Comparative study on the resistance of Suaeda glauca and Suaeda salsa to drought, salt, and alkali stresses

Ecological Engineering 140 (2019) 105593

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Comparative study on the resistance of Suaeda glauca and Suaeda salsa to drought, salt, and alkali stresses

T

Jingsong Lia,b, Tabassum Hussainc, Xiaohui Fenga, Kai Guoa,b, Huanyu Chena,b, Ce Yanga,b, ⁎ Xiaojing Liua,b, a

Key Laboratory of Soil Ecology, Center for Agricultural Resources Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, China University of Chinese Academy of Sciences, China c Institute of Sustainable Halophyte Utilization, University of Karachi, Pakistan b

A R T I C LE I N FO

A B S T R A C T

Keywords: Suaeda glauca Suaeda salsa Salt stress Alkali stress Drought stress Artificial revegetation

Suaeda glauca and Suaeda salsa are annual chenopod herbs that grow well in saline-alkali lands, and they share a number of morphological and physiological traits. We found that the natural distributions of these two halophytes were regionally heterogeneous in the saltmarsh of the Bohai coast, China. In the present study, habitat surveys and laboratory tests were conducted to examine the adaptability of S. glauca and S. salsa in variable environments. The habitat survey showed that S. glauca preferred to establish in soil with a lower moisture, lower EC, and higher pH as compared to S. salsa, suggesting that the adaptability of S. glauca and S. salsa to drought, salt, and alkali conditions varies. In the laboratory, these abiotic stresses were simulated at varying degrees by hydroponic culture. Plant biomass, water content, cations and anions distribution were measured after 10 days treatments. The results showed that (1) the inhibitory effect of the drought treatment on S. salsa shoot fresh weight and water content was less than that on S. glauca. Low and moderate drought treatments inhibited the root growth of S. glauca but promoted S. salsa root growth with Mg2+ and SO42− accumulation. (2) S. glauca and S. salsa were both highly resistant to salinity, and their adaptive strategies were similar. The optimum NaCl concentration for S. salsa was 200 mM, higher than that of 100 mM for S. glauca, and a greater K+ deficiency was observed in S. glauca roots under high salinity treatment. (3) Although high alkali stress was destructive to S. glauca and S. salsa, low alkali treatment promoted the plants root growth, and this promotion in S. glauca was greater than that in S. salsa. Furthermore, low and moderate alkali treatments significantly increased Ca2+ and Mg2+ contents in S. glauca root but had little effect in S. salsa. These results indicated that S. salsa was more tolerant to drought and salt stresses than S. glauca but less tolerant to alkalinity. The resistance variation between the two species was mainly due to their root adaptability and the potential cations regulation. Moreover, our study suggests that S. salsa is an optimal species for the artificial revegetation in high saline land, while S. glauca is more adaptable to alkali land.

1. Introduction Soil salinization and alkalization are common problems worldwide. Saline-alkali soil is not only a hindrance for crop production but also unfavorable for urbanization because of the deserted environment. In China, a 2469 km2 sea reclamation plan was approved by the State Council in 2011–2020 for economic development (Wang et al., 2014a,b). This new land was very saline and without vegetation, inevitably leading to sandstorms and a poor landscape (Li et al., 2015). To solve this problem, attention has been paid to artificial revegetation, which is an effective and sustainable method for ecological

rehabilitation, especially on large spatial scales where the afforest technique based on external soil is restricted (Chen et al., 2018). The harsh soil conditions in saline-alkali land impeded most landscape plants, leading to a critical limiting factor for artificial revegetation. Furthermore, soil salinization frequently occurs with drought and alkali conditions simultaneously, which are all adverse to plants (Ye et al., 2009; Wen et al., 2017; Liu et al., 2018a,b; Lan et al., 2010; Chen et al., 2017). Hence, resistant plant for those dramatic variations was the best choice for establishing vegetation in a stressful environment, and various constraints adaptability and feasibility assessments must be conducted as the preliminary process in ecological revegetation (Teal and

⁎ Corresponding author at: Key Laboratory of Soil Ecology, Center for Agricultural Resources Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, China. E-mail address: [email protected] (X. Liu).

https://doi.org/10.1016/j.ecoleng.2019.105593 Received 27 February 2019; Received in revised form 19 August 2019; Accepted 6 September 2019 0925-8574/ © 2019 Published by Elsevier B.V.

Ecological Engineering 140 (2019) 105593

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separated this slope plane into two isometric parts, each consisting of adjacent quadrats. The higher lines of quadrats were collectively referred to as A, and the lowers lines were referred to as B. Each quadrat was 1.5 m × 1.5 m (shown in Fig. 1b). Soil samples (0–30 cm depth) from each quadrat were taken in May, July, and September 2017. The soil samples were weighed and then dried at 65 °C to the constant weight, soil moisture (%) was calculated by (fresh weight-dry weight)/ dry weight. An extract solution (gravimetric soil: water = 1:5) of the soil sample was used to measure the soil EC, soil pH with conductivity meter (Horiba, B-173) and digital pH meter (Sartorius, PB-10). Habitat soil texture was measured by Mastersizer 3000 (Malven) with air-dried soil samples. In September 2017, plant coverage (%) of S. glauca and S. salsa was measured with the traditional ocular method, and dominance index (Berger-Parker index) was calculated from the ratio of the certain plant number to all plants number in quadrat.

