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

Elucidation of molecular and physiological mechanisms addressing integrated omic approaches for heavy metal stress tolerance in crops

Raju Mondal https://orcid.org/0000-0001-7526-1940 A , Amit Kumar https://orcid.org/0000-0003-1956-0174 B * , Aftab Ahmad Shabnam B and Ashish K. Chaturvedi https://orcid.org/0000-0001-9541-0931 C
+ Author Affiliations
- Author Affiliations

A Mulberry Tissue Culture Lab, Central Sericultural Germplasm Resources Centre (CSGRC), Ministry of Textile, Government of India, Hosur 635109, India.

B Host Plant Division, Central Muga Eri Research and Training Institute, Central Silk Board, Ministry of Textile, Government of India, Lahdoigarh, Jorhat 785700, Assam, India.

C Land and Water Management Research Group, Centre for Water Resources Development and Management, Kunnamangalam, Kozhikode 673571, Kerala, India.

* Correspondence to: amit_bio80@yahoo.com

Handling Editor: Shahid Hussain

Crop & Pasture Science - https://doi.org/10.1071/CP21467
Submitted: 5 July 2021  Accepted: 24 November 2021   Published online: 10 May 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Recent industrialisation has seen an alarming increase in heavy metal pollution, raising the question of how to sustain food production in the presence of heavy metals. Several reviews have addressed the direct and indirect effects of heavy metals on crop physiological and biochemical processes. However, understanding of the physiological and molecular mechanisms requires integrating omic approaches to explore the target mechanism in general in crops, and those insights are still lacking. To date, most of the information related to omic approaches about heavy metals has been sparse and sporadic. This review, by means of examples, attempts to integrate different available proteomic, transcriptomic and genomic approaches in a nutshell along with underlying physiological and molecular mechanisms occurring in crops. Major identified transcription factors (TFs) (MYBs, WRKYs), transgenes (MT2, Nramp6, GSTU3, CIPK, MYB1 and DRE), up-regulated (CAT, SODs, POD and APX), down-regulated (ATPase subunits, Rubisco subunits and photosystem I (PSI) reaction centre) proteins, and miRNA (miR397, miR398a, miR408, OsmiR601 and miR166) for major heavy metals have been summarised. It provides a mode of action of heavy metals and their fate inside the plant. It also elucidates how these omics approaches facilitate in mitigating heavy metal stress and could help in addressing crop tolerance based on these mechanisms. Identifying donors with the aid of novel omic approaches could be useful for the development of HM tolerant crops, promoting future sustainability in heavy-metal-polluted soil and water resources.

Keywords: antioxidant, crop productivity, heavy metal (HM) toxicity, integrated omic study, molecular mechanism, physiological adaptation, plant system, ROS, stress.


References

Agarwal S, Khan S (2020) Heavy metals phytotoxicity: DNA damage. In ‘Cellular and molecular phytotoxicity of heavy metals’. (Eds M Faisal, Q Saquib, AA Alatar, AA Al-Khedhairy) pp. 157–177. (Springer: Cham, Switzerland)

Ai TN, Naing AH, Yun B-W, Lim SH, Kim CK (2018) Overexpression of RsMYB1 enhances anthocyanin accumulation and heavy metals stress tolerance in transgenic petunia. Frontiers in Plant Science 9, 1388
Overexpression of RsMYB1 enhances anthocyanin accumulation and heavy metals stress tolerance in transgenic petunia.Crossref | GoogleScholarGoogle Scholar | 30294338PubMed |

Ángel Martín-Rodríguez J, Ariani A, Leija A, Elizondo A, Fuentes SI, Ramirez M, Gepts P, Hernández G, Formey D (2021) Phaseolus vulgaris MIR1511 genotypic variations differentially regulate plant tolerance to aluminum toxicity. The Plant Journal 105, 1521–1533.
Phaseolus vulgaris MIR1511 genotypic variations differentially regulate plant tolerance to aluminum toxicity.Crossref | GoogleScholarGoogle Scholar | 33300202PubMed |

Anjum SA, Tanveer M, Hussain S, Ashraf U, Khan I, Wang L (2017) Alteration in growth, leaf gas exchange, and photosynthetic pigments of maize plants under combined cadmium and arsenic stress. Water, Air, & Soil Pollution 228, 13
Alteration in growth, leaf gas exchange, and photosynthetic pigments of maize plants under combined cadmium and arsenic stress.Crossref | GoogleScholarGoogle Scholar |

Aqeel M, Khalid N, Tufail A, Ahmad RZ, Akhter MS, Luqman M, Javed MT, Irshad MK, Alamri S, Hashem M, Noman A (2021) Elucidating the distinct interactive impact of cadmium and nickel on growth, photosynthesis, metal-homeostasis, and yield responses of mung bean (Vigna radiata L.) varieties. Environmental Science and Pollution Research 28, 27376–27390.
Elucidating the distinct interactive impact of cadmium and nickel on growth, photosynthesis, metal-homeostasis, and yield responses of mung bean (Vigna radiata L.) varieties.Crossref | GoogleScholarGoogle Scholar | 33507502PubMed |

Ariani A, Romeo S, Groover AT, Sebastiani L (2016) Comparative epigenomic and transcriptomic analysis of Populus roots under excess Zn. Environmental and Experimental Botany 132, 16–27.
Comparative epigenomic and transcriptomic analysis of Populus roots under excess Zn.Crossref | GoogleScholarGoogle Scholar |

Asgher M, Ahmed S, Sehar Z, Gautam H, Gandhi SG, Khan NA (2021) Hydrogen peroxide modulates activity and expression of antioxidant enzymes and protects photosynthetic activity from arsenic damage in rice (Oryza sativa L.). Journal of Hazardous Materials 401, 123365
Hydrogen peroxide modulates activity and expression of antioxidant enzymes and protects photosynthetic activity from arsenic damage in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 32652423PubMed |

Bączek-Kwinta R, Juzoń K, Borek M, Antonkiewicz J (2019) Photosynthetic response of cabbage in cadmium-spiked soil. Photosynthetica 57, 731–739.
Photosynthetic response of cabbage in cadmium-spiked soil.Crossref | GoogleScholarGoogle Scholar |

Baig MA, Ahmad J, Bagheri R, Ali AA, Al-Huqail AA, Ibrahim MM, Qureshi MI (2018) Proteomic and ecophysiological responses of soybean (Glycine max L.) root nodules to Pb and hg stress. BMC Plant Biology 18, 283
Proteomic and ecophysiological responses of soybean (Glycine max L.) root nodules to Pb and hg stress.Crossref | GoogleScholarGoogle Scholar | 30428829PubMed |

