Abstract
The ability to accumulate and tolerate high levels of Al has been reported in relatively few plant families. Up to date there is no report on the Al tolerance or accumulation neither in members of Amaranthaceae nor in the order (Caryophyllales). In this work, we collected three Amaranthus species (A. blitoides, A. retroflexus and A. blitum ) growing as weed on acid soils of tea gardens (pH 4.4–4.7) in the north Iran and analyzed for Al. The Al accumulation in the leaves of collected plants and those grown hydroponically for four weeks with 400 µM Al (125 µM free Al3+ activity) exceeded the critical level of Al accumulation (1 mg g–1 DW). A. blitoides was further studied for Al tolerance mechanisms. Shoot and root biomass and root length were stimulated by 50 µM Al accompanied by improvement of C4 photosynthesis and N uptake and assimilation. The growth of plants was slightly repressed under higher Al (400 µM) exposure accompanied by activation of antioxidant defense system and lignin deposition. A high resistance to toxic Al concentration in A. blitoides was associated with elevated levels of phenolics accumulation and exudation suggesting the contribution of these compounds to both the avoidance and the internal detoxification mechanisms in this species. This is the first report on Al accumulation in Amaranthus species and the results are of interest from the botanical, physiological and ecological points of view.
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References
Adegbola PI, Adetutu A, Olaniyi TD (2020) Antioxidant activity of Amaranthus species from the Amaranthaceae family–A review. South Afr J Bot 133:111–117. https://doi.org/10.1016/j.sajb.2020.07.003
Arroyave C, Tolrà R, Thuy T, Barceló J, Poschenrieder C (2013) Differential aluminum resistance in Brachiaria species. Environ Exp Bot 89:11–18. https://doi.org/10.1016/j.envexpbot.2013.01.001
Ashton AR, Burnell JN, Furbank RT, Jenkins CL, Hatch MD (1990) Enzymes of C4 photosynthesis. In: Lea PJ (ed) Methods in plant biochemistry, vol. 3. Academic Press, San Diego, pp 39–72. https://doi.org/10.1016/B978-0-12-461013-2.50010-1
Assad R, Reshi ZA, Jan S, Rashid I (2017) Biology of amaranths. Bot Rev 83:382–436. https://doi.org/10.1007/s12229-017-9194-1
Assadi M, Massoumi AA, Khatamsaz M, Mozaffrian V (eds) (1988–2011) Flora of Iran. Research institute of forests and rangelands publication. Tehran, pp 1–73 (In Persian). https://doi.org/10.22092/IRN.2019.119036
Barceló J, Poschenrieder C (2002) Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: a review. Environ Exp Bot 48:75–92. https://doi.org/10.1016/S0098-8472(02)00013-8
Barceló J, Poschenrieder CH, Vázquez MD, Gunsé B (1995) Aluminium phytotoxicity. Fertil Res 43:217–223. https://doi.org/10.1007/BF00747705
Blamey FP (2003) A role for pectin in the control of cell expansion. Soil Sci Plant Nutr 49:775–783. https://doi.org/10.1080/00380768.2003.10410339
Bojórquez-Quintal E, Escalante-Magaña C, Echevarría-Machado I, Martínez-Estévez M (2017) Aluminum, a friend or foe of higher plants in acid soils. Front Plant Sci 8:1767. https://doi.org/10.3389/fpls.2017.01767
Boscolo PR, Menossi M, Jorge RA (2003) Aluminum-induced oxidative stress in maize. Phytochemistry 62:181–189. https://doi.org/10.1016/S0031-9422(02)00491-0
Bressan AC, de Oliveira Carvalho Bittencourt BM, Silva GS, Habermann G (2021) Could the absence of aluminum (Al) impair the development of an Al-accumulating woody species from Brazilian savanna? Theor Exp Plant Physiol 33:281–292. https://doi.org/10.1007/s40626-021-00216-y
