Welcome to Acta Agronomica Sinica,

Acta Agronomica Sinica ›› 2023, Vol. 49 ›› Issue (7): 1979-1993.doi: 10.3724/SP.J.1006.2023.24160

• TILLAGE & CULTIVATION·PHYSIOLOGY & BIOCHEMISTRY • Previous Articles     Next Articles

Exogenous salicylic acid improves the tolerance of Yunma 1 (Cannabis sativa L.) to copper stress

XIANG Jia-Ming(), DAI Qian, LIU Li-Jun*()   

  1. College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, Hubei, China
  • Received:2022-07-11 Accepted:2022-11-25 Online:2023-07-12 Published:2023-01-11
  • Contact: *E-mail: liulijun@mail.hzau.edu.cn E-mail:dicerx@163.com;liulijun@mail.hzau.edu.cn
  • Supported by:
    The China Agriculture Research System of MOF and MARA(麻类);The China Agriculture Research System of MOF and MARA(CARS-16-E10)

Abstract:

Industrial hemp is an important natural fiber crop in China. Its main planting areas are richer in copper mines, and the cultivated soil is seriously polluted by copper. Industrial hemp has strong copper tolerance and high biomass and can replace food crops on copper-contaminated soils. It is of great significance to explore how to enhance its copper tolerance. Salicylic acid (SA) plays an important role in plant stress resistance. In this study, to explore the effect of exogenous SA on the copper tolerance and copper enrichment of industrial hemp under copper stress, the copper-sensitive variety Yunma 1 was used as the experimental material. The results showed that copper stress had obvious toxic effects on industrial hemp. Exogenous SA reduced the copper content of hemp fibers and enhanced the absorption and fixation of Cu2+ in roots. The copper content in underground and the copper accumulation were 1610.1% and 857.1% in stress group, respectively, which may be achieved by improving the metabolism of hemicellulose and xyloglucan and the activity of glucosidase. Exogenous SA promoted the photosynthesis and dry matter accumulation of industrial hemp under copper stress, enhanced significantly the oxidoreductase activity, decreased ROS and MDA content, and reduced oxidative damage. The application of exogenous SA under copper stress can specifically induce the relative expression level of CsCIPK25 and CsWRKY32, and enhance the tolerance of industrial hemp under copper stress by regulating ion transport, and copper absorption immobilization, and metal chelate synthesis.

Key words: industrial hemp, copper stress, salicylic acid, the relative expression level of genes

Table 1

Basic information of copper tailings and common soil"

土壤
Soil
全氮含量
Total nitrogen content
(g kg-1)
全磷含量
Total phosphorus content (g kg-1)
全钾含量
Total potassium content (g kg-1)
总铜含量
Total copper content (mg kg-1)
铜尾矿砂Copper tailing sand 0.0252 0.542 0.61 1110.72
普通土壤Ordinary soil 1.9148 0.904 4.09 33.35

Table 2

Primers for qRT-PCR"

基因
Gene name
正义引物
Forward primer (5°-3°)
反义引物
Reverse primer (5°-3°)
CsCIPK25 GAAATGCTCTGCCTTGGCTAT GTGCCACCTCGTAAACCTCC
CsWRKY32 ATCATTTTGGGCATGTAACGGA TTGGCAGATGTGGATGGGTC
CsUBQ TACTGCGCCAGCTAACAAACC GCACCCGTCTGACCTGAATC

Fig. 1

Effects of copper stress and SA spraying on root growth of Yunma 1 at seedling stage C0: no Cu treatment; C1: copper stress; S0: no SA treatment; S1: SA treatment. Different lowercase letters indicate significant differences between the treatments at P < 0.05."

Fig. 2

Effects of SA treatment on the growth of Yunma 1 under copper stress C0: the ordinary soil; C1: copper tailings sand; S0: no SA treatment; S1: SA treatment. Different lowercase letters indicate significant differences between the treatments at P < 0.05."

