Seed Germination of the Halophyte Anabasis Setifera (Amaranthaceae) from Saudi Arabia

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Seed germination of the halophyte Anabasis setifera (Amaranthaceae) from Saudi Arabia.

Journal: Botany

Manuscript ID cjb-2018-0053.R1

Manuscript Type: Article

Date Submitted by the Author: 19-May-2018

Complete List of Authors: Basahi, Mohammed; Shaqra University College of Science and Arts Sajir, biology; Anabasis setifera,Draft halophyte, Temperature, Germination, seed germination Keyword: recovery

Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? :

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Seed germination of the halophyte Anabasis setifera (Amaranthaceae) from

Saudi Arabia.

Mohammed A Basahi

College of Science and Arts Sajir

Shaqra University

P.O. Box 33, Shaqra 11961

Saudi Arabia

[email protected] Draft00966582223689

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Abstract

The main objective of this study was to determine the effects of temperature, light/darkness, and salinity (NaCl) on seed germination of Anabasis setifera Moq. and the effects of alleviating salinity stress using distilled water. One-hundred percent of seeds completed germination at 15/5,

20/10, and 20°C, and a higher percentage of seeds completed germinationin light than in the dark at 20/10 and 25/15°C. The percentage of seeds that completed the germination decreased as salinity increased from 0 to 700 mM NaCl. Seeds that did not complete germination in the 800 or

700 mM NaCl solutions completed its germinationDraft after being transferred to distilled water, with a recovery rate of 94.5% and 75.5%, respectively, at 25/15°C. The inhibitory effect of NaCl on the completion of germination in this species probably occurs via an osmotic effect.

Key Words: Anabasis setifera, halophyte, temperature, germination, seed germination recovery

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Introduction

Germination and establishment are essential in the life cycle of halophytes (Ungar 1978).

Different species of halophytes, such as Haloxylon recurvum Bunge ex Boiss, Atriplex

triangularis Willd., Salicornia europaea L., Salicornia bigelovii Torr., Salicornia stricta

Durmort., Salicornia rubra Nelson, Zygophyllum simplex L., Triglochin maritima L., Salicornia

pacifica Standley, Arthrocnemum indicum Willd., and Diplachne fusca L. germinate in response

to different stimuli (Langlois 1966; Ungar 1967; Rivers and Weber 1971; Chapman 1974; Khan

and Ungar 1984, 1996b, 1999; PhilipupillaiDraft and Ungar 1984; Khan and Weber 1986; Myers and

Morgan 1989; Khan and Gul 1998; Khan et al. 2000). These stimuli include environmental

variables, such as salinity and temperature. For example, El-Keblawy et al. (2016a) investigated

how temperature affected germination of Anabasis setifera Moq. seeds that were collected from

the United Arab Emirates (UAE) and Egypt.

Halophytes germinate in saline environments during the rainy season when the salinity of the

surface soil layers decreases (Chapman 1960; Waisel and Ovadia 1972; Ungar 1978, 1982,

1987b; Ismail 1990). However, most plants, including halophytes, have a higher germination rate

in distilled water, and this decreases as salinity increases (Rozema 1975; Ungar 1978; El-

Sharkawi and Springuel 1979; Woodell 1985). El-Sharkawi and Springuethel (1979) found that

the final percentage of germination in many species is affected by salinity at varying

temperatures. Many environmental factors control halophyte germination in nature, including

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light, temperature, and salinity (Badger and Ungar 1989; Gutterman 1993; Ungar 1995; Huang

and Gutterman 1998; Khan 2003). Ungar (1982) showed that salinity and temperature were the

most important factors, since they determine the time taken for halophyte seeds to complete

germination. Badger and Ungar (1988) stated that for plants to successfully establish in a saline

environment, the duration of germination is essential. Additionally, seedlings are more

vulnerable to physical environmental changes than other life cycle stages. Therefore, the most

important factor for halophytes to successfully establish in inland saline habitats is the timing of

germination. Ungar (1987a) argued that seasonal variation in soil salinity may result in the

extinction of entire plant populations.

