Foliar application of ascorbic acid enhances growth and yield of lettuce (Lactuca sativa) under saline conditions by improving antioxidant defence mechanism
Safina Naz A , Abubakar Mushtaq A , Sajid Ali A , Hafiza Muniba Din Muhammad A , Bushra Saddiq B , Riaz Ahmad C , Faisal Zulfiqar
D , Faisal Hayat E , Rahul Kumar Tiwari F , Milan Kumar Lal F and Muhammad Ahsan Altaf G *
A Department of Horticulture, Bahauddin Zakariya University, Multan 60800, Pakistan.
B Faculty of Agriculture and Environmental Science, Islamia University of Bahawalpur, Bahawalpur 63100, Pakistan.
C Department of Horticulture, The University of Agriculture, Dera Ismail Khan, Pakistan.
D Department of Horticultural Sciences, The Islamia University of Bahawalpur, Pakistan.
E College of Horticulture and Landscape Architecture at Zhongkai University of Agriculture and Engineering, Guangzhou 510225, P. R. China.
F ICAR-Central Potato Research Institute, Shimla 171001, India.
G College of Horticulture, Hainan University, Haikou, Hainan 570228, China.
Abstract
Lettuce (Lactuca sativa L.) production is low because of different environmental stresses. Salt stress significantly reduces lettuce growth and yield. Foliar application of ascorbic acid is considered as a possible way to mitigate the adverse salinity effects on plants. This current study investigated the effect of foliar spray of ascorbic acid (control, 100, 200, 300 and 400 mg/L) to mitigate negative effects of salinity (0, 50, 100 and 150 mM NaCl) in lettuce plants in 2019 and 2020. Salinity level of 200 mM NaCl significantly reduced growth and yield traits; i.e. leaf length and diameter, number of leaves, fresh plant weight, number of roots, root length and root dry weight and these traits increased under foliar application of ascorbic acid concentration of 400 mg/L. Two salinity levels (150 and 200 mM NaCl) × 400 mg/L ascorbic acid enhanced superoxide dismutase (SOD) content in lettuce plants. Peroxidase (POD) content increased in 200 mM NaCl and 400 mg/L ascorbic acid. Catalase (CAT) content increased in 100, 150 and 200 mM NaCl and 400 mg/L ascorbic acid. Ascorbic acid was significantly greater in 200 mM NaCl and 400 mg/L ascorbic acid. Phenolic content was the maximum in 200 mM NaCl and 300 mg/L and 400 mg/L ascorbic acid. Titratable acidity was higher in 0, 50, 100, 150 and 200 mM NaCl and control of ascorbic acid. We conclude that ascorbic acid had potential to mitigate the adverse effects of salinity by reducing oxidative injury in agricultural crops especially lettuce.
Keywords: abiotic stress, antioxidants, ascorbic acid, lettuce, oxidative stress, plant growth, root growth, salinity.
References
Ahmad P, Ahanger MA, Alyemeni MN, Wijaya L, Egamberdieva D, Bhardwaj R, Ashraf M (2017) Zinc application mitigates the adverse effects of NaCl stress on mustard [Brassica juncea (L.) czern & coss] through modulating compatible organic solutes, antioxidant enzymes, and flavonoid content. Journal of Plant Interactions 12, 429-437.
| Crossref | Google Scholar |
Ahmad R, Anjum MA, Balal RM (2020) From markers to genome based breeding in horticultural crops: an overview. Phyton 89, 183-204.
| Crossref | Google Scholar |
Ahmed S, Ahmed S, Roy SK, Woo SH, Sonawane KD, Shohael AM (2019) Effect of salinity on the morphological, physiological and biochemical properties of lettuce (Lactuca sativa L.) in Bangladesh. Open Agriculture 4, 361-373.
| Crossref | Google Scholar |
Alam M, Khan MA, Imtiaz M, Khan MA, Naeem M, Shah SA, Samiullah , Ahmad SH, Khan L (2020) Indole-3-acetic acid rescues plant growth and yield of salinity stressed tomato (Lycopersicon esculentum L.). Gesunde Pflanzen 72, 87-95.
