Abstract
Intensive sulphur fertilisation has been reported to improve the nutrient balance and growth of Cd-exposed plants, but the reasons of this phenomenon and the role of sulphur compounds in the resistance to cadmium are unclear. We investigated sulphur supplementation-induced changes in the surface properties of roots and the level of thiol peptides (PCs) in Cd-stressed Triticum aestivum L. (monocots clade) and Lactuca sativa L. (dicots clade) grown in nutrient solution. The combination of three sulphur (2 mM S—basic level, 6 or 9 mM S—elevated levels) and four cadmium (0, 0.0002, 0.02 or 0.04 mM Cd) concentrations was used. The physicochemical parameters of the roots were determined based on the apparent surface area (Sr), total variable surface charge (Q), cation exchange capacity (CEC) and surface charge density (SCD). In Cd-exposed plants supplied with sulphur, a different character and trend in the physicochemical changes (adsorption and ion exchange) of roots were noted. At the increased sulphur levels, as a rule, the Sr, CEC, Q and SCD values clearly increased in the lettuce but decreased in the wheat in the entire range of the Cd concentrations, except the enhanced Sr of wheat supplied with 6 mM S together with elevated (0.0002 mM) and unchanged (0.02, 0.04 mM Cd) value of this parameter at 9 mM S. This indicates a clade-specific and/or species-specific plant reaction. The 6 mM S appears to be more effective than 9 mM S in alleviation of the cadmium’s toxic effects on roots. It was found that at 0.02 and 0.04 mM Cd, the use of 6 mM S limits the Cd accumulation in the roots of both species in comparison with the basic S fertilisation. Moreover, PC accumulation was much more efficient in wheat than in lettuce, and intensive sulphur nutrition generally induced biosynthesis of these chelating compounds. Physicochemical parameters together with quantitative and qualitative assessment of thiol peptides can be important indicators of the efficiency of root system functioning under cadmium stress. The differences between the species and the multidirectional character of the changes are a result of the involvement of a number of multi-level mechanisms engaged in the defence against metal toxicity.
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References
Abedi T, Mojiri A (2020) Cadmium uptake by wheat (Triticum aestivum L): an overview. Plants (Basel) 9(4):500. https://doi.org/10.3390/plants9040500
Ahmad J, Ali AA, Baig MA, Iqbal M, Haq I, Qureshi MI (2019) Role of phytochelatins in cadmium stress tolerance in plants. In: Hasanuzzaman M, Prasad VNM, Nahar K (eds) Cadmium toxicity and tolerance in plants, from physiology to remediation,1st edn. Science Direct, Academic Press Inc., Cambridge, MA, United States, pp 185–221. https://doi.org/10.1016/B978-0-12-814864-8.00008-5
Ali E, Hussain A, Ullah I, Khan FS, Kausar S, Rashid SA, Rabbani I, Imran M, Ullah Kakar K, Shah JM, Cai M, Jiang L, Hussain N, Sun P (2020) Cadmium phytotoxicity: issues, progress, environmental concerns and future perspectives. Rev Fac Cien Agrar Univ Nac Cuyo 52(1):391–405. https://revistas.uncu.edu.ar/ojs3/index.php/RFCA/article/view/3068
Baig MA, Ahmad J, Ali AA, Qureshi MI (2019) Role of sulfur metabolism in cadmium tolerance. In: Hasanuzzaman M, MNV Prasad, Nahar K (eds) Cadmium tolerance in plants agronomic, molecular, signaling, and omic approaches, 1st edn. Academic Press, Cambridge, MA, United States, pp 335–365. https://doi.org/10.1016/B978-0-12-815794-7.00013-8
