Antioxidant responses to drought and salinity in Lavandula angustifolia Mill.
Keywords:abiotic stress; antioxidant enzymes; oxidative stress; Lamiaceae; non-enzymatic antioxidants; reactive oxygen species
Drought and salinity are amongst the most damaging environmental stressors that can affect a plant's life cycle, from germination to senescence. In the present study were analysed the responses to salinity and drought in greenhouse-controlled conditions of two varieties of Lavandula angustifolia. Three-month-old lavender seedlings were subjected to water deficit and salt stress (100, 200 and 300 mM NaCl) during a 30-day period. Complementing a previous analysis focused on stress tolerance mechanisms based on the regulation of ion transport and the synthesis of osmolytes, we have now evaluated the effects of the water deficit and salt treatments on the generation of secondary oxidative stress, by measuring malondialdehyde levels, and the activation of antioxidant systems, both non-enzymatic and enzymatic, determining total phenolic compounds and flavonoids contents and calculating superoxide dismutase, catalase, ascorbate peroxidase and glutathione reductase specific activities, respectively, in extracts of control and stressed plants. The results obtained confirm that both lavender varieties react in the same way to the applied stress treatments, activating the same antioxidant responses. However, some differences were observed when comparing the specific mechanisms triggered by each type of stress. Thus, the oxidative stress induced under drought conditions was counteracted by accumulation of phenolic compounds and flavonoids, without apparent involvement of antioxidant enzymes. Salt stress, on the other hand, in addition to an increase in flavonoid levels also induced superoxide dismutase and catalase activities. These antioxidant responses are likely to contribute to the relatively high tolerance (as compared to most crops) of lavender to drought and salinity.
Abogadallah GM (2010). Insights into the significance of antioxidative defense under salt stress. Plant Signaling & Behavior 5(4):369-374. https://doi.org/10.4161/psb.5.4.10873
Acosta-Motos JR, Ortuño MF, Bernal-Vicente A, Diaz-Vivancos P, Sánchez-Blanco MJ, Hernandez JA (2017). Plant responses to salt stress: Adaptive mechanisms. Agronomy 7:18. https://doi.org/10.3390/agronomy7010018
Adam KL (2006). Lavender production, products, markets, and entertainment farms, ATTRA. Retrieved 2020 July 26 from www.attra.ncat.org
Aebi H (1984). Catalase in vitro. Methods in Enzymology 105:121-126. https://doi.org/10.1016/S0076-6879(84)05016-3
Aftab T (2019). A review of medicinal and aromatic plants and their secondary metabolites status under abiotic stress. Journal of Medicinal Plants 7(3):99-106.
Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010). Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Critical Reviews in Biotechnology 30(3):161-175. https://doi.org/10.3109/07388550903524243
Al Hassan M, Chaura J, Donat-Torres MP, Boscaiu M, Vicente O (2017). Antioxidant responses under salinity and drought in three closely related wild monocots with different ecological optima. AoB Plants 9(2):plx009. https://doi.org/10.1093/aobpla/plx009
Al Kharusi L, Al Yahyai R, Yaish MW (2019). Antioxidant response to salinity in salt-tolerant and salt-susceptible cultivars of date palm. Agriculture 9:8. https://doi.org/10.3390/agriculture9010008
Alscher RG, Erturk N, Heath LS (2002). Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. Journal of Experimental Botany 53:1331-1341. https://doi.org/10.1093/jexbot/53.372.1331
Arora M, Saxena P, Abdin MZ, Varma A (2020). Interaction between Piriformospora indica and Azotobacter chroococcum diminish the effect of salt stress in Artemisia annua L. by enhancing enzymatic and non-enzymatic antioxidants. Symbiosis 80:61-73. https://doi.org/10.1007/s13199-019-00656-w
Arora M, Saxena P, Abdin, MZ, Varma A (2018). Interaction between Piriformospora indica and Azotobacter chroococcum governs better plant physiological and biochemical parameters in Artemisia annua L. plants grown under in vitro conditions. Symbiosis 75:103-112. https://doi.org/10.1007/s13199-017-0519-y
