INTEGRATIVE MULTI-OMICS INSIGHTS INTO HEAVY METAL STRESS TOLERANCE IN AMARANTHUS: TOWARDS SUSTAINABLE PHYTOREMEDIATION AND NUTRACEUTICAL CROP DEVELOPMENT

L IQRA; S AIMEN; Q ALI

doi:10.64013/bbasr.v2026i1.127

Authors

L IQRA Department of Botany, Division of Science and Technology, University of Education, Lahore, Pakistan
S AIMEN Department of Botany, The Women University Multan, Pakistan
Q ALI Department of Plant Breeding and Genetics, Faculty of Agricultural Sciences, University of the Punjab, P.O BOX. 54590, Lahore, Pakistan

DOI:

https://doi.org/10.64013/bbasr.v2026i1.127

Keywords:

heavy metals, contaminated soil, high-throughput omics, antioxidative defense pathways

Abstract

Amaranthus spp. has great potential as a nutritionally complete, climate-resilient crop that is suited for cultivation on marginal or contaminated soils. However, the continuing increase in the amount of toxic heavy metals i.e., cadmium (Cd), lead (Pb), and arsenic (As) present within soils, is a major limiting factor for crop productivity, food safety, and environmental sustainability. Recent advances in high-throughput omics technologies, which have produced system-level insights related to plant responses to stress, have not been effectively applied to amaranth. This review summarizes current scientific knowledge concerning the molecular mechanisms that underlie the ability of Amaranthus spp. to tolerate heavy metal stress through the use of integrative multi-omics strategies. These tolerance strategies include metal transport, chelation, antioxidant defense, and stress signaling, and will be considered through the lens of systems biology to illustrate how these mechanisms are coordinated with one another. A review of the current state of genomics, transcriptomics, proteomics, and metabolomics research revealed critical issues with data integration, functional validation, and species-specific resources. Constraints such as low genetic diversity, low transformation efficiency, and multi-omics data integration difficulties are discussed. Future directions highlighted the integration of multi-omics with genome editing techniques and artificial intelligence to accelerate the development of heavy metal-tolerant and nutritionally-enhanced amaranth cultivars, thereby supporting sustainable agricultural systems and resilient food systems.

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References

Agarwal, V., Nehra, M. R., Gupta, S., and Nehra, N. (2022). Heavy metals stress tolerance mechanism in crop plants. The Pharma Innovat J 11, 2716-2726.

Ali, M. A., Fahad, S., Haider, I., Ahmed, N., Ahmad, S., Hussain, S., and Arshad, M. (2019). Oxidative stress and antioxidant defense in plants exposed to metal/metalloid toxicity. Reactive oxygen, nitrogen and sulfur species in plants: production, metabolism, signaling and defense mechanisms, 353-370.

Alsherif, E., Okla, M. K., Alaraidh, I. A., Elbadawi, Y. B., AlGarawi, A. M., Khanghahi, M. Y., Crecchio, C., and AbdElgawad, H. (2024). Metabolic and biochemical analyses reveal heavy metals tolerance mechanisms in Amaranthus retroflexus L. Flora 320, 152601.

Ansari, A., Kafeel, M., Gaffar, S. A., and Chaachouay, N. (2024). Heavy Metal Stress and Cellular Antioxidant Systems of Plants: A Review. Agricultural Reviews 45.

Aslam, M., Aslam, A., Sheraz, M., Ali, B., Ulhassan, Z., Najeeb, U., Zhou, W., and Gill, R. A. (2021). Lead toxicity in cereals: Mechanistic insight into toxicity, mode of action, and management. Frontiers in plant science 11, 587785.

Balabantaray, A., Behera, S., Liew, C., Chamara, N., Singh, M., Jhala, A. J., and Pitla, S. (2024). Targeted weed management of Palmer amaranth using robotics and deep learning (YOLOv7). Frontiers in Robotics and AI 11, 1441371.

Barba de la Rosa, A. P., Cetz, J., Bojórquez-Velázquez, E., Martínez, J. P., De León-Rodríguez, A., Espitia-Rangel, E., and Herrera-Estrella, A. (2026). Transcriptome and metabolite profiles reveal differential molecular responses of wild and cultivated amaranth species to water deficit and salt stress. Planta 263, 59.