The halophyte Anabasis setifera (Amaranthaceae)Draft is broadly distributed within the coastal saline

environments of Saudi Arabia, Afghanistan, Iran, India, and Pakistan. The species is often found

alongside other halophytes, such as Suaeda vermiculata Forssk., Prosopis farcta (Banks & Sol.)

J. F. Macbr., Suaeda aegyptiaca (Hasselq.) Zohary, and Atriplex leucoclada Boiss. (Mandaville

1990; Migahid 1996; AL-Turki 1997; Collenette 1998, 1999; Chaudary 1999). El-Keblawy et al.

(2016a) reported that many germination studies have been conducted on Anabasis setifera seeds

that originate from the UAE and Egypt, but none of them have used seeds from Saudi Arabia,

where conditions are different.

This study examined how A. setifera seeds from the saline marshes of Tarut Island on the Gulf

coast of Saudi Arabia, respond to completion of seeds germination. We investigated seed

germination responses to: (a) a broad range of constant and variable temperatures at a

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photoperiod of 12 hours daily; (b) uninterrupted light (20/10 °C) or constant dark (25/15 °C); and

Materials and methods

Collection of seeds

A. setifera seeds were collected from Tarut Island (26°34'18.58" N, 50°03'40.57" E) on 22

December, 2015 (Figure 1). The seeds were air-dried, cleaned, and used immediately in

germination assays.

Effects of light/dark and temperature on germination

Tests of seed germination were carriedDraft out using 9-cm Petri dishes containing two filter paper

layers (Whatman no. 1) moistened with about 10 ml of distilled water. Five replicate Petri dishes

with 20 seeds each were used for each treatment. The Petri dishes were distributed randomly in

temperature-controlled incubators, and their positions were changed daily. The first emergence

of the radicle from the seed was defined as germination (Côme 1982; Redondo et al. 2004).

Observations were made daily for about 1 month and newly germinated seeds were removed

from the Petri dishes. Seeds were incubated at one of five variable temperature regimes (35/25,

30/20, 25/15, 20/10 and 15/5 °C), or four constant temperatures (40, 30, 20, and 10 °C) and a

daily photoperiod of 12 h light: 12 h dark. The variable temperature regimes simulated the likely

diurnal changes in temperatures in the natural habitat. The final percentage of germinated seeds

was calculated as: (1) G (%) = (A/B) × 100 where, A represents the total number of germinated

seeds in 30 days, and B represents the total number of seeds tested (100 seeds) (Li and Shi 2010;

Wang et al. 2013).

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The rate of germination (50% = t50) was calculated as:(2) GSI = G1/N1 + G2/N2 + ... Gn/Nn

where, G1/G2/Gn represent the number of seeds that germinated, and N1/N2/Nn represent the

duration of the experiment (Maguire 1962).

To test the effects of light/dark on germination, seeds were incubated under continuous light or

dark at 20/10 and 25/15°C, respectively. Germination of seeds incubated in the light was

monitored daily, while those incubated in the dark were observed after 15 days (Qu et al. 2008).

Effects of salinity on seed germination and germination recovery

A total of nine salinity treatments were used: 0, 100, 200, 300, 400, 500, 600, 700, and 800 mM

of NaCl. Seeds were germinated in 9-cmDraft Petri dishes with two layers of Whatman No. 1 filter papers, then incubated at 12:12 h light:dark at temperatures of 25:15 °C for about 1 month. Each

treatment had five replicates with 20 seeds each. The Petri dishes were watered with 7 ml of their

respective salinity solutions, and sealed using Nescofilm to prevent evaporation. The solutions

were replaced every 7 days. Germinated seeds were counted daily for a period of 30 days and

seedlings were removed from the petri dishes. Seeds that failed to germinate within the 30-day period were transferred into distilled water and given an additional incubation period of 15 days

in 12:12 h light :dark at temperatures of 25/15 °C . After the 15-day period of recovery, the non-

germinated seeds were tested for viability using 2,3,5-triphenyl tetrazolium chloride (TTC)

solution, as recommended by the International Seed Testing Association (1999). The seeds were

soaked in a solution of 1% TTC for 4 days in a glass vial in the dark at a temperature of 25 °C.

