Alterations in leaf anatomy, quality, and quantity of flavonols and photosynthetic pigments in Nigella sativa L. subjected to drought and salinity stresses

  • Shiva AGHAJANZADEH-GHESHLAGHI Islamic Azad University, Tehran North Branch, Faculty of Biological Science, Department of Biology, Tehran (IR)
  • Maryam PEYVANDI Islamic Azad University, Tehran North Branch, Faculty of Biological Science, Department of Biology, Tehran (IR)
  • Ahmad MAJD Islamic Azad University, Tehran North Branch, Faculty of Biological Science, Department of Biology, Tehran (IR)
  • Hossein ABBASPOUR Islamic Azad University, Tehran North Branch, Faculty of Biological Science, Department of Biology, Tehran (IR)
Keywords: B-carotene, black cumin, flavonols, HPLC, leaf anatomy

Abstract

Nigella sativa was widely used for nutritional and medicinal purposes. The present study investigated the effect of drought and salinity stresses on anatomical leaves structure and some biochemical properties to increase the secondary metabolites. For salt stress plants were treated with NaCl (30, 60 mM), and for drought stress plants were irrigated daily (control), once every two days (2DI) and once every three days (3DI). Compared to control plants, 2DI, 3DI, and NaCl 60 mM treatments increase significantly leaf rutin content, while the amount of rutin in seeds of NaCl 60 mM treated plants showed a significant decrease. 3DI treatment also significantly increased rutin content in seeds compared to NaCl 30 mM and control plants.  The maximum level of quercetin (0.58 mg g−1 DW), kaempferol (0.16 mg g−1 DW), and myricetin (0.04 mg g−1 DW) in leaves were gained in both NaCl treatments. However, the flavonol components were affected more at salinity conditions rather than drought. In all treated plants, the amount of these compounds in leaves was more than in seeds. The highest amount of total phenol (130 mg g−1 DW), flavonoids (11.4 mg g−1 DW), and carotenoid content (1.55 mg g−1 DW) of leaves were observed under 2DI stress. Treated plants probably encountered different changes in the anatomical structure of leaves, including the decrease of phloem area, reducing vascular bundles and diameters, decreasing the number, and increasing the volume of cortex cells. The study also corroborates the cooperation between increasing the antioxidant capacity with the total flavonoid, rutin, and quercetin. Results indicated a higher sensitivity of N. sativa to drought stress than salinity stress and indicated that moderate salinity and drought could enhance secondary metabolites of seeds in this plant. The formation of potent antioxidants via the treatments could be worthy for pharmaceutical industries.

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References

Abdelkrim H, Dhia S, Mostefa K, Farid B, Nadia S, Belkhodja M (2014). Impact of salt stress on morphological and physical behavior of the foliar system by cultivating olive and wild olive trees. International Journal of Current Science 12:161-169. http://www.currentsciencejournal.info/issuespdf/hassani%20Algeria.pdf

Acosta-Motos JR, Ortuno MF, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco MJ, Hernandez JA (2017). Plant responses to salt stress: Adaptive mechanisms. Agronomy 7(1):18. http://doi.org/10.3390/agronomy7010018

Amić D, Davidović-Amić D, Bešlo D, Trinajstić N (2003). Structure-radical scavenging activity relationships of flavonoids. Croatica Chemica Acta 76:55-61. https://doi.org/10.1016/j.phytochem.2006.07.002

Azarafshan M, Peyvandi M, Abbaspour H, Noormohammadi Z, Majd A (2020). The effects of UV-B radiation on genetic and biochemical changes of Pelargonium graveolens L Her. Physiology and Molecular Biology of Plants 26:605-616. http://doi.org10.1007/s12298-020-00758-6

Ball GFM (1988). Fat-soluble vitamin assays in Food Analysis, a comprehensive review. Elsevier, London.

