Salicylic Acid as a Tolerance Inducer of Drought Stress on Sunflower Grown in Sandy Soil

Global climate change has, undoubtedly, negative impact on crop growth and productivity. This is particularly acute in arid and semi–arid regions (Ahmadi and Souri 2018; Souri and Hatamian 2019), which suffer from water scarcity. Therefore, researchers are making continuous attempts to limit such adverse impacts (Saudy et al. 2020; El–Bially et al. 2022). In conjunction with global warming, drought is expected to become more frequent in many regions of the earth (Pokhrel et al. 2021). Drought is one of the major global factors that reduce yield in many crops worldwide (Nawaz et al. 2015). Due to the severity of various abiotic stresses such as drought, several concerns can threaten crop production (Anderson et al. 2020; Zulfiqar and Hancock 2020). Drought is considered one of the results associated climatic changes, thus it represents a major constraint to crop production universally (Farooq et al. 2012). It has been reviewed that exposure of plants to water stress leads to serious physiological and biochemical dysfunctions (Hayat et al. 2010; Makhlouf et al. 2022). Water deficit during critical growth periods of crops reduces their yield and quality, but, however, crops differ in their response to water stress at a given growth stage (El–Bially et al. 2018).

Sunflower (Helianthus annuus L.) is a high yielding oilseed crop and has the potential to bridge up the gap existing between consumption and domestic production of edible oil in Egypt. Sunflower is often reported as a drought–tolerant crop given its high capacity to extract water from the subsoil (Garcia–Vila and Fereres 2012). It has good potential for drought tolerance because of its well–developed root system and to withstand temporary wilting. However, sunflower production is greatly affected by drought (Siddique et al. 2020). It has been reported that sunflower productivity decreases with increasing drought levels (Erdem et al. 2006; Manivannan et al. 2007; Nezami et al. 2008; Siddique et al. 2020; Saudy et al. 2020). Periods of water deficit at any growth stage can cause canopy senescence with subsequent reduction in seed yield (Garcia–Vila and Fereres 2012). Sunflower productivity is mightily regulated by the availability of water and greatest yield losses manifest when water shortage occurs (Yawson et al. 2011).

Under abiotic stresses as drought, synthesizing of protectants by plants is a crucial act in inducing defense responses (Ozturk et al. 2021). In this respect, the endogenous biosynthesis of salicylic acid (SA), as a plant hormone (Smith et al. 2017), is affected by drought (La et al. 2019; Park et al. 2021). In various crops subjected to water deficit conditions, SA had the potentiality to regulate photosynthesis and antioxidant enzymes (Abdelaal 2015), as well as induce proline metabolisms, and antioxidant defense systems (Khan et al. 2014). Use of SA significantly mitigated the adverse impacts of drought and reduced lipid peroxidation (Kang et al. 2013). Therefore, environmental stressed–plant growth was enhanced by exogenous application of SA (Chavoushi et al. 2019; Abbaszadeh et al. 2020).

The relationship between the defense mechanism against drought and the protective impact of salicylic acid on sunflower still requires more investigations. We hypothesized that there is a definite rate of SA which could have the ability to change the fate of some plant physiological events to cope the different levels of drought stress (moderate or severe). Accordingly, the present study was carried out to investigate the effect of irrigation regimes on sunflower performance and for exploring to what extend salicylic acid at different rates can improve the drought tolerance.

