Changes in leaf gas exchange, water relations, biomass production and solute accumulation in Phragmites australis under hypoxic conditions

Acta Ecologica Sinica 31 (2011) 97–102

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Changes in leaf gas exchange, water relations, biomass production and solute accumulation in Phragmites australis under hypoxic conditions Mustapha Gorai a,⇑, Mustapha Ennajeh b, Jie Song c, Habib Khemira b, Mohamed Neffati a a

Laboratoire d’Ecologie Pastorale, Institut des Régions Arides, 4119 Médenine, Tunisia Laboratoire des Biotechnologies Végétales Appliquées à l’Amélioration des Cultures, Faculté des Sciences de Gabès, 6072 Gabès, Tunisia c College of Life Science, Shandong Normal University, 250014 Jinan, China b

a r t i c l e

i n f o

Article history: Received 22 March 2010 Revised 6 November 2010 Accepted 31 December 2010

Keywords: Growth Hypoxia Photosynthesis Reed plant Solute accumulation Water relations

a b s t r a c t The physiological responses to hypoxic stress were studied in the common reed, 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 10, 20 and 30 days of oxygen deficiency. The highest growth of reed seedlings was found in normoxic (aerobic) conditions. Treatment effects on biomass production were relatively consistent within each harvest. Leaf water potential and osmotic potential declined significantly as hypoxia periods increased. However, leaf turgor pressure showed a consistent pattern of increase, suggesting that reed plants adjusted their water status by osmotic adjustment in response to root hypoxia. After 20 and 30 days in the low oxygen treatment, net CO2 assimilation and stomatal conductance were positively associated and the former variable also had a strong positive relationship with transpiration. Short-term hypoxic stress had a slight effect on the ionic status (K+, Ca2+ and Mg2+) of reed plants. In contrast, soluble sugar concentrations increased more under hypoxic conditions as compared to normoxia. These findings indicate that hypoxia slightly affected the physiological behavior of reed plants. Ó 2011 Ecological Society of China. Published by Elsevier B.V. All rights reserved.

1. Introduction Phragmites australis (Cav.) Trin. ex Steud. (synonymous to Phragmites communis Trin.), known as common reed, is a member of the Poaceae that relies on both sexual reproduction and vegetative spreading of its clones. This species has wide ecological and geographical amplitudes and grows under a variety of environmental conditions and develops very well in rather deep water [1–3], but can also tolerate extensive periods of drought with reduced availability of water [4]. Under natural or experimental conditions plants can be subjected to a great range of oxygen availability, from normal levels (normoxia) through deficiency (hypoxia) to total absence (anoxia). Root submergence leads to reduced gas exchange between the plant tissue and the atmosphere, because gases (in particular oxygen) diffuse 104 times more slowly in water than air [5]. These changes include the lowering of the redox status of the soil [6]. In many species, reduced soil conditions may adversely affect plant physiological functioning such as plant nutrition, water relations, activity of photosynthetic enzymes, leaf gas exchange, photosynthetic electron transport and photosystem 2 (PS2) activity [6–12]. Comparing P. australis, Carex cinerascens and Hemarthria ⇑ Corresponding author. Tel.: +216 75633005; fax: +216 75633006. E-mail address: [email protected] (M. Gorai).

altissima from wetland habitats, Li et al. [13] found only C. cinerascens that decreased its net photosynthetic rate and stomatal conductance with flooding. No significant changes in PS2 activity were observed in all three species which suggests that the photosynthetic apparatus was not damaged. In order to tolerate hypoxic stress, they may further undergo biochemical and metabolic changes [14]. The supply of carbohydrates and the regulation of carbohydrate and energy metabolism are important for enduring hypoxic stress. In spite of this, the roots of many plants accumulate sugars, amino acids and reserves when subjected to oxygen deficiency [15,16]. Faced with oxygen depletion in the soil, plants have evolved a wide range of characteristic responses, including morphological and anatomical changes that appear to reduce the impact of the stress [17]. Adaptation of plants to long-term hypoxia is frequently associated with developmental changes such as root aerenchyma formation, internode and petiole elongation, adventitious root development and alteration of root porosity, morphology and depth [14–18]. P. australis is well adapted to waterlogging due particularly to the physiological tolerance of its rhizome to anoxia [19,20] and its aeration capabilities [21–27]. Gries et al. [22] determined 58%, 42% and 23–38% porosity for rhizomes, culms and roots, respectively, whereas Justin and Armstrong [28] by comparing 91 plant species from wetland, non-wetland and intermediate habitats found only Juncus inflexus to have higher root porosity

