Date Log
Copyright (c) 2022 Jurnal Ilmiah Perikanan dan Kelautan
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
1. Copyright of the article is transferred to the journal, by the knowledge of the author, whilst the moral right of the publication belongs to the author.
2. The legal formal aspect of journal publication accessibility refers to Creative Commons Atribusi-Non Commercial-Share alike (CC BY-NC-SA), (https://creativecommons.org/licenses/by-nc-sa/4.0/)
3. The articles published in the journal are open access and can be used for non-commercial purposes. Other than the aims mentioned above, the editorial board is not responsible for copyright violation
The manuscript authentic and copyright statement submission can be downloaded ON THIS FORM.
Metallothionein (MT) Expression and SEM-EDX Mapping on Cymodocea serrulata Seagrass
Corresponding Author(s) : Dwi Rosalina
Jurnal Ilmiah Perikanan dan Kelautan, Vol. 14 No. 2 (2022): JURNAL ILMIAH PERIKANAN DAN KELAUTAN
Abstract
Highlight Research
1. Metallothionein is a protein found in seagrass and functions to bind to heavy metals so as not to damage the seagrass body tissue
Abstract
Lead is a very dangerous heavy metal for organisms because it is carcinogenic, can cause mutations, takes a long time to decompose and has unchanging toxicity. This study on the seagrass Cymodocea serrulata aimed to determine the metallothionein expression quantitatively using the Elisa (Enzyme-Linked Immunosorbent Assay) method and describe the surface structure of C. serrulata roots, rhizomes, and leaves that were exposed to lead using SEM and EDX Mapping methods. The results showed that metallothionein was abundant in C. serrulata tissues (leaves>roots>rhizomes) in both South Bangka and Ketawai Island. SEM showed changes in the morphology and cell size of C. serrulata exposed to lead. EDX and Mapping showed the substance elements found in seagrass tissue. Pb was detected in C. serrulata roots (0.22%) and leaves (0.6%) in South Bangka. This indicates that the seagrass plants are able to absorb heavy metals into their body tissues.
Keywords
Download Citation
Endnote/Zotero/Mendeley (RIS)BibTeX
- Arisandy, K. R., Herawati, E. Y., & Suprayitno, E. (2012). Akumulasi logam berat timbal (Pb) dan gambaran histologi pada jaringan Avicennia marina (forsk.) Vierh di Perairan Pantai Jawa Timur. Jurnal Penelitian Perikanan, 1(1):15-25.
- Baer, K. N., & Benson, W. H. (1987). Influence of chemical and environmental stressors on acute cadmium toxicity. Journal of Toxicology and Environmental Health, 22(1):35-44.
- Baruah, S., Hazarika, K. K., & Sarma, K. P. (2012). Uptake and localization of lead in Eichhornia crassipes grown within a hydroponic system. Advances in Applied Science Research, 3(1):51-59.
- Bayne, B. L., Brown, D. A., Burns, K., Dixon, D. R., Ivanovici, A., Livingstone, D. R., Lowe, D. M., Moore, M. N., Stebbing, A. R. D., & Widdows, J. (1985). The effects of stress and pollution on marine animals. New York: Praeger Scientific.
- Bebianno, M. J., Nott, J. A., & Langston, W. J. (1993). Cadmium metabolism in the clam Rudipes decussata: The role of metallothioneins. Aquatic Toxicology, 27(3-4):315-334.
- Bhalerao, R., Keskitalo, J., Sterky, F., Erlandsson, R., Björkbacka, H., Birve, S. J., Karlsson, J., Gardeström, P., Gustafsson, P., Lundeberg, J., & Jansson, S. (2003). Gene expression in autumn leaves. Plant Physiology, 131(2):430-442.
- Bidayani, E., Rosalina, D., & Utami, E. (2017). Content of heavy metal lead (Pb) in the seagrass Cymodocea serrulata of tin mining South Bangka Regency. Maspari Journal, 9(2):169-176.
