Sains Malaysiana 53(4)(2024): 769-780

http://doi.org/10.17576/jsm-2024-5304-04

Physiological Responses and Tolerance of Three Acacia Species to Cadmium Stress during Germination and Early Seedling Growth

(Tindak Balas Fisiologi dan Toleransi Tiga Spesies Akasia terhadap Tekanan Kadmium semasa Percambahan dan Pertumbuhan Anak Benih Awal)

LA ODE MUHAMMAD MUCHDAR DAVIS^1,*, NURHASANAH², TITI JUHAETI³ & INDRA GUNAWAN⁴

¹Research Center for Genetic Engineering, National Research and Innovation Agency (BRIN), Jl. Raya Jakarta-Bogor Km. 46, Cibinong 16911, West Java, Indonesia

²Biology Education Study Program, Faculty of Education and Teacher Training, Universitas Terbuka, Jl. Cabe Raya Pondok Cabe, Pamulang, Tangerang Selatan, 15418, Indonesia

³Research Center for Plant Conservation, Botanic Garden, and Forestry, National Research and Innovation Agency (BRIN), Jl. Raya Jakarta-Bogor Km. 46, Cibinong 16911, West Java, Indonesia

⁴Research Center for Horticulture and Plantation, National Research and Innovation Agency (BRIN), Jl. Raya Jakarta-Bogor Km. 46, Cibinong 16911, West Java, Indonesia

Diserahkan: 30 Jun 2023/Diterima: 1 Mac 2024

Abstract

Soil contamination with cadmium (Cd) is a serious threat to ecosystems. Phytoremediation is a cost-effective green technology that can be used to clean up Cd pollution, and Acacia species are potential phytoremediation agents due to their fast growth, significant biomass, and tolerance to environmental stresses. Most studies of Cd stress on Acacia focused on later vegetative stages and the tolerances during germination and early seedling are elusive. This study aimed to assess the tolerance of Acacia mangium, Acacia crassicarpa, and Acacia auriculiformis to Cd stress during germination and early seedling growth. In response to 250 μM Cd treatment, A. auriculiformis germination was slightly increased compared to the control. Leaf organ formation remained largely unaffected by Cd stress, except for the true leaf number in A. mangium, which was significantly higher in response to 125 µM Cd than those to 250 µM Cd treatment and control at 8 and 10 weeks after treatment. The onset of phyllode development transition from true leaf was significantly delayed in A. mangium compared with the other two Acacia, irrespective of the presence of Cd. There were no significant differences in leaf gas exchange parameters (photosynthesis, stomatal conductance, and transpiration), leaf-level water use efficiency, or leaf chlorophyll content between Cd-treated and control plants, suggesting that the three Acacia species are tolerant to Cd at both germination and early seedling phases. Cd accumulation during the experiment was very low in A. mangium seedlings (2.8 mg kg^-1 upon 250 µM Cd) and insignificant in A. crassicarpa and A. auriculiformis, indicating non-hyperaccumulation or Cd exclusion at the seedling stage.

Keywords: Acacia auriculiformis; Acacia crassicarpa; Acacia mangium; cadmium; phytoremediation

Abstrak

Pencemaran tanah oleh Cadmium (Cd) merupakan ancaman yang serius bagi ekosistem. Fitoremediasi adalah teknologi hijau yang menjimatkan kos yang dapat digunakan untuk membersihkan pencermaran Cd dan spesies Akasia merupakan agen fitoremediasi yang berpotensi kerana pertumbuhan yang pantas, biojisim yang ketara dan toleransinya terhadap alam sekitar. Kebanyakan kajian tekanan Cd pada Akasia tertumpu pada peringkat vegetatif lanjut sedangkan toleransi semasa percambahan dan fasa anak benih masih belum difahami. Kajian ini bertujuan untuk menilai toleransi Acacia mangium, Acacia crassicarpa dan Acacia auriculiformis terhadap tekanan Cd semasa percambahan dan pertumbuhan awal anak benih. Sebagai gerak balas terhadap rawatan 250 μM Cd, percambahan A. auriculiformismeningkat sedikit apabila dibandingkan dengan kawalan. Pembentukan organ daun sebahagian besarnya tidak dipengaruhi oleh tekanan Cd, kecuali bilangan daun sebenar pada A. mangium, yang lebih tinggi pada rawatan 125 µM Cd berbanding rawatan 250 µM Cd dan kawalan, pada 8 dan 10 minggu selepas rawatan. Permulaan peralihan perkembangan filod daripada daun sebenar telah terlewat dengan ketara pada A. mangium berbanding dua spesies Akasia yang lain, tanpa mengira kehadiran Cd. Tiada perbezaan yang ketara dalam parameter pertukaran gas daun (fotosintesis, kekonduksian stomata, dan transpirasi), kecekapan penggunaan air daun atau kandungan klorofil daun antara tumbuhan yang dirawat dan kawalan, menunjukkan bahawa ketiga-tiga spesies Akasia tersebut adalah toleran terhadap Cd pada kedua-dua fasa percambahan dan awal anak benih. Pengumpulan Cd semasa uji kaji adalah sangat rendah dalam anak benih A. mangium (2.8 mg kg^-1 pada 250 µM Cd) dan tidak ketara dalam A. crassicarpa dan A. auriculiformis, menunjukkan bukan hiper-pengumpulan atau pengecualian Cd pada peringkat anak benih.