Table 3

Effects of exogenous SA on the growth of Yunma 1 under copper stress"

处理
Treatment
株高
Plant height (cm)
茎粗
Stem diameter (mm)
地上部干重
Above-ground dry weight (g)
地下部干重
Under-ground dry weight (g)
C0S0 204.71±5.76 ab 8.14±0.54 ab 27.19±0.81 a 2.53±0.50 ab
C0S1 206.11±7.24 a 8.91±0.37 a 28.51±2.68 a 2.76±0.61 a
C1S0 146.28±8.61 c 7.36±0.37 b 10.50±0.12 d 1.65±0.29 b
C1S1 195.00±6.73 b 8.90±0.58 a 22.74±1.54 bc 2.22±0.19 ab

Fig. 3

Effects of exogenous SA on reactive oxygen species scavenging system of Yunma 1 at seedling stage under copper stress Treatments are the same as those given in Fig. 1. Different lowercase letters indicate significant differences between the treatments at P < 0.05."

Fig. 4

Effects of exogenous SA on copper enrichment in Yunma 1 under copper stress ACC: the above-ground Cu content; UCC: under-ground Cu content; ACA: the above-ground Cu accumulation; UCA: under-ground Cu accumulation; FCC: fiber Cu content; GI: the germination index; VI: vigor index. Treatments are the same as those given in Fig. 2. Different lowercase letters indicate significant differences between the treatments at P < 0.05."

Fig. 5

Effects of copper stress and SA spraying on the differentially expressed genes of Yunma 1 at seedling stage A: Differential gene expression among treatments in transcriptome; B: Effects of exogenous SA on differential gene expression of industrial hemp under copper stress; C: Differential gene expression among all treatments in the transcriptome. Treatments are the same as those given in Fig. 1."

Fig. 6

GO analysis of differentially expressed genes Treatments are the same as those given in Fig. 1."

Fig. 7

KEGG analysis of differentially expressed genes Treatments are the same as those given in Fig. 1."

Fig. 8

Effects of SA treatment on the differentially expressed genes of Yunma 1 under copper stress Treatments are the same as those given in Fig. 1. Different lowercase letters indicate significant differences between the treatments at P < 0.05."

