Chinese Journal OF Rice Science >
Effects of Silicon on Antioxidant Enzyme System and Expression Levels of Genes Related to Cd2+ Uptake and Transportation in Rice Seedlings Under Cadmium Stress
#These authors contributed equally to this work
Received date: 2023-02-14
Revised date: 2023-03-22
Online published: 2023-09-13
【Objective】 To elucidate the effects of exogenous silicon (Si) on plant height, dry weight, antioxidant enzyme system, and the expression levels of Cd2+ related genes in rice under cadmium (Cd) stress, so as to lay a theoretical basis for clarifying the mechanism of Si in alleviating Cd toxicity in rice. 【Method】 Indica rice Fupin 36 (FP36) and Zhongjiazao 17 (ZJZ17) were hydrocultured under two Cd2+ concentrations (0, 5 µmol/L) and three Si treatments (0, 10 µmol/L, 1 mmol/L). The agronomic traits, antioxidant enzyme activities, and the expression levels of Cd2+ uptake/transport-related genes were analyzed. 【Result】 Cadmium stress significantly inhibited the agronomic traits and activities of antioxidant enzymes (superoxide dismutase, peroxidase, catalase, and ascorbic acid oxidase) of ZJZ17 and FP36, but exogenous Si addition could effectively alleviate the toxicity of Cd to rice, and enhance the activities of antioxidant enzymes. Moreover, 1 mmol/L Si treatment exerted a better alleviating effect on Cd stress than 10 µmol/L Si. In addition, Cd stress also affected the contents of soluble protein and malondialdehyde (MDA) in rice, while Si exposure increased soluble protein content but decreased the MDA content, respectively. Cd intervention significantly increased Cd content in different tissues of FP36 and ZJZ17, and its accumulation in roots was significantly higher than that in shoots. However, there was no significant difference in Cd content in rice plants under 10 µmol/L Si addition; and Cd accumulation in rice was significantly decreased as exposed to 1 mmol/L Si at 5 µmol/L Cd2+ concentration, indicating that the Cd accumulation in shoots was higher than that in roots. The expression levels of Cd2+ uptake/transport-related genes followed different trends as subjected to Cd stress and Si treatments. Compared with zero-Cd treatment, the expression levels of OsNRAMP1, OsIRT1 and OsHMA2 were up-regulated under Cd stress, while OsNRAMP5 expression tended to be down-regulated, and the expression level of OsHMA3 remained unchanged. Moreover, the expression levels of OsNRAMP1, OsNRAMP5, OsIRT1, OsHMA2, OsHMA3 were significantly decreased at 1 mmol/L Si concentration. 【Conclusion】 Silicon alleviates the toxicity of Cd to rice by improving the agronomic traits, activating the antioxidant system, and regulating the expression levels of Cd2+ uptake/transport-related genes.
Key words： rice; cadmium stress; silicon; antioxidase system; relative expression of genes
HUANG Qina, XU Youxiang, LIN Guanghao, DANG Hongyang, ZHENG Zhenquan, ZHANG Yan, WANG Han, SHAO Guosheng, YIN Xianyuan . Effects of Silicon on Antioxidant Enzyme System and Expression Levels of Genes Related to Cd2+ Uptake and Transportation in Rice Seedlings Under Cadmium Stress[J]. Chinese Journal OF Rice Science, 2023 , 37(5) : 486 -496 . DOI: 10.16819/j.1001-7216.2023.230203
