Environmental Science and Pollution Research

, Volume 25, Issue 30, pp 30199–30211 | Cite as

Effect of some osmoregulators on photosynthesis, lipid peroxidation, antioxidative capacity, and productivity of barley (Hordeum vulgare L.) under water deficit stress

  • Khaled A. A. Abdelaal
  • Yaser M. Hafez
  • Mohamed M. El-Afry
  • Dalia S. Tantawy
  • Tarek AlshaalEmail author
Research Article


Water deficit stress is an abiotic stress that causes reductions in growth and yield of many field crops around the world. The present research was aimed to elucidate the mitigating efficiency of exogenous application of select osmoregulators and biostimulants, i.e., potassium dihydrogen phosphate, actosol® (humic acid), Amino more (amino acids), and Compound fertilizer, applied as a spray that reached both foliage and the soil, on growth characteristics, antioxidant capacity, and productivity of barley (Hordeum vulgare L. Giza123) under water deficit stress during two successive growing seasons of field experiments in Egypt. Water deficit resulted in stress as estimated by stress indicators and decreased growth and poor health and development as reflected in statistically significant decreases in chlorophyll a and b and major nutrient (NPK) levels in tissues, stem length, number of leaves, and fresh and dry mass as well as yield components such as spike length, grains per spike, biological yield, grain yield, and 1000-grain weight. As a response to water deficit stress, reactive oxygen species (ROS, i.e., superoxide and hydrogen peroxide) levels increased significantly resulting in lipid peroxidation and decreased membrane integrity and significant increases in antioxidant enzymes such as catalase (CAT), polyphenol oxidase (PPO), and peroxidase (POX). All four treatments alleviated the detrimental impacts of water deficit stress as evidenced by statistically significantly increased photosynthetic pigment concentration, tissue NPK levels, growth, and yield parameters compared to the water deficit-stressed control, while the stress responses were significantly reduced. The osmoregulators used either partially restored the growth and yield of osmotic-stressed barley plants or certain treatments enhanced them. All osmoregulators tested mitigated the adverse impacts of water deficit stress on barley plants, but the highest induction was found when plants were treated with actosol®. The beneficial effects of the osmoregulators tested were the strongest overall in the order actosol® ˃ potassium dihydrogen phosphate ˃ Amino more ˃ Compound fertilizer.


Hordeum vulgare L. Water deficit stress Osmoregulators Antioxidant enzymes Reactive oxygen species Electrolyte leakage Lipid peroxidation 



Reactive oxygen species




Hydrogen peroxide








Polyphenol oxidase



The authors would like to thank colleagues at Plant Pathology and Biotechnology Lab. (Accredited according to ISO/17025) and EPCRS Excellence Centre (certified according to ISO/9001, ISO/14001 and OHSAS/18001), Department of Agricultural Botany, Faculty of Agriculture, Kafrelsheikh University, Kafr El-Sheikh, Egypt. The authors would like to thank Prof. Mihály Czakó for the help, valuable suggestions, and discussions.

Funding information

This research was co-financed by the ÚNKP-17-4 New National Excellence Program of the Ministry of Human Capacities. Also, support was given by OTKA KH 124985 and Tempus Public Foundation (TPF), Hungary.