The dehydrogenase enzymes in the living tissue reduces the colourless solution of tetrazolium

chloride to insoluble red formazan, making the living cells appear red, while dead cells remain

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colourless. Germination recovery (%), which is the ability of the un-germinated seeds to

germinate after being transferred from the saline solution to the distilled water was calculated as:

Recovery percentage (%) = [ (a – b)/ (c – b)] × 100

where, a represents the number of germinated seeds within the saline solution and those that

germinated after recovery in distilled water, b represents the number of germinated seeds in the

saline solutions, and c represents the total number of seeds tested in the experiment (Khan and

Ungar 1984).

Statistical analysis

The percentages of seeds that germinated are represented as mean ± SE. Data for germination

and germination recovery percentage Draft were arcsine transformed prior to statistical analysis to

ensure homogeneity of variance. One-way analysis of variance (ANOVA) was used to determine

significant differences between the treatments of temperature, light/dark, and saline solutions.

Results

Effects of temperatures and light/dark on germination

After the 30-day incubation period, the percentages of germination were the highest at the lowest

temperatures, however, they were lower at higher tempertures. For instance, the percentage of

germination was 100%, 85%, and 78% at temperatures of 15/5 °C, 20/10 °C, and 35/25 °C,

respectively (Figures 2 and 3). There was a significant variation (P<0.0001) in the percentage of

germination at different temperatures. The completion of germination in the dark at temperatures

of 25/12 °C and 20/10 °C was significantly lower than that in the light (P<0.0001) (Figure 6).

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Effects of salinity on seed germination and germination recovery

Salinities of 0 and 100 mM NaCl showed no effects on seeds completed germination (Figure 4).

However, the percentages of germination at 200, 300, 400, 500, 600, and 700 mM of NaCl were

significantly lower (P<0.001) than those at 0 and 100 mM of NaCl. There were no seeds

completed germination at a salinity of 800 mM NaCl. The germination rate (tg50) of seeds in

solutions between 0 and 700 mM of NaCl decreased with increasing salinity (Figure 4). Some A. setifera seeds that did not complete germination in the NaCl treatments completed germination

once they were transferred to distilled water, as shown in Figure 5.

DraftDiscussion

Impact of light and temperature on germination

Seeds of A. setifera germinated better at lower temperatures than at higher temperatures. This

was most likely because the main habitat of this species is cool and wet areas that receive plenty

of rain. Therefore, seeds complete germination mainly during the winter season. Anabasis setifera seeds also germinated at a higher rate at varying temperatures than at constant

temperature, although we observed 100% germination at 20 °C. Ignaciuk and Lee (1980) also

observed that different strains of this species exhibited higher percentages of germination at

varying temperatures than at constant temperature. The species included Cakile maritime Scop.,

Atriplex glabriuscula Edmondston, and Anabasis laciniata. Moreover, Al-Turki (1992) observed a higher germination percentage at varying temperatures than at constant temperatures for

Suaeda aegyptiaca seeds collected from Tarut Island.

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El-Keblawy (2016a) reported that A. setifera seeds collected from the UAE and Egypt completed

germination at different temperatures, with up to 46% and 67% of seeds germinating at 25/15 °C,

respectively, and 39% and 83% germinating at 30/20 °C, respectively. However, the current

study indicated that the germination percentage of A. setifera seeds collected from the coast of

the Arabian Gulf was higher than that of seeds from the UAE and Egypt at temperatures of 25/15

and 30/20 °C. Moreover, high temperatures restricted the germination of seeds collected from

Saudi Arabia (75% at 40 °C and 85% at 35/25 °C). Seeds from the UAE and Egypt were also

inhibited by high temperatures, with only 43% and 49% germinating at 35/25 °C, respectively

