Abstract
Typha domingensis Pers. is a plant that grows in marshy environments, where cadmium (Cd) accumulates. The root is the first organ that comes into contact with the metal. The aim of this study was to evaluate the effect of Cd on the roots of T. domingensis. The experiment was conducted in a greenhouse using different Cd concentrations: (1) 0 µM (control), (2) 10 µM, and (3) 50 µM, with 10 replicates for 90 days. The plants were placed in plastic containers containing 5 L of nutrient solution modified with the different Cd concentrations. At the end of the experiment, the roots were measured, sampled, fixed, and subjected to usual plant microtechniques. The slides were observed and photographed under light microscopy and analyzed in ImageJ software. To measure Cd absorption, atomic-absorption spectrometry was used. The data were subjected to analysis of variance and comparison of means by the Scott-Knott test at P < 0.05. When exposed to 50 µM of Cd, the roots accumulated 99.35% of the Cd. At this concentration, there was a reduction in the exodermis but there was an increase in the diameter of the cortical cells and in the proportion of aerenchyma in the cortex. There was an increase in the root cap, which guaranteed the protection of the primary meristems. Therefore, T. domingensis adjusts its root anatomy improving the Cd tolerance and shows potential for phytoremediation purposes.






Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.Data availability
The data supporting the findings of this study are available from the corresponding author, Fabricio José Pereira, upon request.
Ethical approval.
Not applicable.
References
Akguc N, Ozyigit I, Yasar U, Leblebici Z, Yarci C (2010) Use of Pyracantha coccinea Roem. as a possible biomonitor for the selected heavy metals. Int J Environ Sci Technol 7:427–434. https://doi.org/10.1007/BF03326152
Arduini I, Godbold DL, Onnis A (1996) Cadmium and copper uptake and distribution in Mediterranean tree seedlings. Physiol Plant 97:111–117. https://doi.org/10.1111/j.1399-3054.1996.tb00486.x
Arduini I, Masoni A, Mariotti M, Ercoli L (2004) Low cadmium application increase miscanthus growth and cadmium translocation. Environ Exp Bot 52:89–100. https://doi.org/10.1016/j.envexpbot.2004.01.001
Bah AM, Sun H, Chen F, Zhou J, Dai H, Zhang G, Wu F (2010) Comparative proteomic analysis of Typha angustifolia leaf under chromium, cadmium and lead stress. J Hazard Mater 184:191–203. https://doi.org/10.1016/j.jhazmat.2010.08.023
Bali AS, Sidhu GPS, Kumar V (2020) Root exudates ameliorate cadmium tolerance in plants: a review. Environ Chem Lett 18:1243–1275. https://doi.org/10.1007/s10311-020-01012-x
Barlow PW (2002) The root cap: cell dynamics, cell differentiation and cap function. J Plant Growth Regul 21:261–286. https://doi.org/10.1007/s00344-002-0034-z
Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17:21–34. https://doi.org/10.1590/S1677-04202005000100003
Bonanno G, Cirelli GL (2017) Comparative analysis of element concentrations and translocation in three wetland congener plants: Typha domingensis, Typha latifolia and Typha angustifolia. Ecotoxicol Environ Saf 143:92–101. https://doi.org/10.1016/j.ecoenv.2017.05.021
Bonanno G, Borg JA, Di Martino V (2017) Levels of heavy metals in wetland and marine vascular plants and their biomonitoring potential: a comparative assessment. Sci Total Environ 576:796–806. https://doi.org/10.1016/j.scitotenv.2016.10.171