[1] 杨阳, 张云云, 苏文君, 杨明, 郭鸿彦, 刘飞虎. 工业大麻纤维特性与开发利用. 中国麻业科学, 2012, 34: 237-240.
Yang Y, Zhang Y Y, Su W J, Yang M, Guo H Y, Liu F H. Fiber properties and development and utilization of industrial hemp. Plant Fiber Sci China, 2012, 34: 237-240. (in Chinese with English abstract)
[2] Hänsch R, Mendel R R. Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol, 2009, 12: 259-266.
doi: 10.1016/j.pbi.2009.05.006 pmid: 19524482
[3] Palmer C M, Guerinot M L. Facing the challenges of Cu, Fe and Zn homeostasis in plants. Nat Chem Biol, 2009, 5: 333-340.
doi: 10.1038/nchembio.166 pmid: 19377460
[4] 温宗国, 季晓立. 中国铜资源代谢趋势及减量化措施. 清华大学学报(自然科学版), 2013, 53(9): 65-70.
Wen Z G, Ji X L. Copper resource trends and use reduction measures in China. J Tsinghua Univ (Sci Technol Edn), 2013, 53(9): 65-70. (in Chinese with English abstract)
[5] 周东美, 王玉军, 郝秀珍, 陈怀满. 铜矿区重金属污染分异规律初步研究. 农业环境科学学报, 2002, 21: 225-227.
Zhou D M, Wang Y J, Hao X Z, Chen H M. Primary study of distribution of heavy metals in copper mines. J Agro-Environ Sci, 2002, 21: 225-227. (in Chinese with English abstract)
[6] An F, Gao B J, Dai X, Wang M, Wang X H. Efficient removal of heavy metal ions from aqueous solution using salicylic acid type chelate adsorbent. J Hazard Mater, 2011, 192: 956-962.
doi: 10.1016/j.jhazmat.2011.05.050 pmid: 21741170
[7] 胡筑兵, 陈亚华, 王桂萍, 沈振国. 铜胁迫对玉米幼苗生长、叶绿素荧光参数和抗氧化酶活性的影响. 植物学通报, 2006, 23: 129-137.
Hu Z B, Chen Y H, Wang G P, Shen Z G. Effects of copper stress on growth, chlorophyll fluorescence parameters and antioxidant enzyme activities of Zea mays seedlings. Chin Bull Bot, 2006, 23: 129-137. (in Chinese with English abstract)
[8] Zhang H, Hu L Y, Hu K D, He Y D, Wang S H, Luo J P. Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J Integr Plant Biol, 2008, 50: 1518-1529.
doi: 10.1111/j.1744-7909.2008.00769.x
[9] 王晓维, 国勤, 徐健程, 聂亚平, 万进荣, 杨潇一, 杨文亭. 铜胁迫和间作对玉米抗氧化酶活性及丙二醛含量的影响. 农业环境科学学报, 2014, 33: 1890-1896.
Wang X W, Guo Q, Xu J C, Nie Y P, Wan J R, Yang X Y, Yang W T. Effects of copper stresses and intercropping on antioxidant enzyme activities and malondialdehyde contents in maize. J Agro-Environ Sci, 2014, 33: 1890-1896. (in Chinese with English abstract)
[10] David M R, Vladimir S, Ilya R. Intermediates of salicylic acid biosynthesis in tobacco. Plant Physiol, 1998, 118: 565-572.
doi: 10.1104/pp.118.2.565
[11] Zhang Y L, Li X. Salicylic acid: biosynthesis, perception, and contributions to plant immunity. Curr Opin Plant Biol, 2019, 50: 299-336.
[12] 孟雪娇, 邸昆, 丁国华. 水杨酸在植物体内的生理作用研究进展. 中国农学通报, 2010, 26(15): 217-224.
Meng X J, Di K, Ding G H. Progress of study on the physiological role of salicylic acid in plant. Chin Agric Sci Bull, 2010, 26(15): 217-224. (in Chinese with English abstract)
[13] Appu M, Muthukrishnan S. Foliar application of salicylic acid stimulates flowering and induce defense related proteins in finger millet plants. Univ J Plant Sci, 2014, 2: 14-18.
[14] Klessig D F, Malamy J. The salicylic acid signal in plants. Plant Mol Biol, 1994, 26: 1439-1458.
doi: 10.1007/BF00016484 pmid: 7858199
[15] 崔婧. 水杨酸与植物抗逆性. 安徽农学通报, 2007, 13(9): 35-38.