Bayati P, Karimmojeni, H, Razmjoo J (2020). Changes in essential oil yield and fatty acid contents in black cumin (Nigella sativa L.) genotypes in response to drought stress. Industrial Crops and Products 155:112764. http://doi.org/10.1016/j.indcrop.2020.112764

Bensalem N, Helali SM, Chebbi M, Ghnaya T, Ouerghi Z (2020). The interactive effect of nitrate/ammonium ratio and sodium chloride on Tunisian medicinal plant (Nigella sativa L). Journal of Plant Nutrition 1-13. http://doi.org/10.1080/01904167.2020.1711935

Bourgou S, Bettaieb I, Hamrouni I, Marzouk B (2012). Effect of NaCl on fatty acids, phenolics and antioxidant activity of Nigella sativa organs. Acta Physiologiae Plantarum 34:379-386. http://doi.org/10.1007/s11738-011-0836-3

Bourgou S, Kchouk ME, Bellila A, Marzouk B (2010). Effect of salinity on phenolic composition and biological activity of Nigella sativa. Acta Horticulturae 853:57-60. http://doi.org/10.17660/actahortic.2010.853

Bourgou S, Ksouri R, Bellila A, Skandrani I, Falleh H, Marzouk B (2008). Phenolic composition and biological activities of Tunisian Nigella sativa L. shoots and roots. Comptes Rendus Biologies 331:48-55. http://doi.org/10.1016/j.crvi.2007.11.001

Chavarria G, dos Santos HP (2012). Plant water relations: absorption, transport and control mechanisms. Advances in Selected Plant Physiology Aspects http://doi.org/10.5772/33478

Chang CC, Yang MH, Wen HM, Chern JC (2002). Estimation of total flavonoid content in propolis by two complementary colorimetric methods. Journal of Food and Drug Analysis 10(3):178-182. http://doi.org/10.38212/2224-6614.2748

Cosic M, Vujicic MM, Sabovlijevic MS, Sabovlijevic AD (2020). Effects of ABA and NaCl on physiological responses in selected bryophyte species. Botany 98(11):639-650. https://doi.org/10.1139/cjb-2020-0041

Duarte B, Santos D, Marques J, Caçador I (2013). Ecophysiological adaptations of two halophytes to salt stress: photosynthesis, PS II photochemistry and antioxidant feedback–implications for resilience in climate change. Plant Physiology and Biochemistry 67:178-188. https://doi.org/10.1016/j.plaphy.2013.03.004

Elnaggar A, Mosa KA, El-Keblawy A, Tammam A, El-Naggar M (2020). Physiological and biochemical insights for salt stress tolerance in the habitat-indifferent halophyte Salsola drummondii during the vegetative stage. Botany 98(11):673-689. https://doi.org/10.1139/cjb-2019-0160

Elsheery NI, Cao KF (2008). Gas exchange, chlorophyll fluorescence, and osmotic adjustment in two mango cultivars under drought stress. Acta Physiologiae Plantarum 30:769-777.

Erlejman A, Verstraeten S, Fraga C, Oteiza P (2004). The interaction of flavonoids with membranes: potential determinant of flavonoid antioxidant effects. Free Radicals Research 38:1311-1320. http://doi.org.10.1080/10715760400016105

Farooq M, Wahid A, Kobayashi N, Fujita D, Basra S (2009). Plant drought stress: effects, mechanisms and management. In: Sustainable Agriculture. Springer, pp 153-188. http://doi.org/10.1051/agro:2008021

Fayek M, Fayed T, El-Sayed EH, Abd El-Hameed EE (2018). Comparative impacts of salt stress on survival and leaf anatomy traits in olive genotypes. Bioscience Research 15:565-574. http://doi.org/10.1080/14620316.2010.11512670

Ghamarnia H, Jalili Z (2013). Water stress effects on different Black cumin (Nigella sativa L.) components in a semi-arid region. International Journal of Agronomy and Plant Production 4:545-554.

Golkar P, Bakhshi G, Vahabi MR (2020). Phytochemical, biochemical, and growth changes in response to salinity in callus cultures of Nigella sativa L. In Vitro Cellular & Developmental Biology – Plant 56(2):247-258. http://doi.org/10.1007/s11627-020-10058-z

Gray DE, Pallardy SG, Garrett H, Rottinghaus GE (2003). Effect of acute drought stress and time of harvest on phytochemistry and dry weight of St. John's wort leaves and flowers. Planta Medica 69:1024-1030. http://doi.org/10.1055/s-2003-45150