Since drought causes changes in molecular, biochemical, physiological, and morphological aspects resulting in negative effects on plant growth and development (Nam et al. 2020; Taha et al. 2020; Babaei et al. 2021; El–Metwally and Saudy 2021; El–Metwally et al. 2021; Salem et al. 2022), injurious impacts of water deficit on different sunflower traits were occurred (Table 3, 4 and 5). The present study confirmed the negative impact of water deficit/on plant physiological status. Owing to the relationship between the plant biochemical compounds and deficit water, drought stress led to degradation of photosynthesis pigments (chlorophylls and carotenoids), as well as accumulation of proline (Table 3). Such findings are in accordance with those recorded by Manivannan et al. (2007) and Saudy et al. (2021) who reported that subjecting sunflower plants to water deficit caused decreases in total chlorophyll and carotenoids and increases proline content in leaves. During drought, reactive oxygen species (ROS) accumulate, which are toxic at elevated levels, due to reduced electron transport chain activity (Hasanuzzaman et al. 2020). Overproduction of ROS is concomitant to various abiotic stresses (Gill and Tuteja 2010; Hossain et al. 2014; Souri et al. 2019; Hatamian et al. 2020). ROS react with and deteriorate nucleic acids (DNA), proteins, photosynthetic pigments, and membrane lipids (Zulfiqar and Ashraf 2021). Elevated ROS levels lead to inactivation of proteins and inhibit the activity of multiple enzymes involved in metabolic pathways, and result in oxidation of lipids and DNA (Hossain et al. 2014). Consequently, ROS can damage membrane and other essential macromolecules (such as photosynthetic pigments, proteins, DNA and lipids), so reducing contents of chlorophylls and carotenoides as shown under drought stress (Table 3). However, plants have natural defense systems involving non–enzymatic and enzymatic antioxidants that efficiently ameliorate the negative impacts of excessive ROS (Zulfiqar and Ashraf 2021). Moreover, plants acclimate to ROS–induced stress by producing various beneficial compatible solutes, such as proline and glycine betaine (Shemi et al. 2021). Subjecting sunflower plants to drought stress increases proline content while reduced the activity of proline oxidase in leaves (Manivannan et al. 2007). Content of chlorophyll, which is one of the major chloroplast components for photosynthesis, has a positive relationship with photosynthetic rate (Anjum et al. 2011). Degradation in photosynthetic pigments can directly limit photosynthetic potential which adversely affects plant productivity. The decrease in chlorophyll content under drought stress may be the result of pigment photo–oxidation and chlorophyll degradation. Photosynthetic pigments of plants are important for harvesting light and production of reducing powers (Anjum et al. 2011). Accordingly, marked reductions were exhibited in leaf area, head diameter, seed yield/head, seed index, seed yield ha⁻¹, seed oil content and iodine value (Table 4) as well as water use efficiency (Fig. 1) of sunflower subjected to drought stress. Many researchers have reported decreasing performance of sunflower growth under water stress conditions (Erdem et al. 2006; Nezami et al. 2008). Water deficit reduces sunflower yield and quality (El–Bially et al. 2018; El–Metwally et al. 2022). Following drought, stomata close progressively with a parallel decline in net photosynthesis and water–use efficiency (Anjum et al. 2011). The closure of stomata significantly decreases the photosynthetic and transpiration rate (Jaleel et al. 2007) and negatively influences the crop growth and productivity (Du et al. 2010). Drought stress significantly decreased all the photosynthetic parameters, i.e. net photosynthetic rate, stomatal conductance, internal carbon dioxide concentration, as well as water use efficiency (WUE) and transpiration rate (Hayat et al. 2008). The lack of photosynthetic pigment contents in the leaves (Table 3), under stresses, leads to a decrease in the efficiency of photosynthesis, which in turn affects the productivity and decrease seeds oil content of sunflower plants (Saudy et al. 2021). Moreover, the harmful effect of drought could be attributed to reduce the availability of nutrients in soil with disturbance in plant nutritional status associated low water supply (Saudy and El–Metwally 2019; Mubarak et al. 2021; Salem et al. 2021; Abd–Elrahman et al. 2022).

