Upload
others
View
6
Download
0
Embed Size (px)
Citation preview
Draft
Adaptive drought tolerance during germination of Salsola drummondii seeds from saline and non-saline habitats of
the Arid Arabian Deserts
Journal: Botany
Manuscript ID cjb-2018-0174.R1
Manuscript Type: Article
Date Submitted by the Author: 07-Nov-2018
Complete List of Authors: Elnaggar, Attiat; Universidad de Málaga, Departmento de Biología VegetalEl-Keblawy, Ali; University of Sharjah , Applied BiologyMosa, Kareem; University of SharjahNavarro, Teresa; Malaga University
Keyword: Drought tolerance, Germination requirement, maternal salinity, polyethylene glycol, Seed dormancy
Is the invited manuscript for consideration in a Special
Issue? :Not applicable (regular submission)
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
1 ARESEARCH ARTICLE
2 Running title: Drought tolerance during germination in a habitat-indifferent halophyte
3 Adaptive drought tolerance during germination of Salsola drummondii seeds
4 from saline and non-saline habitats of the Arid Arabian Deserts
5
6 Attiat Elnaggar1,3,4, Ali El-Keblawy1, 2,*, Kareem A. Mosa1,5 and Teresa Navarro3
7 1Department of Applied Biology, Faculty of Science, University of Sharjah, PO Box 27272,
8 Sharjah, UAE
9 2Permanent address: Department of Biology, Faculty of Science, Al-Arish University, Egypt
10 3Departmento de Biología Vegetal, Universidad de Málaga, P. O. Box 59, 29080, Málaga, Spain
11 4Department of Botany and Microbiology, Faculty of Science, Alexandria University, Egypt.
12 5Department of Biotechnology, Faculty of Agriculture, Al-Azhar University, Cairo, Egypt
13 *Corresponding author Email: [email protected]; phone +971505432065
Page 1 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
14 Abstract
15 The effects of temperature, light, salinity, and drought on germination of halophytes have been
16 extensively studied. However, few studies have focused on the germination of plants that grow
17 well in both saline and non-saline habitats (i.e., habitat-indifferent halophytes). Here, we assess
18 the impacts of population origin, temperature, and light on drought tolerance, as simulated by
19 polyethylene glycol (PEG), during germination of Salsola drummondii, a habitat-indifferent
20 halophyte from the arid Arabian deserts. Seeds were collected from both saline and non-saline
21 habitats and germinated at six PEG levels at three temperatures and two light regimes. An
22 increase in PEG concentration resulted in a significant reduction in seed germination, especially
23 at higher temperatures. Seeds from the non-saline habitat attained significantly greater
24 germination efficiency at PEG levels up to -1.2 MPa, but there was no difference in germination
25 of seeds between the two habitats at -1.5 MPa PEG concentrations. Saline habitat seeds
26 germinated significantly faster at higher PEG levels. Germination was significantly higher in
27 dark than in light at -1.5 MPa at lower temperatures, but the opposite was true at higher
28 temperatures. Seeds from saline habitats had higher dormancy and faster germination at higher
29 concentrations of PEG due to adaptation to low osmotic potentials.
30 Keywords: Drought tolerance; Germination requirement; maternal salinity; polyethylene glycol;
31 seed dormancy
Page 2 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
32 Introduction
33 Water will become a scarce natural resource with the increasing aridity and growing world
34 population, and this scarcity is expected to be more severe in arid and hyper-arid regions (Evans
35 2009). Several scenarios of climate-change predict an increase in water deficit and aridity in
36 many regions of the world, which necessitates research on plant tolerance to drought stress (Petit
37 et al. 1999). Drought leads to reduction in soil water content, and consequently, is one of the
38 most pernicious environmental stress factors facing plants (Cosgrove and Rijsberman 2014).
39 Plants respond to drought stress through different mechanisms that involve molecular,
40 biochemical, physiological, and morphological changes (Levitt 1972; Turner 1986; Mosa et al.
41 2018). Of the many possible tolerance mechanisms, plants commonly contend with drought
42 through osmotic adjustment and by balancing the ratio of different osmolytes (Flowers and Yeo
43 1986; Nounjan et al. 2018).
44 Germination and recruitment of desert halophytes are affected by environmental factors,
45 such as soil salinity, availability of water, temperature, and light intensity (Baskin and Baskin
46 2014). Such effects of environmental factors are especially obvious in the salt marshes of arid
47 deserts, where evaporation is very high (Khan and Weber 2000; El-Keblawy 2004; El-Keblawy
48 and Bhatt 2015; El-Keblawy et al. 2015). The scarcity of rainfall, coupled with the tendency of
49 soil salinity to increase, makes drought a serious problem facing halophytes of the Arabian arid
50 deserts, where annual average precipitation is very low (e.g., around 100 mm in the United Arab
51 Emirates, UAE, Böer 1997). Under such conditions, seeds of halophytes postpone their
52 germination until arrival of suitable conditions for seedling survival, which usually happens
53 when effective rainfalls increase soil water potential and other conditions, including especially
54 temperature and light, become suitable as well (Khan and Weber 2000; El-Keblawy 2004, 2014).
Page 3 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
55 Several studies have assessed the impacts of these factors - individually or in combination - on
56 salinity tolerance by plants during germination, but few have evaluated the effect of these factors
57 on drought tolerance of halophytes.
58 Environmental maternal effect, which is determined by conditions experienced by
59 maternal plants during seed maturation, often plays a substantial role in controlling the
60 germinability of ripening seeds (Roach and Wulff 1987). It has been reported that maternal
61 habitat and time of seed development affect seed dormancy and germination requirements (Siles
62 et al. 2017; El-Keblawy et al. 2017a, b, 2018; Al-Shamsi et al. 2018). Adaptive maternal effect
63 enhances the progeny’s fitness in an environment similar to that experienced by the maternal
64 plants (Rossiter 1996; Soliman et al. 2018). Several studies have assessed the impact of multiple
65 environmental factors (e.g., temperature, rainfall, light quality, and day length) during seed
66 development and maturation during seed germination (see Roach and Wulff 1987; Fenner 1991;
67 Wulff 1995; Gutterman 2000). However, few studies have assessed the effect of maternal
68 salinity on dormancy and germination requirements of habitat-indifferent halophytes (e.g., El-
69 Keblawy et al. 2016, 2017a, 2018). In Anabasis setifera, seeds from the non-saline habitat have
70 been reported to have significantly higher germination levels than those from the saline habitat at
71 all salinity levels (El-Keblawy et al. 2016). In Suaeda aegyptiaca and S. vermiculata, seeds from
72 the non-saline habitat attained significantly higher germination as compared to those from saline
73 habitat, in lower and moderate salinities. At higher salinities, however, the germination of seeds
74 from the saline habitat was either similar or higher than that for seeds from the non-saline habitat
75 (El-Keblawy et al. 2017a, 2018).Taking into consideration that water deficit (drought) is usually
76 associated with salt stress, it is important to assess the effect of maternal salinity on drought
Page 4 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
77 tolerance and germination requirements during seed germination of habitat-indifferent
78 halophytes (Al-Shamsi et al. 2018).