| Crossref | Google Scholar |
Alayafi AAM (2020) Exogenous ascorbic acid induces systemic heat stress tolerance in tomato seedlings: transcriptional regulation mechanism. Environmental Science and Pollution Research 27, 19186-19199.
| Crossref | Google Scholar |
Ali M, Niaz Y, Abbasi GH, Ahmad S, malik Z, Kamran M, Iqbal R, Zaheer MS, Bodlah MA, Nawaz M, Ali H, Aamer M, Ayaz M (2021) Exogenous zinc induced NaCl tolerance in Okra (Abelmoschus Esculentus) by ameliorating osmotic stress and oxidative metabolism. Communications in Soil Science and Plant Analysis 52, 743-755.
| Crossref | Google Scholar |
Al-Maskri A, Al-Kharusi L, Al-Miqbali H, Khan MM (2010) Effects of salinity stress on growth of lettuce (Lactuca sativa) under closed-recycle nutrient film technique. International Journal of Agricultural Biology 12, 377-380.
| Google Scholar |
Al-swedi FG, Alshamari M, Al Zaidi IHM, Rihan HZ (2020) Impact of salinity stress on seed germination in lettuce (Lactuca Sativa). Journal of Research on the Lepidoptera 51, 374-385.
| Crossref | Google Scholar |
Anjum MA (2010) Response of Cleopatra mandarin seedlings to a polyamine-biosynthesis inhibitor under salt stress. Acta Physiologiae Plantarum 32, 951-959.
| Crossref | Google Scholar |
Arif Y, Singh P, Siddiqui H, Bajguz A, Hayat S (2020) Salinity induced physiological and biochemical changes in plants: an omic approach towards salt stress tolerance. Plant Physiology and Biochemistry 156, 64-77.
| Crossref | Google Scholar |
Azarmi F, Mozafari V, Abbaszadeh Dahaji P, Hamidpour M (2016) Biochemical, physiological and antioxidant enzymatic activity responses of pistachio seedlings treated with plant growth promoting rhizobacteria and Zn to salinity stress. Acta Physiologiae Plantarum 38, 21.
| Crossref | Google Scholar |
Barzegar T, Fateh M, Razavi F (2018) Enhancement of postharvest sensory quality and antioxidant capacity of sweet pepper fruits by foliar applying calcium lactate and ascorbic acid. Scientia Horticulturae 241, 293-303.
| Crossref | Google Scholar |
Billah M, Rohman MM, Hossain N, Shalim Uddin M (2017) Exogenous ascorbic acid improved tolerance in maize (Zea mays L.) by increasing antioxidant activity under salinity stress. African Journal of Agricultural Research 12, 1437-1446.
| Crossref | Google Scholar |
Breś W, Kleiber T, Markiewicz B, Mieloszyk E, Mieloch M (2022) The effect of NaCl stress on the response of lettuce (Lactuca sativa L.). Agronomy 12(2), 244.
| Crossref | Google Scholar |
Camejo D, Frutos A, Mestre TC, del Carmen Piñero M, Rivero RM, Martínez V (2020) Artificial light impacts the physical and nutritional quality of lettuce plants. Horticulture, Environment, and Biotechnology 61, 69-82.
| Crossref | Google Scholar |
Chance B, Maehly AC (1955) Assay of catalases and peroxidases. Methods in Enzymology 2, 764-775.
| Crossref | Google Scholar |
Chen Y, Huang L, Liang X, Dai P, Zhang Y, Li B, Lin X, Sun C (2020) Enhancement of polyphenolic metabolism as an adaptive response of lettuce (Lactuca sativa) roots to aluminum stress. Environmental Pollution 261, 114230.
| Crossref | Google Scholar |
Choi W-G, Toyota M, Kim S-H, Hilleary R, Gilroy S (2014) Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proceedings of the National Academy of Science United States America 111, 6497-6502.
