The DOI matches its Crossref record; 260 of the 261 references it cites were found in a registry or an index.
Advances in “Omics” Approaches for Improving Toxic Metals/Metalloids Tolerance in Plants
Open accessAbstract
Food safety has emerged as a high-urgency matter for sustainable agricultural production. Toxic metal contamination of soil and water significantly affects agricultural productivity, which is further aggravated by extreme anthropogenic activities and modern agricultural practices, leaving food safety and human health at risk. In addition to reducing crop production, increased metals/metalloids toxicity also disturbs plants' demand and supply equilibrium. Counterbalancing toxic metals/metalloids toxicity demands a better understanding of the complex mechanisms at physiological, biochemical, molecular, cellular, and plant level that may result in increased crop productivity. Consequently, plants have established different internal defense mechanisms to cope with the adverse effects of toxic metals/metalloids. Nevertheless, these internal defense mechanisms are not adequate to overwhelm the metals/metalloids toxicity. Plants produce several secondary messengers to trigger cell signaling, activating the numerous transcriptional responses correlated with plant defense. Therefore, the recent advances in omics approaches such as genomics, transcriptomics, proteomics, metabolomics, ionomics, miRNAomics, and phenomics have enabled the characterization of molecular regulators associated with toxic metal tolerance, which can be deployed for developing toxic metal tolerant plants. This review highlights various response strategies adopted by plants to tolerate toxic metals/metalloids toxicity, including physiological, biochemical, and molecular responses. A seven-(omics)-based design is summarized with scientific clues to reveal the stress-responsive genes, proteins, metabolites, miRNAs, trace elements, stress-inducible phenotypes, and metabolic pathways that could potentially help plants to cope up with metals/metalloids toxicity in the face of fluctuating environmental conditions. Finally, some bottlenecks and future directions have also been highlighted, which could enable sustainable agricultural production.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“While HMs are essential to plants, substantially, there are non-essential HMs like chromium (Cr), cadmium (Cd), lead (Pb), manganese (Mn), etc. induce devastating negative impacts on plant growth, culminating in poor crop production and toxicity to human health (Varma, 2021; Lone and Gaffar, 2021; Varma, 2021; Raza et al., 2022; Bhat et al., 2023).”
From Plant hyperaccumulators: a state-of-the-art review on mechanism of heavy metal transport and sequestration (2025) · cites this paper as Raza et al., 2022
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“Phytotoxic effects of HMs include damage to various physiological and metabolic networks at the cellular and molecular levels (Raza et al., 2022; Bhardwaj et al., 2023).”