79 Salsola drummondii Ulbr. (family Amaranthaceae) is a perennial, leaf succulent, habitat-
80 indifferent xerohalophyte. In the United Arab Emirates (UAE), this evergreen species grows
81 equally well in both saline and non-saline soils. The plants associated with S. drummondii in the
82 saline soils are true halophytes (i.e., growing only in saline habitats) and include species such as
83 Aeluropus lagopoides, Halopeplis perfoliata, and Halocnemum strobilaceum. However, species
84 associated with S. drummondii in non-saline habitats are glycophytes, such as Launaea capitata,
85 Cornulaca monacantha, Pennisetum divisum, and Indigofera oblongifolia. Other habitat-
86 indifferent halophytes, such as Suaeda vermiculata and Zygophyllum qatarense, are also
87 recorded as being associated with S. drummondii in the two habitat types (Jongbloed 2003).
88 There are several economic uses of this species. For example, leaves can be burnt to produce
89 soda ash. In addition, different parts of this plant have medicinal uses (Gilani et al. 2010). The
90 leaves can also be used for feeding animals (Qureshi et al. 1993). Furthermore, S. drummondii is
91 an important plant for the restoration of salt-affected or degraded habitats (Dagar and Minhas
92 2016).
93 Both drought and salinity stresses reduce soil water potential. Polyethylene glycol (PEG) can
94 be used to create solutions with various negative water potentials (Money 1989). Drought usually
95 affects plants through affecting soil water potential, i.e., osmotic effect. However, the effect of
96 salinity could be mediated through specific ion toxicity and/or reduced soil osmotic potential
97 (Munns 2002; Kranner and Seal 2013; Maucieri et al. 2018). Polyethylene glycol has been used
98 to simulate drought or water-stress during germination and plant growth (Kołodziejek and
99 Patykowski 2015). Germination inhibition in PEG-treated seeds is attributed mainly to osmotic,
Page 5 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
100 rather than ion-specific toxicity effects, which is usually attributed to salinity. Several
101 researchers used this solute in germination studies to detect whether the effect of salinity on
102 certain species is osmotic and/or ion-specific (Tobe et al. 2000; Sosa et al. 2005; Hameed et al.
103 2013). The marked differences in germination response observed at the same osmotic potentials
104 with NaCl and PEG indicate ionic-specific effects (Sidari et al. 2008). In a Pakistani population,
105 Rasheed et al. (2015) studied germination of S. drummondii and reported that its seeds can
106 germinate in up to 1000 mM NaCl (i.e., almost twice as high as seawater salinity). Tolerance to
107 salinity level differs based on both temperature and light conditions during germination (Rasheed
108 et al. 2015). The survival of S. drummondii in both saline and non-saline habitats makes it a good
109 model for assessing the effect of maternal habitat on seeds’ response to drought and dormancy
110 during germination. As development and maturation of S. drummondii seeds in saline habitats
111 are subjected to both salt and, possibly, water deficit stress of the arid environment, we
112 hypothesize that seeds collected from saline habitats may have a greater drought tolerance as
113 compared to seeds from non-saline habitats, which could be subjected only to water deficit
114 stress. Therefore, the goal of this study was to assess the response of drought tolerance, as
115 simulated by PEG, during the germination stage of S. drummondii seeds collected from saline
116 and non-saline habitats in the presence of different light and temperature regimes. Higher
117 drought tolerance is expected in seeds from saline habitat as this characteristic helps them
118 survive the higher salinity levels of their natural habitats. In addition, we have assessed the
119 significance of the interaction between the main factors (i.e., maternal habitat, drought, light, and
120 temperature) to determine the dependence of drought tolerance on light and temperature during
121 germination of seeds from the two habitat types. This, in turn, will help determine the proper
122 time of germination under natural conditions of seeds from the two habitats. Moreover, it is
Page 6 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
123 important to define a seed population that can tolerate higher drought levels during germination
124 for a species that has the potential to be used in restoration of degraded deserts. The seeds of the
125 habitat type that can tolerate higher drought can be used for restoration purposes even during
126 years that receive little rainfall.
127
128 Materials and methods
129 Study site and seed collection
130 Mature seeds of Salsola drummondii were collected from two sites around Kalba city, the eastern
131 coast of the UAE, during December 2015. One site was saline with compacted surface soils
132 (24°99′68.68″N and 56° 34′91.90″E) and the other was a non-saline sand plain (25° 02′94.17″N
133 and 56° 36′17.56″E). The saline and non-saline soil types could be classified according to the
134 USDA soil taxonomy as Haplosalids and Typic Torripsamments, respectively (Shahid et al.
135 2014). Seeds of each habitat were randomly collected from 50–60 plants. Collected seeds were
136 cleaned and stored in brown paper bags at -18 °C until the experiment was initiated in the first
137 week of January 2016. At that time of the year, effective rainfalls usually occur and therefore
138 germination takes place.
139 Five soil samples were collected from around S. drummondii at each habitat. Soil samples
140 were air dried and sieved. Soil salinity, electrical conductivity (EC), and pH were measured from
141 a 1:5 soil: water suspension (Dahnke and Whitney 1988). After 24h of shaking, the suspension
142 was left undisturbed for 1h, then pH and electrical conductivity (EC) were measured by Thermo
143 Scientific Orion Star A211 pH Benchtop Meter. Salinity was measured using a HQ40d salinity
144 meter (HACH, Loveland, Colorado, USA).
Page 7 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
145 Effects of maternal salinity on drought tolerance at different light intensities and temperatures
146 Polyethylene glycol is an inert polymer. It is nonionic, has high molecular weight, and can be
147 dissolved in water. It is the most preferred osmotic substance that can create solutions with
148 various negative water potentials. We used PEG to assess drought tolerance during germination
149 in order to determine the minimum water potential threshold for germination (Bradford 2002).
150 Solutions with higher levels of PEG have higher negative water potentials (Money 1989; Munns
151 2002). Several studies have used PEG to simulate drought during germination in several species
152 (Okçu et al. 2005; Sidari et al. 2008; Muscolo et al. 2014; Cochrane et al. 2015; Kołodziejek and
153 Patykowski 2015; Cavallaro et al. 2016). As PEG is a non-penetrating polymer, it affects seed
154 germination through its osmotic effect (Munns 2002).