Kata kunci: Acacia auriculiformis; Acacia crassicarpa; Acacia mangium; fitoremediasi; cadmium

RUJUKAN

Ahmad, I., Akhtar, M.J., Zahir, Z.A. & Jamil, A. 2012. Effect of cadmium on seed germination and seedling growth of four wheat (Triticum aestivum L.) cultivars. Pakistan Journal of Botany 44(5): 1569-1574.

Ahsan, N., Lee, S-H., Lee, D-G., Lee, H., Lee, S.W., Bahk, J.D. & Lee, B-H. 2007. Physiological and protein profiles alternation of germinating rice seedlings exposed to acute cadmium toxicity. Comptes Rendus Biologies 330(10): 735-746.

Ang, L.H., Tang, L.K., Ho, W.M., Hui, T.F. & Theseira, G.W. 2010. Phytoremediation of Cd and Pb by four tropical timber species grown on an ex-tin mine in Peninsular Malaysia. International Journal of Environmental and Ecological Engineering 4(2): 70-74.

ATSDR. 2022. ATSDR’s Substance Priority List. https://www.atsdr.cdc.gov/spl/index.html#2022spl Accessed 4 November 2022

Bae, J., Benoit, D.L. & Watson, A.K. 2016. Effect of heavy metals on seed germination and seedling growth of common ragweed and roadside ground cover legumes. Environmental Pollution 213: 112-118.

Baruah, N., Mondal, S.C., Farooq, M. & Gogoi, N. 2019. Influence of heavy metals on seed germination and seedling growth of wheat, pea, and tomato. Water, Air, and Soil Pollution 230: 273.

Bautista, O.V., Fischer, G. & Cárdenas, J.F. 2013. Cadmium and chromium effects on seed germination and root elongation in lettuce, spinach and Swiss chard. Agronomía Colombiana 31(1): 48-57.

Buendía-González, L., Orozco-Villafuerte, J., Cruz-Sosa, F., Barrera-Díaz, C.E. & Vernon-Carter, E.J. 2010. Prosopis laevigata a potential chromium (VI) and cadmium (II) hyperaccumulator desert plant. Bioresource Technology 101(15): 5862-5867.

Cheng, W., Zhang, G., Yao, H. & Zhang, H. 2008. Genotypic difference of germination and early seedling growth in response to Cd stress and its relation to Cd accumulation. Journal of Plant Nutrition 31(4): 702-715.

Ekmekçi, Y., Tanyolaç, D. & Ayhan, B. 2008. Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. Journal of Plant Physiology 165(6): 600-611.

Galiana, A., Chaumont, J., Diem, H.G. & Dommergues, Y.R. 1990. Nitrogen-fixing potential of Acacia mangium and Acacia auriculiformis seedlings inoculated with Bradyrhizobium and Rhizobium spp. Biology and Fertility of Soils 9(3): 261-267.

Ghassali, F., Salkini, A.K., Petersen, S.L., Niane, A.A. & Louhaichi, M. 2012. Germination dynamics of Acacia species under different seed treatments. Range Management and Agroforestry 33(1): 37-42.

Griffin, A.R., Midgley, S.J., Bush, D., Cunningham, P.J. & Rinaudo, A.T. 2011. Global uses of Australian acacias - Recent trends and future prospects. Diversity and Distributions 17(5): 837-847.

Guilherme, M. de S., de Oliveira, H. & da Silva, E. 2015. Cadmium toxicity on seed germination and seedling growth of wheat Triticum aestivum. Acta Scientiarum 4: 499-504.

Haider, F.U., Liqun, C., Coulter, J.A., Cheema, S.A., Wu, J., Zhang, R., Wenjun, M. & Farooq, M. 2021. Cadmium toxicity in plants: Impacts and remediation strategies. Ecotoxicology and Environmental Safety 211: 111887.

Hatfield, J.L. & Dold, C. 2019. Water-use efficiency: Advances and challenges in a changing climate. Frontiers in Plant Science 10: 103.