Banerjee A, Roychoudhury A, Krishnamoorthi S (2016) Emerging techniques to decipher microRNAs (miRNAs) and their regulatory role in conferring abiotic stress tolerance of plants. Plant Biotechnology Reports 10, 185–205.
Emerging techniques to decipher microRNAs (miRNAs) and their regulatory role in conferring abiotic stress tolerance of plants.Crossref | GoogleScholarGoogle Scholar |

Bednarek PT, Orłowska R, Niedziela A (2017) A relative quantitative methylation-sensitive amplified polymorphism (MSAP) method for the analysis of abiotic stress. BMC Plant Biology 17, 79
A relative quantitative methylation-sensitive amplified polymorphism (MSAP) method for the analysis of abiotic stress.Crossref | GoogleScholarGoogle Scholar | 28431570PubMed |

Blanvillain R, Kim JH, Wu S, Lima A, Ow DW (2009) OXIDATIVE STRESS 3 is a chromatin-associated factor involved in tolerance to heavy metals and oxidative stress. The Plant Journal 57, 654–665.
OXIDATIVE STRESS 3 is a chromatin-associated factor involved in tolerance to heavy metals and oxidative stress.Crossref | GoogleScholarGoogle Scholar | 18980652PubMed |

Borges KLR, Salvato F, Loziuk PL, Muddiman DC, Azevedo RA (2019) Quantitative proteomic analysis of tomato genotypes with differential cadmium tolerance. Environmental Science and Pollution Research 26, 26039–26051.
Quantitative proteomic analysis of tomato genotypes with differential cadmium tolerance.Crossref | GoogleScholarGoogle Scholar | 31278641PubMed |

Charfeddine M, Charfeddine S, Bouaziz D, Messaoud RB, Bouzid RG (2017) The effect of cadmium on transgenic potato (Solanum tuberosum) plants overexpressing the StDREB transcription factors. Plant Cell, Tissue and Organ Culture (PCTOC) 128, 521–541.
The effect of cadmium on transgenic potato (Solanum tuberosum) plants overexpressing the StDREB transcription factors.Crossref | GoogleScholarGoogle Scholar |

Chen S, Han X, Fang J, Lu Z, Qiu W, Liu M, Sang J, Jiang J, Zhuo R (2017) Sedum alfrediiSaNramp6 metal transporter contributes to cadmium accumulation in transgenic Arabidopsis thaliana. Scientific Reports 7, 13318
Sedum alfrediiSaNramp6 metal transporter contributes to cadmium accumulation in transgenic Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 29042608PubMed |

Chen YE, Mao HT, Wu N, Khan A, Din AM, Ding CB, Zhang ZW, Yuan S, Yuan M (2019) Different tolerance of photosynthetic apparatus to Cd stress in two rice cultivars with the same leaf Cd accumulation. Acta Physiologiae Plantarum 41, 191
Different tolerance of photosynthetic apparatus to Cd stress in two rice cultivars with the same leaf Cd accumulation.Crossref | GoogleScholarGoogle Scholar |

Chen H, Liang X, Gong X, Reinfelder JR, Chen H, Sun C, Liu X, Zhang S, Li F, Liu C, Zhao J, Yi J (2021a) Comparative physiological and transcriptomic analyses illuminate common mechanisms by which silicon alleviates cadmium and arsenic toxicity in rice seedlings. Journal of Environmental Sciences 109, 88–101.
Comparative physiological and transcriptomic analyses illuminate common mechanisms by which silicon alleviates cadmium and arsenic toxicity in rice seedlings.Crossref | GoogleScholarGoogle Scholar |

Chen P, Li Z, Luo D, Jia R, Lu H, Tang M, Hu Y, Yue J, Huang Z (2021b) Comparative transcriptomic analysis reveals key genes and pathways in two different cadmium tolerance kenaf (Hibiscus cannabinus L.) cultivars. Chemosphere 263, 128211
Comparative transcriptomic analysis reveals key genes and pathways in two different cadmium tolerance kenaf (Hibiscus cannabinus L.) cultivars.Crossref | GoogleScholarGoogle Scholar | 33297170PubMed |

Choi C-S, Sano H (2007) Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants. Molecular Genetics and Genomics 277, 589–600.
Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants.Crossref | GoogleScholarGoogle Scholar | 17273870PubMed |

Coskun D, Deshmukh R, Sonah H, Menzies JG, Reynolds O, Ma JF, Kronzucker HJ, Bélanger RR (2019) The controversies of silicon’s role in plant biology. New Phytologist 221, 67–85.
The controversies of silicon’s role in plant biology.Crossref | GoogleScholarGoogle Scholar |

Dai F, Luo G, Li Z, Wei X, Wang Z, Lin S, Tang C (2020) Physiological and transcriptomic analyses of mulberry (Morus atropurpurea) response to cadmium stress. Ecotoxicology and Environmental Safety 205, 111298
Physiological and transcriptomic analyses of mulberry (Morus atropurpurea) response to cadmium stress.Crossref | GoogleScholarGoogle Scholar | 32950806PubMed |

Dalvi AA, Bhalerao SA (2013) Response of plants towards heavy metals toxicity: an overview of avoidance, tolerance and uptake mechanism. Annals of Plant Sciences 2, 362–368.

Dalyan E, Yüzbaşıoğlu E, Akpınar I (2018) Effect of 24-epibrassinolide on antioxidative defence system against lead-induced oxidative stress in the roots of Brassica juncea L. seedlings. Russian Journal of Plant Physiology 65, 570–578.
Effect of 24-epibrassinolide on antioxidative defence system against lead-induced oxidative stress in the roots of Brassica juncea L. seedlings.Crossref | GoogleScholarGoogle Scholar |

Danouche M, El Ghachtouli N, El Baouchi A, El Arroussi H (2020) Heavy metals phycoremediation using tolerant green microalgae: enzymatic and non-enzymatic antioxidant systems for the management of oxidative stress. Journal of Environmental Chemical Engineering 8, 104460
Heavy metals phycoremediation using tolerant green microalgae: enzymatic and non-enzymatic antioxidant systems for the management of oxidative stress.Crossref | GoogleScholarGoogle Scholar |

Dutta S, Mitra M, Agarwal P, Mahapatra K, De S, Sett U, Roy S (2018) Oxidative and genotoxic damages in plants in response to heavy metals stress and maintenance of genome stability. Plant Signaling & Behavior 13, e1460048
Oxidative and genotoxic damages in plants in response to heavy metals stress and maintenance of genome stability.Crossref | GoogleScholarGoogle Scholar |