Ashraf M (2009). Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnology Advances 27:84-93. https://doi.org/10.1016/j.biotechadv.2008.09.003
Bartels D, Ramanjulu S (2005). Drought and salt tolerance in plants. Critical Reviews in Plant Sciences 24:23-58. https://doi.org/10.1080/07352680590910410
Bautista I, Boscaiu M, Lidón A, Llinares JV, Lull C, Donat MP, … Vicente O (2016). Environmentally induced changes in antioxidant phenolic compounds levels in wild plants. Acta Physiologiae Plantarum 38(1):9. https://doi.org/10.1007/s11738-015-2025-2
Benabdelkader T, Zitouni A, Guitton Y, Jullien F, Maitre D, Casabianca H, … Kameli A (2011). Essential oils from wild populations of algerian Algerian lavandula Lavandula stoechas L.: Composition, chemical variability, and in vitro biological properties. Chemistry & Biodiversity 8:937-953. https://doi.org/10.1002/cbdv.201000301
Ben-Amor N, Hamed KB, Debez A, Grignon C, Abdelly C (2005). Physiological and antioxidant response of the perennial halophytes Crithmum maritimum to salinity. Plant Science 168:889-899. https://doi.org/10.1016/j.plantsci.2004.11.002
Beyer Jr, Wayne F, Fridovich I (1987). Assaying for superoxide dismutase activity: Some large consequences of minor changes in conditions. Analytical Biochemistry 161:559-566. https://doi.org/10.1016/0003-2697(87)90489-1
Biesiada A, Kucharska A (2008). The effect of nitrogen fertilization on yielding and antioxidant activity of lavender (Lavandula angustifolia Mill.). Acta Scientiarum Polonorum Hortorum Cultus 7(2):33-40.
Blainski A, Lopes GC, Palazzodemello JC (2013). Application and analysis of the Folin Ciocalteu method for the determination of the total phenolic content from Limonium Brasiliense L. Molecules 18:6852-6865. https://doi.org/10.3390/molecules18066852
Bradford MM (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:248-254. https://doi.org/10.1016/0003-2697(76)90527-3
Cantor M, Vlas N, Szekely-Varga Z, Jucan D, Zaharia A (2018). The influence of distillation time and the flowering phenophase on quantity and quality of the essential oil of Lavandula angustifolia cv. ‘Codreanca’. Romanian Biotechnological Letters 23(6):14146. https://doi.org/10.26327/RBL2018.192
Carrasco A, Martinez-Gutierrez R, Tomas V, Tudela J (2016). Lavandula angustifolia and Lavandula latifolia essential oils from Spain: Aromatic profile and bioactivities. Planta Medica 82(01/02):163-170. https://doi.org/10.1055/s-0035-1558095
Carrasco-Ríos L, Pinto M (2014). Effect of salt stress on antioxidant enzymes and lipid peroxidation in leaves in two contrasting corn, ‘Lluteno’ and ’Jubilee’. Chilean Journal of Agricultural Research 74(1):89-95. https://dx.doi.org/10.4067/S0718-58392014000100014
Chan Z, Yokawa K, Kim W-Y, Song C-P (2016). ROS Regulation during plant abiotic stress responses. Frontiers in plant science 7:1536. https://doi.org/10.3389/fpls.2016.01536
Chutipaijit S (2016). Changes in physiological and antioxidant activity of indica rice seedlings in response to mannitol-induced osmotic stress. Chilean Journal of Agricultural Research 76(4):455-462. https://dx.doi.org/10.4067/S0718-58392016000400009
Conell JP, Mullet JE (1986). Pea chloroplast glutathione reductase: Purification and characterization Plant Physiology 82:351-356. https://doi.org/10.1104/pp.82.2.351
Couto N, Wood J, Barber J (2016). The role of glutathione reductase and related enzymes on cellular redox homoeostasis network. Free Radical Biology and Medicine 95:27-42. https://doi.org/10.1016/j.freeradbiomed.2016.02.028
Croitoru AE, Piticar A, Burada DC (2016). Changes in precipitation extremes in Romania. Quaternary International 415:325-335. https://doi.org/10.1016/j.quaint.2015.07.028
Del Rio LA, Palma JM, Sandalio LM, Corpas GM, Bueno P, López-Huertas E (1996). Peroxisomes as a source of superoxide and hydrogen peroxide in stressed plants. Biochemical Society Transactions 24:434-438. https://doi.org/10.1042/bst0240434
Ding F, Wang G, Wang M, Zhang S (2018). Exogenous melatonin improves tolerance to water deficit by promoting cuticle formation in tomato plants. Molecules 23:1605. https://doi.org/10.3390/molecules23071605
Evelin H, Kapoor R (2014). Arbuscular mycorrhizal symbiosis modules antioxidant response in salt stressed Trigonella foenum-graecum plants. Mycorrhiza 24:197-208. https://doi.org/10.1007/s00572-013-0529-4
Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, … Ihsan MZ (2017). Crop production under drought and heat stress: plant responses and management options. Frontiers in Plant Science 8:1147. https://doi.org/10.3389/fpls.2017.01147
Forni C, Duca D, Glick BR (2016). Mechanisms of plant response to salt and drought stress and their alteration by rhizobacteria. Plant and Soil 410:335-356. https://doi.org/10.1007/s11104-016-3007-x
Gharsallah C, Fakhfakh H, Grubb D, Gorsane F (2016). Effect of salt stress on ion concentration, proline content, antioxidant enzyme activities and gene expression in tomato cultivars. AoB Plants 8. https://doi.org/10.1093/aobpla/plw055
Gil R, Bautista I, Boscaiu M, Lidón A, Wankhade S, Sánchez H, … Vicente O (2014). Responses of five Mediterranean halophytes to seasonal changes in environmental conditions. AoB Plants 6. https://doi.org/10.1093/aobpla/plu049
Gill SS, Tuteja N (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48:909-930. https://doi.org/10.1016/j.plaphy.2010.08.016
Goharrizi KJ, Moosavi SS, Amirmahani F, Salehi F, Nazari M (2020). Assessment of changes in growth traits, oxidative stress parameters, and enzymatic and non-enzymatic antioxidant defense mechanisms in Lepidium draba plant under osmotic stress induced by polyethylene glycol. Protoplasma 257:459-473. https://doi.org/10.1007/s00709-019-01457-0
Hendawy SF, Khalid KA (2005). Response of sage (Salvia officinalis L.) plants to zinc application under different salinity levels. Journal of Applied Sciences Research 1:147-155.
Hoagland DR, Arnon DI (1950). The water-culture method for growing plants without soil. In California Agricultural Experiment Station Publications Series; College of Agriculture, University of California: Davis, CA, USA.
Hodges DM, Delong JM, Forney CF, Prange RK (1999). Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604-611. https://doi.org/10.1007/s004250050524
Huang H, Ullah F, Zhou D-X, Yi M, Zhao Y (2019). Mechanisms of ROS regulation of plant development and stress responses. Frontiers in Plant Science 10:800. https://doi.org/10.3389/fpls.2019.00800
Hussain M, Park HW, Farooq M, Jabran K, Lee DJ (2013). Morphological and physiological basis of salt resistance in different rice genotypes. International Journal of Agriculture and Biology 15:113-118.
Irimia LM, Patriche CV, Roșca B (2018). Climate change impact on climate suitability for wine production in Romania. Theoretical and Applied Climatology 133(1-2):1-14. https://doi.org/10.1007/s00704-017-2156-z
Kangasjärvi S, Lepistö A, Hännikäinen K, Piippo M, Luomala EM, Aro EM, Rintamäki E (2008). Diverse roles for chloroplast stromal and thylakoidbound ascorbate peroxidases in plant stress responses. Biochemical Journal 412:275-285. https://doi.org/10.1042/BJ20080030
Kaur G, Asthir B (2016). Molecular responses to drought stress in plants. Biologia Plantarum 61(2):201-209. https://doi.org/10.1007/s10535-016-0700-9
Kıvrak Ş (2018). Essential oil composition and antioxidant activities of eight cultivars of Lavender and Lavandin from western Anatolia. Industrial Crops and Products, 117:88-96. https://doi.org/10.1016/j.indcrop.2018.02.089
Koulivand PH, Ghadiri MK, Gorji A (2013). Lavender and the nervous system. Evidence-Based Complementary and Alternative Medicine 10. https://doi.org/10.1155/2013/681304
Kusvuran S, Kiran S, Ellialtioglu SS (2016). Antioxidant enzyme activities and abiotic stress tolerance relationship in vegetable crops. Abiotic and biotic stress in plants-recent advances and future perspectives, 1st ed.; InTech: Croatia pp 481-503.
Lis-Balchin M (2002). Lavender: The genus Lavandula. Taylor and Francis Inc. (1st ed), New York.
Lis-Balchin M (2012). Lavender. In: Handbook of Herbs and Spices. Elsevier, Amsterdam, The Netherlands, pp 329-347.
Matysiak B, Nogowska A (2016). Impact of fertilization strategies on the growth of lavender and nitrates leaching to environment. Horticultural Science 43(2):76-83. https://doi.org/10.17221/12/2015-HORTSCI
Meier U (2001). Growth stages of mono-and dicotyledonous plants. BBCH Monograph Federal Biological Research Centre for Agriculture and Forestry (2nd ed), Germany.