155 To assess drought tolerance during germination of seeds from both the saline and non-
156 saline habitats and to estimate the dependence of the tolerance on incubation temperature and
157 light regimes, seeds from the two habitat types were germinated in six PEG 6000 (Sigma-
158 Aldrich) levels (0, -0.4, -0.7, -1.0, -1.2 and -1.5 MPa) and incubated in three CONVIRON plant
159 growth chambers (model E-15) adjusted at three temperatures, each with two light regimes. The
160 three temperatures were 15/25, 20/30 and 25/35°C with 12-h dark/12-h light cycles, where high
161 temperatures coincided with 12 hrs of white light. The two light regimes were light (12-hr
162 light/12-hr dark) and complete darkness (hereafter referred as light and dark regimes,
163 respectively). The PEG levels used here were selected after a preliminary test to assess the
164 drought tolerance of S. drummondii during germination. The osmotic potentials of the prepared
165 PEG solutions were verified using a Wescor Vapro 5520 (Wescor Inc., UT, USA) capable of
166 measuring osmotic potentials. The lighting in the chamber was white light (1400 µmol m–2 s–1 of
167 photosynthetically active radiation) provided by five (400 W) metal halide and five (400 W) high
Page 8 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
168 pressure sodium lamps. Germination was conducted in 9-cm Petri dishes on two layers of
169 Whatman No. 1 filter paper, moistened with 10 ml of the test solutions. As a precaution to
170 minimize evaporation, the plates were wrapped with parafilm. To achieve the dark treatment, the
171 dishes were wrapped in aluminum foil. Four replicate dishes, each with 25 seeds, were used for
172 each treatment. Visible radicle protrusion was used as an indication for germination. Under the
173 light regime, germinated seeds were counted every other day for 20 days following seed
174 imbibition. Seed viability in each habitat type was assessed for three batches, each consisting of
175 100 seeds, using 1% (w/v) 2,3,5- triphenyl-tetrazolium chloride solution (Bradbeer 1998).
176 Germination recovery
177 At the end of germination experiment (i.e., after 20 days), non-germinated seeds in the different
178 PEG solutions at different light and temperature regimes, were washed and placed in distilled
179 water to determine if they would germinate. This recovery experiment was conducted at the
180 same temperature regimes mentioned above and under the same light conditions. Germinated
181 seeds were counted every other day for 10 days.
182 Calculations and data analyses
183 The rate of germination was estimated by using a modified Timson index of germination
184 velocity: ΣG/t, where G is the percentage of seed germination at 2-day intervals, and t is the total
185 germination period (Khan et al. 2000). The maximum possible value in our data, using this
186 germination rate index, was 50. This value means that all germination occurred in the first count
187 (i.e., after two days).
188 The germination recovery percentage was calculated using the following formula (Khan et al.
189 2000): Recovery percentage = (a-b)/(c-b)*100, where a is the total number of seeds germinated
Page 9 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
190 after being transferred to distilled water, b is the total number of seeds germinated in PEG
191 solution, and c is the total number of seeds.
192 Four-way ANOVAs were used to evaluate the significance of the four factors (i.e., maternal
193 habitat, drought, temperature, and light) and their effects on final germination, germination
194 recovery, and total germination (germination in saline solution plus recovery germination).
195 Three-way ANOVA was used to assess the impacts of maternal habitat, drought, and
196 temperature and their interactions on germination rate index (GRI). Pearson correlation
197 coefficients were calculated to assess the relationship between PEG concentrations and total
198 germination. One way ANOVAs were performed to assess the significant differences between
199 the saline and non-saline habitats in EC, salinity and pH. Tukey’s test (Honestly significant
200 differences, HSD) was used to estimate the least significant differences between the means at P =
201 0.05. Germination percentages were arcsine-transformed to meet ANOVA assumptions. This
202 transformation improved the normality of the data distribution.
203 Results
204 Soil and seed properties of the two habitat types
205 Soils of the saline habitat attained significantly greater electric conductivity (EC) (21.3 mS/cm),
206 in comparison to the non-saline habitat (1.4 mS/cm, F = 270, P < 0.001). In addition, the pH was
207 significantly greater in soils of the saline habitat (pH = 9.0), compared to those of the non-saline
208 habitat (pH = 8.0, F = 83.0, P<0.001). Furthermore, salinity attained significantly greater values
209 in the saline (5.5 g/l) than in the non-saline habitats (0.38 g/l, F = 12.2, P<0.001). There was no
210 significant difference between the average seed mass of the saline (0.680 mg) and non-saline
211 (0.745 mg) habitats (F = 2.2, P>0.05). In addition, seed viability did not differ significantly
Page 10 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
212 between the seed lots of the two habitats (88.7% and 92.6%, for saline and non-saline habitats,
213 respectively, F = 3.2, P>0.05).
214 Final germination in PEG solutions
215 There were significant effects for the main factors and many of their interactions on the final
216 germination of S. drummondii (P<0.05, Table 1). The significant interaction between maternal
217 salinity and PEG concentration indicates that tolerance to drought as simulated by PEG
218 depended on seed source. No germination occurred at -1.8 MPa PEG for seeds from the two
219 habitat types. Seeds of the non-saline habitat attained significantly greater germination levels, as
220 compared to those of the saline habitat, in PEG concentrations up to -1.0 MPa (Fig. 1). The
221 difference diminished in -1.2 MPa PEG and completely disappeared in -1.5 MPa. This result
222 implies that seeds of the non-saline habitat had greater germination in higher osmotic potential,
223 compared to those of the saline habitat. At lower osmotic potentials (-1.5 MPa), however, there
224 was no significant difference in final germination between seeds of the two maternal habitats
225 (Fig. 1a).
226 The interactions between PEG treatment and both temperature and light were significant
227 (P<0.01, Table 1), indicating that the tolerance to PEG osmotic potential depended on these
228 conditions during seed sowing. For example, whereas no significant difference was observed in
229 final germination at lower (15/25 °C) and higher temperatures (25/35 °C) in distilled water and -
230 0.4 MPa PEG, germination was significantly greater at lower than at higher temperatures at PEG
231 levels ≥ -0.7 MPa (Fig. 1b). However, the effect of light on drought tolerance was not clear;
232 whereas germination was significantly greater in light than in dark in -0.7 and -1.2 MPa, there
Page 11 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
233 was no significant difference between germination in light and dark at the other PEG
234 concentrations (Fig. 1c).
235 Germination rate index in the PEG solutions
236 The effects of maternal salinity, PEG, and temperature on GRI were significant (P<0.001, Table
237 2). GRI decreased with increasing PEG concentrations; GRI was 49.6 in the control but reduced
238 to 32.1 at -1.5 MPa. There were significant effects of the interaction between PEG and both
239 maternal salinity and temperature of incubation on the GRI (P<0.001, Table 2). No significant
240 difference in GRI was observed between seeds of the two habitats at lower concentrations of
241 PEG (0, -0.4 and -0.7 MPa). However, seeds of the saline habitat attained significantly higher
242 GRI (i.e., germinated faster) in the higher concentrations of PEG (Fig. 2a). In addition, GRI did
243 not differ between the different temperatures at higher osmotic potentials (PEG levels ≤-1.0
244 MPa). However, at lower osmotic potential (PEG levels= -1.2 and -1.5 MPa), germination was
245 significantly faster at higher than at lower temperatures (Fig. 2b).
