Mapping Plant Biotechnology Research for Low Heavy Metal Accumulation and Crop Safety: A Bibliometric–SLR Study Highlighting CRISPR-Cas9

Authors

  • Nur Meili Zakiyah Universitas Pembangunan Nasional “Veteran” Jawa Timur, Indonesia
  • Bella Rhea Lavifa Sanjaya Dongguk University, Korea
  • Sutini Sutini Universitas Pembangunan Nasional “Veteran” Jawa Timur, Indonesia

DOI:

https://doi.org/10.70609/g-tech.v10i1.8732

Keywords:

Bibliometric–SLR, CRISPR-Cas9, Food security, Heavy metal accumulation, Plant biotechnology

Abstract

Heavy metal contamination in agriculture presents a growing risk to food security, underscoring the need for precise and scalable biotechnological solutions. This study maps the research landscape of plant biotechnology for reducing heavy metal accumulation using an integrated bibliometric analysis (Bibliometrix/Biblioshiny and VOSviewer) combined with a PRISMA-based SLR of 43 English-language empirical articles published between 1997 and 2025. The analysis identifies four major thematic clusters: tolerance mechanisms, field applications, multi-omics, and genome editing that indicating a shift from early physiological studies toward precision biotechnology. The focused SLR reveals that CRISPR-Cas9, although still limited in publication volume, has emerged as a strategically positioned research front, particularly in recent crop-focused genome-editing studies involving agriculturally relevant species. Geographical patterns show strong research productivity in Asia and high scientific influence in Western countries. Despite the modest dataset, this study provides a strategic roadmap for prioritizing CRISPR applications, strengthening interdisciplinary integration, and accelerating biotechnology-based solutions for food safety and sustainable agriculture.

References

Abou Auda, M. M., Symeonidis, L., Hatzistavrou, E., & Yupsanis, T. (2002). Nucleolytic activities and appearance of a new DNase in relation to nickel and manganese accumulation in Alyssum murale. Journal of Plant Physiology, 159(10), 1087–1095. https://doi.org/10.1078/0176-1617-00667 DOI: https://doi.org/10.1078/0176-1617-00667

Acharya, A., Bellaloui, N., Pilipovic, A., Perez, E., Maddox-Mandolini, M., & Fuente, H. D. La. (2025). Current Assessment and Future Perspectives on Phytoremediation of Heavy Metals. Plants, 14(18), 2847. https://doi.org/10.3390/plants14182847 DOI: https://doi.org/10.3390/plants14182847

Akbar, S., Ali, Z., Hussain, S., Mohammad, A., Riaz, Y., Shakeel, A., Ahmad, I., Mussarat, M., Malik, R. N., Khan, K. Y., Sohail, M., & Quraishi, U. M. (2021). Metal accumulation potential, human health risks, and yield attributes of hundred bread wheat genotypes on irrigation with municipal and remediated wastewater. Environmental Science and Pollution Research, 28(26), 35023–35037. https://doi.org/10.1007/s11356-021-13085-4 DOI: https://doi.org/10.1007/s11356-021-13085-4

Clemens, S. (2001). Developing tools for phytoremediation: Towards a molecular understanding of plant metal toleranoe and accumulation. International Journal of Occupational Medicine and Environmental Health, 14(3), 235–239. https://www.scopus.com/inward/record.uri?eid=2-s2.0-0034768385&partnerID=40&md5=1dbb1647781db840e38d2642cff13dea

DalCorso, G., Martini, F., Fasani, E., Manara, A., Visioli, G., & Furini, A. (2021). Enhancement of Zn tolerance and accumulation in plants mediated by the expression of Saccharomyces cerevisiae vacuolar transporter ZRC1. Planta, 253(6). https://doi.org/10.1007/s00425-021-03634-z DOI: https://doi.org/10.1007/s00425-021-03634-z

Ifthikhar, S., Ahmad, K. S., & Jaffri, S. B. (2018). Mycodriven enhancement and inherent phytoremediation potential exploration of plants for lithospheric remediation. Sydowia, 70, 141–153. https://doi.org/10.12905/0380.sydowia70-2018-0141