Weishar, 2005; Shabala, 2013; Shaygan et al., 2017). Suaedas are cosmopolitan annual chenopods that are naturally confined to inland saline lands and tidal wetlands. The succulent nature and salt absorption capacities allow them to thrive in high saline habitats and become pioneer plants in saline-alkali lands (Song and Wang, 2015). As ecologically economic halophytes, Suaedas are widely utilized for the restoration of contaminated or salinized land (KE-FU, 1991; Sun et al., 2016; Zhang et al., 2018). The study of Ravindran et al. (2007) showed that in a single harvest of the plant, S. maritima and S. portulacastrum could remove more than 470 kg sodium chloride from 1 ha saline soil. Furthermore, the planting of S. salsa in the Tianjin Estuary area, China, increased the soil organic matter content by 43.4% and the total soil nitrogen by 17.8% and greatly increased the soil microbial amount, potentially improving the saline soil quality (Lin et al., 2005). S. glauca and S. salsa are native saltmarsh species of the Bohai coast, China. They are morphologically and physiologically similar and have synchronous phenology. While their natural distributions are discrepant, there is rare meta-population of S. glauca and S. salsa (He et al., 2012). This interesting phenomenon provoked us to investigate their natural habitat soils and design a study in which we addressed plant adaptability to various environmental constraints. At present, a large number of reports have focused on the effects of drought, salt, and alkali constraints on plants (Tiwari et al., 2010; Chen et al., 2011; Li et al., 2018; Liu et al., 2018a,b). Drought stress influences plant growth via water and nutrient uptake simultaneously (Chen et al., 2011). Salt stress is caused by excessive neutral salts (NaCl and/or Na2SO4), and it arrests plant growth by a combination of osmotic stress and ionic toxicity (Munns, 2002). Alkali stress is caused mainly by alkali salt (Na2CO3 and/or NaHCO3) with similar damaging factors as those of salt stress but with an added effect of high-pH stress (Yang et al., 2008a,b). Studies reporting alkali stress in high-pH calcareous (Brand et al., 2002), alkaline soil (Hartung et al., 2002), and composite alkali salinity (Yang et al., 2007) clearly indicated that alkali stress was more destructive to plants than neutral salt stress. The study of Yang et al. (2008a,b) on S. glauca showed that alkali stress was more destructive to plant growth than salt stress at equal salinities, and the anion contributions of ionic equilibrium differed under salt and alkali stress (Yang et al., 2008a,b). Kefu et al. (2003) reported that drought stress (PEG-6000) had more serious negative effect on S. salsa than isosmotic NaCl stress. The research of He et al. (2012) focused on the contrasting competitive abilities between S. glauca and S. salsa and their facilitative interactions with T. chinensis (He et al., 2012). However, the comparison of the resistances of S. glauca and S. salsa to those constraints was limited known. The aim of this study was to assess the feasibility of S. glauca and S. salsa for revegetation planning in semi- arid, salt, or alkali lands based on plant adaptability. In this study, field surveys and laboratory tests were conducted with these two species. Plant coverage, dominance index, soil moisture, soil EC and soil pH were measured in the field to confirm the stress factors in habitats. Varying degrees of drought (PEG), salt (NaCl), and alkali (Na2CO3) treatments were applied via hydroponic culture to examine the plant growth, water content, cations and anions distribution in S. glauca and S. salsa seedlings.

2.2. Laboratory tests Seeds of S. glauca and S. salsa were collected in November 2017 and then stored at 4 °C. Seeds were sterilized with 5% sodium hypochlorite solution for 5 min following germination in distilled water at 25/20 °C in the dark. Ten seedlings were placed into the holes of a foam and transferred into cylindrical plastic containers (6.5 cm high, 7.5 cm diameter) filled with 300 ml half-strength Hoagland’s nutrient solution. Polyethylene glycol-6000, NaCl, and Na2CO3 were used to simulate drought, salt, and alkali stress, respectively. In each stress group, three concentrations of solute were applied for varying stress degrees (shown in Table 1). We measured the treatments solution osmotic potential through Dewpoint potential meter (Decagon, WP4C), solution EC through conductivity meter (Horiba, B-173), and solution pH through digital pH meter (Sartorius, PB-10). After 10 days of hydroponic culturing in the growth chamber at 25 °C/20 °C for 14 h/10 h (light: dark), four plants were removed from each treatment and separated into shoots and roots and fresh weight (FW) was measured immediately. Dry weight (DW) of samples was obtained after oven dry at 70 °C for 48 h. The percent water content (WC%) was calculated as follows: WC% = (FW − DW)/DW. The root/shoot ratio was calculated by the dry biomass ratio of roots to shoots. Cations Na+, K+, Ca2+, Mg2+ and anions Cl−, SO42−, NO3− were estimated in a hot water extract with the help of an Ion chromatograph (Dionex ICS2100, China). HCO3− content was measured by the titration method using sulphuric acid, phenothalin, and methyl orange. 2.3. Statistical analyses All experiments were based on four replicated measurements. Data were analyzed with SPSS 16.0 software (SPSS Inc., Chicago, IL, USA). One-way analysis of variance (ANOVA) was performed to test the difference between two habitats and to test the varying degrees stress effects on plants. The term significant indicates differences for which P ≤ 0.05. 3. Results 3.1. Habitat soil survey