Campbell TA, Foy CD (1987) Selection of grain Amaranthus species for tolerance to excess aluminum in an acid soil. J Plant Nutr 10:249–260. https://doi.org/10.1080/01904168709363570
Casado-Vela J, Sellés S, Bru R (2005) Purification and kinetic characterization of polyphenol oxidase from tomato fruits (Lycopersicon esculentum cv. Muchamiel). J Food Biochem 29:381–401. https://doi.org/10.1111/j.1745-4514.2005.00037-x
Chance B, Maehly AC (1955) Assay of catalase and peroxidases. Methods Enzymol 2:764–775. https://doi.org/10.1002/9780470110171.ch14
Chenery EM (1948) Aluminum in the plant world. Part I, general survey in dicotyledons. Kew Bull 3:173–183. https://doi.org/10.2307/4109057
De Andrade LR, Barros LM, Echevarria GF, Do Amaral LI, Cotta MG, Rossatto DR, Haridasan M, Franco AC (2011) Al-hyperaccumulator Vochysiaceae from the Brazilian Cerrado store aluminum in their chloroplasts without apparent damage. Environ Exp Bot 70:37–42. https://doi.org/10.1016/j.envexpbot.2010.05.013
de Souza MC, Lima RA, Poschenrieder C, Tolrà R, Da Costa FB (2018a) Fingerprinting metabolomics in tropical mistletoes: a case study with facultative aluminum-accumulating species. Phytochem Lett 25:90–94. https://doi.org/10.1016/j.phytol.2018.04.013
de Souza MC, Scalon M, Poschenrieder C, Tolrà R, Venâncio T, Teixeira S, Da Costa F (2018b) Aluminium detoxification in facultative (Passovia ovata (Pohl ex DC.) Kuijt and Struthanthus polyanthus Mart. - Loranthaceae) and dependent (Psittacanthus robustus (Mart.) Marloth - Loranthaceae) Al-accumulating mistletoe species from the Brazilian savanna. Phytochemistry 153:58–63. https://doi.org/10.1016/j.phytochem.2018.05.020
Del Río-Celestino M, Font R, Moreno-Rojas R, De Haro-Bailón A (2006) Uptake of lead and zinc by wild plants growing on contaminated soils. Ind Crops Prod 24:230–237. https://doi.org/10.1016/S0031-9422(02)00491-0
Dickerson DP, Pascholati SF, Hagerman AE, Butler LG, Nicholson RL (1984) Phenylalanine ammonia-lyase and hydroxycinnamate: CoA ligase in maize mesocotyls inoculated with Helminthosporium maydis or Helminthosporium carbonum. Physiol Plant Pathol 25:111–123. https://doi.org/10.1016/0048-4059(84)90050-X
Doncheva S, Amenós M, Poschenrieder C, Barceló J (2005) Root cell patterning: a primary target for aluminum toxicity in maize. J Exp Bot 56:1213–1220. https://doi.org/10.1093/jxb/eri115
Fan W, Xu JM, Lou HQ, Xiao C, Chen WW, Yang JL (2016) Physiological and molecular analysis of aluminium-induced organic acid anion secretion from grain amaranth (Amaranthus hypochondriacus L.) roots. Int J Mol Sci 17:608. https://doi.org/10.3390/ijms17050608
Fini A, Brunetti C, Di Ferdinando M, Ferrini F, Tattini M (2011) Stress-induced flavonoid biosynthesis and the antioxidant machinery of plants. Plant Signal Behav 6:709–711. https://doi.org/10.4161/psb.6.5.15069
Foy CD, Campbell TA (1984) Differential tolerances of Amaranthus strains to high levels of aluminum and manganese in acid soils. J Plant Nutr 7:1365–1388. https://doi.org/10.1080/01904168409363287
Foyer CH, Parry M, Noctor G (2003) Markers and signals associated with nitrogen assimilation in higher plants. J Exp Bot 54:585–593. https://doi.org/10.1093/jxb/erg053
Gavassi MA, Dodd IC, Puértolas J, Silva GS, Carvalho RF, Habermann G (2020) Aluminum-induced stomatal closure is related to low root hydraulic conductance and high ABA accumulation. Environ Exp Bot 179:104233. https://doi.org/10.1016/j.envexpbot.2020.104233