- Binz, P. A., & Kägi, J. H. R. (1999). Metallothionein: molecular evolution and classification. In C. Klaassen (Ed.), Metallothionein IV. (pp. 7-8). Basel: Birkhauser-Verlag.
- Butt, A., Mousley, C., Morris, K., Beynon, J., Can, C., Holub, E., Greenberg, J. T., & Buchanan-Wolaston, V. (1998). Differential expression of a senescence enhanced metallothionein gene in Arabidopsis in response to isolates of Peronospora parasitica and Pseudomonas syringiae. The Plant Journal, 16(2):209-221.
- Carpenè, E., Andreani, G., & Isani, G. (2007). Metallothionein Functions and Structural Characteristics. Journal of Trace Elements in Medicine and Biology, 21(1):35-39.
- Choi, D., Kim, H. M., Yun, H. K., Park, J. A., Kim, W. T., & Bok, S. H. (1996). Molecular cloning of a metallothionein-like gene from Nicotiana glutinosa L. and its induction by wounding and tobacco mosaic virus infection. Plant Physiology, 112(1):353-359.
- Cobbett, C., & Goldsbrough, P. (2002). Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annual Review of Plant Biology, 53:159-182.
- Engel, D. W., & Brouwer, M. (1984). Trace metal-binding proteins in marine molluscs and crustaceans. Marine Environmental Research, 13(3):177-194.
- Evans, I. M., Gatehouse, L. N., Gatehouse, J. A., Robinson, N. J., & Croy, R. R. (1990). A gene from pea (Pisum sativum L.) with homology to metallothionein genes. FEBS Letters, 262(1):29-32.
- Frankenne, F., Noí«l-Lambot, F., & Disteche, A. (1980). Isolation and characterization of metallothioneins from cadmium-loaded mussel Mytilus edulis. Comparative Biochemistry and Physiology Part C: Comparative Pharmacology, 66(2):179-182.
- Ghelich, S., & Zarinkamar, F. (2013). SEM studies of leaf surface structure changes due to lead toxicity in Hypericum perforatum L. Global Journal of Biodiversity Science and Management, 3(2):256-263.
- Gomes, M. P., Marques, T. C. L. L. de S. e M., Nogueira, M. de O. G., de Castro, E. M., & Soares, A. M. (2011). Ecophysiological and anatomical changes due to uptake and accumulation of heavy metal in Brachiaria decumbens. Scientia Agricola, 68(5):566-573.
- Guo, W. J., Bundithya, W., & Goldsbrough, P. B. (2003). Characterization of the Arabidopsis metallothionein gene family: tissue-specific expression and induction during senescence and in response to copper. New Phytologist, 159(2):369-381.
- Hall, J. L. (2002). Cellular mechanisms for heavy metal detoxification and tolerance. Journal of Experimental Botany, 53(366):1-11.
- Hertika, A. M. S., Kusriani, K., Indrayani, E., Nurdiani, R., & Putra, R. B. D. S. (2018). Relationship between levels of the heavy metals lead, cadmium and mercury, and metallothionein in the gills and stomach of Crassostrea iredalei and Crassostrea glomerata. F1000 Research, 7:1239.
- Huang, G. Y., & Wang, Y. S. (2009). Expression analysis of type 2 metallothionein gene in mangrove species (Bruguiera gymnorrhiza) under heavy metal stress. Chemosphere, 77(7):1026-1029.
- Huang, G. Y., & Wang, Y. S. (2010). Expression and characterization analysis of type 2 metallothionein from grey mangrove species (Avicennia marina) in response to metal stress. Aquatic Toxicology, 99(1):86-92.
- Inoue, N., Nanbu, R., Hasegawa, N., Higano, J., Kuwahara, H., & Sekiguchi, H. (2012). SEM observations on larval shell morphology of Manila clam Ruditapes philippinarum and their utility. Fisheries Science, 78(6):1237-1243.