2. Materials and methods As shown in Table 2, the most soil particle size in sample A and B were silt, and their soil textures were both silt loam type on soil texture classification in USDA. In sample A, the vegetation coverage and dominance index of S. glauca were significantly (P < 0.05) higher than those of S. salsa (shown in Fig. 2), indicating that S. glauca was the dominant species in A quadrats. Moreover, we found that the S. salsa population was mainly distributed in B quadrats. The soil moisture of B samples was significantly (P < 0.05) higher than that of A samples during the same periods (shown in Fig. 3a). From May to September, the soil EC of A samples varied from 1.5 to 3.6 Ds/m, while it varied

2.1. Field survey The plant communities of S. glauca and S. salsa and their habitat soil surveys were conducted at the costal saltmarsh in Haixing County, Hebei Province, China (117°32′~117°58′E, 38°19′~38°29′N) where the soil was classified as inceptisols according to the Soil Taxonomy, 1999 in NRCS soil classification system. As shown in Fig. 1a, S. glauca naturally established on the high plot of an earthen slope and S. salsa was distributed on the lower part of the slope. We longitudinally 2

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Fig. 1. The natural distributions (a) of S. glauca and S. salsa and the corresponding quadrats on the earthen slope (b). This picture (a) was taken in September 2017 at the saltmarsh of Haixing County, Hebei Province, China. A1-A4 and B1-B4 in picture (b) respectively means the 4 replicates of the plots of A and B.

from 3.0 to 5.1 Ds/m for B samples (shown in Fig. 3b). B samples showed higher soil moisture and EC, but lower soil pH level than A samples. As compared with B, samples A were at a higher elevation where soil desalination and salification happened frequently during the rainy season (June to September) and this iterative process was usually accompanied by soil alkalization. In May, S. glauca seedlings were mostly established in soil with pH of 8.7, and the pH value of S. salsa habitat soil was 8.1 (shown in Fig. 3c).

Table 2 Distribution of the soil particle sizes in sample A and B. Soil sample

Sand (50–2000 µm)%

Silt (2–50 µm)%

Clay (< 2µm)%

A B

20.86 ± 0.16 24.53 ± 0.13

77.40 ± 0.16 74.10 ± 0.13

1.76 ± 0.00 1.37 ± 0.00

were un-changed in all saline treatments (Fig. 6). Low alkalinity (A1) had a little effect on shoot fresh weight of S. glauca and S. salsa, however it enhanced root growth significantly (P < 0.05) (Fig. 4c, d) as compare to the control plants. Further increase in alkalinity in the substrate led a linear declined in shoot FW up to 80% and 70%, while root FW about 70% and 65% in S. glauca and in S. salsa respectively in comparison to control. S. glauca and S. salsa had a similar root/shoot ratio as the control (Fig. 7). Low (D1) and moderate (D2) drought treatments had little effect on S. glauca, while they promoted the root/shoot ratio of S. salsa. With the increasing intensity of salt treatments, the root/shoot ratio of S. glauca and S. salsa decreased. At low (S1) and moderate salt (S2) treatments, the root/shoot ratio of S. salsa was higher than that of S. glauca. High alkali (A3) treatment decreased the root/shoot ratio of S. glauca and S. salsa, but low alkali (A1) treatment promoted this ratio. The promotion in S. glauca by low alkali (A1) treatment was higher than that in S. salsa.

3.2. Plant growth The shoot fresh weight of S. glauca and S. salsa under drought treatments were decreased with increasing stress intensity. In D1 treatment, the fresh weight of S. glauca and S. salsa shoots decreased by 58.2% and 27.0% (shown in Fig. 4a, b) respectively. D1 and D2 treatments inhibited the shoot fresh weight of both Suaedas but had no effect on shoot dry weight (shown in Fig. 5a, b). In D3 treatment, the water content of the S. glauca shoots decreased by 31.4%, while the S. salsa shoot water content decreased by 10.8% (shown in Fig. 6a, b). Furthermore, drought treatments inhibited the root growth of S. glauca, while D1 and D2 treatments promoted the root growth of S. salsa. The fresh weight of S. salsa roots increased by 32.9% with D1 treatment and by 26.3% with D2 treatment (shown in Fig. 4d). The shoot and root weights of both Suaedas increased at S1 and S2 treatments, while decreased at high saline (S3) treatment. Optimum plant weight was observed at 100 and 200 mM NaCl for S. glauca and S. salsa, respectively (Figs. 4 and 5). Water contents in both tested species Table 1 The concentration, osmotic potential, EC, and pH of treatment solutions. Stress

Degree

Label

Solute

Concentration (mM)

Osmotic potential (MPa)

