Elsevier

Flora

Volume 273, December 2020, 151705
Flora

Highlighted Student Research
Physiological responses of the xerohalophyte Suaeda vermiculata to salinity in its hyper-arid environment

https://doi.org/10.1016/j.flora.2020.151705Get rights and content

Highlights

  • Physiological and biochemical stress markers were evaluated in field growing Suaeda vermiculata from different habitats

  • Chlorophyll a, b, carotenoids and leaf succulence showed differences with respect to habitats.

  • Antioxidant enzymes (CAT, APX, GPX) were higher in roots from highly saline site.

  • Lipid peroxidation and hydrogen peroxide varied according to the salinity level.

  • Sodium accumulation indicates its potential role as osmoregulators from heterogenic environment.

Abstract

Few plants can survive and grow equally well in salty and salt-free substrates (i.e., habitat-indifferent halophytes). Such plants provide a good opportunity to understand physiological and biochemical mechanisms underlying salinity tolerance. In this study, we investigated the environmental salinity impacts on several physiological and biochemical features of Suaeda vermiculata, a habitat-indifferent halophyte. Samples of different organs were collected from S. vermiculata from both a highly saline marsh habitat (HSMH) and non-salty gravel plain (NSGP) for the determination of the following physiological and bio-chemical features: chlorophyll and carotenoids, proline, malondialdehyde (MDA), and hydrogen peroxide (H2O2), antioxidant enzymes (Catalase, CAT; guaiacol peroxidase, GPX; Ascorbate peroxidase, APX) activities. Elemental compositions in soil and plant samples from both habitats were also assessed. Results showed that plants from HSMH had significantly lower values of chlorophyll a, b, carotenoids and leaf biomass, compared to those from NSGP. Roots from HSMH attained higher levels of antioxidant enzymes (CAT, GPX, APX) and lower values of reactive oxygen species (MDA and H2O2), indicating that the enzymes are more likely scavenging the reactive oxygen species (ROS). The enzyme activities and ROS levels were much lower in the shoots of both HSMH and NSGP than in roots. Accumulation of sodium was higher in leaves and shoots than roots of S. vermiculata. This study indicates that Suaeda vermiculata is a salt tolerant plant with adaptations to different environments through down-regulation of different biochemical and physiological features to avoid oxidative stress.

Introduction

Effects of salinity on plants include decreased growth, productivity and even death. Specifically, the salt environment could have direct harmful effect to the roots cell growth and associated metabolism. Accumulation of ions such as sodium and chloride within the plant lead to osmotic and / or ion-specific toxicity effects. The accumulation of ions within the plant compromises enzyme functions and disrupts metabolic processes (Munns and Tester, 2008; Hussain et al., 2016). This is mainly due to the production of reactive oxygen species (ROS), such as superoxide anion radicals, hydrogen peroxide and hydroxyl radicals. ROS are formed when electrons with high-energy state are transferred to molecular oxygen (Apel and Hirt, 2004; Flowers and Colmer, 2015; Ma et al., 2019). In order to counteract the toxic effects of ROS, plants usually produce complex defense mechanisms, which include the production of both enzymatic and non-enzymatic antioxidants (Apel and Hirt, 2004; Bose et al., 2014). The enzymatic antioxidative defense system includes guaiacol peroxidase (GPX), catalase (CAT), ascorbate peroxidase (APX), superoxide dismutase (SOD), and non-enzymatic antioxidants include ascorbic acid, α-tocopherol, carotenoids, flavonoids, and the osmolyte proline (You and Chan, 2015; Ismail et al., 2016). The antioxidants capture ROS and detoxify them by inactivation or scavenging mechanisms (You and Chan, 2015).