From Plant hyperaccumulators: a state-of-the-art review on mechanism of heavy metal transport and sequestration (2025) · cites this paper as Raza et al., 2022
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
1 retracted
Items 201–260 of 260
Zhang, F., Xiao, X., Xu, K., Cheng, X., Xie, T., Hu, J., & Wu, X. (2020) · BMC Genomics · doi:10.1186/s12864-020-6558-4 · Cited by 30
Genotoxic effects and proteomic analysis on Allium cepa var. agrogarum L. root cells under Pb stress
Lyu, G., Li, D., Li, S., Ning, C., & Qin, R. (2020) · Ecotoxicology · doi:10.1007/s10646-020-02236-x · Cited by 30
Nagel, K., Lenz, H., Kastenholz, B., Gilmer, F., Averesch, A., Putz, A., Heinz, K., Fischbach, A., Scharr, H., Fiorani, F., et al. (2020) · Plant Methods · doi:10.1186/s13007-020-00631-3 · Cited by 30
A single nucleotide substitution in TaHKT1 ; 5‐D controls shoot Na + accumulation in bread wheat
Borjigin, C., Schilling, R. K., Bose, J., Hrmová, M., Qiu, J., Wege, S., Situmorang, A., Byrt, C. S., Brien, C. J., Berger, B., et al. (2020) · Plant Cell & Environment · doi:10.1111/pce.13841 · Cited by 29
Wang, C., Tang, Z., Zhuang, J., Tang, Z., Huang, X., & Zhao, F. J. (2019) · Molecular Genetics and Genomics · doi:10.1007/s00438-019-01632-1 · Cited by 28
Patel, M., Rangani, J., Kumari, A., & Parida, A. K. (2020) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2020.08.008 · Cited by 28
EFFECT OF NITROGEN FERTILIZER ON GROWTH AND CADMIUM ACCUMULATION INSEDUM ALFREDIIHANCE
Zhu, E., Liu, D., Li, J. G., Li, T., Yang, X., He, Z. L., & Stoffella, P. J. (2010) · Journal of Plant Nutrition · doi:10.1080/01904167.2011.531363 · Cited by 27
Effect of cadmium on the growth of tomato
Rehman, F., Fa, K., Varshney, D. S., Naushin, F., & Rastogi, J. (2011) · Biology and medicine · Cited by 27
Physiological responses, tolerance, and remediation strategies in plants exposed to metalloids
Singh, S., Kumar, V., Datta, S., Dhanjal, D. S., Singh, S., Kumar, S., Kapoor, D., Prasad, R., & Singh, J. (2020) · Environmental Science and Pollution Research · doi:10.1007/s11356-020-10293-2 · Cited by 26
An integrative approach toward biosensing and bioremediation of metals and metalloids
Shukla, A., Srivastava, S., & D’Souza, S. F. (2018) · International Journal of Environmental Science and Technology · doi:10.1007/s13762-018-1766-z · Cited by 25
Mishra, V. K., Gupta, S. K., Chand, R., Yadav, P. S., Singh, S. K., Joshi, A. K., & Varadwaj, P. K. (2019) · Current Plant Biology · doi:10.1016/j.cpb.2019.100105 · Cited by 25
Zhang, P., Zhong, K., Zhong, Z., & Tong, H. (2019) · BMC Plant Biology · doi:10.1186/s12870-019-2036-z · Cited by 25
Selenium modulates cadmium-induced ultrastructural and metabolic changes in cucumber seedlings
Sun, H., Wang, X., Li, H., Bi, J., Yu, J., Liu, X., Zhou, H., & Rong, Z. (2020) · RSC Advances · doi:10.1039/d0ra02866e · Cited by 25
Ibarra, A. A. G., Wróbel, K., Barrientos, E. Y., Escobosa, A. R. C., Gutiérrez-Corona, J. F., Donis, I. E., & Wróbel, K. (2018) · Chemosphere · doi:10.1016/j.chemosphere.2018.12.145 · Cited by 24
Copper accumulation and biochemical responses of Sesuvium portulacastrum (L.)