Cui J. Effects of salicylic acid on resisting adversity of plants. Anhui Agric Sci Bull, 2007, 13(9): 35-38. (in Chinese with English abstract)
[16] Janda T, Szalai G, Pal M. Salicylic acid signalling in plants. Int J Mol Sci, 2020, 21: 2655.
doi: 10.3390/ijms21072655
[17] 丁佳红, 薛正莲, 杨超英. 水杨酸对铜胁迫下水稻幼苗膜脂过氧化作用的影响. 黑龙江农业科学, 2013, (1): 14-18.
Ding J H, Xue Z L, Yang C Y. Effect on different factors on rice callus formation. Heilongjiang Agric Sci, 2013, (1): 14-18. (in Chinese with English abstract)
[18] Al-hakimi A B M, Hama A M. Ascorbic acid, thiamine or salicylic acid induced changes in some physiological parameters in wheat grown under copper stress. Plant Prot Sci, 2011, 47: 92-108.
doi: 10.17221/20/2010-PPS
[19] Hall J L. Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot, 2002, 53: 366.
[20] El-tayeb M A, El-enany A E, Ahmed N L. Salicylic acid-induced adaptive response to copper stress in sunflower (Helianthus annuus L.). Plant Growth Regul, 2006, 50: 191-199.
doi: 10.1007/s10725-006-9118-2
[21] Kováik J, Klejdus B, Hedbavny J, Backor M. Effect of copper and salicylic acid on phenolic metabolites and free amino acids in Scenedesmus quadricauda (Chlorophyceae). Plant Sci, 2010, 178: 307-311.
doi: 10.1016/j.plantsci.2010.01.009
[22] Moravcová S, Tůma J, Dučaiová Z K, Waligorski P, Kula M, Saja D, Slomka A, Baba W, Libik-Konieczny M. Influence of salicylic acid pretreatment on seeds germination and some defence mechanisms of Zea mays plants under copper stress. Plant Physiol Biochem, 2017, 122: 19-30.
doi: 10.1016/j.plaphy.2017.11.007
[23] Guo B, Liang Y, Zhu Y. Does salicylic acid regulate antioxidant defense system, cell death, cadmium uptake and partitioning to acquire cadmium tolerance in rice? J Plant Physiol, 2009, 166: 20-31.
doi: 10.1016/j.jplph.2008.01.002
[24] Khan N, Bano A. Effects of exogenously applied salicylic acid and putrescine alone and in combination with rhizobacteria on the phytoremediation of heavy metals and chickpea growth in sandy soil. Int J Phytorem, 2017, 20: 405-414.
doi: 10.1080/15226514.2017.1381940
[25] Huang Y T, Cai S Y, Chen S Y, Ruan X L, Mei G F, Ruan G H, Cao D D. Salicylic acid enhances sunflower seed germination under Zn2+ stress via involvement in Zn2+ metabolic balance and phytohormone interactions. Sci Hortic, 2020, 275: 109702.
doi: 10.1016/j.scienta.2020.109702
[26] 张亚娟, 王倩, 龙瑜菡, 李璇, 李光菊, 邓纲, 刘飞虎. 不同大麻品种种子萌发期耐重金属铜胁迫能力评价. 中国麻业科学, 2018, 40: 183-191.
Zhang Y J, Wang Q, Long Y H, Li X, Li G J, Deng G, Liu F H. Effects of Cu2+ stress on the seed germination and Cu-tolerance evaluation of industrial hemp. Plant Fiber Sci China, 2018, 40: 183-191. (in Chinese with English abstract)
[27] 刘飞虎, 苏文君, 杜光辉, 杨阳. 一种工业大麻液体栽培方法. 中国专利. CN103621392A. 2013-12-23.
Liu F H, Su W J, Du G H, Yang Y. A method for industrial hemp liquid culture. China Patent: CN103621392A. 2013-12-23 (in Chinese)
[28] Heath R L, Packer L. Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys, 1968, 125: 189-198.
doi: 10.1016/0003-9861(68)90654-1 pmid: 5655425
[29] Dhindsa R S, Matowe W. Drought tolerance in two mosses: correlated with enzymatic defence against liqid peroxidation. J Exp Bot, 2005, 56: 685-694.
