Assessment of differences in anatomical and hydraulic properties of the root and xylem of three willow (Salix L.) clones during phytostabilization after exposure to elevated cadmium

Authors

DOI:

https://doi.org/10.2298/ABS220309016H

Keywords:

Salix, cadmium, root, xylem, hydraulic conductivity

Abstract

Paper description:

  • Understanding root anatomy is a prerequisite for effective selection of willow (Salix) clones for Cd phytoremediation.
  • Root anatomical parameters of three Salix clones treated with two cadmium concentrations in soil were analyzed and the phytoremediation potential was evaluated.
  • Changes in root periderm, secondary phloem (cortex), and wood (secondary and primary xylem) in the lumen of individual vessels of root secondary and primary xylem were observed in treated clones.
  • The anatomical structure and the hydraulic properties of root provide new insight into genotype-specific differences in response to elevated Cd concentrations.

Abstract: An anatomical study of adventitious roots of three Salix clones, B-44, SV068 and SM4041, treated with 3 and 6 mg Cd kg-1 dry weight in soil in a greenhouse experiment. The aim was to analyze the anatomical characteristics of roots in response to pollution by cadmium and to assess the potential application of anatomical and hydraulic characteristics in the selection of the most suitable Salix clones for phytostabilization of pollutants in soils. Anatomical parameters measured in this study included root cross-sectional area, root diameter, the proportion of periderm, secondary phloem (cortex) and wood (secondary and primary xylem), and parameters of the vessels (lumen area, diameter and frequency). Based on the measurements of individual vessel lumens and the number of vessels, the theoretical hydraulic conductivity (kh) of roots was calculated. The effects of applied Cd concentrations on root traits were studied in clones and control plants. Following treatments with both Cd concentrations, plants of clone B-44 had the highest values of most parameters and significantly higher kh in comparison with control samples due to the significantly larger root cross-sectional area and lumen of vessels. It was concluded that these characteristics can serve for effective evaluation and selection of clones for remediation of sites contaminated with cadmium.

Downloads

Download data is not yet available.

References

Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP. Unravelling cadmium toxicity and tolerance in plants: Insight into regulatory mechanisms. Environ Exp Bot. 2012;83:33-46. https://doi.org/10.1016/j.envexpbot.2012.04.006

Pajević S, Borišev M, Nikolić N, Arsenov DD, Orlović S, Župunski M. Phytoextraction of Heavy Metals by Fast-Growing Trees: A Review. In: Ansari A, Gill S, Gill R, Lanza G, Newman L, editors. Phytoremediation: Management of Environmental Contaminants, Vol 3. Cham: Springer International Publishing; 2016. p. 29-64. https://doi.org/10.1007/978-3-319-40148-5_2

Arsenov D, Župunski M, Borišev M, Nikolić N, Orlović S, Pilipović A, Pajević S. Exogenously Applied Citric Acid Enhances Antioxidant Defense and Phytoextraction of Cadmium by Willows (Salix Spp.). Water Air Soil Pollut. 2017;228:221. https://doi.org/10.1007/s11270-017-3405-6

Haider FU, Liqun C, Coulter JA, Cheema SA, Wu J, Zhang R, Wenjun M, Farooq M. Cadmium toxicity in plants: Impacts and remediation strategies. Ecotoxicol Environ Saf. 2021;211:111887. https://doi.org/10.1016/j.ecoenv.2020.111887

Liu L, Li W, Song W, Guo M. Remediation techniques for heavy metal-contaminated soils: Principles and applicability. Sci Total Environ. 2018;633:206-19. https://doi.org/10.1016/j.scitotenv.2018.03.161

Yan A, Wang Y, Tan SN, Mohd Yusof ML, Ghosh S, Chen Z. Phytoremediation: A Promising Approach for Revegetation of Heavy Metal-Polluted Land. Front Plant Sci. 2020;11:359. https://doi.org/10.3389/fpls.2020.00359

