Register      Login
Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Cadmium and arsenic provoke mostly distinct but partly overlapping responses in Brassica juncea

Allah Dad Khan A , Muhammad Sayyar Khan https://orcid.org/0000-0003-0579-1772 A C , Sajid Ali Khan Bangash A , Kashif Naeem B , Abdullah Jalal A and Muhammad Tayyab A
+ Author Affiliations
- Author Affiliations

A Institute of Biotechnology and Genetic Engineering, The University of Agriculture Peshawar, Khyber Pakhtunkhwa, Pakistan.

B National Institute of Genomics and Advanced Biotechnology, NARC, Park Road, Islamabad, Pakistan.

C Corresponding author. Email: sayyar@aup.edu.pk

Crop and Pasture Science - https://doi.org/10.1071/CP21157
Submitted: 3 March 2021  Accepted: 7 May 2021   Published online: 3 September 2021

Abstract

Among the toxic heavy metal(loid)s, cadmium (Cd) and arsenic (As) have devastating effects on crop productivity and human health. In plants, mechanisms of detoxification of Cd and As proceed via a glutathione (GSH) dependent common pathway, despite their different modes of toxicity. In this context, the present study aimed to investigate how the common detoxification mechanisms for Cd and As influence the physiological and biochemical responses of seedlings of an important plant used for phytoremediation purposes, Brassica juncea, under Cd and As stress. We demonstrated that Cd and As trigger mostly distinct, but partly overlapping, responses in B. juncea. Exposure of B. juncea seedlings to 100 μM Cd stress for 12 days in a hydroponic system led to a significant reduction in the growth of roots and shoots, and in total chlorophyll content. However, As stress caused a decline in root length only. High-performance liquid chromatography analyses revealed a significant increase in cysteine levels in roots and shoots in response to As stress compared with control and Cd-treated plants. Concomitant elevated sulfur content in response to As stress was observed in roots and shoots. In terms of GSH content, Cd and As triggered similar responses, with a significant decrease in GSH in roots, and non-significant changes in shoots, compared with untreated plants. Inductively coupled plasma-atomic emission spectroscopy revealed that under Cd stress, plants preferentially accumulated zinc (Zn) in the roots compared with iron (Fe) and manganese (Mn). Responses in roots under As and Cd stress were similar with respect to Fe accumulation but opposite in terms of Zn and Mn accumulation. Our data provide valuable insights for design of future strategies for sustainable plant growth on As and Cd polluted soils.

Keywords: chlorophyll, glutathione, heavy metals, sulfur, toxicity.


References

Ahmad P, Sarwat M, Bhat NA, Wani MR, Kazi AG, Tran L-SP (2015) Alleviation of cadmium toxicity in Brassica juncea L. (Czern. & Coss.) by calcium application involves various physiological and biochemical strategies. PLoS One 10, e0114571
Alleviation of cadmium toxicity in Brassica juncea L. (Czern. & Coss.) by calcium application involves various physiological and biochemical strategies.Crossref | GoogleScholarGoogle Scholar | 25629695PubMed |

Babel S, Kurniawan TA (2004) Cr(VI) removal from synthetic wastewater using coconut shell charcoal and commercial activated carbon modified with oxidizing agents and/or chitosan. Chemosphere 54, 951–967.
Cr(VI) removal from synthetic wastewater using coconut shell charcoal and commercial activated carbon modified with oxidizing agents and/or chitosan.Crossref | GoogleScholarGoogle Scholar | 14637353PubMed |

Bao T, Sun T, Sun L (2012) Effect of cadmium on physiological responses of wheat and corn to iron deficiency. Journal of Plant Nutrition 35, 1937–1948.
Effect of cadmium on physiological responses of wheat and corn to iron deficiency.Crossref | GoogleScholarGoogle Scholar |

Bashir H, Ibrahim MM, Bagheri R, Ahmad J, Arif IA, Baig MA, Qureshi MI (2015) Influence of sulfur and cadmium on antioxidants, phytochelatins and growth in Indian mustard. AoB Plants 7, plv001
Influence of sulfur and cadmium on antioxidants, phytochelatins and growth in Indian mustard.Crossref | GoogleScholarGoogle Scholar | 25587194PubMed |