Bello, A. A., Muhammad, I. A., Yunusa, A., Mikail, T. A., Hamza, I., Habib, I., and Muhammad, M. (2021). Heavy metals contamination of agricultural land and their impact on food safety. European Journal of Nutrition & Food Safety 13, 104-111.

Bhat, B. A., Rather, M. A., Bilal, T., Nazir, R., Qadir, R. U., and Mir, R. A. (2025). Plant hyperaccumulators: a state-of-the-art review on mechanism of heavy metal transport and sequestration. Frontiers in Plant Science 16, 1631378.

Bojórquez-Velázquez, E., Zamora-Briseño, J. A., Barrera-Pacheco, A., Espitia-Rangel, E., Herrera-Estrella, A., and Barba de la Rosa, A. P. (2024). Comparative Proteomic Analysis of Wild and Cultivated Amaranth Species Seeds by 2-DE and ESI-MS/MS. Plants 13, 2728.

Chawla, N., Kumar, S., and Gupta, L. (2024). Advancing phytoremediation from lab research to field applications. In "Environmental Engineering and Waste Management: Recent Trends and Perspectives", pp. 471-498. Springer.

Chen, X., Zhao, Y., Zhong, Y., Chen, J., and Qi, X. (2023). Deciphering the functional roles of transporter proteins in subcellular metal transportation of plants. Planta 258, 17.

Cho, J. Y., Hamayun, M., and Kim, H.-Y. (2025). Growth dynamics and metabolite profiling of four Korean Sedum species in a vertical farming system: Implications for antioxidant and tyrosinase inhibitory activities. Industrial Crops and Products 234, 121588.

Chowdhury, F. N., and Rahman, M. M. (2024). Source and distribution of heavy metal and their effects on human health. In "Heavy metal toxicity: Human health impact and mitigation strategies", pp. 45-98. Springer.

Clawson, H., Lee, B. T., Raney, B. J., Barber, G. P., Casper, J., Diekhans, M., Fischer, C., Gonzalez, J. N., Hinrichs, A. S., and Lee, C. M. (2023). GenArk: towards a million UCSC genome browsers. Genome Biology 24, 217.

Clouse, J., Adhikary, D., Page, J., Ramaraj, T., Deyholos, M., Udall, J., Fairbanks, D., Jellen, E., and Maughan, P. (2016). The amaranth genome: genome, transcriptome, and physical map assembly. The Plant Genome 9, plantgenome2015.07.0062.

Escolà, G., Garcia-Molina, A., Almira-Casellas, M., Poschenrieder, C., and Busoms, S. (2026). Transcriptomic Insights into Plant Adaptation. In "Plant Transcriptomics and Epitranscriptomics: Decoding the RNA Landscape", pp. 67-101. Springer.

Fang, X., Jin, W., Liang, Q., Liang, Z., and Sun, M. (1996). Electron-microscopic study of microsporogenesis in male-sterile and male-fertile grain amaranth (Amaranthus hypochondriacus L.). Developmental & Reproductive Biology.

Farooq, M., and Siddique, K. H. (2022). "Neglected and underutilized crops: Future smart food," Elsevier.

Galahitigama, H., Amarasiri, D., Wijesooriya, M. M., Wijesekara, H., and Rinklebe, J. (2025). Wild plants as a promising tool for phytoremediation of trace metal (loid) s contaminated soil: A review. Reviews of Environmental Contamination and Toxicology 263, 12.

Ganger, S., Harale, G., and Majumdar, P. (2023). Clustered regularly interspaced short palindromic repeats/CRISPR-associated (CRISPR/Cas) systems: Discovery, structure, classification, and general mechanism. In "CRISPR/Cas-Mediated Genome Editing in Plants", pp. 65-97. Apple Academic Press.

Gudu, S., and Gupta, V. (1988). Male-sterility in the grain amaranth (Amaranthus hypochondriacus ex-Nepal) variety Jumla. Euphytica 37, 23-26.

