并緩解葉片損傷和壞死[21–22]。此外, 根部內皮層的硅沉積降低了凱氏帶的孔隙度, 減少了重金屬通過根部維管束進行質外體運輸, 降低了植物地上部位重金屬的含量[23]。因此, 硅緩解植物重金屬脅迫最終體現(xiàn)在其地上部、根系、穗部和籽粒干生物量的顯著提高[24-25]。

圖1 硅緩解植物重金屬脅迫表現(xiàn)及其生物學機制

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

1.2 促進植物細胞組織發(fā)育

從微觀角度觀察, 重金屬使植物細胞發(fā)生超微結構障礙[26], 如光合作用及呼吸作用相關細胞器受損、細胞核破裂和消失等[27–28], 研究表明, 添加Si顯著提高總蛋白含量和膜穩(wěn)定性, 在植物細胞重金屬解毒中起著關鍵作用[29]。Cui等[30]對水稻細胞的形態(tài)學研究顯示, Cd脅迫下細胞器的完整性發(fā)生了嚴重的破壞, 而通過添加納米硅, 即使在高濃度Cd情況下細胞也幾乎保持完整。Guo等認為, Si對植物細胞結構的積極作用主要體現(xiàn)為恢復葉綠體的基粒片層和膜結構并增加線粒體嵴的數(shù)量[26,28]。此外, Si可提高細胞壁再生率、降低原生質體對重金屬的吸收, 從而增加細胞原生質體再生能力和活力[31]。

可見, 硅可通過修復受損結構、增加根部營養(yǎng)吸收、抑制根部對重金屬的吸收、改善植物細胞超微結構障礙, 促進受重金屬脅迫植物正常生長發(fā)育, 有利于維持植物細胞和組織的構造的完整性。這些生理學、形態(tài)學和超微結構變化與硅參與植物體內多種調控和防御機制相關。

2 調控植物基因表達

2.1 轉運基因表達

重金屬脅迫下硅參與植物體內的多種調控, 硅的施用促進了Lsi1、Lsi2和Lsi6三個硅轉運蛋白的表達[32], Lsi1和Lsi2主要定位在根部, 分別位于外胚層和內胚層細胞的遠端和近端, 負責硅的吸收和外排; Lsi6主要位于木質部薄壁細胞, 參與硅的卸載[10,32]。此外, 在植物營養(yǎng)吸收上, 硅差異調控了與N、P、K運轉利用相關的12個關鍵基因(NR、NIR、AMT、NR、GS、GOGAT、PT、PHT1、PHT2、APase、KAT1和HAK10), 提高了植物體內的常量和微量元素含量, 確保了植物正常生長[32,34]。

硅修飾的基因表達影響著植物體內多種轉運蛋白活性, 在減少重金屬吸收以及增強植物營養(yǎng)吸收等方面發(fā)揮重要作用[35–36]。研究表明, 重金屬轉運ATP酶(HMA)、低親和力陽離子轉運蛋白(LCT)和天然抗性相關巨噬細胞蛋白(Nramp)可調控多種植物體內重金屬的吸收和轉運, 且不同的金屬轉運蛋白在不同組織中的表達具有完全不同的意義[37–39]。Peng發(fā)現(xiàn)Nramp5主要在根部表達, 負責將Cd從土壤轉運到根細胞[40], 而Nramp1定位于質膜上, 參與植物體內的Cd運輸[38]。Greger等研究發(fā)現(xiàn)硅可通過抑制LCT1和HMA2基因的表達降低小麥吸收和轉運Cd的能力[33]。與之相反, 硅增強擬南芥對銅超耐受性與轉運蛋白SvHMA5I和SvHMA5II基因表達增強有關[41]。

2.2 植物螯合物合成與分泌

植物體內的螯合作用降低了游離重金屬的含量。硅可促進植物螯合肽(PCs)和金屬硫蛋白(MTs)兩類不同的富含半胱氨酸的蛋白螯合劑的合成[28], 在重金屬解毒的中起著重要作用。研究發(fā)現(xiàn), 在As、Cd、Cu、Hg和Pb等重金屬離子脅迫條件下, 還原型谷胱甘肽通過PC酶合成植物螯合肽[42–43], 并與重金屬形成復合物, 然后通過腺苷三磷酸結合盒式轉運蛋白運輸?shù)揭号莼蚣毎庑纬煞€(wěn)定螯合物[44-45]。MTs是重金屬脅迫下誘導基因編碼而成, 是一種富含硫的蛋白質, 在大多數(shù)被子植物中均有發(fā)現(xiàn)[43]。與PCs類似, MTs可與金屬離子結合, 有助于降低細胞液環(huán)境的金屬毒性[29]。