| [1] | Chang C, Yin R, Zhang H, Yao L. Bioaccumulation and health risk assessment of heavy metals in the soil-rice system in a typical seleniferous area in Central China[J]. Environmental?Toxicology and Chemistry, 2019, 38(7): 1577-1584. |
| [2] | Mclaughlin M J, Whatmuff M, Warne M, Heemsbergen D, Barry G, Bell M, Nash D, Pritchard D. A field investigation of solubility and food chain accumulation of biosolid-cadmium across diverse soil types[J]. Environmental Chemistry, 2006, 3: 428-432. |
| [3] | Ismael M A, Elyamine A M, Moussa M G, Cai M, Zhao X, Hu C. Cadmium in plants: Uptake, toxicity, and its interactions with selenium fertilizers[J]. Metallomics, 2019, 11(2): 255-277. |
| [4] | Uraguchi S, Kiyono M, Sakamoto T, Watanabe I, Kuno K. Contributions of apoplasmic cadmium accumulation, antioxidative enzymes and induction of phytochelatins in cadmium tolerance of the cadmium-accumulating cultivar of black oat (Avena strigosa Schreb.)[J]. Planta, 2009, 230(2): 267-276. |
| [5] | Wu Z, Yin X, Bañuelos G S, Lin Z Q, Liu Y, Li M, Yuan L. Indications of selenium protection against cadmium and lead toxicity in oilseed rape (Brassica napus L.)[J]. Frontiers in?Plant?Science, 2016, 7: 1875. |
| [6] | 戴青云, 刘代欢, 王德新, 李鹏祥, 朱维, 桂娟. 硅对水稻生长的影响及其缓解镉毒害机理研究进展[J]. 中国农学通报, 2020, 36(5): 86-92. |
| [6] | Dai Q Y, Liu D H, Wang D X, Li P X, Zhu W, Gui J. A review on silicon: Effect on rice growth and its mechanism of relieving cadmium toxicity[J]. Chinese Agricultural Science Bulletin, 2020, 36(5): 86-92. (in Chinese with English abstract) |
| [7] | Khan I, Awan S A, Rizwan M, Ali S, Hassan M J, Brestic M, Zhang X, Huang L. Effects of silicon on heavy metal uptake at the soil-plant interphase: A review[J]. Ecotoxicology and Environmental Safety, 2021, 222: 112510. |
| [8] | 高子翔, 周航, 杨文弢, 辜娇峰, 陈立伟, 杜文琪, 徐珺, 廖柏寒. 基施硅肥对土壤镉生物有效性及水稻镉累积效应的影响[J]. 环境科学, 2017(12): 5299-5307. |
| [8] | Gao Z X, Zhou H, Yang W T, Gu J F, Chen L W, Du W Q, Xu J, Liao B H. Impacts of silicon fertilizer as base manure on cadmium bioavailability in soil and on cadmium accumulation in rice plants[J]. Environmental Science, 2017(12): 5299-5307. (in Chinese with English abstract) |
| [9] | 魏晓, 张鹏博, 赵丹丹, Bocharnikova E, Matichenkov V, Dmitry D. 水稻土施硅对土壤-水稻系统中镉的降低效果[J]. 生态学报, 2018, 38(5): 1600-1606. |
| [9] | Wei X, Zhang P B, Zhao D D, Elena B, Vladimir M, Demin D. Cadmium status in paddy soil in a rice system under silicon fertilization[J]. Acta Ecologica Sinica, 2018, 38(5): 1600-1606. (in Chinese with English abstract) |
| [10] | 秦淑琴, 黄庆辉. 硅对水稻吸收镉的影响[J]. 新疆环境保护, 1997, 19(3): 51-53. |
| [10] | Qin S Q, Huang Q H. Effect of silicon on cadmium uptake by rice[J]. Environmental Protection of Xingjiang, 1997, 19(3): 51-53. (in Chinese with English abstract) |
| [11] | 郑文杰, 卢剑, 刘模发. 施用液体硅肥降低稻米中镉含量效果研究[J]. 现代化农业, 2016(7): 30-31. |
| [11] | Zheng W J, Lu J, Liu M F. Effect of liquid silicon fertilizer on reducing cadmium content in rice[J]. Modernization Agriculture, 2016(7): 30-31. (in Chinese with English abstract) |
| [12] | Wang H Y, Wen S L, Chen P, Zhang L, Cen K, Sun G X. Mitigation of cadmium and arsenic in rice grain by applying different silicon fertilizers in contaminated fields[J]. Environmental Science and Pollution Research International, 2016, 23(4): 3781-3788. |