  1. Abd El-Aal FS, Shafeek MR, Ahmed AA, Shaheen AM (2005) Response of growth and yield of onion plants to potassium fertilizer and humic acid. J Agric Sci Mansoura Univ 30(1):441–452Google Scholar
  2. Abd El-Samad HM, Shaddad MAK, Barakat N (2010) The role of amino acids in improvement in salt tolerance of crop plants. J of Stress Physiol and Bioch 6(3):25–37Google Scholar
  3. Abdalla M, El-Khoshiban N (2007) The influence of water stress on growth, relative water content, photosynthetic pigments, some metabolic and hormonal contents of two Triticum aestivum cultivars. J Appl Sci Res 3(12):2062–2074Google Scholar
  4. Abdelaal K (2015a) Effect of salicylic acid and abscisic acid on morpho-physiological and anatomical characters of faba bean plants (Vicia faba L.) under drought stress. J Plant Prod Mansoura Univ 6(11):1771–1788Google Scholar
  5. Abdelaal K (2015b) Pivotal role of bio and mineral fertilizer combinations on morphological, anatomical and yield characters of sugar beet plant (Beta vulgaris L.). Middle East J Agric Res 4(4):717–734Google Scholar
  6. Abdelaal K, Hafez Y, Badr M, Youseef W, Esmaeil S (2014) Biochemical, histological and molecular changes in susceptible and resistant wheat cultivars inoculated with stripe rust fungus Puccinia striiformis f. sp. tritici. Egyp J Biol Pest Control 24:421–429Google Scholar
  7. Abdelaal K, Hafez Y, Sabagh AEL, Saneoka H (2017) Ameliorative effects of Abscisic acid and yeast on morpho-physiological and yield characteristics of maize plant (Zea mays L.) under drought conditions. Fresenius Environ Bull 26(2):7372–7383Google Scholar
  8. Abdelaal K, Omara I, Hafez Y, Esmail S, Sabagh AEL (2018) Anatomical, biochemical and physiological changes in some Egyptian wheat cultivars inoculated with Puccinia graminis f. sp. tritici. Fresenius Environ Bull 27(1):296–305Google Scholar
  9. Ádám A, Farkas T, Somlyai G, Hevesi M, Király Z (1989) Consequence of O2 ·- generation during a bacterially induced hypersensitive reaction in tobacco: deterioration of membrane lipids. Physiol Mol Plant Pathol 34:13–26CrossRefGoogle Scholar
  10. Aebi HE (1983) Catalase. “Methods of Enzymatic Analysis”, 3rd ed. Verlag Chemie, Weinheim, pp 273–286Google Scholar
  11. Al-Fraihat AH, Al-Tabbal JA, Abu-Darwish MS, Alhrout HH, Hasan HS (2018) Response of onion (Allium cepa) crop to foliar application of humic acid under rain-fed conditions. Int J Agric Biol 20(5):1235–1241Google Scholar
  12. Albayrak S, Camas N (2005) Effects of different levels and application times of humic acid on root and leaf yield and yield components of forage turnip (Brassica rapa L.). J Agron 4(2):130–133CrossRefGoogle Scholar
  13. Ali LKM, Elbordiny MM (2009) Response of wheat plants to potassium humate application. J Appl Sci Res 5(9):1202–1209Google Scholar
  14. Alobaidy MG (2008) Effect of putrescine and humic acid on cotton plant growing under salinity stress conditions. M Sc in Agric Sci (Plant Physiology), Cairo University, EgyptGoogle Scholar
  15. ARCTECH Inc (2015) Technical Bulletin # 5 humic acid: a review of characteristics, properties, analytical methods and applications EPA Dialogue Committee Response, 2015(1):
  16. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141(2):391–396CrossRefGoogle Scholar
  17. Aydin A, Kant C, Turan M (2012) Humic acid application alleviate salinity stress of bean (Phaseolus vulgaris L.) plants decreasing membrane leakage. African J Agric Res 7(7):1073–1086Google Scholar
  18. Barati V, Ghadiri H, Zand-Parsa S, Karimian N (2015) Nitrogen and water use efficiencies and yield response of barley cultivars under different irrigation and nitrogen regimes in a semi-arid Mediterranean climate. Arch Agron Soil Sci 61(1):15–32CrossRefGoogle Scholar
  19. Behairy AG, Mahmoud AR, Shafeek MRA, H A, Hafez MM (2015) Growth, yield and bulb quality of onion plants (Allium cepa L.) as affected by foliar and soil application of potassium. Middle East J Agric Res 4(1):60–66Google Scholar
  20. Bettoni MM, Mogor AF, Pauletti V, Goicoechea N (2017) The interaction between mycorrhizal inoculation, humic acids supply and elevated atmospheric CO2 increases energetic and antioxidant properties and sweetness of yellow onion. Hortic Environ Biotechnol 58(5):432–440CrossRefGoogle Scholar
