Abstract
Abiotic stress factors such as drought, flooding, cold, heat waves, ultra violet radiations, oxidizing agents and salinity in the current era of climate change is jeopardizing the plant growth and development leading to crop failure worldwide. Engineered plants with improved tolerance to abiotic stresses would provide opportunities to adapt crops to future climates coupled with enhanced food productivity and sustainable agricultural development. Growth and development of plants involve a wide range of sophisticated genetic, hormonal, metabolic and environmental events which are tightly regulated by internal and external cues, such as phytohormones (including various biostimulants and different organic and inorganic elicitors), temperature, light irradiation, etc. Out of these, phytohormones such as jasmonates, gibberellins, abscisic acid, brassinosteroids, nitric oxide, salicylic acid, etc. have evolved to control vital functions in regulating various plant physiological and developmental processes, ranging from seed germination, photosynthesis, leaf senescence, pollen growth, to plant defense responses, and ameliorating various abiotic stresses. The role of such phytohormones in conferring plant adaptation under dynamic climate changes is still in infancy stage. Few reports are available on the current topic. In this chapter, we attempt to summarize recent studies that have provided insights of the plant environmental adaptability and the multidimensional role of different phytohormones viz. salicylic acid (SA), nitric oxide (NO) and hydrogen sulphite (H2S) in regulating various developmental processes and stress tolerance, taken together with the molecular mechanisms of phytohormone signalling.
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28.1 Introduction
According to an estimate of Food and Agricultural Organization [FAO] (2009), the aim of world agriculture for increasing the 70% food production by the year 2050 for approximately 2.3 billion newborn populations is facing a great hurdle in the light of hunger, poverty coupled with the dynamic environmental factors and over-exploitation of natural endowments. A global emerging problem in current times is climate change and global warming which can be considered as ‘global warning’ to plant stress physiologists as well. A variation in global climate is further supposed to accelerate as global climatic projections indicate a significant increase of 2–4 °C in mean temperature over the next half of the present century (IPCC Intergovernmental Panel on Climate Change 2007). A global level, agriculture is widely considered as one of the prime prone sectors affected by a change in climatic conditions (Abbas 2013). Climate change and agriculture are correlated, as a change in climate of a particular region is the main reason of biotic and abiotic stresses, which pose severe impact on the agriculture. Changing environmental pattern and variability in climate accelerate the impacts of abiotic stresses in crop plants (Thornton et al. 2014; Raza et al. 2019). The crop productivity improvement under abiotic stress is one of the biggest and prime challenges faced by the agricultural scientific community worldwide. Despite extensive research being done in the field, the research for yielding abiotic stress-resistant crops remains very scanty. This can be attributed to the complex nature of environment × genotype interactions and particularly, the capacity to quantify the dynamic physiological response profile of crop plants to a dynamic environment (Moshelion and Altman 2015; Dalal et al. 2019).
Abiotic stress factors such as salinity, drought, heavy metals, UV-B radiation, air pollution and heat stress will further intensity these effects (Khan et al. 2015; Pereira 2016; Wani et al. 2018; Ali et al. 2019) and may strongly impact yield of crop plants and quality of agricultural products (Knutti et al. 2016; Pereira 2016; Feller et al. 2017). Efforts have been made to know potential tolerance mechanisms and plant response under such stressed conditions. As plants are sessile organisms, they continuously encounter different environmental pressures at morphological, physiological, biochemical and molecular levels. Plants have to adapt to these abiotic stresses induced adverse impacts at cellular and subcellular levels to optimally perform the growth and development. Under the danger of climate change, the adaptive underlying mechanisms of plants should perform optimally to counter these challenges. Nevertheless, these adaptive mechanisms can be engineered by exogenous application of phytohormones. In the present chapter, an attempt is made to exploit the tendency of external application of some phytohormones in different crop plants to boost their tolerance against environmental pressures. In the following section, we are discussing the potentiality of hydrogen sulphide, nitric oxide, and salicylic acid mediated mechanisms in countering salinity, drought, heat and metal stress in different species of plants.