Hoque, M. N., Tahjib-Ul-Arif, M., Hannan, A., Sultana, N., Akhter, S., Hasanuzzaman, M., Akter, F., Hossain, M. S., Sayed, M. A., and Hasan, M. T. (2021). Melatonin modulates plant tolerance to heavy metal stress: morphological responses to molecular mechanisms. International journal of molecular sciences 22, 11445.

Huang, R., Xing, C., Yang, Y., Yu, W., Zeng, L., Li, Y., Tan, Z., and Li, Z. (2024). Phytoremediation and environmental effects of three Amaranthaceae plants in contaminated soil under intercropping systems. Science of the Total Environment 914, 169900.

Hussain, B., Abbas, A., Saleem, A. R., Riaz, L., Rahman, S. U., Liu, S., Pu, S., and Farooq, M. (2024). Uptake, agglomeration, and detoxification of trace metals and metalloids in plants. Journal of Soil Science and Plant Nutrition 24, 4965-4983.

Imadi, S. R., Kazi, A. G., Ahanger, M. A., Gucel, S., and Ahmad, P. (2015). Plant transcriptomics and responses to environmental stress: an overview. Journal of genetics 94, 525-537.

Ioniță, M. F., Dunca, E. C., and Radu, S. M. (2026). Molecular and Cellular Mechanisms of Plant Responses to Heavy Metal Stress in Mining-Impacted Environments. Plants 15, 1045.

Kress, W. J., Soltis, D. E., Kersey, P. J., Wegrzyn, J. L., Leebens-Mack, J. H., Gostel, M. R., Liu, X., and Soltis, P. S. (2022). Green plant genomes: What we know in an era of rapidly expanding opportunities. Proceedings of the National Academy of Sciences 119, e2115640118.

Lancíková, V., Kačírová, J., and Hricová, A. (2023). Identification and gene expression analysis of cytosine-5 DNA methyltransferase and demethylase genes in Amaranthus cruentus L. under heavy metal stress. Frontiers in Plant Science 13, 1092067.

Lancíková, V., Tomka, M., Žiarovská, J., Gažo, J., and Hricová, A. (2020). Morphological responses and gene expression of grain Amaranth (Amaranthus spp.) growing under Cd. Plants 9, 572.

Lightfoot, D., Jarvis, D. E., Ramaraj, T., Lee, R., Jellen, E., and Maughan, P. (2017). Single-molecule sequencing and Hi-C-based proximity-guided assembly of amaranth (Amaranthus hypochondriacus) chromosomes provide insights into genome evolution. BMC biology 15, 74.

Liu, C., Wen, L., Cui, Y., Ahammed, G. J., and Cheng, Y. (2024). Metal transport proteins and transcription factor networks in plant responses to cadmium stress. Plant cell reports 43, 218.

Liu, Z., Song, J., Miao, W., Yang, B., Zhang, Z., Chen, W., Tan, F., Suo, H., Dai, X., and Zou, X. (2021). Comprehensive proteome and lysine acetylome analysis reveals the widespread involvement of acetylation in cold resistance of pepper (Capsicum annuum L.). Frontiers in Plant Science 12, 730489.

Ma, X., Vaistij, F. E., Li, Y., Jansen van Rensburg, W. S., Harvey, S., Bairu, M. W., Venter, S. L., Mavengahama, S., Ning, Z., and Graham, I. A. (2021). A chromosome‐level Amaranthus cruentus genome assembly highlights gene family evolution and biosynthetic gene clusters that may underpin the nutritional value of this traditional crop. The Plant Journal 107, 613-628.

Macías-Naranjo, S. M., Arjona, J. M., Huebra-Montero, L., Rubio-Heras, J., Sánchez-Vicente, I., García-Molina, C. G., Aparicio, N., and Albertos, P. (2026). Amaranth, the ancient pseudocereal: a promising crop for climate-resilient agriculture and healthy diets. Frontiers in Plant Science 17, 1716624.