EC (Ds/m)

pH

drought

low moderate high low moderate high low moderate high

D1 D2 D3 S1 S2 S3 A1 A2 A3

PEG-6000 PEG-6000 PEG-6000 NaCl NaCl NaCl Na2CO3 Na2CO3 Na2CO3

17.3 21.4 36.7 100.0 200.0 400.0 7.0 14.0 28.0

−0.83 −0.85 −0.98 −1.29 −1.45 −1.98 −0.62 −0.69 −0.85

0.66 0.60 0.52 11.27 20.60 38.12 1.11 1.13 1.28

6.23 6.23 6.22 6.22 6.21 6.21 10.26 10.71 11.09

salt

alkali

3

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(a)

40

A B

100

35

a 80

Soil moisture (%)

Vegetation coverage (%)

120

b

60 40

c

20

30

20 15

c

7

Ds /m

Dominance index

EC

0.6

0.0

bc cd

4 3

a

cd d

1

b S. glauca

ab

5

2

ab

0.2

(b)

6

a

0.8

0.4

b

5

(b) a

b

b

a

10

0 8

1.0

a

a

25

0 1.2

S. glauca S. salsa

(a)

0 14

S. salsa

12

Fig. 2. Vegetation coverage (%) (a) and dominance index (b) of S. glauca and S. salsa in quadrats A and B. Values represent means ± S.E. (n = 4). Values at each treatment group followed by different letters are significantly different according to the one-way ANOVA (P < 0.05).

pH

10

(c) a

b

ab

b

a

b

8 6 4

3.3. Cations distribution

2

As showed in Table 3, the shoot K+ contents of both Suaedas decreased under drought stresses. In the D3 treatment, the S. glauca shoot K+ content was reduced by 62.8% and that of S. salsa was reduced by 32.7% in comparison to the control plants respectively. Drought treatment significantly (P < 0.05) decreased the Ca2+ and Mg2+ contents in S. glauca shoots but had little effect on S. salsa shoots. The effect of salinity on S. glauca shoot cations contents was in consistent with that on S. salsa. With the increasing salt stress intensity, the shoot Na+ content increased sharply, the shoot K+, Ca2+, and Mg2+ contents decreased significantly (P < 0.05) in both S. glauca and S. salsa. Alkali treatment also promoted the shoot Na+ accumulation in Suaedas, but in A3 treatment, the shoot Na+ accumulation in S. glauca and S. salsa were both less than that in A2 treatment. In D1 and D2 treatments, increasing root K+ accumulation was observed in both S. glauca and S. salsa. D2 treatment promoted 43.3% root K+ content in S. glauca and 66.3% root K+ content in S. salsa (showed in Table 4). In the control, the root of Suaedas accumulated more Na+ than shoot, but an opposite tendency was observed under salt treatments. When exposed to NaCl solution, the increase of Na+ content in both S. glauca and S. salsa root was lower than that in shoot respectively. Salinity inhibited more root K+ accumulation in S. glauca than that in S. salsa. In S3 treatment, the root K+ content of S. salsa decreased by 6.53%, while it decreased by 42.40% for S. glauca (showed in Table 4). A2 and A3 treatments significantly (P < 0.05) promoted the root Ca2+ and Mg2+ accumulation in S. glauca, while the root Ca2+ and Mg2+ contents were unchanged in S. salsa under the same treatments.

0

May

July

September

Fig. 3. Various soil attributes, soil moisture (%) (a), soil electrical conductivity, EC (b), and soil pH (c) of samples A and B in the months of May, July and September. Values represent means ± S.E (n = 4). Values at each treatment group followed by different letters are significantly different according to the one-way ANOVA (P < 0.05).

increasing drought stress intensity, while shoot SO42− content in S. salsa were unchanged under drought treatments. Salt treatment and alkali treatment both promoted the Cl− accumulation and inhibited NO3− accumulation in S. glauca and S. salsa, The Cl− accumulation promotion effect of saline treatment was greatly larger that of alkaline. Salt treatments significantly inhibited the shoot SO42− content in S. glauca and had little effect on that in S. salsa. The change of shoot SO42− content in S. glauca was also different from that in S. salsa under alkali conditions. The NO3− content in Suaedas root decreased sharply under salt and alkali treatments in comparison to the control (shown in Table 6). Salt treatments had little effect on root SO42− content in both S. glauca and S. salsa, while alkali significantly (P < 0.05) inhibited the root SO42− accumulation in S. glauca, promoted root SO42− accumulation in S. salsa. The promotion effect of alkali treatment on HCO3− contents in S. glauca root was lower than in S. salsa root. The root HCO3− content in S. glauca increased 109.1% and that in S. salsa increased 148.0% under low alkali (A1) treatment. In the control group, the shoot Na+/K+ of S. glauca (0.05) was less than that of S. salsa (0.24) (shown in Fig. 8). With increasing salt and alkali stress intensities, the Na+/K+ ratios increased in both species. Furthermore, the change in K+/Na+ ratios in S. glauca was similar with that in S. salsa. Drought stress showed little effect on shoot Na+/K+ ratio in S. glauca but greatly increased the shoot Na+/K+ ratio in S. salsa.