Angulo-Bejarano PI, Puente-Rivera J, Cruz-Ortega R. Metal and Metalloid Toxicity in Plants: An Overview on Molecular Aspects. Plants. 2021;10(4):635. https://doi.org/10.3390/plants10040635

Marmiroli M, Pietrini F, Maestri E, Zacchini M, Marmiroli N, Massacci A. Growth, physiological and molecular traits in Salicaceae trees investigated for phytoremediation of heavy metals and organics. Tree physiol. 2011;31(12):1319-34. https://doi.org/10.1093/treephys/tpr090

Borišev M, Pajević S, Nikolić N, Krstić B, Župunski M, Kebert M, Pilipović A, Orlović S. Response of Salix alba L. to heavy metals and diesel fuel contamination. Afr J Biotechnol. 2012;11:14313-9. https://doi.org/10.5897/AJB12.1004

Luković J, Merkulov L, Pajević S, Zorić L, Nikolić N, Borišev M, Karanović D. Quantitative assessment of effects of cadmium on the histological structure of poplar and willow leaves. Water Air Soil Pollut. 2012;223(6):2979-93. https://doi.org/10.1007/s11270-012-1081-0

Vaculík M, Konlechner C, Langer I, Adlassnig W, Puschenreiter M, Lux A, Hauser MT. Root anatomy and element distribution vary between two Salix caprea isolates with different Cd accumulation capacities. Environ Pollut. 2012;163:117-26. https://doi.org/10.1016/j.envpol.2011.12.031

Arsenov D, Nikolić N, Borišev M, Župunski M, Orlović S, Pilipović A, Pajević S. Greenhouse assessment of citric acid-assisted phytoremediation of cadmium by willows (Salix spp.)- effect on photosynthetic performances and metal tolerance. Balt For. 2019;25(2):203-12. https://doi.org/10.46490/vol25iss2pp203

Dos Santos Utmazian MN, Wieshammer G, Vega R, Wenzel WW. Hydroponic screening for metal resistance and accumulation of cadmium and zinc in twenty clones of willows and poplars. Environmental pollution. 2007;148(1):155-65. https://doi.org/10.1016/j.envpol.2006.10.045

Cao Y, Zhang Y, Ma C, Li H, Zhang J, Chen G. Growth, physiological responses, and copper accumulation in seven willow species exposed to Cu-a hydroponic experiment. Environ Sci Pollut Res Int. 2018;25(20):19875-86. https://doi.org/10.1007/s11356-018-2106-z

Lebrun M, Miard F, Nandillon R, Hattab-Hambli N, Scippa GS, Bourgerie S, Morabito D. Eco-restoration of a mine technosol according to biochar particle size and dose application: study of soil physico-chemical properties and phytostabilization capacities of Salix viminalis. J Soils Sediments. 2018;18(6):2188-202. https://doi.org/10.1007/s11368-017-1763-8

Lux A, Martinká M, Vaculík M, White PJ. Root responses to cadmium in the rhizosphere: a review. J Exp Bot. 2011;62(1):21-37. https://doi.org/10.1093/jxb/erq281

Kahle H. Response of roots of trees to heavy metals. Environ Exp Bot. 1993;33(1):99-119. https://doi.org/10.1016/0098-8472(93)90059-O

Rucińska-Sobkowiak R. Water relations in plants subjected to heavy metal stresses. Acta Physiol Plant. 2016;38:257. https://doi.org/10.1007/s11738-016-2277-5

Tőszér D, Magura T, Simon E. Heavy metal uptake by plant parts of willow species: a meta-analysis. J Hazard Mater. 2017;336:101-9. https://doi.org/10.1016/j.jhazmat.2017.03.068

Lux A, Šottníková A, Opatrná J, Greger M. Differences in structure of adventitious roots in Salix clones with contrasting characteristics of cadmium accumulation and sensitivity. Physiol Plant. 2004;120(4):537-45. https://doi.org/10.1111/j.0031-9317.2004.0275.x