Boominathan R, Doran PM (2003) Cadmium tolerance and antioxidative defenses in hairy roots of the cadmium hyperaccumulator, Thlaspi caerulescens. Biotechnol Bioeng 83:158–167. https://doi.org/10.1002/bit.10656
Bukatsch F (1972) Bemerkungen zur Doppelfärbung: Astrablau-Safranin. Mikrokosmos 61:225–255
Cardwell AJ, Hawker DW, Greenway M (2002) Metal accumulation in aquatic macrophytes from southeast Queensland, Australia. Chemosphere 48:653–663. https://doi.org/10.1016/S0045-6535(02)00164-9
Corrêa FF, Pereira MP, Kloss RB, Castro EM, Pereira FJ (2017a) Leaf ontogeny and meristem activity of Typha domingensis Pers. (Typhaceae) under different phosphate concentrations. Aquat Bot 136:43–51. https://doi.org/10.1016/j.aquabot.2016.09.007
Corrêa FF, Pereira MP, Madail RH, Santos BR, Barbosa S, Castro EM, Pereira FJ (2017b) Anatomical traits related to stress in high density populations of Typha angustifolia L. (Typhaceae). Braz J Biol 77:52–59. https://doi.org/10.1590/1519-6984.09715
Dalla Vecchia F, La Rocca N, Moro I, Faveri S, Andreoli C, Rascio N (2005) Morphogenetic, ultrastructural and physiological damages suffered by submerged leaves of Elodea canadensis exposed to cadmium. Plant Sci J 168:329–338. https://doi.org/10.1016/j.plantsci.2004.07.025
Di Toppi LS, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130. https://doi.org/10.1016/S0098-8472(98)00058-6
Díaz AS, Aguiar GM, Pereira MP, Castro EM, Magalhães PC, Pereira FJ (2018) Aerenchyma development in different root zones of maize genotypes under water limitation and different phosphorus nutrition. Biol Plant 62:561–568. https://doi.org/10.1007/s10535-018-0773-8
Díaz AS, Cruz YC, Duarte VP, Castro EM, Magalhães PC, Pereira FJ (2021) The role of reactive oxygen species and nitric oxide in the formation of root cortical aerenchyma under cadmium contamination. Physiol Plant 173https://doi.org/10.1111/ppl.13582
Feder N, O’Brien TP (1968) Plant microtechnique: some principles and new methods. Am J Bot 55:123–142. https://doi.org/10.1002/j.1537-2197.1968.tb06952.x
Ferreira DF (2011) Sisvar: a computer statistical analysis system. Ciênc Agrotec 35:1039–1042. https://doi.org/10.1590/S1413-70542011000600001
Gall JE, Boyd RS, Rajakaruna N (2015) Transfer of heavy metals through terrestrial food webs: a review. Environ Monit Assess 187:1–21. https://doi.org/10.1007/s10661-015-4436-3
Gratão PL, Prasad MNV, Cardoso PF, Lea PJ, Azevedo RA (2005) Phytoremediation: green technology for the clean up of toxic metals in the environment. Braz J Plant Physiol 17:53–64. https://doi.org/10.1590/S1677-04202005000100005
Gunawardena AH (2008) Programmed cell death and tissue remodelling in plants. J Exp Bot 59:445–451. https://doi.org/10.1093/jxb/erm189
Gussarsson M (1994) Cadmium-induced alterations in nutrient composition and growth of betula pendula seedlings: The significance of fine roots as a primary target for cadmium toxicity. J Plant Nutr 17:2151–2163. https://doi.org/10.1080/01904169409364871
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn 347:1–34
Hozhina EI, Khramov AA, Gerasimov PA, Kumarkov AA (2001) Uptake of heavy metals, arsenic, and antimony by aquatic plants in the vicinity of ore mining and processing industries. J Geochem Explor 74:153–162. https://doi.org/10.1016/S0375-6742(01)00181-9
Johansen DA (1940) Plant microtechnique. McGraw-Hill, New York