Ghanati F, Morita A, Yokota H (2005) Effects of aluminum on the growth of tea plant and activation of antioxidant system. Plant Soil 276:133–141. https://doi.org/10.1007/s11104-005-3697-y
Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in Higher. Plants Plant Physiol 59:309–314. https://doi.org/10.1104/pp.59.2.309
Hajiboland R, Poschenrieder C (2015) Localization and compartmentation of Al in the leaves and roots of tea plants. Phyton 84:86–100. https://doi.org/10.32604/phyton.2015.84.086
Hajiboland R, Bahrami Rad S, Barceló J, Poschenrieder C (2013a) Mechanisms of aluminum-induced growth stimulation in tea (Camellia sinensis). J Plant Nutr Soil Sci 176:616–625. https://doi.org/10.1002/jpln.201200311
Hajiboland R, Barceló J, Poschenrieder C, Tolrá R (2013b) Amelioration of iron toxicity: a mechanism for aluminum-induced growth stimulation in tea plants. J Inorg Biochem 128:183–187. https://doi.org/10.1016/j.jinorgbio.2013.07.007
Hajiboland R, Bastani S, Bahrami-Rad S, Poschenrieder C (2015) Interactions between aluminum and boron in tea (Camellia sinensis) plants. Acta Physiol Plant 37:1–3. https://doi.org/10.1007/s11738-015-1803-1
Hajiboland R, Panda CK, Lastochkina O, Gavassi MA, Habermann G, Pereira JF (2022) Aluminum toxicity in plants: present and future. J Plant Growth Regul 28:1–33. https://doi.org/10.1007/s00344-022-10866-0
Haridasan M (1982) Aluminium accumulation by some cerrado native species of central Brazil. Plant Soil 65:265–273. https://doi.org/10.1007/BF02374657
Haridasan M (2008) Nutritional adaptations of native plants of the cerrado biome in acid soils. Braz J Plant Physiol 20:183–195. https://doi.org/10.1590/S1677-04202008000300003
Hawkesford M, Horst W, Kichey T, Lambers H, Schjoerring J, Møller IS, White P (2012) Functions of macronutrients. In: Marschner, P (ed) Marschner’s mineral nutrition of higher plants. Academic Press, London, pp 135–189. https://doi.org/10.1016/B978-0-12-384905-2.00006-6
Hodges DM, Delong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acidreactive- substances assay for estimating lipid peroxidation in plant tissue containing anthocyanin and other interfering compounds. Planta 207:604–611. https://doi.org/10.1007/s004250050524
Hoekenga OA, Magalhaes JV (2011) Mechanisms of aluminum tolerance. In: Costa de Oliveira A, Varshney R (eds) Root Genomics. Springer, Berlin, p 133–153. https://doi.org/10.1007/978-3-540-85546-0_6
Husted S, Hebbern CA, Mattsson M, Schjoerring JK (2000) A critical experimental evaluation of methods for determination of NH4+ in plant tissue, xylem sap and apoplastic fluid. Physiol Plant 109:167–179. https://doi.org/10.1034/j.1399-3054.2000.100209.x
Jahed RR, Hosseini SM, Kooch Y (2014) The effect of natural and planted forest stands on soil fertility in the Hyrcanian region. Iran. Biodiversitas: J Biol Divers 15:206–214. https://doi.org/10.13057/biodiv/d150213
Jansen S, Broadley MR, Robbrecht E, Smets E (2002a) Aluminum hyperaccumulation in angiosperms: a review of its phylogenetic significance. Bot Rev 68:235–269. https://doi.org/10.1663/0006-8101(2002)068[0235:AHIAAR]2.0.CO;2
Jansen S, Watanabe T, Smets E (2002b) Aluminium accumulation in leaves of 127 species in Melastomataceae, with comments on the order Myrtales. Ann Bot 90:53–64. https://doi.org/10.1093/aob/mcf142
Jaworski EG (1971) Nitrate reductase assay in intact plant tissues. Biochem Biophys Res Commun 43:1274–1279. https://doi.org/10.1016/S0006-291X(71)80010-4
Johnson CM, Stout PR, Broyer TC, Carlton AB (1957) Comparative chloride requirements of different plant species. Plant Soil 8:337–353. https://doi.org/10.1007/BF01666323