1872-2032/$ - see front matter Ó 2011 Ecological Society of China. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.chnaes.2010.12.003

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than P. australis with maximum values of 53% and 51.9%, respectively. In P. australis both humidity- and Venturi-induced convections enhance greatly the oxygen regime of the rhizome and the efflux of oxygen to the rhizosphere from adventitious roots and their laterals [29]. By measuring root and rhizome respiration at different temperatures (5–20 °C) and oxygen concentrations (0– 0.21 mmol L–1), Gries et al. [22] showed that P. australis is able to maintain aerobe respiration at low concentrations and the saturation concentration was estimated to be less than 0.03 mmol O2 L–1 at 20 °C. Plant responses to hypoxia depend upon plant organ, developmental stage and genotype, as well as the magnitude (frequency and time of exposure) of stress [14,30–32]. The response to environmentally induced oxygen deprivation has been studied in species that range from submergence sensitive to submergence tolerant. Determination of species-specific hypoxia tolerance and the responsible mechanisms will contribute to an understanding of common patterns of colonization and zonation and their dynamics in wetland habitats. The aim of the present research was to investigate, for P. australis seedlings grown under hydroponic conditions, whether duration of hypoxia stress is related to growth, leaf water relations, gas exchange characteristics and solute accumulation. 2. Materials and methods 2.1. Plant material and treatments Seeds of P. australis were collected in November 2003 from a location near Gabès (33°430 N, 10°160 E; southeast Tunisia). Seeds were surface sterilized in 0.58% (w/v) sodium hypochlorite solution for one min and germinated on filter paper in 90 mm Petri dishes at controlled conditions [33]. Seedlings were transferred for hydroponic growth using aerated Hewitt nutrient solution [34] containing: 1.5 mM MgSO4, 1.6 mM KH2PO4, 0.4 mM K2HPO4, 3 mM KNO3, 2 mM NH4NO3, 3.5 mM Ca(NO3)2, 0.5 ppm MnCl2, 0.04 ppm CuSO4, 0.05 ppm ZnSO4, 0.02 ppm Mo7O24(NH4)6, 0.5 ppm H3BO3 [35] and 45 lM EDTA-Fe [36]. All nutrient solutions were renewed every week. Plants were grown in a growth chamber as follows: 25 °C ± 1 °C temperature, 50% day and 75% night relative humidity and 16–8 h-day-night photoperiod, and 250 lmol m–2 s–1 photosynthetic active radiations (PAR). The experiment design was two levels of root hypoxic treatment (normoxia and hypoxia)  three different durations of treatment (10, 20 and 30 days)  six replicates. After 2 months of hydroponic growth, root hypoxia was initiated by stopping aeration, with shoots always maintained in air. Aeration of hydroponic tanks was arrested for 10, 20 and 30 days in the hypoxic treatments or continued for the same length of time in normoxic controls. The oxygen pressure was measured with a Jenway 9500 Dissolved Oxygen Meter (Jenway, London, UK). Ten milliliters of culture media were removed from the non-aerated (hypoxic) and aerated tanks at 5 and 15 cm below the surface and immediately transferred into the electrode chamber. Three repetitions were carried out for each measurement. 2.2. Growth and water relationships Four harvests were made, at the beginning of treatment and 10, 20, and 30 days later. At the harvests, leaves, stems and roots were successively rinsed three times in cold water and blotted between two layers of filter paper. The fresh weight (FW) was measured immediately, and the dry weight (DW) after 48 h of desiccation in an oven at 60 °C. The water content (WC) of different tissues was determined as WC (g H2O g1 DW) = (FW  DW)/DW. Leaf