doi: 10.1093/jxb/eri051
[30] Gutteridge J M C, Halliwell B. The measurement and mechanism of lipid peroxidation in biological systems. Trends Biochem Sci, 1990, 15: 129-135.
pmid: 2187293
[31] Rao M V, Paliyath G, Ormrod D P. Ultraviolet-band ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiol, 1996, 110: 125-136.
[32] 谢玲玲, 王金龙, 伍国强. 植物CBL-CIPK信号系统响应非生物胁迫的调控机制. 植物学报, 2021, 56: 614-626.
doi: 10.11983/CBB21024
Xie L L, Wang J L, Wu G Q. Regulatory mechanisms of the plant CBL-CIPK signaling system in response to abiotic stress. Chin Bull Bot, 2021, 56: 614-626. (in Chinese with English abstract)
[33] 谢政文, 王连军, 陈锦洋, 王娇, 苏一钧, 杨新笋, 曹清河. 植物WRKY转录因子及其生物学功能研究进展. 中国农业科技导报, 2016, 18(3): 46-54.
Xie Z W, Wang L J, Chen J Y, Wang J, Su Y J, Yang X S, Cao Q H. Studies on WRKY transcription factors and their biological functions in plants. J Agric Sci Technol, 2016, 18(3): 46-54. (in Chinese with English abstract)
[34] 张桐, 李智强, 伍国强. WRKY转录因子在植物逆境响应中的作用. 生物技术通报, 2021, 27(10): 203-215.
Zhang T, Li Z Q, Wu G Q. Role of WRKY transcription factor in plant response to stresses. Biotechnol Bull, 2021, 27(10): 203-215. (in Chinese with English abstract)
[35] 林义章, 徐磊. 铜污染对高等植物的生理毒害作用研究. 中国生态农业学报, 2007, 15: 201-204.
Lin Y Z, Xu L. Physiological toxicity of copper pollution to higher plant. Chin J Eco-Agric, 2007, 15: 201-204. (in Chinese with English abstract)
[36] Li Z Y, Ma Z W, Kuijp T J, Yuan Z W, Huang L. A review of soil heavy metal pollution from mines in China: pollution and health risk assessment. Sci Total Environ, 2014, 468-469: 843-853.
doi: 10.1016/j.scitotenv.2013.08.090
[37] Dixit V, Pandey V, Shyam R. Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). J Exp Bot, 2001, 52: 1101-1109.
pmid: 11432926
[38] Bai X Y, Dong Y J, Wang Q H, Xu L L, Kong J, Liu S. Effects of lead and nitric oxide on photosynthesis, antioxidative ability, and mineral element content of perennial ryegrass. Biol Plant, 2014, 59: 163-170.
doi: 10.1007/s10535-014-0476-8
[39] Ghori N H, Ghori T, Hayat M Q, Imadi S R, Gul A, Altay V, Ozturk M. Heavy metal stress and responses in plants. Int J Environ Sci Technol, 2019, 16: 3.
[40] Sun L, Zhang X H, Wang O, Yang E D, Cao Y Y, Sun R B. Lowered Cd toxicity, uptake and expression of metal transporter genes in maize plant by ACC deaminase-producing bacteria Achromobacter sp. J Hazard Mater, 2022, 423: 127036.
doi: 10.1016/j.jhazmat.2021.127036
[41] Duff S M G, Sarath G, Plaxton W C. The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant, 1994, 90: 791-800.
doi: 10.1111/ppl.1994.90.issue-4
[42] 朱守晶, 史文娟. 苎麻液泡膜质子焦磷酸酶基BnVP1的克隆及镉胁迫下的表达分析. 农业生物技术学报, 2021, 29: 1485-1494.
Zhu S J, Shi W J. Cloning of the vacuolar H+-pyrophosphatases gene BnVP1 from ramie (Boehmeria nivea) and expression analysis under cadmium stress. J Agric Biotechnol, 2021, 29: 1485-1494. (in Chinese with English abstract)
[43] Swigoňová Z, Mohsen A W, Vockley J. Acyl-CoA Dehydrogenases: dynamic history of protein family evolution. J Mol Evol, 2009, 69: 176-193.
doi: 10.1007/s00239-009-9263-0 pmid: 19639238
[44] 郝向阳, 孙雪丽, 王天池, 吕科良, 赖钟雄, 程春振. 植物PAL基因及其编码蛋白的特征与功能研究进展. 热带作物学报, 2018, 39: 1452-1461.
