Abstract
The plants of pea (Pisum sativum L.) were grown under NaCl and/or NiCl2 stress, to comparatively evaluate stress-mitigating effects of pure proline and naturally proline-enriched Lolium perenne (L.) aqueous leaf extract. Both stress factors (salinity and nickel) significantly reduced plant biomass, chlorophyll content, photosynthetic activity, stomatal conductance, intercellular carbon dioxide (CO2) level, number of stomata, stomatal size, water-use efficiency, relative water content (RWC), and the membrane stability index (MSI). However, the proline and glycinebetaine contents, lipid peroxidation, electrolyte leakage, and activities of antioxidant enzymes (superoxide dismutase, peroxidase, catalase, ascorbate peroxidase, guaiacol peroxidase, and glutathione reductase) were significantly increased. Exogenously applied proline and Lolium perenne (LP) leaf extracts significantly overcame the nickel and/or salinity-induced toxic effects on growth, RWC, and various photosynthetic attributes. However, follow-up treatment with proline and LP-leaf-extract detoxified the stress caused by NiCl2 and/or NaCl, by suppressing lipid peroxidation and electrolyte leakage, accelerating the antioxidant enzyme activities, and improving the MSI, leaf/root proline, and glycinebetaine contents. LP-leaf-extract proved to be better than pure proline for improving growth, gas exchange parameters, osmolytes, RWC, and antioxidant enzyme activities. As LP-leaf-extract was enriched with a substantial amount of proline along with many other essential osmoprotectants, it was found to be as effective as pure proline in ameliorating growth, some major physiological attributes, and non-enzymatic and enzymatic antioxidant activities in the pea, under nickel and/or salinity stress. Thus, it could be used as an alternative inexpensive source of proline, to be used as a mitigating agent for protecting plants against the deleterious effects of nickel and/or salinity stress.
Similar content being viewed by others
References
Abdel-Basset R, Issa A, Adam M (1995) Chlorophyllase activity: effects of heavy metals and calcium. Photosynthetica 31:421–425
Agami RA (2013) Alleviating the adverse effects of NaCl stress in maize seedlings by pretreating seeds with salicylic acid and 24-epibrassinolide. S Afr J Bot 88:171–177
Ali B, Hayat S, Fariduddin Q, Ahmad A (2008) 24-Epibrassinolide protects against the stress generated by salinity and nickel in Brassica juncea. Chemosphere 72:1387–1392
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15
Balal RM, Khan MM, Shahid MA, Mattson NS, Abbas T, Ashfaq M, Garcia-Sanchez F, Ghazanfer U, Gimeno V, Iqbal Z (2012) Comparative studies on the physiobiochemical, enzymatic, and ionic modifications in salt-tolerant and salt-sensitive Citrus rootstocks under NaCl stress. J Am Soc Horti Sci 137:86–95
Banu MNA, Hoque MA, Watanabe-Sugimoto M, Matsuoka K, Nakamura Y, Shimoishi Y, Murata Y (2009) Proline and glycinebetaine induce antioxidant defense gene expression and suppress cell death in cultured tobacco cells under salt stress. J Plant Physiol 166:146–156
Barrs H, Weatherley P (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428
Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Bauddh K, Singh RP (2012) Growth, tolerance efficiency and phytoremediation potential of Ricinus communis (L.) and Brassica juncea (L.) in salinity and drought affected cadmium contaminated soil. Ecotox Environ Safe 85:13–22
Ben Ahmed C, Ben Rouina B, Sensoy S, Boukhriss M, Ben Abdullah F (2010) Exogenous proline effects on photosynthetic performance and antioxidant defense system of young olive tree. J Agri Food Chem 58:4216–4222
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Brown PH, Welch RM, Cary EE (1987) Nickel: a micronutrient essential for higher plants. Plant Physiol 85:801–803