Junglee S, Urban L, Sallanon H, Lopez-Lauri F (2014) Optimized assay for hydrogen peroxide determination in plant tissue using potassium iodide. Am J Anal Chem 5:730–736. https://doi.org/10.4236/ajac.2014.51108
Kidd PS, Llugany M, Poschenrieder CH, Gunse B, Barcelo J (2001) The role of root exudates in aluminium resistance and silicon‐induced amelioration of aluminium toxicity in three varieties of maize (Zea mays L.). J Exp Bot 52:1339–1352. https://doi.org/10.1093/jexbot/52.359.1339
Kigel J (1994) Development and ecophysiology of Amaranths. In: Paredes-Lopez O (ed) Amaranth biology, chemistry and technology. CRC Press, Boca Raton, pp 39–73. https://doi.org/10.1201/9781351069601-4
Kochian LV, Piñeros MA, Liu J, Magalhaes JV (2015) Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu Rev Plant Biol 66:571–598. https://doi.org/10.1146/annurev-arplant-043014-114822
Kollmeier M, Felle HH, Horst WJ (2000) Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum? Plant Physiol 122:945–956. https://doi.org/10.1104/pp.122.3.945
Lambers H, de Britto CP, Oliveira RS, Silveira FA (2020) Towards more sustainable cropping systems: lessons from native Cerrado species. Theor Exp Plant Physiol 32:175–194. https://doi.org/10.1007/s40626-020-00180-z
Liu Q, Luo L, Zheng L (2018) Lignins: biosynthesis and biological functions in plants. Int J Mol Sci 19:335. https://doi.org/10.3390/ijms19020335
Manquián-Cerda K, Cruces E, Escudey M, Zúñiga G, Calderón R (2018) Interactive effects of aluminum and cadmium on phenolic compounds, antioxidant enzyme activity and oxidative stress in blueberry (Vaccinium corymbosum L.) plantlets cultivated in vitro. Ecotoxicol Environ Safety 150:320–326. https://doi.org/10.1016/j.ecoenv.2017.12.050
McDonald M, Mila I, Scalbert A (1996) Precipitation of metal ions by plant polyphenols: optimal conditions and origin of precipitation. J Agric Food Chem 44:599–606. https://doi.org/10.1021/jf950459q
Michalak A (2010) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol J Environ Stud 15:523–530
Morrison IM (1972) A semi-micromethod for the determination of lignin and its use in predicting the digestibility of forage crops. J Sci Food Agric 23:455–463. https://doi.org/10.1002/jsfa.2740230405
Mroczek A (2015) Phytochemistry and bioactivity of triterpene saponins from Amaranthaceae family. Phytochem Rev 14:577–605. https://doi.org/10.1007/s11101-015-9394-4
Müller K, Borsch T (2005) Phylogenetics of Amaranthaceae based on matK/trnK sequence data: evidence from parsimony, likelihood, and bayesian analyses. Ann Mo Bot Gard 92:66–102
Nunes-Nesi A, Fernie AR, Stitt M (2010) Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol Plant 3:973–996. https://doi.org/10.1093/mp/ssq049
Ohya T, Morimura Y, Saji H, Mihara T, Ikawa T (1997) Purification and characterization of ascorbate peroxidase in roots of Japanese radish. Plant Sci 125:137–145. https://doi.org/10.1016/S0168-9452(97)00063-0
Osawa H, Endo I, Hara Y, Matsushima Y, Tange T (2011) Transient proliferation of proanthocyanidin-accumulating cells on the epidermal apex contributes to highly aluminum-resistant root elongation in camphor tree. Plant Physiol 155:433–446. https://doi.org/10.1104/pp.110.166967
Petry RD, Ortega GG, Silva WB (2001) Flavonoid content assay: influence of the reagent concentration and reaction time on the spectrophotometric behavior of the aluminium chloride-flavonoid complex. Pharmazie 56:465–470
Pirzadah TB, Malik B, Tahir I, Rehman RU, Hakeem KR, Alharby HF (2019) Aluminum stress modulates the osmolytes and enzyme defense system in Fagopyrum species. Plant Physiol Biochem 144:178–186. https://doi.org/10.1016/j.plaphy.2019.09.033
