Combined effect of NaCl-salinity and hypoxia on growth, photosynthesis, water relations and solute accumulation in Phragmites australis plants

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Abstract

Aim of the present study was to investigate the effects of two key environmental factors of estuarine ecosystems, salinity and hypoxia, on the physiological attributes in reed plants (Phragmites australis (Cav.) Trin. ex Steudel). Growth, leaf gas exchange, water (and ion) relations, and osmotic adjustment were determined in hydroponically grown plants exposed to hypoxia at varying NaCl-salinity concentrations (0, 50, 100, and 200 mM). Plants grew well under hypoxia treatment with standard nutrient solution without added salt and at NaCl concentrations up to 100 mM. Reed plants were able to produce and allocate phytomass to all their organs even at the highest salt level (200 mM NaCl). In plants subjected to hypoxia at various water potentials no clear relationships were found between growth and photosynthetic parameters except for gs, whereas growth displayed a highly significant correlation with plant–water relations. A and gs of reed plants treated with hypoxia at varying water potential of nutrient solutions were positively correlated and the former variable also had a strong positive relationship with E. Leaf Ψw and Ψπ followed a similar trend and declined significantly as water potential of watering solutions was lowered. Highly significant positive correlations were identified between leaf Ψw and photosynthetic parameters. At all NaCl concentrations, the increase in total inorganic ions resulted from increased Na+ and Cl while K+, Ca2+, and Mg2+ concentrations decreased with increasing osmolality of nutrient solutions. Common reed has an efficient mechanism of Na+ exclusion from the leaves and exhibited a high leaf K+/Na+ selectivity ratio over a wide range of salinities under hypoxia treatment. In Phragmites australis grown in 200 mM NaCl, K+ contributed 17% toΨπ, whereas Na+ and Cl accounted for only 11% and 6%, respectively. At the same NaCl concentration, the estimated contribution of proline to Ψπ was less than 0.2%. Changes in leaf turgor occurred with a combined effect of salinity and hypoxia, suggesting that reed plants could adjust their water status sufficiently.

Introduction

Common reed, Phragmites australis (Cav.) Trin. ex Steudel (synonymous to P. communis Trin.), is a widespread species in the temperate regions of the word (Den Hartog et al., 1989). It’s typical habitats are fresh and brackish water areas of swamps, riversides, and lakesides. In the coastal Mediterranean region of Tunisia, P. australis is the main emergent plant species occupying shallow marshes and fringes of lagoons. It is often the key-species in wetland ecosystems and propagates in several ways, by seed dispersion and vegetative from vertical and horizontal rhizomes and stolons. P. australis is well adapted to waterlogging due particularly to the physiological tolerance of its rhizome to anoxia (Brändle and Crawford, 1987; Engloner, 2009; Wijte and Gallagher, 1996) and its aeration capabilities (Armstrong and Armstrong, 1990; Armstrong et al., 1999; Brix, 1990; Gries et al., 1990; Weisner, 1988). Variability of water depth may affect the performance of P. australis by constraining oxygen supply to the below-ground parts of the plant (White and Ganf, 2002). However, reed plants have adapted to terrestrial habitats and various ecotypes have evolved with resistance to drought, salinity and low temperature (Engloner, 2009; Gorai et al., 2007; Haslam, 1975; Matoh et al., 1988; Pagter et al., 2005; Wang et al., 1998; Zheng et al., 2000). Among these, salinity is a well-known stressor of P. australis, leading to reduced vigor and success in brackish and salt marshes (Burdick et al., 2001). According to the literature limits of salt tolerance of reed plants vary widely (Gorai et al., 2007; Hellings and Gallagher, 1992; Hootsmans and Wiegman, 1998; Lissner and Schierup, 1997), but differing levels of salt tolerance among ecotypes have been reported, which might be due to high plasticity and/or genetic factors (Brix, 1999; Clevering and Lissner, 1999).

In wetland habitats, several environmental constraints may influence plant growth and physiological attributes. Factors that can vary spatially within wetlands include salinity and hypoxia. Determination of species-specific salt and waterlogging tolerance and the responsible mechanisms will contribute to an understanding of common patterns of colonization and zonation of the plants occurrences and the dynamics in saline environments. The experiments reported here represent a contribution to this approach. The aim of the present research was to investigate, for P. australis seedlings grown under hydroponic conditions, whether combination of hypoxia with increasing osmolality of nutrient solution was related to growth, water relations, leaf gas exchange and solute accumulation. Our primary hypothesis stated that plant growth and solute accumulation were the most important factors related to the specific effects of ions under NaCl-salinity. To test this, we determined dry matter partitioning, relative growth rate and inorganic and organic solute composition of hydroponically grown reed plants. A second hypothesis proposes that leaf gas exchange and plant–water relations are intimately related with plant growth.

Section snippets

Plant material and culture conditions

Seeds of P. australis were collected in November 2003 from a location near Gabès (southeast Tunisia). Seeds were surface sterilized in 0.58% (w/v) sodium hypochlorite solution for 1 min and germinated on filter paper in 90 mm Petri dishes at controlled conditions (Gorai et al., 2006). Seedlings were transferred to 3 L-plastic tanks for hydroponic growth, using aerated Hewitt nutrient solution (Hewitt, 1966), containing macronutrients (mM): MgSO4 (1.5), KH2PO4 (1.6), K2HPO4 (0.4), KNO3 (3), NH4NO3

Growth and chlorotic status

Three-month-old reed plants were grown hydroponically with continuous air bubbling, at which time a 21 days hypoxic treatment (H) was applied by arrest of air bubbling. Shoots were always maintained in air. As shown in Fig. 1, oxygen levels were maintained at about 20% in the aerated solutions while oxygen levels in the hypoxic solutions rapidly decreased to 8% within 1 day and by 2 day had stabilized to about 4%. There was no gradient of oxygen between 5 and 15 cm below the surface.

P. australis

Discussion

Hypoxia and salinity are two key environmental factors (stresses) of estuarine ecosystems. The ability to overcome multiple and simultaneous stresses is of great importance for the plant growth and survival in such environments (Lichtenthaler, 1996). This study evaluated the physiological response of P. australis grown under interactive effects of salinity and hypoxia in nutrient solution.

The reed plants grew optimally under hypoxia control conditions and at moderate salinity in comparison with

Acknowledgements

The authors are grateful to Prof. Rainer Lösch and anonymous referees for their critical reading and revision of the manuscript.

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