Mansoor, S., Ali, A., Kour, N., Bornhorst, J., AlHarbi, K., Rinklebe, J., Abd El Moneim, D., Ahmad, P., and Chung, Y. S. (2023). Heavy metal induced oxidative stress mitigation and ROS scavenging in plants. Plants 12, 3003.

Miernyk, J. A., and Hajduch, M. (2011). Seed proteomics. Journal of proteomics 74, 389-400.

Mohanta, T. K., Bashir, T., Hashem, A., Abd_Allah, E. F., Khan, A. L., and Al-Harrasi, A. S. (2018). Early events in plant abiotic stress signaling: interplay between calcium, reactive oxygen species and phytohormones. Journal of Plant Growth Regulation 37, 1033-1049.

Moshood, A. Y., Abdulraheem, M. I., Li, L., Zhang, Y., Raghavan, V., and Hu, J. (2025). Deciphering nutrient stress in plants: integrative insight from metabolomics and proteomics. Functional & Integrative Genomics 25, 38.

Nawaz, M., Hassan, M. U., Chattha, M. U., Mahmood, A., Shah, A. N., Hashem, M., Alamri, S., Batool, M., Rasheed, A., and Thabit, M. A. (2022). Trehalose: A promising osmo-protectant against salinity stress—physiological and molecular mechanisms and future prospective. Molecular Biology Reports 49, 11255-11271.

Ningombam, L., Hazarika, B., Yumkhaibam, T., Heisnam, P., and Singh, Y. D. (2024). Heavy metal priming plant stress tolerance deciphering through physiological, biochemical, molecular and omics mechanism. South African Journal of Botany 168, 16-25.

Nkuna, M., Gavhi, P., Kanyerere, A. M., Ikebudu, V. C., Ndou, N., Faro, A., Doumbia, I. Z., Ajayi, R. F., Mulidzi, A. R., and Lewu, N. (2025). Drought tolerance mechanisms in grain and vegetable Amaranthus species: Physiological, biochemical and molecular insights. Horticulturae 11, 1226.

Nyonje, W. A., Makokha, A., Owino, W., Lin, C.-Y., Yang, R.-Y., and Abukutsa-Onyango, M. (2025). Nutritional metabolite accumulation and transcription of selected biosynthesis genes in response to drought stress in leaf amaranth (Amaranthus sp.). Scientific African 27, e02526.

Pal, A., Swain, S. S., Mukherjee, A. K., and Chand, P. K. (2013). Agrobacterium pRi T^ sub L^-DNA rolB and T^ sub R^-DNA Opine Genes Transferred to the Spiny Amaranth (Amaranthus spinosus L.), A nutraceutical crop. Food technology and Biotechnology 51, 26.

Peng, Z., Rehman, A., Li, X., Jiang, X., Tian, C., Wang, X., Li, H., Wang, Z., He, S., and Du, X. (2023). Comprehensive evaluation and transcriptome analysis reveal the salt tolerance mechanism in semi-wild cotton (Gossypium purpurascens). International Journal of Molecular Sciences 24, 12853.

Qi, H., Han, X., Huang, J., Wu, X., and Han, J. (2026). Integrated Transcriptomic, Proteomic, and Metabolomic Analysis of a Chromosome Segment Substitution Line Reveals the Regulatory Mechanism Governing Fatty Acids and Storage Proteins in Soybean Seeds. Genes 17, 432.

Raiyemo, D. A., Montgomery, J. S., Cutti, L., Abdollahi, F., Llaca, V., Fengler, K., Lopez, A. J., Morran, S., Saski, C. A., and Nelson, D. R. (2025). Chromosome‐level assemblies of Amaranthus palmeri, Amaranthus retroflexus, and Amaranthus hybridus allow for genomic comparisons and identification of a sex‐determining region. The Plant Journal 121, e70027.

Ravi, B., Foyer, C. H., and Pandey, G. K. (2023). The integration of reactive oxygen species (ROS) and calcium signalling in abiotic stress responses. Plant, Cell & Environment 46, 1985-2006.

Raza, A., Tabassum, J., Zahid, Z., Charagh, S., Bashir, S., Barmukh, R., Khan, R. S. A., Barbosa Jr, F., Zhang, C., and Chen, H. (2022). Advances in “omics” approaches for improving toxic metals/metalloids tolerance in plants. Frontiers in Plant Science 12, 794373.