| Crossref | Google Scholar |
Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. The Plant Journal 90, 856-867.
| Crossref | Google Scholar |
Delavar K, Ghanati F, Behmanesh M, Zare-Maivan H (2018) Physiological parameters of silicon-treated maize under salt stress conditions. Silicon 10, 2585-2592.
| Crossref | Google Scholar |
Dlamini BB, Wahome PK, Masarirambi MT, Oseni TO, Nxumalo KA (2019) Effects of salinity on the vegetative growth of tuberose (Polianthes tuberosa L.). Journal of Horticultural Science Ornamental Plants 11, 144-151.
| Crossref | Google Scholar |
Dolatabadian A, Saleh Jouneghani R (2009) Impact of exogenous ascorbic acid on antioxidant activity and some physiological traits of common bean subjected to salinity stress. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 37, 165-172.
| Crossref | Google Scholar |
El-Araby HG, El-Hefnawy SFM, Nassar MA, Elsheery NI (2020) Comparative studies between growth regulators and nanoparticles on growth and mitotic index of pea plants under salinity. African Journal of Biotechnology 19, 564-575.
| Crossref | Google Scholar |
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiology 155, 2-18.
| Crossref | Google Scholar |
Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology 59, 309-314.
| Crossref | Google Scholar |
Hajivar B, Zare Bavani MR (2020) The alleviation of the adverse effects of salinity stress in the tomato (Solanum lycopersicum L. cv. Mobin) by application of ascorbic acid. Journal of Plant Productions 43, 349-362.
| Crossref | Google Scholar |
Hameed A, Gulzar S, Aziz I, Hussain T, Gul B, Khan MA (2015) Effects of salinity and ascorbic acid on growth, water status and antioxidant system in a perennial halophyte. AoB Plants 7, plv004.
| Crossref | Google Scholar |
Ighodaro OM, Akinloye OA (2018) First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defence grid. Alexandria Journal of Medicine 54, 287-293.
| Crossref | Google Scholar |
Kamal MA, Saleem MF, Shahid M, Awais M, Khan HZ, Ahmed K (2017) Ascorbic acid triggered physiochemical transformations at different phenological stages of heat-stressed Bt cotton. Journal of Agronomy and Crop Science 203, 323-331.
| Crossref | Google Scholar |
Kaya C, Akram NA, Ashraf M, Sonmez O (2018) Exogenous application of humic acid mitigates salinity stress in maize (Zea mays L.) plants by improving some key physico-biochemical attributes. Cereal Research Communications 46, 67-78.
| Crossref | Google Scholar |
Khalid MF, Hussain S, Anjum MA, Ahmad S, Ali MA, Ejaz S, Morillon R (2020) Better salinity tolerance in tetraploid vs diploid volkamer lemon seedlings is associated with robust antioxidant and osmotic adjustment mechanisms. Journal of Plant Physiology 244, 153071.
| Crossref | Google Scholar |
Kim SY, Lim JH, Park MR, Kim YJ, Park TI, Seo YW, Choi KG, Yun SJ (2005) Enhanced antioxidant enzymes are associated with reduced hydrogen peroxide in barley roots under saline stress. Journal of Biochemistry and Molecular Biology 38, 218-224.
| Crossref | Google Scholar |
Laifa I, Hajji M, Farhat N, Elkhouni A, Smaoui A, M’nif A, Hamzaoui AH, Savouré A, Abdelly C, Zorrig W (2021) Beneficial effects of silicon (Si) on sea barley (Hordeum marinum Huds.) under salt stress. Silicon 13, 4501-4517.
| Crossref | Google Scholar |
Liang W, Ma X, Wan P, Liu L (2018) Plant salt-tolerance mechanism: a review. Biochemical and Biophysical Research Communications 495, 286-291.