Bayçu G, Moustaka J, Gevrek N, Moustakas M (2018) Chlorophyll fluorescence imaging analysis for elucidating the mechanism of photosystem II acclimation to cadmium exposure in the hyperaccumulating plant Noccaea caerulescens. Materials 11(12):2580. https://doi.org/10.3390/ma11122580
Chen A, Komives EA, Schroeder JI (2006) An improved grafting technique for mature Arabidopsis plants demonstrates long-distance shoot-to-root transport of phytochelatins in Arabidopsis. Plant Physiol 141(1):108–120. https://doi.org/10.1104/pp.105.072637
Choppala G, Saifullah Bolan N, Bibi S, Iqbal M, Rengel Z, Kunhikrishnan A, Ashwart N, Ok YS (2014) Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Crit Rev Plant Sci 33(5):374–391. https://doi.org/10.1080/07352689.2014.903747
Cuppett SL, Mccluskey MM, Paparozzi ET, Parkhurst A (1999) Nitrogen and sulfur effects on leaf lettuce quality. J Food Qual 22(4):363–373. https://doi.org/10.1111/j.1745-4557.1999.tb00170.x
Dawuda MM, Liao W, Hu L, Yu J, Xie J, Calderón-Urrea A, Jin X, Wu Y (2019) Root tolerance and biochemical response of Chinese lettuce (Lactuca sativa L.) genotypes to cadmium stress. PeerJ 7:7530. https://doi.org/10.7717/peerj.7530
Dong J, Mao WH, Zhang GP, Wu FB, Cai Y (2007) Root excretion and plant tolerance to cadmium toxicity - a review. Plant Soil Environ 53:193–200. https://doi.org/10.17221/2205-PSE
Elgharbawy SS, Abdelhamid MIE, Mansour E, Salem AH (2021) Rapid screening wheat genotypes for tolerance to heavy metals. In: Awaad H, Abu-hashim M, Negm A (eds) Mitigating environmental stresses for agricultural sustainability in Egypt, 1st edn. Springer Nature, Springer Cham, Switzerland, pp 175–185. https://doi.org/10.1007/978-3-030-64323-2_6
Ernst WHO, Krauss GJ, Verkleij JAC, Wesenberg D (2008) Interaction of heavy metals with the sulphur metabolism in angiosperms from an ecological point of view. Plant Cell Environ 31(1):123–143. https://doi.org/10.1111/j.1365-3040.2007.01746.x
Gong JM, Lee DA, Schroeder JI (2003) Long-distance root-to-shoot transport of phytochelatins and cadmium in Arabidopsis. Proc Natl Acad Sci USA 100(17):10118–10123. https://doi.org/10.1073/pnas.1734072100
Haider FU, Liqun C, Coulter JA, Cheema SA, Wu J, Zhang R, Wenjun M, Farooq M (2021) Cadmium toxicity in plants: impacts and remediation strategies. Ecotoxicol Environ Saf 211:111887. https://doi.org/10.1016/j.ecoenv.2020.111887
Hasanuzzaman M, Bhuyan MHMB, Mahmud JA, Nahar K, Mohsin SM, Parvin K, Fujita M (2018) Interaction of sulfur with phytohormones and signalling molecules in conferring abiotic stress tolerance to plants. Plant Signal Behav 13(5):1477905. https://doi.org/10.1080/15592324.2018.1477905
Hasanuzzaman M, Prasad MNV, Nahar K (2019) Cadmium tolerance in plants: agronomic, molecular, signaling, and omic approaches, 1st edn. Academic Press, Elsevier Science & Technology, London, UK, p 630. https://doi.org/10.1016/C2017-0-03749-7
Hernández-Baranda Y, Rodríguez-Hernández P, Peña-Icart M, Meriño-Hernández Y, Cartaya-Rubio O, Postal G, San José de las Lajas M (2019) Toxicity of cadmium in plants and strategies to reduce its effects Case study: The tomato. Cult Trop 40(3):10
Hoseini SM, Zargari F (2013) Cadmium in plants: a review. Int J Farm All Sci 2(17):579–581
Hucker CA (2016) Organic amendments for reducing the plant uptake of cadmium from New Zealand soils. Ph.D. Thesis, Lincoln University, Lincoln, New Zealand