246 Germination recovery
247 There were significant effects of maternal salinity, drought, and temperature, but not light, on
248 germination recovery (P<0.001, Table 1). The significant effect of the interaction between
249 maternal salinity and PEG indicates that recovery of seeds from different PEG concentrations
250 depended on the seed source (i.e., maternal habitat). Germination recovery occurred mainly in
251 seeds that failed to germinate in -1.2 and -1.5 MPa and was significantly greater for seeds of
252 plants in non-saline habitats than for those of plants in saline habitats (Fig. 3a). In addition, the
253 response of germination recovery at different concentrations of PEG depended on temperature of
254 incubation; the interaction between PEG concentration and temperature was significant (P<0.01,
Page 12 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
255 Table 1). There was no significant effect for temperature on germination recovery in all osmotic
256 potential, expect in the lowest osmotic potential (-1.5 MPa), in which germination recovery was
257 significantly greater at lower than at higher temperatures (Fig. 3b). The interaction between PEG
258 and light was non-significant. However, recovery was greater for seeds incubated in light, as
259 compared to those in dark, in osmotic potential -1.2 and -1.5 MPa. (Fig. 3c).
260 Total germination
261 All the four main factors showed significant effects on the total germination (i.e., germination in
262 PEG solution plus germination recovery) (P<0.05). However, only three interactions between the
263 main factors were significant, compared to six significant interactions for germination in PEG
264 (Table 1). In addition, Pearson correlation coefficients assessing the relationship between total
265 germination and PEG concentrations indicated significant negative relationships at all
266 temperatures for seeds of the non-saline habitat (r = - 0.77, P<0.001 at 15/25 °C; r = - 0.59,
267 P<0.001 at 20/30 °C; r = - 0.65, P<0.001 at 25/35 °C). For seeds of the saline habitat, however,
268 the negative relationship was significant at 15/25 °C (r = - 0.50, P<0.001) and 20/30 °C (r = -
269 0.49, P<0.001), but not at 25/35 °C (r = - 0.04, P>0.05).This result indicates that the germination
270 of S. drummondii seeds of the saline habitats was less affected by the increase in PEG
271 concentration at higher temperatures, but seeds of the non-saline habitats were negatively
272 affected by the increase in the PEG concentrations at all temperatures.
273 Discussion
274 The results of our study showed significantly greater germination of seeds from the non-saline
275 habitat as compared with those from saline habitat in all PEG concentrations up to -1.2 MPa. At -
276 1.5 MPa; however, there were non-significant differences in the final germination of the two
277 seed lots. The results also showed insignificant differences in the viability of non-saline and
Page 13 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
278 saline habitat seeds. This indicates that seeds from the saline habitat are more dormant, as
279 compared to those from the non-saline habitats when germinated in lower osmotic potential
280 solutions of PEG. Maruyama et al. (2016) explained the higher dormancy observed in Impatiens
281 capensis seeds produced under maternal drought stress to be a mechanism for desiccation
282 avoidance/drought tolerance in heterogeneously dry sites. The greater dormancy of the saline
283 habitat seeds of S. drummondii helps them postpone their germination until the onset of
284 favorable conditions for seedling establishment. Such conditions usually occur when effective
285 rainfall happens at lower temperatures during winter (e.g., during November – February, El-
286 Keblawy 2004, 2017).
287 The combined effect of soil temperature and water content on seed germination is an
288 environmental signal that could determine the germination time (Fyfield and Gregory 1989). Our
289 results showed non-significant differences between the germination of seeds at the three
290 temperatures, when S. drummondii seeds were incubated at low levels of drought (0 and -0.4
291 MPa). At higher drought levels, however, germination was significantly reduced at high
292 temperatures (25/35 °C) as compared to lower temperatures (15/25 °C). This could be an
293 ecological adaptation to reduce germination at the end of the growing season, when conditions
294 are not favorable for seedling establishment (Hameed et al. 2013; El-Keblawy et al. 2015;
295 Rasheed et al. 2015). In general, exposing seeds to two stress factors (drought and high
296 temperatures) would affect the integrity of cell membranes (Raison 1986). Electrolyte leakage
297 resulting from loss of membrane integrity at higher temperatures reduced germination in several
298 species, such as Brassica spp. (Thornton et al. 1990) and Brassica olearcea (Jett et al. 1996).
299 Germination of S. drummondii was significantly greater under dark conditions than under
300 light at the highest concentration of PEG (-1.5 MPa), when seeds were incubated at lower
Page 14 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
301 temperatures (15/25 °C), but the reverse was true at higher temperatures (25/35 °C). This result
302 might be ecologically important for the survival of S. drummondii in arid desert conditions.
303 During dry years, when soil water potential is low, seeds germinate only when rainfalls occur at
304 cooler temperatures and seeds are allowed to germinate under conditions of darkness, e.g., while
305 being covered with litter or by remaining in a soil crack. Such conditions enhance seedling
306 establishment in arid deserts, where soils have lower rates of water retention (El-Keblawy 2017).
307 Both drought and salinity lower the plant water potential by reducing the free energy of
308 water available for the plant to be below that of pure free water. To avoid desiccation, the water
309 potential of the symplast must be adjusted (Flowers and Yeo 1986). Osmotic adjustment could
310 be through ion contents or production of organic osmolytes (Ghoulam et al. 2002). In a study
311 assessing salinity tolerance in S. drummondii, Rasheed et al. (2015) reported that some seeds
312 were able to germinate in 1000 mM NaCl (around -5.0 MPa). In the present study, however,
313 seeds of S. drummondii germinated only to less than 20% in -1.5 MPa PEG solutions. The
314 greater tolerance to lower osmotic potential resulted from NaCl than that from PEG has been
315 reported in several other species. In Ceratonia silique, for example, germination was
316 significantly reduced by a water stress simulated by a moderate level of PEG (−0.5 MPa), but it
317 occurred in higher levels of NaCl (−1.0 MPa, Cavallaro et al. 2016). Similarly, the effects of
318 NaCl on both germination and seedling growth of three pea cultivars was significantly less,
319 compared to the effect of PEG (Okçu et al. 2005). Furthermore, germination of Henophyton
320 deserti seeds was less affected by NaCl, as compared with PEG (Gorai et al. 2014).