Poschenrieder C, Gunsé B, Corrales I, Barceló J (2008) A glance into aluminum toxicity and resistance in plants. Sci Total Environ 400:356–368. https://doi.org/10.1016/j.scitotenv.2008.06.003
Poschenrieder C, Cabot C, Martos S, Gallego B, Barceló J (2013) Do toxic ions induce hormesis in plants? Plant Sci 212:15–25. https://doi.org/10.1016/j.plantsci.2013.07.012
Poschenrieder C, Tolra R, Hajiboland R, Arroyave C, Barceló J (2015) Mechanisms of hyper-resistance and hyper-tolerance to aluminum in plants. In: Panda S, Baluška F (eds) Aluminum stress adaptation in plants. Springer, Switzerland, pp 81–98. https://doi.org/10.1007/978-3-319-19968-9_5
Ranieri A, Castagna A, Baldan B, Soldatini GF (2001) Iron deficiency differently affects peroxidase isoforms in sunflower. J Exp Bot 52:25–35. https://doi.org/10.1093/jexbot/52.354.25
Rechinger KH (1963–2010) Flora Iranica. Naturhistorischen Museum Wien, Wien, pp 1–178
Sellers BA, Smeda RJ, Johnson WG, Kendig JA, Ellersieck MR (2003) Comparative growth of six Amaranthus species in Missouri. Weed Sci 51:329–333. https://doi.org/10.1614/0043-1745(2003)051[0329:CGOSAS]2.0.CO;2
Simpson MG (2010) Plant systematics. Academic Press, Elsevier, pp 301–302
Singh N, Singh P, Shevkani K, Virdi AS (2019) Amaranth: Potential source for flour enrichment. In: Preedy VR, Watson RS (eds) Flour and breads and their fortification in health and disease prevention. Academic Press, UK, pp 123–135. https://doi.org/10.1016/B978-0-12-814639-2.00010-1
Swain T, Hillis EE (1959) The phenolic constituents of Prunus domestica I. The quantitative analysis of phenolic constituents. J Sci Food Agric 10:63–68. https://doi.org/10.1002/jsfa.2740100110
Tabuchi A, Matsumoto H (2001) Changes in cell-wall properties of wheat (Triticum aestivum) roots during aluminum-induced growth inhibition. Physiol Plant 112:353–358. https://doi.org/10.1034/j.1399-3054.2001.1120308.x
Tahara K, Hashida K, Otsuka Y, Ohara S, Kojima K, Shinohara K (2014) Identification of a hydrolyzable tannin, oenothein B, as an aluminum-detoxifying ligand in a highly aluminum-resistant tree, Eucalyptus camaldulensis. Plant Physiol 164:683–693. https://doi.org/10.1104/pp.113.222885
Takeda K, Yamashita T, Takahashi A, Timberlake C (1990) Stable blue complexes of anthocyanin-aluminium-3-p-coumaroyl- or 3-caffeoyl-quinic acid involved in the blueing of Hydrangea flower. Phytochem 29:1089–1191. https://doi.org/10.1016/0031-9422(90)85409-9
Tennant D (1975) A test of a modified line intersect method of estimating root length. J Ecol 1:995–1001. https://doi.org/10.1016/0031-9422(90)85409-9
Tolrà RP, Poschenrieder C, Luppi B, Barceló J (2005) Aluminium-induced changes in the profiles of both organic acids and phenolic substances underlie Al tolerance in Rumex acetosa L. Environ Exp Bot 54:231–238. https://doi.org/10.1016/j.envexpbot.2004.07.006
Tolrà R, Barceló J, Poschenrieder C (2009) Constitutive and aluminium-induced patterns of phenolic compounds in two maize varieties differing in aluminium tolerance. J Inorg Biochem 103:1486–1490. https://doi.org/10.1016/j.jinorgbio.2009.06.013
Tolrà R, Martos S, Hajiboland R, Poschenrieder C (2020) Aluminium alters mineral composition and polyphenol metabolism in leaves of tea plants (Camellia sinensis). J Inorg Biochem 204:110956. https://doi.org/10.1016/j.jinorgbio.2019.110956
Tsutsumi N, Tohya M, Nakashima T, Ueno O (2017) Variations in structural, biochemical, and physiological traits of photosynthesis and resource use efficiency in Amaranthus species (NAD-ME-type C4). Plant Prod Sci 20:300–312. https://doi.org/10.1080/1343943X.2017.1320948