Ike, A., Sriprang, R., Ono, H., Murooka, Y., & Yamashita, M. (2008). Promotion of metal accumulation in nodule of Astragalus sinicus by the expression of the iron-regulated transporter gene in Mesorhizobium huakuii subsp. rengei B3. Journal of Bioscience and Bioengineering, 105(6), 642–648. https://doi.org/10.1263/jbb.105.642 DOI: https://doi.org/10.1263/jbb.105.642

Irshad, S., Xie, Z., Qing, M., Ali, H., Ali, I., Ahmad, N., Rizwan Khan, M., & Nawaz, A. (2024). Application of coconut shell activated carbon filter in vertical subsurface flow constructed wetland for enhanced multi-metal bioremediation and antioxidant response of Salvinia cucullate. Environmental Pollution, 346. https://doi.org/10.1016/j.envpol.2024.123597 DOI: https://doi.org/10.1016/j.envpol.2024.123597

Khan, S. R., Singh, S. K., & Rastogi, N. (2017). Heavy metal accumulation and ecosystem engineering by two common mine site-nesting ant species: Implications for pollution-level assessment and bioremediation of coal mine soil. Environmental Monitoring and Assessment, 189(4). https://doi.org/10.1007/s10661-017-5865-y DOI: https://doi.org/10.1007/s10661-017-5865-y

Kim, I. S., Kang, K. H., Johnson-Green, P., & Lee, E. J. (2003). Investigation of heavy metal accumulation in Polygonum thunbergii for phytoextraction. Environmental Pollution, 126(2), 235–243. https://doi.org/10.1016/S0269-7491(03)00190-8 DOI: https://doi.org/10.1016/S0269-7491(03)00190-8

Kumar, A., Dubey, A. K., Kumar, V., Ansari, M. A., Narayan, S., Meenakshi, Kumar, S., Pandey, V., Shirke, P. A., Pande, V., & Sanyal, I. (2020). 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. https://doi.org/10.1016/j.ecoenv.2020.110252 DOI: https://doi.org/10.1016/j.ecoenv.2020.110252

Kumar, V., AlMomin, S., Al-Shatti, A., Al-Aqeel, H., Al-Salameen, F., Shajan, A. B., & Nair, S. M. (2019). Enhancement of heavy metal tolerance and accumulation efficiency by expressing Arabidopsis ATP sulfurylase gene in alfalfa. International Journal of Phytoremediation, 21(11), 1112–1121. https://doi.org/10.1080/15226514.2019.1606784 DOI: https://doi.org/10.1080/15226514.2019.1606784

Liu, X., Wang, H., He, F., Du, X., Ren, M., & Bao, Y. (2022). The TaWRKY22–TaCOPT3D pathway governs cadmium uptake in wheat. International Journal of Molecular Sciences, 23(18). https://doi.org/10.3390/ijms231810379 DOI: https://doi.org/10.3390/ijms231810379

Lu, J., Xing, G., Zhang, Y., Zhang, H., Wu, T., Tian, Z., & Qu, L. (2024). Genome-wide identification, expression and function analysis of the MTP gene family in tulip (Tulipa gesneriana). Frontiers in Plant Science, 15. https://doi.org/10.3389/fpls.2024.1346255 DOI: https://doi.org/10.3389/fpls.2024.1346255

Lu, M., Jiao, S., Gao, E., Song, X., Li, Z., Hao, X., Rensing, C., & Wei, G. (2017). Transcriptome response to heavy metals in Sinorhizobium meliloti CCNWSX0020 reveals new metal resistance determinants that also promote bioremediation by Medicago lupulina in metal-contaminated soil. Applied and Environmental Microbiology, 83(20). https://doi.org/10.1128/AEM.01244-17 DOI: https://doi.org/10.1128/AEM.01244-17

Mills, R. F., Valdes, B., Duke, M., Peaston, K. A., Lahner, B., Salt, D. E., & Williams, L. E. (2010). Functional significance of AtHMA4 C-terminal domain in Planta. PLoS ONE, 5(10). https://doi.org/10.1371/journal.pone.0013388 DOI: https://doi.org/10.1371/journal.pone.0013388