Hao X Y, Sun X L, Wang T C, Lyu K L, Lai Z X, Cheng C Z. Characteristics and functions of plant Phenylalanine Ammonia Lyase genes and the encoded proteins. Chin J Trop Crops, 2018, 39: 1452-1461. (in Chinese with English abstract)
[45] 罗才林. 水杨酸和茉莉酸甲酯胁迫下白及响应与苯丙氨酸解氨酶基因的克隆. 遵义医科大学硕士学位论文, 贵州遵义, 2019.
Luo C L. Phenylalanine Ammonia-lyase Gene Cloning during Stress Responses Against Salicylic Acid and Methyl Jasmonate in Bletilla striata. MS Thesis of Zunyi Medical University, Zunyi, Guizhou, China, 2019. (in Chinese with English abstract)
[46] 乔枫, 张丽, 耿贵工, 陈志, 曾阳, 谢惠春. CoCl2胁迫下青稞苯丙氨酸解氨酶基因的克隆与表达分析. 中国农业大学学报, 2021, 26(3): 18-27.
Qiao F, Zhang L, Geng G G, Chen Z, Zeng Y, Xie H C. Cloning and expression of phenylalanine ammonialyase gene of Hordeum vulgare var. nudum under CoCl2 stress. J China Agric Univ, 2021, 26(3): 18-27. (in Chinese with English abstract)
[47] 李文文. 外源水杨酸对铜胁迫下菊芋的调控效应及其耐铜机理研究. 浙江师范大学硕士学位论文, 浙江金华, 2021.
Li W W. Regulatory Effect of Exogenous Salicylic Acid on Heliantus tuberosus L. under Copper Stress and the Mechanism of Copper. MS Thesis of Zhejiang Normal University, Jinhua, Zhejiang, China, 2021. (in Chinese with English abstract)
[48] Jia H L, Wang X H, Wei T, Wang M, Liu X, Hua L, Ren X H, Guo J K, Li J S. Exogenous salicylic acid regulates cell wall polysaccharides synthesis and pectin methylation to reduce Cd accumulation of tomato. Ecotoxicol Environ Saf, 2021, 207: 111550.
doi: 10.1016/j.ecoenv.2020.111550
[49] Zhang Z W, Deng Z L, Tao Q, Peng H Q, Wu F, Fu Y F, Yang X Y, Xu P Z, Li Y, Wang C Q, Chen Y E, Yuan M, Lan T, Tang X Y, Chen G D, Zeng J, Yuan S. Salicylic and glutamate mediate different Cd accumulation and tolerance between Brassica napus and B. juncea. Chemosphere, 2022, 292: 133466.
[50] Kaur G, Sharma P, Rathee S, Singh H P, Batish D R, Kohli R K. Salicylic acid pre-treatment modulates Pb2+-induced DNA damage vis-à-vis oxidative stress in Allium cepa roots. Environ Sci Pollut Res, 2021, 28: 51989-52000.
doi: 10.1007/s11356-021-14151-7
[51] Wang L, Li R, Yan X X, Liang X F, Sun Y B, Xu Y M. Pivotal role for root cell wall polysaccharides in cultivar-dependent cadmium accumulation in Brassica chinensis L. Ecotoxicol Environ Saf, 2020, 194: 110369.
doi: 10.1016/j.ecoenv.2020.110369
[52] 陈娜, 潘丽娟, 迟晓元, 陈明娜, 王通, 王冕, 杨珍, 胡冬青, 王道远, 禹山林. 花生果糖-1,6-二磷酸醛缩酶基因AhFBA1的克隆与表达. 作物学报, 2014, 40: 934-941.
doi: 10.3724/SP.J.1006.2014.00934
Chen N, Pan L J, Chi L Y, Chen M N, Wang T, Wang M, Yang Z, Hu D Q, Wang D Y, Yu S L. Cloning and expression of fructose-1,6-bisphosphate aldolase gene AhFBA1 in peanut (Arachis hypogaea L.). Acta Agron Sin, 2014, 40: 934-941. (in Chinese with English abstract)
doi: 10.3724/SP.J.1006.2014.00934
[53] 王晨, 李家儒. 植物β-葡萄糖苷酶的研究进展. 生物资源, 2021, 43(2): 101-109.
Wang C, Li J R. Research progress of plant β-glucosidase. Biotic Resour, 2021, 43(2): 101-109. (in Chinese with English abstract)
[54] 崔慧萍, 周薇, 郭长虹. 植物过氧化物酶体在活性氧信号网络中的作用. 中国生物化学与分子生物学报, 2017, 33: 220-226.
Cui H P, Zhou W, Guo C H. The role of plant peroxisomes in ROS signaling network. Chin J Biochem Mol Biol, 2017, 33: 220-226. (in Chinese with English abstract)