Lokhande, V. H., Patade, V. Y., Srivastava, S., Suprasanna, P., Shrivastava, M., & Awasthi, G. (2020) · Materials Today Proceedings · doi:10.1016/j.matpr.2020.07.117 · Cited by 24
Dalyan, E., Yüzbaşıoğlu, E., Keskin, B. C., Yıldızhan, Y., Memon, A. R., Ünal, M., & Yüksel, B. (2017) · Environmental and Experimental Botany · doi:10.1016/j.envexpbot.2017.05.001 · Cited by 23
Song, X., Zhang, C., Chen, W., Zhu, Y., & Wang, Y. (2020) · Plant-Environment Interactions · doi:10.1002/pei3.10013 · Cited by 23
Self-citationMišúthová, A., Slováková, Ľ., Kollárová, K., & Vaculík, M. (2021) · Plant Physiology and Biochemistry · doi:10.1016/j.plaphy.2021.10.012 · Cited by 23
Xu, X., Zhang, S., Zhang, C., Li, T., Jia, Y., Wang, G., Yang, Z., Xian, J., Yang, Y., & Zhou, W. (2020) · Environmental Science and Pollution Research · doi:10.1007/s11356-020-08387-y · Cited by 22
Self-citationMorphological Responses and Gene Expression of Grain Amaranth (Amaranthus spp.) Growing under Cd
Lancíková, V., Tomka, M., Žiarovská, J., Gažo, J., & Hricová, A. (2020) · Plants · doi:10.3390/plants9050572 · Cited by 22
Nickel effect on root-meristem cell division in Plantago lanceolata (Plantaginaceae) seedlings
Pavlova, D. K. (2017) · Australian Journal of Botany · doi:10.1071/bt17054 · Cited by 21
Campos, N. V., Arcanjo‐Silva, S., de Freitas-Silva, L., de Araújo, T. O., Fernandes, D. P. D. S., & Azevedo, A. A. (2018) · Environmental Science and Pollution Research · doi:10.1007/s11356-017-1085-9 · Cited by 21
Yadav, B. S., Singh, S., Srivastava, S., Singh, N. K., & Mani, A. (2019) · Journal of Plant Biochemistry and Biotechnology · doi:10.1007/s13562-019-00486-3 · Cited by 21
Zeng, R., Farooq, M. U., Wang, L., Yang, S., Zheng, T., Ye, X., Jia, X., & Zhu, J. (2019) · Biomolecules · doi:10.3390/biom9040130 · Cited by 21
Oliveira, B. R. M., de Almeida, A.-A. F., Pirovani, C. P., Barroso, J. P., Neto, C. H. D. C., Santos, N. A., Ahnert, D., Baligar, V. C., & Mangabeira, P. A. O. (2020) · Ecotoxicology · doi:10.1007/s10646-020-02178-4 · Cited by 21
MicroRNAs and Their Exploration for Developing Heavy Metal-tolerant Plants
Jamla, M., Patil, S., Joshi, S., Khare, T. R., & Kumar, V. (2021) · Journal of Plant Growth Regulation · doi:10.1007/s00344-021-10476-2 · Cited by 21
Comparative proteomic analysis of pepper ( Capsicum annuum L.) seedlings under selenium stress
Zhang, C., Xu, B., Geng, W., Shen, Y., Xuan, D., Lai, Q., Shen, C., Jin, C., & Yu, C. (2019) · PeerJ · doi:10.7717/peerj.8020 · Cited by 20
Self-citationGenetic dissection of spike-related traits in wheat (Triticum aestivum L.) under aluminum stress
Farokhzadeh, S., Fakheri, B. A., Nezhad, N. M., Tahmasebi, S., & Mirsoleimani, A. (2020) · Genetic Resources and Crop Evolution · doi:10.1007/s10722-020-00907-6 · Cited by 19
Farokhzadeh, S., Fakheri, B. A., Nezhad, N. M., Tahmasebi, S., Mirsoleimani, A., & Heidari, B. (2020) · Australian Journal of Agricultural Research · doi:10.1071/cp19511 · Cited by 19
The maize shoot ionome: Its interaction partners, predictive power, and genetic determinants
Stich, B., Benke, A., Schmidt, M., Urbany, C., Shi, R., & Nicolaus Von Wirén, A. (2020) · Plant Cell & Environment · doi:10.1111/pce.13823 · Cited by 19