另一方面, 硅促進黃酮類(如, 槲皮素)、酚類化合物(如, 兒茶素)和有機酸(如, 檸檬酸、蘋果酸和烏頭酸)等螯合物的分泌, 限制了重金屬的遷移[46-47]。多胺和氨基酸在隔離重金屬方面也起著重要作用。Bosnic發(fā)現(xiàn)硅供給顯著增加Cu暴露下黃瓜植株葉片中螯合物煙堿胺(NA)和組氨酸(His)的濃度, 使NA: Cu和His: Cu摩爾比超過了控制值, 增強了植株對銅的耐受性[48]。然而, 關于Si對這些蛋白質活性和豐度影響的信息還很缺乏, Si緩解重金屬脅迫的機制在分子和遺傳水平上還不清楚。需要更多的遺傳實驗來確定Si與重金屬脅迫之間的連鎖關系, 以研究金屬和Si在不同植物中的運輸、沉積和轉運相關基因的表達水平。

3 增強植物抗氧化防御系統(tǒng)

3.1 抑制氧化應激產物的產生

植物在細胞器的光合作用和呼吸過程中可代謝產生了活性氧(ROS)[30,49], 而在重金屬脅迫作用下, 線粒體、葉綠體和過氧化物酶體等細胞器代謝產生過量ROS, 包括單線態(tài)氧(1O2), 超氧陰離子(O2-), 過氧化氫(H2O2)和羥基自由基(·OH)等[19,50], 這些活性氧可對蛋白質、DNA和脂質造成嚴重的氧化損傷[51–52]。同時, 重金屬脅迫造成丙二醛(MDA)、電解質滲漏(EL)等脂質過氧化物增加, 導致細胞內酶活性和氨基酸失調以及蛋白質氧化, 使植物生長受抑制[26,53–55]。研究顯示, 硅降低了Cd、Pb、As、Al、Ni、Cu、Cr等重金屬脅迫下小麥、水稻、玉米、芥菜、棉花等植物葉片和根系的ROS、MDA和EL等的含量, 在維持細胞結構完整以及光合氣體交換上發(fā)揮重要作用[19,24,44,56–58]。

3.2 增加酶類抗氧化劑的產生

酶類抗氧化劑是抵抗ROS的第一道防線。硅普遍增加了這些酶類抗氧化劑在植物體內的含量, 在降低膜脂過氧化, 保護植物細胞免受氧化損傷發(fā)揮著作用[51,59]。超氧化物歧化酶(SOD)能有效地清除葉綠體中的超氧陰離子自由基[49,60]; 過氧化氫酶(CAT)位于植物細胞的過氧化物酶體中, 其主要作用是催化SOD反應產生的H2O2[57,61–62]; 抗壞血酸過氧化物酶(APX)在多種細胞器以不同形式出現(xiàn)并發(fā)揮著作用, 在清除H2O2上發(fā)揮著作用[19,63]; 愈創(chuàng)木酚過氧化物酶(POD)主要對抗細胞壁中的自由基[64]; 而乙醛酶系統(tǒng)(GlyⅠ和GlyⅡ)酶參與者甲基乙二醛(MG)的解毒[65]。Geng等研究表明, 硅顯著提高受有機砷污染的水稻植株SOD、CAT和POD活性, 暗示了硅積極參與活性氧的清除并緩解了有機砷的毒害[49]。

3.3 增加非酶類抗氧化劑的產生

非酶抗氧化劑是抵御ROS的第二道防線。抗壞血酸(ASA)是一種在線粒體中合成的水溶性抗氧化劑, 可以直接清除細胞內的ROS, 并作為APX的反應基質, 是植物細胞中最有效的抗氧化劑[32]; 谷胱甘肽(GSH)是另一種重要的水溶性抗氧化劑, 而類胡蘿卜素是一類酚類化合物, 他們在清除葉綠體中的1O2和·OH方面發(fā)揮著重要作用[66–67]; 生育酚(TCP)最重要的作用是可以清除類囊體膜中產生的1O2、O2-和·OH[54]。研究發(fā)現(xiàn), 硅的應用使植物組織及細胞中非酶抗氧化劑水平上升, 顯著提高了Cd脅迫植物的生長發(fā)育、總蛋白含量和膜穩(wěn)定性[49,54,68]。

3.4 硅介導酶/非酶抗氧化劑清除ROS機制

在重金屬脅迫下, Si可抑制植物體內氧化應激物的產生, 并通過激活酶和非酶抗氧化系統(tǒng)來降低植物細胞氧化損傷, 其作用機制如圖2所示。然而, 抗氧化酶活性與植物種類、年齡、硅調節(jié)時間和條件有關[69–71], 同時, Si促進抗氧化劑活性的增強只在溫和的金屬脅迫下起作用, 在較高的金屬濃度下添加Si將導致SOD等酶活性顯著降低[71]。