Radziemska M, Vaverková MD, Baryła A. Phytostabilization-Management Strategy for Stabilizing Trace Elements in Contaminated Soils. Int J Environ Res Public Health. 2017;14(9):958. https://doi.org/10.3390/ijerph14090958

Yang W, Zhao F, Zhang X, Ding Z, Wang Y, Zhu Z, Yang X. Variations of cadmium tolerance and accumulation among 39 Salix clones: implications for phytoextraction. Environ Earth Sci. 2015;73(7):3263-74. https://doi.org/10.1007/s12665-014-3636-4

Hrkić Ilić Z, Pajević S, Borišev M, Luković J. Assessment of phytostabilization potential of two Salix L. clones based on the effects of heavy metals on the root anatomical traits. Environ Sci Pollut Res. 2020;27(23):29361-83. https://doi.org/10.1007/s11356-020-09228-8

Tyree MT, Ewers FW. The hydraulic architecture of trees and other woody plants. New Phytol. 1991;119(3):345-60. https://doi.org/10.1111/j.1469-8137.1991.tb00035.x

Ogasa M, Miki NH, Murakami Y, Yoshikawa K. Recovery performance in xylem hydraulic conductivity is correlated with cavitation resistance for temperate deciduous tree species. Tree Physiol. 2013;33(4):335-44. https://doi.org/10.1093/treephys/tpt010

Scholz A, Klepsch M, Karimi Z, Jansen S. How to quantify conduits in wood? Front Plant Sci. 2013;4:56. https://doi.org/10.3389/fpls.2013.00056

McElrone AJ, Pockman WT, Martinez-Vilalta J, Jackson RB. Variation in xylem structure and function in stems and roots of trees to 20 m depth. New Phytol. 2004;163:507-17. https://doi.org/10.1111/j.1469-8137.2004.01127.x

Gonçalves B, Correia CM, Silva AP, Bacelar EA, Santos A, Ferreira H, Moutinho-Pereira JM. Variation in xylem structure and function in roots and stems of scion-rootstock combinations of sweet cherry tree (Prunus avium L.). Trees. 2007;21:121-30. https://doi.org/10.1007/s00468-006-0102-2

Shah FUR, Ahmad N, Masood KR, Peralta-Videa JR, Ahmad FDA. Heavy Metal Toxicity in Plants. In: Ashraf M, Ozturk M, Ahmad MSA, editors. Plant Adaptation and Phytoremediation, Dordrecht:Springer; 2010. p. 71-97. https://doi.org/10.1007/978-90-481-9370-7_4

De Silva NDG, Cholewa E, Ryser P. Effects of combined drought and heavy metal stresses on xylem structure and hydraulic conductivity in red maple (Acer rubrum L.). J Exp Bot. 2012;63:5957-66. https://doi.org/10.1093/jxb/ers241

Gomes MP, Marques TCLL de SeM, Nogueira M de OG, Castro EM de, Soares ÂM. Ecophysiological and anatomical changes due to uptake and accumulation of heavy metal in Brachiaria decumbens. Sci Agric. 2011;68(5):566-73. https://doi.org/10.1590/S0103-90162011000500009

Poschenrieder Ch, Barcelo J. Water relations in heavy metals. In: Prasad MNV, Hagemeyer J, editors. Heavy metal stress in plants: from molecules to ecosystems. Berlin: Springer-Verlag; 1999. p. 207-29. https://doi.org/10.1007/978-3-662-07745-0_10

Almeida-Rodríguez AM, Gómes MP, Loubert-Hudon A, Joly S, Labrecque M. Symbiotic association between Salix purpurea L. and Rhizophagus irregularis: modulation of plant responses under copper stress. Tree Physiol. 2016;36(4):407-20. https://doi.org/10.1093/treephys/tpv119

Sperry JS, Nichols KL, Sullivan JEM, Eastlack SE. Xylem Embolism in Ring-Porous, Diffuse-Porous, and Coniferous Trees of Northern Utah and Interior Alaska. Ecology. 1994;75(6):1736-52. https://doi.org/10.2307/1939633

