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Journal of Arid Land  2020, Vol. 12 Issue (2): 283-293    DOI: 10.1007/s40333-020-0054-1
Research article     
Maternal salinity improves yield, size and stress tolerance of Suaeda fruticosa seeds
Syed Z SHAH1,2, Aysha RASHEED1, Bilquees GUL1, Muhammad A KHAN1, Brent L NIELSEN3, Abdul HAMEED1,*()
1 Institute of Sustainable Halophyte Utilization, University of Karachi, Karachi 75270, Pakistan
2 Govt. Degree Boys College, Sector 4E, New Saeedabad, Baldia Town, Karachi 75760, Pakistan
3 Department of Microbiology & Molecular Biology, Brigham Young University, Provo, UT 84602, USA
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Abstract  

Shrubby seablite or lani (Suaeda fruticosa Forssk) is a perennial euhalophyte with succulent leaves, which could be planted on arid-saline lands for restoration and cultivated as a non-conventional edible or cash crop. Knowledge about the impacts of maternal saline environment on seed attributes of this important euhalophyte is lacking. This study investigated the effects of maternal salinity on yield, size and stress tolerance of S. fruticosa seeds. Seedlings of S. fruticosa were grown in a green net house under increasing maternal salinity levels (0, 300, 600 and 900 mM NaCl) until seed production. Total yield, size, stress tolerance and germination of the descended seeds under different maternal saline conditions were examined. Plants grown under saline conditions (300, 600 and 900 mM NaCl) produce a substantially higher quantity of seeds than plants grown under non-saline condition (0 mM NaCl). Low maternal salinity (300 mM NaCl) improves seed size. Seeds produced under all maternal salinity levels display a higher tolerance to low temperature (night/day thermoperiod of 10°C/20°C), whereas seeds produced under 300 mM NaCl maternal saline condition show a better tolerance to high temperature (night/day thermoperiod of 25°C/35°C) during germination. Seeds from all maternal saline conditions germinate better in the 12 h photoperiod (12 h light/12 h dark) than in the dark (24 h dark); however, seeds produced from low and moderate maternal saline conditions (300 and 600 mM NaCl) show a higher germination in the dark than those from control and high maternal saline conditions (0 and 900 mM NaCl). In general, maternal salinity is found to improve yield, size and stress tolerance of S. fruticosa seeds.



Key wordseuhalophyte      maternal salinity      salt tolerance      seed germination      non-saline condition      Suaeda fruticosa     
Received: 15 February 2019      Published: 10 March 2020
Corresponding Authors:
About author: *Corresponding author: Abdul HAMEED (E-mail: ahameed@uok.edu.pk)
Cite this article:

Syed Z SHAH, Aysha RASHEED, Bilquees GUL, Muhammad A KHAN, Brent L NIELSEN, Abdul HAMEED. Maternal salinity improves yield, size and stress tolerance of Suaeda fruticosa seeds. Journal of Arid Land, 2020, 12(2): 283-293.

URL:

http://jal.xjegi.com/10.1007/s40333-020-0054-1     OR     http://jal.xjegi.com/Y2020/V12/I2/283

Fig. 1 Effects of maternal salinity on seed production of Suaeda fruticosa plant. (a), qualitative seed production per plant; (b), total seed number per plant; (c) total seed mass per plant. F-values are given. * means significance at P<0.05 level and ** means significance at P<0.01 level (ANOVA). Bars represent standard errors. Different lowercase letters indicate significant difference (P<0.05) among different maternal salinity treatments (Post-hoc Bonferroni test).
Fig. 2 Effects of maternal salinity on seed size (a and b) of Suaeda fruticosa plants. Bars represent standard errors. Different lowercase letters indicate significant difference (P<0.05) among different maternal salinity treatments (Post-hoc Bonferroni test).
Factor Final germination percentage Germination rate
MS 9.730*** 9.221***
T 2.334* 15.669***
MS×T 5.379** 4.604**
Table 1 ANOVA indicating effects of maternal salinity (MS), incubation temperature (T) and their interaction on mean final germination percentage (%) and germination rate of Suaeda fruticosa seeds
Fig. 3 Effects of maternal salinity on final germination percentage and germination rate of Suaeda fruticosa seeds under different thermoperiods. Bars represent means with standard errors. Different lowercase letters indicate significant difference (P<0.05) among maternal salinity treatments (Post-hoc Bonferroni test).
