Abstract
The indiscriminate use of fertilizers and chemical pesticides can lead to boron contamination of the soil. Decontamination in general is expensive and results in other impacts. Phytoremediation is a sustainable alternative for soil restoration. Astronium fraxinifolium Schott (Anacardiaceae) is a tree species native to the Cerrado that is considered to be a pioneer species and a selective xerophyte, and it has been widely used in the reforestation and restoration of degraded areas. This study set out to characterize the physiology and anatomy of A. fraxinifolium under different boron concentrations and to assess the tolerance and phytoremediation potential of the species. An experiment with a completely randomized design was conducted in a greenhouse. The carbon allocation and chlorophyll content of leaves of A. fraxinifolium were determined. Boron concentration and the species’ tolerance index were calculated from root and shoot samples. Levels of amino acids, proteins, total carbohydrates, starch, phenolic compounds, and anatomical analysis were also measured. A. fraxinifolium showed tolerance to boron concentrations in the substrate and accumulated a greater amount of the element in the aerial part, showing its phytoextraction ability. No significant differences were found in the physiology of A. fraxinifolium; however, some anatomical changes were observed. In the leaves, there were changes in the thickness of the abaxial surface of the epidermis and palisade and spongy parenchyma, and total leaf thickness, and in the roots, there were changes in the thickness of the phloem, diameter of vessel elements, and number of vessel elements per square millimeter. However, boron did not interfere in the development and survival of A. fraxinifolium, which points to the possibility that the species has phytoremediation potential.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Accioly AMA, Siqueira JO (2000) Contaminação química e biorremediação do solo. In: Novais RF, Alvarez VH, Schaefer CE (eds) Tópicos Em Ciência Do Solo. Sociedade Brasileira de Ciência do Solo, Viçosa, pp 299–352
Allende KL, Fletcher TD, Sun G (2012) The effect of substrate media on the removal of arsenic, boron and iron from an acidic wastewater in planted column reactors. Chem Eng J 179:119–130. https://doi.org/10.1016/j.cej.2011.10.069
Appezzato-da-Glória B, Carmello-Guerreiro SM (2006) Anatomia Vegetal. UFV, Viçosa
Araujo MA, Leite MCM, Camargos LS, Martins AR (2020) Tolerance evaluation and morphophysiological responses of Astronium graveolens, a native Brazilian Cerrado, to addition of lead in soil. Ecotoxicol Environ Saf 195:110524. https://doi.org/10.1016/j.ecoenv.2020.110524
Aydın M, Kustutan F (2009) Research on weed species for phytoremediation of boron polluted soil. African J Biotechnol 8(18):4514–4518
Babaoǧlu M, Gezgin S, Topal A et al (2004) Gypsophila sphaerocephala Fenzl ex Tchihat.: A boron hyperaccumulator plant species that may phytoremediate soils with toxic b levels. Turk J Botany 28:273–278
Bieleski RL, Turner NA (1966) Separation and estimation of amino acids in crude plant extracts by thin-layer electrophoresis and chromatography. Anal Biochem 17:278–293. https://doi.org/10.1016/0003-2697(66)90206-5
Blevins DG, Lukaszewski KM (1998) Boron in plant structure and function. Annu Rev Plant Biol 49:481–500
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Brandão MCS, Martins FM, Accioly AMA et al (2018) Phytoremediation potential and morphological changes of plants growing in the vicinity of lead smelter plant. Int J Environ Sci Technol 15:361–372. https://doi.org/10.1007/s13762-017-1403-2
Callegari et al (2017) Oxidant and antioxidant compounds, gas exchange and growth of young Schizolobium parahyba var. amazonicum plants under high boron and calcium concentrations. Emirates J Food Agric 29:994–1002. https://doi.org/10.9755/ejfa.2017.v29.i12.1571
Camacho-Cristóbal JJ, Rexach J, González-Fontes A (2008) Boron in plants: deficiency and toxicity. J Integr Plant Biol 50:1247–1255. https://doi.org/10.1111/j.1744-7909.2008.00742.x