water potential (Ww) was measured using a pressure chamber (pms Instruments Co., Corvallis, OR, USA) after 10, 20 and 30 days of normoxia or hypoxia treatment, according to Scholander et al. [37]. After measuring of Ww, the samples were frozen in liquid nitrogen and stored at 20 °C. Leaf tissues were thawed and centrifuged at 1200  g for 25 min at 4 °C to extract the cell sap. A vapor pressure osmometer (Wescor 5520, Logan, UT, USA) was used to determine osmolality of the sap expressed from leaves, which was converted to osmotic potential (Wp), by the van’t Hoff equation: Wp = –ciRT, where ci is the measured osmolality (mosmol Kg–1), R is the ideal gas constant and T is the absolute temperature (K) [38]. Turgor potential (Wp) was determined using the relationship: Wp = Ww – Wp. 2.3. Leaf gas exchange characteristics Photosynthetic gas exchange parameters were measured using an LCA-4 portable photosynthesis system (ADC, BioScientific Ltd., Hoddensdon, UK). During measurements, the relative air humidity was maintained at 60% and leaf temperature was 25 °C in the leaf chamber. The CO2 concentration in the leaf chamber was set at 360 lmol mol1. The leaf was irradiated with PAR of 1500 lmol m2 s1 of internal light source. The third youngest fully expanded leaf was used for these measurements. Readings were logged every 30 s until stable values for leaf CO2 assimilation rates (A), transpiration rates (E) and stomatal conductance (gs) were reached. 2.4. Ions and soluble sugars determination K+, Ca2+ and Mg2+ were assayed by using a Schimazu AA-6800 atomic absorption spectrophotometer (Shimadzu Ltd., Kyoto, Japan) after nitric acid extraction (HNO3, 0.5%) of the finely grounded dry matter. Soluble sugars were extracted and estimated according to Robyt and White [39]. 2.5. Statistical analysis Data were analysed using SPSS for Windows, version 11.5. A two-way analysis of variance (ANOVA) was carried out to test effects of main factors (treatment and duration) and their interaction on the physiological parameters. 3. Results Two-month-old reed plants were grown hydroponically under normoxic conditions, at which different durations of root hypoxic treatment (10, 20 or 30 days) were applied by arrest of aeration. Shoots were always maintained in air. As shown in Fig. 1, oxygen levels were maintained at about 20% in the aerated tank while oxygen levels in the hypoxic tank rapidly decreased to 8% within 1 day and then remained at 4% throughout the experiment period. There was no gradient of oxygen between 5 and 15 day cm below the surface. The highest growth of P. australis seedlings were recorded in aerobic conditions (Table 1). The whole plant dry mass was significantly affected by hypoxic treatment and by duration (Table 2). Treatment effects on biomass production were relatively consistent within each harvest. Leaf and stem dry mass of seedlings decreased under hypoxic conditions as compared to controls, while root dry weight was not significantly affected. In addition, oxygen-deficiency duration significantly affected the biomass production of different organs (Table 2). Root hypoxic growth conditions slightly decreased the hydration of leaves and roots as compared to that of seedlings from

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Table 2 Results of a two-way ANOVA of traits related to growth, water relations, CO2 and H2O exchange and solute accumulation for Phragmites australis plants by hypoxic treatment (T), duration (D) and their interaction.

Oxygen percentage

25 20

Parameter

Main factors

10 5 0

0

5

10

15

20

25

30

Time (days) Fig. 1. Variation of oxygen percentage in aerated and non-aerated hydroponics tanks as a function of the duration of hypoxic treatment. The oxygen pressure was measured using a Jenway 9500 DO2 m at 5 cm (h, D) and 15 cm (j, N) below the surface of the nutrient solution in the aerated and non-aerated hydroponic tanks, respectively.