Choudhary B (1990) Residual effect of eight vegetable oils in chickpea against pulse beetle, Callosobruchus chinensis (Linnaeus). Indian J Plant Prot 18:89–92
Dalton DA, Russell SA, Evans HJ (1988) Nickel as a micronutrient element for plants. BioFactors (Oxford, Engl) 1:11–19
Dinkova-Kostova AT (2008) Phytochemicals as protectors against ultraviolet radiation: versatility of effects and mechanisms. Planta Med 74:1548–1559
Drazkiewicz M, Baszynski T (2010) Interference of nickel with the photosynthetic apparatus of Zea mays. Ecotox Environ Safe 73:982–986
Fedina IS, Tsonev T, Guleva EI (1993) The effect of pre-treatment with proline on the responses of Pisum sativum to salt stress. Photosynthetica 29:521–527
Giannopolitis CN, Ries SK (1977) Superoxide dismutases I. Occurrence in higher plants. Plant Physiol 59:309–314
Giridhara M, Siddaramappa R (2002) Effect of heavy metals on urease activity in soil. Curr Res Univ Argric Sci Bangalore 31:4–5
Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70:303–307
Guerrier G, Patolia J (1989) Comparative salt-responses of excised cotyledons and seedlings of pea to various osmotic and ionic stresses. J Plant Physiol 135:330–336
Hamilton PB, Van-Slyke DD (1973) Amino acid determination with ninhydrin. J Biol Chem 150:231–233
Harrington K, Thatcher A, Kemp P (2006) Mineral composition and nutritive value of some common pasture weeds. New Zeal Plant Prot 59:261–267
Hayat S, Maheshwari P, Wani AS, Irfan M, Alyemeni MN, Ahmad A (2012) Comparative effect of 28-homobrassinolide and salicylic acid in the amelioration of NaCl stress in Brassica juncea L. Plant Physiol Biochem 53:61–68
Hayat S, Hayat Q, Alyemeni MN, Ahmad A (2013) Proline enhances antioxidative enzyme activity, photosynthesis and yield of Cicer arietinum L. exposed to cadmium stress. Acta Botanica Croatica 72:10–22
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: II. Role of electron transfer. Arch Biochem Biophys 125:850–857
Hernandez J, Olmos E, Corpas F, Sevilla F, Del RL (1995) Salt-induced oxidative stress in chloroplasts of pea plants. Plant Sci 105:151–167
Heuer B (1994) Osmoregulatory role of proline in water and salt-stressed plants. In: Pessaraskli M II (ed) Handbook of plant and crop stress. Marcel Dekker, New York, pp 363–381
Hussein M, Nadia E, Gereadly H, El-Desuki M (2006) Role of puterscine in resistance to salinity of pea plants (Pisum sativum L.). J Appl Sci Res 2:598–604
Islam MM, Hoque MA, Okuma E, Banu MNA, Shimoishi Y, Nakamura Y, Murata Y (2009) Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J Plant Physiol 166:1587–1597
Jarup L (2003) Hazards of heavy metal contamination. Bri Med Bull 68:167–182
Juge N, Mithen R, Traka M (2007) Molecular basis for chemoprevention by sulforaphane: a comprehensive review. Cell Mol Life Sci 64:1105–1127
Julkinen-Tieto R (1985) Phenolic constituents in the leaves of northern willows: methods for the analysis of certain phenolics. Agri Food Chem 33:213–217
Kemble A, MacPherson H (1954) Liberation of amino acids in perennial rye grass during wilting. Biochem J 58:46–49
Khan N (2003) NaCl-inhibited chlorophyll synthesis and associated changes in ethylene evolution and antioxidative enzyme activities in wheat. Biol Plant 47:437–440
Khan MR, Khan MM (2010) Effect of varying concentration of nickel and cobalt on the plant growth and yield of chickpea. Aust J Basic Appl Sci 4:1036–1046
Khan N, Nazar R, Anjum N (2009) Growth, photosynthesis and antioxidant metabolism in mustard (Brassica juncea L.) cultivars differing in ATP-sulfurylase activity under salinity stress. Sci Hortic 122:455–460