321 The greater tolerance of S. drummondii to NaCl, compared to drought simulated by PEG
322 indicates that osmotic, rather than toxicity effect would be responsible for the failure of
323 germination of this species in saline solutions. The result also indicates that PEG might cause
Page 15 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
324 irreversible damage to the cells (Yu and Rengel 1999). The rehydration of desiccated seeds after
325 being treated with PEG could be associated with damage of the plasma lemma, and consequently
326 leakage of cell solutes (Hendricks and Taylorson 1976; Yu and Rengel 1999). Changes in
327 organelle morphology and function, and disruption of organelle membranes due to desiccation
328 associated with water stress have been also reported in other species (see Dhindsa and Bewley
329 1977). The ability of S. drummondii to tolerate and recover from -5.0 MPa NaCl (Rasheed et al.
330 2015), but only in -1.5 MPa PEG (our study) indicates that this species is more adapted to saline
331 than drought conditions. In fact, this species produce flowers and fruits before the onset of the
332 rainy season (October – November), despite the fact that it has a very shallow root system to tap
333 groundwater, indicating that it depends on atmospheric moisture as a non-conventional source
334 for water, in absence of soil water during the dry summer (Dirks et al. 2016).The ability of the
335 plants of S. drummondii to flower and fruit in the absence of conventional soil water indicates
336 that they are relying on moisture absorption from air rather than soil. Consequently, as seeds
337 have a limited ability to absorb atmospheric moisture, they cannot tolerate soil moisture
338 deficiency as adult plants do.
339 Climatic factors, in particular temperature and water availability, have a considerable
340 influence on plant recruitment and survival (Gurvich et al. 2017). These factors are critical
341 drivers for seed dormancy and germination. Consequently, plant recruitment and population
342 dynamics will certainly be affected by projected climate change (Walck et al. 2011). Evans
343 (2009) used 18 global climate models and predicted an overall temperature increase of ∼1.4 K
344 by mid-century, increasing to almost 4 K by late-century for the Middle East. In addition, he also
345 predicted increases in the length of the dry season and changes in the timing of the maximum
346 precipitation that will impact the growing season (Evan 2009). Our results showed that seeds of
Page 16 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
347 S. drummondii from both saline and non-saline habitats germinated to more than 40% under high
348 levels of drought (-1.2 MPa). In addition, more than 25% of the seeds germinated at high
349 temperatures (i.e. above the average of the growing season, Böer B 1997) (Fig. 1a,b). The broad
350 windows of germination under different temperature and light regimes and the ability of seeds to
351 germinate under relatively lower osmotic potentials indicate that S. drummondii is less
352 threatened by the projected climate change in the Middle East.
353 Plants are sedentary organisms that have little choice for the suitable environment where
354 they can grow and reproduce. Environmental stresses that are experienced by paternal plants can
355 induce phenotypic changes that span multiple generations (Münzbergová and Hadincová 2017).
356 Transgenerational plasticity provides phenotypic variation that contributes to adaptation to
357 environmental stresses (Vu et al. 2015). Transgenerational phenotypic plasticity in progeny traits
358 can occur through maternal and/or epigenetic effects (Soliman et al. 2018). Maternal effects in
359 plants include the maternal genetic effects caused by maternal inheritance of plastids in addition
360 to non-inheritance effect of endosperm, seed coat, resource provisioning of nutrient resources,
361 hormones, proteins and transcripts (Vu et al. 2015; Verslues 2016). Whereas environmental
362 maternal effects are usually diminished in the first generation, epigenetic effects transmit
363 heritable plastic responses to environmental cues (Uller et al. 2008). In our study, it is not clear
364 whether the differences in seed dormancy, germination responses and drought tolerance between
365 seeds from saline and those from non-saline habitats are due to maternal and/or epigenetic
366 effects. Therefore, further studies are needed to separate epigenetic effect from maternal salinity
367 effect in habitat-indifferent halophytes, such as S. drummondii. For example, reciprocal
368 transplant experiments between the two populations should be conducted and seed germination
Page 17 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
369 response and drought tolerance from these plants should be compared. Another approach could
370 be through growing micropropagated plants from the two populations in both habitat types.
371 Conclusion
372 Seeds of the non-saline habitats had significantly lower dormancy and higher germination in
373 PEG concentrations up to -1.2 MPa, as compared with seeds of the saline habitat. The relatively
374 higher dormancy of the saline habitat seeds indicates that they prefer to postpone their
375 germination until the arrival of proper conditions for seedling establishment, which is usually
376 after winter rainfalls in the arid Arabian deserts. The faster germination of saline habitat seeds in
377 lower osmotic potential solutions indicates that they establish themselves shortly after rainfalls,
378 especially in years that receive less than average rainfalls.
379 Acknowledgements
380 This work was partially supported through a grant from the University of Sharjah Research
381 Office that supported to the Environmental and Chemical Biology Research Group (Grant #
382 150404).The authors would like to thank Mr. Mohammed Hassan, Sharjah Research Academy
383 for his help in seeds collection.
384 References
385 Al-Shamsi, N., El-Keblawy, A., Mosa, K., and Navarro, T. 2018. Drought tolerance and
386 germination response to light and temperature for seeds of saline and non-saline habitats of the
387 habitat-indifferent desert halophyte Suaeda vermiculata. Acta Physiol. Plant. 40: 200 . DOI :
388 10.1007/s11738-018-2771-z.
389 Baskin, C.C., and Baskin, J.M. 2014. Seeds, ecology, biogeography, and evolution of dormancy
390 and germination, 2nd ed. Elsevier/Academic Press, San Diego.
Page 18 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
391 Böer, B. 1997. An introduction to the climate of the United Arab Emirates. J. Arid Environ.
392 35(1): 3-16. DOI: 10.1006/jare.1996.0162
393 Bradbeer, J.W. 1998. Seed Dormancy and Germination. Chapman and Hall, New York, USA.
394 Bradford, K.J. 2002. Applications of hydrothermal time to quantifying and modeling seed
395 germination and dormancy. Weed Sci. 50: 248-260. DOI: 10.1614/0043-
396 1745(2002)050[0248:AOHTTQ]2.0.CO;2
397
398 Cavallaro, V., Barbera, A.C., Maucieri, C., Gimma, G., Scalisi, C., and Patanè, C. 2016.
399 Evaluation of variability to drought and saline stress through the germination of different
400 ecotypes of carob (Ceratonia siliqua L.) using a hydrotime model. Ecol. Eng. 95: 557-566.
401 DOI: 10.1016/j.ecoleng.2016.06.040
402 Cochrane, J.A., Hoyle, G.L., Yates, C.J., Wood, J., and Nicotra, A.B. 2015. Evidence of
403 population variation in drought tolerance during seed germination in four Banksia (Proteaceae)
404 species from Western Australia. Aust. J. Bot. 62: 481-489. DOI: 10.1071/BT14132
405 Cosgrove, W.J., and Rijsberman, F.R. 2014. World water vision: making water everybody's
406 business. Routledge, Abingdon-on-Thames.