Ezaki B, Higashi A, Nanba N, Nishiuchi T (2016) An S-adenosyl methionine synthetase (SAMS) gene from Andropogon virginicus L. confers aluminum stress tolerance and facilitates epigenetic gene regulation in Arabidopsis thaliana. Frontiers in Plant Science 7, 1627
An S-adenosyl methionine synthetase (SAMS) gene from Andropogon virginicus L. confers aluminum stress tolerance and facilitates epigenetic gene regulation in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 27877178PubMed |

Fan W, Liu CY, Cao B, Ma S, Hu J, Xiang Z, Zhao A (2021) A meta-analysis of transcriptomic profiles reveals molecular pathways response to cadmium stress of Gramineae. Ecotoxicology and Environmental Safety 209, 111816
A meta-analysis of transcriptomic profiles reveals molecular pathways response to cadmium stress of Gramineae.Crossref | GoogleScholarGoogle Scholar | 33360213PubMed |

Farooq MA, Hong Z, Islam F, Noor Y, Hannan F, Zhang Y, Ayyaz A, Mwamba TM, Zhou W, Song W (2021) Comprehensive proteomic analysis of arsenic induced toxicity reveals the mechanism of multilevel coordination of efficient defense and energy metabolism in two Brassica napus cultivars. Ecotoxicology and Environmental Safety 208, 111744
Comprehensive proteomic analysis of arsenic induced toxicity reveals the mechanism of multilevel coordination of efficient defense and energy metabolism in two Brassica napus cultivars.Crossref | GoogleScholarGoogle Scholar | 33396070PubMed |

Feng X, Han L, Chao D, Liu Y, Zhang Y, Wang R, Guo J, Feng R, Xu Y, Ding Y, Huang B, Zhang G (2017) Ionomic and transcriptomic analysis provides new insight into the distribution and transport of cadmium and arsenic in rice. Journal of Hazardous Materials 331, 246–256.
Ionomic and transcriptomic analysis provides new insight into the distribution and transport of cadmium and arsenic in rice.Crossref | GoogleScholarGoogle Scholar | 28273574PubMed |

Figlioli F, Sorrentino MC, Memoli V, Arena C, Maisto G, Giordano S, Capozzi F, Spagnuolo V (2019) Overall plant responses to Cd and Pb metal stress in maize: growth pattern, ultrastructure, and photosynthetic activity. Environmental Science and Pollution Research 26, 1781–1790.
Overall plant responses to Cd and Pb metal stress in maize: growth pattern, ultrastructure, and photosynthetic activity.Crossref | GoogleScholarGoogle Scholar | 30456613PubMed |

Gallo-Franco JJ, Sosa CC, Ghneim-Herrera T, Quimbaya M (2020) Epigenetic control of plant response to heavy metals stress: a new view on aluminum tolerance. Frontiers in Plant Science 11, 2025
Epigenetic control of plant response to heavy metals stress: a new view on aluminum tolerance.Crossref | GoogleScholarGoogle Scholar |

Georgiadou EC, Kowalska E, Patla K, Kulbat K, Smolińska B, Leszczyńska J, Fotopoulos V (2018) Influence of heavy metals (Ni, Cu, and Zn) on nitro-oxidative stress responses, proteome regulation and allergen production in basil (Ocimum basilicum L.) plants. Frontiers in Plant Science 9, 862
Influence of heavy metals (Ni, Cu, and Zn) on nitro-oxidative stress responses, proteome regulation and allergen production in basil (Ocimum basilicum L.) plants.Crossref | GoogleScholarGoogle Scholar | 30026745PubMed |

Gong B, Nie W, Yan Y, Gao Z, Shi Q (2017) Unravelling cadmium toxicity and nitric oxide induced tolerance in Cucumis sativus: insight into regulatory mechanisms using proteomics. Journal of Hazardous Materials 336, 202–213.
Unravelling cadmium toxicity and nitric oxide induced tolerance in Cucumis sativus: insight into regulatory mechanisms using proteomics.Crossref | GoogleScholarGoogle Scholar | 28494308PubMed |

Hasan MK, Cheng Y, Kanwar MK, Chu X-Y, Ahammed GJ, Qi Z-Y (2017) Responses of plant proteins to heavy metal stress – a review. Frontiers in Plant Science 8, 1492
Responses of plant proteins to heavy metal stress – a review.Crossref | GoogleScholarGoogle Scholar | 28928754PubMed |

Hasanuzzaman M, Fujita M (2013) Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology 22, 584–596.
Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system.Crossref | GoogleScholarGoogle Scholar | 23430410PubMed |

Helaoui S, Boughattas I, Hattab S, Mkhinini M, Alphonse V, Livet A, Bousserrhine N, Banni M (2020) Physiological, biochemical and transcriptomic responses of Medicago sativa to nickel exposure. Chemosphere 249, 126121
Physiological, biochemical and transcriptomic responses of Medicago sativa to nickel exposure.Crossref | GoogleScholarGoogle Scholar | 32065994PubMed |

Huang SQ, Peng J, Qiu CX, Yang ZM (2009) HM-regulated new microRNAs from rice. Journal of Inorganic Biochemistry 103, 282–287.
HM-regulated new microRNAs from rice.Crossref | GoogleScholarGoogle Scholar | 19081140PubMed |

Huihui Z, Xin L, Zisong X, Yue W, Zhiyuan T, Meijun A, Yuehui Z, Wenxu Z, Nan X, Guangyu S (2020) Toxic effects of heavy metals Pb and Cd on mulberry (Morus alba L.) seedling leaves: photosynthetic function and reactive oxygen species (ROS) metabolism responses. Ecotoxicology and Environmental Safety 195, 110469
Toxic effects of heavy metals Pb and Cd on mulberry (Morus alba L.) seedling leaves: photosynthetic function and reactive oxygen species (ROS) metabolism responses.Crossref | GoogleScholarGoogle Scholar | 32179235PubMed |

Hussain S, Khaliq A, Noor MA, Tanveer M, Hussain HA, Hussain S, Shah T, Mehmood T. (2020) Metal toxicity and nitrogen metabolism in plants: an overview. In ‘Carbon and nitrogen cycling in soil’. (Eds R Datta, RS Meena, SI Pathan, MT Ceccherini) pp. 221–248. (Springer)

Jakubowska D, Janicka-Russak M, Kabała K, Migocka M, Reda M (2015) Modification of plasma membrane NADPH oxidase activity in cucumber seedling roots in response to cadmium stress. Plant Science 234, 50–59.
Modification of plasma membrane NADPH oxidase activity in cucumber seedling roots in response to cadmium stress.Crossref | GoogleScholarGoogle Scholar | 25804809PubMed |