Fig. 4 Effects of maternal salinity on final germination percentage and germination rate of Suaeda fruticosa seeds in 200 mM NaCl solution. F-values are given. * means significance at P<0.05 level and ** means significance at P<0.01 level (ANOVA). Bars represent standard errors. Different lowercase letters indicate significant difference (P<0.05) among maternal salinity treatments (Post-hoc Bonferroni test).
Fig. 5 Effects of maternal salinity on final germination percentage of Suaeda fruticosa seeds under the 12 h photoperiod (12 h light/12 h dark) and under the dark treatment (24 h dark). The black circles represent final germination percentages under the 12 h photoperiod (12 h light/12 h dark) and the rectangles represent final germination percentages under 24 h dark treatment. Bars represent standard errors. Different capital letters indicate significant difference (P<0.05) among different maternal salinity treatments under the 12 h photoperiod treatment (Post-hoc Bonferroni test), while different lowercase letters indicate significant difference (P<0.05) among different maternal salinity treatments under the dark treatment (Post-hoc Bonferroni test). F-values are given for the significant effects of maternal salinity (MS), photoperiod (L) and their interaction (MS×L) on mean final germination percentage, represented as FMS, FL and FMS×L, respectively. * means significance at P<0.05 level; ** means significance at P<0.01 level; *** means significance at P<0.001 level (ANOVA).
Fig. 6 Pictorial model indicating the effects of maternal salinity on yield, size and stress tolerance of Suaeda fruticosa seeds. Black circle depicts the seed and the radius indicates the seed size.
[1]   Bankaji I, Cacador I, Sleimi N. 2016. Assessing of tolerance to metallic and saline stresses in the halophyte Suaeda fruticosa: The indicator role of antioxidative enzymes. Ecological Indicators, 64: 297-308.
doi: 10.1016/j.ecolind.2016.01.020
[2]   Bewley J D, Black M. 1994. Seeds. Boston: Springer Press, 1-33.
[3]   Bui E N. 2013. Soil salinity: A neglected factor in plant ecology and biogeography. Journal of Arid Environments, 92: 14-25.
doi: 10.1016/j.jaridenv.2012.12.014
[4]   Di Caterina R, Giuliani M M, Rotunno T, et al. 2007. Influence of salt stress on seed yield and oil quality of two sunflower hybrids. Annals of Applied Biology, 151(2): 145-154.
doi: 10.1111/aab.2007.151.issue-2
[5]   El-Keblawy A, Gairola S, Bhatt A. 2016. Maternal salinity environment affects salt tolerance during germination in Anabasis setifera: A facultative desert halophyte. Journal of Arid Land, 8(2): 254-263.
doi: 10.1007/s40333-015-0023-2
[6]   El-Keblawy A, Gairola S, Bhatt A, et al. 2017. Effects of maternal salinity on salt tolerance during germination of Suaeda aegyptiaca, a facultative halophyte in the Arab Gulf desert. Plant Species Biology, 32(1): 45-53.
doi: 10.1111/psbi.2017.32.issue-1
[7]   El-Keblawy A, Al-Shamsi N, Mosa K. 2018. Effect of maternal habitat, temperature and light on germination and salt tolerance of Suaeda vermiculata, a habitat-indifferent halophyte of arid Arabian deserts. Seed Science Research, 28(2): 140-147.
doi: 10.1017/S0960258518000144
[8]   Epstein E. 1972. Physiological genetics of plant nutrition. In: Mineral Nutrition of Plants: Principles and Perspectives. New York: John Wiley and Sons Press, 325-344.
[9]   Flowers T J, Colmer T D. 2008. Salinity tolerance in halophytes. New Phytologist, 179: 945-963.
doi: 10.1111/j.1469-8137.2008.02531.x pmid: 18565144
[10]   Flowers T J, Galal H K, Bromham L. 2010. Evolution of halophytes: multiple origins of salt tolerance in land plants. Functional Plant Biology, 37(7): 604-612.
doi: 10.1007/s10142-011-0218-3 pmid: 21472467
[11]   Freitag H, Hedge I C, Jaffri S M H, et al. 2001. Chenopodiaceae. Flora of Pakistan 204. Karachi: Missouri Botanical Garden Press and the University of Karachi, 1-218.
[12]   Galloway L F. 2005. Maternal effects provide phenotypic adaptation to local environmental conditions. New Phytologist, 166(1): 93-100.
doi: 10.1111/j.1469-8137.2004.01314.x pmid: 15760354
[13]   Gul B, Ansari R, Flowers T J, et al. 2013. Germination strategies of halophyte seeds under salinity. Environmental and Experimental Botany, 92: 4-18.
doi: 10.1016/j.envexpbot.2012.11.006
[14]   Gulzar S, Khan M A, Ungar I A. 2001. Effect of temperature and salinity on the germination of Urochondra setulosa. Seed Science and Technology, 29: 21-29.