Ismael MA, Elyamine AM, Moussa MG, Cai M, Zhao X, Hu C (2019) Cadmium in plants: uptake, toxicity, and its interactions with selenium fertilizers. Metallomics 11(2):255–277. https://doi.org/10.1039/c8mt00247a
Jia H, Wang X, Dou Y, Liu D, Si W, Fang H, Zhao C, Chen S, Xi J, Li J (2016) Hydrogen sulfide-cysteine cycle system enhances cadmium tolerance through alleviating cadmium-induced oxidative stress and ion toxicity in Arabidopsis roots. Sci Rep 6(1):39702. https://doi.org/10.1038/srep39702
Jibril SA, Hassan SA, Ishak CF, Megat Wahab PE (2017) Cadmium toxicity affects phytochemicals and nutrient elements composition of lettuce (Lactuca sativa L.). Adv Agric 2017:1236830. https://doi.org/10.1155/2017/1236830
Józefaciuk G, Shin JS (1996a) A modified back-titration method to measure soil titration curves minimizing soil acidity and dilution effects. Korean J Soil Sci Fert 29(4):321–327
Józefaciuk G, Shin JS (1996b) Distribution of apparent surface dissociation constants of some Korean soils as determined from back titration curves. Korean J Soil Sci Fert 29(4):328–335
Juszczuk IM, Szal B, Rychter AM (2012) Oxidation-reduction and reactive oxygen species homeostasis in mutant plants with respiratory chain complex I dysfunction. Plant Cell Environ 35(2):296–307. https://doi.org/10.1111/j.1365-3040.2011.02314.x
Karamanos RE, Harapiak JT, Flore NA (2013) Sulphur application does not improve wheat yield and protein concentration. Can J Soil Sci 93(2):223–228. https://doi.org/10.4141/cjss2012-068
Keunen E, Remans T, Bohler S, Vangronsveld J, Cuypers A (2011) Metal-induced oxidative stress and plant mitochondria. Int J Mol Sci 12(10):6894–6918. https://doi.org/10.3390/ijms12106894
Kimura K, Yamasaki S (2001) Root length and diameter measurement using NIH Image: application of the line-intercept principle for diameter estimation. Plant Soil 234(1):37–46. https://doi.org/10.1023/A:1010501905868
Kimura K, Yamasaki S (2003) Accurate root length and diameter measurement using NIH image: use of Pythagorean distance for diameter estimation. Plant Soil 254:305–315. https://doi.org/10.1023/A:1025563602641
Kimura K, Kikuchi S, Yamasaki S (1999) Accurate root length measurement by image analysis. Plant Soil 216:117–127. https://doi.org/10.1023/A:1004778925316
Klapheck S, Fliegner W, Zimmer I (1994) Hydroxymethyl-phytochelatins [(-glutamylocysteine)n-serine] are metal-induced peptides of the Poaceae. Plant Physiol 104(4):1325–1332. https://doi.org/10.1104/pp.104.4.1325
Kosynets O, Szatanik- Kloc A, Szerement J (2012) Changes in apparent surface area of roots of ryegrass (Lolium multiflorum L.), determined by Cd stress (in Polish). Acta Agrophys 19(3):587–595
Kubier A, Wilkin RT, Pichler T (2019) Cadmium in soils and groundwater: a review. App Geochem 108:104388. https://doi.org/10.1016/j.apgeochem.2019.104388
Lu Y, Wang QN, Li J, Xiong J, Zhou LN, He SL, Zhang JG, Chen ZA, He SG, Liu H (2019) Effects of exogenous sulfur on alleviating cadmium stress in tartary buckwheat. Sci Rep 9(1):7397. https://doi.org/10.1038/s41598-019-43901-4
Lux A, Martinka M, Vaculík M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62(1):21–37. https://doi.org/10.1093/jxb/erq281
Maghrebi M, Baldoni E, Lucchini G, Vigani G, Valè G, Sacchi GA, Nocito FF (2021) Analysis of cadmium root retention for two contrasting rice accessions suggests an important role for OsHMA2. Plants (basel) 10(4):806. https://doi.org/10.3390/plants10040806