Jia X, Zhao Y, Liu T, Huang S (2016) Elevated CO2 affects secondary metabolites in Robinia pseudoacacia L. seedlings in Cd- and Pb-contaminated soils. Chemosphere 160, 199–207.
Elevated CO2 affects secondary metabolites in Robinia pseudoacacia L. seedlings in Cd- and Pb-contaminated soils.Crossref | GoogleScholarGoogle Scholar | 27376859PubMed |

Jian M, Zhang D, Wang X, Wei S, Zhao Y, Ding Q, Han Y, Ma L (2020) Differential expression pattern of the proteome in response to cadmium stress based on proteomics analysis of wheat roots. BMC Genomics 21, 1301
Differential expression pattern of the proteome in response to cadmium stress based on proteomics analysis of wheat roots.Crossref | GoogleScholarGoogle Scholar |

Jin Q, Xue Z, Dong C, Wang Y, Chu L, Xu Y (2015) Identification and characterization of microRNAs from tree peony (Paeonia ostii) and their response to copper stress. PLoS ONE 10, e0117584
Identification and characterization of microRNAs from tree peony (Paeonia ostii) and their response to copper stress.Crossref | GoogleScholarGoogle Scholar | 25658957PubMed |

Jin JF, Wang ZQ, He QY, Wang JY, Li PF, Xu JM, Zheng SJ, Fan W, Yang JL (2020) Genome-wide identification and expression analysis of the NAC transcription factor family in tomato (Solanum lycopersicum) during aluminum stress. BMC Genomics 21, 237
Genome-wide identification and expression analysis of the NAC transcription factor family in tomato (Solanum lycopersicum) during aluminum stress.Crossref | GoogleScholarGoogle Scholar |

Jing XQ, Shalmani A, Zhou MR, Shi PT, Muhammad I, Shi Y, Sharif R, Li WQ, Liu WT, Chen KM (2020) Genome-wide identification of malectin/malectin-like domain containing protein family genes in rice and their expression regulation under various hormones, abiotic stresses, and heavy metal treatments. Journal of Plant Growth Regulation 39, 492–506.
Genome-wide identification of malectin/malectin-like domain containing protein family genes in rice and their expression regulation under various hormones, abiotic stresses, and heavy metal treatments.Crossref | GoogleScholarGoogle Scholar |

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 N, You FM, Datla R, Ravichandran S, Jia B, Cloutier S (2020) Genome-wide identification of ATP binding cassette (ABC) transporter and heavy metal associated (HMA) gene families in flax (Linum usitatissimum L.). BMC Genomics 21, 722
Genome-wide identification of ATP binding cassette (ABC) transporter and heavy metal associated (HMA) gene families in flax (Linum usitatissimum L.).Crossref | GoogleScholarGoogle Scholar | 33076828PubMed |

Kim YH, Khan AL, Waqas M, Lee IJ (2017) Silicon regulates antioxidant activities of crop plants under abiotic-induced oxidative stress: a review. Frontiers in Plant Science 6, 510
Silicon regulates antioxidant activities of crop plants under abiotic-induced oxidative stress: a review.Crossref | GoogleScholarGoogle Scholar |

Kimatu JN, Jiang L, Ngezahayo F, Songdi C, Quan-Yuan Y, Pang J, Liu B (2013) Alteration in cytosine DNA methylation patterns and levels induced by aluminium toxicity stress in maize varieties. International Journal of Modern Agriculture 2, 9–25.

Kumar V, AlMomin S, Al-Shatti A, Al-Aqeel H, Al-Salameen F, Shajan AB, Nair SM (2019) Enhancement of heavy metal tolerance and accumulation efficiency by expressing Arabidopsis ATP sulfurylase gene in alfalfa. International Journal of Phytoremediation 21, 1112–1121.
Enhancement of heavy metal tolerance and accumulation efficiency by expressing Arabidopsis ATP sulfurylase gene in alfalfa.Crossref | GoogleScholarGoogle Scholar | 31044606PubMed |

Kumar A, Dubey AK, Kumar V, Ansari MA, Narayan S Kumar A, Dubey AK, Kumar V, Ansari MA, Narayan S Kumar A, Dubey AK, Kumar V, Ansari MA, Narayan S (2020a) Over-expression of chickpea glutaredoxin (CaGrx) provides tolerance to heavy metals by reducing metal accumulation and improved physiological and antioxidant defence system. Ecotoxicology and Environmental Safety 192, 110252
Over-expression of chickpea glutaredoxin (CaGrx) provides tolerance to heavy metals by reducing metal accumulation and improved physiological and antioxidant defence system.Crossref | GoogleScholarGoogle Scholar | 32014725PubMed |

Kumar A, Kumar A, Cabral-Pinto MMS, Chaturvedi AK, Shabnam AA, Subrahmanyam G, Mondal R, Gupta DK, Malyan SK, Kumar SS, Khan SA, Yadav KK (2020b) Lead toxicity: health hazards, influence on food chain, and sustainable remediation approaches. International Journal of Environmental Research and Public Health 17, 2179
Lead toxicity: health hazards, influence on food chain, and sustainable remediation approaches.Crossref | GoogleScholarGoogle Scholar |

Kumar A, Jigyasu DK, Kumar A, Subrahmanyam G, Mondal R, Shabnam AA, Cabral-Pinto MMS, Malyan SK, Chaturvedi AK, Gupta DK, Fagodiya RK, Khan SA, Bhatia A (2021a) Nickel in terrestrial biota: comprehensive review on contamination, toxicity, tolerance and its remediation approaches. Chemosphere 275, 129996
Nickel in terrestrial biota: comprehensive review on contamination, toxicity, tolerance and its remediation approaches.Crossref | GoogleScholarGoogle Scholar | 33647680PubMed |

Kumar A, Subrahmanyam G, Mondal R, Cabral-Pinto MMS, Shabnam AA, Jigyasu DK, Malyan SK, Fagodiya RK, Khan SA, Kumar A, Yu Z-G (2021b) Bio-remediation approaches for alleviation of cadmium contamination in natural resources. Chemosphere 268, 128855
Bio-remediation approaches for alleviation of cadmium contamination in natural resources.Crossref | GoogleScholarGoogle Scholar | 33199107PubMed |