  21. Bettoni MM, Mogor AF, Pauletti V, Goicoechea N, Aranjuelo I, Garmendia I (2016) Nutritional quality and yield of onion as affected by different application methods and doses of humic substances. J Food Compos Anal 51:37–44CrossRefGoogle Scholar
  22. Block RJ (1968) A manual of paper chromatography and paper electrophoresis. Academic Press, New YorkGoogle Scholar
  23. Cakmak I (2005) The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J Plant Nutr Soil Sci 168(4):521–530CrossRefGoogle Scholar
  24. Cao WX, Tibbitts TW (1992) Potassium content effect on growth, gas exchange and mineral accumulation in potatoes. J Plant Nutr 15(9):1359–1371CrossRefGoogle Scholar
  25. Chen G, C Liu, Z Gao, Y Zhang, H Jiang, L Zhu, D Ren, L Yu, G Xu and Q Qian (2017). OsHAK1, a high-affinity potassium transporter, positively regulates responses to drought stress in rice. Front Plant Sci 8Google Scholar
  26. Clarke JM, McCaig TN (1982) Excised-leaf water retention capability as an indicator of drought resistance of Triticum genotypes. Can J Plant Sci 62(3):571–578CrossRefGoogle Scholar
  27. Davenport SB, Gallego SM, Benavides MP, Tomaro ML (2003) Behaviour of anti-oxidant defense system in the adaptive response to salt stress in (Helianthus annuus L.) cell. Plant Growth Reg 40:81–88Google Scholar
  28. Denre M, Ghanti S, Sarkar K (2014) Effect of humic acid application on accumulation of mineral nutrition and pungency in garlic (Allium sativum L.) cultivars. Int J Biotechnol Mol Biol Res 5(2):7–12CrossRefGoogle Scholar
  29. Donald CM, Hamblin J (1976) The biological yield and harvest index of cereals as agronomic and plant breeding criteria. Adv Agron 28:361–405CrossRefGoogle Scholar
  30. Duncan B (1955) Multiple ranges and multiple F-test. Biometrics 11:1–42CrossRefGoogle Scholar
  31. Egilla JN, Davies FT, Boutton TW (2005) Drought stress influences leaf water content, photosynthesis, and water-use efficiency of Hibiscus rosa-sinensis at three potassium concentrations. Photosynthetica 43(1):135–140CrossRefGoogle Scholar
  32. Ekinci M, Esringu A, Dursun A, Yildirim E, Turan M, Karaman MR, Arjumend T (2015) Growth, yield, and calcium and boron uptake of tomato (Lycopersicon esculentum L.) and cucumber (Cucumis sativus L.) as affected by calcium and boron humate application in greenhouse conditions. Turk J Agric For 39(5):613–632CrossRefGoogle Scholar
  33. Fallahi H-R, Ghorbany M, Aghhavani-Shajari M, Samadzadeh A, Asadian AH (2017) Qualitative response of roselle to planting methods, humic acid application, mycorrhizal inoculation and irrigation management. J Crop Improv 31(2):192–208Google Scholar
  34. Farooq M, Wahid A, Lee DJ, Cheema SA, Aziz T (2010) Comparative time course action of the foliar applied Glycinebetaine, salicylic acid, nitrous oxide, brassinosteroids and spermine in improving drought resistance of rice. J Agron Crop Sci 196(5):336–345CrossRefGoogle Scholar
  35. Gómez KA, Gómez AA, I International Rice Research (1984) Statistical procedures for agricultural research. John Wiley & Sons, New YorkGoogle Scholar
  36. Hafez YM, Abdelaal KAA, Eid ME, Mehiar FF (2016) Morpho-physiological and biochemical responses of barley plants (Hordeum vulgare L.) against barley net blotch disease with application of non-traditional compounds and fungicides. Egypt J Biol Pest Control 26(2):261–268Google Scholar
  37. Hafez YM, Bacso R, Kiraly Z, Kuenstler A, Kiraly L (2012) Up-regulation of antioxidants in tobacco by low concentrations of H2O2 suppresses necrotic disease symptoms. Phytopathology 102(9):848–856CrossRefGoogle Scholar
  38. Hafez YM, Mourad RY, Mansour M, Abdelaal KAA (2014) Impact of non-traditional compounds and fungicides on physiological and biochemical characters of barely infected with Blumeria graminis f. sp. hordei under field condtitions. Egypt J Biol Pest Control 24(2):445–453Google Scholar
  39. Hameed A, Bibi N, Akhter J, Lqbal N (2011) Differential changes in antioxidants, proteases, and lipid peroxidation in flag leaves of wheat genotypes under different levels of water deficit conditions. Plant Physiol Biochem 49(2):178–185CrossRefGoogle Scholar