Bertoli AC, Cannata MG, Carvalho R, Bastos ARR, Freitas MP, dos Santos Augusto A (2012) Lycopersicon esculentum submitted to Cd-stressful conditions in nutrition solution: nutrient contents and translocation. Ecotoxicology and Environmental Safety 86, 176–181.
Lycopersicon esculentum submitted to Cd-stressful conditions in nutrition solution: nutrient contents and translocation. Crossref | GoogleScholarGoogle Scholar |

Bhuiyan MSU, Min SR, Jeong WJ, Sultana S, Choi KS, Lee Y, Liu JR (2011) Overexpression of AtATM3 in Brassica juncea confers enhanced heavy metal tolerance and accumulation. Plant Cell, Tissue and Organ Culture 107, 69–77.
Overexpression of AtATM3 in Brassica juncea confers enhanced heavy metal tolerance and accumulation.Crossref | GoogleScholarGoogle Scholar |

Bricker TJ, Pichtel J, Brown HJ, Simmons M (2001) Phytoextraction of Pb and Cd from a superfund soil: effects of amendments and croppings. Journal of Environmental Science and Health. Part A, Toxic/Hazardous Substances & Environmental Engineering 36, 1597–1610.
Phytoextraction of Pb and Cd from a superfund soil: effects of amendments and croppings.Crossref | GoogleScholarGoogle Scholar |

Cahoon RE, Lutke WK, Cameron JC, Chen S, Lee SG, Rivard RS, Rea PA, Jez JM (2015) Adaptive engineering of phytochelatin-based heavy metal tolerance. The Journal of Biological Chemistry 290, 17321–17330.
Adaptive engineering of phytochelatin-based heavy metal tolerance.Crossref | GoogleScholarGoogle Scholar | 26018077PubMed |

Cailliatte R, Schikora A, Briat J-F, Mari S, Curie C (2010) High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. The Plant Cell 22, 904–917.
High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions.Crossref | GoogleScholarGoogle Scholar | 20228245PubMed |

Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88, 1707–1719.
Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants.Crossref | GoogleScholarGoogle Scholar | 16914250PubMed |

DalCorso G, Farinati S, Maistri S, Furini A (2008) How plants cope with cadmium: staking all on metabolism and gene expression. Journal of Integrative Plant Biology 50, 1268–1280.
How plants cope with cadmium: staking all on metabolism and gene expression.Crossref | GoogleScholarGoogle Scholar | 19017114PubMed |

Dixon DP, Cummins I, Cole DJ, Edwards R (1998) Glutathione-mediated detoxification systems in plants. Current Opinion in Plant Biology 1, 258–266.
Glutathione-mediated detoxification systems in plants.Crossref | GoogleScholarGoogle Scholar | 10066594PubMed |

Duman F, Ozturk F, Aydin Z (2010) Biological responses of duckweed (Lemna minor L.) exposed to the inorganic arsenic species As(III) and As(V): effects of concentration and duration of exposure. Ecotoxicology 19, 983–993.
Biological responses of duckweed (Lemna minor L.) exposed to the inorganic arsenic species As(III) and As(V): effects of concentration and duration of exposure.Crossref | GoogleScholarGoogle Scholar | 20221688PubMed |

Farnese FS, Oliveira J, Farnese MS, Gusman GS, Silveira NM, Siman LI (2014) Uptake arsenic by plants: Effects on mineral nutrition, growth and antioxidant capacity. Idesia 32, 99–106.
Uptake arsenic by plants: Effects on mineral nutrition, growth and antioxidant capacity.Crossref | GoogleScholarGoogle Scholar |