[15]   Guo J, Suo S, Wang B S. 2015. Sodium chloride improves seed vigour of the euhalophyte Suaeda salsa. Seed Science Research, 25(3): 335-344.
doi: 10.1017/S0960258515000239
[16]   Hadi S M S, Ahmed M Z, Hameed A, et al. 2018. Seed germination and seedling growth responses of toothbrush tree (Salvadora persica Linn.) to different interacting abiotic stresses. Flora, 243: 45-52.
doi: 10.1016/j.flora.2018.04.002
[17]   Hameed A, Ahmed M Z, Khan M A. 2006. Comparative effects of NaCl and sea salt on seed germination of coastal halophytes. Pakistan Journal of Botany, 38: 1605-1612.
[18]   Hameed A, Hussain T, Gulzar S, et al. 2012. Salt tolerance of a cash crop halophyte Suaeda fruticosa: biochemical responses to salt and exogenous chemical treatments. Acta Physiologiae Plantarum, 34(6): 2331-2340.
doi: 10.1007/s11738-012-1035-6
[19]   Hameed A, Ahmed M Z, Gulzar S, et al. 2013. Seed germination and recovery responses of Suaeda heterophylla to abiotic stresses. Pakistan Journal of Botany, 45(5): 1649-1656.
[20]   Hameed A, Rasheed A, Gul B, et al. 2014. Salinity inhibits seed germination of perennial halophytes Limonium stocksii and Suaeda fruticosa by reducing water uptake and ascorbate dependent antioxidant system. Environmental and Experimental Botany, 107: 32-38.
doi: 10.1016/j.envexpbot.2014.04.005
[21]   He H, de Souza Vidigal D, Snoek L B, et al. 2014. Interaction between parental environment and genotype affects plant and seed performance in Arabidopsis. International Journal of Experimental Botany, 65(22): 6603-6615.
doi: 10.1093/jxb/eru378 pmid: 25240065
[22]   Holeski L M, Jander G, Agrawal A A. 2012. Transgenerational defense induction and epigenetic inheritance in plants. Trends in Ecology & Evolution, 27(11): 618-626.
doi: 10.1016/j.tree.2012.07.011 pmid: 22940222
[23]   Ievinsh G. 2006. Biological basis of biological diversity: physiological adaptations of plants to heterogeneous habitats along a sea coast. Acta Universitatis Latviensis, 710: 53-79.
[24]   Khan M A, Ungar I A. 1984. The effect of salinity and temperature on the germination of polymorphic seeds and growth of Atriplex triangularis Willd. American Journal of Botany, 71(4): 481-489.
pmid: 19298000
[25]   Khan M A, Ungar I A. 1998. Seed germination and dormancy of Polygonum aviculare L. as influenced by salinity, temperature, and gibberellic acid. Seed Science Technology, 26: 107-117.
[26]   Khan M A, Ungar I A, Showalter A M. 2000. The effect of salinity on the growth, water status, and ion content of a leaf succulent perennial halophyte, Suaeda fruticosa (L.) Forssk. Journal of Arid Environments, 45(1): 73-84.
doi: 10.1006/jare.1999.0617
[27]   Khan M A, Gul B. 2006. Ecophysiology of High Salinity Tolerant Plants. Dordrecht: Springer Press, 11-30.
[28]   Khan M A, Ansari R, Ali H, et al. 2009. Panicum turgidum, a potentially sustainable cattle feed alternative to maize for saline areas. Agriculture, Ecosystems and Environment, 129(4): 542-546.
doi: 10.1016/j.agee.2008.10.014
[29]   Labidi N, Ammari M, Mssedi D, et al. 2010. Salt excretion in Suaeda fruticosa. Acta Biologica Hungarica, 61(3): 299-312.
doi: 10.1556/ABiol.61.2010.3.6 pmid: 20724276
[30]   Lariguet P, Ranocha P, de Meyer M, et al. 2013. Identification of a hydrogen peroxide signalling pathway in the control of light-dependent germination in Arabidopsis. Planta, 238(2): 381-395.
doi: 10.1007/s00425-013-1901-5
[31]   Manzoor S, Hameed A, Khan M A, et al. 2017. Seed germination ecology of a medicinal halophyte Zygophyllum propinquum: responses to abiotic factors. Flora, 233: 163-170.