- Kägi, J. H. R. (1991). Overview of metallothionein. Methods in Enzymology, 205:613-626.
- Kawashima, I., Inokuchi, Y., Chino, M., Kimura, M., & Shimizu, N. (1991). Isolation of a gene for a metallothionein-like protein from soybean. Plant & Cell Physiology, 32(6):913-916.
- Lafabrie, C., Pergent-Martini, C., & Pergent, G. (2008). Metal contamination of Posidonia oceanica meadows along the Corsican coastline (Mediterranean). Environmental Pollution, 151(1):262-268.
- Lane, B., Kajioka, R., & Kennedy, T. (1987). The wheat-germ ec protein is a Zinc-containing metallothionein. Biochemistry and Cell Biology, 65(11):1001-1005.
- Langston, W. J., & Zhou, M. (1986). Evaluation of the significance of metal binding proteins in The Gastropod Littorina littorea. Marine Biology, 92:505-515.
- Laplaze, L., Gherbi, H., Duhoux, E., Pawlowski, K., Auguy, F., Guermache, F., Franche, C., & Bogusz, D. (2002). Symbiotic and non-symbiotic expression of CgMT1, a metallothionein-like gene from the actinorhizal tree Casuarina glauca. Plant Molecular Biology, 49:81-92.
- Lee, J., Shim, D., Song, W. Y., Hwang, I., & Lee, Y. (2004). Arabidopsis metallothioneins 2a and 3 enhance resistance to cadmium when expressed in Vicia faba guard cells. Plant Molecular Biology, 54:805-815.
- Leszczyszyn O. I., Imam, H. T., & Blindauer, C. A. (2013). Diversity and distribution of plant metallothioneins: A review of structure, properties and functions. Metallomics, 5(9):1146-1169.
- Lima, L. K. S., Silva, J. F. L., Da Silva, M. G. C., & Vieira, M. G. A. (2014). Lead biosorption by Salvinia natans biomass: equilibrium study. A Journal of the Italian Association of Chemical Engineering, 38:97-102.
- Linde, A. R., & Garcia-Vazquez, E. (2006). A simple assay to quantify metallothionein helps to learn about bioindicator and environment health. Biochemistry and Molecular Biology Education, 34(5):360-363.
- Liu, P., Goh, C. J., Loh, C. S., Pua, E. C. (2002). Differential expression and characterization of three metallothionein-like genes in cavendish banana (Musa acuminata). Plant Physiology, 114(2):241-250.
- Malar, S., Vikram, S. S., & Favas, P. J. C., & Perumal, V. (2014). Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhornia crassipes (Mart.)]. Botanical Studies, 55(54):1-11.
- Miranda J. R. D., Thomas, M. A., Thurman, D. A., & Tomsett, A. B. (1990). Metallothionein genes from the flowering plant Mimulus guttatus. FEBS Letters, 260(2):277-280.
- Murphy, A., Zhou, J., Goldsbrough, P. B., Taiz, L. (1997) Purification and immunological identification of metallothioneins 1 and 2 from Arabidopsis thaliana. Plant Physiology, 113(4):1293-1301.
- Noí«l-Lambot, F., Gerday, Ch., & Disteche, A. (1978). Distribution of Cd, Zn and Cu in liver and gills of the eel Anguilla anguilla with special reference to metallothioneins. Comparative Biochemistry and Physiology Part C: Comparative Pharmacology, 61(1):177-187.
- Ozyigit, I., & Akinci, S. (2009). Effects of some stress factors (aluminum, cadmium and drought) on stomata of Roman Nettle (Urtica pilulifera L.). Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 37(1):108-115.