Han RM, Zhang JP, Skibsted LH (2012) Reaction dynamics of flavonoids and carotenoids as antioxidants. Molecules 17:2140-2160. http://doi.org/10.3390/molecules17022140

Habibi G (2018). Effects of mild and severe drought stress on the biomass, phenolic compounds production and photochemical activity of Aloe vera (L.) Burm. f. Acta Agriculturae Slovenica 111:463-476. http://doi.org/10.14720/aas.2018.111.2.19

Habibi G, Ajory N (2015). The effect of drought on photosynthetic plasticity in Marrubium vulgare plants growing at low and high altitudes. Journal of Plant Research 128(6):987-994. http://doi.org/10.1007/s10265-015-0748-1

Haj Seyed Hadi MR, Darzi MT, Ghandehari Z (2012). Effect of irrigation treatment and Azospirillum inoculation on yield and yield component of balck cumin (Nigella sativa L.). Journal of Medicinal Plants Resources 6:4553-4561. http://doi.org/10.5897/JMPR12.228

Hussain K, Majeed A, Nawaz K, Nisar MF (2009). Effect of different levels of salinity on growth and ion contents of black seeds (Nigella sativa L.). Current Research Journal of Biological Science 1:135-138. http://doi.org10.1007/978-3-319-68717-9_10

Iqbal MS, Iqbal Z, Hashem A, Al‑Arjani ALF, Abd‑Allah EF, Jafri A, Ansari SA, Ansari MI (2021). Nigella sativa callus treated with sodium azide exhibit augmented antioxidant activity and DNA damage inhibition. Scientific Reports 11:13954. http://doi.org/10.1038/s41598-021-93370-x

Johansen DA (1940). Plant Microtechnique. McGraw-Hill, New York, pp 523.

Kabiri R, Nasibi F, Farahbakhsh H (2014). Effect of exogenous salicylic acid on some physiological pa¬rameters and alleviation of drought stress in Nigella sativa plant under hydroponic culture. Plant Protection Science 50:43-51. https://doi.org/10.17221/56/2012-PPS

Kiani SP, Maury P, Sarrafi A, Grieu P (2008). QTL analysis of chlorophyll fluorescence parameters in sunflower (Helianthus annuus L.) under well-watered and water-stressed conditions. Plant Science 175:565-573. http://doi.org.10/1016/j.plantsci.2008.06.002

Ksouri R, Megdiche W, Debez A, Falleh H, Grignon C, Abdelly C (2007). Salinity effects on polyphenol content and antioxidant activities in leaves of the halophyte Cakile maritima. Plant Physiology and Biochemistry 45:244-249. http://doi.org/10.1016/j.plaphy.2007.02.001

Lichtenthaler HK (1987) Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods in Enzymology 350-382. http://doi.org/10.1016/0076-6879(87)48036-1

Linnaeus C (1753). Species Plantarum. London, 1 (392).

Mahajan M, Kumar V, Yadav SK (2011). Effect of flavonoid-mediated free IAA regulation on growth and development of in vitro-grown tobacco seedlings. International Journal of Plant Developmental Biology 5:42-48.

Marček T, Hamow KÁ, Végh B, Janda T, Darko E (2019) Metabolic response to drought in six winter wheat genotypes PLoS One14(2):e0212411. http://doi.org/10.1371/journal.pone.0212411

Marinova D, Ribarova F, Atanassova M (2005). Total phenolics and total flavonoids in Bulgarian fruits and vegetables. Journal of the University of Chemical Technology and Metallurgy 40(3):255-260.

Mozaffari F S, Ghorbanli M, Babai A, Sepehr MF (2000). The effect of water stress on the seed oil of Nigella sativa L. Journal of Essential Oil Research 12(1):36-38. http://doi.org/10.1080/10412905.2000.9712036

Munns R, Tester M (2008). Mechanisms of salinity tolerance. Annual Review of Plant Biology 59:651-681.