Farooq MA, Li L, Ali B, Gill RA, Wang J, Ali S, Gill MB, Zhou W (2015) Oxidative injury and antioxidant enzymes regulation in arsenic-exposed seedlings of four Brassica napus L. cultivars. Environmental Science and Pollution Research International 22, 10699–10712.
Oxidative injury and antioxidant enzymes regulation in arsenic-exposed seedlings of four Brassica napus L. cultivars.Crossref | GoogleScholarGoogle Scholar | 25752633PubMed |

Fassel VA (1978) Quantitative elemental analyses by plasma emission spectroscopy. Science 202, 183–191.
Quantitative elemental analyses by plasma emission spectroscopy.Crossref | GoogleScholarGoogle Scholar | 17801907PubMed |

Flores-Cáceres ML, Hattab S, Hattab S, Boussetta H, Banni M, Hernández LE (2015) Specific mechanisms of tolerance to copper and cadmium are compromised by a limited concentration of glutathione in alfalfa plants. Plant Science 233, 165–173.
Specific mechanisms of tolerance to copper and cadmium are compromised by a limited concentration of glutathione in alfalfa plants.Crossref | GoogleScholarGoogle Scholar | 25711824PubMed |

Frankenberger, W, Arshad, M (2002) Volatilization of arsenic. In ‘Environmental chemistry of arsenic’. (Ed. WT Frankenberger Jr) pp. 363–380. (Marcel Dekker: New York)

Ghosh M, Singh S (2005) A review on phytoremediation of heavy metals and utilization of its by-products. Applied Ecology and Environmental Research 3, 1–18.
A review on phytoremediation of heavy metals and utilization of its by-products.Crossref | GoogleScholarGoogle Scholar |

Hédiji H, Djebali W, Belkadhi A, Cabasson C, Moing A, Rolin D, Brouquisse R, Gallusci P, Chaïbi W (2015) Impact of long-term cadmium exposure on mineral content of Solanum lycopersicum plants: consequences on fruit production. South African Journal of Botany 97, 176–181.
Impact of long-term cadmium exposure on mineral content of Solanum lycopersicum plants: consequences on fruit production.Crossref | GoogleScholarGoogle Scholar |

Hernández LE, Lozano-Rodrıguez E, Gárate A, Carpena-Ruiz R (1998) Influence of cadmium on the uptake, tissue accumulation and subcellular distribution of manganese in pea seedlings. Plant Science 132, 139–151.
Influence of cadmium on the uptake, tissue accumulation and subcellular distribution of manganese in pea seedlings.Crossref | GoogleScholarGoogle Scholar |

Hong Y-S, Song K-H, Chung J-Y (2014) Health effects of chronic arsenic exposure. Journal of Preventive Medicine and Public Health 47, 245
Health effects of chronic arsenic exposure.Crossref | GoogleScholarGoogle Scholar | 25284195PubMed |

Huot J, Lambert H, Lavoie JN, Guimond A, Houle F, Landry J (1995) Characterization of 45‐kDa/54‐kDa HSP27 kinase, a stress‐sensitive kinase which may activate the phosphorylation‐dependent protective function of mammalian 27‐kDa heat‐shock protein HSP27. European Journal of Biochemistry 227, 416–427.
Characterization of 45‐kDa/54‐kDa HSP27 kinase, a stress‐sensitive kinase which may activate the phosphorylation‐dependent protective function of mammalian 27‐kDa heat‐shock protein HSP27.Crossref | GoogleScholarGoogle Scholar | 7851416PubMed |

Inouhe M (2005) Phytochelatins. Brazilian Journal of Plant Physiology 17, 65–78.
Phytochelatins.Crossref | GoogleScholarGoogle Scholar |

Jing D, Fei-bo W, Guo-ping Z (2005) Effect of cadmium on growth and photosynthesis of tomato seedlings. Journal of Zhejiang University. Science. B. 6, 974

Jobe TO, Sung DY, Akmakjian G, Pham A, Komives EA, Mendoza‐Cózatl DG, Schroeder JI (2012) Feedback inhibition by thiols outranks glutathione depletion: a luciferase‐based screen reveals glutathione‐deficient γ‐ECS and glutathione synthetase mutants impaired in cadmium‐induced sulfate assimilation. The Plant Journal 70, 783–795.
Feedback inhibition by thiols outranks glutathione depletion: a luciferase‐based screen reveals glutathione‐deficient γ‐ECS and glutathione synthetase mutants impaired in cadmium‐induced sulfate assimilation.Crossref | GoogleScholarGoogle Scholar | 22283708PubMed |