[55] Pan W H, Zheng Z Z, Yan X, Shen J Q, Shou J X, Jiang L X, Pan J W. Overexpression of CBL interacting protein kinase 2 improves plant tolerance to salinity and mercury. Biol Plant, 2019, 63: 183-192.
[56] Li G Z, Zheng Y X, Chen S J, Liu J, Wang P F, Wang Y H, Guo T C, Kang G Z. TaWRKY74 participates copper tolerance through regulation of TaGST1 expression and GSH content in wheat. Ecotoxicol Environ Saf, 2021, 221: 112469.
doi: 10.1016/j.ecoenv.2021.112469
[57] Shi K, Liu X, Zhu Y P, Bai Y X, Shan D Q, Zheng X D, Wang L, Zhang H X, Wang C Y, Yan T C, Zhou F F, Hu Z H, Sun Y Z, Guo Y, Kong J. MdWRKY11 improves copper tolerance by directly promoting the expression of the copper transporter gene MdHMA5. Hortic Res, 2020, 7: 105.
doi: 10.1038/s41438-020-0326-0
[58] Linger P, Müssig J, Fischer H, Kobert J. Industrial hemp (Cannabis sativa L.) growing on heavy metal contaminated soil: fibre quality and phytoremediation potential. Ind Crops Prod, 2002, 16: 33-42.
doi: 10.1016/S0926-6690(02)00005-5
[59] Zehra S S, Arshad M, Mahmood T, Waheed A. Assessment of heavy metal accumulation and their translocation in plant species. Afr J Biotechnol, 2009, 8: 2802-2810.
[60] Wang L N, Yang X Y, Ren Z H, Hu X Y, Wang X F. Alleviation of photosynthetic inhibition in copper-stressed tomatoes through rebalance of ion content by exogenous nitric oxide. Turk J Bot, 2015, 39: 10-22.
doi: 10.3906/bot-1312-17
[61] 王龙, 樊婕, 魏畅, 李鸽子, 张静静, 焦秋娟, 陈果, 孙娈姿, 柳海涛. 外源抗坏血酸对铜胁迫菊苣幼苗生长的缓解效应. 草业学报, 2021, 30(4): 150-159.
doi: 10.11686/cyxb2020411
Wang L, Fan J, Wei C, Li G Z, Zhang J J, Jiao Q J, Chen G, Sun R Z, Liu H T. Mitigative effect of exogenous ascorbic acid on the growth of copper-stressed chicory (Cichorium intybus) seedlings. Acta Pratac Sin, 2021, 30(4): 150-159. (in Chinese with English abstract)
[62] 许艳萍, 吕品, 张庆滢, 郭蓉, 邓纲, 郭鸿彦, 杨明. 不同工业大麻品种对田间5种重金属吸收积累特性的比较. 农业环境与发展, 2020, 37(1): 106-114.
Xu Y P, Lyu P, Zhang Q Y, Guo R, Deng G, Guo H Y, Yang M. Comparison of the absorption and accumulation characteristics of five heavy metals among different industrial hemp varieties. J Agric Resour Environ, 2020, 37(1): 106-114. (in Chinese with English abstract)
[1] Yan-Ping XU, Ming YANG, Hong-Yan GUO, Qing-Hui YANG. Phytoremediation potential of five industrial hemp varieties on five heavy metal polluted soils [J]. Acta Agronomica Sinica, 2020, 46(12): 1970-1978.
[2] LI Run-Zhi, JIN Qing, LI Zhao-Hu, WANG Ye, PENG Zhen, DUAN Liu-Sheng. Salicylic acid improved salinity tolerance of Glycyrrhiza uralensis Fisch during seed germination and seedling growth stages [J]. Acta Agronomica Sinica, 2020, 46(11): 1810-1816.
[3] Ren-Feng XUE, Li WANG, Ming FENG, Wei-De GE. Identification and Expression Analysis of Likely Orthologs of Tobacco Salicylic Acid Binding Protein 2 in Common Beans [J]. Acta Agronomica Sinica, 2018, 44(05): 642-649.
[4] LI Shuai,ZHAO Qiu-Ling,PENG Yang,XU Yi,LI Jia-Na,NI Yu*. Effects of SA, MeJA, and ACC on Leaf Cuticular Wax Constituents, Structure and Permeability in Brassica napus [J]. Acta Agron Sin, 2016, 42(12): 1827-1833.
