Abstract

This study addressed the research gap in the comprehensive elemental profiling and bio-accessibility assessment of various plant parts of two indigenous varieties of Carissa carandas (karonda) types.
Fresh fruits, leaves, bark, and roots were freeze-dried, ground, and sieved (300 μm). The samples underwent microwaveassisted digestion with sub-boiled nitric acid and hydrogen peroxide, followed by inductively coupled plasma mass spectrometry to quantify 20 elements. The list included major (P, K, Ca, Na, and Mg), minor (B, Mn, Fe, Cu, Zn, etc.), and toxic trace elements (Ni, Cd, Pb, etc.). The hydrochloric acid extractability was assessed using 0.03 N HCl incubation at 37°C for 4 h to simulate gastric conditions.
The study revealed significant tissue-specific variations in the mineral content: the leaf samples exhibited the highest levels of phosphorus (3,836.69 mg/kg) and magnesium (4,682.87 mg/kg), the fruits were rich in potassium (2,971.64 mg/kg), the bark accumulated high calcium amounts (8,823.55 mg/kg), and roots contained elevated sodium levels (2,129.18 mg/kg). The hydrochloric acid extractability also varied, with potassium and phosphorus showing high extractability in the fruit samples (80.06 and 87.51%, respectively) while magnesium and boron were more extractable in the leaves. Such toxic elements as lead (43.32 mg/kg, roots) and cadmium (1.22 mg/kg, bark) exceeded permissible limits, raising safety concerns.
C. carandas proved to be a potential source of essential minerals, particularly its leaves and fruits, which demonstrated good nutraceutical prospects. The study provides a scientific basis for targeted use of specific C. carandas plant parts with an outlook of in-vivo bioavailability examination.

Keywords

Carissa carandas, karonda, inductively coupled plasma mass spectrometry, mineral bio-accessibility, hydrochloric acid extractability, trace elements

References

1. Bano Z, Begum S, Ali SS, Kiran Z, Siddiqui BS, et al. Phytochemicals from Carissa carandas with potent cytotoxic and anti-inflammatory activities. Natural Product Research. 2022;36(6):1587–1592. https://doi.org/10.1080/14786419.2021.1886101
2. Saxena D, Misra KK, Rai R. Studies on suitability of cultivars, picking dates and drying methods for the preparation of karonda (Carissa carandus L.) fruit powder. Indian Journal of Horticulture. 2016;73(2):267–273. http://doi.org/10.5958/0974-0112.2016.00059.1
3. Shaheen S, Jaffer M, Khan F, Hussain K, Hanif U, et al. Morpho-palynological assessment of medicinal flora of district Lahore, Pakistan based on LM and SEM. Microscopy Research and Technique. 2018;81:1397–1405. https://doi.org/10.1002/jemt.23096
4. Singh K, Singh SP. Karonda: A medicinal plant with immense economic potentials. AgriCos E-Newsletter 2021;2(2);83–86.
5. Bilal A, Adnan M, Mushtaq A, Blama A. A brief study of phytochemical profile and pharmacological applications of Carissa carandas ( L.). International Journal of Chemical and Biochemical Sciences. 2015;8:92–96.
6. Hua Z, Zhen-Yu W, Xin Y, Hai-Tian Z, Ying-Chun Z, et al. Determination of free amino acids and 18 elements in freeze-dried strawberry and blueberry fruit using an Amino Acid Analyzer and ICP-MS with micro-wave digestion. Food Chemistry. 2014;147:189–194. https://doi.org/10.1016/j.foodchem.2013.09.118
7. Fotirić Akšić M, Nešović M, Ćirić I, Tešić Ž, Pezo L, et al. Chemical fruit profiles of different raspberry cultivars grown in specific norwegian agroclimatic conditions. Horticulturae. 2022;8(9):765. https://doi.org/10.3390/horticulturae8090765
8. Adamczuk N, Ośko J, Grembecka M, Konieczyński P, Migas P, et al. Evaluation of the content of micro- and macroelements in raspberries depending on the species, cultivar variety, and geographical environment. Nutrients. 2023;15(17):3782. https://doi.org/10.3390/nu15173782
9. Cristea G, Dehelean A, Puscas R, Covaciu FD, Hategan AR, et al. Characterization and differentiation of wild and cultivated berries based on isotopic and elemental profiles. Applied Sciences. 2023;13(5):2980. https://doi.org/10.3390/app13052980
10. Shen J, Yuan L, Zhang J, Li H, Bai Z, et al. Phosphorus dynamics: From soil to plant. Plant Physiology. 2011;156(3):997–1005. https://doi.org/10.1104/pp.111.175232
11. Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, et al. Opportunities for improving phosphorus-use efficiency in crop plants. New Phytologist. 2012;195:306–320. https://doi.org/10.1111/j.1469-8137.2012.04190.x
12. Imenšek N, Sem V, Kolar M, Ivančič A, Kristl J. The distribution of minerals in crucial plant parts of various elderberry (Sambucus spp.) interspecific hybrids. Plants. 2021;10(4):653. https://doi.org/10.3390/plants10040653
13. Duhan A, Khetarpaul N, Bishnoi S. Changes in phytates and HCl extractability of calcium, phosphorus, and iron of soaked, dehulled, cooked, and sprouted pigeon pea cultivar (UPAS-120). Plant Foods for Human Nutrition. 2002;57:275–284. https://doi.org/10.1023/A:1021814919592
14. Ishfaq M, Wang Y, Yan M, Wang Z, Wu L, et al. Physiological essence of magnesium in plants and its widespread deficiency in the farming system of China. Frontiers in Plant Science. 2022;13:802274. https://doi.org/10.3389/fpls.2022.802274
15. Ahmed N, Zhang B, Bozdar B, Chachar S, Rai M, et al. The power of magnesium: Unlocking the potential for increased yield, quality, and stress tolerance of horticultural crops. Frontiers in Plant Science. 2023;14:1285512. https://doi.org/10.3389/fpls.2023.1285512
16. Bibi S, Irshad M, Ullah F, Mahmood Q, Shahzad M, et al. Phosphorus extractability in relation to soil properties in different fields of fruit orchards under similar ecological conditions of Pakistan. Frontiers in Ecology and Evolution. 2023;10:1077270. https://doi.org/10.3389/fevo.2022.1077270
17. Kuzin A, Solovchenko A. Essential role of potassium in apple and its implications for management of orchard fertilization. Plants. 2021;10(12):2624. https://doi.org/10.3390/plants10122624
18. Cheng L. Optimizing nitrogen and potassium management to foster apple tree growth and cropping without getting “burned”. New York Fruit Quarterly. 2013;21(1):21–24.
19. Wang S, Song M, Guo J, Huang Y, Zhang F, et al. The potassium channel FaTPK1 plays a critical role in fruit quality formation in strawberry (Fragaria × ananassa). Plant Biotechnology Journal. 2018;16:737–748. https://doi.org/10.1111/pbi.12824
20. Razzaque AHM, Hanafi MM. Effect of potassium on growth, yield and quality of pineapple in tropical peat. Fruits. 2001;56(1):45–49.
21. Fromm J. Wood formation of trees in relation to potassium and calcium nutrition. Tree Physiology. 2010;30(9):1140–1147. https://doi.org/10.1093/treephys/tpq024
22. Hocking B, Tyerman SD, Burton RA, Gilliham M. Fruit calcium: Transport and physiology. Frontiers in Plant Science. 2016;7:569. https://doi.org/10.3389/fpls.2016.00569
23. Keisham M, Mukherjee S, Bhatla SC. Mechanisms of sodium transport in plants–progresses and challenges. International Journal of Molecular Sciences. 2018;19(3):647. https://doi.org/10.3390/ijms19030647
24. Zhao S, Zhang Q, Liu M, Zhou H, Ma C, et al. Regulation of plant responses to salt stress. International Journal of Molecular Sciences. 2021;22(9):4609. https://doi.org/10.3390/ijms22094609
25. Yamaguchi T, Hamamoto S, Uozumi N. Sodium transport system in plant cells. Frontiers in Plant Science. 2013;4:410. https://doi.org/10.3389/fpls.2013.00410
26. Datta S, Sinha BK, Bhattacharjee S, Seal T. Nutritional composition, mineral content, antioxidant activity and quantitative estimation of water soluble vitamins and phenolics by RP-HPLC in some lesser used wild edible plants. Heliyon. 2019;5(3):e01431. https://doi.org/10.1016/j.heliyon.2019.e01431
27. Brdar-Jokanović M. Boron toxicity and deficiency in agricultural plants. International Journal of Molecular Sciences. 2020;21(4):1424. https://doi.org/10.3390/ijms21041424
28. Ali F, Ali A, Gul H, Sharif M, Sadiq A, et al. Effect of boron soil application on nutrients efficiency in tobacco leaf. American Journal of Plant Sciences. 2015;6:1391–1400. http://doi.org/10.4236/ajps.2015.69139
29. Marschner P. Marschner’s mineral nutrition of higher plants. 3rd ed. NY: Academic Press; 2012, 651 p. https://doi.org/10.1016/C2009-0-63043-9
30. Diviš P, Pořízka J, Vespalcov M, Matějíček A, Kaplan J. Elemental composition of fruits from different black elder (Sambucus nigra L.) cultivars grown in the Czech Republic. Journal of Elementology. 2015;20(3):549–557. https://doi.org/10.5601/jelem.2015.20.1.758