Mohamed, H. I., Ullah, I., Toor, M. D., Tanveer, N. A., Din, M. M. U., Basit, A., Sultan, Y., Muhammad, M., & Rehman, M. U. (2025). Heavy metals toxicity in plants: understanding mechanisms and developing coping strategies for remediation: a review. Bioresources and Bioprocessing, 12(1), 95. https://doi.org/10.1186/s40643-025-00930-4 DOI: https://doi.org/10.1186/s40643-025-00930-4

Mohite, B. V., Koli, S. H., & Patil, S. V. (2018). Heavy metal stress and its consequences on exopolysaccharide (EPS)-producing Pantoea agglomerans. Applied Biochemistry and Biotechnology, 186(1), 199–216. https://doi.org/10.1007/s12010-018-2727-1 DOI: https://doi.org/10.1007/s12010-018-2727-1

Nahar, N., Rahman, A., Nawani, N. N., Ghosh, S., & Mandal, A. (2017). Phytoremediation of arsenic from the contaminated soil using transgenic tobacco plants expressing ACR2 gene of Arabidopsis thaliana. Journal of Plant Physiology, 218, 121–126. https://doi.org/10.1016/j.jplph.2017.08.001 DOI: https://doi.org/10.1016/j.jplph.2017.08.001

Nehnevajova, E., Herzig, R., Federer, G., Erismann, K.-H., & Schwitzguébel, J.-P. (2005). Screening of sunflower cultivars for metal phytoextraction in a contaminated field prior to mutagenesis. International Journal of Phytoremediation, 7(4), 337–349. https://doi.org/10.1080/16226510500327210 DOI: https://doi.org/10.1080/16226510500327210

Nehnevajova, E., Schmülling, T., Herzig, T., & Schwitzguébel, J. P. (2009). Increased tolerance of sunflower mutant seedlings to Cd and Zn in hydroponic culture. Agrochimica, 53(6), 353–366. https://www.scopus.com/inward/record.uri?eid=2-s2.0-76749117279&partnerID=40&md5=4dc4e27cb889fc3d5485d10f41dcbf24

Nguyen, N. H., Nguyen, Q. T., Dang, D. H., & Emery, R. J. N. (2023). Phytohormones enhance heavy metal responses in Euglena gracilis: Evidence from uptake of Ni, Pb and Cd and linkages to hormonomic and metabolomic dynamics. Environmental Pollution, 320. https://doi.org/10.1016/j.envpol.2023.121094 DOI: https://doi.org/10.1016/j.envpol.2023.121094

Palmer, C. E., Warwick, S., & Keller, W. (2001). Brassicaceae (Cruciferae) family, plant biotechnology, and phytoremediation. International Journal of Phytoremediation, 3(3), 245–287. https://doi.org/10.1080/15226510108500059 DOI: https://doi.org/10.1080/15226510108500059

Pence, N. S., Larsen, P. B., Ebbs, S. D., Letham, D. L. D., Lasat, M. M., Garvin, D. F., Eide, D., & Kochian, L. V. (2000). The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proceedings of the National Academy of Sciences of the United States of America, 97(9), 4956–4960. https://doi.org/10.1073/pnas.97.9.4956 DOI: https://doi.org/10.1073/pnas.97.9.4956

Picault, N., Cazalé, A. C., Beyly, A., Cuiné, S., Carrier, P., Luu, D. T., Forestier, C., & Peltier, G. (2006). Chloroplast targeting of phytochelatin synthase in Arabidopsis: Effects on heavy metal tolerance and accumulation. Biochimie, 88(11), 1743–1750. https://doi.org/10.1016/j.biochi.2006.04.016 DOI: https://doi.org/10.1016/j.biochi.2006.04.016

Ranger, M., Nkongolo, K. K., Michael, P., & Beckett, P. (2008). Genetic differentiation of jack pine (Pinus banksiana) and red pine (P. resinosa) populations from metal contaminated areas in Northern Ontario (Canada) using ISSR markers. Silvae Genetica, 57(6), 333–340. DOI: https://doi.org/10.1515/sg-2008-0049