- Pearce, L. L., Gandley, R. E., Han, W., Wasserloos, K., Stitt, M., Kanai, A. J., McLaughlin, M. K., Pitt, B. R. & Levitan, E. S. (2000). Role of metallothionein in nitric oxide signaling as revealed by a new green fluorescent fusion protein. Proceedings of the National Academy of Sciences, 97(1):477-482.
- Probst, G. S., Bousquet, W. F., & Miya, T. S. (1977). Correlation of hepatic metallothionein concentrations with acute cadmium toxicity in the mouse. Toxicology and Applied Pharmacology, 39(1):61-69.
- Rai, A. K., Kulshreshtha, K., Srivastava, P. K., & Mohanty, C. S. (2010). Leaf surface structure alterations due to particulate pollution in some common plants. The Environmentalist, 30:18-23.
- Ramamurthy, N., & Kannan, S. (2009). SEM-EDS analysis of soil and plant (Calotropis Gigantea Linn) collected from an industrial village, Cuddalore Dt, Tamil Nadu, India. Romanian Journal of Biophysics, 19(3): 219-226.
- Rand, G. M., & Petrocelli, S. R. (1985). Fundamentals of aquatic toxicology. New York: Kemisphere Publishing Corporation.
- Rafia, A., Saba, H., & Shabana, A. (2006). Phytotoxicity of Pb: I. Effect of Pb on germination, growth, morphology and histomorphology of Phaseolus mungo and Lens culinaris. Pakistan Journal of Biological Sciences, 9(5): 979-984.
- Robinson, N. J., Evans, I. M., Mulcrone, J., Bryden, J., & Tommey, A. M. (1992). Genes with similarity to metallothionein gees and copper, zink ligands in Pisum sativum L. Plant and Soil, 141:291-298.
- Rosalina, D., Herawati, E. Y., Risjani, Y., & Musa, M. (2018a). Lamun diversity in regency of South Bangka Province Bangka Belitung Islands. EnviroScienteae, 14(1):21-28.
- Rosalina, D., Herawati, E. Y., Musa, M., & Risjani Y. (2018b). Lead (Pb) adsorption in roots, rhizomes, and leaves of seagrass Cymodocea serrulata. Fresenius Environment Bulletin, 27(12A):9156-9166.
- Rosalina, D., Herawati, E. Y., Musa, M., Sofarini, D., Amin, M., & Risjani, Y. (2019a). Lead accumulation and its histological impact on Cymodocea serrulata Seagrass in the laboratory. Sains Malaysiana, 48(4):813-822.
- Rosalina, D., Herawati, E. Y., Musa, M., Sofarini, D., & Risjani, Y. (2019b). Short communication: Anatomical changes in the roots, rhizomes and leaves of seagrass (Cymodocea serrulata) in responses to lead. Biodiversitas Journal of Biological Diversity, 20(9):2583-2588.
- Rumahlatu, D., Corebima, A. B., Amin, M., & Rachman, F. (2012). The effect of Cadmium on metallothionein protein expression of Diadema setosum (Echinoidea; Echinodermata). Jurnal Penelitian Perikanan, 1:26-35.
- Shi, G., & Cai, Q. (2009). Leaf plasticity in peanut (Arachis hypogaea L.) in response to heavy metal stress. Environmental and Experimental Botany, 67(1):112-117.
- Singh, S., & Sinha, S. (2004). Scanning electron microscopic studies and growth response of the plants of Helianthus annuus L. grown on tannery sludge amended soil. Environment International, 30(3):389-395.
- Sridhar, B. B. M., Diehl, S. V., Han, F. X., Monts, D. L., & Su, Y. (2005). Anatomical changes due to uptake and accumulation of Zn and Cd in Indian mustard (Brassica juncea). Environmental and Experimental Botany, 54(2):131-141.
- Sugiura, H., Kawasaki, Y., Suzuki, T., & Maegawa, M. (2009). The structural and histochemical analyses and chemical characters of the cuticle and epidermal walls of cotyledon in ungerminated seeds of Zostera marina L. Fisheries Science, 75(369):369-377.
