Limoniastrum guyonianum behavior under seasonal conditions fluctuations of Sabkha Aïn Maïder (Tunisia)

Highlights

• In natural biotope, high salinity resulted a deficit in K⁺, Ca²⁺, and Mg²⁺ content.

• Salinity and/or drought reduced plant water potential and photosynthesis activity.

• Sucrose, fructose, glucose, citrate and malate contribute to the osmoregulation.

• Twenty phenolic compounds were identified in the shoot of L. guyonianum.

• In summer, the environmental factors enhanced phenolic content and antioxidant activity.

Abstract

In Sabkha biotope, several environmental factors (i.e., salinity, drought, temperature, etc.) especially during dry season affect halophytes developments. To cope with these harmful conditions, halophytes use multiple mechanisms of adaptations. In this study, we focused on the effect of environmental condition changes over a year in the Sabkha of Aïn Maïder (Medenine - Tunisia) on the physiological and biochemical behavior of Limoniastrum guyonianum using a modeling approach. Our study showed that the model depicted well (R² > 0.75) the monthly fluctuations of the studied parameters in this habitat. During the dry period (June to September), the salinity of the soil increased remarkably (high level of EC and Na⁺ content), resulting in high Na⁺ content in the aerial parts followed by a nutrient deficiency in K⁺, Ca²⁺, and Mg²⁺. As a result of this disruption, L. guyonianum decreased its water potential to more negative values to maintain osmotic potential using inorganic osmolytes (i.e., Na⁺) and organic osmolytes (i.e., sugars: sucrose, fructose, glucose, and xylitol, and organic acids: citric and malic acids). In addition, CO₂ assimilation rate, stomatal conductance, transpiration rate, and photosynthetic pigments decreased significantly with increasing salinity. The phenolic compounds contents and the antioxidant activity increased significantly in the dry period as a result of increased levels of H₂O₂ and lipid peroxidation. This increase was highly correlated with soil salinity and air temperature. The maintenance of tissue hydration (i.e., moderate decrease of relative water content), the accumulation of sugars and organic acids, the enhancement of phenolic compounds amounts, and the increase of antioxidant activity during the dry period suggest that L. guyonianum possesses an efficient tolerance mechanism that allows the plant to withstand the seasonal fluctuations of climatic conditions in its natural biotope.

Introduction

The Mediterranean region, especially the southern basin, is characterized by a large fluctuation of precipitation in terms of quantity and distribution throughout the year, severe drought, and high temperatures associated with a significant evapo-transpiration favouring the accumulation of salts in the soil. This situation has become more complex with the tangible impact of climate change which increases desertification and soil salinization leading to the restriction of cultivated areas (Abdel Latef, 2010; Rozema and Flowers, 2008). Besides this stressful condition, the overgrazing aggravates the situation of wild plants, some species have disappeared, and others are threatened, growing genetic erosion leading to a huge forage deficit which accentuated desertification phenomenon (Abdellaoui et al., 2017; Aïdoud et al., 2006). These environmental changes have increased marginalized lands generally characterized by low yield and reduced economic income. Currently, the exploitation of these areas has become a necessity (Munns and Tester, 2008). The sustainable and equitable management of these vulnerable ecosystems with high added value can be achieved by valuing plant species chosen according to their degree of adaptation and their ecological and economic importance.

Halophytes have a high tolerance to salinity and could potentially be exploited due to their ecological and economic interests (Abdelly et al., 2006; Laudadio et al., 2009; Nedjimi, 2011) seem to constitute a valuable tool for the creation of productive systems under extreme environmental conditions. Generally, the halophytes dominate the marginal saline areas thanks to their ability to tolerate very high soil salinity and to achieve their life cycle independent of the salt effects, which gives these plants a great important role in the restoration, rehabilitation, and protection of saline biotope (Flowers and Colmer, 2008). Besides, the saline agriculture of many forages and edible halophytes is more and more recommended in recent years (Rozema and Schat, 2013; Salem et al., 2010; Ventura et al., 2015). In saline biotope of arid regions, halophytes are exposed to a set of environmental factors such as severe salinity, drought, high temperature, low precipitation, and high UV-radiation (Chaves et al., 2002; Elnaggar et al., 2020; Souid et al., 2018), which can lead to various abiotic stresses. To counteract the stressful conditions, these plants exhibit a series of complementary potent adequate and effective tolerance mechanisms such as physiological, biochemical, and morpho-anatomical adaptation.