Roth, U., Von Roepenack-Lahaye, E., & Clemens, S. (2006). Proteome changes in Arabidopsis thaliana roots upon exposure to Cd²⁺. Journal of Experimental Botany, 57(15), 4003–4013. https://doi.org/10.1093/jxb/erl170 DOI: https://doi.org/10.1093/jxb/erl170

Ruta, L. L., Banu, M. A., Neagoe, A. D., Kissen, R., Bones, A. M., & Farcasanu, I. C. (2018). Accumulation of Ag(I) by Saccharomyces cerevisiae cells expressing plant metallothioneins. Cells, 7(12). https://doi.org/10.3390/cells7120266 DOI: https://doi.org/10.3390/cells7120266

Ruta, L. L., Kissen, R., Nicolau, I., Neagoe, A. D., Petrescu, A. J., Bones, A. M., & Farcasanu, I. C. (2017). Heavy metal accumulation by Saccharomyces cerevisiae cells armed with metal binding hexapeptides targeted to the inner face of the plasma membrane. Applied Microbiology and Biotechnology, 101(14), 5749–5763. https://doi.org/10.1007/s00253-017-8335-0 DOI: https://doi.org/10.1007/s00253-017-8335-0

Salem, Z. B., Laffray, X., Ashoour, A., Ayadi, H., & Aleya, L. (2014). Metal accumulation and distribution in the organs of reeds and cattails in a constructed treatment wetland (Etueffont, France). Ecological Engineering, 64, 1–17. https://doi.org/10.1016/j.ecoleng.2013.12.027 DOI: https://doi.org/10.1016/j.ecoleng.2013.12.027

Salt, D. E., Pickering, I. J., Prince, R. C., Gleba, D., Dushenkov, S., Smith, R. D., & Raskin, I. (1997). Metal accumulation by aquacultured seedlings of Indian mustard. Environmental Science and Technology, 31(6), 1636–1644. https://doi.org/10.1021/es960802n DOI: https://doi.org/10.1021/es960802n

Sapara, K. K., Khedia, J., Agarwal, P., Gangapur, D. R., & Agarwal, P. K. (2019). SbMYB15 transcription factor mitigates cadmium and nickel stress in transgenic tobacco by limiting uptake and modulating antioxidative defence system. Functional Plant Biology, 46(8), 702–714. https://doi.org/10.1071/FP18234 DOI: https://doi.org/10.1071/FP18234

Sauge-Merle, S., Cuiné, S., Carrier, P., Lecomte-Pradines, C., Luu, D.-T., & Peltier, G. (2003). Enhanced toxic metal accumulation in engineered bacterial cells expressing Arabidopsis thaliana phytochelatin synthase. Applied and Environmental Microbiology, 69(1), 490–494. https://doi.org/10.1128/AEM.69.1.490-494.2003 DOI: https://doi.org/10.1128/AEM.69.1.490-494.2003

Taghizadeh, M., Asghari, F., Solgi, M., & Khadivi, A. (2025). Genotypic variations of Tamarix aphylla (L.) H.Karst. population for heavy metal phytoremediation: A case study in Markazi province, Iran. BMC Plant Biology, 25(1). https://doi.org/10.1186/s12870-025-06940-w DOI: https://doi.org/10.1186/s12870-025-06940-w

Tiwari, S., Singh, S. N., & Garg, S. K. (2012). Stimulated phytoextraction of metals from fly ash by microbial interventions. Environmental Technology (United Kingdom), 33(21), 2405–2413. https://doi.org/10.1080/09593330.2012.670269 DOI: https://doi.org/10.1080/09593330.2012.670269

Ullah, R., Bakht, J., Shafi, M., Iqbal, M., Khan, A., & Saeed, M. (2011). Phyto-accumulation of heavy metals by sunflower (Helianthus annuus L.) grown on contaminated soil. African Journal of Biotechnology, 10(75), 17192–17198. https://doi.org/10.5897/AJB11.1832 DOI: https://doi.org/10.5897/AJB11.1832

