Sains Malaysiana 51(9)(2022): 2803-2816

http://doi.org/10.17576/jsm-2022-5109-06

Comparative Arsenic Tolerance and Accumulation Potential between Wild Tagetes patula and Tagetes minuta

(Toleransi dan Potensi Pengumpulan Arsenik Perbandingan antara Tagetes patula dan Tagetes minuta Liar)

IRUM SHAHZADI^1,*, MOHAMMAD MAROOF SHAH¹, IRRUM SALEEM AKHTAR¹, TARIQ ISMAIL², RAZA AHMAD¹, ISMAT NAWAZ³, MARIA SIDDIQUE⁴, SOFIA BAIG⁵, AYESHA BAIG¹ & UMMARA WAHEED⁶

¹Department of Biotechnology, COMSATS University Islamabad, Abbottabad Campus, 22060, Pakistan

²Department of Pharmacy, COMSATS University Islamabad, Abbottabad Campus, 22060, Pakistan

³Department of Biosciences, COMSATS University Islamabad, 45550, Pakistan

⁴Department of Environmental Sciences, COMSATS University Islamabad, Abbottabad Campus, 22060, Pakistan

⁵Institute of Environmental Sciences and Engineering (IESE), National University of Sciences and Technology, H-12, Islamabad, 44000, Pakistan

⁶Institute of Plant Breeding & Biotechnology, MNS University of Agriculture, Multan, Pakistan

Received: 21 August 2021/Accepted: 2 April 2022

Abstract

Arsenic (As) is a bioactive metalloid that is highly toxic to humans, animals, and plants. Environmental contamination of As especially in groundwater increases due to natural and anthropogenic activities. The present study was performed to evaluate the potential of wild Tagetes species for the phytoremediation of As contaminated soil/water. This comparative research aims to analyze As accumulation and tolerance in two wild species of Tagetes, T. minuta and T. patula. The 20 days old seedlings were grown hydroponically and exposed to the different concentrations of As, 0, 50, 150, and 300 µM As₂O₃ for 1-, 4- and 7- days intervals. Effect of As stress was measured on the rate of seed germination, growth parameters like fresh and dry biomass weight, root/shoot length, chlorophyll contents and As contents in root and shoot in both Tagetes species. Increasing concentration of As restricts the growth activity of T. minuta with toxicity symptoms on leaves such as chlorosis. Accumulation of As in the shoot was significantly (p ≤ 0.01) high (634 µg g^-1 DW) in T. patula as compared to T. minuta (397 µg g^-1 DW) at 300 µM As₂O₃. Both Tagetes species exhibited high variation for As tolerance parameters as well as for As accumulation patterns. Comparatively good tolerance and accumulation of As in T. patula suggests that this species could be used in phytoextraction and re-vegetation in As contaminated sites.

Keywords: Arsenic; phytoremediation; Tagetes minuta; Tagetes patula

Abstrak

Arsenik (As) ialah metaloid bioaktif yang sangat toksik kepada manusia, haiwan dan tumbuhan. Pencemaran persekitaran disebabkan As terutamanya pada air dalam tanah meningkat disebabkan oleh aktiviti semula jadi dan antropogen. Kajian ini dilakukan untuk menilai potensi spesies Tagetes liar sebagai fitoremediasi tanah/air yang tercemar As. Kajian perbandingan ini bertujuan untuk menganalisis pengumpulan dan kerintangan As dalam dua spesies Tagetes liar, T. minuta dan T. patula. Anak pokok berusia 20 hari telah ditanam secara hidroponik dan didedahkan kepada kepekatan As berbeza iaitu 0, 50, 150 dan 300 µM As₂O₃ untuk selang 1-, 4- dan 7 hari. Kesan tekanan As diukur dengan melihat kepada kadar percambahan biji benih, parameter pertumbuhan seperti berat biojisim segar dan kering, panjang akar/pucuk, kandungan klorofil dan kandungan As dalam akar dan pucuk pada kedua-dua spesies Tagetes. Peningkatan kepekatan As menyekat aktiviti pertumbuhan T. minuta dengan gejala ketoksikan seperti klorosis pada daun. Pengumpulan As dalam pucuk T. patula adalah tinggi (634 µg g^-1 DW) dan berbeza secara bererti (p≤0.01) berbanding T. minuta (397 µg g^-1 DW) pada 300 µM As₂O₃. Terdapat variasi yang tinggi bagi parameter berkait kerintangan As begitu juga dengan corak pengumpulan As pada kedua-dua spesies Tagetes. Kerintangan dan pengumpulan As dalam T. patula yang agak baik menunjukkan bahawa spesies ini boleh digunakan dalam fitoekstraksi dan boleh ditanam di lokasi tercemar As.