Márquez-García B, Horemans N, Torronteras R, Córdoba F (2012) Glutathione depletion in healthy cadmium-exposed Erica andevalensis. Environ Exp Bot 75(1):159–166. https://doi.org/10.1016/j.envexpbot.2011.09.009
Matraszek R, Hawrylak-Nowak B, Chwil S, Chwil M (2016) Macroelemental composition of cadmium stressed lettuce plants grown under conditions of intensive sulphur nutrition. J Environ Manag 180:24–34. https://doi.org/10.1016/j.jenvman.2016.05.017
Matraszek R, Chwil S, Hawrylak-Nowak B, Kozłowska-Strawska J (2017) Effect of sulphur and cadmium on macronutrient balance in spring wheat. Proc Natl Acad Sci India Sec B: Biol Sci 87(3):927–936. https://doi.org/10.1007/s40011-015-0658-y
Matraszek-Gawron R, Hawrylak-Nowak B (2019) Sulfur nutrition level modifies the growth, micronutrient status, and cadmium distribution in cadmium-exposed spring wheat. Physiol Mol Biol Plants 25(2):421–432. https://doi.org/10.1007/s12298-018-00635-3
Mendoza-Cózatl DG, Butko E, Springer F, Torpey JW, Komives EA, Kehr J, Schroeder JI (2008) Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus A role for thiol-peptides in the long-distance transport of cadmium and the effect of cadmium on iron translocation. Plant J 54(2):249–259. https://doi.org/10.1111/j.1365-313X.2008.03410.x
Meuwly P, Thibault P, Schwan AE, Rauser WE (1995) Three families of thiol peptides are induced by cadmium in maize. Plant J 7(3):391–400. https://doi.org/10.1046/j.1365-313x.1995.7030391.x
Mir IR, Rather BA, Masood A, Majid A, Sehar Z, Anjum NA, Sofo A, D’Ippolito I, Khan NA (2021) Soil sulfur sources differentially enhance cadmium tolerance in Indian mustard (Brassica juncea L.). Soil Syst 5(2):29. https://doi.org/10.3390/soilsystems5020029
Nederlof MM, De Wit JC, Van Riemsdijk WH, Koopal LK (1993) Determination of proton affinity distributions for humic substances. Environ Sci Technol 27(5):846–856. https://doi.org/10.1021/es00042a006
Nocito FF, Lancilli C, Crema B, Fourcroy P, Davidian JC, Sacchi GA (2006) Heavy metal stress and sulfate uptake in maize roots. Plant Physiol 141(3):1138–1148. https://doi.org/10.1104/pp.105.076240
Polish Standard PN-Z-19010–1 (1997) Soil quality. Evaluation of specific surface area with sorption of water vapor method (BET). Polish Committee for Standardization, Warsaw, Poland. [in Poilsh: Norma PN-Z-19010-1. Jakość gleby. Oznaczanie powierzchni właściwej gleb metodą sorpcji pary wodnej (BET). Polski Komitet Nonnalizncyjny, Warszawa, 1997]
Rizwan M, Ali S, Abbas T, Zia-ur-Rehman M, Hannan F, Keller C, Al-Waber MI, Ok YS (2016) Cadmium minimization in wheat: a critical review. Ecotoxicol Environ Saf 130:43–53. https://doi.org/10.1016/j.ecoenv.2016.04.001
Shen C, Fu HL, Liao Q, Huang B, Fan X, Liu XY, Xin JL, Huang YY (2021) Transcriptome analysis and physiological indicators reveal the role of sulfur in cadmium accumulation and transportation in water spinach (Ipomoea aquatica Forsk.). Ecotoxicol Environ Saf 225:112787. https://doi.org/10.1016/j.ecoenv.2021.112787
Song X, Yue X, Chen W, Jiang H, Han Y, Li X (2019) Detection of cadmium risk to the photosynthetic performance of Hybrid Pennisetum. Front Plant Sci 10:798. https://doi.org/10.3389/fpls.2019.00798
Szatanik-Kloc A (2016) Changes in the size of the apparent surface area and adsorption energy of the rye roots by low pH and the presence of aluminium ions induced. Int Agrophys 30(3):375–381. https://doi.org/10.1515/intag-2016-0008