Carolyn Watson M, Banuelos GS, O’Leary JW, Riley JJ (1994) Trace element composition of Atriplex grown with saline drainage water. Agric Ecosyst Environ 48:157–162. https://doi.org/10.1016/0167-8809(94)90086-8
Çelik H, Turan MA, Aşık BB et al (2019) Effects of soil-applied materials on the dry weight and boron uptake of maize shoots (Zea Mays L.) under high boron conditions. Commun Soil Sci Plant Anal 50:811–826. https://doi.org/10.1080/00103624.2019.1589477
Çöl M, Çöl C (2003) Environmental boron contamination in waters of Hisarcik area in the Kutahya Province of Turkey. Food Chem Toxicol 41:1417–1420. https://doi.org/10.1016/S0278-6915(03)00160-1
Costa BGP, Justino GC, Aguiar LF et al (2019) Boron phytoremediation: Stizolobium aterrimum is tolerant and can be used for phytomanagement of boron excess in soils. Int J Environ Stud 76:329–337. https://doi.org/10.1080/00207233.2018.1497883
Craw D, Rufaut CG, Haffert L, Todd A (2006) Mobilisation and attenuation of boron during coal mine rehabilitation, Wangaloa, New Zealand. Sci Total Environ 368:444–455. https://doi.org/10.1016/j.scitotenv.2006.04.020
da Silva EA, Cassiolato AMR, Maltoni KL, Scabora MH (2008) Efeitos da rochagem e de resíduos orgânicos sobre aspectos químicos e microbiológicos de um subsolo exposto e sobre o crescimento de Astronium fraxinifolium Schott. Rev Árvore 32:323–333. https://doi.org/10.1590/S0100-67622008000200015
da Silva TJ, Hansted FAS, Tonello PS, Goveia D (2019) Phytoremediation of soils contaminated with metals: current outlook and prospects of use of forest species. Rev Virtual Quím 11:18–34. https://doi.org/10.21577/1984-6835.20190003
Dey A, Dwivedi BS, Meena MC, Datta SP (2013) Adsorption-desorption of boron in major soils of India. J Indian Soc Soil Sci 61:179–187
de Miranda LPM, Tarsitano MAA, Alves MC, Rodrigues RAF (2011) Custo para implantação de Astronium fraxinifolium Schott em área degradada utilizando-se adubos verdes e lodo de esgoto. Pesq Agrop Trop 41. https://doi.org/10.5216/pat.v41i4.10053
de Oliveira PC, Dutra AM, Ceruti FC (2012) Qualidade das Águas Superficiais e o Uso da Terra: Estudo de Caso Pontual em Bacia Hidrográfica do Oeste do Paraná. Floresta Ambient 19:32–43. https://doi.org/10.4322/floram.2012.005
DeLong C, Cruse R, Wiener J (2015) The soil degradation paradox: compromising our resources when we need them the most. Sustainability 7:866–879. https://doi.org/10.3390/su7010866
dos Santos GCG, Rodella AA (2007) Efeito da adição de fontes de matéria orgânica como amenizantes do efeito tóxico de B, Zn, Cu, Mn e Pb no cultivo de Brassica juncea. Rev Bras Ciência do Solo 31:793–804. https://doi.org/10.1590/S0100-06832007000400019
Dridi I, Tlili A, Fatnassi S et al (2018) Effects of boron distribution on sugar beet crop yield in two Tunisian soils. Arab J Geosci 11:400. https://doi.org/10.1007/s12517-018-3741-x
Farias MSS et al (2007) Avaliação dos níveis de boro e chumbo na água do Rio Cabelo – João Pessoa –PB. Engenharia Ambiental, Espírito Santo do Pinhal 4:024–031
Folin O, Ciocalteu V (1927) On tyrosine and tryptophan determination proteins. J Biol Chem 73:627–650
Goldbach HE, Wimmer MA (2007) Boron in plants and animals: is there a role beyond cell-wall structure? J Plant Nutr Soil Sci 170:39–48. https://doi.org/10.1002/jpln.200625161
Gomes MP, Marques TCLLSM, Carneiro MMLC, Soares ÂM (2012) Anatomical characteristics and nutrient uptake and distribution associated with the Cd-phytoremediation capacity of Eucalyptus camaldulenses Dehnh. J Soil Sci Plant Nutr 12(3):481–496. https://doi.org/10.4067/S0718-95162012005000010
Huang J-H, Cai Z-J, Wen S-X et al (2014) Effects of boron toxicity on root and leaf anatomy in two Citrus species differing in boron tolerance. Trees 28:1653–1666. https://doi.org/10.1007/s00468-014-1075-1
Johansen DA (1940) Plant microtechnique. McGraw-Hill, New York
Kitamura AE, Alves MC, Suzuki LGAS, Paz Gonzalez A (2008) Recuperação de um solo degradado com a aplicação de adubos verdes e lodo de esgoto. Rev Bras Ciênc Solo 32:405–416. https://doi.org/10.1590/S0100-06832008000100038