Kata kunci: Arsenik; fitoremediasi; Tagetes minuta; Tagetes patula

References

Abbas, G., Murtaza, B., Bibi, I., Shahid, M., Niazi, N.K., Khan, M.I., Amjad, M., Hussain, M. & Natasha. 2018. Arsenic uptake, toxicity, detoxification, and speciation in plants: Physiological, biochemical, and molecular aspects. International Journal of Environmental Research and Public Health 15(1): 59.

Abid, R., Mahmood, S., Zahra, S., Ghaffar, S., Malik, M. & Noreen, S. 2021. Jatropha curcas L. and Pongamia pinnata L. exhibited differential growth and bioaccumulation pattern irrigated with wastewater. Sains Malaysiana 50(3): 559-570.

Ahmad, A.M., Gaur, R. & Gupta, M. 2012. Comparative biochemical and RAPD analysis in two varieties of rice (Oryza sativa) under arsenic stress by using various biomarkers. Journal of Hazardous Materials 217-218: 141-148.

Angulo-Bejarano, P.I., Puente-Rivera, J. & Cruz-Ortega, R. 2021. Metal and metalloid toxicity in plants: An overview on molecular aspects. Plants 10(4): 635.

Anjum, S.A., 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.

Antenozio, M.L., Giannelli, G., Marabottini, R., Brunetti, P., Allevato, E., Marzi, D., Capobianco, G., Bonifazi, G., Serranti, S., Visioli, G., Stazi, S.R. & Cardarelli, M. 2021. Phytoextraction efficiency of Pteris vittata grown on a naturally As‑rich soil and characterization of As‑resistant rhizosphere bacteria. Scientific Reports 11: 6794.

Armendariz, A.L., Talano, M.A., Travaglia, C., Reinoso, H., Oller, A.L.W. & Agostini, E. 2016. Arsenic toxicity in soybean seedlings and their attenuation mechanisms. Plant Physiology and Biochemistry 98: 119-127.

Arnon, D.I. 1949. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24(1): 1-15.

Atabaki, N., Shaharuddin, A.A., Ahmad, A.S., Nulit, R. & Abiri, R. 2020. Assessment of water mimosa (Neptunia oleracea Lour.) morphological, physiological, and removal efficiency for phytoremediation of arsenic-polluted water. Plants 9(11): 1500.

Baker, A.J.M. & Brooks, R.R. 1989. Terrestrial higher plants which hyperaccumulate metallic elements - A review of their distribution, ecology and phytochemistry. Biorecovery 1: 811.

Banerjee, A., Sarkar, S., Gorai, S., Kabiraj, A. & Bandopadhyay, R. 2021. High arsenic tolerance in Brevundimonas aurantiaca PFAB1 from an arsenic-rich Indian hot spring. Electronic Journal of Biotechnology 53: 1-7.

Behera, K.K. 2014. Phytoremediation, Transgenic Plants and Microbes. Switzerland: Springer, Cham. pp. 65-85.

Bianconi, D., Pietrini, F., Massacci, A. & Iannelli, M.A. 2013. Uptake of cadmium by Lemna minor, a (hyper?-) accumulator plant involved in phytoremediation applications. E3S Web of Conference 1: 13002.

Chandrakar, V., Naithani, S.C. & Keshavkant, S. 2016. Arsenic-induced metabolic disturbances and their mitigation mechanisms in crop plants: A review. Biologia 71: 367-377.

Chintakovid, W., Visoottiviseth, P., Khokiattiwong, S. & Lauengsuchonkul, S. 2007. Potential of the hybrid marigolds for arsenic phytoremediation and income generation of remediators in Ron Phibun District, Thailand. Chemosphere 70(8): 1532-1537.

Choudhury, M.R., Islam, M.S., Ahmed, Z.U. & Nayar, F. 2016. Phytoremediation of heavy metal contaminated Buriganga riverbed sediment by Indian mustard and marigold plants. Environmental Progress & Sustainable Energy 35(1): 117-124.

Chung, J., Yu, S. & Hong, Y.S. 2014. Environmental source of arsenic exposure. Journal of Preventive Medicine and Public Health 47(5): 253-257.

Coakley, S., Cahill, G., Enright, A.M., Rourke, B.O. & Petti, C. 2019. Cadmium hyperaccumulation and translocation in impatiens glandulifera: From foe to friend? Sustainability 11(8): 5018.