407 Dagar, J.C., and Minhas, P.S. 2016. Global Perspectives on Agroforestry for the Management of
408 Salt-Affected Soils. In Agroforestry for the Management of Waterlogged Saline Soils and
409 Poor-Quality Waters. Edited by J.C. Dagar and P.S. Minhas. Springer, New Delhi. pp. 5–32.
410 Dahnke, W.C., and Whitney, D.A. 1988. Measurement of soil salinity. In Recommended
411 Chemical Soil Test, Procedures for the North Central Region. Edited by W.C. Dahnke. North
Page 19 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
412 Central Regional Publication No. 221. North Dakota: Missouri Agricultural Experiment
413 Station SB 1001, Columbia. pp. 32–34
414 Dhindsa, R.S., and Bewley, J.D. 1977. Water stress and protein synthesis. Plant Physiol. 59(2):
415 295–300. DOI: 10.1104/pp.59.2.295
416 Donohue, K., and Schmitt, J. 1998. Maternal environmental effects in plants. In Maternal Effects
417 as Adaptations. Edited by T.A. Mousseau and C.W. Fox. Oxford University Press, Oxford. pp.
418 137–158.
419 Dirks, I., Raviv, B., Shelef, O., Hill, A., Eppel, A., Aidoo, M.K., Hoefgen, B., Rapaport, T., Gil,
420 H., Geta, E., and Kochavi, A. 2016. Green roofs: what can we learn from desert plants? Israel
421 J. Ecol. Evol. 62 (1-2): 58-67. DOI: 10.1080/15659801.2016.1140619
422 El-Keblawy, A. 2004. Salinity effects on seed germination of the common desert range
423 grass, Panicum turgidum. Seed Sci. Technol. 32(3): 873-874. DOI: 10.15258/sst.2004.32.3.24
424 El-Keblawy, A. 2014. Effects of Seed Storage on Germination of Desert Halophytes with
425 Transient Seed Bank. In Sabkha Ecosystem IV. Edited by M. A. Khan, B. Böer, G. S. Kust
426 and H. J. Barth. Springer, Dordrecht. pp. 193-203.
427 El-Keblawy, A. 2017. Light and temperature requirements during germination of potential
428 perennial grasses for rehabilitation of degraded sandy Arabian Deserts. Land Degrad. Dev.
429 28(5): 1687–1695. DOI: 10.1002/ldr.2700
430 El-Keblawy, A., and Al-Rawai, A. 2006. Effects of seed maturation time and dry storage on light
431 and temperature requirements during germination in invasive Prosopis juliflora. Flora,
432 201(2): 135-143.DOI: 10.1016/j.flora.2005.04.009
Page 20 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
433 El-Keblawy, A., Al-Shamsi, N., and Mosa, K. 2018. Effect of maternal habitat, temperature and
434 light on germination and salt tolerance of Suaeda vermiculata, a habitat-indifferent halophyte
435 of arid Arabian deserts. Seed Sci. Res. 28(2): 140-147. DOI: 10.1017/S0960258518000144
436 El-Keblawy, A., Bhatt, A., and Gairola, S. 2015. Storage on maternal plants affects light and
437 temperature requirements during germination in two small seeded halophytes in the Arabian
438 deserts. Pak. J. Bot. 47: 1701-1708.
439 El-Keblawy, A., and Bhatt, A. 2015. Aerial seed bank affects germination behaviour of two
440 small seeded halophytes in the Arabian deserts. J. Arid Environ. 115: 10-17 DOI:
441 10.1016/j.jaridenv.2015.02.001
442 El-Keblawy, A., Gairola, S., and Bhatt, A. 2016. Maternal salinity environment affects salt
443 tolerance during germination in Anabasis setifera: A facultative desert halophyte. J. Arid
444 Land, 8(2): 254-263. DOI: 10.1007/s40333-015-0023-2
445 El-Keblawy, A., Gairola, S., Bhatt, A., and Mahmoud T. 2017a. Effects of maternal salinity on
446 salt tolerance during germination of Suaeda aegyptiaca: a facultative halophyte in the Arab
447 Gulf desert. Plant Species Biol. 32(1): 45-53. DOI: 10.1111/1442-1984.12127
448 El-Keblawy, A., Shabana, H.A., Navarro, T., and Soliman, S. 2017b. Effect of maturation time
449 on dormancy and germination of Citrullus colocynthis (Cucurbitaceae) seeds from the Arabian
450 hyper-arid deserts. BMC Plant Biol. 17(1): 263. DOI: 10.1186/s12870-017-1209-x
451 Evans, J.P. 2009. 21st century climate change in the Middle East. Clim. Change, 92(3-4): 417-
452 432. DOI: 10.1007/s10584-008-9438-5
453 Fenner, M. 1991. The effects of the parent environment on seed germinability. Seed Sci. Res.
454 1(2): 75–84. DOI: 10.1017/S0960258500000696
Page 21 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
455 Feulner, G.R. 2006. Rainfall and climate records from Sharjah Airport: Historical data for the
456 study of recent climatic periodicity in the UAE. Tribulus, 16(1): 3-9.
457 Flowers, T.J., and Yeo, A.R. 1986. Ion relations of plants under drought and salinity. Funct.
458 Plant Biol. 13(1): 75-91. DOI: 10.1071/PP9860075
459 Fyfield, T.P., and Gregory, P.J. 1989. Effects of temperature and water potential on germination,
460 radicle elongation and emergence of mung bean. J. Exp. Bot. 40(6): 667-674. DOI:
461 10.1093/jxb/40.6.667
462 Gilani, S.A., Fujii, Y., Shinwari, Z.K., Adnan, M., Kikuchi, A., and Watanabe, K.N. 2010.
463 Phytotoxic studies of medicinal plant species of Pakistan. Pak. J. Bot. 42(2): 987-996.
464 Available from http://pakbs.org/pjbot/PDFs/42(2)/PJB42(2)0987.pdf
465 Gorai, M., El Aloui, W., Yang, X., and Neffati, M. 2014. Toward understanding the ecological
466 role of mucilage in seed germination of a desert shrub Henophyton deserti: interactive effects
467 of temperature, salinity and osmotic stress. Plant Soil, 374(1-2): 727-738. DOI:
468 10.1007/s11104-013-1920-9
469 Ghoulam, C., Foursy, A., and Fares, K. 2002. Effects of salt stress on growth, inorganic ions and
470 proline accumulation in relation to osmotic adjustment in five sugar beet cultivars. Environ.