Leblebici S, Unal D (2017) Response of Triticum aestivum L. to boron stress. Russ J Plant Physiol 64:869–875. https://doi.org/10.1134/S1021443717060073
Leite UT et al (2003) Níveis críticos foliares de Boro, Cobre, Manganês e Zinco em milho. Bioscience Journal 19:115–125
Liu C, Dai Z, Cui M et al (2018) Arbuscular mycorrhizal fungi alleviate boron toxicity in Puccinellia tenuiflora under the combined stresses of salt and drought. Environ Pollut 240:557–565. https://doi.org/10.1016/j.envpol.2018.04.138
Lorenzi H (2002) Árvores Brasileiras, 4th edn. Instituto Plantarum, Nova Odessa
Menezes JM, Prado RB, da Silva Júnior GC et al (2009) Qualidade da água e sua relação espacial com as fontes de contaminação antrópicas e naturais: bacia hidrográfica do rio São Domingos - RJ. Eng Agrícola 29:687–698. https://doi.org/10.1590/S0100-69162009000400019
Metwally AM, Radi AA, El-Shazoly RM, Hamada AM (2018) The role of calcium, silicon and salicylic acid treatment in protection of canola plants against boron toxicity stress. J Plant Res 131:1015–1028. https://doi.org/10.1007/s10265-018-1008-y
Miwa K, Takano J, Omori H et al (2007) Plants tolerant of high boron levels. Science (80- ) 318:1417. https://doi.org/10.1126/science.1146634
Moraga NB, Amoroso MJ, Rajal VB (2014) Strategies to ameliorate soils contaminated with boron compounds. In: Bioremediation in Latin America. Springer International Publishing, Cham, pp 41–51
Nable RO, Banuelos GS, Paul JG (1997) Boron toxicity. Plant Soil 193:181–198. https://doi.org/10.1023/A:1004272227886
Niaz A et al (2016) Impacts of residual boron on wheat applied to previous cotton crop under alkaline calcareous soils of Punjab. Sci Lett 4:33–39
Paixão AP, Junior EF, Hiraki SS et al (2017) Crescimento, fotossíntese e atividade enzimática de genótipos de algodoeiro herbáceo submetidos ao cloreto de mepiquat. Cult Agronôm Rev Ciênc Agronôm 26:540–553. https://doi.org/10.32929/2446-8355.2017v26n4p540-553
Pawlowski ML, Helfenstein J, Frossard E, Hartman GL (2019) Boron and zinc deficiencies and toxicities and their interactions with other nutrients in soybean roots, leaves, and seeds. J Plant Nutr 42:634–649. https://doi.org/10.1080/01904167.2019.1567782
Powell RL, Kimerle RA, Coyle GT, Best GR (1997) Ecological risk assessment of a wetland exposed to boron. Environ Toxicol Chem 16:2409–2414. https://doi.org/10.1002/etc.5620161129
Rámila CDP, Leiva ED, Bonilla CA et al (2015) Boron accumulation in Puccinellia frigida, an extremely tolerant and promising species for boron phytoremediation. J Geochem Explor 150:25–34. https://doi.org/10.1016/j.gexplo.2014.12.020
Rocha Filho JV d C, Haag HP, de Oliveira GD, Sarruge JR (1979) Influência do boro no crescimento e na composição química de Eucalyptus grandis. An da Esc Super Agric Luiz Queiroz 36:139–152. https://doi.org/10.1590/S0071-12761979000100009
Sakai WS (1973) Simple method for differential staining of paraffin embedded plant material using toluidine blue O. Stain Technol 48:247–249. https://doi.org/10.3109/10520297309116632
Salvador JO, Moreira A, Malavolta E, Cabral CP (2003) Influência do boro e do manganês no crescimento e na composição mineral de mudas de goiabeira. Ciênc Agrotecnol 27:325–331. https://doi.org/10.1590/S1413-70542003000200011
Samet H, Çıkılı Y (2019) Response of purslane (Portulaca oleracea L.) to excess boron and salinity: physiological approach. Russ J Plant Physiol 66:316–325. https://doi.org/10.1134/S1021443719020110
Sang W, Huang Z-R, Qi Y-P et al (2015) An investigation of boron-toxicity in leaves of two citrus species differing in boron-tolerance using comparative proteomics. J Proteome 123:128–146. https://doi.org/10.1016/j.jprot.2015.04.007
Sarafi E, Tsouvaltzis P, Chatzissavvidis C et al (2017) Melatonin and resveratrol reverse the toxic effect of high boron (B) and modulate biochemical parameters in pepper plants (Capsicum annuum L.). Plant Physiol Biochem 112:173–182. https://doi.org/10.1016/j.plaphy.2016.12.018