Kim DY, Bovet L, Kushnir S, Noh EW, Martinoia E, Lee Y (2006) AtATM3 is involved in heavy metal resistance in Arabidopsis. Plant Physiol 140:922–932. https://doi.org/10.1104/pp.105.074146
Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534. https://doi.org/10.1146/annurev-arplant-042809-112156
Kraus JE, Arduin M (1997) Manual básico de métodos em morfologia vegetal. EDUR Seropédica, Rio de Janeiro
Li LZ, Tu C, Peijnenburg WJ, Luo YM (2017) Characteristics of cadmium uptake and membrane transport in roots of intact wheat (Triticum aestivum L.) seedlings. Environ Pollut 221:351–358. https://doi.org/10.1016/j.envpol.2016.11.085
Li J, Yu J, Du D, Liu J, Lu H, Yan C (2019) Analysis of anatomical changes and cadmium distribution in Aegiceras corniculatum (L) Blanco roots under cadmium stress. Mar Pollut Bull 149:110536. https://doi.org/10.1016/j.marpolbul.2019.110536
Li H, Zheng X, Tao L, Yang Y, Gao L, Xiong J (2019b) Aeration increases cadmium (Cd) retention by enhancing iron plaque formation and regulating pectin synthesis in the roots of rice (Oryza sativa) seedlings. Rice 12:1–14. https://doi.org/10.1186/s12284-019-0291-0
Loix C, Huybrechts M, Vangronsveld J, Gielen M, Keunen E, Cuypers A (2017) Reciprocal interactions between cadmium-induced cell wall responses and oxidative stress in plants. Front Plant Sci 8:1867. https://doi.org/10.3389/2Ffpls.2017.01867
Lux A, Martinka M, Vaculík M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37. https://doi.org/10.1093/jxb/erq281
MacFarlane GR, Burchett MD (2000) Cellular distribution of copper, lead and zinc in the grey mangrove, Avicennia marina (Forsk.) Vierh. Aquat Bot 68:45–59. https://doi.org/10.1016/S0304-3770(00)00105-4
Malec P, Maleva MG, Prasad MNV, Strzałka K (2010) Responses of Lemna trisulca L. (Duckweed) exposed to low doses of cadmium: thiols, metal binding complexes, and photosynthetic pigments as sensitive biomarkers of ecotoxicity. Protoplasma 240:69–74. https://doi.org/10.1007/s00709-009-0091-2
Martinka M, Vaculik M, Lux A (2014) Plant cell responses to cadmium and zinc. In: Nick P, Opatrný Z. Applied Plant Cell Biology. Springer, Plant Cell Monographs 22: 09–246.
Mohamed AA, Castagna A, Ranieri A, di Toppi LS (2012) Cadmium tolerance in Brassica juncea roots and shoots is affected by antioxidant status and phytochelatin biosynthesis. Plant Physiol Biochem 57:15–22. https://doi.org/10.1016/j.plaphy.2012.05.002
Moussa HR, El-Gamal SM (2010) Effect of salicylic acid pretreatment on cadmium toxicity in wheat. Biol Plant 54:315–320. https://doi.org/10.1007/s10535-010-0054-7
Oliveira JPV, Pereira MP, Duarte VP, Corrêa FF, Castro EM, Pereira FJ (2018) Cadmium tolerance of Typha domingensis Pers. (Typhaceae) as related to growth and leaf morphophysiology. Braz J Biol 78:509–516. https://doi.org/10.1590/1519-6984.171961
Pereira FJ, Magalhães PC, Souza TCD, Castro EMD, Alves JD (2010) Atividade do sistema antioxidante e desenvolvimento de aerênquima em raízes de milho “Saracura.” Pesqui Agropecu Bras 45:451–456. https://doi.org/10.1590/S0100-204X2010000500003
Pereira MP, Almeida Rodrigues LC, Corrêa FF, Castro EM, Ribeiro VE, Pereira FJ (2016) Cadmium tolerance in Schinus molle trees is modulated by enhanced leaf anatomy and photosynthesis. Trees 30:807–814. https://doi.org/10.1007/s00468-015-1322-0
Pereira FJ, Castro EM, Pires MF, Oliveira CD, Pasqual M (2017) Anatomical and physiological modifications in water hyacinth under cadmium contamination. J Appl Bot Food Qual 90:10–17. https://doi.org/10.5073/JABFQ.2017.090.003