3.4. Anions distribution Drought treatments inhibited the shoot NO3− accumulation in both Suaedas, the shoot NO3− content decreased 66.2% in S. glauca and 43.7% in S. salsa in comparison to control plants (shown in Table 5). The shoot SO42− content in S. glauca decreased significantly with 4

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Fig. 4. Effects of drought, salt, and alkali treatments on the fresh weight (mg plant−1) of S. glauca and S. salsa. (a) S. glauca shoot; (b) S. salsa shoot; (c) S. glauca root; (d) S. salsa root. Values represent means ± S.E (n = 4). Values at each treatment group followed by different letters are significantly different according to the one-way ANOVA (P < 0.05).

Na+ vacuole compartmentation, which helps enhance the cellular water absorption capacity and alleviates Na+ injury in the leaves (Wang et al., 2001; Ma et al., 2004). From this research, we suggested that S. glauca and S. salsa shared the similar response traits to salinity which means the salt-tolerance strategies, like Na+ vacuole compartmentation also occurred in S. glauca. As salt-accumulating plants, Suaedas have been reported to accumulate substantial amounts of Na+ in their shoots with a weak K+ selectivity over Na+ (Reimann and Breckle, 1993; Wang et al., 2002). In our study, the Na+ content in Suaedas root was larger than that in shoot without stress treatment, but if exposed to NaCl treatment, more Na+ accumulation in Suaedas shoot was observed than root clearly. Moreover, shoot K+, Ca2+, and Mg2+ deficiencies occurred simultaneously because of the Na+ influx, even in

4. Discussion For most halophytes (Flowers and Colmer, 2008; Rozentsvet et al., 2017), low salinity treatment promotes plant growth, but if the NaCl level reaches 200 mM, more than 90% of the plant called halophytes will die (Flowers and Colmer, 2015). In this study, S. glauca and S. salsa survived up to 400 mM NaCl, and there was no significant difference between their biomass and that of the control plants. Moreover, S. salsa and S. glauca optimum growth at 200 mM and 100 mM NaCl respectively. It suggested that the salt tolerant of Suaedas was extremely broad and S. salsa was more adapted to the salinity condition than S. glauca. Numbers of researches reported that a series of salt tolerance genes in S. salsa, such as SsNHX1 and V-H+-ATPase, played an important role in

Fig. 5. Effects of drought, salt, and alkali treatments on the dry weight (mg plant−1) of S. glauca and S. salsa. (a) S. glauca shoot; (b) S. salsa shoot; (c) S. glauca root; (d) S. salsa root. Values represent means ± S.E (n = 4). Values at each treatment group followed by different letters are significantly different according to the one-way ANOVA (P < 0.05).

5

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Fig. 6. Effects of drought, salt, and alkali treatments on the water content (%) of S. glauca and S. salsa. (a) S. glauca shoot; (b) S. salsa shoot; (c) S. glauca root; (d) S. salsa root. Values represent means ± S.E (n = 4). Values at each treatment group followed by different letters are significantly different according to the oneway ANOVA (P < 0.05).

0.30 0.24

Root /shoot ratio

that S. glauca was less drought resistant than S. salsa. On the one hand, the resistant plant usually devoted more biomass on root growth for facilitating the soil water absorbing in arid regions. The drought resistance diversity in S. glauca and S. salsa partly result from the different root adaptability and growth mechanism. This result was accordance with the research on two cultivars of wheat under drought stress (Duan, 2017). On the other hand, Ca2+ and Mg2+ are important for the normal plant metabolize regulations, and the apparent Ca2+ and Mg2+ stability in S. salsa shoot under drought stress was administered to its strong drought tolerance. However, the habitat investigation result was in contrast to the laboratory test. The filed suryey showed that S. glauca established in soils with less moisture than S. salsa, suggesting the higher drought tolerant in S. glauca. It was reported that waterlogging was destructive for the germination of S. glauca (Duan et al., 2018), which may be related to the limited soil moisture for the S. glauca population habitat. Above all, the assessment of S. glauca drought tolerance is complex and perplexing, further studies are needed for the discrepancies in drought resistance between S. glauca and S. salsa. According to Gulnar et al. (2014) and Jianaer et al. (2007), alkaline stress on halophytes is more destructive than salt and drought stress (Gulnar et al., 2014; Jianaer et al., 2007). The deleterious effects of alkaline stress include osmotic stress, ion toxicity and high-pH stress, and the latter is usually fatal to plant growth (Yang et al., 2008a,b; Guo et al., 2009). In our study, alkali stress was injurious to the shoot growth of both Suaedas, and when the pH up to 11.0, the root growth was significantly inhibited by alkali treatment. This root injury was obviously greater than drought and salt treatments; however, low alkali treatment promoted the root growth of Suaeda plants. In the present study, it was hard to determine whether this promotion effect of Na2CO3 was due to an osmotic stimulation effect as mentioned before or the regulation effect of Na+. Regardless, the promotion of Na2CO3 in S. glauca was greater than that in S. salsa, indicating that S. glauca was more adaptable to alkali conditions than S. salsa. We also observed the Ca2+ and Mg2+ contents increasing in S. glauca roots at 7 and 14 mM Na2CO3, while there was little effect on S. salsa under the same treatments. These results suggested that the inherent difference in alkaline tolerance between S. glauca and S. salsa mainly relies on their root physiological traits. The laboratory test and habitat investigation both implied that S. glauca seedlings were more alkali tolerant than S. salsa.