Table 1 Leaf, stem, root and whole plant dry weight (DW, g plant–1) of Phragmites australis when 2-month old plants were subjected for 10, 20, and 30 days to normoxic (N) or hypoxic (H) conditions in nutrient solution. Parameter

Treatment Time (day) 10

20

30

Leaf dry weight N H

0.152 ± 0.025a 0.357 ± 0.060a 0.431 ± 0.095a 0.124 ± 0.023a 0.246 ± 0.051b 0.392 ± 0.063a

Stem dry weight

N H

0.133 ± 0.028a 0.429 ± 0.044a 0.494 ± 0.080a 0.119 ± 0.022a 0.291 ± 0.073b 0.407 ± 0.063a

Root dry weight N H

0.041 ± 0.004a 0.123 ± 0.024a 0.146 ± 0.032a 0.039 ± 0.004a 0.103 ± 0.034b 0.131 ± 0.022a

Whole plant dry weight

0.326 ± 0.051a 0.909 ± 0.105a 1.071 ± 0.198a 0.282 ± 0.046a 0.641 ± 0.148b 0.930 ± 0.125a

N H

TD

Treatment (T)

Duration (D)

Degrees of freedom Leaf dry weight Stem dry weight Root dry weight Whole plant dry weight Leaf water content Stem water content Root water content Leaf water potential (Ww) Leaf osmotic potential (Wp) Leaf turgor (Wp) CO2 assimilation rates (A) Transpiration rate (E) Stomatal conductance (gs)

1 5.94* 11.68** 1.66ns 8.56** 7.20* 1.91 ns 5.01* 64.61*** 112.37*** 8.89** 23.38*** 18.92*** 16.28***

2 43.25*** 68.61*** 38.51*** 62.92** 9.92*** 8.08** 1.25ns 38.75*** 106.92*** 17.58*** 55.31*** 11.07*** 16.39***

2 1.15 ns 2.36ns 0.29ns 1.58ns 0.20ns 1.83ns 0.25ns 13.81*** 8.26** 2.26ns 1.81ns 0.71ns 0.68ns

Leaves Concentration Concentration Concentration Concentration

of of of of

K Mg Ca SS

6.36* 13.75** 12.47** 19.27**

21.48*** 5.08* 15.86*** 15.52***

0.92ns 2.53ns 0.35ns 0.12ns

Stems Concentration Concentration Concentration Concentration

of of of of

K Mg Ca SS

0.23ns 0.54ns 1.18ns 6.69*

33.06*** 1.21ns 0.26ns 9.12**

2.17ns 0.77ns 0.20ns 0.07ns

Roots Concentration Concentration Concentration Concentration

of of of of

K Mg Ca SS

0.97ns 0.26ns 4.07ns 12.06**

11.60*** 0.10ns 1.05ns 11.81**

4.67* 1.07ns 1.09ns 0.78ns

15

SS: soluble sugars. ns = non-significant. * P < 0.05, Numbers are F-values significant. ** P < 0.01, Numbers are F-values significant. *** P < 0.001; Numbers are F-values significant.

Means (n = 6 ± 95% confidence limits) within a column followed by the same letter are not significantly different between treatments at the 0.05 probability level based on student’s t-tests.

20 Normoxia Hypoxia

WC (g H2O g–1 DW)

15 the aerobic treatment, and only variability of the stem water content was not significantly affected (Fig. 2, Table 2). The water content of leaves and stems was significantly affected by treatment duration irrespective of whether roots were subjected to normoxic or hypoxic conditions; however, root water content did not show any significant effect. Leaf Ww and Wp of P. australis seedlings were significantly lower in plants subjected to hypoxic conditions than in controls (Fig. 3a and b), and were significantly affected by an interaction (Table 2). Data for Wp showed a consistent pattern increasing under hypoxia and was significantly affected by hypoxia and by duration of treatment (Fig. 3c, Table 2). After 20 and 30 days in the low oxygen treatment, P. australis plants decreased their net photosynthetic rates as compared to controls (Table 3). The reduction in A was due to hypoxia and duration of treatment. In the same treatments values of gs were significantly decreased and were correlated with lower transpiration rates with R2 = 0.79 (Tables 2 and 3). The chlorophyll (Chl) concentrations did not differ significantly by hypoxic treatment and by duration (on average 2.23, 0.86 and 3.09 mg g–1 FW, respectively, for Chl a, Chl b and Chl Total, data not shown). Reed plants cultivated under hypoxic conditions showed a slight variation in their ionic status. The concentrations of K were more abundant in stems than in roots and leaves, respectively,