31. Kuang X, Wang W, Hu J, Liu W, Zeng W. Subcellular distribution and chemical forms of manganese in Daucus carota in relation to its tolerance. Frontiers in Plant Science. 2022;13:1–14. https://doi.org/10.3389/fpls.2022.947882
32. Oteng P, Otchere JK, Adusei S, Mensah RQ, Tei-Mensah E. Vitamin analysis, trace elements content, and their extractabilities in Tetrapleura tetraptera. Journal of Chemistry. 2020;2020:1608341. https://doi.org/10.1155/2020/1608341
33. Liu Y, Zhao M, Chen J, Yang S, Chen J, et al. Comparative transcriptome analysis reveals complex physiological response and gene regulation in peanut roots and leaves under manganese toxicity stress. International Journal of Molecular Sciences. 2023;24(2):1161. https://doi.org/10.3390/ijms24021161
34. Mohammadzadeh H, Mirzaei J, Farashiyani ME, Soheili F, Woodward S, et al. Variation in the nutrient contents of leaves, bark, and wood of Persian oak trees (Quercus brantii) affected by decline. BioResources. 2021;16(3):4704–4715. https://doi.org/10.15376/biores.16.3.4704-4715
35. Ancuceanu R, Dinu M, Hovaneţ MV, Anghel AI, Popescu CV, et al. A survey of plant iron content – a semi-systematic review. Nutrients. 2015;7(12):10320–10351. https://doi.org/10.3390/nu7125535
36. Page V, Feller U. Heavy metals in crop plants: Transport and redistribution processes on the whole plant level. Agronomy. 2015;5(3):447–463. https://doi.org/10.3390/agronomy5030447
37. Młynarczyk K, Walkowiak-Tomczak D, Staniek H, Kidoń M, Łysiak GP. The content of selected minerals, bioactive compounds, and the antioxidant properties of the flowers and fruit of selected cultivars and wildly growing plants of Sambucus nigra L. Molecules. 2020;25(4):876. https://doi.org/10.3390/molecules25040876
38. Yadav AK, Abbassi R, Kumar N, Satya S, Sreekrishnan TR, et al. The removal of heavy metals in wetland microcosms: Effects of bed depth, plant species, and metal mobility. Chemical Engineering Journal. 2012;211–212:501–507. https://doi.org/10.1016/j.cej.2012.09.039
39. Deng H, Ye ZH, Wong MH. Accumulation of lead, zinc, copper and cadmium by 12 wetland plant species thriving in metal-contaminated sites in China. Environmental Pollution. 2004;132(1):29–40. https://doi.org/10.1016/j.envpol.2004.03.030
40. Chen G, Li J, Han H, Du R, Wang X. Physiological and molecular mechanisms of plant responses to copper stress. International Journal of Molecular Sciences. 2022;23(21):12950. https://doi.org/10.3390/ijms232112950
41. Yruela I. Copper in plants: Acquisition, transport and interactions. Functional Plant Biology. 2009;36(5):409–430. https://doi.org/10.1071/FP08288
42. Gul Z, Akbar A, Leghari SK, Kakar AUR, Khan N, et al. Daily dose standardization based on essential and nonessential trace element presence in Berberis baluchistanica ahrendt bark, leaf, and root. BioMed Research International. 2022;2022:6811613. https://doi.org/10.1155/2022/6811613
43. Dos Santos Utmazian MN, Wenzel WW. Cadmium and zinc accumulation in willow and poplar species grown on polluted soils. Journal of Plant Nutrition and Soil Science. 2007;170(2):265–272. https://doi.org/10.1002/jpln.200622073
44. Xie R, Zhao J, Lu L, Brown P, Lin X, et al. Seasonal zinc storage and a strategy for its use in buds of fruit trees. Plant Physiology. 2020;183(3):1200–1212. https://doi.org/10.1104/pp.19.01563
45. Sasmaz M, Sasmaz A. The accumulation of strontium by native plants grown on Gumuskoy mining soils. Journal of Geochemical Exploration. 2017;181:236–242. https://doi.org/10.1016/j.gexplo.2017.08.001
46. Watts P, Howe P. Strontium and strontium compounds. IPCS concise international chemical assessment documents. 2010;77:1–63. https://elibrary.ru/LTZLXB
47. Kalinowska M, Hawrylak-Nowak B, Szymańska M. The influence of two lithium forms on the growth, L-ascorbic acid content and lithium accumulation in lettuce plants. Biological Trace Element Research. 2013;152:251–257. https://doi.org/10.1007/s12011-013-9606-y
48. Magalhaes JR, Wilcox GE, Rocha AN, Silva FL. Research on lithium-phytological metabolism ano recovery of hypo-lithium. Pesquisa Agropecuária Brasileira. 1990;25:1781–1787.