S. glauca S. salsa

drought

salt

alkali

0.18 0.12 0.06

gh e hi rat e od m w lo

gh e hi rat e od m w lo

K C

gh e hi rat e od m w lo

0.00

Fig. 7. Effects of drought, salt, and alkali treatments on the root/shoot ratio of S. glauca and S. salsa. Values represent means ± S.E (n = 4).

low and moderate salinity. It was notable that less K+, Ca2+, and Mg2+ deficiency in Suaedas root than in shoot under salt stresses. The inferior salt resistant of S. glauca as compared to S. salsa may resulted from the poorer root K+ maintenance ability under high salinity which indicated the potential root physiology mechanisms related to ion selective absorption. This contrasting salt adaptability partly explained why S. salsa distributed in the soil with higher soil salinity than S. glauca. The injurious effects of drought stress are mainly mediated via water potential stress mechanisms (Chen et al., 2011). In the PEG treatment with an osmotic potential of −0.98 MPa, the shoot fresh biomass of both S. glauca and S. salsa reduced more than 50% as compared with the control, while no significant difference was observed in the salt treatment at −1.98 MPa. Without the regulation of sodium ions, drought stress showed a relatively stronger inhibition effect on Suaeda plants than salinity. Form the Figs. 4 to 6, we found that drought treatment arrested Suaedas plant growth, mainly owing to the restriction of shoot water uptake and the moisture loss in S. glauca was greater than in S. salsa at the same stress intensity. Our study revealed 6

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Table 3 Cations contents (mmol g−1 DW) in the shoots of S. glauca and S. salsa. Shoot Na+

Treatment

Shoot K+

S. glauca

S. salsa

CK D1 D2 D3

0.13 0.18 0.12 0.11

± ± ± ±

0.01b 0.01a 0.01b 0.02b

0.46 0.49 0.67 0.68

± ± ± ±

CK S1 S2 S3

0.13 5.29 6.16 8.76

± ± ± ±

0.01c 0.11b 0.63b 0.51a

0.46 4.81 5.35 8.22

CK A1 A2 A3

0.13 3.36 4.53 2.73

± ± ± ±

0.01c 0.41b 0.30a 0.13b

0.46 2.44 3.25 2.47

Shoot Ca2+

S. glauca

S. salsa

0.02b 0.07ab 0.07a 0.13a

2.34 1.72 1.31 0.87

± ± ± ±

0.05a 0.07b 0.15c 0.08d

1.90 1.56 1.56 1.28

± ± ± ±

± ± ± ±

0.02c 0.20b 0.22b 1.09a

2.34 0.55 0.41 0.41

± ± ± ±

0.05a 0.05b 0.01c 0.06c

1.90 0.64 0.34 0.43

± ± ± ±

0.02c 0.18b 0.28a 0.36b

2.34 0.96 0.92 0.31

± ± ± ±

0.05a 0.10b 0.14b 0.03c

1.90 0.77 0.54 0.27

Shoot Mg2+

S. glauca

S. salsa

S. glauca

S. salsa

0.13a 0.17ab 0.09ab 0.13b

0.41 0.25 0.20 0.14

± ± ± ±

0.01a 0.01b 0.02c 0.01d

0.52 0.39 0.41 0.35

± ± ± ±

0.02a 0.05a 0.02a 0.04a

0.43 0.30 0.24 0.17

± ± ± ±

0.04a 0.02b 0.01b 0.02c

0.60 0.52 0.58 0.47

± ± ± ±

0.02a 0.10a 0.01a 0.06a

± ± ± ±

0.13a 0.00b 0.09c 0.04bc

0.41 0.13 0.11 0.14

± ± ± ±

0.01a 0.01b 0.05b 0.03b

0.52 0.15 0.10 0.17

± ± ± ±

0.02a 0.00bc 0.04c 0.02b

0.43 0.07 0.06 0.14

± ± ± ±

0.04a 0.02b 0.01b 0.06b

0.60 0.13 0.10 0.15

± ± ± ±

0.02a 0.00b 0.04b 0.03b

± ± ± ±

0.13a 0.06b 0.02bc 0.04c

0.41 0.21 0.17 0.08

± ± ± ±

0.01a 0.01b 0.01c 0.01d

0.52 0.28 0.21 0.13

± ± ± ±

0.02a 0.03b 0.01bc 0.01c

0.43 0.06 0.08 0.04

± ± ± ±

0.04a 0.01b 0.01b 0.01b

0.60 0.20 0.17 0.11

± ± ± ±

0.02a 0.01b 0.02bc 0.01c

Values represent means ± S.E (n = 4). Values at each treatment group followed by different letters are significantly different according to the one-way ANOVA (P < 0.05). Table 4 Cations contents (mmol g−1 DW) in the roots of S. glauca and S. salsa. Treatment