(El-Keblawy et al. 2016a). The t50 for germination in A. setifera seeds from Saud Arabia was

very fast at 25/15, 30/20 and 35/25, 30 and 40°C (1 day). However, the delay in t50 for

germination at 15/5 and 20/10°C and 10Draft and 20°C was about 2-3 days in comparison with other

temperatures. This result (50% Germination) is in complete agreement with that for A. setifera

collected from Egypt and UAE (El-Keblawy et al. 2016a). This study showed that the percentage

of germination of A. setifera seeds in their natural habitat is probably slow during the winter

season, but this percentage increases as temperature increases. This was presumably because the

number of seeds germinating in the soil decreases during the growing season. To understand the

full germination capabilities of this species, more studies should be conducted in situ.

The germination percentage of A. setifera seeds also increased at higher light intensities. These

results were similar to those of desert plant species, such as Artemisia monosperma Delile

(Asteraceae), A. sphaerocephala, and A. ordosica (Huang and Gutterman 1998, 1999, 2000).

Several halophytic species, such as Halocnemum strobilaceum (Pall.) Bieb. and A. setifera

responded positively when subjected to increased light at varying temperatures (Qu et al. 2008;

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El-Keblawy et al. 2016a). This indicates that A. setifera seeds in their natural habitat can

successfully germinate if they are placed on or near the surface under suitable environmental

conditions. Similar responses were observed by Baskin and Baskin (1998) for seeds that thrive in

saline and desert environments. Field observations showed that A. setifera produced flowers

from early October to the end of November, and produced seeds at the beginning of December.

Therefore, it is possible that the germination of A. setifera takes place in winter, which is

characterized by low temperatures and high rainfall (See Fig. 2,3).

Impact of salinity on germination and germination recovery

Many studies have established the effects of salinity on seed germination in halophytic plants

(Waisel 1958; Ungar 1962; Ungar andDraft Capilupo 1969; Williams and Ungar 1972; Joshi and

Iyengar 1977; Sheikh and Mahmood 1986). In this study, the germination of Saudi Arabian A. setifera seeds decreased at higher concentrations of NaCl. At 700 mM NaCl, germination was

observed in only 10% and 0% of seeds. Results from several other halophytes, Aeluropus

massauensis (Fresen) Mattei, Atriplex griffithii Moq., Cressa cretica L., Suaeda aegyptiaca, S.

vermiculata, and S. monoica (Mahmoud 1984; Khan 1991; Al-Turki 1992; Khan and Rizvi

1994) were similar. Therefore, the ability of A. setifera seeds to tolerate salinity was higher than

that of Atriplex griffithii, S. fruticosa, Triglochin maritima, S. aegyptiaca, Zygophyllum simplex,

Haloxylon recurvum, S. vermiculata, and S. monoica (Al-Turki 1992; Khan and Rizvi 1994;

Khan and Ungar 1996a, 1998, 2001). However, the ability of A. setifera seeds to tolerate salinity

was lower than that of other halophytes Cressa cretica, Salicornia bigelovii, Salicornia pacifica,

Tamarix pentandra Pall., Salicornia rubra, and Arthrocnemum indicum (Ungar 1967; Rivers and

Weber 1971; Khan and Weber 1986; Khan 1991; Khan and Gul 1998; Khan et al. 2000).

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Germination of seeds from these species originating from the UAE, Egypt, and Saudi Arabia

declined as the level of salinity increased. However, seeds from Saudi Arabia germinated at a

higher salinity (9.5% at 700mM NaCl) than those from Egypt and United Arab Emirates (at 600

mM NaCl) (El-Keblawy et al. 2016b). This implies that Saudi Arabian seeds are more tolerant to

salinity than those from the UAE and Egypt.