Coelho, L.C., Bastos, A.R.R., Pinho, P.J., Souza, G.A., Carvalho, J.G., Coelho, V.A.T., Oliveira, L.C.A., Domingues, R.R. & Faquin, V. 2017. Marigold (Tagetes erecta): The potential value in the phytoremediation of chromium. Pedosphere 27(3): 559-568.

Danh, L.T., Truong, P., Mammucari, R. & Foster, N.A. 2014. Critical review of the arsenic uptake mechanisms and phytoremediation potential of Pteris vittate. International Journal of Phytoremediation 16(5): 429-453.

Dobslaw, D., Woiski, C., Kiel, M., Kuch, B. & Breuer, J. 2021. Plant uptake, translocation and metabolism of PBDEs in plants of food and feed industry: A review.Reviews in Environmental Science and Biotechnology 20: 75-142.

Dushenko, W.T., Bright, D.A. & Reimer, K.J. 1995. Arsenic bioaccumulation and toxicity in aquatic macrophytes to gold-mine effluent: Relationship with environmental partitioning, metal uptake and nutrients. Aquatic Botany 50: 141-158.

Elisa, C., Alisson, B. & Borges, C. 2020. Use of plants in the remediation of arsenic contaminated waters. Water Environment Research 92(2): 1669-1676.

Hashim, M.A., Mukhopadhyay, S., Sahu, J.N. & Sengupta, B. 2011. Remediation technologies for heavy metal contaminated ground water. Journal of Environmental Management 92(10): 2355-2388.

Hong, H.S., Choi, A.S., Yoon, H. & Cho, K.S. 2011. Screening of Cucumis sativus as a new arsenic-accumulating plant and its arsenic accumulation in hydroponic culture. Environmental Geochemistry and Health 33(Supplementary 1): 143-149.

Jiang, Y., Lei, M., Duan, L. & Philip, L. 2015. Integrating phytoremediation with biomass valorisation and critical element recovery: A UK contaminated land perspective. Biomass and Bioenergy 83: 328-339.

Kumar, S., Dubey, R.S., Tripathi, R.D., Chakrabarty, D. & Trivedi, P.K. 2015. Omics and biotechnology of arsenic stress and detoxification in plants: Current updates and prospective. Environment International 74: 221-230.

Leblanc, M.S., Mckinney, E.C. Meagher, R.B. & Smith, A.P. 2013. Hijacking membrane transporters for arsenic phytoextraction. Journal of Biotechnology 163(1): 1-9.

Li, C.X., Shu-Li, F., Yun, S., Li-Na, J., Yang, L.U. & Xiao-Li, H. 2007. Effects of arsenic on seed germination and physiological activities of wheat seedlings. Journal of Environmental Sciences 19(6): 725-732.

Li, N., Wang, J. & Song, W.Y. 2016. Arsenic uptake and translocation in plants. Plant Cell Physiology 57(1): 4-13.

Li, R., Dong, F., Yang, G., Zhang, W., Zong, M., Nie, X., Zhou, L., Babar, A., Liu, J.,  Ram, K.B., Fan, C. & Zeng Y. 2020. Characterization of arsenic and uranium pollution surrounding a uranium mine in southwestern China and phytoremediation potential. Polish Journal of Environmental Studies 29(1): 173-185.

Li, Y., Sun, Y., Jiang, J. & Liu, J. 2019. Spectroscopic determination of leaf chlorophyll content and color for genetic selection on Sassafras tzumu. Plant Methods 15: 73.

Lin, A., Zhang, X., Zhu, Y.G. & Zhao, F.J. 2008. Arsenate-induced toxicity: Effects on antioxidative enzymes and DNA damage in Vicia faba. Environmental Toxicology and Chemistry 27(2): 413-419.

Lyubenova, L., Pongrac, P., Vogel-Mikus, K., Mezek, G.K., Vavpetic, P., Grlj, N., Regvar, M., Pelicon, P. & Schroder, P. 2013. The fate of arsenic, cadmium and lead in Typha latifolia: A case study on the applicability of micro-PIXE in plant ionomics. Journal of Hazardous Material 15: 371-378.

Madanan, M.T., Shah, I.K., George, K. & Kaushal, R.K. 2021. Application of aztec marigold (Tagetes erecta L.) for phytoremediation of heavy metal polluted lateritic soil. Environmental Chemistry and Ecotoxicology 3: 17-22.