Miller G, Shulaev V, Mittler R (2008). Reactive oxygen signalling and abiotic stress. Physiologia Plantarum 133(3):481-489. https://doi.org/10.1111/j.1399-3054.2008.01090.x
Mittal N, Thakur S, Verma H, Kaur A (2018). Interactive effect of salinity and ascorbic acid on Brassica rapa L. plants. Global Journal of Bio-Science and Biotechnology 7:27-29.
Mokhtarzadeh S, Hajyzadeh M, Ahmad H, Khawar KM (2013). The problems in acclimatisation of in vitro multiplied plants of Lavandula angustifolia Miller under field conditions. Journal of Biotechnology 988:71-76. https://doi.org/10.17660/actahortic.2013.988.6
Morales M, Munné-Bosch S (2019). Malondialdehyde: Facts and artifacts. Plant Physiology 180(3):1246-1250. https://doi.org/10.1104/pp.19.00405
Munns R, Tester M (2008). Mechanisms of salinity tolerance. Annual Review of Plant Biology 59:651-681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Nakano Y, Asada K (1981). Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant and Cell Physiology 22:867-888. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Nareshkumar A, Subbarao S, Vennapusa AR, Ashwin V, Banarjee R, Kulkarni MJ, … Udayakumar M (2020). Enzymatic and non-enzymatic detoxification of reactive carbonyl compounds improves the oxidative stress tolerance in cucumber, tobacco and rice seedlings. Journal of Plant Growth Regulation 39:1359-1372. https://doi.org/10.1007/s00344-020-10072-w
Omamt EN, Hammes PS, Robbertse PJ (2006). Differences in salinity tolerance for growth and water-use efficiency in some amaranth (Amaranthus spp.) genotypes. New Zealand Journal of Crop and Horticultural Science 34:11-22. https://doi.org/10.1080/01140671.2006.9514382
Pisulewska E, Puchalska H, Zaleski T, Janeczko Z (2009). Effect of environmental conditions on yield and quality of narrow-leaved lavender (Lavandula angustifolia Mill). Ecological Chemistry and Engineering 16(7):845-854.
Plesa IM, González-Orenga S, Al Hassan M, Sestras AF, Vicente O, Prohens J, … Boscaiu M (2018). Effects of drought and salinity on European larch (Larix decidua Mill.) seedlings. Forests 9:320, https://doi.org/10.3390/f9060320
Prăvălie R, Sîrodoev I, Patriche C, Roșca B, Piticar A, Bandoc G, … Mănoiu V (2020). The impact of climate change on agricultural productivity in Romania. A country-scale assessment based on the relationship between climatic water balance and maize yields in recent decades. Agricultural Systems 179:102767. https://doi.org/10.1016/j.agsy.2019.102767
Prusinowska R, Śmigielski KB (2014). Composition, biological properties and therapeutic effects of lavender (Lavandula angustifolia L). A review. Herba Polonica 60(2):56-66. https://doi.org/10.2478/hepo-2014-0010
Rao MPN, Dong Z-Y, Xiao M, Li W-J (2019). Effect of salt stress on plants and role of microbes in promoting plant growth under salt stress. In: Biocontrol of Lepidopteran Pests, Springer: Cham, Germany pp 423-435. https://doi.org/10.1007/978-3-030-18975-4_18
Rodríguez-Calzada T, Qian M, Strid Å, Neugart S, Schreiner M, Torres-Pacheco I, Guevara-González RG (2019). Effect of UV-B radiation on morphology, phenolic compound production, gene expression, and subsequent drought stress responses in chili pepper (Capsicum annuum L.). Plant Physiology and Biochemistry 134:94-102. https://doi.org/10.1016/j.plaphy.2018.06.025
Seidler-Àoīykowska K, Mordalski R, Kucharski W, Kċdzia B, Bocianowski J (2014). Yielding and quality of lavender flowers (Lavandula angustifolia Mill.) from organic cultivation. Acta Scientarum Polonorum Hortorum Cultus 13(6):173-183.