Rekha, K., Usha, B., and Keeran, N. S. (2021). Role of ABC transporters and other vacuolar transporters during heavy metal stress in plants. In "Metal and nutrient transporters in abiotic stress", pp. 55-76. Elsevier.

Salgotra, R. K., and Chauhan, B. S. (2023). Genetic diversity, conservation, and utilization of plant genetic resources. Genes 14, 174.

Samodelov, S. L., Kullak-Ublick, G. A., Gai, Z., and Visentin, M. (2020). Organic cation transporters in human physiology, pharmacology, and toxicology. International journal of molecular sciences 21, 7890.

Sandhu, P. K., Kumar, R., Nandula, V., and Tharayil, N. (2025). Integrated multi-omics analysis reveals divergent molecular responses in Palmer amaranth (Amaranthus palmeri) biotypes susceptible and resistant to glyphosate. bioRxiv, 2025.07. 20.665775.

Segura-Jiménez, M. E., and Jacobo-Velázquez, D. A. (2025). Amaranthus spp.: A multifunctional crop at the nexus of nutrition, health, and sustainable innovation. Journal of Agriculture and Food Research 24, 102322.

Sethi, S. (2023). Phytochelatins: Heavy metal detoxifiers in plants. In "Advanced and innovative approaches of environmental biotechnology in industrial wastewater treatment", pp. 361-379. Springer.

Sharma, J. K., Kumar, N., Singh, N. P., and Santal, A. R. (2023). Phytoremediation technologies and their mechanism for removal of heavy metal from contaminated soil: An approach for a sustainable environment. Frontiers in plant science 14, 1076876.

Srivastava, A. K., Kumari, S., Singh, R. P., Khan, M., Mishra, P., and Xie, X. (2025). Harnessing the interplay of protein posttranslational modifications: Enhancing plant resilience to heavy metal toxicity. Microbiological Research 295, 128112.

Tóth, G., Hermann, T., Da Silva, M. R., and Montanarella, L. (2016). Heavy metals in agricultural soils of the European Union with implications for food safety. Environment international 88, 299-309.

Vollmer, S. K., Stetter, M. G., and Hensel, G. (2025). First successful targeted mutagenesis using CRISPR/Cas9 in stably transformed grain amaranth tissue. Plant Biotechnology Journal.

Wainstein, T., Elliott, A. M., and Austin, J. C. (2023). Considerations for the use of qualitative methodologies in genetic counseling research. Journal of Genetic Counseling 32, 300-314.

Xie, M., Chen, W., Lai, X., Dai, H., Sun, H., Zhou, X., and Chen, T. (2019). Metabolic responses and their correlations with phytochelatins in Amaranthus hypochondriacus under cadmium stress. Environmental pollution 252, 1791-1800.

Xing, J., Cai, H., Lin, Z., Zhao, L., Xu, H., Song, Y., Wang, Z., Liu, C., Hu, G., and Zheng, J. (2024). Examining the function of macrophage oxidative stress response and immune system in glioblastoma multiforme through analysis of single-cell transcriptomics. Frontiers in Immunology 14, 1288137.

Yadav, A., and Yadav, K. (2024). From humble beginnings to nutritional powerhouse: the rise of Amaranth as a climate-resilient superfood. Tropical Plants 3.

Yap, C. K., Yaacob, A., Tan, W. S., Al-Mutairi, K. A., Cheng, W. H., Wong, K. W., Berandah Edward, F., Ismail, M. S., You, C.-F., and Chew, W. (2022). Potentially toxic metals in the high-biomass non-hyperaccumulating plant Amaranthus viridis: human health risks and phytoremediation potentials. Biology 11, 389.

Zhao, Z., Zhu, K., Tang, D., Wang, Y., Wang, Y., Zhang, G., Geng, Y., and Yu, H. (2021). Comparative analysis of mitochondrial genome features among four Clonostachys species and insight into their systematic positions in the order Hypocreales. International Journal of Molecular Sciences 22, 5530.