  40. Hammerschmidt R, Nuckles EM, Kuc J (1982) Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletotrichum lagenarium. Physiol Plant Pathol 20(1):73–82CrossRefGoogle Scholar
  41. Han Y, Yin S, Huang L, Wu X, Zeng J, Liu X, Qiu L, Munns R, Chen Z-H and Zhang G (2018) A sodium transporter HvHKT1;1 confers salt tolerance in barley via regulating tissue and cell ion homeostasis. Plant Cell PhysiolGoogle Scholar
  42. Helaly M, Mohammed Z, El-Shaeery N, Abdelaal K, Nofal I (2017) Cucumber grafting onto pumpkin can represent an interesting tool to minimize salinity stress. Physiological and anatomical studies. Middle East J Agric Res 6(4):953–975Google Scholar
  43. Horwitz W (2005). Official methods of analysis of AOAC International. Gaithersburg, Maryland, AOAC InternationalGoogle Scholar
  44. Hueckelhoven R, Fodor J, Preis C, Kogel K-H (1999) Hypersensitive cell death and papilla formation in barley attacked by the powdery mildew fungus are associated with hydrogen peroxide but not with salicylic acid accumulation. Plant Physiol (Rockville) 119(4):1251–1260CrossRefGoogle Scholar
  45. Hussain M, Malik MA, Farooq M, Ashraf MY, Cheema MA (2008) Improving drought tolerance by exogenous application of glycinebetaine and salicylic acid in sunflower. J Agron Crop Sci 194(3):193–199CrossRefGoogle Scholar
  46. Jackson ML (1967) Soil chemical analysis. Prentice-Hall, New DelhiGoogle Scholar
  47. Kant S and Kafkafi U (2002) Potassium and abiotic stresses in plants. Potassium for sustainable crop production. N. S. Pasricha and S. K. Bansal. Gurgaon, India, Potash Institute of India: 233–251Google Scholar
  48. Kaya C, Tuna AL, Ashraf M, Altunlu H (2007) Improved salt tolerance of melon (Cucumis melo L.) by the addition of proline and potassium nitrate. Environ Exp Bot 60(3):397–403CrossRefGoogle Scholar
  49. Kazemi M (2013) Vegetative and reproductive growth of tomato plants affected by calcium and humic acid. Bull Env Pharmacol Life Sci 2(11):24–29Google Scholar
  50. Kesba HH, Al-Shalaby MEM (2008) Survival and reproduction of Meloidogyne incognita on tomato as affected by humic acid. Nematology 10:243–249CrossRefGoogle Scholar
  51. Kiraly L, Hafez YM, Fodor J, Kiraly Z (2008) Suppression of tobacco mosaic virus-induced hypersensitive-type necrotization in tobacco at high temperature is associated with downregulation of NADPH oxidase and superoxide and stimulation of dehydroascorbate reductase. J Gen Virol 89:799–808CrossRefGoogle Scholar
  52. Kotob S, El Shall S and Walla DS (2009) Applications of actosol® humic acid products in Egypt. ASA-CSSA-SSSA Symposium 98—microbial and humic amendments: advances in understanding their effects on soils and plants: I, November 1–5, 2009. Pittsburg, PA, USAGoogle Scholar
  53. Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169(2):323–330CrossRefGoogle Scholar
  54. Lichtenthaler HK (1987) [34] Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology, Academic Press 148:350–382CrossRefGoogle Scholar
  55. Mahmoud H, Youssif S (2015) Response of garlic (Allium sativum L.) to natural fertilizers and ores under Ras Sudr conditions. Middle East J Appl Sci 5(4):1174–1183Google Scholar
  56. Malik CP, Singh MB (1980) In: Plant Enzymology and Histoenzymology. Kalyani Publishers, Indian and printed in Navin, Shanndara. Delhi pp 54–56Google Scholar
  57. Marschner P (2012) Marschner’s mineral nutrition of higher plants, 3rd edn. Elsevier/Academic Press, Amsterdam; BostonGoogle Scholar
  58. McGranahan DA, Poling BN (2018) Trait-based responses of seven annual crops to elevated CO2 and water limitation. Renew Agric Food Syst 33(3):259–266CrossRefGoogle Scholar
  59. Milford GFJ and Johnston AE (2007). Potassium and nitrogen interactions in crop production. Proceedings (International Fertiliser Society), no. 615., York, International Fertiliser SocietyGoogle Scholar
  60. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410CrossRefGoogle Scholar
  61. Peterburgski A (1968) Handbook of agronomic chemistry (in Russian). Kolos Publishing House, Moscow, pp 29–68Google Scholar
  62. Qiu L, Wu D, Ali S, Cai S, Dai F, Jin X, Wu F, Zhang G (2011) Evaluation of salinity tolerance and analysis of allelic function of HvHKT1 and HvHKT2 in Tibetan wild barley. Theor Appl Genet 122(4):695–703CrossRefGoogle Scholar