Drought exaggerates the salinity stress in salty substrates of arid and semi-arid deserts, where both stresses are common phenomena (Rengasamy, 2002; Yadav et al., 2011). Therefore, plants have largely developed several mechanisms that allow them to tolerate the decrease in water potential resulting from soil salinity and drought stresses (Munns and Tester, 2008). In order to overcome drought and salinity stresses, halophytes control the uptake and compartmentalization of elements such as Na, K and Cl and the synthesis of organic ‘compatible’ solutes (Carillo et al., 2011; Ismail et al., 2016). In addition, the accumulated elements play a crucial role in plant growth and development in response to environmental stress. For example, when Na level increases in plant tissues, it hinders the absorption, uptake and translocation of other essential minerals (Hu and Schmidhalter, 2005). Several authors reported that, under salt stress, other elements such as Ca relocate Na from the root cell plasmalemma, and thus contribute to significant reduction in the influx of ions into the cytoplasm (Munns and Tester, 2008; Hussain et al., 2016). White et al. (2017) assessed Na accumulation in the shoot system of 334 species of Caryophyllales order, to which Suaeda vermiculata belongs, grown in a non-saline medium of a hydroponic system and found that a disproportionate number of these species behave as Na-hyperaccumulators. These authors have identified Na-hyperaccumulators as those which accumulate abnormally large amounts of Na in their shoot (>4 mg Na/g dry matter) when grown in non-saline habitats (<20 mM Na in the rhizosphere solution). It has been reported that Na compartmentalizes in vacuoles to avoid inhibition of enzymes in the cytoplasm and also helps to tolerate the excess sodium accumulation in cytoplasm (Flowers and Colmer, 2015; Shabala, 2013). In addition, it has been reported that Na could be used directly for osmotic adjustment in different halophytes such as Atriplex canescens and Sesuvium portulacastrum, Distichlis spicata and Suaeda aegyptiaca, to cope with water deficit (Sabzalian et al., 2018). Several authors demonstrated that Na is an essential element required in cellular homeostasis and also serves as osmo-regulator under stress condition in different halophytes (Balnokin et al., 2005; Pilon-Smits and LeDuc, 2009; Ismail et al., 2016; Elnaggar et al., 2020).

Halophytes and xerophytes are distinguished groups in arid deserts since they possess special adaptations that can help them tolerating salt and drought stresses (Balnokin et al., 2005; Sabzalian et al., 2018). Halophytes and leaf succulent xerophytes often dominate in dry and salt-degraded marginal environments of arid zones because of their ability to tolerate salinity and drought (Jiménez-Becker et al., 2019). Studying the morphological, physiological and biochemical attributes of halophytic plants relative to habitat salinity could be a good tool for understanding how these plants can tolerate both drought and salinity stresses (Volkov and Flowers, 2019; Shoukat et al., 2020; Bueno et al., 2020). A meticulous research into this topic could help physiologists, biochemists and molecular biologists to understand tolerances of halophytes to salinity and drought in dry habitats differing in salinity level.

Halophytes differ in their tolerance to salinity. Whereas true halophytes (commonly named obligatory or euhalophytes) grow only in salty habitats, facultative halophytes can grow and survive on salty soils, but their optimal growth takes place in soils that are free of salt or at least contain low-salt substrates (Rozema, 1996; Rozema and Schat, 2013). In addition, other groups of halophytes called “habitat-indifferent halophytes” are still able to cope with salinity, but they survive equally well in both saline and non-saline soils (Cushman, 2001). Several habitat-indifferent halophytes were reported to survive in both hyper-saline and non-saline soils of the arid Arabian deserts. Among these are Anabasis setifera (El-Keblawy et al., 2016a,b), Aeluropus lagopoides (Bhatt et al., 2020), Salsola drummondii (Elnaggar et al., 2019; El-Keblawy et al., 2020), Suaeda aegyptiaca (El-Keblawy et al., 2017a) and Suaeda vermiculata (El-Keblawy et al., 2018; Al-Shamsi et al., 2018). Several studies have assessed the impact of salinity stress on halophytes growing in different salinity levels under controlled conditions in the labs or for plants collected from one habitat type (Munns and Tester, 2008; Flowers and Colmer, 2015). However, few studies assess the impacts of salinity tolerance on morphological, physiological and biochemical strategies of habitat-indifferent halophytes. Therefore, the objective of this study was to evaluate the tissue-specific strategies of S. vermiculata to deal with ion toxicity under different environments (highly saline marsh and non-salty gravel plain) for plants growing in the field. Studying a habitat-indifferent halophyte that is evolutionary developed and survives under different salinity conditions could provide insights about mechanisms of salt tolerance. We hypothesize different physiological and biochemical responses in the habitat-indifferent S. vermiculata to the salinity level of the two habitats. We assume that the plants of the highly saline marsh habitat rely more on inorganic ions, especially sodium, as osmoregulator, but those of the non-salty gravel plain rely more on organic osmoregulators such as proline. We also expect a differential response to high salinity in the roots and shoots of plants growing in the HSMH; the roots are in direct contact to high salt levels, but leaves could be adapted through Na compartmentalization in vacuoles.