Unnisa, S. A., Seshabala, P., & Reddy, P. C. S. (2008). Synergistic use of transgenic plant to remediate the soil. Pollution Research, 27(2), 269–272. https://www.scopus.com/inward/record.uri?eid=2-s2.0-49349107128&partnerID=40&md5=77c7f347e3f23b437b253377c912653a

Vaseem, H., Singh, V. K., & Singh, M. P. (2020). An ecofriendly approach to decontaminate toxic metals from coal washery effluent using the mushroom Pleurotus ostreatus. SN Applied Sciences, 2(9). https://doi.org/10.1007/s42452-020-03376-9 DOI: https://doi.org/10.1007/s42452-020-03376-9

Wang, L., Wang, Y., Dai, S., & Wang, B. (2024). Surface display of multiple metal-binding domains in Deinococcus radiodurans alleviates cadmium and lead toxicity in rice. International Journal of Molecular Sciences, 25(23). https://doi.org/10.3390/ijms252312570 DOI: https://doi.org/10.3390/ijms252312570

Wang, Y., Wen, J., Li, S., Li, J., Yu, H., Li, Y., Ren, X., Wang, L., Tang, J., Zhang, X., Liu, Z., & Peng, L. (2024). Upgrading pectin methylation for consistently enhanced biomass enzymatic saccharification and cadmium phytoremediation in rice Ospmes site-mutants. International Journal of Biological Macromolecules, 262. https://doi.org/10.1016/j.ijbiomac.2024.130137 DOI: https://doi.org/10.1016/j.ijbiomac.2024.130137

Wei, Y. Y., Zheng, Q., Liu, Z. P., & Yang, Z. M. (2011). Regulation of tolerance of Chlamydomonas reinhardtii to heavy metal toxicity by heme oxygenase-1 and carbon monoxide. Plant and Cell Physiology, 52(9), 1665–1675. https://doi.org/10.1093/pcp/pcr102 DOI: https://doi.org/10.1093/pcp/pcr102

Wojas, S., Hennig, J., Plaza, S., Geisler, M., Siemianowski, O., Skłodowska, A., Ruszczyńska, A., Bulska, E., & Antosiewicz, D. M. (2009). Ectopic expression of Arabidopsis ABC transporter MRP7 modifies cadmium root-to-shoot transport and accumulation. Environmental Pollution, 157(10), 2781–2789. https://doi.org/10.1016/j.envpol.2009.04.024 DOI: https://doi.org/10.1016/j.envpol.2009.04.024

Zhang, S., Lu, Y., Han, H., Geng, H., Zhang, Q., Zhang, Y., & Zheng, X. (2025). Application of Phragmites australis in bioremediation of acid mine drainage: Enhancing water quality and remodeling aqueous microbial communities. Journal of Hazardous Materials, 498. https://doi.org/10.1016/j.jhazmat.2025.139988 DOI: https://doi.org/10.1016/j.jhazmat.2025.139988

Zhao, Y. N., Wang, M. Q., Li, C., Cao, H. W., Rono, J. K., & Yang, Z. M. (2022). The metallochaperone OsHIPP56 gene is required for cadmium detoxification in rice crops. Environmental and Experimental Botany, 193. https://doi.org/10.1016/j.envexpbot.2021.104680 DOI: https://doi.org/10.1016/j.envexpbot.2021.104680

Zheng, X., Jiang, J., Wang, C., Hua, Y., Huang, H., Xu, Y., Wei, P., Tao, J., Cao, P., Kang, Z., Li, X., Gao, Q., & Chen, Q. (2024). NRAMP6c plays a key role in plant cadmium accumulation and resistance in tobacco (Nicotiana tabacum L.). Ecotoxicology and Environmental Safety, 271. https://doi.org/10.1016/j.ecoenv.2023.115885 DOI: https://doi.org/10.1016/j.ecoenv.2023.115885

Downloads

Published

2026-01-10

How to Cite

Mapping Plant Biotechnology Research for Low Heavy Metal Accumulation and Crop Safety: A Bibliometric–SLR Study Highlighting CRISPR-Cas9. (2026). G-Tech: Jurnal Teknologi Terapan, 10(1), 212-225. https://doi.org/10.70609/g-tech.v10i1.8732