28.2 Hydrogen Sulphide (H2S)
Hydrogen sulphide (also known as dihydrogen sulphide or sulfane), is a chemical compound with the chemical formula H2S. It is a colourless gas, with a characteristic foul odour of rotten eggs. Production of H2S involves microbial (usually by sulphate reducing microorganisms) breakdown of organic matter in an anaerobic condition, such as sewers and sewages. H2S is a new gaseous signalling molecule that have different sources and subcellular compartments generally associated with cysteine metabolism in a plant body (Gotor et al. 2013; Scuffi et al. 2014; Birke et al. 2015; Corpas et al. 2019a) that tends to regulate physiological process in plants (Li et al. 2016a; Mostofa et al. 2015; Banerjee et al. 2018; Corpas et al. 2019b) and have tendency to show adaptation to various environmental stresses which includes heavy metal exposure, temperature, drought and salt stresses (Lisjak et al. 2013; Li et al. 2016b; He et al. 2018). H2S can likely exert anti-inflammatory, antioxidant, cyto-protective, antiapoptotic and organ protective effects, further improving environmental stress tolerance of cells (Yuan et al. 2017). It was believed to be a toxic gas and tend to have hazardous effects on environment but by recent several researches it has emerged as an important molecule that helps in signalling with numerous effects on various physiological processes both related to plants as well as animal systems. After nitric oxide (NO) and carbon monoxide (CO), H2S has been recognized as the third endogenous gaso-transmitter in plants. Hydrogen sulphide plays a vital role in cell signalling pathways by being an important component. In plants, H2S generation can be related to cysteine (cys) metabolism (Papenbrock et al. 2007). D-Cys desulfhydrase (D-CDES) and L-Cys desulfhydrase (LSD) derogate cysteine to hydrogen sulphide, ammonia and pyruvate and hence are responsible for the release of H2S into cell (Kopriva 2006). Moreover, participation of H2S in ethylene-induced stomatal closure has also been proven. Increase in glutathione level, alterations of enzyme activities and influences on both NO and H2O2 metabolisms are some of the intracellular effects of H2S. Recent studies have also showed that in regulation of proharvest senescence of horticulture H2S plays an important role. In the accompanying section, the role of H2S under various abiotic stresses is discussed briefly.
28.2.1 Role of H2S in Salt Stress
Salt stress is included in abiotic kind of stress that usually limits the agricultural productivity mostly seen in arid and semiarid regions of the world. It tends to be one of the major environmental stresses which results in ionic toxicity and induces an osmotic stress in plants to a major extent that leads to different nutritional disorders. H2S is known to enhance the salt tolerance, as is seen in barley seedling roots where it acts as a messenger molecule resulting in the modulation of different physiological processes in plant by decreasing the net K+ efflux (Chen et al. 2015). Moreover, the effect of H2S was seen in poplar species as well. When poplar was subjected to salt stress, both long term as well as short term, it results in increased Na+ efflux as well as an increased H+ influx for its roots caused by NaHS. Depolarization-activated K+ channels resulted in K+ loss induced by NaCl. Other researches revealed about the role of H2S in salt stress in rice plants. Results have shown a decreased growth with NaHS. Salt stressed rice plants have a decreased content of chlorophyll, carotenoid and soluble proteins. Under salt stress, a vital role of H2S was witnessed in ion homeostasis, where the ability to decrease the uptake of Na+ and Na+/K+ ratio and to balance mineral contents. Furthermore, it was revealed how implication of this gaso-transmitter, H2S, can manage the salt stress that makes the rice plants to adapt the adversities of environment (Mostofa et al. 2015). In a study performed on the roots of Arabidopsis thaliana, Li et al. (2014) exposed the plants to 100 mM NaCl stress which caused electrolyte leakage and disturbed the Na+/K+ ratio. However, the follow-up treatment with NaHS enhanced the salt tolerance by maintaining the homeostasis of ions via regulating the plasma membrane Na+/H+ antiporter system. It has also been documented that salt stress also initiate biosynthesis of endogenous H2S. In a study carried out in seedlings of Medicago sativa, Lai et al. (2014) found that there was subsequent increase in the biosynthesis of H2S from 30 to 70 nmol g−1 FW when the concentration of NaCl increased from 50 to 300 mM. Integrity of photosynthetic apparatus can be deteriorated by salt stress which eventually has an immense effect on photosynthetic efficiency of plant. In Nicotiana tabacum, Da Silva et al. (2017b) observed that salinity stress induced the accumulation of endogenous H2S was responsible for redox defense systems to prevent the inhibitory effects of salinity stress. Thus, it is clear that H2S is an important molecule in plants implicated to confer salt stress tolerance.