Root Na+

Root K+

S. glauca

S. salsa

CK D1 D2 D3

0.25 0.37 0.37 0.33

± ± ± ±

0.04b 0.06a 0.01a 0.01ab

0.70 0.94 1.15 0.67

± ± ± ±

CK S1 S2 S3

0.25 2.02 3.13 3.62

± ± ± ±

0.04d 0.17c 0.24b 0.45a

0.70 1.92 2.40 3.09

CK A1 A2 A3

0.25 1.38 1.71 1.63

± ± ± ±

0.04c 0.09b 0.22a 0.02ab

0.70 1.92 2.40 3.09

Root Ca2+

S. glauca

S. salsa

0.11a 0.16a 0.13a 0.14a

2.45 2.98 3.51 2.94

± ± ± ±

0.18b 0.16ab 0.10a 0.10ab

1.99 2.83 3.31 1.96

± ± ± ±

± ± ± ±

0.11c 0.19b 0.17b 0.10a

2.45 2.42 2.20 1.41

± ± ± ±

0.28a 0.22a 0.17a 0.08b

1.99 2.14 2.02 1.86

± ± ± ±

0.11c 0.19b 0.17b 0.10a

2.45 1.24 0.91 0.46

± ± ± ±

0.28a 0.10b 0.12b 0.05c

1.99 1.15 0.84 0.53

Root Mg2+

S. glauca

S. salsa

S. glauca

S. salsa

0.18b 0.20ab 0.11a 0.18b

0.08 0.12 0.15 0.12

± ± ± ±

0.02b 0.02ab 0.02a 0.01ab

0.10 0.13 0.11 0.06

± ± ± ±

0.03a 0.04a 0.02a 0.02a

0.13 0.18 0.17 0.17

± ± ± ±

0.02a 0.02a 0.04a 0.02a

0.37 0.50 0.72 0.37

± ± ± ±

0.01b 0.13ab 0.06a 0.11b

± ± ± ±

0.28a 0.08a 0.04a 0.23a

0.08 0.07 0.08 0.11

± ± ± ±

0.02ab 0.00b 0.01b 0.01a

0.10 0.04 0.06 0.03

± ± ± ±

0.03a 0.00ab 0.00b 0.01b

0.13 0.10 0.11 0.22

± ± ± ±

0.02b 0.03b 0.03b 0.05a

0.37 0.27 0.29 0.38

± ± ± ±

0.01a 0.01b 0.01b 0.01a

± ± ± ±

0.28a 0.05b 0.12b 0.11b

0.08 0.24 0.23 0.12

± ± ± ±

0.02b 0.02a 0.04a 0.02b

0.10 0.13 0.11 0.05

± ± ± ±

0.03a 0.01a 0.03a 0.00a

0.13 0.32 0.42 0.29

± ± ± ±

0.02b 0.04a 0.09a 0.05a

0.37 0.41 0.47 0.46

± ± ± ±

0.01a 0.02a 0.17a 0.09a

Values represent means ± S.E (n = 4). Values at each treatment group followed by different letters are significantly different according to the one-way ANOVA (P < 0.05). Table 5 Anions contents (mmol g−1 DW) in the shoots of S. glauca and S. salsa. Treatment