Hossain, M.L., Huda, S.M.S. & Hossain, M.K. 2009. Effects of industrial and residential sludge on seed germination and growth parameters of Acacia auriculiformis seedlings. Journal of Forestry Research 20(4): 331-336.

Huybrechts, M., Cuypers, A., Deckers, J., Iven, V., Vandionant, S., Jozefczak, M. & Hendrix, S. 2019. Cadmium and plant development: An agony from seed to seed. International Journal of Molecular Sciences 20(16): 3971. doi: 10.3390/ijms20163971

Jaishankar, M., Tseten, T., Anbalagan, N., Mathew, B.B. & Beeregowda, K.N. 2014. Toxicity, mechanism and health effects of some heavy metals. Interdisciplinary Toxicology 7(2): 60-72. doi: 10.2478/intox-2014-0009

Karalija, E., Selović, A., Dahija, S., Demir, A., Samardžić, J., Vrobel, O., Ćavar Zeljković, S. & Parić, A. 2021. Use of seed priming to improve Cd accumulation and tolerance in Silene sendtneri, novel Cd hyper-accumulator. Ecotoxicology and Environmental Safety 210: 111882. doi: 10.1016/j.ecoenv.2020.111882

Khalid, S., Shahid, M., Niazi, N.K., Murtaza, B., Bibi, I. & Dumat, C. 2017. A comparison of technologies for remediation of heavy metal contaminated soils. Journal of Geochemical Exploration 182: 247-268.

Kirkham, M.B. 2006. Cadmium in plants on polluted soils: Effects of soil factors, hyperaccumulation, and amendments. Geoderma 137(1-2): 19-32.

Koutika, L.S. & Richardson, D.M. 2019. Acacia mangium Willd: benefits and threats associated with its increasing use around the world. Forest Ecosystems 6: 2.

Krämer, U. 2010. Metal hyperaccumulation in plants. Annual Review of Plant Biology 61: 517-534.

Krantev, A., Yordanova, R., Janda, T., Szalai, G. & Popova, L. 2008. Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. Journal of Plant Physiology 165(9): 920-931.

Kubier, A., Wilkin, R.T. & Pichler, T. 2019. Cadmium in soils and groundwater: A review. Applied Geochemistry: Journal of the International Association of Geochemistry and Cosmochemistry 108: 104388. doi: 10.1016/J.APGEOCHEM.2019.104388

Kumari, B.M.R. & Nagaraja, N. 2023. Studies on phytoremediation of chromated copper arsenate (CCA) using Acacia plant species (Fabaceae). International Journal of Phytoremediation 25(12): 1669-1675.

Küpper, H., Parameswaran, A., Leitenmaier, B., Trtílek, M. & Šetlík, I. 2007. Cadmium-induced inhibition of photosynthesis and long-term acclimation to cadmium stress in the hyperaccumulator Thlaspi caerulescens. New Phytologist 175(4): 655-674.

Lefevre, I., Marchal, G., Corréal, E., Zanuzzi, A. & Lutts, S. 2009. Variation in response to heavy metals during vegetative growth in Dorycnium pentaphyllum Scop. Plant Growth Regulation 59: 1-11.

Li, Q., Lu, Y., Shi, Y., Wang, T., Ni, K., Xu, L., Liu, S., Wang, L., Xiong, Q. & Giesy, J.P. 2013. Combined effects of cadmium and fluoranthene on germination, growth and photosynthesis of soybean seedlings. Journal of Environmental Sciences 25(9): 1936-1946.

Lin, Y.F. & Aarts, M.G.M. 2012. The molecular mechanism of zinc and cadmium stress response in plants. Cellular and Molecular Life Sciences 69(19): 3187-3206.

Majid, N.M., Islam, M.M. & Mathew, L. 2012. Heavy metal uptake and translocation by mangium (Acacia mangium) from sewage sludge contaminated soil. Australian Journal of Crop Science 6(8): 1228-1235.

McGrath, S.P. & Zhao, F.J. 2003. Phytoextraction of metals and metalloids from contaminated soils. Current Opinion in Biotechnology 14(3): 277-282.

Merlot, S., de la Torre, V.S.G. & Hanikenne, M. 2021. Physiology and molecular biology of trace element hyperaccumulation. In Agromining: Farming for Metals, edited by van der Ent, A., Baker, A.J., Echevarria, G., Simonnot, M. & Morel, J.L. Springer: Cham. pp. 155-181.

Mok, H.F., Majumder, R., Laidlaw, W.S., Gregory, D., Baker, A.J.M. & Arndt, S.K. 2012. Native Australian species are effective in extracting multiple heavy metals from biosolids. International Journal of Phytoremediation 15(7): 615-632.

