Abstract
A short term pot trail was employed to evaluate the exposure of mixed heavy metals (Cu, Pb and Zn) on growth, radial oxygen loss (ROL) and root anatomy in Bruguiera gymnorrhiza. The possible function of BgC4H, a cytochrome P450 gene, on root lignification was also discussed. The exposures of mixed Cu, Pb and Zn directly reduce O2 leakage at root surface. The reduced ROL inhibited by heavy metals was mainly ascribed by the changes in root anatomical features, such as decreased root porosity together with increased lignification within the exodermis. BgC4H was found to be up-regulated after 0.5-day metal exposure, and remained higher transcript levels within 3-day metal exposure when compared to control roots. Besides, the inhibited photosynthesis may also result in less oxygen can be transported to the underground roots. In summary, the mangrove B. gymnorrhiza appeared to react to external mixed metal contaminants by developing a lignified and impermeable exodermis, and such a root barrier induced by mixed Cu, Pb and Zn appeared to be an adaptive response to block metal ions enters into the roots.
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Abubakar US, Zulkifli SZ, Ismail A (2018) Heavy metals bioavailability and pollution indices evaluation in the mangrove surface sediment of Sungai Puloh, Malaysia. Environ Earth Sci 77:225. https://doi.org/10.1007/s12665-018-7399-1
Agoramoorthy G, Chen FA, Hsu MJ (2008) Threat of heavy metal pollution in halophtytic and mangrove plants of Tamil Nadu, India. Environ Pollut 155:320–326
Armstrong J, Armstrong W (2005) Rice: sulfide-induced barriers to root radial oxygen loss, Fe2+ and water uptake, and lateral root emergence. Ann Bot 96:625–638
Armstrong W, Wright E (1975) The theoretical basis for the manipulation of flux data obtained by the cylindrical platinum electrode technique. Physiol Plant 35:21–26
Bodegom PMV, Kanter MD, Bakker C, Aerts R (2005) Radial oxygen loss, a plastic property of dune slack plant species. Plant Soil 271:351–364
Cheng H, Liu Y, Tam NFY, Wang X, Li SY, Chen GZ, Ye ZH (2010) The role of radial oxygen loss and root anatomy on zinc uptake and tolerance in mangrove seedlings. Environ Pollut 158:1189–1196
Cheng H, Chen DT, Tam NFY, Chen GZ, Li SY, Ye ZH (2012) Interactions among Fe2+, S2−, and Zn2+ tolerance, root anatomy and radial oxygen loss in mangrove plants. J Exp Bot 63:2619–2630
Cheng H, Jiang ZY, Liu Y, Ye ZH, Wu ML, Sun CC, Sun FL, Fei J, Wang YS (2014) Metal (Cu, Pb and Zn) uptake and tolerance by mangroves in relation to root anatomy and lignification/suberization. Tree Physiol 34:646–656
Cheng H, Wang YS, Fei J, Jiang ZY, Ye ZH (2015a) Differences in root aeration, iron plaque formation and waterlogging tolerance in six mangroves along a continues tidal gradient. Ecotoxicology 242:1659–1667
Cheng H, Wang YS, Liu Y, Ye ZH, Wu ML, Sun CC (2015b) Pb uptake and tolerance in the two mangroves with different root lignification and suberization. Ecotoxicology 24:1650–1658
Colmer TD (2003a) Aerenchyma and an inducible barrier to radial oxygen loss facilitate root aeration in upland, paddy and deep-water rice (Oryza sativa L.). Ann Bot 91:301–309
Colmer TD (2003b) Long-distance transport of gases in plants: a perspective on internal aeration and radial loss from roots. Plant Cell Environ 26:17–36
Colmer TD, Pedersen O (2008) Oxygen dynamics in submerged rice (Oryza sativa). New Phytol 178:326–334
Evans DE (2003) Aerenchyma formation. New Phytol 161:35–49
Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690
He B, Li RL, Chai MW, Qiu GY (2014) Threat of heavy metal contamination in eight mangrove plants from the Futian mangrove forest, China. Environ Geochem Health 36:467–476.