| [13] | 赵明柳, 唐守寅, 董海霞, 李荭荭, 吴竹麟, 黄俊星, 王果. 硅酸钠对重金属污染土壤性质和水稻吸收Cd Pb Zn的影响[J]. 农业环境科学学报, 2016, 35(9): 1653-1659. |
| [13] | Zhao M L, Tang S Y, Dong H X, Li H H, Wu Z L, Huang J X, Wang G. 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. (in Chinese with English abstract) |
| [14] | Nwugo C C, Huerta A J. Silicon-induced cadmium resistance in rice (Oryza sativa)[J]. Journal of Plant Nutrition and Soil Science, 2008, 171(6):841-848. |
| [15] | 龚金龙, 张洪程, 龙厚元, 胡雅杰, 戴其根, 霍中洋, 许轲, 魏海燕, 高辉. 水稻中硅的营养功能及生理机制的研究进展[J]. 植物生理学报, 2012, 48(1): 1-10. |
| [15] | Gong J L, Zhang H C, Long H Y, Hu Y J, Dai Q G, Huo Z Y, Xu K, Wei H Y, Gao H. Progress in research of nutrition functions and physiological mechanisms of silicon in rice[J]. Plant Physiology Journal, 2012, 48 (1): 1-10. (in Chinese with English abstract) |
| [16] | 胡瑞芝, 方水娇, 陈桂秋. 硅对杂交水稻生理指标及产量的影响[J]. 湖南农业大学学报: 自然科学版, 2001, 27(5): 335-338. |
| [16] | Hu R Z, Fang S J, Chen G Q. Effects of silicon on the physiological targets and yield of hybrid rice[J]. Journal of Hunan Agricultural University: Natural Sciences, 2001, 27(5): 335-338. (in Chinese) |
| [17] | Enstone D E, Peterson C A, Ma F. Root endodermis and exodermis: Structure, function, and responses to the environment[J]. Journal of Plant Growth Regulation, 2002, 21: 335-351. |
| [18] | Sasaki A, Yamaji N, Yokosho K, Ma J F. Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice[J]. Plant Cell, 2012, 24(5): 2155-2167. |
| [19] | Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, Arao T, Nakanishi H, Nishizawa N K. The OsNRAMP1 iron transporter is involved in Cd accumulation in rice[J]. Journal of Experimental Botany, 2011, 62(14): 4843-4850. |
| [20] | Nakanishi H, Ogawa I, Ishimaru Y, Mori S, Nishizawa N K. Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice[J]. Soil Science and Plant Nutrition, 2006, 52(4): 464-469. |
| [21] | Ishimaru Y, Takahashi R, Bashir K, Shimo H, Senoura T, Sugimoto K, Ono K, Yano M, Ishikawa S, Arao T, Nakanishi H, Nishizawa N K. Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport[J]. Scientific Reports, 2012, 2: 286. |
| [22] | Takahashi R, Ishimaru Y, Shimo H, Ogo Y, Senoura T, Nishizawa N K, Nakanishi H. The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice[J]. Plant Cell Environment, 2012, 35(11): 1948-1957. |
| [23] | Sasaki A, Yamaji N, Ma J F. Overexpression of OsHMA3 enhances Cd tolerance and expression of Zn transporter genes in rice[J]. Journal of Experimental Botany, 2014, 65(20): 6013-6021. |
| [24] | Kim Y H, Khan A L, Kim D H, Lee S Y, Kim K M, Waqas M, Jung H Y, Shin J H, Kim J G, Lee I J. Silicon mitigates heavy metal stress by regulating P-type heavy metal ATPases, Oryza sativa low silicon genes, and endogenous phytohormones[J]. BMC Plant Biology, 2014, 14: 13. |
| [25] | Ma J, Cai H, He C, Zhang W, Wang L. A hemicellulose-bound form of silicon inhibits cadmium ion uptake in rice (Oryza sativa) cells[J]. New Phytologist, 2015, 206(3): 1063-1074. |