Mandal, P. 2017. An insight of environmental contamination of arsenic on animal health. Emerging Contaminants3(1): 17-22.

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.

Nawa, I., Iqbal, M., Bliek, M. & Schat, H. 2017. Salt and heavy metal tolerance and expression levels of candidate tolerance genes among four extremophile Cochlearia species with contrasting habitat preferences. Science of the Total Environment 585: 731-741.

Pietrini, F., Iori, V., Pietrosanti, L., Zacchini, M. & Massacci, A. 2020. Evaluation of multiple responses associated with arsenic tolerance and accumulation in Pteris vittata L. plants exposed to high As concentrations under hydroponics. Water 12(1): 3127.

R Core Team. 2018. R: A Language and Environment for Statistical Computing. Vienna: Austria.

Reichman, S.M. 2002. The responses of plants to metal toxicity: A review focusing on copper, manganese & zinc. Australian Minerals and Energy Environment Foundation 14: 22-26.

Sahoo, P.K. & Kim, K. 2013. A review of the arsenic concentration in paddy rice from the perspective of geoscience. Geosciences Journal 17: 107-122.

Salim, F., Setiadi, Y., Sopandie, D. & Yani, M. 2020. Adaptation selection of plants for utilization in phytoremediation of soil contaminated by crude oil fadliah. HAYATI Journal of Biosciences 27(1): 45-56.

Sathya, V., Mahimairaja, S., Bharani, A. & Krishnaveni, A. 2020. Influence of soil bioamendments on the availabilty of nickel and phytoextraction capability of Marigold from the contaminated soil. International Journal of Plant & Soil Science 31(5): 1-12.

Sghaier, D.B., Duarte, B., Bankaji, I., Caçador, I. & Sleimi, N. 2015. Growth, chlorophyll fluorescence and mineral nutrition in the halophyte Tamarix gallica cultivated in combined stress conditions: Arsenic and NaCl. Journal of Photochemistry and Photobiology 149: 204-214.

Shahzadi, I., Ahmad, R., Hassan, A. & Shah, M.M. 2010. Optimization of DNA extraction from seeds and fresh leaf tissues of wild marigold (Tagetes minuta) for polymerase chain reaction analysis. Genetics and Molecular Research 9(1): 386-393.

Singh, H.P., Batish, D.R., Kohli, R.K. & Arora, K. 2007. Arsenic-induced root growth inhibition in mung bean (Phaseolus aureus Roxb.) is due to oxidative stress resulting from enhanced lipid peroxidation. Plant Growth Regulator 53: 65-73.

Singh, R., Singh, S., Parihar, P., Singh, V.P. & Prasad, S.M. 2015. Arsenic contamination, consequences and remediation techniques: A review. Ecotoxicology and Environmental Safety 112: 247-270.

Souri, Z., Karimi, N. & Sandalio, L.M. 2017. Arsenic hyperaccumulation strategies: An overview. Frontiers in Cell and Developmental Biology 5: 67.

Stoeva, N. & Bineva, T.  2003. Oxidative changes and photosynthesis in oat plants grown in As contaminated soil. Bulgarian Journal of Plant Physiology 29: 87.

Tripathi, R.D., Srivastava, S., Mishra, S., Singh, N., Tuli, R., Gupta, D.K. & Maathuis, F.J.M. 2007. Arsenic hazards: Strategies for tolerance and remediation by plants. Trends in Biotechnology 25: 158.

Wei, J.L., Lai, H.Y. & Chen, Z.S. 2012. Chelator effects on bioconcentration and translocation of cadmium by hyperaccumulators, Tagetes patula and Impatiens walleriana. Ecotoxicology and Environmental Safety 84(4): 173-178.

Wellburn, A.R. 1994. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144(3): 307-313.

Wiszniewska, A. 2021. Priming Strategies for benefiting plant performance under toxic trace metal exposure. Plants 10(4): 623.

Yanitch, A., Brereton, N.J., Gonzalez, E., Labrecque, M., Joly, S. & Pitre, F.E. 2017. Transcriptomic response of purple willow (Salix purpurea) to arsenic stress. Frontiers in Plant Sciences 8: 1115.

Zvobgo, G., Sehar, S., Lwalaba, J., Mapodzeke, J.M. & Zhang, G.P. 2018. The tolerance index and translocation factor were used to identify the barley genotypes with high arsenic stress tolerance. Communications in Soil Science and Plant Analysis 49(1): 50-62.

^*Corresponding author; email: irumayaz@cuiatd.edu.pk