Spannl S, Homeier J, Bräuning A. Nutrient-Induced Modifications of Wood Anatomical Traits of Alchornea lojaensis (Euphorbiaceae). Front Earth Sci. 2016;4:50. https://doi.org/10.3389/feart.2016.00050

Quintana-Pulido C, Villalobos-González L, Muñoz M, Franck N, Pastenes C. Xylem structure and function in three grapevine varieties. Chil J Agric Res. 2018;78(3):419-28. https://doi.org/10.4067/S0718-58392018000300419

James SA, Meinzer FC, Goldstein G, Woodruff D, Jones T, Restom T, Mejia M, Clearwater M, Campanello P. Axial and radial water transport and internal water storage in tropical forest canopy trees. Oecologia. 2003;134:37-45. https://doi.org/10.1007/s00442-002-1080-8

Freschet GT, Pages L, Iversen CM, Comas LH, Rewald B, Roumet C, Klimesova J, Zadworny M, Poorter H, Postma JA, Adams TS, Bagniewska-Zadworna A, Bengough AG, Blancaflor EB, Brunner I, Cornelissen JHC, Garnier E, Gessler A, Hobbie SE, Meier IC, Mommer L, Picon-Cochard C, Rose L, Ryser P, Scherer-Lorenzen M, Soudzilovskaia NA, Stokes A, Sun T, Valverde-Barrantes OJ, Weemstra M, Weigelt A, Wurzburger N, York LM, Batterman SA, Gomes de Moraes M, Janecek S, Lambers H, Salmon V, Tharayil N, McCormack ML. A starting guide to root ecology: strengthening ecological concepts and standardising root classification, sampling, processing and trait measurements. New Phytol. 2021;232:973-1122. https://doi.org/10.1111/nph.17572

Mrak T, Dovč N, Gričar J, Hoshika Y, Paoletti E, Kraigher H. Poplar root anatomy after exposure to elevated O3 in combination with nitrogen and phosphorus. Trees. 2021;35:1233-45. https://doi.org/10.1007/s00468-021-02111-0

Mrak T, Gričar J. Atlas of woody plant roots. Morphology and anatomy with special emphasis on fine roots. 1st ed. Ljubljana: The Silva Slovenica Publishing Centre; 2016. 106 p. https://doi.org/10.20315/SFS.147

McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB, Leppälammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M. Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol. 2015;207:505-518. https://doi.org/10.1111/nph.13363

Strock CF, Morrow de la Riva L, Lynch JP. Reduction in Root Secondary Growth as a Strategy for Phosphorus Acquisition. Plant Physiol. 2018;176(1):691-703. https://doi.org/10.1104/pp.17.01583

Day SD, Wiseman PE, Dickinson SB, Harris JR. Contemporary Concepts of Root System Architecture of Urban Trees. Arboric Urban For. 2010;36(4):149-59. https://doi.org/10.48044/jauf.2010.020

Kirfel K, Leuschner C, Hertel D, Schuldt B. Influence of Root Diameter and Soil Depth on the Xylem Anatomy of Fine- to Medium-Sized Roots of Mature Beech Trees in the Top- and Subsoil. Front Plant Sci.2017;8:1-13. https://doi.org/10.3389/fpls.2017.01194

Schuldt, B, Leuschner C, Brock N, Horna V. Changes in wood density, wood anatomy and hydraulic properties of the xylem along the root-to-shoot flow path in tropical rainforest trees. Tree Physiol. 2013;33:161-74. https://doi.org/10.1093/treephys/tps122

Zorić L, Ljubojević M, Merkulov L, Luković J, Ognjanov V. Anatomical Characteristics of Cherry Rootstocks as Possible Preselecting Tools for Prediction of Tree Vigor. J Plant Growth Regul. 2012;31(3):320-31. https://doi.org/10.1007/s00344-011-9243-7

Zhao X. Spatial variation of vessel grouping in the xylem of Betula platyphylla Roth. J Plant Res. 2016;129:29-37. https://doi.org/10.1007/s10265-015-0768-x