| Crossref | Google Scholar |
Mahmoudi H, Kaddour R, Huang J, Nasri N, Olfa B, M’Rah S, Hannoufa A, Lachaâl M, Ouerghi Z (2011) Varied tolerance to NaCl salinity is related to biochemical changes in two contrasting lettuce genotypes. Acta Physiologiae Plantarum 33(5), 1613-1622.
| Crossref | Google Scholar |
Mahpara S, Shahnawaz M, Rehman K, Ahmad R, Khan FU (2019) Nitrogen fertilization induced drought tolerance in sunflower: a review. Pure and Applied Biology 8(2), 1675-1683.
| Crossref | Google Scholar |
Min K, Chen K, Arora R (2020) A metabolomics study of ascorbic acid-induced in situ freezing tolerance in spinach (Spinacia oleracea L.). Plant Direct 4, e00202.
| Crossref | Google Scholar |
Mittler R (2017) ROS are good. Trends in Plant Sciences 22, 11-19.
| Crossref | Google Scholar |
Mushtaq A, Khan Z, Khan S, Rizwan S, Jabeen U, Bashir F, Ismail T, Anjum S, Masood A (2020) Effect of silicon on antioxidant enzymes of wheat (Triticum aestivum L.) grown under salt stress. Silicon 12, 2783-2788.
| Crossref | Google Scholar |
Naz H, Akram NA, Ashraf M (2016) Impact of ascorbic acid on growth and some physiological attributes of cucumber (Cucumis sativus) plants under water-deficit conditions. Pakistan Journal of Botany 48, 877-883.
| Google Scholar |
Negrão S, Schmöckel SM, Tester M (2017) Evaluating physiological responses of plants to salinity stress. Annals of Botany 119, 1-11.
| Crossref | Google Scholar |
Niu J, Liu C, Huang M, Liu K, Yan D (2021) Effects of foliar fertilization: a review of current status and future perspectives. Journal of Soil Science and Plant Nutrition 21, 104-118.
| Crossref | Google Scholar |
Noreen S, Faiz S, Akhter MS, Shah KH (2019) Influence of foliar application of osmoprotectants to ameliorate salt stress in sunflower (Helianthus annuus L.). Sarhad Journal of Agriculture 35, 1316-1325.
| Crossref | Google Scholar |
Noreen S, Sultan M, Akhter MS, Shah KH, Ummara U, Manzoor H, Ulfat M, Alyemeni MN, Ahmad P (2021) Foliar fertigation of ascorbic acid and zinc improves growth, antioxidant enzyme activity and harvest index in barley (Hordeum vulgare L.) grown under salt stress. Plant Physiology and Biochemistry 158, 244-254.
| Crossref | Google Scholar |
Omaye ST, David Turnbull J, Sauberlich HE (1979) Selected methods for the determination of ascorbic acid in animal cells, tissues, and fluids. Methods in Enzymology 62, 3-11.
| Crossref | Google Scholar |
Ozgen M, Scheerens JC, Reese RN, Miller RA (2010) Total phenolic, anthocyanin contents and antioxidant capacity of selected elderberry (Sambucus canadensis L.) accessions. Pharmacognosy Magazine 6, 198-203.
| Google Scholar |
Rabiei Z, Hosseini SJ, Pirdashti H, Hazrati S (2020) Physiological and biochemical traits in coriander affected by plant growth-promoting rhizobacteria under salt stress. Heliyon 6, e05321.
| Crossref | Google Scholar |
Rouphael Y, Kyriacou MC (2018) Enhancing quality of fresh vegetables through salinity eustress and biofortification applications facilitated by soilless cultivation. Frontiers in Plant Science 9, 1254.
| Crossref | Google Scholar |
Salehi H, Bahadoran M (2015) Growth and flowering of two tuberose (Polianthes tuberosa L.) cultivars under deficit irrigation by saline water. Journal of Agricultural Science and Technology 17, 415-426.