High levels of salt cause stress to plants, as it disrupts homeostasis in ion supply and the water

potential in plant cells (Yeo 1983). This suggests that germination of A. setifera might have been

inhibited via osmosis. Previous studies showed the extent to which NaCl affected the

germination of Suaeda depressa (Pursh) Watson, S. vermiculata, S. monoica, and S. aegyptiaca

seeds collected from Saudi Arabian countriesDraft (Ungar and Capilupo 1969; Williams and Ungar

1972; AL-Turki 1992). Ignaciuk and Lee (1980) established that NaCl inhibited germination of

seeds via osmosis in Atriplex sp., and via ion exchange in Salsola kali (Dumort.) Guterm. and

Cakile maritime. Therefore, multiple studies have concluded that NaCl inhibits germination of

halophytes via osmosis (Ungar 1962; Mooring et al. 1971; Mahamoud et al. 1983b; Smith 1985;

Woodell 1985). Other studies have demonstrated that many halophyte seeds exposed to a saline

environment can still germinate after immersion in distilled water (Baskin and Baskin 1998). Gul

and Weber (1999) showed that Allenrolfea occidentalis (S. Wats.) Kuntze seeds rapidly

recovered from the effects of salinity after being transferred into distilled water and subsequently

completed its germination. In Suaeda monoica (Al-birk population) seeds, the germination

recovery was 18% after soaking in 400 mM of NaCl solution. However, when seeds were soaked

in 600 mM of NaCl, germination increased to 43% (AL-Turki 1992). The current study shows

that seeds of A. setifera that failed to germinate in a highly saline environment recovered well

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when they were transferred to distilled water. Therefore, the germination of A. setifera seeds at

low salinity and the ability to recover from high salinity can explain their adaptability to saline

environments.

These results can be used to compare experimental and in situ contexts for these plants in their

natural environment, especially arid areas. In arid habitats, soil salinity is accelerated by the

evaporation of water during the summer season. This has the potential to cause salinity stress for

seeds and seedlings. During this period, the rate of seed germination is very low, and when they

germinate, their chances of growing to maturity are also very low. However, when the

germinated seeds exposed to heavy rainfall, the accumulated salts are leached out which might

increase the chance of growing. AccordingDraft to Uhvits (1946), saline environments restrict

germination mainly via the toxic effects of ions on the embryo. The increased osmotic ability of

the medium prevents uptake of water (Ayers 1952; Macke and Ungar 1971; Boorman 1968;

Mahmoued et al. 1983a).

Conclusions

The role of soil salinity in regulating the germination of A. setifera seeds enables it to adapt and thrive in the saline environments along the coastal regions of the Arabian Gulf. Moreover, germination of A. setifera seeds in a less saline habitat, or after recovering from a highly saline environment, might best be interpreted as an adaptive response to saline habitats. These results also showed that A. setifera seeds are more likely to germinate during the winter season, when temperatures are low and rainfall is high. Additionally, A. setifera seeds have a higher survival index in saline habitats than other halophytes.

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Acknowledgments

My sincere appreciation goes to Professor Carol Baskin at the University of Kentucky, for

reviewing and commenting on the manuscript, as well as helping to make the English better.

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Figure Legends

Figure 1. Map of locations samples

Figure 2. The effect of five alternating temperatures on seed germination of

Anabasis setifera (12h light/12h dark) Means at the same temperature that have the same letters are not significantly different P<0.05. Vertical bars indicate standard errors of means (mean ± SE) .

Draft

Figure 3. The effect of four constant temperatures on seed germination of Anabasis setifera (12h light/12h dark) Means at the same temperature that have the same letters are not significantly different P<0.05. Vertical bars indicate standard errors of means

(mean ± SE) .

Figure 4. The effect of salinity ( Nacl mM) on seed germination of Anabasis setifera at 25/15 oC (12h light/12h dark) Means with the same lowercase letter do not differ significantly at P<0.05. Vertical bars indicate standard errors of means (mean ± SE) .

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Figure 5. recovery after transferring seeds to distilled water (12h light/12h) dark

Means with the same lowercase letter do not differ significantly at P<0.05. Vertical

bars indicate standard errors of means (mean ± SE) .

Figure 6. Effect of continuous light and continuous dark on germination at two

temperature regimes. Means with the same lowercase letter do not differ significantly

P<0.05. Vertical bars indicate standard errors of means (mean ± SE) .

Draft

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Figure 2.

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Figure 3.

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Figure 5.

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Figure 6.

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