doi: 10.1016/j.flora.2017.06.004
[32]   Minuto L, Roccotiello E, Casazza G. 2011. New seed morphological features in Moehringia L. (Caryophyllaceae) and their taxonomic and ecological significance. Plant Biosystems, 145(1): 60-67.
doi: 10.1080/11263504.2010.527629
[33]   Moir-Barnetson L, Veneklaas E J, Colmer T D. 2016. Salinity tolerances of three succulent halophytes (Tecticornia spp.) differentially distributed along a salinity gradient. Functional Plant Biology, 43(8): 739-750.
doi: 10.1071/FP16025
[34]   Oueslati S, Ksouri R, Falleh H, et al. 2012. Phenolic content, antioxidant, anti-inflammatory and anticancer activities of the edible halophyte Suaeda fruticosa Forssk. Food Chemistry, 132(2): 943-947.
doi: 10.1016/j.foodchem.2011.11.072
[35]   Pujol J A, Calvo J F, Ramirez-Diaz L. 2000. Recovery of germination from different osmotic conditions by four halophytes from southeastern Spain. Annals of Botany, 85(2): 279-286.
doi: 10.1006/anbo.1999.1028
[36]   Qadir M, Quillérou E, Nangia V, et al., 2014. Economics of salt-induced land degradation and restoration. Natural Resources Forum, 38(4): 282-295.
doi: 10.1111/1477-8947.12054
[37]   Rehman J U, Saqib N U, Akhtar N, et al., 2013. Hepatoprotective activity of aqueous-methanolic extract of Suaeda fruticosa in paracetamol-induced hepatotoxicity in rabbits. Bangladesh Journal of Pharmacology, 8(4): 378-381.
doi: 10.3329/bjp.v8i3.16631
[38]   Samia O, Riadh K, Hanen F, et al. 2011. Phenolic content, antioxidant, anti-inflammatory and anticancer activities of the edible halophyte Suaeda fruticosa Forssk. Food Chemistry, 132(2): 943-947.
doi: 10.1016/j.foodchem.2011.11.072
[39]   Song J, Feng G, Tian C Y, et al. 2005. Strategies for adaptation of Suaeda physophora, Haloxylon ammodendron and Haloxylon persicum to a saline environment during seed-germination stage. Annals of Botany, 96(3): 399-405.
doi: 10.1093/aob/mci196 pmid: 16002418
[40]   Song J, Zhou J C, Zhao W W, et al. 2016. Effects of salinity and nitrate on production and germination of dimorphic seeds applied both through the mother plant and exogenously during germination in Suaeda salsa. Plant Species Biology, 31(1): 19-28.
doi: 10.1111/psbi.2016.31.issue-1
[41]   Towhidi A, Saberifar T, Dirandeh E. 2011. Nutritive value of some herbage for dromedary camels in the central arid zone of Iran. Tropical Animal Health and Production, 43(3): 617-622.
doi: 10.1007/s11250-010-9741-9
[42]   Wang F, Xu Y G, Wang S, et al. 2015. Salinity affects production and salt tolerance of dimorphic seeds of Suaeda salsa. Plant Physiology and Biochemistry, 95: 41-48.
doi: 10.1016/j.plaphy.2015.07.005 pmid: 26184090
[43]   Weber D J, Ansari R, Gul B, et al. 2007. Potential of halophytes as source of edible oil. Journal of Arid Environments, 68(2): 315-321.
doi: 10.1093/aob/mcu194 pmid: 25288631
[44]   Yadav S, Mishra A, Jha B. 2018. Elevated CO2 leads to carbon sequestration by modulating C4 photosynthesis pathway enzyme (PPDK) in Suaeda monoica and S. fruticosa. Journal of Photochemistry and Photobiology B, 178: 310-315.
doi: 10.1016/j.jphotobiol.2017.11.022 pmid: 29175605
[45]   Zhou J C, Fu T T, Sui N, et al. 2016. The role of salinity in seed maturation of the euhalophyte Suaeda salsa. Plant Biosystems, 150(1): 83-90.
doi: 10.1080/11263504.2014.976294
[46]   Zia S, Egan T P, Khan M A. 2007. Population studies of Limonium stocksii (Plumbaginacea) from a salt desert near the Arabian Sea Coast. Communications in Soil Science and Plant Analysis, 38(15-16): 1975-1990.
doi: 10.1080/00103620701548514
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