- Usha, B., Prashanth, S. R., & Parida, A. (2007). Differential expression of two metallothionein encoding genes during heavy metal stress in the mangrove species, Avicennia marina (Forsk.) Vierh. Current Science, 93(9):1215-1219.
- Weryszko-Chmielewska, E., & Chwil, M. (2005). Lead-induced histological and ultrastructural changes in the leaves of soybean (Glycine max (L.) Merr). Soil Science and Plant Nutrition, 51(2):203-212.
- Yu, L. H., Liu, J., & Umeda, M. (2000). Cloning and sequence characteristics of the genomic gene of a rice metallothionein. Chinese Science Bulletin, 45:153-161.
- Zhou, J., & Goldsbrough, P. B. (1995). Structure, organization and expression of the metallothionein gene family in Arabidopsis. Molecular and General Genetics MGG, 248:318-32.
- Zhou, G., Xu, Y. F., & Liu, J. Y. (2005). Characterization of a rice class II metallothionein gene: tissue expression patterns and induction in response to abiotic factors. Journal of Plant Physiology, 162(2):686-689.
References
Arisandy, K. R., Herawati, E. Y., & Suprayitno, E. (2012). Akumulasi logam berat timbal (Pb) dan gambaran histologi pada jaringan Avicennia marina (forsk.) Vierh di Perairan Pantai Jawa Timur. Jurnal Penelitian Perikanan, 1(1):15-25.
Baer, K. N., & Benson, W. H. (1987). Influence of chemical and environmental stressors on acute cadmium toxicity. Journal of Toxicology and Environmental Health, 22(1):35-44.
Baruah, S., Hazarika, K. K., & Sarma, K. P. (2012). Uptake and localization of lead in Eichhornia crassipes grown within a hydroponic system. Advances in Applied Science Research, 3(1):51-59.
Bayne, B. L., Brown, D. A., Burns, K., Dixon, D. R., Ivanovici, A., Livingstone, D. R., Lowe, D. M., Moore, M. N., Stebbing, A. R. D., & Widdows, J. (1985). The effects of stress and pollution on marine animals. New York: Praeger Scientific.
Bebianno, M. J., Nott, J. A., & Langston, W. J. (1993). Cadmium metabolism in the clam Rudipes decussata: The role of metallothioneins. Aquatic Toxicology, 27(3-4):315-334.
Bhalerao, R., Keskitalo, J., Sterky, F., Erlandsson, R., Björkbacka, H., Birve, S. J., Karlsson, J., Gardeström, P., Gustafsson, P., Lundeberg, J., & Jansson, S. (2003). Gene expression in autumn leaves. Plant Physiology, 131(2):430-442.
Bidayani, E., Rosalina, D., & Utami, E. (2017). Content of heavy metal lead (Pb) in the seagrass Cymodocea serrulata of tin mining South Bangka Regency. Maspari Journal, 9(2):169-176.
Binz, P. A., & Kägi, J. H. R. (1999). Metallothionein: molecular evolution and classification. In C. Klaassen (Ed.), Metallothionein IV. (pp. 7-8). Basel: Birkhauser-Verlag.
Butt, A., Mousley, C., Morris, K., Beynon, J., Can, C., Holub, E., Greenberg, J. T., & Buchanan-Wolaston, V. (1998). Differential expression of a senescence enhanced metallothionein gene in Arabidopsis in response to isolates of Peronospora parasitica and Pseudomonas syringiae. The Plant Journal, 16(2):209-221.
Carpenè, E., Andreani, G., & Isani, G. (2007). Metallothionein Functions and Structural Characteristics. Journal of Trace Elements in Medicine and Biology, 21(1):35-39.
Choi, D., Kim, H. M., Yun, H. K., Park, J. A., Kim, W. T., & Bok, S. H. (1996). Molecular cloning of a metallothionein-like gene from Nicotiana glutinosa L. and its induction by wounding and tobacco mosaic virus infection. Plant Physiology, 112(1):353-359.