Not only SA had a beneficial effect on plant growth and development under water stress conditions but also under normal water supply. In this respect, SA is one of the main plant growth regulators that play a vital role in controlling and modulating photosynthesis under both normal and stressful condition (Arif et al. 2020). SA has key role in enhancing photosynthesis by upregulating photosynthetic enzyme and carbohydrate metabolism (Khodary 2004). SA application increased photosynthetic activity, chlorophyll content, and enzyme activity under both normal and stress conditions (Li et al. 2014). Therefore, total chlorophyll and carotenoids increased while proline content decreased with SA supply under every irrigation level (Table 3). Such findings may be reflected and interpreted, partially at least, the enhancements achieved in sunflower growth and productivity due to exogenous application of SA. The enhancement in sunflower growth with application of SA could be attributed to the role of SA in maintenance the photosynthetic machinery and activity, then promoting the plant growth. SA, which is a plant hormone (Davies 2010) is a multifaceted plant growth regulator which participates in a wide range of growth, metabolism and defense systems; it acts a typical plant hormone modulating all plant responses and providing plant immunity against various stresses (Arif et al. 2020). SA enhances various physiological processes like photosynthesis, chlorophyll and other pigment, plant growth and development, and flowering (Arif et al. 2020). SA plays a key role in providing tolerance to the plants exposed to water stress, i.e. drought or flooding (Hayat et al. 2010). Exogenous application of SA facilitates growth; and flowering; up–regulates photosynthesis; increases the activity of enzymatic and non–enzymatic antioxidants (Arif et al. 2020). Additionally, the generation of ROS during drought stress requires up–regulation of detoxification systems such as super oxide dismutase (SOD) and catalase enzymes and biosynthesis of ROS scavengers (You and Chan 2015). Herein, SA enhances the activities of antioxidants enzyme system i.e. ascorbate peroxidase (APX) and superoxide dismutase (SOD) with a concomitant decline in the activity of catalase (CAT), and can protect and enhance the enzymes of nitrate metabolism under stressful environments (reviewed by Hayat et al. 2010). Also, SA enhances the activity of ROS scavenger enzymes, participates in eliciting abiotic stress responses such as drought (Arif et al. 2020), Application of SA in drought–stressed plants resulted in growth recovery, increased photosynthesis, and reduced oxidative stress (Zulfiqar et al. 2021). Therefore, foliar application of SA improved leaf area, head diameter, seed yield/head, seed index, seed yield ha⁻¹ (Table 4), oil seed content and iodine value (Table 5) as well as WUE (Fig. 2) of sunflower. Also, WUE increases with alleviating water stress by applying SA (Fig. 3). Thus, the maximal values of WUE were recorded with WR_100% × SA_1.0, followed by that of WR_100% × SA_0.5. These findings could be owing to producing seed yields under such conditions more than under other ones, resulting in higher WUE values. At low WUE, photosynthetic carbon assimilation is decreased due to decreasing flow of CO₂ into mesophyll tissue and the closure of stomata (Chaves et al. 2003; Flexas et al. 2004). Following drought, stomata close progressively with a parallel decline in net photosynthesis and WUE (Anjum et al. 2011). Moreover, different concentrations of SA increased total leaf chlorophyll content, photosynthesis and stomatal conductance under normal and stress conditions (Bastam et al. 2012; Ghasemzadeh and Jaafar 2013). SA stimulated CO₂ fixation and efficiency of photosynthetic quantum (Poór et al. 2011). SA also helped to ignite photosynthetic process by closing stomata and by suppressing or slowing electron transport metabolism of PSII (Janda et al. 2012). Photosynthesis, stomatal conductance, gaseous exchange, CO₂ assimilation rate, and chlorophyll content were enhanced after applying SA (Babar et al. 2014). SA elevated photosynthetic rate by facilitating carboxylation rate, chlorophyll amount that is SPAD values and by increasing turgor (Tahjib–Ul–Arif et al. 2018). Additionally, SA increased the chlorophyll, carotenoid, nitrogen, potassium and phosphorus level and nitrate reductase activity (Hashmi et al. 2012). It also maintains membrane integrity of chloroplast membrane (Huang et al. 2016).

It is interesting to conclude that salicylic acid has a substantial role for ameliorating growth and yield of sunflower. Such effect was more pronounced under water deficit, where salicylic acid partially alleviated the detrimental impact of low irrigation level. The current study proved that salicylic acid could be regarded as an inducer for drought tolerance. In this respect, compared to the farmer common practice (WR_100% × SA_0.0), SA_0.5 and SA_1.0 alleviated the yield losses from 21.0% to 15.8 and 14.4% as well as 46.2% to 40.8 and 40.1% under lowering water supply by 15 and 30%, respectively. The global climatic changes and water scarcity, as in arid and semi–arid regions, often obligate farmers to irrigate the crops using water amounts less than required or optimum. This means subjecting crop plants to drought stress, leading to yield losses. Therefore, inserting the plant growth regulator salicylic acid as a save and cheap practice in drought–imposed sunflower cultivation has become important to relatively alleviate the associated deleterious of water deficit.