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Osmoregulation and osmoprotection in the leaf cells of two olive cultivars subjected to severe water deficit

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Abstract

In this study, we compared the efficacy of defense mechanisms against severe water deficit in the leaves of two olive (Olea europaea L.) cultivars, ‘Chemlali’ and ‘Meski’, reputed drought resistant and drought sensitive, respectively. Two-year old plants growing in sand filled 10-dm3 pots were not watered for 2 months. Changes in chlorophyll fluorescence parameters and malondialdehyde content as leaf relative water content (RWC) decreased showed that ‘Chemlali’ was able to maintain functional and structural cell integrity longer than ‘Meski’. Mannitol started to accumulate later in the leaves of ‘Chemlali’ but reached higher levels than in the leaves of ‘Meski’. The latter accumulated several soluble sugars at lower dehydration. ‘Chemlali’ leaves also accumulated larger quantities of phenolic compounds which can improve its antioxidant response. Furthermore, the activity of three antioxidant enzymes catalase (CAT), peroxidase (POD) and ascorbate peroxidase (APX) increased as leaf RWC decreased. However, differences were observed between the two cultivars for CAT and POD but not for APX. The activity of the first two enzymes increased earlier in ‘Meski’, but reached higher levels in ‘Chemlali’. At low leaf hydration levels, ‘Chemlali’ leaves accumulated mannitol and phenolic compounds and had increased CAT and POD activities. These observations suggest that ‘Chemlali’ was more capable of maintaining its leaf cell integrity under severe water stress because of more efficient osmoprotection and antioxidation mechanisms.

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References

  • Aebi H (1984) Catalase in vitro. In: Colowick SP, Kaplane NO (eds) Meth Enzymol 105:121–126

  • Alonso M, Arranz D, Reboto V, Rodrïguez-Cabello JC (2001) Effect of a-, b- and g-cyclodextrins on the inverse temperature transition of the bioelastic thermo-responsive polymer poly(VPGVG). Macromol Chem Phys 202:3027–3034. doi:10.1002/1521-3935(20011001)202:15<3027::AID-MACP3027>3.0.CO;2-B

    Article  CAS  Google Scholar 

  • Angelopoulos K, Dichio B, Xiloyannis C (1996) Inhibition of photosynthesis in Olive trees (Olea europaea L.) during water stress and rewatering. J Exp Bot 301:1093–1100. doi:10.1093/jxb/47.8.1093

    Article  Google Scholar 

  • Arora A, Byrem TM, Nair MG, Strasbug GM (2000) Modulation of liposomal membrane fluidity by flavonoids. Arch Biochem Biophys 373:102–109. doi:10.1006/abbi.1999.1525

    Article  PubMed  CAS  Google Scholar 

  • Bacelar EA, Santos DL, Moutinho-Pereira JM, Gonçalves BC, Ferreira HF, Correia CM (2006) Immediate responses and adaptative strategies of three olive cultivars under contrasting water availability regimes: changes on structure and chemical composition of foliage and oxidative damage. Plant Sci 170:596–605. doi:10.1016/j.plantsci.2005.10.014

    Article  CAS  Google Scholar 

  • Bajji M, Kinet JM, Lutts S (2002) Osmotic and ionic effects of NaCl on germination, early seedling growth, and ion content of Atriplex halimus (Chenopodiaceae). Can J Bot 80:297–304. doi:10.1139/b02-008

    Article  CAS  Google Scholar 

  • Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot (Lond) 91:179–194. doi:10.1093/aob/mcf118

    Article  CAS  Google Scholar 

  • Bohnert HJ, Nelson DE, Jensenayb RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111

    Article  PubMed  CAS  Google Scholar 

  • Boussadia O, Ben Mariem F, Mechri B, Boussetta W, Braham M, Ben El Hadj S (2008) Response to drought of two olive tree cultivars (cv Koroneki and Meski). Sci Hortic (Amsterdam) 116:388–393. doi:10.1016/j.scienta.2008.02.016

    Article  Google Scholar 

  • Boyer JS, Ort DR, Ortiz-Lopez A (1987) Photophosphorylation at low water potentials. Curr Top Plant Biochem Physiol 6:69–73