Kumar N, Pal M, Singh A, SaiRam KS, Srivastava GC (2010) Exogenous proline alleviates oxidative stress and increase vase life in rose (Rosa hybrida L. ‘Grand Gala’). Sci Hortic 127:79–85
Kupper H, Küpper F, Spiller M (1998) In situ detection of heavy metal substituted chlorophylls in water plants. Photosynth Res 58:123–133
Louahlia S, Macduff J, Ourry A, Humphreys M, Boucaud J (1999) Nitrogen reserve status affects the dynamics of nitrogen remobilization and mineral nitrogen uptake during recovery of contrasting cultivars of Lolium perenne from defoliation. New Phytol 142:451–462
Maehly A, Chance B (1954) Catalases and peroxidases. Methods Biochem Anal 1:357–424
Mittler R, Vanderauwera S, Gollery M, Van BF (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498
Moya JL, Gómez-Cadenas A, Primo-Millo E, Talon M (2003) Chloride absorption in salt-sensitive Carrizo citrange and salt-tolerant Cleopatra mandarin citrus rootstocks is linked to water use. J Exp Bot 54:825–833
Najafi F, Khavari-Nejad R, Rastgar-Jazii F, Sticklen M (2007) Growth and some physiological attributes of pea (Pisum sativum L.) as affected by salinity. Pak J Biol Sci 10:2752–2759
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Nazar R, Khan NA, Singh S, Anjum NA (2008) Photosynthetic traits and activities of antioxidant enzymes in blackgram (Vigna mungo L. Hepper) under cadmium stress. Am J Plant Physiol 3:25–32
Noreen Z, Ashraf M (2009) Assessment of variation in antioxidative defense system in salt-treated pea (Pisum sativum) cultivars and its putative use as salinity tolerance markers. J Plant Physiol 166:1764–1774
Noreen S, Ashraf M, Hussain M, Jamil A (2009) Exogenous application of salicylic acid enhances antioxidative capacity in salt stressed sunflower (Helianthus annuus L.) plants. Pak J Bot 41:473–479
Omoto E, Taniguchi M, Miyake H (2012) Adaptation responses in C4 photosynthesis of maize under salinity. J Plant Physiol 169:469–477
Osman HS (2015) Enhancing antioxidant–yield relationship of pea plant under drought at different growth stages by exogenously applied glycine betaine and proline. Ann Agric Sci. doi:10.1016/j.aoas.2015.10.004
Ozden M, Demirel U, Kahraman A (2009) Effects of proline on antioxidant system in leaves of grapevine (Vitis vinifera L.) exposed to oxidative stress by H2O2. Sci Hortic 119:163–168
Ozturk ZN, Talamé V, Deyholos M, Michalowski CB, Galbraith DW, Gozukirmizi N, Tuberosa R, Bohnert HJ (2002) Monitoring large-scale changes in transcript abundance in drought-and salt-stressed barley. Plant Mol Biol 48:551–573
Pandey N, Sharma CP (2002) Effect of heavy metal Co2+, Ni2+ and Cd2+ on growth and metabolism of cabbage. Plant Sci 163:753–758
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotox Environ Safe 60:324–349
Riazi A, Matruda K, Arslam A (1985) Water stress induces changes in concentration of proline and other solutes in growing regions. J Exp Bot 36:1716–1725
Sanchez DH, Siahpoosh MR, Roessner U, Udvardi M, Kopka J (2008) Plant metabolomics reveals conserved and divergent metabolic responses to salinity. Physiol Plant 132:209–219
Sandoval-Gil JM, Marín-Guirao L, Ruiz JM (2012) The effect of salinity increase on the photosynthesis, growth and survival of the Mediterranean seagrass Cymodocea nodosa. Estuar Coast Shelf S 115:260–271
Shahbaz M, Mushtaq Z, Andaz F, Masood A (2013) Does proline application ameliorate adverse effects of salt stress on growth, ions and photosynthetic ability of eggplant (Solanum melongena L.)? Sci Hortic 164:507–511
Shahid M, Pervez M, Balal R, Mattson N, Rashid A, Ahmad R, Ayyub C, Abbas T (2011) Brassinosteroid (24-epibrassinolide) enhances growth and alleviates the deleterious effects induced by salt stress in pea (Pisum sativum L.). Aust J Crop Sci 5:500–510