Kumar A, Chaturvedi AK, Surendran U, Shabnam AA, Singh A, Vinodakumar SN, Tamuly B, Malyan SK, Khan SA, Cabral-Pinto MMS, et al. (2021c) Mechanistic overview of metal tolerance in edible plants: A physiological and molecular perspective. In ‘Handbook of bioremediation’. (Eds M Hasanuzzaman, MNV Prasad) pp. 23–47 (Academic Press: London, UK)

Lai J-L, Liu Z-W, Luo X-G (2020) A metabolomic, transcriptomic profiling, and mineral nutrient metabolism study of the phytotoxicity mechanism of uranium. Journal of Hazardous Materials 386, 121437
A metabolomic, transcriptomic profiling, and mineral nutrient metabolism study of the phytotoxicity mechanism of uranium.Crossref | GoogleScholarGoogle Scholar | 31899027PubMed |

Li J, Zhang M, Sun J, Mao X, Wang J, Liu H, Zheng H, Li X, Zhao H, Zou D (2020) Heavy metal stress-associated proteins in rice and Arabidopsis: genome-wide identification, phylogenetics, duplication, and expression profiles analysis. Frontiers in Genetics 11, 477
Heavy metal stress-associated proteins in rice and Arabidopsis: genome-wide identification, phylogenetics, duplication, and expression profiles analysis.Crossref | GoogleScholarGoogle Scholar | 32457808PubMed |

Li D, He G, Tian W, Huang Y, Meng L, He Y, Wu D, Liu Y, He T (2021) Genome-wide identification of metal tolerance genes in potato (Solanum tuberosum): response to two heavy metal stress.
Genome-wide identification of metal tolerance genes in potato (Solanum tuberosum): response to two heavy metal stress.Crossref | GoogleScholarGoogle Scholar | 35523650PubMed |

Lin M-Z, Jin M-F (2018) Soil Cu contamination destroys the photosynthetic systems and hampers the growth of green vegetables. Photosynthetica 56, 1336–1345.
Soil Cu contamination destroys the photosynthetic systems and hampers the growth of green vegetables.Crossref | GoogleScholarGoogle Scholar |

Liu H, Zhao H, Wu L, Liu A, Zhao F-J, Xu W (2017) Heavy metal ATPase 3 (HMA3) confers cadmium hypertolerance on the cadmium/zinc hyperaccumulator Sedum plumbizincicola. New Phytologist 215, 687–698.
Heavy metal ATPase 3 (HMA3) confers cadmium hypertolerance on the cadmium/zinc hyperaccumulator Sedum plumbizincicola.Crossref | GoogleScholarGoogle Scholar |

Liu J, Gao Y, Tang Y, Wang D, Chen X, Yao Y, Guo Y (2019) Genome-wide identification, comprehensive gene feature, evolution, and expression analysis of plant metal tolerance proteins in tobacco under heavy metal toxicity. Frontiers in Genetics 10, 345
Genome-wide identification, comprehensive gene feature, evolution, and expression analysis of plant metal tolerance proteins in tobacco under heavy metal toxicity.Crossref | GoogleScholarGoogle Scholar | 31105736PubMed |

Liu S, Li Y, Liu L, Min J, Liu W, Li X, Pan X, Lu X, Deng Q (2020a) Comparative proteomics in rice seedlings to characterize the resistance to cadmium stress by high-performance liquid chromatography-tandem mass spectrometry (HPLC-MS/MS) with isobaric tag for relative and absolute quantitation (iTRAQ). Analytical Letters 53, 807–820.
Comparative proteomics in rice seedlings to characterize the resistance to cadmium stress by high-performance liquid chromatography-tandem mass spectrometry (HPLC-MS/MS) with isobaric tag for relative and absolute quantitation (iTRAQ).Crossref | GoogleScholarGoogle Scholar |

Liu Y, Kang T, Cheng J-S, Yi Y-J, Han J-J, Cheng H-L, Li Q, Tang N, Liang M-X (2020b) Heterologous expression of the metallothionein PpMT2 gene from Physcomitrella patens confers enhanced tolerance to heavy metal stress on transgenic Arabidopsis plants. Plant Growth Regulation 90, 63–72.
Heterologous expression of the metallothionein PpMT2 gene from Physcomitrella patens confers enhanced tolerance to heavy metal stress on transgenic Arabidopsis plants.Crossref | GoogleScholarGoogle Scholar |

Łukowski A, Dec D (2018) Influence of Zn, Cd, and Cu fractions on enzymatic activity of arable soils. Environmental Monitoring and Assessment 190, 278
Influence of Zn, Cd, and Cu fractions on enzymatic activity of arable soils.Crossref | GoogleScholarGoogle Scholar | 29651592PubMed |

Lv A, Wen W, Fan N, Su L, Zhou P, An Y (2021) Dehydrin MsDHN1 improves aluminum tolerance of alfalfa (Medicago sativa L.) by affecting oxalate exudation from root tips. The Plant Journal 108, 441–458.
Dehydrin MsDHN1 improves aluminum tolerance of alfalfa (Medicago sativa L.) by affecting oxalate exudation from root tips.Crossref | GoogleScholarGoogle Scholar | 34363255PubMed |

Ma X, Yu D, Shao W, Xu M, Zuo Z, Wang H, Meng Y (2018) Transcriptome-wide identification and characterization of the copper and cadmium stress-responsive small RNAs and their targets in Arabidopsis thaliana. Plant and Soil 429, 391–405.
Transcriptome-wide identification and characterization of the copper and cadmium stress-responsive small RNAs and their targets in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Madhan M, Mahesh K, Rao SS (2014) Effect of 24-epibrassinolide on aluminium stress induced inhibition of seed germination and seedling growth of Cajanus cajan (L.) Millsp. International Journal of Multidisciplinary and Current Research 2, 286–290.