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3

    Article  PubMed  CAS  Google Scholar 

  • Chartzoulakis K, Patakas A, Bosabalidis A (1999) Changes in water relations, photosynthesis and leaf anatomy induced by intermittent drought in two olive cultivars. Environ Exp Bot 42:113–120. doi:10.1016/S0098-8472(99)00024-6

    Article  Google Scholar 

  • Chartzoulakis K, Bosabalidis A, Patakas A, Vemmos S (2000) Effects of water stress on water relations, gas exchange and leaf structure of olive tree. Acta Hortic 537:241–247

    Google Scholar 

  • Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought: from genes to the whole plant. Funct Plant Biol 30:239–264. doi:10.1071/FP02076

    Article  CAS  Google Scholar 

  • Christie WW, Brechany EY, Marekov IN, Stefanov KL, Andreev SN (1994) The fatty acids of the sponge Hymeniacidon sanguinea from the Black Sea. Comp Biochem Physiol B 109:245–252. doi:10.1016/0305-0491(94)90008-6

    Article  Google Scholar 

  • Connor DJ (2005) Adaptation of olive (Olea europaea L.) to water environments. Aust J Agric Res 56:1181–1189

    Article  Google Scholar 

  • Demmig-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626. doi:10.1146/annurev.pp.43.060192.003123

    Article  CAS  Google Scholar 

  • Dichio B, Xiloyannis C, Angelopoulos K, Nuzzo V, Bufo S, Celano G (2003) Drought-induced variations of water relations parameters in Olea europaea. Plant Soil 257:381–389. doi:10.1023/A:1027392831483

    Article  CAS  Google Scholar 

  • Dichio B, Xiloyannis C, Sofo A, Montanaro G (2006) Osmotic adjustment in leaves and roots of olive tree (Olea europaea L.) during drought stress and rewatering. Tree Physiol 26:179–185

    Article  PubMed  Google Scholar 

  • Ennajeh M, Vadel AM, Khemira H, Ben Mimoun M, Hellali R (2006) Defense mechanisms against water deficit in two olive (Olea europaea L.) cultivars ‘Meski’ and ‘Chemlali’. J Hortic Sci Biotechnol 81:99–104

    Google Scholar 

  • Ennajeh M, Tounekti T, Vadel AM, Khemira H, Cochard H (2008) Water relations and drought-induced embolism in two olive (Olea europaea L.) varieties ‘Meski’ and ‘Chemlali’ under severe drought conditions. Tree Physiol 28:971–976

    PubMed  Google Scholar 

  • Fernández JE, Moreno F (1999) Water use by the olive tree. J Crop Prod 2:101–162. doi:10.1300/J144v02n02_05

    Article  Google Scholar 

  • Fernández JE, Moreno F, Girón IF, Blázquez OM (1997) Stomatal control of water use in olive leaves. Plant Soil 190:179–192. doi:10.1023/A:1004293026973

    Article  Google Scholar 

  • Foyer CH, Descourvieres P, Kunert KJ (1994) Protection against oxygen radicals: an important defense mechanism studied in transgenic plants. Plant Cell Environ 17:579–587. doi:10.1111/j.1365-3040.1994.tb00146.x

    Article  Google Scholar 

  • Genty B, Briantais J, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    CAS  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Mol Biol 51:463–499. doi:10.1146/annurev.arplant.51.1.463

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: 1. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. doi:10.1016/0003-9861(68)90654-1

    Article  PubMed  CAS  Google Scholar 

  • 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. doi:10.1007/s004250050524

    Article  CAS  Google Scholar 

  • Kasraoui MF, Braham M, Denden M, Mehri H, Garcia M, Lamaze T, Attia F (2006) Effet du déficit hydrique au niveau de la phase photochimique du PSII chez deux variétés d’olivier. C R Biol 329:98–105

    PubMed  CAS  Google Scholar 

  • Kramer PJ, Brix H (1965) Measurment of water deficit in plants. UNESCO. Arid Zon Res 25:343–531