Ueno O (2001) Ultrastructural localization of photosynthetic and photorespiratory enzymes in epidermal, mesophyll, bundle sheath and vascular bundle cells of the C4 dicot Amaranthus viridis. J Exp Bot 52:1003–1013. https://doi.org/10.1093/jexbot/52.358.1003
Von Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant Soil 171:1–5. https://doi.org/10.1007/BF00009558
Wallace G, Fry SC (1994) Phenolic components of the plant cell wall. Int Rev Cytol 151:229–267. https://doi.org/10.1016/S0074-7696(08)62634-0
Watanabe T (2022) Basic understanding of aluminum accumulating plants. Eurasian J For Res 22:59–62. https://doi.org/10.14943/EJFR.22.59
Watanabe T, Murata Y, Osaki M (2009) Amaranthus tricolor has the potential for phytoremediation of cadmium-contaminated soils. Commun Soil Sci Plant Anal 40:3158–3169. https://doi.org/10.1080/00103620903261676
Wenzl P, Patino GM, Chaves AL, Mayer JE, Rao IM (2001) The high level of aluminum resistance in signal grass is not associated with known mechanisms of external aluminum detoxification in root apices. Plant Physiol 125:1473–1484. https://doi.org/10.1104/pp.125.3.1473
Yemm EW, Cocking EC (1955) The determination of amino acids with ninhydrin. Analyst 80:209–213. https://doi.org/10.1039/AN9558000209
Zhang L, Liu R, Gung BW, Tindall S, Gonzalez JM, Halvorson JJ, Hagerman AE (2016) Polyphenol–aluminum complex formation: Implications for aluminum tolerance in plants. J Agric Food Chem 64:3025–3033. https://doi.org/10.1021/acs.jafc.6b00331
Zhang X, Long Y, Huang J, Xia J (2019) Molecular mechanisms for coping with Al toxicity in plants. Int J Mol Sci 20:1551. https://doi.org/10.3390/ijms20071551
Zhao XQ, Shen RF (2018) Aluminum–nitrogen interactions in the soil–plant system. Front Plant Sci 9:807. https://doi.org/10.3389/fpls.2018.00807
Zhou XX, Yang LT, Qi YP, Guo P, Chen LS (2015) Mechanisms on boron-induced alleviation of aluminum-toxicity in Citrus grandis seedlings at a transcriptional level revealed by cDNA-AFLP analysis. PLOS One 10:e0115485. https://doi.org/10.1371/journal.pone.0115485
Zhu XF, Lei GJ, Wang ZW, Shi YZ, Braam J, Li GX, Zheng SJ (2013) Coordination between apoplastic and symplastic detoxification confers plant aluminum resistance. Plant Physiol 162:1947–1955. https://doi.org/10.1104/pp.113.219147
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This work was supported by University of Tabriz, International and Academic Cooperation Directorate, in the framework of TabrizU-300 program.
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FN carried out the experiment, performed all biochemical and mineral analyses. RH conceived the work with the help of CP, EK, AM and SYS-L, was responsible for experimental design, interpretation of results and writer of the manuscript. SYS-L contributed to the plant analyses. EK identified the plants distribution areas and collected the seeds. AM determined the collected plants. CP performed critical revision of the manuscript, corrected and improved the manuscript. The manuscript has been read and approved by all named authors.
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Nazari, F., Hajiboland, R., Salehi-Lisar, SY. et al. Aluminum accumulation in Amaranthus species and mechanisms of Al tolerance. Biologia 78, 2029–2047 (2023). https://doi.org/10.1007/s11756-023-01348-z
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DOI: https://doi.org/10.1007/s11756-023-01348-z