| [26] | Adrees M, Ali S, Rizwan M, Zia-Ur-Rehman M, Ibrahim M, Abbas F, Farid M, Qayyum M F, Irshad M K. Mechanisms of silicon-mediated alleviation of heavy metal toxicity in plants: A review[J]. Ecotoxicology and Environmental Safety, 2015, 119: 186-197. |
| [27] | Chen D, Chen D, Xue R, Long J, Lin X, Lin Y, Jia L, Zeng R, Song Y. Effects of boron, silicon and their interactions on cadmium accumulation and toxicity in rice plants[J]. Journal of Hazardous Materials, 2019, 367: 447-455. |
| [28] | Liu J, Ma J, He C, Li X, Zhang W, Xu F, Lin Y, Wang L. Inhibition of cadmium ion uptake in rice (Oryza sativa) cells by a wall-bound form of silicon[J]. New Phytologist, 2013, 200(3): 691-699. |
| [29] | 李江遐, 张军, 马友华, 蔡慢弟, 高飞. 硅对镉胁迫条件下两个水稻品种镉亚细胞分布、非蛋白巯基物质含量的影响[J]. 农业环境科学学报, 2018, 36(6): 1066-1071. |
| [29] | Li J, Zhang J, Ma Y, Cai M D, Gao F. Effects of silicon on cadmium accumulation and non-protein thiol content in the seedlings of two rice varieties under cadmium stress[J]. Journal of Agro-Environment Science, 2018, 37(6): 1066-1071. (in Chinese with English abstract) |
| [30] | Riaz M, Kamran M, Rizwan M, Ali S, Parveen A, Malik Z, Wang X. Cadmium uptake and translocation: Selenium and silicon roles in Cd detoxification for the production of low Cd crops: A critical review[J]. Chemosphere, 2021, 273: 129690. |
| [31] | Zhou Q, Shao G S, Zhang Y X, Dong Q, Wang H, Chen S H, Cao L Y, Shen X H. The difference of cadmium accumulation between the indica and japonica subspecies and the mechanism of it[J]. Plant Growth Regulation, 2017, 81: 523-532. |
| [32] | Huang Q N, An H, Yang Y J, Liang Y, Shao G S. Effects of Mn-Cd antagonistic interaction on Cd accumulation and major agronomic traits in rice genotypes by different Mn form[J]. Plant Growth Regulation, 2017, 82: 317-331. |
| [33] | 赵世杰, 苍晶. 植物生理学实验指导[M]. 北京: 中国农业出版社, 2015: 143-145, 225-236. |
| [33] | Zhao S J, Cang J. Laboratory Guides for Plant Physiology[M]. Beijing: Chinese Agricultural Science and Technology Press, 2015: 143-145, 225-236. (in Chinese with English abstract) |
| [34] | Huang Q N, Wu Y L, Shao G S. Root aeration promotes the cadmium accumulation in rice by regulating the iron uptake system[J]. Rice Science, 2021, 28(5): 511-520. |
| [35] | Livak K J, Schmittgen T D. Analysis of relative gene expression data using real time quantitative PCR and the 2-ΔΔct method[J]. Methods, 2001, 25: 402-408. |
| [36] | 陈喆, 张淼, 叶长城, 毛懿德, 周细红, 雷鸣, 魏祥东, 铁柏清. 富硅肥料和水分管理对稻米镉污染阻控效果研究[J]. 环境科学学报, 2015, 35(12): 4003-4011. |
| [36] | Chen Z, Zhang M, Ye C C, Mao Y D, Zhou X H, Lei M, Wei X D, Tie B Q. Mitigation of Cd accumulation in rice (Oryza sativa L.) with Si fertilizers and irrigation managements[J]. Acta Scientiae Circumstantiae, 2015, 35(12): 4003-4011. (in Chinese with English abstract) |
| [37] | 李园星露, 叶长城, 刘玉玲, 李丹阳, 刘寿涛, 罗海艳, 刘孝利, 铁柏清, 孙健. 硅肥耦合水分管理对复合污染稻田土壤As-Cd生物有效性及稻米累积阻控[J]. 环境科学, 2018, 39(2): 944-952. |
| [37] | LI-Yuan X L, Ye C C, Liu Y L, Li D Y, Liu S T, Luo H Y, Liu X L, Tie B Q, Sun J. Bioavailability of silicon fertilizer coupled water management on soil bioavailability and cumulative control of rice in compound contaminated paddy soils[J]. Environmental Science, 2018, 39(2): 944-952. (in Chinese with English abstract) |