Shahid M, Balal R, Pervez M, Abbas T, Ashfaq M, Ghazanfar U, Afzal M, Rashid A, Garcia-Sanchez F, Mattson N (2012) Differential response of pea (Pisum sativum L.) genotypes to salt stress in relation to the growth, physiological attributes antioxidant activity and organic solutes. Aust J Crop Sci 6:828–838
Shahid MA, Ashraf MY, Pervez MA, Ahmad R, Balal RM, Garcia-Sanchez F (2013) Impact of salt stress on concentrations of Na+, Cl− and organic solutes concentration in pea cultivars. Pak J Bot 45:755–761
Shalygo N, Kolesnikova N, Voronetskaya V, Averina N (1999) Effects of Mn2+, Fe2+, Co2+, and Ni2+ on chlorophyll accumulation and early stages of chlorophyll formation in greening barley seedlings. Russ J Plant Physiol 46:496–501
Singh K, Pandey S (2011) Effect of nickel-stresses on uptake, pigments and antioxidative responses of water lettuce, Pistia stratiotes (L). J Environ Biol 32:391–394
Sirko A, Brodzik R (2000) Plant ureases: roles and regulation. Acta Biochim Pol 47:1189–1194
Smith IK, Vierheller TL, Thorne CA (1988) Assay of glutathione reductase in crude tissue homogenates using 5,5′-dithiobis (2-nitrobenzoic acid). Anal Biochem 175:408–413
Soshinkova T, Radyukina N, Korolkova D, Nosov A (2013) Proline and functioning of the antioxidant system in Thellungiella salsuginea plants and cultured cells subjected to oxidative stress. Russ J Plant Physiol 60:41–54
Sullivan CY, Ross W (1979) Selecting for drought and heat resistance in grain sorghum. Stress Physiol Crop Plants 4:263–281
Suresh K (2008) Antimicrobial and phytochemical investigation of the leaves of Carica papaya L., Cynodon dactylon (L.) Pers., Euphorbia hirta L., Melia azedarach L. and Psidium guajava L. Ethnobotanical Leaflets 157:1184–1189
Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97
Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Annals Bot 91:503–527
Tripathy BC, Oelmuller R (2012) Reactive oxygen species generation and signaling in plants. Plant Signal Behav 7:1621–1633
Urbanek H, Kuzniak-Gebarowska E, Herka K (1991) Elicitation of defence responses in bean leaves by Botrytis cinerea polygalacturonase. Acta Physiol Plant 13:23–29
Velikova V, Tsonev T, Loreto F, Centritto M (2011) Changes in photosynthesis, mesophyll conductance to CO2, and isoprenoid emissions in Populus nigra plants exposed to excess nickel. Environ Pollut 159:1058–1066
Wani AS, Ahmad A, Hayat S, Fariduddin Q (2013) Salt-induced modulation in the growth, photosynthesis and antioxidant system in two varieties of Brassica juncea. Saudi J Biol Sci 20:183–193
Yang Y, Zhang Y, Wei X, You J, Wang W, Lu J, Shi R (2011) Comparative antioxidative responses and proline metabolism in two wheat cultivars under short term lead stress. Ecotox Environ Safe 74:733–740
Yusuf M, Fariduddin Q, Ahmad A (2012) 24-Epibrassinolide modulates growth, nodulation, antioxidant system, and osmolyte in tolerant and sensitive varieties of Vigna radiata under different levels of nickel: a shotgun approach. Plant Physiol Biochem 57:143–153
Zouari M, Elloumi N, Ahmed CB, Delmail D, Rouina BB, Abdallah FB, Labrousse P (2016) Exogenous proline enhances growth, mineral uptake, antioxidant defense, and reduces cadmium-induced oxidative damage in young date palm (Phoenix dactylifera L.). Ecol Eng 86:202–209
Acknowledgments
The authors highly acknowledge the Higher Education Commission of Pakistan for their financial assistance vide Project No. 20-2315/NRPU/R&D/HEC/12 to conduct this investigation.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Balal, R.M., Shahid, M.A., Javaid, M.M. et al. Foliar treatment with Lolium perenne (Poaceae) leaf extract alleviates salinity and nickel-induced growth inhibition in pea. Braz. J. Bot 39, 453–463 (2016). https://doi.org/10.1007/s40415-016-0253-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40415-016-0253-3