Munzuroglu, O. & Zengin, F.K. 2006. Effect of cadmium on germination, coleoptile and root growth of barley seeds in the presence of gibberellic acid and kinetin. Journal of Environmental Biology 27(4): 671-677.

Muradoglu, F., Gundogdu, M., Ercisli, S., Encu, T., Balta, F., Ze Jaafar, H. & Zia-Ul-Haq, M. 2015. Cadmium toxicity affects chlorophyll a and b content, antioxidant enzyme activities and mineral nutrient accumulation in strawberry. Biological Research 48: 11. doi: 10.1186/S40659-015-0001-3

Ng, C.C., Boyce, A.N., Rahman, M.M., Abas, M.R. & Mahmood, N.Z. 2018. Phyto-evaluation of Cd-Pb using tropical plants in soil-leachate conditions. Air, Soil and Water Research 2018: 11.

Nirola, R., Megharaj, M., Palanisami, T., Aryal, R., Venkateswarlu, K. & Naidu, R. 2015. Evaluation of metal uptake factors of native trees colonizing an abandoned copper mine–a quest for phytostabilization. Journal of Sustainable Mining 14(3): 115-123.

Peralta, J.R., Gardea-Torresdey, J.L., Tiemann, K.J., Gomez, E., Arteaga, S., Rascon, E. & Parsons, J.G. 2001. Uptake and effects of five heavy metals on seed germination and plant growth in alfalfa (Medicago sativa L.). Bulletin of Environmental Contamination and Toxicology 66(6): 727-734.

Pilon-Smits, E. 2005. Phytoremediation. Annual Review of Plant Biology 56(1): 15-39.

El Rasafi, T., Nouri, M., Bouda, S. & Haddioui, A. 2016. The effect of Cd, Zn and Fe on seed germination and early seedling growth of wheat and bean. Ekológia (Bratislava) 35(3): 213-223.

Rascio, N. & Navari-Izzo, F. 2011. Heavy metal hyperaccumulating plants: How and why do they do it? And what makes them so interesting? Plant Science 180(2): 169-181.

Ray, P.D., Huang, B-W. & Tsuji, Y. 2012. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cellular signalling 24(5): 981-990.

Riveiro, S.F., Cruz, Ó., Casal, M. & Reyes, O. 2020. Fire and seed maturity drive the viability, dormancy, and germination of two invasive species: Acacia longifolia (Andrews) Willd. and Acacia mearnsii De Wild. Annals of Forest Science 77(2): 60. doi: 10.1007/s13595-020-00965-x

Sari, E., Giyanto & Sudadi, U. 2016. Acacia auriculiformis and Eragrostis chariis: Potential vegetations from tin-mined lands in Bangka Island as Pb and Sn phytoremediator. Jurnal Ilmu Tanah dan Lingkungan 18(1): 1-7.

Shabir, R., Abbas, G., Saqib, M., Shahid, M., Shah, G.M., Akram, M., Niazi, N.K., Naeem, M.A., Hussain, M. & Ashraf, F. 2018. Cadmium tolerance and phytoremediation potential of acacia (Acacia nilotica L.) under salinity stress. International Journal of Phytoremediation 20(7): 739-746.

Suman, J., Uhlik, O., Viktorova, J. & Macek, T. 2018. Phytoextraction of heavy metals: A promising tool for clean-up of polluted environment? Frontiers in Plant Science 9: 1476. doi: 10.3389/fpls.2018.01476

Taeprayoon, P., Homyog, K. & Meeinkuirt, W. 2022. Organic amendment additions to cadmium-contaminated soils for phytostabilization of three bioenergy crops. Scientific Reports 12: 13070. doi: 10.1038/S41598-022-17385-8

Titov, A.F., Talanova, V.V. & Boeva, N.P. 1996. Growth responses of barley and wheat seedlings to lead and cadmium. Biologia Plantarum 38(3): 431-436.

Ulusu, Y., Öztürk, L. & Elmastaş, M. 2017. Antioxidant capacity and cadmium accumulation in parsley seedlings exposed to cadmium stress. Russian Journal of Plant Physiology 64(6): 883-888.

Verbruggen, N., Hermans, C. & Schat, H. 2009. Molecular mechanisms of metal hyperaccumulation in plants. New Phytologist 181(4): 759-776.

Zhang, G., Yu, Z., Zhang, L., Yao, B., Luo, X., Xiao, M. & Wen, D. 2022. Physiological and proteomic analyses reveal the effects of exogenous nitrogen in diminishing Cd detoxification in Acacia auriculiformis. Ecotoxicology and Environmental Safety 229: 113057. doi: 10.1016/J.ECOENV.2021.113057

*Pengarang untuk surat-menyurat; email: laod004@brin.go.id