Nakabayashi R, Yonekura‐Sakakibara K, Urano K, Suzuki M, Yamada Y, Nishizawa T, Matsuda F, Kojima M, Sakakibara H, Shinozaki K (2014). Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. The Plant Journal 77:367-379. http://doi.org/10.1111/tpj.12388

Nolan RH, Tarin T, Santini NS, McAdam SA, Ruman R, Eamus D (2017). Differences in osmotic adjustment, foliar abscisic acid dynamics, and stomatal regulation between an isohydric and anisohydric woody angiosperm during drought. Plant Cell Environment 40:3122-3134. http://doi.org/10.1111/pce.13077

Oh MM, Trick HN, Rajashekar C (2009). Secondary metabolism and antioxidants are involved in environmental adaptation and stress tolerance in lettuce. Journal of Plant Physiology 166:180-191. http://doi.org.10.1016/j.jplph.2008.04.015

Ola HAE, Reham EF, Eisa S, Habib S (2012). Morpho-anatomical changes in salt stressed kallar grass (Leptochloa fusca L. Kunth). Research Journal of Agriculture and Biological Sciences 8:158-166.

Plaza B, Jimenez S, Segura M, Contreras J, Lao M (2009). Physiological stress caused by salinity in cordyline fruticosa and its indicators. Communications in Soil Science and Plant Analysis 40:473-484. https://doi.org/10.1080/00103620802649211

Pourcel L, Routaboul JM, Cheynier V, Lepiniec L, Debeaujon I (2007). Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trends in Plant Science 12:29-36. https://doi.org/10.1016/j.tplants.2006.11.006

Shojaie B, Mostajeran A, Ghanadian M (2016). Flavonoid dynamic responses to different drought conditions: amount, type, and localization of flavonols in roots and shoots of Arabidopsis thaliana L. Turkish Journal of Biology 40:612-622.

Singh R (2015). Medicinal plants: a review. Journal of Plant Sciences 3(1):50-55.

Talamè V, Ozturk NZ, Bohnert HJ, Tuberosa R (2007). Barley transcript profiles under dehydration shock and drought stress treatments: a comparative analysis. Journal of Experimental Botany 58:229-240. https://doi.org/10.1093/jxb/erl163

Tattini M, Galardi C, Pinelli P, Massai R, Remorini D, Agati G (2004). Differential accumulation of flavonoids and hydroxycinnamates in leaves of Ligustrum vulgare under excess light and drought stress. New Phytologist 163:547-561. https://doi.org/10.1111/j.1469-8137.2004.01126.x

Toma CC, Olah NK, Vlase L, Mogoșan C, Mocan A (2015). Comparative studies on polyphenolic composition, antioxidant and diuretic effects of Nigella sativa L. (black cumin) and Nigella damascena L.(lady-in-a-mist) seeds. Molecules 20:9560-9574. https://doi.org/10.3390/molecules20069560

Valifard M, Mohsenzadeh S, Kholdebarin B, Rowshan V (2014). Effects of salt stress on volatile compounds, total phenolic content and antioxidant activities of Salvia mirzayanii. South African Journal of Botany 93:92-97. https://doi.org/10.1016/j.sajb.2014.04.002

Wei H, Li L, Yan X, Wang Y (2013). Effects of soil drought stress on the accumulation of alkaloids and flavonoids in motherwort. Advances in Information Sciences and Service Sciences 15:795-803. https://doi.org/10.4156/aiss.vol5.issue6.94

Wilcox LJ, Balderes DA, Wharton B, Tinkelenberg AH, Rao G, Sturley SL (2002). Transcriptional profiling identifies two members of the ATP-binding cassette transporter superfamily required for sterol uptake in yeast. Journal of Biological Chemistry 277(36):32466-72. https://doi.org/10.1074/jbc.M204707200

Yaginuma S, Shiraishi T, Ohya H, Igarashi K (2002). Polyphenol increases in safflower and cucumber seedlings exposed to strong visible light with limited water. Bioscience, Biotechnology, and Biochemistry 66:65-72. https://doi.org/10.1271/bbb.66.65

Published
2021-09-07
How to Cite
AGHAJANZADEH-GHESHLAGHI, S., PEYVANDI, M., MAJD, A., & ABBASPOUR, H. (2021). Alterations in leaf anatomy, quality, and quantity of flavonols and photosynthetic pigments in Nigella sativa L. subjected to drought and salinity stresses. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 49(3), 12398. https://doi.org/10.15835/nbha49312398
Section
Research Articles
CITATION
DOI: 10.15835/nbha49312398