Ren, W., Liu, Y., Zhou, M., Shi, Z., Wang, T., Zhao, J., & Li, Y. (2019) · Journal of Integrative Agriculture · doi:10.1016/s2095-3119(18)62140-9 · Cited by 18
Farokhzadeh, S., Fakheri, B. A., Nezhad, N. M., Tahmasebi, S., Mirsoleimani, A., & McIntyre, C. L. (2019) · Genes & Genomics · doi:10.1007/s13258-019-00895-7 · Cited by 18
Gashi, B., Osmani, M., Sali Ali, A. L. I. U., Zogaj, M., & Kastrati, F. (2020) · Journal of Environmental Science and Health Part B · doi:10.1080/03601234.2020.1721229 · Cited by 18
Martín‐Rodríguez, J. Á., Ariani, A., Leija, A., Elizondo, A., Fuentes, S. I., Ramı́rez, M., Gepts, P., Hernández, G., & Formey, D. (2020) · The Plant Journal · doi:10.1111/tpj.15129 · Cited by 18
Metabolic analysis in Malus halliana leaves in response to iron deficiency
Zhang, X., Jia, X., Zhang, R., Zhu, Z.-L., Liu, B., Gao, L.-Y., & Wang, Y. (2019) · Scientia Horticulturae · doi:10.1016/j.scienta.2019.108792 · Cited by 17
Biochar Assisted Remediation of Toxic Metals and Metalloids
Dhiman, S., Ibrahim, M. F. M., Devi, K., Sharma, N., Kapoor, N., Kaur, R., Sharma, N., Tikoria, R., Ohri, P., Mir, B. A., et al. (2021) · Wiley eBooks · doi:10.1002/9781119670391.ch7 · Cited by 17
Genotypic difference of cadmium tolerance and the associated microRNAs in wild and cultivated barley
Yu, J., Wu, L., Fu, L., Shen, Q., Kuang, L., Wu, D., & Zhang, G. (2019) · Plant Growth Regulation · doi:10.1007/s10725-019-00479-1 · Cited by 16
MetaBridge: An Integrative Multi‐Omics Tool for Metabolite‐Enzyme Mapping
Blimkie, T. M., Lee, A. H., & Hancock, R. E. W. (2020) · Current Protocols in Bioinformatics · doi:10.1002/cpbi.98 · Cited by 16
Investigation and genome-wide association study of grain copper content in Chinese common wheat
Zhao, L., Pan, Y., Dong, Z., Zheng, Y., Liu, J., Geng, J., Ren, Y. N., Zhang, N., & Chen, F. (2020) · Journal of Cereal Science · doi:10.1016/j.jcs.2020.102991 · Cited by 15
Consequence of chromium-tainted soil on physical and biochemical responses of Vigna radiata L.
Rath, B. S., Hota, S., Subhadarsini, S., Dash, D., & Das, P. (2019) · Journal of Applied Biology & Biotechnology · doi:10.7324/jabb.2019.70107 · Cited by 14
MicroRNA mediated regulation of gene expression in response to heavy metals in plants
Dubey, S., Shri, M., & Chakrabarty, D. (2021) · Journal of Plant Biochemistry and Biotechnology · doi:10.1007/s13562-021-00718-5 · Cited by 14
Diana Sáenz de la, O., Cedillo-Jiménez, C. A., García-Ortega, L. F., Martínez-Reséndiz, M., Robles-Bustos, D. A., Cruz–Hernández, A., & Guevara-González, R. G. (2019) · Physiology and Molecular Biology of Plants · doi:10.1007/s12298-019-00716-x · Cited by 13
Kök, A. B., Mungan, M. D., Doğanlar, S., & Frary, A. (2019) · Chemosphere · doi:10.1016/j.chemosphere.2019.125665 · Cited by 13
Liu, L., Yin, H., Liu, Y., Shen, L., Yang, X., Zhang, D., Li, M., & Yan, M. (2021) · Processes · doi:10.3390/pr9071099 · Cited by 13
Transcriptome profile analysis of cadmium tolerance in Chinese flowering cabbage
Wang, J., Li, H., Zou, D., Zhao, J., Fan, L., & Wu, T. (2017) · Horticulture Environment and Biotechnology · doi:10.1007/s13580-017-0075-7 · Cited by 12