471 Exp. Bot. 47(1): 39-50. DOI: 10.1016/S0098-8472(01)00109-5
472 Gutterman, Y. 2000. Environmental factors and survival strategies of annual plant species in the
473 Negev Desert, Israel. Plant Species Biol. 15(2): 113-125. DOI: 10.1046/j.1442-
474 1984.2000.00032.x
475 Hameed, A., Ahmed, M.Z., Gulzar, S., Gul, B., Alam, J., Hegazy, A.K., Alatar, A.R.A.,
476 and Khan, M.A. 2013. Seed germination and recovery responses of Suaeda heterophylla to
Page 22 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
477 abiotic stresses. Pak. J. Bot. 45(5): 1649-1656. Available from
478 http://www.pakbs.org/pjbot/PDFs/45(5)/24.pdf
479 Hendricks, S.B., and Tayloroson, R.B. 1976. Variation in germination and amino acid leakage of
480 seeds with temperature related to membrane phase change. Plant Physiol. 58(1): 7-11. DOI:
481 10.1104/pp.58.1.7
482 Jett, L.W., Welbaum, G.E., and Morse, R.D. 1996. Effects of matric and osmotic priming
483 treatments on broccoli seed germination. J. Am. Soc. Hort. Sci. 121(3): 423-429. Available
484 from http://journal.ashspublications.org/content/121/3/423.full.pdf+html
485 Jongbloed, M. 2003. The comprehensive guide to the wild flowers of the United Arab Emirates.
486 Environmental Research and Wildlife Development Agency, Abu Dhabi, UAE, 567 .
487 Khan, M.A., Gul, B., and Weber, D.J. 2000. Germination responses of Salicornia rubra to
488 temperature and salinity. J. Arid Environ. 45: 207-214. DOI: 10.1006/jare.2000.0640
489 Kołodziejek, J., and Patykowski, J. 2015. Effect of environmental factors on germination and
490 emergence of invasive Rumex confertus in Central Europe. The Scientific World Journal, 1-10
491 DOI: 10.1155/2015/170176
492 Kranner, I., and Seal, C.E. 2013. Salt stress, signalling and redox control in seeds. Funct. Plant
493 Biol. 40(9): 848-859. DOI: 10.1071/FP13017
494 Muscolo, A., Sidari, M., Anastasi, U., Santonoceto, C., and Maggio, A. 2014. Effect of PEG-
495 induced drought stress on seed germination of four lentil genotypes. J. Plant Interact. 9(1):
496 354-363. DOI: 10.1080/17429145.2013.835880
497 Levitt, J. 1972. Responses of Plants to Environmental Stresses. Academic Press, New York.
Page 23 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
498 Maruyama, C., Goepfert, Z., Squires, K., Maclay, T., Teal-Sullivan, Q., and Heschel, M.S. 2016.
499 Effects of population site and maternal drought on establishment physiology in Impatiens
500 capensis Meerb. (Balsaminaceae). Rhodora, 118(973): 32–45. DOI: 10.3119/15-14
501 Maucieri, C., Caruso, C., Bona, S., Borin, M., Barbera, A. C., and Cavallaro, V. 2018. Influence
502 of salinity and osmotic stress on germination process in an old sicilian landrace and a modern
503 cultivar of Triticum Durum Desf. Cereal Res. Commun. 46(2), 253-262
504 Money, N.P. 1989. Osmotic pressure of aqueous polyethylene glycols. Plant Physiol. 91(2): 766–
505 769. DOI: 10.1104/pp.91.2.766
506 Mosa, K.A., Ismail, A., and Helmy, M. 2017. Plant Stress Tolerance. An Integrated Omics
507 Approach. Springer.
508 Munns, R. 2002. Comparative physiology of salt and water stress. Plant Cell Environ. 25(2):
509 239-250. DOI: 10.1046/j.0016-8025.2001.00808.x
510 Münzbergová, Z., and Hadincová, V. 2017. Transgenerational plasticity as an important
511 mechanism affecting response of clonal species to changing climate. Ecol. Evol. 7: 5236-5247.
512 DOI: 10.1002/ece3.3105
513 Nounjan, N., Chansongkrow, P., Charoensawan, V., Siangliw, J.L., Toojinda, T., Chadchawan,
514 S., and Theerakulpisut, P. 2018. High performance of photosynthesis and osmotic adjustment
515 are associated with salt tolerance ability in rice carrying drought tolerance QTL: physiological
516 and co-expression network analysis. Front. Plant Sci. 9: 1135. DOI: 10.3389/fpls.2018.01135
517 Okçu, G., Kaya, M.D., and Atak, M. 2005. Effects of salt and drought stresses on germination
518 and seedling growth of pea (Pisum sativum L.). Turk. J. Agric. For. 29(4): 237-242.
Page 24 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
519 Petit, J.R., Jouzel, J., Raynaud, D., Barkov, N.I., Barnola, J.M., Basile, I., Bender, M.,
520 Chappellaz, J., Davis, M., Delaygue, G., Delmotte, M., Kotlyakov, V.M., Legrand, M.,
521 Lipenkov, V.Y., Lorius, C., Pepin, L., Ritz, C., Saltzman, E., and Stievenard, M. 1999.
522 Climate and atmospheric history of the past 420,000 years from the Vostok ice core,
523 Antarctica. Nature, 399(6735): 429-436. DOI: 10.1038/20859
524 Qureshi, R.H., Aslam, M., and Rafiq, M. 1993. Expansion in the use of forage halophytes in
525 Pakistan. In Productive use of saline land. Edited by N. Davidson and R. Galloway. ACIAR
526 Proceedings, Canberra, Australia. pp.12-16.
527 Raison, J.K. 1986. Alterations in the physical properties and thermal response of membrane
528 lipids: Correlations with acclimation to chilling and high temperature. In Frontiers of
529 membrane research in agriculture. Edited by J.B. S.t. John, E. Berlin and P.C. Jackson.
530 Rowman and Allanheld, Totowa. pp. 383–401.
531 Rasheed, A., Hameed, A., Khan, M.A., and Gul, B. 2015. Effects of salinity, temperature, light
532 and dormancy regulating chemicals on seed germination of Salsola drummondii Ulbr. Pak. J.