Mesa-Marín J, Del-Saz NF, Rodríguez-Llorente ID, Redondo-Gómez S, Pajuelo E, Ribas-Carbó M, Mateos-Naranjo E (2018) PGPR reduce root respiration and oxidative stress enhancing spartina maritima root growth and heavy metal rhizoaccumulation. Frontiers in Plant Science 9, 1500
PGPR reduce root respiration and oxidative stress enhancing spartina maritima root growth and heavy metal rhizoaccumulation.Crossref | GoogleScholarGoogle Scholar | 30386359PubMed |

Mills RF, Krijger GC, Baccarini PJ, Hall JL, Williams LE (2003) Functional expression of AtHMA4, a P1B-type ATPase of the Zn/Co/Cd/Pb subclass. The Plant Journal 35, 164–176.
Functional expression of AtHMA4, a P1B-type ATPase of the Zn/Co/Cd/Pb subclass.Crossref | GoogleScholarGoogle Scholar | 12848823PubMed |

Mondal R, Antony S, Roy S, Chattopadhyay SK (2021a) Programmed cell death (PCD) in plant: molecular mechanism, regulation, and cellular dysfunction in response to development and stress. In ‘Regulation and dysfunction of apoptosis. Vol. 2’. (Ed. Y Tutar) pp. 1–20. (IntechOpen)

Mondal R, Kumar A, Chattopadhyay SK (2021b) Structural property, molecular regulation and functional diversity of glutamine synthetase in higher plants: a data-mining bioinformatics approach. The Plant Journal 108, 1565–1584.
Structural property, molecular regulation and functional diversity of glutamine synthetase in higher plants: a data-mining bioinformatics approach.Crossref | GoogleScholarGoogle Scholar | 34628690PubMed |

Pan W, Shen J, Zheng Z, Yan X, Shou J, Wang W, Jiang L, Pan J (2018a) Overexpression of the Tibetan Plateau annual wild barley (Hordeum spontaneum) HsCIPKs enhances rice tolerance to heavy metal toxicities and other abiotic stresses. Rice 11, 51
Overexpression of the Tibetan Plateau annual wild barley (Hordeum spontaneum) HsCIPKs enhances rice tolerance to heavy metal toxicities and other abiotic stresses.Crossref | GoogleScholarGoogle Scholar | 30209684PubMed |

Pan Y, Zhu M, Wang S, Ma G, Huang X, Qiao C, Wang R, Xu X, Liang Y, Lu K, Li J, Qu C (2018b) Genome-Wide characterization and analysis of metallothionein family genes that function in metal stress tolerance in Brassica napus L. International Journal of Molecular Sciences 19, 2181
Genome-Wide characterization and analysis of metallothionein family genes that function in metal stress tolerance in Brassica napus L.Crossref | GoogleScholarGoogle Scholar |

Popa C, Petrus M (2017) Heavy metals impact at plants using photoacoustic spectroscopy technology with tunable CO2 laser in the quantification of gaseous molecules. Microchemical Journal 134, 390–399.
Heavy metals impact at plants using photoacoustic spectroscopy technology with tunable CO2 laser in the quantification of gaseous molecules.Crossref | GoogleScholarGoogle Scholar |

Pour AH, Özkan G, Nalci Ö, Haliloğlu K (2019) Estimation of genomic instability and DNA methylation due to aluminum (Al) stress in wheat (Triticum aestivum L.) using iPBS and CRED-iPBS analyses. Turkish Journal of Botany 43, 27–37.
Estimation of genomic instability and DNA methylation due to aluminum (Al) stress in wheat (Triticum aestivum L.) using iPBS and CRED-iPBS analyses.Crossref | GoogleScholarGoogle Scholar |

Qiao K, Gong L, Tian Y, Wang H, Chai T (2018) The metal-binding domain of wheat heavy metal ATPase 2 (TaHMA2) is involved in zinc/cadmium tolerance and translocation in Arabidopsis. Plant Cell Reports 37, 1343–1352.
The metal-binding domain of wheat heavy metal ATPase 2 (TaHMA2) is involved in zinc/cadmium tolerance and translocation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 29936635PubMed |

Rai A, Tripathi P, Dwivedi S, Dubey S, Shri M, Kumar S, Tripathi PK, Dave R, Kumar A, Singh R, Adhikari B, Bag M, Tripathi RD, Trivedi PK, Chakrabarty D, Tuli R (2011) Arsenic tolerances in rice (Oryza sativa) have a predominant role in transcriptional regulation of a set of genes including sulphur assimilation pathway and antioxidant system. Chemosphere 82, 986–995.
Arsenic tolerances in rice (Oryza sativa) have a predominant role in transcriptional regulation of a set of genes including sulphur assimilation pathway and antioxidant system.Crossref | GoogleScholarGoogle Scholar | 21075415PubMed |

Rai KK, Pandey N, Meena RP, Rai SP (2021) Biotechnological strategies for enhancing heavy metal tolerance in neglected and underutilized legume crops: a comprehensive review. Ecotoxicology and Environmental Safety 208, 111750
Biotechnological strategies for enhancing heavy metal tolerance in neglected and underutilized legume crops: a comprehensive review.Crossref | GoogleScholarGoogle Scholar | 33396075PubMed |

Raza A, Habib M, Kakavand SN, Zahid Z, Zahra N, Sharif R, Hasanuzzaman M (2020) Phytoremediation of cadmium: physiological, biochemical, and molecular mechanisms. Biology 9, 177
Phytoremediation of cadmium: physiological, biochemical, and molecular mechanisms.Crossref | GoogleScholarGoogle Scholar |

Rono JK, Zhang BQ, Liu XS, Wang MQ, Wang LL, Wu XC, Chen X, Cao HW, Yang ZM (2019) Identification of novel rice (Oryza sativa) HPP and HIPP genes tolerant to heavy metal toxicity. Ecotoxicology and Environmental Safety 175, 8–18.
Identification of novel rice (Oryza sativa) HPP and HIPP genes tolerant to heavy metal toxicity.Crossref | GoogleScholarGoogle Scholar | 30878662PubMed |

Saad RB, Hsouna AB, Saibi W, Hamed KB, Brini F, Ghneim-Herrera T (2018) A stress-associated protein, LmSAP, from the halophyte Lobularia maritima provides tolerance to heavy metals in tobacco through increased ROS scavenging and metal detoxification processes. Journal of Plant Physiology 231, 234–243.
A stress-associated protein, LmSAP, from the halophyte Lobularia maritima provides tolerance to heavy metals in tobacco through increased ROS scavenging and metal detoxification processes.Crossref | GoogleScholarGoogle Scholar | 30312968PubMed |

Seneviratne M, Rajakaruna N, Rizwan M, Madawala HM, Ok YS, Vithanage M (2019) HM-induced oxidative stress on seed germination and seedling development: a critical review. Environmental Geochemistry and Health 41, 1813–1831.
HM-induced oxidative stress on seed germination and seedling development: a critical review.Crossref | GoogleScholarGoogle Scholar | 28702790PubMed |

Shabbir Z, Sardar A, Shabbir A, Abbas G, Shamshad S, Khalid S, Natasha , Murtaza G, Dumat C, Shahid M (2020) Copper uptake, essentiality, toxicity, detoxification and risk assessment in soil–plant environment. Chemosphere 259, 127436
Copper uptake, essentiality, toxicity, detoxification and risk assessment in soil–plant environment.Crossref | GoogleScholarGoogle Scholar | 32599387PubMed |