[5] XU Gen-Di,GE Shu-Fang,ZAHNG Yi,WU Yu-Huang,MEI Xiao-Man,LIU Peng. Effect of Salicylic Acid on Growth and Nutrient Uptake in Hydroponic Tobacco under Cu Stress [J]. Acta Agron Sin, 2015, 41(06): 956-962.
[6] ZHENG Xiao-Min,GUO Nan,GAO Tian-Shu,GONG Hui-Ming,ZHANG Tao. Cloning and Expression Analysis of Defensin Genes from Brassica napus [J]. Acta Agron Sin, 2015, 41(05): 725-732.
[7] NI Yu,WANG Jing,SONG Chao,XIA Rui-E,SUN Zheng-Yuan,GUO Yan-Jun,LI Jia-Na. Effects of SA Induction on Leaf Cuticular Wax and Resistance to Sclerotinia sclerotiorurn in Brassica napus [J]. Acta Agron Sin, 2013, 39(01): 110-117.
[8] HE Jin-Huan;WANG Peng-Tao;WANG Wen-Jing;SONG Chun-Peng. Effect of Salicylic Acid on Stomatal Movement and K Channel on Plasma Membrane of Guard Cell in Vicia faba L. [J]. Acta Agron Sin, 2007, 33(09): 1479-1487.
[9] ZENG Fu-Hua;YI Ke;XU Xiang-Li;WANG Hai-Hua. Relationship between the Changes of Active Oxygen Species and Defense Enzymes in Suspension Cultured Cells Treated by Different Inducers [J]. Acta Agron Sin, 2005, 31(01): 18-23.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] Li Shaoqing, Li Yangsheng, Wu Fushun, Liao Jianglin, Li Damo. Optimum Fertilization and Its Corresponding Mechanism under Complete Submergence at Booting Stage in Rice[J]. Acta Agronomica Sinica, 2002, 28(01): 115 -120 .
[2] Wang Lanzhen;Mi Guohua;Chen Fanjun;Zhang Fusuo. Response to Phosphorus Deficiency of Two Winter Wheat Cultivars with Different Yield Components[J]. Acta Agron Sin, 2003, 29(06): 867 -870 .
[3] Yan Mei;Yang Guangsheng;Fu Tingdong;Yan Hongyan. Studies on the Ecotypical Male Sterile-fertile Line of Brassica napus L.Ⅲ. Sensitivity to Temperature of 8-8112AB and Its Inheritance[J]. Acta Agron Sin, 2003, 29(03): 330 -335 .
[4] Wang Yongsheng;Wang Jing;Duan Jingya;Wang Jinfa;Liu Liangshi. Isolation and Genetic Research of a Dwarf Tiilering Mutant Rice[J]. Acta Agron Sin, 2002, 28(02): 235 -239 .
[5] WANG Li-Yan;ZHAO Ke-Fu. Some Physiological Response of Zea mays under Salt-stress[J]. Acta Agron Sin, 2005, 31(02): 264 -268 .
[6] TIAN Meng-Liang;HUNAG Yu-Bi;TAN Gong-Xie;LIU Yong-Jian;RONG Ting-Zhao. Sequence Polymorphism of waxy Genes in Landraces of Waxy Maize from Southwest China[J]. Acta Agron Sin, 2008, 34(05): 729 -736 .
[7] HU Xi-Yuan;LI Jian-Ping;SONG Xi-Fang. Efficiency of Spatial Statistical Analysis in Superior Genotype Selection of Plant Breeding[J]. Acta Agron Sin, 2008, 34(03): 412 -417 .
[8] WANG Yan;QIU Li-Ming;XIE Wen-Juan;HUANG Wei;YE Feng;ZHANG Fu-Chun;MA Ji. Cold Tolerance of Transgenic Tobacco Carrying Gene Encoding Insect Antifreeze Protein[J]. Acta Agron Sin, 2008, 34(03): 397 -402 .
[9] ZHENG Xi;WU Jian-Guo;LOU Xiang-Yang;XU Hai-Ming;SHI Chun-Hai. Mapping and Analysis of QTLs on Maternal and Endosperm Genomes for Histidine and Arginine in Rice (Oryza sativa L.) across Environments[J]. Acta Agron Sin, 2008, 34(03): 369 -375 .
[10] XING Guang-Nan, ZHOU Bin, ZHAO Tuan-Jie, YU De-Yue, XING Han, HEN Shou-Yi, GAI Jun-Yi. Mapping QTLs of Resistance to Megacota cribraria (Fabricius) in Soybean[J]. Acta Agronomica Sinica, 2008, 34(03): 361 -368 .