Shah A, Smith DL (2020). Flavonoids in agriculture: chemistry and roles in biotic and abiotic stress responses, and microbial associations. Agronomy 10:1209. https://doi.org/10.3390/agronomy10081209
Shan C, Zhou Y, Liu M (2015). Nitric oxide participates in the regulation of the ascorbate-glutathione cycle by exogenous jasmonic acid in the leaves of wheat seedlings under drought stress. Protoplasma 252(5):1397-1405. https://doi.org/10.1007/s00709-015-0756-y
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012). Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany 26. https://doi.org/10.1155/2012/217037
Sharma P, Kharkwal AC, Abdin MZ, Varma A (2016). Piriformospora indica-mediated salinity tolerance in Aloe vera plantlets. Symbiosis 72:103-115. https://doi.org/10.1007/s13199-016-0449-0
Shi QH, Zhu ZJ (2008). Effects of exogenous salicylic acid on manganese toxicity, element contents and antioxidative system in cucumber. Environmental and Experimental Botany 63:317-326. https://doi.org/10.1016/j.envexpbot.2007.11.003
Szekely-Varga Z, González-Orenga S, Cantor M, Jucan D, Boscaiu M, Vicente O (2020). Effects of drought and salinity on two commercial varieties of Lavandula angustifolia Mill. Plants 9:637. https://doi.org/10.3390/plants9050637
The Plant List, Version 1, Published on the Internet. Retrieved 2020 July 27 from http://www.theplantlist.org
Todea (Morar) IM, González-Orenga S, Boscaiu M, Plazas M, Sestras AF, Prohens J, … Sestras RE (2020). Responses to water deficit and salt stress in silver fir (Mill.) seedlings. Forests 11:395. https://doi.org/10.3390/f11040395
Upson T, Andrews S (2004). The genus Lavandula. Timber Press Inc. (1st ed), USA.
Van Breusegem F, Vranová E, Dat Jf, Inzé D (2001). The role of active oxygen species in plant signal transduction. Plant Science 161:405-414. https://doi.org/10.1016/S0168-9452(01)00452-6
Wang CQ, Li RC (2008). Enhancement of superoxide dismutase activity in the leaves of white clover (Trifolium repens L.) in response to polyethylene glycol-induced water stress. Acta Physiologiae Plantarum 30:841-847. http://doi.org/10.1007/s11738-008-0189-8
Wang P, Sun X, Li C, Wei Z, Liang D, Ma F (2013). Long-term exogenous application of melatonin delays drought-induced leaf senescence in apple. Journal of Pineal Research 54:292-302. https://doi.org/10.1111/jpi.12017
Wells R, Truong F, Adal AM, Sarker LS, Mahmoud SS (2018). Lavandula essential oils: a current review of applications in medicinal, food, and cosmetic industries of lavender. Natural Product Communications 13(10):1403-1417. https://doi.org/10.1177/1934578X1801301038
Xia H, Ni Z, Hu R, Lin L, Deng H, Wang J, … Liao M (2020). Melatonin alleviates drought stress by a non-enzymatic and enzymatic antioxidative system in kiwifruit seedlings. International Journal of Molecular Sciences 21(3):852. https://doi.org/10.3390/ijms21030852
Yang Y, Han C, Liu Q, Lin B, Wang J (2008). Effect of drought and low light on growth and enzymatic antioxidant system of Picea asperata seedlings. Acta Physiologiae Plantarum 30:433-440. http://doi.org/10.1007/s11738-008-0140-z
Zgallaï H, Stepp K, Lemeur R (2006). Effects of different levels of water stress on leaf water potential, stomatal resistance, protein and chlorophyll content and certain anti‐oxidative enzymes in tomato plants. Journal of Integrative Plant Biology 48:679-685. https://doi.org/10.1111/j.1744-7909.2006.00272.x
Zhishen J, Mengcheng T, Jianming W (1999). The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chemistry 64:555-559. https://doi.org/10.1016/S0308-8146(98)00102-2
Zhou C, Busso CA, Yang YG, Zhang Z, Wang ZW, Yang YF, Han XG (2017). Effect of mixed salt stress on malondialdehyde, proteins and antioxidant enzymes of Leymus chinensis in three leaf colors. Phyton - International Journal of Experimental Botany 86:205-213.
Zhu Y, Luo X, Nawaz G, Yin J, Yang J (2020). Physiological and biochemical responses of four cassava cultivars to drought stress. Scientific Reports 10(1):6968. https://doi.org/10.1038/s41598-020-63809-8
How to Cite
Open Access Journal:
The journal allows the author(s) to retain publishing rights without restriction. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles, or use them for any other lawful purpose, without asking prior permission from the publisher or the author.