Among the main mechanisms used to cope with saline stress, these can be mentioned: control of Na⁺ and Cl⁻ fluxes, salt vacuolar compartmentalization, salt secretion (secretary glands or hairs) and/or the excretion of excess salt, succulence, the accumulation of compatible osmolytes and organic acids, activation of antioxidant enzymes and the biosynthesis of effective antioxidant compounds (Flowers and Colmer, 2008; He et al., 2019; Yamamoto et al., 2015). Under stressful conditions, osmotic adjustment is a vital strategy for the plant to control osmotic homeostasis between vacuole and cytoplasm, helping to maintain tissue hydration. This osmoregulation is related to the ability of plants to accumulate certain inorganic ions (Na⁺ and Cl⁻) and organic compounds (such as proline, glycine betaine, sugars, and organic acids) to regulate the osmotic potential (Raven, 1985; Shabala and Shabala, 2011; Slama et al., 2015). The stressful environmental conditions also can cause oxidative stress by promoting the reactive oxygen species (ROS) generation (Munns, 2002; Yang and Guo, 2018). To mitigate the oxidative damage (lipids peroxidation, proteins, and DNA degradation) induced by abiotic stress, plants have developed an effective antioxidant defence system that can be of enzymatic nature through the activation of several antioxidant enzymes and/or the accumulation of secondary metabolites (Boughalleb et al., 2020; Isayenkov and Maathuis, 2019). Phenolic compounds like phenolic acids and flavonoids are classified among the most important secondary metabolites that can play an antioxidant role in minimizing the harmful effects of abiotic stress (Falleh et al., 2013; Ksouri et al., 2008; Shafeiee and Ehsanzadeh, 2019). In addition to their role in osmotic adjustment and the protection of plasma membrane integrity, many osmolytes such as proline, glycine betaine, soluble sugars, play a role in scavenging reactive oxygen species (ROS) (Abd El-Maboud and Abd Elbar, 2020; Slama et al., 2015; Szabados and Savouré, 2010).

Limoniastrum guyonianum Boiss belonging to the Plumbaginaceae family growing in the deserts of North Africa especially in Northern Sahara (Algeria, Tunisia) in the salty soils of the great chotts (Quezel and Santa, 1963). This halophyte is characterized by the presence of salt glands that contribute to salt excess excretion (Ding et al., 2010; Yuan et al., 2016). Commonly used for dune stabilization and landscaping (Zouhaier et al., 2015b) also used in folk medicine as anti-dysenteric, antibacterial, antidiabitic (Hammami et al., 2011; Telli et al., 2016). Photochemical studies have shown that this species presents anti-inflammatory and antitumor proprieties (Krifa et al., 2015; Trabelsi et al., 2013). However, no study has been carried out on the impacts of environmental condition changes on L. guyonianum grown in their natural habitats yet. Saline habitats could be subjected; in addition to salinity; to high temperature, drought, flooding, active deflation depending on site and seasons (Al Hassan et al., 2017b; Souid et al., 2018)). Thus, halophytes behavior to their habitats environmental conditions is complex. In our study, L. guyonianum grows in the shott of Sebkha of Aïn Maider – (Boughrara- Medenine, Tunisia), a salt-encrusted plain subjected to periodic flooding (Oueslati, 1992). Consequently, this study aimed to evaluate the monthly physiological and biochemical behavior of L. guyonianum in relation to the environmental conditions of the Sabkha of Aïn Maïder by modeling its response to seasonal climatic conditions over a year and examining the possible relationship between responses changes and the metrolo-edaphic conditions in its natural biotope.