| Google Scholar |
Shahzad S, Ali S, Ahmad R, Ercisli S, Anjum MA (2022) Foliar application of silicon enhances growth, flower yield, quality and postharvest life of tuberose (Polianthes tuberosa L.) under saline conditions by improving antioxidant defense mechanism. Silicon 14, 1511-1518.
| Crossref | Google Scholar |
Shin YK, Bhandari SR, Jo JS, Song JW, Cho MC, Yang EY, Lee JG (2020) Response to salt stress in lettuce: changes in chlorophyll fluorescence parameters, phytochemical contents, and antioxidant activities. Agronomy 10, 1627.
| Crossref | Google Scholar |
Skłodowska M, Gapińska M, Gajewska E, Gabara B (2009) Tocopherol content and enzymatic antioxidant activities in chloroplasts from NaCl-stressed tomato plants. Acta Physiologiae Plantarum 31, 393-400.
| Crossref | Google Scholar |
Soerjomataram I, Oomen D, Lemmens V, Oenema A, Benetou V, Trichopoulou A, Coebergh JW, Barendregt J, de Vries E (2010) Increased consumption of fruit and vegetables and future cancer incidence in selected European countries. European Journal of Cancer 46, 2563-2580.
| Crossref | Google Scholar |
Tang X, Mu X, Shao H, Wang H, Brestic M (2015) Global plant-responding mechanisms to salt stress: physiological and molecular levels and implications in biotechnology. Critical Reviews in Biotechnology 35, 425-437.
| Crossref | Google Scholar |
Tanveer K, Gilani S, Hussain Z, Ishaq R, Adeel M, Ilyas N (2020) Effect of salt stress on tomato plant and the role of calcium. Journal of Plant Nutrition 43, 28-35.
| Crossref | Google Scholar |
Vighi IL, Benitez LC, Amaral MN, Moraes GP, Auler PA, Rodrigues GS, Deuner S, Maia LC, Braga EJB (2017) Functional characterization of the antioxidant enzymes in rice plants exposed to salinity stress. Biologia Plantarum 61, 540-550.
| Crossref | Google Scholar |
Wang S, Melnyk JP, Tsao R, Marcone MF (2011) How natural dietary antioxidants in fruits, vegetables and legumes promote vascular health. Food Research International 44, 14-22.
| Crossref | Google Scholar |
Wang Q, Liang X, Dong Y, Xu L, Zhang X, Kong J, Liu S (2013) Effects of exogenous salicylic acid and nitric oxide on physiological characteristics of perennial ryegrass under cadmium stress. Journal of Plant Growth Regulation 32, 721-731.
| Crossref | Google Scholar |
Wang Y-H, Zhang G, Chen Y, Gao J, Sun Y-R, Sun M-F, Chen J-P (2019) Exogenous application of gibberellic acid and ascorbic acid improved tolerance of okra seedlings to NaCl stress. Acta Physiologiae Plantarum 41, 93.
| Crossref | Google Scholar |
Weisany W, Sohrabi Y, Heidari G, Siosemardeh A, Ghassemi-Golezani K (2012) Changes in antioxidant enzymes activity and plant performance by salinity stress and zinc application in soybean (Glycine max L.). Plant Omics 5, 60-67.
| Google Scholar |
Weisany W, Sohrabi Y, Heidari G, Siosemardeh A, Badakhshan H (2014) Effects of zinc application on growth, absorption and distribution of mineral nutrients under salinity stress in soybean (Glycine max L.). Journal of Plant Nutrition 37, 2255-2269.
| Crossref | Google Scholar |
Zeeshan M, Lu M, Sehar S, Holford P, Wu F (2020) Comparison of biochemical, anatomical, morphological, and physiological responses to salinity stress in wheat and barley genotypes deferring in salinity tolerance. Agronomy 10, 127.
| Crossref | Google Scholar |
Zhang T, Shi Z, Zhang X, Zheng S, Wang J, Mo J (2020) Alleviating effects of exogenous melatonin on salt stress in cucumber. Scientia Horticulturae 262, 109070.
| Crossref | Google Scholar |