Schoderboeck L, Mühlegger S, Losert A et al (2011) Effects assessment: boron compounds in the aquatic environment. Chemosphere 82:483–487. https://doi.org/10.1016/j.chemosphere.2010.10.031
Sorreano MCM, Rodrigues RR, Boaretto AE (2012) Guia de nutrição de plantas para espécies florestais nativas. Oficina de Textos, São Paulo
Tombuloglu H, Tombuloglu G, Sakcali MS et al (2017) Proteomic analysis of naturally occurring boron tolerant plant Gypsophila sphaerocephala L. in response to high boron concentration. J Plant Physiol 216:212–217. https://doi.org/10.1016/j.jplph.2017.06.013
Türker OC, Böcük H, Yakar A (2013) The phytoremediation ability of a polyculture constructed wetland to treat boron from mine effluent. J Hazard Mater 252–253:132–141. https://doi.org/10.1016/j.jhazmat.2013.02.032
Türker OC, Vymazal J, Türe C (2014) Constructed wetlands for boron removal: a review. Ecol Eng 64:350–359. https://doi.org/10.1016/j.ecoleng.2014.01.007
Veloso CAC, Muraoka T, Malavolta E, de Carvalho JG (1995) Influência do manganês sobre a nutrição mineral e crescimento da pimenteira do reino (Piper nigrum L.). Sci Agric 52:376–383. https://doi.org/10.1590/S0103-90161995000200028
Wilkins DA (1978) The measurement of tolerance to edaphic factors by means of root growth. New Phytologist 80:623–633. https://doi.org/10.1111/j.1469-8137.1978.tb01595.x
Yao Z, Li J, Xie H, Yu C (2012) Review on remediation technologies of soil contaminated by heavy metals. Procedia Environ Sci 16:722–729. https://doi.org/10.1016/j.proenv.2012.10.099
Ye ZH, Lin Z-Q, Whiting SN et al (2003) Possible use of constructed wetland to remove selenocyanate, arsenic, and boron from electric utility wastewater. Chemosphere 52:1571–1579. https://doi.org/10.1016/S0045-6535(03)00497-1
Yemm EW, Cocking EC (1955) The determination of amino-acids with ninhydrin. Analyst 80:209–214. https://doi.org/10.1039/AN9558000209
Zago VCP, das Dores NC, Watts BA (2019) Strategy for phytomanagement in an area affected by iron ore dam rupture: a study case in Minas Gerais State, Brazil. Environ Pollut 249:1029–1037. https://doi.org/10.1016/j.envpol.2019.03.060
Zhao F-J, McGrath SP (2009) Biofortification and phytoremediation. Curr Opin Plant Biol 12:373–380. https://doi.org/10.1016/j.pbi.2009.04.005
Zhen M, Cui M, Xia J et al (2019) Effect of nitrogen and phosphorus on alleviation of boron toxicity in Puccinellia tenuiflora under the combined stresses of salt and drought. J Plant Nutr 42:1594–1604. https://doi.org/10.1080/01904167.2019.1628982
Acknowledgements
The authors are thankful for the financial support received by the “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq) and the “Fundação de Amparo à Pesquisa do Estado de São Paulo” (FAPESP).
Funding
This study was funded by the National Council for Scientific and Technological Development [CNPq-Brazil, process number 130355/2018-6] and the São Paulo Research Foundation [FAPESP-Brazil, process number 2018/01498-6].
Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Author information
Authors and Affiliations
Contributions
Marilaine Cristina Marques Leite—conduction, collecting data, statistical analysis, and organization and discussion of data.
Maycon Anderson de Araujo—conduction, collecting data, and discussion of data.
Wesller da Silva de Paiva—conduction, collecting data, and discussion of data.
Liliane Santos Camargos—adviser, organization and discussion of data.
Aline Redondo Martins—adviser, organization and discussion of data (leader of the research group).
Corresponding author
Ethics declarations
Ethical approval
Not applicable.
Consent to participate
Not applicable.
Consent to publish
Not applicable.
Competing interests
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
Leite, M.C.M., de Araujo, M.A., da Silva de Paiva, W. et al. Morphological responses and tolerance of a tree native to the Brazilian Cerrado Astronium fraxinifolium Schott to boron toxicity. Environ Sci Pollut Res 29, 6900–6910 (2022). https://doi.org/10.1007/s11356-021-15710-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-15710-8