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Effect of High Salinity on Atriplex Portulacoides: Growth, Leaf Water Relations and Solute Accumulation in Relation with Osmotic Adjustment

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Effect of High Salinity on Atriplex Portulacoides: Growth, Leaf Water Relations and Solute Accumulation in Relation with Osmotic Adjustment South African Journal of Botany 95 (2014) 70–77 Contents lists available at ScienceDirect South African Journal of Botany journal homepage: www.elsevier.com/locate/sajb Effect of high salinity on Atriplex portulacoides: Growth, leaf water relations and solute accumulation in relation with osmotic adjustment Maali Benzarti a,1, Kilani Ben Rejeb a,b,1, Dorsaf Messedi a, Amira Ben Mna c, Kamel Hessini a, Mustapha Ksontini c, Chedly Abdelly a, Ahmed Debez a,⁎ a Laboratoire des Plantes Extrêmophiles, Centre de Biotechnologie de Borj-Cedria (CBBC), BP 901, Hammam-Lif 2050, Tunisia b Adaptation des plantes aux contraintes environnementales, UR5, Université Pierre et Marie Curie (UPMC), Case 156, 4 Place Jussieu, 75252 Paris cedex 05, France c Unité d'agrosylvopastoralisme, Institut National de Recherches en génie Rural, Eau et Forêts (INRGREF), Ariana 2080, Tunisia article info abstract Article history: Atriplex (Halimione) portulacoides is a halophyte with potential interest for saline soil reclamation and Received 10 December 2013 phytoremediation. Here, we assess the impact of salinity reaching up to two-fold seawater concentration Received in revised form 20 August 2014 (0–1000 mM NaCl) on the plant growth, leaf water status and ion uptake and we evaluate the contribution Accepted 24 August 2014 of inorganic and organic solutes to the osmotic adjustment process. A. portulacoides growth was optimal at Available online xxxx 200 mM NaCl but higher salinities (especially 800 and 1000 mM NaCl) significantly reduced plant growth. + − Edited by JM Farrant Na and Cl contents increased upon salt exposure especially in the leaves compared to the roots. Interestingly, no salt-induced toxicity symptoms were observed and leaf water content was maintained even at the highest sa- fi Keywords: linity level. Furthermore, leaf succulence and high instantaneous water use ef ciency (WUEi) under high salinity Halophyte significantly contributed to maintain leaf water status of this species. Leaf pressure–volume curves showed that 100 Salinity salt-challenged plants adjusted osmotically by lowering osmotic potential at full turgor (Ψπ )alongwithade- Pressure–volume curves crease in leaf cell elasticity (values of volumetric modulus elasticity (ε) increased). As a whole, our findings indi- Water relations cate that A. portulacoides is characterized by a high plasticity in terms of salt-response. Preserving leaf hydration Osmotic adjustment and efficiently using Na+ for the osmotic adjustment especially at high salinities (800–1000 mM NaCl), likely through its compartmentalization in leaf vacuoles, are key determinants of such a performance. The selective ab- sorption of K+ over Na+ in concomitance with an increase in the K+ use efficiency also accounted for the overall plant salt tolerance. © 2014 SAAB. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/). 1. Introduction terrastat). In general salinity can reduce plant growth or damage the plant through: (i) osmotic effect (caused by low water potential + − Salinity is among the most adverse environmental issues for agricul- (Ψw)), (ii) toxic effect (mainly due to Na and Cl ) and (iii) alteration ture, since it affects about 5% of the cultivated areas throughout the of the nutritional balance. To survive with the detrimental effects of salt world. The United Nations Food and Agriculture Organization estimates stress, plants have evolved various combating mechanisms. Among that there are currently 4 million km2 of salinized land and a similar these, ion exclusion, along with other strategies such as adjustment of + area that is affected by sodicity, a condition in which Na ions represent the cell osmotic potential (Ψπ) is of special importance (Türkan and more than 15% of the exchangeable cations (www.fao.org/agl/agl1/ Demiral, 2009). The latter response termed as osmotic adjustment (OA) involves transport, active accumulation, and compartmentaliza- Abbreviations: A, net CO2 assimilation rate; AWC, apoplastic water content; DW, dry tion of inorganic ions and organic compounds (Flowers and Colmer, weight; FAA, free amino acids; FW, fresh weight; GB, glycine betaine; KAE, potassium ab- 2008). During osmotic adjustment cells tend to compartmentalize fi fi – sorption ef ciency; KUE, potassium use ef ciency; OA, osmotic adjustment; P V curves, most of the absorbed ions in vacuoles at the same time as they synthe- pressure–volume curves; RWC, relative water content; RWC0, relative water content at + + size and accumulate compatible organic solutes in the cytoplasm, in theturgor loss point; SK/Na, selectivity of K over Na ;T,transpirationrate;TSS,totalsoluble sugar;WC,watercontent; WUEi, instantaneouswater use efficiency; ε, volumetric modulus order to maintain the osmotic equilibrium between these two compart- Ψ Ψ Ψ elasticity; s, osmotic potential of each measured solute; w, water potential; π,osmotic ments (Parida and Das, 2005). Clearly, tolerance in the form of OA plays Ψ0 Ψ100 potential; π, osmotic potential at the turgor loss point; π , osmotic potential at full an important role in salt-tolerant plants thriving in saline environments turgor. (Flowers and Colmer, 2008). ⁎ Corresponding author. Tel.: +216 79 325 848; fax: +216 79 325 638. fi E-mail address: [email protected] (A. Debez). Halophytes are de ned as plants that live in naturally saline habitats 1 Both authors contributed equally. or that complete their life cycle at a salt concentration of at least http://dx.doi.org/10.1016/j.sajb.2014.08.009 0254-6299/© 2014 SAAB. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/). M. Benzarti et al. / South African Journal of Botany 95 (2014) 70–77 71 200 mM NaCl (Flowers et al., 2010). Facing the increasing salinization with 0.5% (w/v) toluidine blue, were examined using a Zeiss light mi- throughout the world, domestication of these plants as cash crop spe- croscope. Axio software was used to measured leaf cross-section cies, better known as biosaline agriculture, is a currently emerging ap- thickness. proach (Debez et al., 2011). Better understanding of the physiological and molecular mechanisms enabling halophytes to survive and main- 2.3. Water content, succulence and instantaneous water use efficiency tain productivity in saline environments is also a critical issue for re- (WUEi) searchers. A large group of species of Atriplex genus belonging to halophytes having ecological and agronomic importance are frequent Leaf water content was calculated as the difference between fresh in many arid and semi-arid regions of the world, particularly in habitats weight (FW) and dry weight (DW) and is expressed on a dry mass that combine relatively high soil salinity with aridity (Benzarti et al., basis WC = (FW − DW) / DW. Leaf succulence was estimated by divid- 2013) and therefore constitute a useful material for the identification ing leaf water content by leaf surface area (Debez et al., 2004). WUEi of physiological mechanisms involved in salt stress resistance. Atriplex was calculated as the ratio: net CO2 assimilation rate (A) / transpiration (Halimione) portulacoides (Sea purslane) is a widespread C3-type peren- rate (T). Total leaf surface area was measured by a leaf area meter (por- nial halophyte common on salt marshes of Europe, North Africa and table area meter LI/3000A, LI-COR). The gas exchange measurements South-West Asia. Its crunchy and salt tasting leaves are edible as a nat- were made with a portable photosynthesis system (LCA4). ural condiment (Wright, 2009). Interestingly, recent data indicate that this plant could be valorized as a source of valuable phytochemicals, in- 2.4. Inorganic cation contents cluding phenolic compounds (Rodrigues et al., 2014; Vilela et al., 2014). High productivity and capacity to grow in heavy metal contaminated Dried samples of roots, stems and leaves were finely ground. Ion ex- + + soils (Sousa et al., 2008) also make this species potentially useful for sa- traction was achieved in 0.5% HNO3.Na and K were assayed by flame line soil reclamation and phytoremediation purposes and even as fod- emission photometry (Corning, UK) and Cl− by coulometry (Büchler der plants. Recently, we reported that A. portulacoides displayed an chloridometer), while Ca2+ was determined using atomic absorption effective antioxidant defense protecting the photosynthetic machinery spectrometry (VARIAN, Spectra AA 220 FS). + + from salt-induced photodamage under extreme (up to 1000 mM The selectivity of K over Na (SK/Na) was estimated from ion con- NaCl) salinity (Benzarti et al., 2012). Yet, the involvement of the osmotic tents as (Debez et al., 2004): adjustment in the salt stress tolerance of this species especially when hihi ¼ þ= þ þ þ = þ= þ þ þ : challenged with extreme salinity is still unknown. It has to be pointed SK=Na K K Na K K Na leaves medium out that in soils in Mediterranean areas like Tunisia, salinity level may dramatically rise during the long summer season as a result of both The potassium absorption efficiency (KAE) and potassium use effi- high evaporation rate and reduced water availability, resulting in salin- ciency (KUE) were calculated as: ity levels that my exceed seawater salinity. Therefore, we evaluated here the responses of Tunisian population of A. portulacoides when ex- þ KAE μmol K =mg DW posed up to twofold seawater NaCl salinity (1000 mM) in terms of roots ¼ þ = growth, water relations and organic and inorganic solute accumulation Total plant K amount average root DW in relation to osmotic adjustment. where the average root DW is the logarithmic average of the root dry 2. Material and methods weight, =μ þ ¼ = þ : 2.1. Plant material and culture conditions KUE mg DW mol K Whole plant DW total K amount Young plants of A. portulacoides were obtained using cuttings col- lected from mother plants. Uniformly rooted plantlets were trans- 2.5. Organic solute content ferred to pots containing inert sand.
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