Pietrini F, Iannelli MA, Pasqualini S, Massacci A (2003) Interaction of cadmium with glutathione and photosynthesis in developing leaves and chloroplasts of Phragmites australis (Cav.) Trin. ex Steudel. Plant Physiol 133:829–837. https://doi.org/10.1104/pp.103.026518
Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39. https://doi.org/10.1146/annurev.arplant.56.032604.144214
Polle A, Schützendübel A (2003) Heavy metal signalling in plants: linking cellular and organismic responses. Plant Abiotic Stress 4:187–215. https://doi.org/10.1007/978-3-540-39402-0_8
Prasad MN, Oliveira Freitas HM (2003) Metal hyperaccumulation in plants: biodiversity prospecting for phytoremediation technology. Electron J Biotechnol 6:285–321. https://doi.org/10.2225/vol6-issue3-fulltext-6
Qiuyue S, Junran W, Jinhua Z, Jiang Z, Hangfeng W, Jiayue W, Donghua L (2016) Cadmium localization and its toxic effects on root tips of barley. Zemdirbyste 103:151‒158. https://doi.org/10.13080/z-a.2016.103.020
Ribeiro ES, Pereira MP, Castro EMD, Baroni GDR, Corrêa FF, Pereira FJ (2015) Relações da anatomia radicular na absorção, no acúmulo e na tolerância ao chumbo em Echinodorus grandiflorus. Rev Bras Eng Agric Amb 19:605–612. https://doi.org/10.1590/1807-1929/agriambi.v19n6p605-612
Rodrigues AC, Estelita MEM (2004) Anatomia da raiz de Cyperus giganteus Vahl (Cyperaceae) em desenvolvimento. Braz J Bot 27:629–638. https://doi.org/10.1590/S0100-84042004000400003
Ronzan M, Piacentini D, Fattorini L, Della Rovere F, Eiche E, Riemann M, Falasca G (2018) Cadmium and arsenic affect root development in Oryza sativa L. negatively interacting with auxin. Environ Exp Bot 151:64–75. https://doi.org/10.1016/j.envexpbot.2018.04.008
Santos JCB, Castro EM, Duarte VP, Pereira MP, Corrêa FF, Pereira FJ (2021) Root growth and anatomy of Typha domingensis Pers. related to phosphorus availability. Acta Limnol Bras 33:e19. https://doi.org/10.1590/S2179-975X2120
Schussler EE, Longstreth DJ (1996) Aerenchyma develops by cell lysis in roots and cell separation in leaf petioles in Sagittaria lancifolia (Alismataceae). Am J Bot 83:1266–1273. https://doi.org/10.1002/j.1537-2197.1996.tb13910.x
Seago JL, Peterson CA, Enstone DE, Scholey CA (1999) Development of the endodermis and hypodermis of Typha glauca Godr. and Typha angustifolia L. roots. Can J Bot 77:122–134. https://doi.org/10.1139/b98-173
Sesin S, Davy CM, Freeland JR (2021) Review of Typha spp (cattails) as toxicity test species for the risk assessment of environmental contaminants on emergent macrophytes. Environ Pollut 284:117105. https://doi.org/10.1016/j.envpol.2021.117105
Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52. https://doi.org/10.1590/S1677-04202005000100004
Siddiqui S, Meghvansi MK, Wani MA, Jabee F (2009) Evaluating cadmium toxicity in the root meristem of Pisum sativum L. Acta Physiol Plant 31:531–536. https://doi.org/10.1007/s11738-008-0262-3
Sidhu GPS, Singh HP, Batish DR, Kohli RK (2017) Tolerance and hyperaccumulation of cadmium by a wild, unpalatable herb Coronopus didymus (L.) Sm. (Brassicaceae). Ecotoxicol Environ Saf 135:209–215. https://doi.org/10.1016/j.ecoenv.2016.10.001
Singh R, Tripathi RD, Dwivedi S, Singh M, Trivedi PK, Chakrabarty D (2010) Cadmium-induced biochemical responses of Vallisneria spiralis. Protoplasma 245:97–103. https://doi.org/10.1007/s00709-010-0146-4
Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6:1143. https://doi.org/10.3389/fpls.2015.01143
Souza VL, Silva DDC, Santana KB, Mielke MS, Almeida AAFD, Mangabeira PAO, Rocha EA (2009) Efeitos do cádmio na anatomia e na fotossíntese de duas macrófitas aquáticas. Acta Bot Bras 23:343–354. https://doi.org/10.1590/S0102-33062009000200006
Sun Y, Sun G, Xu Y, Wang L, Liang X, Lin D (2013) Assessment of sepiolite for immobilization of cadmium-contaminated soils. Geoderma 193:149–155. https://doi.org/10.1016/j.geoderma.2012.07.012
Uraguchi S, Fujiwara T (2012) Cadmium transport and tolerance in rice: perspectives for reducing grain cadmium accumulation. Rice 5:1–8. https://doi.org/10.1186/1939-8433-5-5
Welz B, Sperling M (2008) Atomic absorption spectrometry. Wiley-VCH, Weinheim
Wilkins DA (1978) The measurement of tolerance to edaphic factors by means of root growth. New Phytol 80:623–633. https://doi.org/10.1111/j.1469-8137.1978.tb01595.x
Xiong J, An L, Lu H, Zhu C (2009) Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230:755–765. https://doi.org/10.1007/s00425-009-0984-5
Xu W, Shi W, Yan F, Zhang B, Liang J (2011) Mechanisms of cadmium detoxification in cattail (Typha angustifolia L.). Aquat Bot 94:37–43. https://doi.org/10.1016/j.aquabot.2010.11.002
Yuan HM, Huang X (2016) Inhibition of root meristem growth by cadmium involves nitric oxide-mediated repression of auxin accumulation and signalling in Arabidopsis. Plant Cell Environ 39:120–135. https://doi.org/10.1111/pce.12597
Funding
The authors thank CNPq [Conselho Nacional de Desenvolvimento Científico e Tecnológico (National Counsel of Technological and Scientific Development)], CAPES [Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Coordination for the Improvement of Higher Education Personnel)], and FAPEMIG [Fundação de Amparo à Pesquisa do estado de Minas Gerais (Minas Gerais State Research Foundation)] for the funding and research grants awarded to perform the present study.
Author information
Authors and Affiliations
Contributions
J. P. V. O.: conceptualizing, designing and performing the experiments, analyzing the data, curating the data, and writing the first draft of the manuscript; M. P. P.: performing the experiments, analyzing the data, and writing the manuscript; V. P. D.: performing the experiments, analyzing the data, and writing the manuscript; F. F. C.: performing the experiments, analyzing the data, and writing the manuscript; E. M. C.: acquiring resources, analyzing the data, and writing the manuscript; F. J. P.: advising the first author, conceptualizing, acquiring resources, designing and running the experiments, analyzing the data, curating the data, administering the project and writing the manuscript.
Corresponding author
Ethics declarations
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflict of interest
The authors declare no competing interests.
Additional information
Responsible Editor: Elena Maestri.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
de Oliveira, J.P.V., Pereira, M.P., Duarte, V.P. et al. Root anatomy, growth, and development of Typha domingensis Pers. (Typhaceae) and their relationship with cadmium absorption, accumulation, and tolerance. Environ Sci Pollut Res 29, 19878–19889 (2022). https://doi.org/10.1007/s11356-022-18842-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-022-18842-7