28.2.2 Role of H2S in Heat Stress
Heat stress can be defined as excessive increase in soil and air temperatures above a threshold level for ample time that cause usually an irreversible damage to plant physiological functions as well as its development which includes the rate of reproductive development or the photosynthetic rate which can be seen in decreased seed or fruit production. As the plants are sessile, they have to tolerate the temperatures provided by their environment which can never be always optimal (Bita and Gerats 2013). Heat stress can affect the plant in different manners either by high day or high night temperatures or by either high air or high soil temperatures. Several research groups have suggested the implication of H2S to tolerate both high and low temperatures. Heat stress can be attributed as a direct effect of global warming (Banerjee and Roychoudhury 2018). A synchronized antioxidant network is activated by H2S to achieve heat shock protection. It was seen that electrolyte leakage and the production of MDA due to membrane lipid peroxidation was significantly reduced by H2S released from NaHS (Li et al. 2012). H2S interacts with various physiological regulators like Ca2+ and proline. It has been seen that maize seedling when treated with NaHS have elevated the activity of pro-biosynthetic enzyme that facilitated viability of seedling under heat stress due to high endogenous accumulation of proline (Li et al. 2013). Under the heat stress the rate of germination of maize seeds can be increased by NaHS, a derivative of H2S and also enhance the tissue viability and the accumulation of malondialdehyde (MDA) caused by heat treatment has also been lowered (Li et al. 2013). In maize the heat tolerance induced by salicylic acid (SA) is enhanced by NaHS that acts as H2S donor (Li et al. 2015b). Recently, an increase in heat tolerance was achieved by the application of NaHS on wheat seedling through foliage. High temperature in plants also triggers the biosynthesis of the H2S (Fu et al. 2013). In Nicotiana tabacum, when seedlings are under 35 °C, it was found that the expression of LCD was increased which was responsible for the biosynthesis of H2S (Chen et al. 2016). H2S donor also induces the thermotolerance in strawberry plants which were exposed to 42 °C (Christou et al. 2014). They observed that H2S root pretreatment activates systemic thermotolerance via the coordinated network of transcriptional regulation of heat shock proteins and aquaporin.
28.2.3 Role of H2S in Drought Stress
The availability of water content in soil is reduced and various environmental factors that cause a continuous loss of water either by transpiration (loss of water from aerial parts of plant in the form of moisture or water vapour) or by evaporation (process of vaporization) lead to a condition known as drought stress (also known as water stress). It is one of the most important abiotic environmental stresses and can be regarded as a multidimensional stress because it can cause alteration in various physiological as well as morphological functions of a plant. Drought stress connects plant development and yield. Primarily it can affect the crop productivity and hence can weaken the global food security and can increase other related adverse consequences like desiccation, osmotic imbalance, drooping and much more. Different plant species have different tolerance to drought stress. Drought stress tolerance and protection can be regulated by H2S (Jin et al. 2011, 2013, 2017). Mitigation of drought susceptibility can be achieved by H2S (Zhang et al. 2010b). Reduced activity of lipoxygenase (LOX) and malondialdehyde (MDA) content along with increased activities of ascorbate peroxidase (APX) and catalase (CAT) was reported when wheat seedlings were treated with NaHS, a derivative of H2S (Zhang et al. 2010a). In seedlings of Arabidopsis thaliana, Shen et al. (2013) conducted an experiment and found that wild type seeds treated with polyethylene glycol (PEG-8000) mimicked drought stress, which trigger the biosynthesis of H2S. They concluded their study by observing that H2S improved drought resistance through regulating the expression of drought associated miRNAs in Arabidopsis. When wheat seeds were exposed to PEG 6000 induced drought stress for 2 days, a rapid increase from 1.5 to 3.5 mmol g−1 dry weight of H2S production was measured (Zhang et al. 2010a). They further observed that H2S treatment slowed down the activity of lipogenase. Some researchers showed that prolonged exposure to H2S results in increased stomatal aperture whereas short-term exposure to H2S can result in closure of stomata (García-Mata and Lamattina 2010; Lisjak et al. 2010, 2011). In case of wheat (Triticum aestivum L.), drought responsive genes regulated by H2S were also studied.