Kapoor D, Kaur S, Bhardwaj R (2014) Physiological and biochemical changes in Brassica juncea plants under Cd-induced stress. BioMed Research International 2014, 726070
Physiological and biochemical changes in Brassica juncea plants under Cd-induced stress.Crossref | GoogleScholarGoogle Scholar | 25133178PubMed |

Khan MS, Haas FH, Samami AA, Gholami AM, Bauer A, Fellenberg K, Reichelt M, Hänsch R, Mendel RR, Meyer AJ (2010) Sulfite reductase defines a newly discovered bottleneck for assimilatory sulfate reduction and is essential for growth and development in Arabidopsis thaliana. The Plant Cell 22, 1216–1231.
Sulfite reductase defines a newly discovered bottleneck for assimilatory sulfate reduction and is essential for growth and development in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 20424176PubMed |

Kumar M, Gogoi A, Kumari D, Borah R, Das P, Mazumder P, Tyagi VK (2017) Review of perspective, problems, challenges, and future scenario of metal contamination in the urban environment. Journal of Hazardous, Toxic and Radioactive Waste 21, 04017007
Review of perspective, problems, challenges, and future scenario of metal contamination in the urban environment.Crossref | GoogleScholarGoogle Scholar |

Liu Q, Hu C, Tan Q, Sun X, Su J, Liang Y (2008) Effects of As on As uptake, speciation, and nutrient uptake by winter wheat (Triticum aestivum L.) under hydroponic conditions. Journal of Environmental Sciences 20, 326–331.
Effects of As on As uptake, speciation, and nutrient uptake by winter wheat (Triticum aestivum L.) under hydroponic conditions.Crossref | GoogleScholarGoogle Scholar |

López-Millán A-F, Sagardoy R, Solanas M, Abadía A, Abadía J (2009) Cadmium toxicity in tomato (Lycopersicon esculentum) plants grown in hydroponics. Environmental and Experimental Botany 65, 376–385.
Cadmium toxicity in tomato (Lycopersicon esculentum) plants grown in hydroponics.Crossref | GoogleScholarGoogle Scholar |

Mendoza-Cózatl D, Loza-Tavera H, Hernández-Navarro A, Moreno-Sánchez R (2005) Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants. FEMS Microbiology Reviews 29, 653–671.
Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants.Crossref | GoogleScholarGoogle Scholar | 16102596PubMed |

Nouairi I, Ammar WB, Youssef NB, Daoud DBM, Ghorbal MH, Zarrouk M (2006) Comparative study of cadmium effects on membrane lipid composition of Brassica juncea and Brassica napus leaves. Plant Science 170, 511–519.
Comparative study of cadmium effects on membrane lipid composition of Brassica juncea and Brassica napus leaves.Crossref | GoogleScholarGoogle Scholar |

Nouairi I, Ammar WB, Youssef NB, Daoud DBM, Ghorbal MH, Zarrouk M (2009) Antioxidant defense system in leaves of Indian mustard (Brassica juncea) and rape (Brassica napus) under cadmium stress. Acta Physiologiae Plantarum 31, 237–247.

Pal A, Gin KY-H, Lin AY-C, Reinhard M (2010) Impacts of emerging organic contaminants on freshwater resources: review of recent occurrences, sources, fate and effects. The Science of the Total Environment 408, 6062–6069.
Impacts of emerging organic contaminants on freshwater resources: review of recent occurrences, sources, fate and effects.Crossref | GoogleScholarGoogle Scholar | 20934204PubMed |

Patra M, Bhowmik N, Bandopadhyay B, Sharma A (2004) Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environmental and Experimental Botany 52, 199–223.
Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance.Crossref | GoogleScholarGoogle Scholar |