Cobbett, C., & Goldsbrough, P. (2002). Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annual Review of Plant Biology, 53:159-182.
Engel, D. W., & Brouwer, M. (1984). Trace metal-binding proteins in marine molluscs and crustaceans. Marine Environmental Research, 13(3):177-194.
Evans, I. M., Gatehouse, L. N., Gatehouse, J. A., Robinson, N. J., & Croy, R. R. (1990). A gene from pea (Pisum sativum L.) with homology to metallothionein genes. FEBS Letters, 262(1):29-32.
Frankenne, F., Noí«l-Lambot, F., & Disteche, A. (1980). Isolation and characterization of metallothioneins from cadmium-loaded mussel Mytilus edulis. Comparative Biochemistry and Physiology Part C: Comparative Pharmacology, 66(2):179-182.
Ghelich, S., & Zarinkamar, F. (2013). SEM studies of leaf surface structure changes due to lead toxicity in Hypericum perforatum L. Global Journal of Biodiversity Science and Management, 3(2):256-263.
Gomes, M. P., Marques, T. C. L. L. de S. e M., Nogueira, M. de O. G., de Castro, E. M., & Soares, A. M. (2011). Ecophysiological and anatomical changes due to uptake and accumulation of heavy metal in Brachiaria decumbens. Scientia Agricola, 68(5):566-573.
Guo, W. J., Bundithya, W., & Goldsbrough, P. B. (2003). Characterization of the Arabidopsis metallothionein gene family: tissue-specific expression and induction during senescence and in response to copper. New Phytologist, 159(2):369-381.
Hall, J. L. (2002). Cellular mechanisms for heavy metal detoxification and tolerance. Journal of Experimental Botany, 53(366):1-11.
Hertika, A. M. S., Kusriani, K., Indrayani, E., Nurdiani, R., & Putra, R. B. D. S. (2018). Relationship between levels of the heavy metals lead, cadmium and mercury, and metallothionein in the gills and stomach of Crassostrea iredalei and Crassostrea glomerata. F1000 Research, 7:1239.
Huang, G. Y., & Wang, Y. S. (2009). Expression analysis of type 2 metallothionein gene in mangrove species (Bruguiera gymnorrhiza) under heavy metal stress. Chemosphere, 77(7):1026-1029.
Huang, G. Y., & Wang, Y. S. (2010). Expression and characterization analysis of type 2 metallothionein from grey mangrove species (Avicennia marina) in response to metal stress. Aquatic Toxicology, 99(1):86-92.
Inoue, N., Nanbu, R., Hasegawa, N., Higano, J., Kuwahara, H., & Sekiguchi, H. (2012). SEM observations on larval shell morphology of Manila clam Ruditapes philippinarum and their utility. Fisheries Science, 78(6):1237-1243.
Kägi, J. H. R. (1991). Overview of metallothionein. Methods in Enzymology, 205:613-626.
Kawashima, I., Inokuchi, Y., Chino, M., Kimura, M., & Shimizu, N. (1991). Isolation of a gene for a metallothionein-like protein from soybean. Plant & Cell Physiology, 32(6):913-916.
Lafabrie, C., Pergent-Martini, C., & Pergent, G. (2008). Metal contamination of Posidonia oceanica meadows along the Corsican coastline (Mediterranean). Environmental Pollution, 151(1):262-268.
Lane, B., Kajioka, R., & Kennedy, T. (1987). The wheat-germ ec protein is a Zinc-containing metallothionein. Biochemistry and Cell Biology, 65(11):1001-1005.
Langston, W. J., & Zhou, M. (1986). Evaluation of the significance of metal binding proteins in The Gastropod Littorina littorea. Marine Biology, 92:505-515.