Hose E, Clarkson DT, Steudle E, Schreiber L, Hartung W (2001) The exodermis: a variable apoplastic barrier. J Exp Bot 52:2245–2264
Huang GY, Wang YS (2010) Physiological and biochemical responses in the leaves of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza) exposed to multiple heavy metals. J Hazard Mater 182:848–854
Jackson MB, Armstrong W (1999) Formation of aerenchyma and processes of plant ventilation in relation to soil flooding and submergence. Plant Biol 1:274–287
Jacob DL, Otte ML (2003) Conflicting process in the wetland plant rhizosphere: metal retention or mobilization? Water Air Soil Pollut 3:91–104
Kludze HK, DeLaune RD, Patrick WH (1993) Aerenchyma formation and methane and oxygen exchange in rice. Soil Sci Soc Am J 57:386–391
Krishnamurthy P, Ranathunge K, Franke R, Prakash HS, Schreiber L, Mathew MK (2009) The role of root apoplastic transport barriers in salt tolerance of rice (Oryza sativa L.). Planta 230:119–134
Krishnamurthy P, Jyothi-Prakash PA, Qin L, He J, Lin QS, Loh CS, Kumar PP (2014) Role of hydrophobic barriers in salt exclusion of a mangrove plant Avicennia officinalis. Plant Cell Environ 37:1656–1671
Kulichikhin K, Yamauchi T, Watanabe K, Nakazono M (2014) Biochemical and molecular characterization of rice (Oryza sativa L.) roots forming a barrier to radial oxygen loss. Plant Cell Environ 37:2406–2420
Laskov C, Horn O, Hupfer M (2006) Environmental factors regulating the radial oxygen loss from roots of Myriophyllum spicatum and Potamogeton crispus. Aquat Bot 84:333–340
Lenzewski N, Muller P, Meier RJ, Liebsch G, Jensen K, Koop-Jakobsen K (2018) Dynamics of oxygen and carbon dioxide in rhizospheres of Lobelia dortmanna—a planar optode study of belowground gas exchange between plants and sediment. New Phytol 218:131–141
Li YL, Fan XR, Shen QR (2008) The relationship between rhizosphere nitrification and nitrogen-use efficiency in rice plants. Plant Cell Environ 31:73–85
Liu QQ, Zheng L, He F, Zhao FJ, Shen ZG, Zheng LQ (2015) Transcriptional and physiological analyses identify a regulatory role for hydrogen peroxide in the lignin biosynthesis of copper-stressed rice roots. Plant Soil 387:323–336
Lovelock CE, Feller IC, McKee KL, Thompson R (2005) Variation in mangrove forest structure and sediment characteristics in Bocas del Toro, Panama. Caribb J Sci 41:456–464
Lovelock CE, Cahoon DR, Friess DA, Guntenspergen GR, Krauss KW, Reef R, Rogers K, Saunders ML, Sidik F, Swales A, Saintilan N, Thuyen LX, Triet T (2015) The vulnerability of Indo-Pacific mangrove forests to sea-level rise. Nature 526:559–563
MacFarlane GR, Burchett MD (2002) Toxicity, growth and accumulation relationships of copper, lead and zinc in the grey mangrove Avicennia marina (Forsk.) Vierh. Mar Environ Res 54:65–84
MacFarlane GR, Koller CE, Blomberg SP (2007) Accumulation and partitioning of heavy metals in mangroves: a synthesis of field-based studies. Chemosphere 69:1454–1464
Peng YL, Wang YS, Fei J, Sun CC, Cheng H (2015) Ecophysiological differences between three mangrove seedlings (Kandelia obovata, Aegiceras corniculatum, and Avicennia marina) exposed to chilling stress. Ecotocicology 24:1722–1732
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2004–2007
Pi N, Tam NFY, Wu Y, Wong MH (2009) Root anatomy and spatial pattern of radial oxygen loss of eight true mangrove species. Aquat Bot 90:222–230
Qiu YW, Yu KF, Zhang G, Wang WX (2011) Accumulation and partitioning of seven trace metals in mangroves and sediment cores from three estuarine wetlands of Hainan Island, China. J Hazard Mater 190:631–638
Sablla E, Luvisi A, Aprile A, Negro C, Vergine M, Nicolì F, Miceli A, Bellis LD (2018) Xylella fastidiosa induces differential expression of lignification related-genes and lignin accumulation in tolerant olive trees cv. Leccino. J Plant Physiol 220:60–68
Shannon MC, Grieve CM, Francois LE (1994) Whole plant response to salinity. In: Wilkinson RE (ed). Plant-environment interactions. Marcel Dekker, New York, NY, p 199–244
Schreiber L, Hartmann K, Skrabs M, Zeier J (1999) Apoplastic barriers in roots: chemical composiiton of endodermal and hypodermal cell walls. J Exp Bot 50:1267–1280