Per TS, Khan NA, Masood A, Fatma M (2016) Methyl jasmonate alleviates cadmium-induced photosynthetic damages through increased S-assimilation and glutathione production in mustard. Frontiers in Plant Science 7, 1933
Methyl jasmonate alleviates cadmium-induced photosynthetic damages through increased S-assimilation and glutathione production in mustard.Crossref | GoogleScholarGoogle Scholar | 28066485PubMed |

Pickering IJ, Prince RC, George MJ, Smith RD, George GN, Salt DE (2000) Reduction and coordination of arsenic in Indian mustard. Plant Physiology 122, 1171–1178.
Reduction and coordination of arsenic in Indian mustard.Crossref | GoogleScholarGoogle Scholar | 10759512PubMed |

Prasad MNV (2008) ‘Trace elements as contaminants and nutrients: consequences in ecosystems and human health.’ (John Wiley & Sons: New York)

Praveen A, Pandey C, Ehasanullah K, Panthri M, Gupta M (2020) Silicon-mediated genotoxic alterations in Brassica juncea under arsenic stress: a comparative study of biochemical and molecular markers. Pedosphere 30, 517–527.
Silicon-mediated genotoxic alterations in Brassica juncea under arsenic stress: a comparative study of biochemical and molecular markers.Crossref | GoogleScholarGoogle Scholar |

Rahman M, Haq N, Williams I (2016) Phytoaccumulation of arsenic, cadmium and lead by Brassica juncea parents and their F1 hybrids. Journal of Environmental Protection 7, 613–622.
Phytoaccumulation of arsenic, cadmium and lead by Brassica juncea parents and their F1 hybrids.Crossref | GoogleScholarGoogle Scholar |

Rai PK, Lee SS, Zhang M, Tsang YF, Kim K-H (2019) Heavy metals in food crops: health risks, fate, mechanisms, and management. Environment International 125, 365–385.
Heavy metals in food crops: health risks, fate, mechanisms, and management.Crossref | GoogleScholarGoogle Scholar | 30743144PubMed |

Rauser WE (1995) Phytochelatins and related peptides. Structure, biosynthesis, and function. Plant Physiology 109, 1141
Phytochelatins and related peptides. Structure, biosynthesis, and function.Crossref | GoogleScholarGoogle Scholar | 8539285PubMed |

Rodríguez-Serrano M, Romero-Puertas MC, Pazmino DM, Testillano PS, Risueño MC, Luis A, Sandalio LM (2009) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiology 150, 229–243.
Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium.Crossref | GoogleScholarGoogle Scholar | 19279198PubMed |

Salt DE, Blaylock M, Kumar NP, Dushenkov V, Ensley BD, Chet I, Raskin I (1995) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Nature Biotechnology 13, 468–474.
Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants.Crossref | GoogleScholarGoogle Scholar |

Sanchez-Fernandez R, Fricker M, Corben LB, White NS, Sheard N, Leaver CJ, Van Montagu M, Inzé D, May MJ (1997) Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control. Proceedings of the National Academy of Sciences of the United States of America 94, 2745–2750.
Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control.Crossref | GoogleScholarGoogle Scholar | 11038608PubMed |

Santos CS, Monteiro MS, Soares AM, Loureiro S (2012) Characterization of cholinesterases in plasma of three Portuguese native bird species: application to biomonitoring. PLoS One 7, e33975
Characterization of cholinesterases in plasma of three Portuguese native bird species: application to biomonitoring.Crossref | GoogleScholarGoogle Scholar | 22470503PubMed |

Schneider T, Haag-Kerwer A, Maetz M, Niecke M, Povh B, Rausch T, Schüßler A (1999) Micro-pixe studies of elemental distribution in Cd-accumulating Brassica juncea L. Nuclear Instruments & Methods in Physics Research Section B-beam Interactions with Materials and Atoms 158, 329–334.