| [38] | Vaculík M, Lux A, Luxová M, Tanimoto E, Lichtscheidl I. Silicon mitigates cadmium inhibitory effects in young maize plants[J]. Environmental and Experimental Botany, 2009, 67(1): 52-58. |
| [39] | Vatehová Z, Kollárová K, Zelko I, Richterová-Kučerová D, Bujdoš M, Lišková D. Interaction of silicon and cadmium in Brassica juncea and Brassica napus[J]. Biologia, 2012, 67(3): 498-504. |
| [40] | Guo B, Liu C, Ding N F, Fu Q L, Li N Y. Silicon alleviates cadmium toxicity in two cypress varieties by strengthening the exodermis tissues and stimulating phenolic exudation of roots[J]. Journal of Plant Growth Regulation, 2016, 35(2): 420-429. |
| [41] | Wu J, Guo J, Hu Y, Gong H. Distinct physiological responses of tomato and cucumber plants in silicon-mediated alleviation of cadmium stress[J]. Frontiers in Plant Science, 2015, 6: 453. |
| [42] | Shi G R, Zhang Z, Liu C F. Silicon influences cadmium translocation by altering subcellular distribution and chemical forms of cadmium in peanut roots[J]. Archives of Agronomy and Soil Science, 2017, 63(1) : 117-123. |
| [43] | Wang H Y, Wen S L, Chen P, Zhang L, Cen K, Sun G X. Mitigation of cadmium and arsenic in rice grain by applying different silicon fertilizers in contaminated fields[J]. Environmental Science and Pollution Research International, 2016, 23(4): 3781-3788. |
| [44] | Wang Y C, Hu Y H, Duan Y K, Feng R, Gong H. Silicon reduces long-term cadmium toxicities in potted garlic plants[J]. Acta Physiologiae Plantarum, 2016, 38: 211. |
| [45] | Cui J, Liu T, Li F, Yi J, Liu C, Yu H. Silica nanoparticles alleviate cadmium toxicity in rice cells: Mechanisms and size effects[J]. Environmental Pollution, 2017, 228: 363-369. |
| [46] | Bhat J A, Shivaraj S M, Singh P, Navadagi D B, Tripathi D K, Dash P K, Solanke A U, Sonah H, Deshmukh R. Role of silicon in mitigation of heavy metal stresses in crop plants[J]. Plants (Basel), 2019, 8(3): 71. |
| [47] | Cui J, Li Y, Jin Q, Li F. Silica nanoparticles inhibit arsenic uptake into rice suspension cells via improving pectin synthesis and the mechanical force of the cell wall[J]. Environmental Science: Nano, 2020, 7: 162-171. |
| [48] | 赵颖, 李军. 硅对水稻吸收镉的影响[J]. 东北农业大学学报, 2010, 41(3): 59-64. |
| [48] | Zhao Y, Li J. Effect of silicon on cadmium uptake by rice[J]. Journal of Northeast Agricultural University, 2010, 41(3): 59-64. (in Chinese with English abstract) |
| [49] | Shi X H, Zhang C C, Wang H, Zhang F S. Effect of Si on the distribution of Cd in rice seedlings[J]. Plant and Soil, 2005, 272: 53-60. |
| [50] | Guo L, Chen A, He N, Yang D, Liu M D. Exogenous silicon alleviates cadmium toxicity in rice seedlings in relation to Cd distribution and ultrastructure changes[J]. Journal of Soils and Sediments, 2018, 18: 1691-1700. |
| [51] | 黄秋蝉, 黎晓峰, 沈方科, 阳继辉, 李耀燕, 张维珺. 硅对水稻幼苗镉的解毒作用及其机制研究[J]. 农业环境科学学报, 2007, 26(4): 1307-1311. |
| [51] | Huang Q C, Li X F, Shen F K, Yang J H, Li Y Y, Zhang W J. Cadmium resistance improved by silicon and corresponding mechanisms in Oryza sativa L. seedlings[J]. Journal of Agro-Environment Science, 2007, 26(4): 1307-1311. (in Chinese with English abstract) |
| [52] | 孙梦梦, 徐劼, 张玲玲, 施德剑, 赵玺童. 硅对镉胁迫下植物生长影响的研究进展[J]. 广州化工, 2019, 47(13): 41-43. |