Kacálková L, Tlustoš P, Száková J. Phytoextraction of Risk Elements by Willow and Poplar Trees. Int J Phytoremediation. 2015;17(5):414-21. https://doi.org/10.1080/15226514.2014.910171

Hamim H, Miftahudin M, Setyaningsih L. Cellular and ultrastructure alteration of plant roots in response to metal stress. In: Ratnadewi D, Hamim H, editors. 1st ed. Plant growth and regulation-alterations to sustain unfavorable conditions. London: IntechOpen; 2018. p. 21-41. https://doi.org/10.5772/intechopen.79110

Luković J, Krstić L, Halgašev M, Merkulov L, Nikolić N. The influence of different concentrations of cadmium on structural characteristics of poplar clones root. In: Gruev B, Nikolova M, Donev A, editors. Proceedings Of The Balkan Scientific Conference Of Biology In Plovdiv. Plovdiv: Plovdiv University Press; 2005. p. 468-74.

Zacchini M, Iori V, Mugnozza GS, Pietrini F, Massacci A. Cadmium accumulation and tolerance in Populus nigra and Salix alba. Biol Plant. 2011;55(2):383-6. https://doi.org/10.1007/s10535-011-0060-4

Balestri M, Ceccarini A, Forino LMC, Zelko I, Martinka M, Lux A, Ruffini Castiglione M. Cadmium uptake, localization and stress-induced morphogenic response in the fern Pteris vittata. Planta. 239(5):1055-64. https://doi.org/10.1007/s00425-014-2036-z

Schume H, Grabner M, Eckmüllner O. The influence of an altered groundwater regime on vessel properties of hybrid poplar. Trees. 2004;18:184-94. https://doi.org/10.1007/s00468-003-0294-7

Domec JC, Schäfer K, Oren R, Kim HS, McCarthy HR. Variable conductivity and embolism in roots and branches of four contrasting tree species and their impacts on whole-plant hydraulic performance under future atmospheric CO2 concentration. Tree Physiol. 2010; 30(8):1001-15. https://doi.org/10.1093/treephys/tpq054

Tombesi S, Johnson SR, Day KR, De Jong TM. Relationships between xylem vessel characteristics, calculated axial hydraulic conductivity and size-controlling capacity of peach rootstocks. Ann Bot. 2010;105:327-31. https://doi.org/10.1093/aob/mcp281

Loval SA, Cerrillo T, Spavento E, Caballé G, Meier AM, Monteoliva S. Wood structure, xylem functionality and growth of six Salix clones in two sites with different environmental stress in Argentina. Rev Árvore. 2018;42(1):e420110. https://doi.org/10.1590/1806-90882018000100010

Tyree M, Zimmermann M. Xylem Structure and The Ascent of Sap. 2nd ed. Berlin, Heidelberg: Springer; 2002. 284 p. https://doi.org/10.1007/978-3-662-04931-0

Lamoreaux RJ, Chaney WR. (1977). Growth and Water Movement in Silver Maple Seedlings Affected by Cadmium. Journal of Environment Quality. 1977;6(2):201-05. https://doi.org/10.2134/jeq1977.00472425000600020021x

Cai J, Tyree MT. The Impact of Vessel Size on Vulnerability Curves: Data and Models for Within-Species Variability in Saplings of Aspen, Populus tremuloides Michx. Plant Cell Environ. 2010;33(7):1059-69. https://doi.org/10.1111/j.1365-3040.2010.02127.x

Downloads

Published

2022-06-27

How to Cite

1.
Hrkić Ilić Z, Borišev M, Zorić L, Arsenov D, Luković J. Assessment of differences in anatomical and hydraulic properties of the root and xylem of three willow (Salix L.) clones during phytostabilization after exposure to elevated cadmium. Arch Biol Sci [Internet]. 2022Jun.27 [cited 2022Aug.9];74(2):169-80. Available from: https://www.serbiosoc.org.rs/arch/index.php/abs/article/view/7554

Issue

Section

Articles

Most read articles by the same author(s)