Section snippets

Description of the study sites

The study sites are located at the northeast coast of the United Arab Emirates (UAE) near Kalba city. The sites differ in salinity, soil texture and plant community structure. One site is a highly saline marsh habitat (HSMH) (24° 59′ 09′′ N, 56° 21′ 22′′ E) and other is a non-salty gravel plain (NSGP) (25° 01′ 24" N, 55° 21′ 31" E). The study did not involve any danger or harm to the ecosystem and did not include endangered or protected species. Climate of this region is described as typical

Variation in salinity and elemental composition in soils and plants

Salinity and EC attained significantly higher values in the HSMH, as compared with the NSGP; they were more than 10-folds higher in HSMH than in NSGP (Tables 1A and 2). The pH, however, did not differ between the two habitats (Table 2). The concentrations of the macronutrients Na, K and Ca were significantly higher (P < 0.05, Table 1a) in HSMH soils, as compared to the NSGP soils by a factor of 3.7, 3.0 and 1.7, respectively. On the other hand, concentrations of Mg, Fe, Mn and Zn were greater

Discussion

In the hyper-arid climate of the Arabian Peninsula, drought and salinity are main stress factors that impede the physiological and biochemical traits of plants and ultimately can affect plant distribution (El-Keblawy et al., 2017b; Ma et al., 2019). However, halophytic plants can adjust their biochemical and cellular phenomena to avoid or escape such environmental stresses. In this study, we found that S. vermiculata adjusted several physiological and biochemical attributes to survive in both

Conclusion

The present research showed that the habitat type (saline and non-saline) influences the morpho-physiological attributes of S. vermiculata in the hyper-arid UAE desert. The high salinity triggered greater production of H2O2 in roots of plants from the highly saline marsh habitat (HSMH) compared to those of the non-salty gravel plain (NSGP). The high level of proline in roots of HSMH and in shoots of NSGP implies that the role of proline differs according to habitat and organ. Higher

Credit Author Statement

NAS performed all the experiments. NAS, MIH, and designed and carried out the experiment and evaluations. AEK designed and supervised the project. MIH and AEK wrote, corrected and finalized the manuscript.

Data Availability

Available data are presented in the manuscript.

Author Contributions

NAS performed all the experiments and helped in drafting the manuscript. AEK designed and supervised the project. MIH and AEK wrote, corrected and revised the final version of the manuscript.

Funding

This study was partially supported by the Research Office of the University of Sharjah, to Environmental and Chemical Biology Research Group.

Declaration of Competing Interest

The authors declare that the research was conducted in the absence of any commercial or financial means that could be construed as a potential conflict of interest.

Acknowledgments

We are grateful to Dr. Attiat Elnaggar her assistance in the lab and field works.

References (70)

  • J. Rozema et al.

    Salt tolerance of halophytes, research questions reviewed in the perspective of saline agriculture

    Environ. Exp. Bot.

    (2013)
  • E. Shoukat et al.

    Short and long term salinity induced differences in growth and tissue specific ion regulation of Phragmites karka

    Flora

    (2020)
  • L. Szabados et al.

    Proline: a multifunctional amino acid

    Trends Plant Sci

    (2010)
  • V. Velikova et al.

    Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines

    Plant Sci

    (2000)
  • Y. Wang et al.

    Effects of salt, alkali and salt–alkali mixed stresses on seed germination of the halophyte Salsola ferganica (Chenopodiaceae)

    Acta Ecol. Sinica

    (2013)
  • M. Al Hassan et al.

    Antioxidant responses under salinity and drought in three closely related wild monocots with different ecological optima

    AoB Plants

    (2017)
  • M. Al Hassan et al.

    Stress tolerance mechanisms in Juncus: responses to salinity and drought in three Juncus species adapted to different natural environments

    Funct. Plant Biol.

    (2016)
  • N. Al-Shamsi et al.

    Drought tolerance and germination response to light and temperature for seeds of saline and non-saline habitats of the habitat-indifferent desert halophyte Suaeda vermiculata

    Acta Physiol. Plant.

    (2018)
  • K. Apel et al.

    Reactive oxygen species: metabolism, oxidative stress and signal transduction

    Annu. Rev. Plant Biol.

    (2004)
  • A. Arzani et al.

    Smart engineering of genetic resources for enhanced salinity tolerance in crop plants

    Crit. Rev. Plant Sci.

    (2016)
  • Y.V. Balnokin et al.

    Significance of Na+ and K+ for sustained hydration of organ tissues in ecologically distinct halophytes of the family Chenopodiaceae

    Russ. J. Plant Physiol.

    (2005)
  • L.S. Bates et al.

    Rapid determination of free proline for water-stress studies

    Plant Soil

    (1973)
  • A. Bhatt et al.

    Effects of light, temperature, salinity, and maternal habitat on seed germination of Aeluropus lagopoides (Poaceae): an economically important halophyte of arid Arabian deserts

    Botany

    (2020)
  • J. Bose et al.