Shoot Cl−

Shoot NO3−

Shoot SO42−

Shoot HCO3−

S. glauca

S. salsa

S. glauca

S. salsa

S. glauca

S. salsa

S. glauca

S. salsa

CK D1 D2

0.18 ± 0.01ab 0.22 ± 0.01a 0.19 ± 0.02ab

0.54 ± 0.02b 0.64 ± 0.09ab 0.78 ± 0.07a

0.12 ± 0.02a 0.09 ± 0.01b 0.07 ± 0.01b

0.11 ± 0.00a 0.14 ± 0.02a 0.13 ± 0.01a

3.31 ± 0.03a 2.23 ± 0.10b 1.70 ± 0.18c

2.52 ± 0.02a 1.77 ± 0.23b 1.70 ± 0.12ab

0.04 ± 0.01ab 0.05 ± 0.01a 0.03 ± 0.01b

0.16 ± 0.02a 0.11 ± 0.01b 0.11 ± 0.02b

D3 CK S1 S2 S3

0.17 0.18 4.18 4.99 8.81

± ± ± ± ±

0.02b 0.01c 0.23b 0.74b 0.83a

0.80 0.54 3.43 3.81 7.72

± ± ± ± ±

0.12a 0.02c 0.16bc 0.55b 0.71a

0.04 0.12 0.04 0.05 0.04

± ± ± ± ±

0.00c 0.02a 0.01b 0.03b 0.01b

0.12 0.11 0.14 0.11 0.10

± ± ± ± ±

0.03a 0.00a 0.01a 0.02a 0.00a

1.12 3.31 1.60 1.46 0.60

± ± ± ± ±

0.06d 0.03a 0.15b 0.06b 0.02c

1.42 2.52 1.24 0.78 0.55

± ± ± ± ±

0.14ab 0.02a 0.04b 0.25bc 0.10c

0.03 ± 0.01b 0.04 ± .001b 0.10 ± 0.01a 0.08 ± 0.02ab 0.09 ± 0.01ab

0.11 0.16 0.10 0.16 0.10

± ± ± ± ±

0.02b 0.02a 0.02a 0.05a 0.03a

CK A1 A2 A3

0.18 0.42 0.83 0.59

± ± ± ±

0.01c 0.05b 0.12a 0.04b

0.54 0.57 0.71 0.75

± ± ± ±

0.02b 0.05b 0.10ab 0.09a

0.12 0.14 0.08 0.03

± ± ± ±

0.02ab 0.03a 0.01b 0.00c

0.11 0.32 0.43 0.29

± ± ± ±

0.00c 0.02ab 0.05a 0.01b

3.31 2.46 2.07 0.56

± ± ± ±

0.03a 0.21b 0.24b 0.07c

2.52 1.74 1.52 0.57

± ± ± ±

0.02a 0.10b 0.08b 0.07c

0.04 0.46 0.53 0.60

0.16 0.37 0.62 1.41

± ± ± ±

0.02c 0.04bc 0.07b 0.04a

± ± ± ±

0.01b 0.05ab 0.05a 0.06a

Values represent means ± S.E (n = 4). Values at each treatment group followed by different letters are significantly different according to the one-way ANOVA (P < 0.05).

5. Conclusion

suggested that S. salsa is a good candidate for ecological revegetation in highly saline soils and that S. glauca is more adapted to alkaline land.

In summary, this study showed that S. salsa had a stronger tolerance to salt and drought stress than S. glauca, but its tolerance to alkaline was less than that of S. glauca, mainly due to their roots variable responses, especially the potential cations regulation. This contrasting adaptability

Declaration of Competing Interest The authors declare that they have no known competing financial 7

Ecological Engineering 140 (2019) 105593

J. Li, et al.

Table 6 Anions contents (mmol g−1 DW) in the roots of S. glauca and S. salsa. Treatment

Root Cl−

Root NO3−

Root SO42−

S. glauca

S. salsa

S. glauca

S. salsa

CK D1 D2 D3

0.23 0.38 0.44 0.44

± ± ± ±

0.03b 0.05a 0.01a 0.03a

0.74 1.43 1.62 1.01

± ± ± ±

0.15b 0.07a 0.13a 0.14ab

0.11 0.13 0.19 0.29

± ± ± ±

0.01c 0.01c 0.01b 0.01a

0.13 0.42 0.47 0.28

± ± ± ±

CK S1 S2 S3

0.23 2.37 3.39 4.33

± ± ± ±

0.03d 0.25c 0.19b 0.42a

0.74 2.88 3.38 4.31

± ± ± ±

0.15c 0.01b 0.14b 0.16a

0.11 0.11 0.08 0.13

± ± ± ±

0.01a 0.05a 0.01a 0.04a

0.13 0.16 0.12 0.09

CK A1 A2 A3

0.23 0.35 0.60 0.61

± ± ± ±

0.03c 0.04b 0.04a 0.05a

0.74 0.69 1.04 1.32

± ± ± ±

0.15ab 0.07b 0.13ab 0.09a

0.11 0.07 0.07 0.06

± ± ± ±

0.01a 0.00b 0.02b 0.01b

0.13 0.50 0.49 0.36

Root HCO3−

S. glauca

S. salsa

S. glauca

S. salsa

0.02b 0.04a 0.05a 0.06ab

1.26 1.57 1.76 1.63

± ± ± ±

0.01c 0.09b 0.15a 0.09ab

1.29 1.57 1.66 1.16

± ± ± ±

0.28a 0.02a 0.03a 0.07a

0.22 0.37 0.26 0.29

± ± ± ±

0.02b 0.04a 0.04ab 0.03ab

0.22 0.89 0.83 0.45

± ± ± ±

0.02c 0.04a 0.06a 0.03b

± ± ± ±

0.02a 0.08a 0.04a 0.02a

1.26 0.95 1.13 0.36

± ± ± ±

0.10a 0.05b 0.15a 0.04c

1.29 0.72 0.52 0.25

± ± ± ±

0.28a 0.07ab 0.06b 0.10b

0.22 0.28 0.26 0.60

± ± ± ±

0.02b 0.03b 0.02b 0.04a

0.25 0.61 0.48 0.92

± ± ± ±

0.04c 0.08ab 0.05b 0.05a

± ± ± ±

0.02b 0.07a 0.06a 0.07ab

1.26 0.89 0.56 0.17

± ± ± ±

0.10a 0.08b 0.04c 0.04d

1.29 0.50 0.49 0.36

± ± ± ±

0.28a 0.07a 0.06a 0.07ab

0.22 0.46 0.45 0.48

± ± ± ±

0.02b 0.05a 0.06a 0.05a

0.25 0.62 0.85 1.26

± ± ± ±

0.02c 0.07b 0.06ab 0.08a

Values represent means ± S.E (n = 4). Values at each treatment group followed by different letters are significantly different according to the one-way ANOVA (P < 0.05).

24.0

salt

23.0

Shoot Na+/ K+

22.0

alkali

drought

21.0

gh e hi rat e od m w lo

gh e hi rat e od m w lo

K C

gh e hi rat e od m w lo

16.0 12.0 8.0 4.0 0.8 0.6 0.4 0.2 0.0

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Fig. 8. Effects of drought, salt, and alkali treatments on the shoot Na+/K+ ratio of S. glauca and S. salsa. Values represent means ± S.E (n = 4).

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