Shahid M, Khalid S, Abbas G, Shahid N, Nadeem M, Sabir M, Aslam M, Dumat C (2015) Heavy metal stress and crop productivity. In ‘Crop production and global environmental issues’. (Ed. KR Hakeem) pp. 1–25. (Springer: Cham)

Singh N, Ma LQ, Vu JC, Raj A (2009) Effects of arsenic on nitrate metabolism in arsenic hyperaccumulating and non-hyperaccumulating ferns. Environmental Pollution 157, 2300–2305.
Effects of arsenic on nitrate metabolism in arsenic hyperaccumulating and non-hyperaccumulating ferns.Crossref | GoogleScholarGoogle Scholar | 19406540PubMed |

Singh M, Kumar J, Singh S, Singh VP, Prasad SM, Singh MPVVB (2015) Adaptation strategies of plants against heavy metal toxicity: a short review. Biochemistry & Pharmacology 4, 2167–2501.
Adaptation strategies of plants against heavy metal toxicity: a short review.Crossref | GoogleScholarGoogle Scholar |

Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016) Heavy metals tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Frontiers in Plant Science 6, 1143
Heavy metals tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics.Crossref | GoogleScholarGoogle Scholar | 26904030PubMed |

Singh P, Singh I, Shah K (2019) Reduced activity of nitrate reductase under heavy metal cadmium stress in rice: an in silico answer. Frontiers in Plant Science 9, 1948
Reduced activity of nitrate reductase under heavy metal cadmium stress in rice: an in silico answer.Crossref | GoogleScholarGoogle Scholar | 30697220PubMed |

Songmei L, Jie J, Yang L, Jun M, Shouling X, Yuanyuan T, Youfa L, Qingyao S, Jianzhong H (2019) Characterization and evaluation of OsLCT1 and OsNramp5 mutants generated through CRISPR/Cas9-mediated mutagenesis for breeding low Cd rice. Rice Science 26, 88–97.
Characterization and evaluation of OsLCT1 and OsNramp5 mutants generated through CRISPR/Cas9-mediated mutagenesis for breeding low Cd rice.Crossref | GoogleScholarGoogle Scholar |

Srivastava RK, Pandey P, Rajpoot R, Rani A, Dubey RS (2014) Cadmium and lead interactive effects on oxidative stress and antioxidative responses in rice seedlings. Protoplasma 251, 1047–1065.
Cadmium and lead interactive effects on oxidative stress and antioxidative responses in rice seedlings.Crossref | GoogleScholarGoogle Scholar | 24482190PubMed |

Srivastava D, Verma G, Chauhan AS, Pande V, Chakrabarty D (2019) Rice (Oryza sativa L.) tau class glutathione S-transferase (OsGSTU30) overexpression in Arabidopsis thaliana modulates a regulatory network leading to heavy metals and drought stress tolerance. Metallomics 11, 375–389.
Rice (Oryza sativa L.) tau class glutathione S-transferase (OsGSTU30) overexpression in Arabidopsis thaliana modulates a regulatory network leading to heavy metals and drought stress tolerance.Crossref | GoogleScholarGoogle Scholar | 30516767PubMed |

Sundarmoorthy P, Sankarganesh K, Selvaraj M, Baskaran L, Chidambaram AA (2015) Chromium induced changes in soybean (Glycine max L.) metabolism. World Scientific News 16, 145–178.

Suzuki N, Yamaguchi Y, Koizumi N, Sano H (2002) Functional characterization of a heavy metal binding protein CdI19 from Arabidopsis. The Plant Journal 32, 165–173.
Functional characterization of a heavy metal binding protein CdI19 from Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 12383082PubMed |

Tang L, Mao B, Li Y, Lv Q, Zhang L, Chen C, He H, Wang W, Zeng X, Shao Y, Pan Y, Hu Y, Peng Y, Fu X, Li H, Xia S, Zhao B (2017) Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Scientific Reports 7, 14438
Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield.Crossref | GoogleScholarGoogle Scholar | 29089547PubMed |

Tang F, Xiao Z, Sun F, Shen S, Chen S, Chen R, Zhu M, Zhang Q, Du H, Lu K, Li J, Qu C (2020) Genome-wide identification and comparative analysis of diacylglycerol kinase (DGK) gene family and their expression profiling in Brassica napus under abiotic stress. BMC Plant Biology 20, 473
Genome-wide identification and comparative analysis of diacylglycerol kinase (DGK) gene family and their expression profiling in Brassica napus under abiotic stress.Crossref | GoogleScholarGoogle Scholar | 33059598PubMed |

Taspinar MS, Aydin M, Sigmaz B, Yagci S, Arslan E, Agar G (2018) Aluminum-induced changes on DNA damage, DNA methylation and LTR retrotransposon polymorphism in maize. Arabian Journal for Science and Engineering 43, 123–131.
Aluminum-induced changes on DNA damage, DNA methylation and LTR retrotransposon polymorphism in maize.Crossref | GoogleScholarGoogle Scholar |

Tian W, He G, Qin L, Li D, Meng L, Huang Y, He T (2021) Genome-wide analysis of the NRAMP gene family in potato (Solanum tuberosum): identification, expression analysis and response to five heavy metals stress. Ecotoxicology and Environmental Safety 208, 111661
Genome-wide analysis of the NRAMP gene family in potato (Solanum tuberosum): identification, expression analysis and response to five heavy metals stress.Crossref | GoogleScholarGoogle Scholar | 33396171PubMed |

Tiwari S, Lata C (2018) Heavy metal stress, signaling, and tolerance due to plant-associated microbes: an overview. Frontiers in Plant Science 9, 452
Heavy metal stress, signaling, and tolerance due to plant-associated microbes: an overview.Crossref | GoogleScholarGoogle Scholar | 29681916PubMed |

Upadhyay SK, Ahmad M, Srivastava AK, Abhilash PC, Sharma B (2021) Optimization of eco-friendly novel amendments for sustainable utilization of Fly ash based on growth performance, hormones, antioxidant, and heavy metal translocation in chickpea (Cicer arietinum L.) plant. Chemosphere 267, 129216
Optimization of eco-friendly novel amendments for sustainable utilization of Fly ash based on growth performance, hormones, antioxidant, and heavy metal translocation in chickpea (Cicer arietinum L.) plant.Crossref | GoogleScholarGoogle Scholar | 33340884PubMed |

Valdés-López O, Yang SS, Aparicio-Fabre R, Graham PH, Reyes JL, Vance CP, Hernández G (2010) MicroRNA expression profile in common bean (Phaseolus vulgaris) under nutrient deficiency stresses and manganese toxicity. New Phytologist 187, 805–818.
MicroRNA expression profile in common bean (Phaseolus vulgaris) under nutrient deficiency stresses and manganese toxicity.Crossref | GoogleScholarGoogle Scholar |