Laplaze, L., Gherbi, H., Duhoux, E., Pawlowski, K., Auguy, F., Guermache, F., Franche, C., & Bogusz, D. (2002). Symbiotic and non-symbiotic expression of CgMT1, a metallothionein-like gene from the actinorhizal tree Casuarina glauca. Plant Molecular Biology, 49:81-92.
Lee, J., Shim, D., Song, W. Y., Hwang, I., & Lee, Y. (2004). Arabidopsis metallothioneins 2a and 3 enhance resistance to cadmium when expressed in Vicia faba guard cells. Plant Molecular Biology, 54:805-815.
Leszczyszyn O. I., Imam, H. T., & Blindauer, C. A. (2013). Diversity and distribution of plant metallothioneins: A review of structure, properties and functions. Metallomics, 5(9):1146-1169.
Lima, L. K. S., Silva, J. F. L., Da Silva, M. G. C., & Vieira, M. G. A. (2014). Lead biosorption by Salvinia natans biomass: equilibrium study. A Journal of the Italian Association of Chemical Engineering, 38:97-102.
Linde, A. R., & Garcia-Vazquez, E. (2006). A simple assay to quantify metallothionein helps to learn about bioindicator and environment health. Biochemistry and Molecular Biology Education, 34(5):360-363.
Liu, P., Goh, C. J., Loh, C. S., Pua, E. C. (2002). Differential expression and characterization of three metallothionein-like genes in cavendish banana (Musa acuminata). Plant Physiology, 114(2):241-250.
Malar, S., Vikram, S. S., & Favas, P. J. C., & Perumal, V. (2014). Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhornia crassipes (Mart.)]. Botanical Studies, 55(54):1-11.
Miranda J. R. D., Thomas, M. A., Thurman, D. A., & Tomsett, A. B. (1990). Metallothionein genes from the flowering plant Mimulus guttatus. FEBS Letters, 260(2):277-280.
Murphy, A., Zhou, J., Goldsbrough, P. B., Taiz, L. (1997) Purification and immunological identification of metallothioneins 1 and 2 from Arabidopsis thaliana. Plant Physiology, 113(4):1293-1301.
Noí«l-Lambot, F., Gerday, Ch., & Disteche, A. (1978). Distribution of Cd, Zn and Cu in liver and gills of the eel Anguilla anguilla with special reference to metallothioneins. Comparative Biochemistry and Physiology Part C: Comparative Pharmacology, 61(1):177-187.
Ozyigit, I., & Akinci, S. (2009). Effects of some stress factors (aluminum, cadmium and drought) on stomata of Roman Nettle (Urtica pilulifera L.). Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 37(1):108-115.
Pearce, L. L., Gandley, R. E., Han, W., Wasserloos, K., Stitt, M., Kanai, A. J., McLaughlin, M. K., Pitt, B. R. & Levitan, E. S. (2000). Role of metallothionein in nitric oxide signaling as revealed by a new green fluorescent fusion protein. Proceedings of the National Academy of Sciences, 97(1):477-482.
Probst, G. S., Bousquet, W. F., & Miya, T. S. (1977). Correlation of hepatic metallothionein concentrations with acute cadmium toxicity in the mouse. Toxicology and Applied Pharmacology, 39(1):61-69.
Rai, A. K., Kulshreshtha, K., Srivastava, P. K., & Mohanty, C. S. (2010). Leaf surface structure alterations due to particulate pollution in some common plants. The Environmentalist, 30:18-23.
Ramamurthy, N., & Kannan, S. (2009). SEM-EDS analysis of soil and plant (Calotropis Gigantea Linn) collected from an industrial village, Cuddalore Dt, Tamil Nadu, India. Romanian Journal of Biophysics, 19(3): 219-226.
Rand, G. M., & Petrocelli, S. R. (1985). Fundamentals of aquatic toxicology. New York: Kemisphere Publishing Corporation.