  63. Rai VK (2002) Role of amino acids in plant responses to stresses. Biol Plant 45(4):481–487CrossRefGoogle Scholar
  64. Robredo A, Pérez-López U, de la Maza HS, González-Moro B, Lacuesta M, Mena-Petite A, Muñoz-Rueda A (2007) Elevated CO2 alleviates the impact of drought on barley improving water status by lowering stomatal conductance and delaying its effects on photosynthesis. Environ Exp Bot 59(3):252–263CrossRefGoogle Scholar
  65. Saleem MF, Raza MAS, Ahmad S, Khan IH, Shahid AM (2016) Understanding and mitigating the impacts of drought stress in cotton—a review. Pak J Agric Sci 53(3):609–623Google Scholar
  66. Samarah NH (2005). Effects of drought stress on growth and yield of barley. Agronomy for sustainable development, Springer Verlag/EDP Sciences/INRA 25 (1): 145–149CrossRefGoogle Scholar
  67. Sarwat MI, EI-Sherif MH (2007) Increasing salt tolerance in some barley genotypes (Hordeum vulgare) by using kinetin and benzyladenin. World J Agric Sci 3(5):617–629Google Scholar
  68. Shahryari R, Gadimov A, Gurbanov E and Valizade M (2009). Applications of potassium humate to wheat for organic agriculture in Iran. Asian Journal of Food and Agro-Industry (Special Issue): S164-S168Google Scholar
  69. Shahzad K, Rauf M, Ahmed M, Malik ZA, Habib I, Ahmed Z, Mahmood K, Ali R, Masmoudi K, Lemtiri-Chlieh F, Gehring C, Berkowitz GA, Saeed NA (2015) Functional characterisation of an intron retaining K+ transporter of barley reveals intron-mediated alternate splicing. Plant Biol 17(4):840–851CrossRefGoogle Scholar
  70. Siddiqui MH, Al-Khaishany MY, Al-Qutami MA, Al-Whaibi MH, Grover A, Ali HM, Al-Wahibi MS, Bukhari NA (2015) Response of different genotypes of faba bean plant to drought stress. Int J Mol Sci 16(5):10214–10227CrossRefGoogle Scholar
  71. Singh M, Kumar J, Singh S, Singh VP, Prasad SM (2015) Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. Rev Environ Sci Bio-Technol 14(3):407–426CrossRefGoogle Scholar
  72. Song ZZ, Yang SY, Zuo J, Su YH (2014) Over-expression of ApKUP3 enhances potassium nutrition and drought tolerance in transgenic rice. Biol Plant 58(4):649–658CrossRefGoogle Scholar
  73. Stevenson FJ (1994) Humus chemistry genesis, composition, reactions, 2nd edn. John Wiley & Sons, New YorkGoogle Scholar
  74. Szalai G, Janda T, Paldi E, Szigeti Z (1996) Role of light in the development of post-chilling symptoms in maize. J Plant Physiol 148(3–4):378–383CrossRefGoogle Scholar
  75. Tisdale SL, Nelson WL, Beaton JD (1990) Soil fertility and fertilizers. Macmillan, New York, N.Y., pp 60–62Google Scholar
  76. Tiwari JK, Munshi AD, Kumar R, Pandey RN, Arora A, Bhat JS, Sureja AK (2010) Effect of salt stress on cucumber: Na+-K+ ratio, osmolyte concentration, phenols and chlorophyll content. Acta Physiol Plant 32(1):103–114CrossRefGoogle Scholar
  77. Treichel S (1975) Effect of NaCl on concentration of proline in different halophytes. Zeitschrift Fur Pflanzenphysiologie 76(1):56–68CrossRefGoogle Scholar
  78. Vaseva I, Akiscan Y, Simova-Stoilova L, Kostadinova A, Nenkova R, Anders I, Feller U, Demirevska K (2012) Antioxidant response to drought in red and white clover. Acta Physiol Plant 34(5):1689–1699CrossRefGoogle Scholar
  79. Wang WX, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218(1):1–14CrossRefGoogle Scholar
  80. Wu H, Zhu M, Shabala L, Zhou M, Shabala S (2015) K+ retention in leaf mesophyll, an overlooked component of salinity tolerance mechanism: a case study for barley. J Integr Plant Biol 57(2):171–185CrossRefGoogle Scholar
  81. Zhang H, Xiao W, Yu W, Yao L, Li L, Wei J and Li R (2018). Foxtail millet SiHAK1 excites extreme high-affinity K+ uptake to maintain K+ homeostasis under low K+ or salt stress. Plant Cell ReportsGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.EPCRS Excellence Center, Plant Pathology and Biotechnology Laboratory, Agricultural Botany Department, Faculty of AgricultureKafrelsheikh UniversityKafr El-SheikhEgypt
  2. 2.Soil and Water Sciences Department, Faculty of AgricultureKafrelsheikh UniversityKafr El-SheikhEgypt
  3. 3.Department of Agricultural Botany, Plant Physiology and Biotechnology, Institute of Crop SciencesUniversity of Debrecen - AGTCDebrecenHungary

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