Effects of different irradiance levels on some antioxidant enzymes and on malondialdehyde content during rewatering in olive tree
Introduction
The response of plants to water stress is a species- and cultivar-dependent characteristic. In Mediterranean ecosystems, in which the summer months are characterized by elevated temperatures, high irradiance levels and lack of precipitation, plants are subjected to a continuous and severe water deficit [1]. Under these adverse environmental conditions, photoinhibition, photooxidation and photorespiration occur [2], [3].
Plants are particularly susceptible to photoinhibition when exposed to bright light [4], [5], [6] and environmental stresses as drought [7], chilling [8], [9] and heat [10]. The synergic action of high irradiance level and water stress reduces the capacity of the photosynthetic systems to utilize incident radiation, leading to a higher degree of photodamage [2], [11]. Under environmental conditions, where the photon energy is in excess of CO2 assimilation, photosystem II (PSII) is the primary target for photoinhibition, while PSI is more stable than PSII, receiving a damage usually less significant and strictly related to the rate of electron flow from PSII and the presence of oxygen [12], [13], [14].
The limitation of CO2 assimilation in water-stressed plants causes the over-reduction of photosynthetic electron chain. This excess of reducing power determines a redirection of photon energy into processes that favour the production of activated oxygen species (AOS), mainly in the photosynthetic [15] and mitochondrial electron transport chains [16]. Being toxic for the cells, AOS are efficiently eliminated by non-enzymatic (α-tocopherol, β-carotene, phenolic compounds, ascorbate, glutathione) and enzymatic antioxidants [17], [18]. The enzymatic antioxidant system include superoxide dismutase (SOD; EC 1.15.1.1), which catalyzes the reaction from O2− to H2O2, and catalase (CAT; EC 1.11.1.6), ascorbate peroxidase (APX; EC 1.11.1.11) and guaiacol peroxidase (POD; EC 1.11.1.7), which are able to detoxify the H2O2 produced [2].
All the enzymes mentioned above exist in plant tissues in multiple forms. The three known types of SOD are classified by their metal cofactor and are mainly located in chloroplasts, cytosol and mitochondria [12], [19]. APX isozymes are generally located in chloroplasts, but microsomal, peroxisomal and membrane-bound forms, as well as soluble cytosolic and apoplastic isozymes, also exist [18]. CAT isoforms are particularly abundant in the glyoxysomes and in the peroxysomes [20]. POD have vacuolar and apoplastic forms which can use a wide range of substrates [21], including indoleacetic acid (IAA), and are so involved in auxin catabolism [22]. Polyphenol oxidase (PPO; EC 1.30.3.1), a copper enzyme located in plastids, acts on phenols in the presence of oxygen, catalysing the oxidation of o-diphenols into o-chinones [23]. When the accumulation of AOS under water stress conditions exceeds the removing capacity of the antioxidant system, the effects of oxidative damage arise, including peroxidation of membrane lipids, destruction of photosynthetic pigments and inactivation of photosynthetic enzymes [17].
Lipoxygenases (LOX; EC 1.13.11.12), located in cytosol [24], microsomes [25], plasma membrane [26] and oil bodies [27], catalyse the dioxygenation of polyunsaturated fatty acids containing a cis,cis-1,4-pentadiene moiety, producing hydroperoxy fatty acids, which are highly reactive compounds, toxic to the cell. Different LOX isozyme forms are involved in many physiological processes such as flowering [28], seed germination [29], formation of flavours and aroma in plant products [30], plant growth and development [31], pigment bleaching, senescence, pest resistance, wound stress and biosynthesis of regulatory molecules such as traumatin and jasmonic acid, which have growth-inhibitory properties analogous to those of abscisic acid [24].
Malondialdehyde (MDA), a decomposition product of polyunsaturated fatty acids hydroperoxides, has been utilized very often as a suitable biomarker for lipid peroxidation [32], which is an effect of oxidative damage. Nonetheless, lipids are not the only targets for MDA action; in fact MDA damages DNA, forming adducts to deoxyguanosine and deoxyadenosine [33].
Olive (Olea europaea L.) is a sclerophyll tree species with a high degree of drought tolerance [34]. In olive tree, severe drought stress causes closure of stomata [35], inhibition of photosynthesis [7] and transpiration [36], reduction of gas exchange [37] and changes in root and canopy dynamics [38], [39], but little is known about the effects of water deficit on antioxidant enzyme activities and oxidative damage in this species. Olive tree is able to restore leaf water potentials (LWP) and chlorophyll fluorescence after rewatering, but the rapid recovery of tissue water status is often coupled to a non-recovery of leaf functionality that lasts several days and is correlated with the level of stress previously reached [7]. The persisting deficit in leaf gas exchange found in this species could not be imputed to the non-recovery of cell turgor but, as observed in other species, to other factors probably involving the biochemical [40], [41] and hormonal balance [42], [43]. A complete understanding of the biochemical and metabolic factors involved in olive tree’s defence strategies against drought stress is of paramount importance to crop improvement but is, at present, lacking. The aim of this study was to investigate the influence of different levels of irradiance on antioxidant enzymes and LOX activities and on MDA level in olive tree during rewatering. We hypothesize that semi-shade conditions could minimize the oxidative effect of the damage following a period of water stress.
Section snippets
Study site and experimental design
Trials were conducted on self-planted 2-year-old Olea europaea L. plants, cv. ‘Coratina’, measuring 130–150 cm in height. The study site was located at the ‘Pantanello’ Agricultural Experiment Station in Metaponto (southern Italy, Basilicata region—40°24′N, 16°48′E). The experimental period started on 3 July and ended on 22 August, 2001.
Olive plants grew uniformly outdoors in 0.016 m3 containers filled with a mixture of loam, peat and sand (in proportion of 1:1:1). Pots were covered with plastic
Environmental conditions and physiological parameters
The highest value of maximum temperature was 37.5 °C on 7/29 and the mean of all the daily maximum values was 32.6 °C; RH pattern showed the highest value (44.4%) on 8/22, with a mean of 29.2%; VPD range was between 2.2 (on 7/5) and 5.0 kPa (on 8/11), with a mean value of 3.6 kPa; PPFD level showed a slight decrement during the experimental period, especially in the last 3 days of the trial (Fig. 1).
The mean predawn LWP in CP was −0.34 MPa. LWP in SHP increased during the whole rewatering period,
Discussion
Rewatering treatment following the water stress phase produced a rapid increase in LWP both in SHP and NSHP paralleled by slower increases in photosynthetic gas exchange (Fig. 2B–E). The delay in recovery of photosynthetic rate during rewatering, more marked in NSHP, is probably due to a light-dependent inactivation of the primary photochemistry associated with PSII occurred during the previous water stress [7] or to the downregulation of electron transport, as recently underlined by Nogués and
Acknowledgements
We thank Dr. Giuseppe Montanaro for his help in LCA-4 use and Prof. Elvira Di Nardo for her contribution in statistical analysis. We are grateful to Antonio Ditaranto and Angelo Mossuto for technical assistance.
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