    Google Scholar 

  • Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot (Lond) 98:693–713. doi:10.1093/aob/mcl114

    Article  Google Scholar 

  • Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ 25:275–294. doi:10.1046/j.0016-8025.2001.00814.x

    Article  PubMed  CAS  Google Scholar 

  • Lo Gullo MA, Salleo S (1988) Different strategies of drought resistance in three Mediterranean sclerophyllous trees growing in the same environmental conditions. New Phytol 108:267–276. doi:10.1111/j.1469-8137.1988.tb04162.x

    Article  Google Scholar 

  • Lu C, Zhang J (1998) Effect of water stress on photosynthesis, chlorophyll fluorescence and photoinhibition in wheat plants. Aust J Plant Physiol 25:883–892

    Article  CAS  Google Scholar 

  • Marchi S, Tognetti R, Minnocci A, Borghi M, Sebastiani L (2008) Variation in mesophyll anatomy and photosynthetic capacity during leaf development in a deciduous mesophyte fruit tree (Prunus persica) and sclerophyllous Mediterranean shrub (Olea europaea). Trees (Berl). doi:10.1007/s00468-008-0216-9

  • Masia A (2003) Physiological effects of oxidative stress in relation to ethylene in post-harvest produce. In: Hodges DM (ed) Post-harvest oxidative stress in horticultural crops. Food Products Press, New York, pp 165–197

    Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668. doi:10.1093/jexbot/51.345.659

    Article  PubMed  CAS  Google Scholar 

  • Morgan JM (1984) Osmoregulation and water in higher plants. Annu Rev Plant Physiol 35:299–319. doi:10.1146/annurev.pp.35.060184.001503

    Article  Google Scholar 

  • Moriana A, Villalobos FJ, Fereres E (2002) Stomatal and photosynthetic responses of olive (Olea europaea L.) leaves to water deficits. Plant Cell Environ 25:395–405. doi:10.1046/j.0016-8025.2001.00822.x

    Article  Google Scholar 

  • Ngo TT, Lenhoff HM (1980) A sensitive and versatile chromogenic assay for peroxidase and peroxidase-coupled reactions. Anal Biochem 105:389–397. doi:10.1016/0003-2697(80)90475-3

    Article  PubMed  CAS  Google Scholar 

  • Nogués S, Baker NR (2000) Effects of drought on photosynthesis in Mediterranean plants grown under enhanced UV-B radiation. J Exp Bot 51:1309–1317. doi:10.1093/jexbot/51.348.1309

    Article  PubMed  Google Scholar 

  • Peltzer D, Dreyer E, Polle A (2002) Differential temperature dependencies of antioxidative enzymes in two contrasting species: Fagus sylvatica and Coleus blumei. Plant Physiol Biochem 40:141–150. doi:10.1016/S0981-9428(01)01352-3

    Article  CAS  Google Scholar 

  • Pennycooke JC, Cox S, Stushnoff JC (2005) Relationship of cold acclimation, total phenolic content and antioxidant capacity with chilling tolerance in petunia (Petunia × hybrida). Environ Exp Bot 53:225–232. doi:10.1016/j.envexpbot.2004.04.002

    Article  CAS  Google Scholar 

  • Ranjbarfordoei A, Samson R, Van Damme P (2006) Chlorophyll fluorescence performance of sweet almond [Prunus dulcis (Miller) D. Webb] in response to salinity stress induced by NaCl. Photosynthetica 44:513–522. doi:10.1007/s11099-006-0064-z

    Article  CAS  Google Scholar 

  • Rejšková A, Patková L, Stodůlková E, Lipavská H (2007) The effect of abiotic stresses on carbohydrate status of olive shoots (Olea europaea L.) under in vitro conditions. J Plant Physiol 164:174–184. doi:10.1016/j.jplph.2005.09.011

    Article  PubMed  CAS  Google Scholar 

  • Roháček K (2002) Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 40:13–29. doi:10.1023/A:1020125719386

    Article  Google Scholar 

  • Rousseaux MS, Benedetti JP, Searles PS (2008) Leaf-level responses of olive trees (Olea europaea) to the suspension of irrigation during the winter in arid region of Argentina. Sci Hortic (Amsterdam) 115:135–141. doi:10.1016/j.scienta.2007.08.005