Ifie, J. E., IFIE-ETUMAH, S. O., & Ikhajiagbe, B. (2020) · Acta agriculturae Slovenica · doi:10.14720/aas.2020.115.1.969 · Cited by 12
Weber, M., Beyene, B., Nagler, N., Herfert, J., Schempp, S., Klecker, M., & Clemens, S. (2020) · The Plant Journal · doi:10.1111/tpj.14779 · Cited by 12
Wang, W., Ding, G., White, P. J., Wang, M., Zou, J., Xu, F., Hammond, J. P., & Shi, L. G. (2020) · Annals of Botany · doi:10.1093/aob/mcaa055 · Cited by 10
Komárková, M., Chromy, J., Pokorná, E., Soudek, P., & Máchová, P. (2020) · Plants · doi:10.3390/plants9111485 · Cited by 10
SLIDE – a web-based tool for interactive visualization of large-scale – omics data
Ghosh, S., Datta, A., Tan, K. S., & Choi, H. (2018) · Bioinformatics · doi:10.1093/bioinformatics/bty534 · Cited by 8
Singh, M., Ameta, K. D., Kaushik, R. A., & Rajawat, K. S. (2020) · Current Journal of Applied Science and Technology · doi:10.9734/cjast/2019/v38i630452 · Cited by 8
QTL excavation and analysis of candidate genes in contents of As, Cu, Fe, Hg and Zn in rice grain
Mei, L. U., Li, S., Wang, S., HongYu, Z. H. U., XuDong, Z. H. U., Zhang, Y., XianMei, W. U., Rao, Y., YueXing, W. A. N. G., & Han, L. (2020) · Scientia Sinica Vitae · doi:10.1360/ssv-2020-0052 · Cited by 8
Alka, S., Shahir, S., Ibrahim, N., Rahmad, N. B., Haliba, N., & Manan, F. A. (2021) · 3 Biotech · doi:10.1007/s13205-021-02864-y · Cited by 8
NAPPN: Who We Are, Where We Are Going, and Why You Should Join Us!
Carroll, A. A., Clarke, J., Fahlgren, N., Gehan, M. A., Lawrence‐Dill, C. J., & Lorence, A. (2019) · The Plant Phenome Journal · doi:10.2135/tppj2018.08.0006 · Cited by 7
Ye, Z., Zeng, J., Ye, L., Long, L., & Zhang, G. (2020) · Euphytica · doi:10.1007/s10681-020-2556-5 · Cited by 7
Machado: Open source genomics data integration framework
Mudadu, M. A., & Zerlotini, A. (2020) · GigaScience · doi:10.1093/gigascience/giaa097 · Cited by 7
Lead induced changes in biomarkers and proteome map of Chicory (Cichorium intybus L.)
Malik, B., & Pirzadah, T. B. (2020) · Current Botany · doi:10.25081/cb.2020.v11.6182 · Cited by 5
Mthembu, M. S., Odinga, C., Bux, F., & Swalaha, F. M. (2019) · Springer eBooks · doi:10.1007/978-981-13-1891-7_14 · Cited by 4
Kar, S., Mai, H., Khalouf, H., Abdallah, H. B., Flachbart, S., Fink‐Straube, C., Bräutigam, A., Xiong, G., Shang, L., Panda, S. K., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.01.070516 · Cited by 3
Integration of “Omic” Approaches to Unravel the Heavy Metal Tolerance in Plants
Pirzadah, T. B., Malik, B., & Hakeem, K. R. (2019) · Springer eBooks · doi:10.1007/978-3-030-19318-8_4 · Cited by 2
Flagged first, then by citations
1 of the 261 references couldn’t be matched to a known paper.
Research works printed but not linked: 6
- Bahmani, 2012, Effect of cadmium chloride on growth parameters of different bean genotypes (Phaseolus vulgaris L.)., ARPN J. Agric. Biol. Sci., 7, 35
- Kakeshpour, 2020, Tomato Class II Glutaredoxin Mutants Generated Via Multiplex CRISPR/Cas9 Genome Editing Technology are Susceptible to Multiple Abiotic Stresses.