533 Bot. 47: 11-19. Available from http://www.pakbs.org/pjbot/PDFs/47(1)/02.pdf
534 Roach, D.A., and Wulff, R.D. 1987. Maternal effects in plants. Annu. Rev. Ecol. Syst. 18(1):
535 209-235. DOI: 10.1146/annurev.es.18.110187.001233
536 Rossiter, M.C. 1998. The role of environmental variation in parental effects expression.
537 In Maternal Effects as Adaptations. Edited by T.A. Mousseau, and C.W. Fox. Oxford
538 University Press, Oxford, UK. pp. 112–134.
539 Rossiter, M. 1996. Incidence and consequences of inherited environmental effects. Annu. Rev.
540 Ecol. Syst. 27(1): 451-476. DOI: 10.1146/annurev.ecolsys.27.1.451
Page 25 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
541 Shahid, S.A., Abdelfattah, M.A., Wilson, M.A., Kelley, J.A., and Chiaretti, J.V. 2014. United
542 Arab Emirates keys to soil taxonomy. Springer , Netherlands
543 Soliman, S., El-Keblawy, A., Mosa, K.A., Helmy, M., and Wani, S.H. 2018. Understanding the
544 Phytohormones Biosynthetic Pathways for Developing Engineered Environmental Stress-
545 Tolerant Crops. In Biotechnologies of Crop Improvement. Edited by S. Gosal and S. Wani.
546 Springer, Cham. pp. 417-450.
547 Sidari, M., Mallamaci, C., and Muscolo, A. 2008. Drought, salinity and heat differently affect
548 seed germination of Pinus pinea. J. For. Res. 13(5): 326-330. DOI: 10.1007/s10310-008-0086-
549 4
550 Siles, L., Müller, M., Cela, J., Hernández, I., Alegre, L., and Munné-Bosch, S. 2017. Marked
551 differences in seed dormancy in two populations of the Mediterranean shrub, Cistus albidus
552 L. Plant Ecol. Divers. 10(2-3): 231-240. DOI: 10.1080/17550874.2017.1350765
553 Sosa, L., Llanes, A., Reinoso, H., Reginato, M., and Luna, V. 2005. Osmotic and specific ion
554 effects on the germination of Prosopis strombulifera. Ann. Bot. 96(2): 261–267. DOI:
555 doi.org/10.1093/aob/mci173
556 Thornton, J.M., Powell, A.A., and Matthews, S. 1990. Investigation of the relationship between
557 seed leachate and the germination of Brassica seed. Ann. Appl. Biol. 117(1): 129–135. DOI:
558 10.1111/j.1744-7348.1990.tb04201.x
559 Turner, N.C.1986. Adaptation to water deficits: a changing perspective. Funct. Plant
560 Biol. 13(1):175-190. DOI: 10.1071/PP9860175
561 Uller, T. 2008. Developmental plasticity and the evolution of parental effects. Trends Ecol.
562 Evol. 23:432-438. DOI: 10.1016/j.tree.2008.04.005
Page 26 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
563 Wulff, R.D. 1995. Environmental maternal effects on seed quality and germination. In Seed
564 Development and Germination. Edited by J. Kigel and G. Galili. Marcel Dekker, New York.
565 pp. 491–505.
566 Yu, Q., and Rengel, Z. 1999. Drought and salinity differentially influence activities of
567 superoxide dismutases in narrow-leafed lupins. Plant Sci. 142(1): 1-11. DOI: 10.1016/S0168-
568 9452(98)00246-5
569 Verslues, P.E. 2016. ABA and cytokinins: challenge and opportunity for plant stress
570 research. Plant Mol. Biol. 91: 629-640. DOI: 10.1007/s1110
571 Vu, W.T., Chang, P.L., Moriuchi, K.S., and Friesen, M.L. 2015. Genetic variation of
572 transgenerational plasticity of offspring germination in response to salinity stress and the seed
573 transcriptome of Medicago truncatula. BMC Evol. Biol. 15: 59. DOI: 10.1186/s12862-015-
574 0322-4
Page 27 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
576
577 Table 1. Results of four-way ANOVA showing the effects of maternal salinity and environmental factors
578 during incubation (drought, as stimulated by PEG, temperature and light) and their interactions on final
579 germination in PEG solution, germination recovery after seeds transferred from PEG to distilled water
580 and total germination (i.e., germination in PEG solutions plus germination recovery) of Salsola
581 drummondii seeds
Final germination Recovery germination
Total germination
Source of variation df Mean Squares
F-Ratio Mean Squares
F-Ratio Mean Squares
F-Ratio
Maternal salinity (MS) 1 3.016 411.6*** 0.030 58.60*** 3.757 434.40***PEG 5 1.801 245.8*** 0.046 90.27*** 1.276 147.56***Temperature (T) 2 0.250 34.2*** 0.009 18.19*** 0.376 43.44***Light (L) 1 0.140 19.2*** 0.001 1.850 0.113 13.06***MS * PEG 5 0.158 21.5*** 0.016 31.98*** 0.067 7.71***MS * T 2 0.003 0.458 0.001 1.874 0.004 0.486MS * L 1 0.003 0.403 0.000 0.031 0.004 0.427PEG * T 10 0.024 3.22** 0.006 12.17*** 0.035 4.00***PEG * L 5 0.027 3.68** 0.000 0.948 0.024 2.72*T * L 2 0.068 9.29*** 0.001 0.996 0.077 8.90***MS * PEG * T 10 0.009 1.246 0.001 1.595 0.010 1.178MS * PEG * L 5 0.021 2.92* 0.001 1.597 0.020 2.136MS * T * L 2 0.002 0.322 0.002 3.37* 0.001 0.068PEG * T * L 10 0.021 2.9** 0.000 0.677 0.017 2.007MS * PEG * T * L 10 0.008 1.088 0.001 1.65 0.010 1.196Error 216 0.007 0.001 0.009
582
583 Table 2. Results of three-way ANOVA showing the effects of maternal salinity, and PEG concentration
584 and temperature and their interactions on germination rate index of Salsola drummondii seeds
Source of variation df Mean Squares F-Ratio PMaternal salinity (MS) 1 0.247 46.971 <0.001PEG 5 0.471 89.674 <0.001Temperature (T) 2 0.051 9.723 <0.001MS * PEG 5 0.055 10.404 <0.001MS * T 2 0.004 0.793 nsPEG * T 10 0.010 1.848 nsMS * PEG * T 10 0.005 0.920 nsError 108 0.005
585
Page 28 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
586 Figure captions
587 Fig. 1. Interactive effects of drought, as simulated using PEG, with (a) maternal salinity, (b)
588 temperature of incubation and (c) light of incubation on final germination percentage (mean ±
589 S.E.) of Salsola drummondii seeds.
590
591 Fig. 2. Interactive effects of drought, as simulated using PEG, with (a) maternal salinity and (b)
592 temperature of incubation on germination rate index (mean ± S.E.) of Salsola drummondii seeds.
593
594 Fig. 3. Interactive effects of drought, as simulated using PEG, with (a) maternal salinity, (b)
595 temperature of incubation and (c) light of incubation on germination recovery percentage (mean
596 ± S.E.) of Salsola drummondii seeds.
Page 29 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
Fig. 1.
a) Maternal salinity
(b) Temperature
(c) Light
Page 30 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
Fig. 2.
(a) Maternal salinity
(b) Temperature
Page 31 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany
Draft
Fig. 3.
(a) Maternal salinity
(b) Temperature
(c) Light
Page 32 of 32
https://mc06.manuscriptcentral.com/botany-pubs
Botany