| [52] | Sun M M, Xu J, Zhang L L, Shi D J, Zhao X T. Research progress on effects of silicon on plant growth under cadmium stress[J]. Guangzhou Chemical Industry, 2019, 47(13): 41-43. (in Chinese with English abstract) |
| [53] | Farooq M A, Ali S, Hameed A, Ishaque W, Mahmood K, Iqbal Z. Alleviation of cadmium toxicity by silicon is related to elevated photosynthesis, antioxidant enzymes; suppressed cadmium uptake and oxidative stress in cotton[J]. Ecotoxicology and Environmental Safety, 2013, 96: 242-249. |
| [54] | Feng J, Shi Q, Wang X, Wei M, Yang F, Xu H. Silicon supplementation ameliorated the inhibition of photosynthesis and nitrate metabolism by cadmium (Cd) toxicity in Cucumis sativus L[J]. Scientia Horticulturae, 2010, 123(4): 521-530. |
| [55] | Keller C, Rizwan M, Davidian J C, Pokrovsky O S, Bovet N, Chaurand P, Meunier J D. Effect of silicon on wheat seedlings (Triticum turgidum L.) grown in hydroponics and exposed to 0 to 30 μM Cu[J]. Planta, 2015, 241(4): 847-860. |
| [56] | 贾茜茹, 刘奋武, 樊文华. 硅对Cd胁迫下黄瓜苗期光合及抗氧化酶系统的影响[J]. 水土保持学报, 2018, 32(4): 321-326. |
| [56] | Jia Q R, Liu F E, Fan W H. Effects of silicon on photosynthesis and antioxidant enzymes of cucumber seedling under cadmium stress[J]. Journal of Soil and Water Conservation, 2018, 32(4): 321-326. (in Chinese with English abstract) |
| [57] | 孟红梅, 汤燕. 硅对镉胁迫下板蓝根种子萌发及生理特性的影响[J]. 种子, 2011, 30(11): 37-40. |
| [57] | Meng H M, Tang Y. Effect of silicon on radix isatidis seed germination and seedings growth phyiological characteristics under cadmium stress[J]. Seed, 2011, 30(11): 37-40. (in Chinese with English abstract) |
| [58] | Wang S H, Wang F Y, Gao S C. Foliar application with nano-silicon alleviates Cd toxicity in rice seedlings[J]. Environmental Science and Pollution Research International, 2015, 22(4): 2837-2845. |
| [59] | Srivastava R K, Pandey P, Rajpoot R, Rani A, Gautam A, Dubey R S. Exogenous application of calcium and silica alleviates cadmium toxicity by suppressing oxidative damage in rice seedlings[J]. Protoplasma, 2015, 252(4): 959-975. |
| [60] | Wu Z, Wang F, Liu S, Du Y, Li F, Du R, Wen D, Zhao J. Comparative responses to silicon and selenium in relation to cadmium uptake, compartmentation in roots, and xylem transport in flowering Chinese cabbage (Brassica campestris L. ssp. chinensis var. utilis) under cadmium stress[J]. Environment and Experimental Botany, 2016, 131: 173-180. |
| [61] | Miyadate H, Adachi S, Hiraizumi A, Tezuka K, Nakazawa N, Kawamoto T, Katou K, Kodama I, Sakurai K, Takahashi H, Satoh-Nagasawa N, Watanabe A, Fujimura T, Akagi H. OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles[J]. New Phytologist, 2011, 189(1): 190-199. |
| [62] | Zhang X F, Hu Z H, Yan T X, Lu R R, Peng C L, Li S S, Jing Y X. Arbuscular mycorrhizal fungi alleviate Cd phytotoxicity by altering Cd subcellular distribution and chemical forms in Zea mays[J]. Ecotoxicology and Environmental Safety, 2019, 171: 352-360. |
| [63] | Huang H, Li M, Rizwan M, Dai Z, Yuan Y, Hossain M M, Cao M, Xiong S, Tu S. Synergistic effect of silicon and selenium on the alleviation of cadmium toxicity in rice plants[J]. Journal of Hazardous Materials, 2021, 401: 123393. |
/
| 〈 |
|
〉 |