10

5

0 10

20

Leaves

30

10

20

Stems

30

10

20

30

Roots

Fig. 2. Changes in tissue water content (WC, g H2O g–1 DW) of Phragmites australis when 2-month old plants were subjected for 10, 20, and 30 days to normoxic or hypoxic conditions in nutrient solution. Data represent mean ± 95% confidence limits (n = 6).

while the concentrations of Ca and Mg were higher in leaves than in roots and stems, respectively (Fig. 4a–c). Leaf-ion concentrations were significantly affected by hypoxia and by duration of treatment (Table 2). In both stems and roots, inorganic solute concentrations were not significantly affected by hypoxic treatment; however, the concentrations of K showed significant changes as

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increasing hypoxic periods (Fig. 4b, and c; Table 2). The concentrations of soluble sugars in different organs were stimulated by decreased oxygen levels and by increasing hypoxic periods (Fig. 4a–c, Table 2). The soluble sugar concentrations were higher in leaves than in stems and roots, respectively. After 20 and

0.0

Ψw (MPa)

0.5 -1.0 -1.5 -2.0 -2.5 -3.0 0.0

(a)

Ψπ (MPa)

0.5 -1.0 -1.5 -2.0 -2.5

(b)

-3.0 2.0 Normoxia

(c)

Hypoxia

Ψp (MPa)

1.5

1.0

0.5

0.0 10

20

30

Duration of hypoxic treatment (days) Fig. 3. Changes in (a) water potential (Ww, MPa), (b) osmotic potential (Wp, MPa) and (c) pressure turgor (Wp, MPa) in leaves of Phragmites australis when 2-month old plants were subjected for 10, 20 and 30 days to normoxic or hypoxic conditions in nutrient solution. Data represent mean ± 95% confidence limits (n = 6).

30 days, leaf-soluble sugar concentrations were significantly higher under hypoxic conditions than in controls.

4. Discussion Plants react to hypoxic conditions by developing strategies ranging from complete tolerance to avoidance [40]. Our experiments clearly show that P. australis responds to root hypoxia by decreasing slightly its leaf and whole plant growth. The present data agree with previous earlier findings reported on Spartina patens [41], Lepidium latifolium [42] and Trifolium subterraneum [31]. Reduction in photosynthetic activity is another consequence of low oxygen availability and may be due either to stomatal closure or to non-stomatal inhibition [9,43]. The present study depicts that the stomatal conductance decreased in plants subjected to increasing hypoxic periods, indicating that the significant photosynthetic depression, observed after 20 and 30 days of treatment may at least partly be caused by deficiency of CO2 supply due to stomatal closure. It appears that the net CO2 assimilation, stomatal conductance, and transpiration of reed plants were positively associated and identified high positive relationships. Other factors may contribute to the reduction in photosynthetic capacity including low leaf chlorophyll content. Leaf chlorophyll content decreases in some wetland plants that are subjected to low oxygen conditions [44], but no detectable changes were found in our experiments, in accordance with data obtained previously by Pezeshki et al. [10]. Changes in chlorophyll fluorescence emission arising mainly from the PS II provide information on almost all aspects of photosynthetic activity. According to Li et al. [13] no damage to the photochemical apparatus of photosynthesis was observed in leaves of P. australis under flooded conditions. Our data show that hypoxic conditions decreased slightly the water content of leaves as compared to that of seedlings from the normoxic controls. Stomatal closure during flooding is a behavior that regulates the water balance of susceptible plants and is a critical response in preventing leaf dehydration [45]. Furthermore, leaf water potential and osmotic potential of P. australis seedlings were significantly lower than controls at different durations of hypoxia. In this way, the decrease in transpiration rate along with the lower leaf water potential and osmotic potential in flooded conditions suggest that stomatal conductance was effective in regulating the water status of P. australis. Clearly, a consistent pattern of increase in leaf turgor pressure was shown with low oxygen concentration. These data are closely aligned with those in Pezeshki [6] and Sousa and Sodek [46] for wetland plants inhabiting flooded soils. In flooded conditions, plant nutrition is influenced by soil flooding and the associated reducing soil conditions [47]. In some wetland plants ion uptake may continue partly because of the internal O2 supply system [48] but partial anoxia in roots can reduce solute

