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Effects of Salinity on the Growth, Physiology and Relevant Gene Expression of an Annual Halophyte Grown from Heteromorphic Seeds

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Effects of Salinity on the Growth, Physiology and Relevant Gene Expression of an Annual Halophyte Grown from Heteromorphic Seeds Research Article Effects of salinity on the growth, physiology and relevant gene expression of an annual halophyte grown from heteromorphic seeds Jing Cao†, Xiu Yun Lv†, Ling Chen, Jia Jia Xing and Hai Yan Lan* Xinjiang Key Laboratory of Biological Resources and Genetic Engineering, College of Life Science and Technology, Xinjiang University, Urumqi 830046, China Received: 3 April 2015; Accepted: 6 September 2015; Published: 17 September 2015 Associate Editor: Tim J. Flowers Citation: Cao J, Lv XY, Chen L, Xing JJ, Lan HY. 2015. Effects of salinity on the growth, physiology and relevant gene expression of an annual halophyte grown from heteromorphic seeds. AoB PLANTS 7: plv112; doi:10.1093/aobpla/plv112 Abstract. Seed heteromorphism provides plants with alternative strategies for survival in unfavourable environ- ments. However, the response of descendants from heteromorphic seeds to stress has not been well documented. Suaeda aralocaspica is a typical annual halophyte, which produces heteromorphic seeds with disparate forms and dif- ferent germination characteristics. To gain an understanding of the salt tolerance of descendants and the impact of seed heteromorphism on progeny of this species, we performed a series of experiments to investigate the plant growth and physiological parameters (e.g. osmolytes, oxidative/antioxidative agents and enzymes), as well as expression pat- terns of corresponding genes. Results showed that osmolytes (proline and glycinebetaine) were significantly increased − and that excess reactive oxygen species (O2 , H2O2) produced under high salinity were scavenged by increased levels of antioxidant enzymes (superoxide dismutase, ascorbate peroxidase and glutathione reductase) and corresponding antioxidants (ascorbic acid and glutathione). Moreover, enhancement of phosphoenolpyruvate carboxylase activity at high salt intensity had a positive effect on photosynthesis. The descendants from heteromorphic seeds presented no significant difference in performance with or without salinity. In conclusion, we found that high salinity induced the same active physiological responses in plants from heteromorphic seeds of S. aralocaspica, there was no carry-over of seed heteromorphism to plants: all the descendants required salinity for optimal growth and adaptation to their natural habitat. Keywords: Antioxidative system; descendants from dimorphic seeds; gene expression; physiological response; salinity tolerance; Suaeda aralocaspica. behaviours (Sorensen 1978; Manda´kandPysˇek 2001; Introduction Bra¨ndel 2004, 2007). These adaptations evolved in Seed heteromorphism is a phenomenon in which an indi- response to adverse environments (Imbert 2002). Accord- vidual plant is able to produce different types of seeds ing to seed type, seed heteromorphism can be classified with diverse morphologies or germination and dormancy into di- or polymorphism. In dimorphic seeds, a brown † These authors contributed equally to this work. * Corresponding author’s e-mail address: [email protected] Published by Oxford University Press on behalf of the Annals of Botany Company. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/ licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properlycited. AoB PLANTS www.aobplants.oxfordjournals.org & The Authors 2015 1 Cao et al. — Effects of salinity on plants from heteromorphic seeds seed is usually larger, non-dormant and can germinate Suaeda aralocaspica, the only species of the Borszczo- quickly, but the seedling mortality is much higher (a high- wia section of the genus Suaeda in the Amaranthaceae, risk strategy; Venable 1985a) than a black seed. The latter is a monoecious annual halophyte with a single-cell C4 is smaller, dormant and more sensitive to the environment photosynthesis pathway (Voznesenskaya et al.2001) than the brown seed and can enter the seed bank to com- and which is distributed in saline–alkaline sandy soils in pensate population size in an unpredictable environment the southern margin of Junggar Basin in China (Li 1979; (Venable 1985a). Seed heteromorphism is an important Mao 1994). Plants grow up to 20–50 cm high with unisex- strategy for plants to adapt to environmental stress by ual flowers (Commissione Redactorum Florae Xinjiangensis extending the germination time, minimizing the risk of a 1994) and can produce heteromorphic seeds with dispar- single germination and ensuring the successful expansion ate forms and different germination characteristics of the population (Weber 2009). (Wang et al. 2008).Thebrownseed,withoblateshapeand