注: 酶類: 超氧化物歧化酶(SOD), 過氧化氫酶(CAT), 抗壞血酸過氧化物酶(APX), 脫氫抗壞血酸還原酶(DHAR), 谷胱甘肽過氧化物酶(GPX), 谷胱甘肽S-轉移酶(GST), 單脫氫抗壞血酸還原酶(MDHAR), 谷胱甘肽還原酶(GR)。非酶類: 抗壞血酸(ASA), 脫氫抗壞血酸(DHA), 谷胱甘肽(GSH), 氧化型谷胱甘肽(GSSG), 生育酚(TCP), 類胡蘿卜素。

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

4 建立重金屬屏障

4.1 減少植物重金屬向地上部位傳輸

植物根部通過截留重金屬, 限制重金屬向地上部位運輸, 保證了植物的正常生長發(fā)育[24,44,73]。添加硅基改良劑后, 植物積累的As、Cr、Cd和Pb大部分保留在根中, 使根中重金屬的生物濃縮因子(BCF值)明顯高于枝條[74–75]。硅介導金屬脅迫下植物根部內胚層的形成, 是減少重金屬向地上部分遷移的重要機制之一[47]。Shi等[75]通過質外體熒光示蹤劑PTS證明了植物根部內胚層附近的硅沉積部分地物理阻斷了Cd通過根部質外體的旁路流動, 從而抑制了Cd通過質外體途徑向上運輸。

4.2 促進植物低代謝細胞器對重金屬隔離

硅在細胞壁中沉積并與重金屬結合[76–-77], 限制了重金屬的運輸, 是硅降低植物金屬毒性的機制之一[79–80]。通過X射線顯微和電感耦合等離子體質譜法分析, 發(fā)現(xiàn)Cd和Si主要在植物細胞的細胞壁中積累[30,81], 這是由于硅以有機硅化合物的形式積累在細胞壁中, 并與重金屬結合, 減少了重金屬向細胞質的遷移[82]。Ma等[83]發(fā)現(xiàn)當懸浮細胞的細胞壁中存在Si時, 植物細胞壁在Cd脅迫下表現(xiàn)出優(yōu)先積累金屬的位置, 主要是通過修飾壁多糖成分, 形成Si-半纖維素基質-Zn復合物來限制Cd的吸收, 減輕了Cd的細胞毒性。

液泡中含有各種類型的有機酸和蛋白質等能與重金屬離子結合, 在重金屬截留、鈍化和解毒方面發(fā)揮著重要作用[29,44], 而硅能有效地促進了重金屬從原生質體到液泡的轉運[84]。在重金屬脅迫下, 硅可促進液泡膜上H+-焦磷酸化酶(OVP)和ATPase酶(V-ATPase)的表達, 這兩種酶提供了驅動金屬離子和其他分子進入液泡的質子梯度[85-86]。類似的, 硅增強了重金屬轉運ATP酶3(HMA3)的表達, 使重金屬轉運進入液泡[30]。

可見, 通過限制植物體內重金屬遷移和金屬在組織、器官區(qū)域化影響是Si促進植物緩解重金屬脅迫的重要機制。然而, 這一機制因植物種類、基因類型和重金屬種類不同而存在較大差異[87]。

5 結論與展望

硅通過單個或多個機制的聯(lián)合作用調控植物生長發(fā)育, 在緩解植物重金屬脅迫上發(fā)揮著重要作用。其生物學機制體現(xiàn)在減少重金屬吸收及增強植物重金屬耐受能力兩方面, 通過調控基因表達、增強植物抗氧化能力及建立重金屬屏障等促使植物恢復正常細胞結構和生長狀態(tài)。然而, 這些機制可能與植物種類、基因類型、重金屬種類、生長條件、脅迫時間等因素有關, 其作用機制極為復雜, 需重點開展的研究工作主要包括: (1)多金屬復合污染自然土壤環(huán)境下活性硅緩解植物重金屬脅迫的協(xié)同機制; (2)活性硅在土壤中的老化機理及其對植物重金屬脅迫緩解的長效機制; (3)新型活性硅材料的研制、施加工藝與修復效應。

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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, 陳濤, 蔣少軍, 等. 活性硅緩解植物重金屬脅迫及其生物學機制研究進展[J]. 生態(tài)科學, 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

國家重點研發(fā)計劃項目(2018YFC1802803); NSFC-廣東省聯(lián)合基金(U1901218)

林翰志(1993—), 男, 廣東陽江人, 博士研究生, 主要從事土壤重金屬污染修復研究, E-mail: xtulhz@126.com

晏波, 男, 博士, 教授, 主要從事資源綜合利用, 水污染控制, 土壤重金屬污染修復研究, E-mail: bo.yan@m.scnu.edu.cn