Table 3 Leaf gas exchange characteristics of Phragmites australis when 2-month old plants were subjected for 10, 20, and 30 days to normoxic (N) or hypoxic (H) conditions in nutrient solution. Parameter

Treatment

Time (day) 10

20

30

9.53 ± 0.28a 8.92 ± 0.43a 2.23 ± 0.65a 1.65 ± 0.19a 0.151 ± 0.047a 0.112 ± 0.021a

10.92 ± 0.83a 9.07 ± 0.20b 3.46 ± 0.12ª 2.33 ± 0.73b 0.213 ± 0.006a 0.152 ± 0.044b

13.54 ± 0.88a 11.89 ± 0.59b 3.70 ± 0.61a 2.56 ± 0.52b 0.279 ± 0.056a 0.196 ± 0.011b

CO2 assimilation rate (A) (lmol m–2 s–1)

Transpiration rate (E) (mmol m–2 s–1) Stomatal conductance (gs) (mol m–2 s–1)

N H N H N H

Means (n = 6 ± 95% confidence limits) within a column followed by the same letter are not significantly different between treatments at the 0.05 probability level based on student’s t-tests.

M. Gorai et al. / Acta Ecologica Sinica 31 (2011) 97–102

Normoxia Hypoxia

(a)

1.5

101

a critical response in preventing leaf dehydration. Furthermore, the decrease in transpiration rate along with the lower leaf water potential and osmotic potential suggest that stomatal conductance was effective in regulating the water balance of this species under hypoxic conditions.

1.0

References 0.5

0.0

(b)

Contents (mmol g−1 DW)

102030102030102030102030 K+Ca2+Mg2+SS

1.5

1.0

0.5

0.0

(c)

102030102030102030102030 K+Ca2+Mg2+SS

1.5

1.0

0.5

0.0 10

20

30

10

20

+ 2+ K K+Ca2+Mg2+SS Ca

30

10

20

Mg2+

30

10

20

30

SS

Fig. 4. Changes in K+, Ca2+, Mg2+ and soluble sugar (SS) contents (mmol g–1 DW) in (a) leaves, (b) stems, and (c) roots of Phragmites australis when 2-month old plants were subjected for 10, 20 and 30 days to normoxic or hypoxic conditions in nutrient solution. Data represent mean ± 95% confidence limits (n = 6).

intake [49]. Our data show that hypoxic treatment has a significant effect on leaf concentrations of K+, Mg2+ and Ca2+ in reed plants. Low oxygen concentration in the media has been shown to decrease the nutrient uptake in Spartina sp. [7,50,51] and low internal oxygen concentration has been shown to decrease the growth rate of P. australis, probably due to decreased nutrient acquisition [52]. The supply of carbohydrates and the regulation of carbohydrate and energy metabolism are important for enduring hypoxic stress [53,54]. Our results showed that soluble sugar concentrations in roots were enhanced in reed plants subjected to hypoxic conditions. The present data agree with previous earlier findings revealing that the roots of many plants accumulate sugars when subjected to oxygen deficiency [15,54]. From these results, it can be concluded that root hypoxia slightly affected the physiological behavior of P. australis plants. It appears that plants under deprived-oxygen conditions remain able to produce phytomass. Short-term hypoxic stress had a slight effect on the ionic status of reed plants, while leaf-soluble sugar concentrations increased as compared to normoxic conditions. Reed plants tolerate oxygen deficiency by maintaining its growth attributes and water (and ion) relations. The net CO2 assimilation and stomatal conductance of reed plants were positively associated and the former variable also had a strong positive relationship with transpiration. This behavior regulates the water status and is

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