    ROS homeostasis in halophytes in the context of salinity stress tolerance

    J. Exp. Bot.

    (2014)
  • P. Carillo et al.

    Salinity stress and salt tolerance

  • J.C. Cushman

    Osmoregulation in plants: implications for agriculture

    Am. Zool.

    (2001)
  • J.C. Cushman et al.

    Large-scale mRNA expression profiling in the common ice plant, Mesembryanthemum crystallinum, performing C3 photosynthesis and Crassulacean acid metabolism (CAM)

    J. Exp. Bot.

    (2008)
  • W.C. Dahnke et al.

    Measurement of soil salinity

    Recommended chemical soil test procedures for the North Central Region

    (1988)
  • K. Das et al.

    Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants

    Front. Environ. Sci.

    (2014)
  • K. Dehan et al.

    Salt tolerance of the wild relatives of the cultivated tomato: Responses of Solanum pennellii to high salinity

    Irrig. Sci.

    (1978)
  • J.N. Egilla et al.

    Drought stress influences leaf water content, photosynthesis, and water-use efficiency of Hibiscus rosa-sinensis at three potassium concentrations

    Photosynthetica

    (2005)
  • A. El-Keblawy et al.

    Maternal habitat affects germination requirements of Anabasis setifera, a succulent shrub of the Arabian Deserts

    Acta. Bot. Bras.

    (2016)
  • A. El-Keblawy et al.

    Maternal salinity environment affects salt tolerance during germination in Anabasis setifera: a facultative desert halophyte

    J. Arid Land

    (2016)
  • A. El-Keblawy et al.

    Effect of maternal habitat, temperature and light on germination and salt tolerance of Suaeda vermiculata, a habitat-indifferent halophyte of arid Arabian deserts

    Seed Sci. Res.

    (2018)
  • A. El-Keblawy et al.

    Effects of maternal salinity on salt tolerance during germination of Suaeda aegyptiaca: a facultative halophyte in the Arab Gulf desert

    Plant Species Biol

    (2017)
  • Cited by (12)

    • Anatomical and physiological systematics of Capparis decidua (Forsskal.) Edgew from different habitats of Cholistan Desert, Pakistan

      2022, Biochemical Systematics and Ecology
      Citation Excerpt :

      Increased sclerification is a characteristic property of many salt-tolerant plant species and is vital in minimizing water loss (Keshavarzi 2020). Ion accumulation in the plant inhibits enzyme functioning and interrupts metabolic processes (Al-Shamsi et al., 2020). Several authors have observed that during salt stress, other components such as Ca move Na from the root cell plasmalemma, resulting in a considerable decrease in ion influx into the cytoplasm (Munns and Tester, 2008).

    • Impacts of osmopriming on mitigation of the negative effects of salinity and water stress in seed germination of the aromatic plant Lavandula stoechas L.

      2022, Journal of Applied Research on Medicinal and Aromatic Plants
      Citation Excerpt :

      Several studies have compared the effect of salinity and water deficit and reported a greater harmful effect of salinity than iso-osmotic PEG on seed germination of species, such as Ceratonia siliqua (Cavallaro et al., 2016), Henophyton deserti (Gorai et al., 2014), and Prosopis juliflora (Aljasmi et al., 2021). However, the harmful effect of the PEG was greater than that of NaCl in other species, including Suaeda vermiculata (Al-Shamsi et al., 2020; El-Keblawy et al., 2018) and Haloxylon stocksii (Rasheed et al., 2019). The negative effects of salinity on seed germination occur either through creating a lower osmotic potential that reduces water imbibition and/or through ion-specific toxicity (Carillo et al., 2011; Bewley and Black, 2012; Safdar et al., 2019).

    • Inhibitory mechanism of low-oxygen-storage treatment in postharvest internal bluing of radish (Raphanus sativus) roots

      2021, Food Chemistry
      Citation Excerpt :

      Therefore, increased CAT, GPX, and APX expression led to the decreased H2O2 and O2− levels observed in this study. These findings are in agreement with those of a previous study, which indicated that CAT, GPX, and APX are involved in scavenging ROS (Al-Shamsi, Hussain, & El-Keblawy, 2020) and therefore prevent oxidative color changes (Wang, Yang, Zhao, & Zhang, 2020; Zhou, Wang, Gu, Ma, & Yang, 2020). A previous study indicated that 24-epibrassinolide induces POD, CAT, and APX activity and suppresses ASA loss (Gao, Chai, Cheng, & Cao, 2017).

    View all citing articles on Scopus
    View full text