Wang Y, Liu W, Shen H, Zhu X, Zhai L, Xu L, Wang R, Gong Y, Limera C, Liu L (2015) Identification of radish (Raphanus sativus L.) miRNAs and their target genes to explore miRNA-mediated regulatory networks in lead (Pb) stress responses by high-throughput sequencing and degradome analysis. Plant Molecular Biology Reporter 33, 358–376.
Identification of radish (Raphanus sativus L.) miRNAs and their target genes to explore miRNA-mediated regulatory networks in lead (Pb) stress responses by high-throughput sequencing and degradome analysis.Crossref | GoogleScholarGoogle Scholar |

Wang M-Q, Bai Z-Y, Xiao Y-F, Li Y, Liu Q-L, Zhang L, Pan Y-Z, Jiang B-B, Zhang F (2019) Transcriptomic analysis of Verbena bonariensis roots in response to cadmium stress. BMC Genomics 20, 877
Transcriptomic analysis of Verbena bonariensis roots in response to cadmium stress.Crossref | GoogleScholarGoogle Scholar | 31747870PubMed |

Wang Y-M, Yang Q, Xu H, Liu Y-J, Yang H-L (2020) Physiological and transcriptomic analysis provide novel insight into cobalt stress responses in willow. Scientific Reports 10, 2308
Physiological and transcriptomic analysis provide novel insight into cobalt stress responses in willow.Crossref | GoogleScholarGoogle Scholar | 32047223PubMed |

Xu B, Wang Y, Zhang S, Guo Q, Jin Y, Chen J, Gao Y, Ma H (2017) Transcriptomic and physiological analyses of Medicago sativa L. roots in response to lead stress. PLoS ONE 12, e0175307
Transcriptomic and physiological analyses of Medicago sativa L. roots in response to lead stress.Crossref | GoogleScholarGoogle Scholar | 28388670PubMed |

Xue ZC, Li JH, Li DS, Li SZ, Jiang CD, Liu LA, Wang SY, Kang WJ (2018) Bioaccumulation and photosynthetic activity response of sweet sorghum seedling (Sorghum bicolor L. Moench) to cadmium stress. Photosynthetica 56, 1422–1428.
Bioaccumulation and photosynthetic activity response of sweet sorghum seedling (Sorghum bicolor L. Moench) to cadmium stress.Crossref | GoogleScholarGoogle Scholar |

Yang C-H, Zhang Y, Huang C-F (2019) Reduction in cadmium accumulation in japonica rice grains by CRISPR/Cas9-mediated editing of OsNRAMP5. Journal of Integrative Agriculture 18, 688–697.
Reduction in cadmium accumulation in japonica rice grains by CRISPR/Cas9-mediated editing of OsNRAMP5.Crossref | GoogleScholarGoogle Scholar |

Zhang S, Zhang H, Qin R, Jiang W, Liu D (2009) Cadmium induction of lipid peroxidation and effects on root tip cells and antioxidant enzyme activities in Vicia faba L. Ecotoxicology 18, 814–823.
Cadmium induction of lipid peroxidation and effects on root tip cells and antioxidant enzyme activities in Vicia faba L.Crossref | GoogleScholarGoogle Scholar | 19468834PubMed |

Zhang G, Cui Y, Ding X, Dai Q (2013) Stimulation of phenolic metabolism by silicon contributes to rice resistance to sheath blight. Journal of Plant Nutrition and Soil Science 176, 118–124.
Stimulation of phenolic metabolism by silicon contributes to rice resistance to sheath blight.Crossref | GoogleScholarGoogle Scholar |

Zhang Y, Lai J-L, Ji X-H, Luo X-G (2020a) Unraveling response mechanism of photosynthetic metabolism and respiratory metabolism to uranium-exposure in Vicia faba. Journal of Hazardous Materials 398, 122997
Unraveling response mechanism of photosynthetic metabolism and respiratory metabolism to uranium-exposure in Vicia faba.Crossref | GoogleScholarGoogle Scholar | 32512460PubMed |

Zhang H, Xu Z, Guo K, Huo Y, He G, Sun H, Guan Y, Xu N, Yang W, Sun G (2020b) Toxic effects of heavy metal Cd and Zn on chlorophyll, carotenoid metabolism and photosynthetic function in tobacco leaves revealed by physiological and proteomics analysis. Ecotoxicology and Environmental Safety 202, 110856
Toxic effects of heavy metal Cd and Zn on chlorophyll, carotenoid metabolism and photosynthetic function in tobacco leaves revealed by physiological and proteomics analysis.Crossref | GoogleScholarGoogle Scholar | 32629202PubMed |

Zhao FY, Han XL, Zhang SY (2019) Combined treatment with cadmium and zinc enhances lateral root development by regulating auxin redistribution and cell-cycle gene expression in rice seedlings. Russian Journal of Plant Physiology 66, 597–608.
Combined treatment with cadmium and zinc enhances lateral root development by regulating auxin redistribution and cell-cycle gene expression in rice seedlings.Crossref | GoogleScholarGoogle Scholar |

Zheng S, Liu S, Feng J, Wang W, Wang Y, Yu Q, Liao Y, Mo Y, Xu Z, Li L, Gao X, Jia X, Zhu J, Chen R (2021a) Overexpression of a stress response membrane protein gene OsSMP1 enhances rice tolerance to salt, cold and heavy metal stress. Environmental and Experimental Botany 182, 104327
Overexpression of a stress response membrane protein gene OsSMP1 enhances rice tolerance to salt, cold and heavy metal stress.Crossref | GoogleScholarGoogle Scholar |

Zheng X, Wu K, Sun P, Zhouyang S, Wang Y, Wang H, Zheng Y, Li Q (2021b) Effects of substrate types on the transformation of heavy metal speciation and bioavailability in an anaerobic digestion system. Journal of Environmental Sciences 101, 361–372.
Effects of substrate types on the transformation of heavy metal speciation and bioavailability in an anaerobic digestion system.Crossref | GoogleScholarGoogle Scholar |

Zhou ZS, Zeng HQ, Liu ZP, Yang ZM (2012) Genome-wide identification of Medicago truncatula microRNAs and their targets reveals their differential regulation by heavy metal. Plant, Cell & Environment 35, 86–99.
Genome-wide identification of Medicago truncatula microRNAs and their targets reveals their differential regulation by heavy metal.Crossref | GoogleScholarGoogle Scholar |