    Article  Google Scholar 

  • Serraj R, Sinclair TR (2002) Osmolyte accumulation: can it really help increase crop yield under drought conditions? Plant Cell Environ 25:333–341. doi:10.1046/j.1365-3040.2002.00754.x

    Article  PubMed  Google Scholar 

  • Shen ZG, Zhao FJ, McGrath SP (1997) Uptake and transport of zinc in the hyperaccumulator Thlaspi caerulescens and the non-hyperaccumulator Thlaspi ochroleucum. Plant Cell Environ 20:898–906. doi:10.1046/j.1365-3040.1997.d01-134.x

    Article  CAS  Google Scholar 

  • Smirnoff N (1993) The role of active oxygen in the response to water deficit and desiccation. New Phytol 125:27–58. doi:10.1111/j.1469-8137.1993.tb03863.x

    Article  CAS  Google Scholar 

  • Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28:1057–1060. doi:10.1016/0031-9422(89)80182-7

    Article  CAS  Google Scholar 

  • Sofo A, Dichio B, Xiloyannis C, Masia A (2004) Lipoxygenase activity and proline accumulation in leaves and roots of olive tree in response to drought stress. Physiol Plant 121:58–65. doi:10.1111/j.0031-9317.2004.00294.x

    Article  PubMed  CAS  Google Scholar 

  • Sofo A, Dichio B, Xiloyannis C, Masia A (2005) Antioxidant defences in olive trees during drought stress: changes in activity of some antioxidant enzymes. Funct Plant Biol 32:45–53. doi:10.1071/FP04003

    Article  CAS  Google Scholar 

  • Sofo A, Manfreda S, Dichio B, Fiorentino M, Xiloyannis C (2007) The olive tree: a paradigm for drought tolerance in Mediterranean climates. Hydrol Earth Syst Sci Discuss 4:2811–2835

    Google Scholar 

  • Spanos GA, Wrolstad RE (1990) Influence of variety, maturity, processing and storage on the phenol composition of pear juice. J Agric Food Chem 38:817–824. doi:10.1021/jf00093a049

    Article  CAS  Google Scholar 

  • Syros T, Yupsanis T, Economou A (2001) Factors affecting the determination of peroxidase activity of Ebenus cretica L. cuttings. A preliminary survey. J Prop Ornam Plants 1:50–53

    Google Scholar 

  • Tambussi EA, Casadesus J, MunnéBosch S, Araus JL (2002) Photoprotection in water stressed plants of durum wheat (Triticum turgidum var. durum): changes in chlorophyll fluorescence, spectral signature and photosynthetic pigments. Funct Plant Biol 29:35–44. doi:10.1071/PP01104

    Article  CAS  Google Scholar 

  • Ushimaru T, Maki Y, Sano S, Koshiba K, Asada K, Tsuji H (1997) Induction of enzymes involved in the ascorbate-dependent antioxidative system, namely ascorbate peroxidase, monodehydroascorbate reductase and dehydroascorbate reductase, after exposure to air of rice (Oryza sativa) seedlings germinated under water. Plant Cell Physiol 38:541–549

    CAS  Google Scholar 

  • Vendruscolo ECG, Schuster I, Pileggi M, Scapim CA, Molinari HBC, Marur CJ, Vieira LGE (2007) Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. J Plant Physiol 164:1367–1376. doi:10.1016/j.jplph.2007.05.001

    Article  PubMed  CAS  Google Scholar 

  • Xiloyannis C, Pezzarosa B, Jorba J, Angelini P (1988) Effect of soil water content on gas exchange in olive trees. Adv Hortic Sci 2:58–63

    Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71. doi:10.1016/S1360-1385(00)01838-0

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Habib Khemira.

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Ennajeh, M., Vadel, A.M. & Khemira, H. Osmoregulation and osmoprotection in the leaf cells of two olive cultivars subjected to severe water deficit. Acta Physiol Plant 31, 711–721 (2009). https://doi.org/10.1007/s11738-009-0283-6

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