Rafia, A., Saba, H., & Shabana, A. (2006). Phytotoxicity of Pb: I. Effect of Pb on germination, growth, morphology and histomorphology of Phaseolus mungo and Lens culinaris. Pakistan Journal of Biological Sciences, 9(5): 979-984.
Robinson, N. J., Evans, I. M., Mulcrone, J., Bryden, J., & Tommey, A. M. (1992). Genes with similarity to metallothionein gees and copper, zink ligands in Pisum sativum L. Plant and Soil, 141:291-298.
Rosalina, D., Herawati, E. Y., Risjani, Y., & Musa, M. (2018a). Lamun diversity in regency of South Bangka Province Bangka Belitung Islands. EnviroScienteae, 14(1):21-28.
Rosalina, D., Herawati, E. Y., Musa, M., & Risjani Y. (2018b). Lead (Pb) adsorption in roots, rhizomes, and leaves of seagrass Cymodocea serrulata. Fresenius Environment Bulletin, 27(12A):9156-9166.
Rosalina, D., Herawati, E. Y., Musa, M., Sofarini, D., Amin, M., & Risjani, Y. (2019a). Lead accumulation and its histological impact on Cymodocea serrulata Seagrass in the laboratory. Sains Malaysiana, 48(4):813-822.
Rosalina, D., Herawati, E. Y., Musa, M., Sofarini, D., & Risjani, Y. (2019b). Short communication: Anatomical changes in the roots, rhizomes and leaves of seagrass (Cymodocea serrulata) in responses to lead. Biodiversitas Journal of Biological Diversity, 20(9):2583-2588.
Rumahlatu, D., Corebima, A. B., Amin, M., & Rachman, F. (2012). The effect of Cadmium on metallothionein protein expression of Diadema setosum (Echinoidea; Echinodermata). Jurnal Penelitian Perikanan, 1:26-35.
Shi, G., & Cai, Q. (2009). Leaf plasticity in peanut (Arachis hypogaea L.) in response to heavy metal stress. Environmental and Experimental Botany, 67(1):112-117.
Singh, S., & Sinha, S. (2004). Scanning electron microscopic studies and growth response of the plants of Helianthus annuus L. grown on tannery sludge amended soil. Environment International, 30(3):389-395.
Sridhar, B. B. M., Diehl, S. V., Han, F. X., Monts, D. L., & Su, Y. (2005). Anatomical changes due to uptake and accumulation of Zn and Cd in Indian mustard (Brassica juncea). Environmental and Experimental Botany, 54(2):131-141.
Sugiura, H., Kawasaki, Y., Suzuki, T., & Maegawa, M. (2009). The structural and histochemical analyses and chemical characters of the cuticle and epidermal walls of cotyledon in ungerminated seeds of Zostera marina L. Fisheries Science, 75(369):369-377.
Usha, B., Prashanth, S. R., & Parida, A. (2007). Differential expression of two metallothionein encoding genes during heavy metal stress in the mangrove species, Avicennia marina (Forsk.) Vierh. Current Science, 93(9):1215-1219.
Weryszko-Chmielewska, E., & Chwil, M. (2005). Lead-induced histological and ultrastructural changes in the leaves of soybean (Glycine max (L.) Merr). Soil Science and Plant Nutrition, 51(2):203-212.
Yu, L. H., Liu, J., & Umeda, M. (2000). Cloning and sequence characteristics of the genomic gene of a rice metallothionein. Chinese Science Bulletin, 45:153-161.
Zhou, J., & Goldsbrough, P. B. (1995). Structure, organization and expression of the metallothionein gene family in Arabidopsis. Molecular and General Genetics MGG, 248:318-32.
Zhou, G., Xu, Y. F., & Liu, J. Y. (2005). Characterization of a rice class II metallothionein gene: tissue expression patterns and induction in response to abiotic factors. Journal of Plant Physiology, 162(2):686-689.