- Lin, 2011, The detoxification effect of nitrogen on cadmium stress in Populus yunnanensis., Bot. Res. J., 4, 13
- Muntean, 2019, Heavy metals’ uptake from soil in potato tubers: an ionomic approach., ProEnvironment, 12, 159
- Parmar, 2013, Physiological, biochemical and molecular response of plants against heavy metals stress., Int. J. Curr. Res., 5, 80
- Shenton, 2019, Plant omics data center and CATchUP: web databases for effective gene mining utilizing public RNA-Seq-based transcriptome data, The Model Legume Medicago Truncatula, 1137
Cited by
Sorted by citations
Raza, A., Salehi, H., Rahman, M. A., Zahid, Z., Haghjou, M. M., Kakavand, S. N., Charagh, S., Osman, H. S., Albaqami, M., Zhuang, Y., et al. (2022) · Frontiers in Plant Science · doi:10.3389/fpls.2022.961872 · Cited by 319
Self-citationSmart reprograming of plants against salinity stress using modern biotechnological tools
Raza, A., Tabassum, J., Fakhar, A. Z., Sharif, R., Chen, H., Zhang, C., Ju, L., Fotopoulos, V., Siddique, K. H. M., Singh, R. K., et al. (2022) · Critical Reviews in Biotechnology · doi:10.1080/07388551.2022.2093695 · Cited by 259
Self-citationAnalysis of Heavy Metal Impacts on Cereal Crop Growth and Development in Contaminated Soils
Vasilachi, I. C., Stoleru, V., & Gavrilescu, M. (2023) · Agriculture · doi:10.3390/agriculture13101983 · Cited by 210
Multidimensional role of silicon to activate resilient plant growth and to mitigate abiotic stress
Mir, R. A., Bhat, B. A., Yousuf, H., Islam, S. T., Raza, A., Rizvi, M. A., Charagh, S., Albaqami, M., Sofi, P. A., & Zargar, S. M. (2022) · Frontiers in Plant Science · doi:10.3389/fpls.2022.819658 · Cited by 178
Self-citationMulti-omics revolution to promote plant breeding efficiency
Mahmood, U., Li, X., Fan, Y., Chang, W., Niu, Y., Li, J., Qu, C., & Lu, K. (2022) · Frontiers in Plant Science · doi:10.3389/fpls.2022.1062952 · Cited by 145
Metadata
- Authors
- Raza, A., Tabassum, J., Zahid, Z., Charagh, S., Bashir, S., Barmukh, R., Khan, R. S. A., Barbosa, F., Zhang, C., Chen, H., Zhuang, W., & Varshney, R. K.
- Affiliations
- Fujian Agriculture and Forestry University (CN)
- Chinese Academy of Agricultural Sciences (CN)
- National University of Sciences and Technology (PK)
- International Crops Research Institute for the Semi-Arid Tropics (IN)
- University of Agriculture Faisalabad (PK)
- Universidade de São Paulo (BR)
- Murdoch University (AU)
- Corresponding author
- Zhuang, Weijian
- Varshney, Rajeev K.
- ORCID
- Venue
- Frontiers in Plant Science
- Publisher
- Frontiers Media SA
- Published
- 2022-01-04
- Volume
- 12
- Pages
- 794373-794373
- ISSN
- 1664-462X (ISSN-L)
- PMC
- PMC8764127
- OpenAlex
- W4206241292
- Cited by
- 132
- References
- 261
- Citations by year
- 2026: 32 · 2025: 24 · 2024: 31 · 2023: 23 · 2022: 22
- FWCI
- 2.29
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Frontiers in Plant Science (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Open Access Repository of ICRISAT (International Crops Research Institute for the Semi-Arid Tropics) (acceptedVersion)
- Murdoch University Research Portal (submittedVersion, cc-by)
- Murdoch University Research Portal (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Bill and Melinda Gates Foundation (OPP1114827)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Micronutrient Interactions and Effects
- Physical Sciences › Environmental Science › Pollution › Heavy metals in environment
- Keywords
- metalloids, heavy metal toxicity, plant stress response, omics approaches, transcriptomics, proteomics, metabolomics, ionomics, phenomics, plant defense, stress-inducible genes, food safety, soil and water contamination
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