49. Ha NTH, Sakakibara M, Sano S, Nhuan MT. Uptake of metals and metalloids by plants growing in a lead-zinc mine area, Northern Vietnam. Journal of Hazardous Materials. 2011;186(2–3):1384–1391. https://doi.org/10.1016/j.jhazmat.2010.12.020.
50. Shtangeeva I. Temporal variability of gallium in natural plants. Toxics. 2023;11(8):675. https://doi.org/10.3390/toxics11080675
51. EFSA CONTAM Panel (EFSA Panel on Contaminants in the Food Chain). Scientific opinion on the risks to public health related to the presence of chromium in food and drinking water. EFSA Journal. 2014;12(3):3595. https://doi.org/10.2903/j.efsa.2014.3595
52. Antonkiewicz J, Jasiewicz C, Koncewicz-Baran M, Sendor R. Nickel bioaccumulation by the chosen plant species. Acta Physiologiae Plantarum. 2016;38:40. https://doi.org/10.1007/s11738-016-2062-5
53. Pishchik V, Mirskaya G, Chizhevskaya E, Chebotar V, Chakrabarty D. Nickel stress-tolerance in plant-bacterial associations. PeerJ. 2021;9:e12230. https://doi.org/10.7717/peerj.12230
54. Rue M, Paul ALD, Echevarria G, Van Der Ent A, Simonnot MO, et al. Uptake, translocation and accumulation of nickel and cobalt in: Berkheya coddii, a “metal crop” from South Africa. Metallomics. 2020;12(8):1278–1289. https://doi.org/10.1039/d0mt00099j
55. Zhao XQ, Shen RF. Aluminum–nitrogen interactions in the soil–plant system. Frontiers in Plant Science. 2018;9:807. https://doi.org/10.3389/fpls.2018.00807.
56. Ofoe R, Thomas RH, Asiedu SK, Wang-Pruski G, Fofana B, et al. Aluminum in plant: Benefits, toxicity and tolerance mechanisms. Frontiers in Plant Science. 2023;13:1085998. https://doi.org/10.3389/fpls.2022.1085998
57. Magalhães MOL, do Amaral Sobrinho NMB, Zonta E, Becerra AT, Lastra-Bravo XB, et al. Reducing conditions on barium absorption in rice plants cultured in BaSO4-enriched soil. Acta Scientiarum. Agronomy. 2014;36(1):119–127. (In Portuguese) https://doi.org/10.4025/actasciagron.v36i1.17539
58. Wei C, Deng Q, Wu F, Fu Z, Xu L. Arsenic, antimony, and bismuth uptake and accumulation by plants in an old antimony mine, China. Biological Trace Element Research. 2011;144:1150–1158. https://doi.org/10.1007/s12011-011-9017-x
59. Pietrini F, Passatore L, Carloni S, Massimi L, Astolfi ML, et al. Bismuth exposure affects morpho-physiological performances and the ionomic profile in garden cress (Lepidium sativum L.) plants. Frontiers in Environmental Science. 2023;11:1221573. https://doi.org/10.3389/fenvs.2023.1221573
60. Aransiola SA, Ijah UJJ, Abioye OP. Phytoremediation of lead polluted soil by Glycine max L. Applied and Environmental Soil Science. 2013;2013(1):631619. https://doi.org/10.1155/2013/631619
61. Sharma P, Dubey RS. Lead toxicity in plants. Brazilian Journal of Plant Physiology. 2005;17(1):35–52. https://doi.org/10.1590/s1677-04202005000100004
62. Street JJ, Lindsay WL, Sabey BR. Solubility and plant uptake of cadmium in soils amended with cadmium and sewage sludge. Journal of Environmental Quality. 1977;6(1):72–77. https://doi.org/10.2134/jeq1977.00472425000600010016x
63. Hocaoglu-Ozyigit A, Nazli Genc B. Cadmium in plants, humans and the environment. Frontiers in Life Sciences and Related Technologies. 2020;1(1):12–21.