Szatanik-Kloc A, Sokołowska Z, Hrebelna N (2007) Effect of pH under Cd-stress on surface charge of barley (Hordeum vulgare L.) (in Polish). Acta Agrophys 10(2):473–482
Szatanik-Kloc A, Sokołowska Z, Hrebelna N (2007b) Effect of Pb-stress on selected physicochemical surface properties of barley (Hordeum vulgare L.) roots. Int Agrophys 21:399–405
Szatanik-Kloc A, Boguta P, Bowanko G (2009a) Effect of aluminium ions on free surface area andenergetic characteristics of barley and clover roots. Int Agrophys 23(4):383–389
Szatanik-Kloc A, Warchulska P, Józefaciuk G (2009) Changes in variable charge and acidity of rye (Secale cereal L.) roots surface under Zn-stress. Acta Physiol Plant 31(1):59–64. https://doi.org/10.1007/s11738-008-0200-4
Szatanik-Kloc A, Szerement J, Józefaciuk G (2017) The role of cell walls and pectins in cation exchange and surface area of plant roots. J Plant Physiol 215:85–90. https://doi.org/10.1016/j.jplph.2017.05.017
Szatanik-Kloc A (2010) Changes in the surface properties of plant root determined by aluminium and copper phytotoxicity (in Polish). Habilitation thesis no. 176, Institute of Agrophysics Polish Academy of Sciences in Lublin, Poland, Acta Agrophys, pp. 122
Ullah S, Khan J, Hayat K, Abdelfattah Elateeq A, Salam U, Yu B, Ma Y, Wang H, Tang ZH (2020) Comparative study of growth, cadmium accumulation and tolerance of three chickpea (Cicer arietinum L.) cultivars. Plants (Basel) 9(3):310. https://doi.org/10.3390/plants9030310
Van Riemsdijk WH, Koopal LK, De Wit JCM (1987) Heterogeneity and electrolyte adsorption: intrinsic and electrostatic effects. Neth J Soil Sci 35(3):241–257. https://doi.org/10.18174/njas.v35i3.16722
Wójcik M, Tukendorf A (1999) Cd-tolerance of maize, rye and wheat seedlings. Acta Physiol Plant 21:99–107. https://doi.org/10.1007/s11738-999-0063-3
Wu Q, Su N, Chen Q, Shen W, Shen Z, Xia Y, Cui J (2015) Cadmium-induced hydrogen accumulation is involved in cadmium tolerance in Brassica campestris by reestablishment of reduced glutathione homeostasis. PLoS ONE 10(10):0139956. https://doi.org/10.1371/journal.pone.0139956
Zhao H, Guan J, Liang Q, Zhang X, Hu H, Zhang J (2021) Effects of cadmium stress on growth and physiological characteristics of sassafras seedlings. Sci Rep 11:9913. https://doi.org/10.1038/s41598-021-89322-0
Zhou X, Zhao C, Sun J, Cao Y, Fu L (2021) Classification of heavy metal Cd stress in lettuce leaves based on WPCA algorithm and fluorescence hyperspectral technology. Infrared Phys Technol 119:103936. https://doi.org/10.1016/j.infrared.2021.103936
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Renata Matraszek Gawron: conceptualization, methodology, formal analysis, investigation, writing—original draft preparation, writing—review and editing, visualization, supervision. Barbara Hawrylak-Nowak: conceptualization, methodology, formal analysis, investigation, writing—original draft preparation, writing—review and editing, visualization, supervision. Katarzyna Rubinowska: methodology, formal analysis, investigation, writing—review and editing.
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Matraszek-Gawron, R., Hawrylak-Nowak, B. & Rubinowska, K. The effect of sulphur supplementation on cadmium phytotoxicity in wheat and lettuce: changes in physiochemical properties of roots and accumulation of phytochelatins. Environ Sci Pollut Res 31, 16375–16387 (2024). https://doi.org/10.1007/s11356-024-32259-4
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DOI: https://doi.org/10.1007/s11356-024-32259-4