Selvaraj K, Sevugaperumal R, Ramasubramanian V (2015) Phytoextraction: using Brassica as a hyper accumulator. Biochemistry & Physiology 4, 2

Seth CS, Chaturvedi PK, Misra V (2008) The role of phytochelatins and antioxidants in tolerance to Cd accumulation in Brassica juncea L. Ecotoxicology and Environmental Safety 71, 76–85.
The role of phytochelatins and antioxidants in tolerance to Cd accumulation in Brassica juncea L.Crossref | GoogleScholarGoogle Scholar | 18082263PubMed |

Seth CS, Misra V, Chauhan L (2012) Accumulation, detoxification, and genotoxicity of heavy metals in Indian mustard (Brassica juncea L.). International Journal of Phytoremediation 14, 1–13.
Accumulation, detoxification, and genotoxicity of heavy metals in Indian mustard (Brassica juncea L.).Crossref | GoogleScholarGoogle Scholar | 22567690PubMed |

Shah A, Rajab H, Jalal A, Ajmal M, Bangash S, Ahmad D, Khan M (2020) Inoculation of Brassica napus L. genotypes with endophytic bacteria promote growth and alleviate cadmium toxicity. Journal of Animal and Plant Sciences 30, 1187–1193.

Shanmugaraj, BM, Malla, A, Ramalingam, S (2019) Cadmium stress and toxicity in plants: an overview. In ‘Cadmium toxicity and tolerance in plants’. pp. 1–17. (Academic Press: Cambridge, MA, USA)

Shri M, Kumar S, Chakrabarty D, Trivedi PK, Mallick S, Misra P, Shukla D, Mishra S, Srivastava S, Tripathi RD (2009) Effect of arsenic on growth, oxidative stress, and antioxidant system in rice seedlings. Ecotoxicology and Environmental Safety 72, 1102–1110.
Effect of arsenic on growth, oxidative stress, and antioxidant system in rice seedlings.Crossref | GoogleScholarGoogle Scholar | 19013643PubMed |

Singh S, Juwarkar A, Kumar S, Meshram J, Fan M (2007) Effect of amendment on phytoextraction of arsenic by Vetiveria zizanioides from soil. International Journal of Environmental Science and Technology 4, 339–344.
Effect of amendment on phytoextraction of arsenic by Vetiveria zizanioides from soil.Crossref | GoogleScholarGoogle Scholar |

Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Current Opinion in Plant Biology 12, 364–372.
Mechanisms to cope with arsenic or cadmium excess in plants.Crossref | GoogleScholarGoogle Scholar | 19501016PubMed |

Vert G, Grotz N, Dédaldéchamp F, Gaymard F, Guerinot ML, Briat J-F, Curie C (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. The Plant Cell 14, 1223–1233.
IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth.Crossref | GoogleScholarGoogle Scholar | 12084823PubMed |

Viehweger K (2014) How plants cope with heavy metals. Botanical Studies 55, 35
How plants cope with heavy metals.Crossref | GoogleScholarGoogle Scholar | 28510963PubMed |

Yamaguchi C, Takimoto Y, Ohkama-Ohtsu N, Hokura A, Shinano T, Nakamura T, Suyama A, Maruyama-Nakashita A (2016) Effects of cadmium treatment on the uptake and translocation of sulfate in Arabidopsis thaliana. Plant & Cell Physiology 57, 2353–2366.
Effects of cadmium treatment on the uptake and translocation of sulfate in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Yoshihara T, Hodoshima H, Miyano Y, Shoji K, Shimada H, Goto F (2006) Cadmium inducible Fe deficiency responses observed from macro and molecular views in tobacco plants. Plant Cell Reports 25, 365–373.
Cadmium inducible Fe deficiency responses observed from macro and molecular views in tobacco plants.Crossref | GoogleScholarGoogle Scholar | 16344960PubMed |

Zarcinas B, Cartwright B, Spouncer L (1987) Nitric acid digestion and multi‐element analysis of plant material by inductively coupled plasma spectrometry. Communications in Soil Science and Plant Analysis 18, 131–146.
Nitric acid digestion and multi‐element analysis of plant material by inductively coupled plasma spectrometry.Crossref | GoogleScholarGoogle Scholar |