Besides enhancing the chances of successful germin- soft seed coat, has a size 3.2 × 2.8 × 0.7 mm (length × ation, seed heteromorphism may also have a significant width × height) and can germinate quickly, while the black impact on the growth, physiological characters and stress seed, with elliptical shape and hard seed coat, has a size tolerance of the descendants (Table 1). The seedlings des- 2.5 × 2.3 × 1.4 mm and is dormant. To understand the cended from heteromorphic seeds may present signifi- salt tolerance of the descendants grown from the two cant differences in growth rate and size, which could seed morphs of S. aralocaspica and the impact of seed het- persist throughout the life of the plant or may disappear eromorphism on the progeny, a series of experiments were in the subsequent stages of development (Wang et al. designed to address the following questions: (i) What are the 2010). The non-synchronous germination among hetero- growth, physiological and biochemical responses of the des- morphic seeds usually results in different size of the seed- cendants from dimorphic seeds to long-term NaCl treat- lings. Within a species, although the seeds with relatively ment, as well as changes in gene expression pattern? (ii) Is larger embryos can grow into larger seedlings than those there any different impact of seed heteromorphism on the grown from seeds with smaller embryos, the root-to-shoot progeny with or without salinity? ratio is similar between the two, which suggests that the development of heteromorphic plants is in synchrony Methods (Imbert and Ronce 2001). Seed heteromorphism can also have an effect in descendants in response to stress Seed collection (Table 1). Mature fruits of S. aralocaspica were harvested from plants Previously, the majority of studies have focussed on growing in their natural habitat in a desert saline soil at how environmental factors such as salinity and tempera- the Wujiaqu 103 regiment (44829′821′′N, 87831′181′′E) in ture affect dormancy and germination of heteromorphic October 2010, in Xinjiang, China. Seeds were air-dried at seeds (Khan and Ungar 1984; Khan et al. 2001a, b; Wang room temperature, then cleaned and sieved to remove et al. 2008; Aguado et al. 2011; Li et al. 2011); only a few the impurities and stored at 4 8C, 10–12 % relative humid- attempts have been made to investigate the physio- ity, in brown paper bags for experiments performed logical carry-over on descendant plants under stress between 2011 and 2012. (Redondo-Go´mez et al.2008; Wang et al.2008; Jiang et al.2012). In Suaeda splendens, the seedlings derived Plant growth and salinity treatment from both seed morphs showed little difference in growth Seeds of S. aralocaspica were sown in pots containing and photosynthesis in the presence of high salinity, which perlite : vermiculite (1 : 3) at a temperature regime of was the first report on the carry-over of salinity tolerance 17–22 8C, 10–20 % relative humidity, a natural light from different seed morphs to established seedlings and source of 100–500 mmol m22 s21 and a 12–14 h light/ plants (Redondo-Go´mez et al.2008). To our knowledge, 10–12 h dark photoperiod. Prior to sowing, the black the first report, which linked physiological responses seeds were stratified according to Wang et al. (2008) so with differential gene expression in seedlings derived that seedling emergence was uniform. In short, the from dimorphic seeds, was from Atriplex centralasiatica black seeds were placed on two layers of filter paper on (Xu et al.2011) and in which a molecular description of top of washed quartz sand, which were moistened with differential salt tolerance in dimorphic seeds was provided. distilled water [water : sand ¼ 1.2 : 10 (w/w)] in metal In the present study, we extended these findings to boxes, which were placed in a refrigerator at 4 8Cinthe responses on salt tolerance of the plants from dimorphic dark for 10 days. Subsequently, the brown and black seeds of S. aralocaspica, including morphological, physio- seeds were sown at the same time. Seedlings were culti- logical and biochemical changes, as well as relevant vated with half-strength Hoagland (Arnon and Hoagland gene expression profiles. 1940) solution for 2 months and then treated with 2 AoB PLANTS www.aobplants.oxfordjournals.org & The Authors 2015 Cao et al. — Effects of salinity on plants from heteromorphic seeds Table 1. Different behaviours between descendants grown from heteromorphic seeds under natural habitat and various stress conditions. Environment Species Seed type Descendant behaviour Reference ............................................................................................................................................................................ Natural Agropyron Larger seed/smaller Seedling large/seedling small (difference disappears Zhang
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