Simone OD, Haase K, Müller E, Junk WJ, Hartmann K, Schreiber L, Schmidt W (2003) Apoplastic barriers and oxygen transport properties of hypodermal cell walls in roots from four Amazonian tree species. Plant Physiol 132:206–217
Soukup A, Armstrong W, Schreiber L, Franke R, Votrubová O (2007) Apoplastic barriers to radial oxygen loss and solute penetration: a chemical and functional comparison of the exodermis of two wetland species, Phragmites australis and Glyceria maxima. New Phytol 173:264–278
Tam NFY, Li SH, Lan CY, Chen GZ, Li MS, Wong YS (1995) Nutrients and heavy metal contamination of plants and sediments in Futian mangrove forest. Hydrobiologia 295:149–158
Tao ST, Wang DY, Jin C, Sun W, Liu X, Zhang SL (2015) Cinnamate-4-hydroxylase gene is involved in the step of lignin biosynthesis in Chinese white Pear. J Am Soc Hortic Sci 140:573–579
Thomas R, Fang XX, Ranathunge K, Anderson TR, Peterson CA, Bernard A (2007) Soybean root suberin: anatomical distribution, chemical composition, and relationship to partial resistance to Phytophthora sojae. Plant Physiol 144:311
Ure AM, Quevauviller P, Muntau H, Griepink B (1993) Speciation of heavy metals in soils and sediments. An account of the improvement and harmonization of extraction techniques undertaken under the auspices of the BCR of the commission of the European communities. Int J Environ Anal Chem 51:135–151
Wang YS (2019) Molecular ecology of mangroves. The Science Publishing Company, Beijing, China
Xu QT, Yang L, Zhou ZQ, Mei FZ, Qu LH, Zhou GS (2013) Process of aerenchyma formation and reactive oxygen species induced by waterlogging in wheat seminal roots. Plant Soil 238:969–982
Yamauchi T, Colmer TD, Pedersen O, Nakazono M (2018) Regulation of root traits for internal aeration and tolerance to soil waterlogging-flooding stress. New Phytol 176:1118–1130
Yan Q, Si JR, Cui XX, Peng H, Chen X, Xiang H, Dou DL (2019) The soybean cinnamate 4-hydroxylase gene GmC4H1 contributes positively to plant defense via increasing lignin content. Plant Growth Regul 88:139–149
Yoo YH, Choi HK, Jung KH (2015) Genome-wide identification and analysis of genes associated with lysigenous aerenchyma formation in rice roots. J Plant Biol 58:117–127
Zhang FQ, Wang YS, Lou ZP, Dong JD (2007) Effect of heavy metal stress on antioxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Chemosphere 67:44–50
Zhao Y, Wang X, Wang YS, Jiang ZY, Ma XY, Inyang AI, Cheng H (2019) Effects of salt on root aeration, nitrification, and nitrogen uptake in mangroves. Forests 10:1131. https://doi.org/10.3390/f10121131
Zhou YW, Zhao B, Peng YS, Chen GZ (2010) Influence of mangrove reforestation on heavy metal accumulation and speciation in intertidal sediments. Mar Pollut Bull 60:1319–1324
Acknowledgements
This research was supported by the National Natural Science Foundation of China (No. U1901211, No. 41676086, No. 41706118, No. 4143096, No. 41876126 and No. 41506127), the National Key Research and Development Plan (No. 2017FY100700), the International Partnership Program of Chinese Academy of Sciences (No. 133244KYSB20180012), the Strategic Priority Research Program of the Chinese Academy of Sciences (No. XDA23050200, No. XDA13010500 and No. XDA13020503), Key Special Project for Introduced Talents Team of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (No. GML2019ZD0305), Innovation Academy of South China Sea Ecology and Environmental Engineering, Chinese Academy of Sciences (No. ISEE2019ZR02 and No. ISEE2018ZD02), Natural Science Foundation of Guangdong province (No. 2014A030313783), Science and Technology Project of Guangdong province (No. 2016A020222011), Guangdong special branch plans young talent with scientific and technological innovation (No. 2016TQ03Z985), Guangzhou Science and Technology Project (No. 20171001013).
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Cheng, H., Wang, YS., Li, CD. et al. Mixture of Pb, Zn and Cu on root permeability and radial oxygen loss in the mangrove Bruguiera gymnorrhiza. Ecotoxicology 29, 691–697 (2020). https://doi.org/10.1007/s10646-020-02234-z
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DOI: https://doi.org/10.1007/s10646-020-02234-z