28.2.4 Role of H2S in Metal Stress
Increased anthropogenic and industrial activities lead to the contamination of water and soil by heavy metals growing as one of the most concerned global environmental problems (Fang et al. 2016; Ye et al. 2017; Wani et al. 2018). Metal stress is responsible for the retarded plant growth as well as development. Moreover, they have a deleterious effect on plant’s physiological processes. The major heavy metal toxicants may include lead (Pb), cadmium (Cd), chromium (Cr), copper (Cu), nickel (Ni) and zinc (Zn) (Macomber and Hausinger 2011; Wang et al. 2013; Ye et al. 2017; Qin et al. 2018; Zhou et al. 2018; Wani et al. 2018). Various effects like chromosomal aberration, membrane damage, colonization inhibition, oxidative stress, antioxidant enzyme upregulation and even cell death can be caused by the presence of the heavy metals even if these are present in trace amounts (Gong et al. 2009; Ali et al. 2014, 2018; Huang et al. 2015). Blockage of the casparian strips or due to tapering by cell wall of roots can result in accumulation of heavy metals in root cells. The efficiency of toxicants removal and alleviation of heavy metals can be done by the application of H2S. Lead, a heavy metal effects the germination, growth (root elongation and cell division) and various biochemical and physiological attributes (photosynthesis, nutrients uptake, respiration and hormonal equilibrium) in cauliflower, which are however mitigated by the application of NaHS, a donor of H2S. Accumulation of higher amounts of zinc in soil can result from excessive use of zinc enriched fertilizers and the industrial activities. This accumulation can affect the quality of both vegetables and fruit crop. Both the shoot as well as root dry weight of pepper (Capsicum annuum L.) plant was reduced due to zinc stress, whereas, proline content and leaf electrolyte leakage (EL) were enhanced. Pertinence of NaHS increased both the shoot and root growth in zinc stressed plant, but also reduced the leaf EL and proline content in pepper plant. NaHS promoted the plant growth and photosynthesis in chromium stressed plant (Ali et al. 2013). While in wheat plants NaHS can help in relieving the reduction in germination of seeds caused by copper stress (Zhang et al. 2008). Moreover, oilseed rape (Brassica napus L.) stressed by heavy metal lead, alleviated by NaHS, results in growth, photosynthesis and cell structure improvement (Ali et al. 2014). Chen et al. (2018) studied the effect of exogenous H2S on Brassica oleracea L. seed germination and seedling growth under Pb (0.25 and 0.5 mM) stress. They found that Pb markedly inhibited seed germination and seedling growth, root length, shoot length and fresh weight. In addition, they observed that NaHS elevated endogenous contents and reduced the Pb induced malonyldialdehyde, superoxide anion and hydrogen peroxide production. Zanganeh et al. (2018) studied the impacts of seed priming with H2S along with salicylic acid on possible metabolic pathway of amino acids in maize plant under Pb stress. They observed that H2S along with salicylic acid play a significant role in regulating the metabolism of methionine and arginine in maize under Pb stress condition. Mostofa et al. (2015) studied the alleviative role of H2S in rice plants under Cd stress. Their results revealed Cd-induced growth inhibition and biomass reduction. Cd-mediated oxidative stress in rice plants was evidenced by observing increased levels of superoxide, hydrogen peroxide, methylglyoxal and malondialdehyde. H2S reduced the extent of Cd-induced oxidative stress via enhancing redox status and the activities of enzymes related to reactive oxygen species metabolism and methylglyoxal detoxification system. They confirmed the beneficial effect of H2S under Cd stress by using H2S-scavenger hypotaurine that abolished the beneficial effect of H2S in rice plants.
28.3 Nitric Oxide (NO)
Nitric oxide with the formula NO is a colourless gas and is considered as one of the principal oxides of nitrogen. Nitric oxide is a free radical, i.e. it is having an unpaired electron. It is a highly diffusible gas having the ability to diffuse through biological membranes readily. NO has an immense role in various physiological and biochemical (hence is a bioactive molecule) processes of plants. It shows dual character at different concentrations. At low concentrations, it acts as a signalling molecule whereas at higher concentrations, it can damage the cell resulting in nitro-oxidative stress. Hence it has been proven to be useful as well as harmful for plant. Beside this, NO is associated with signal transduction. NO, like H2O2 is considered as an important signalling molecule which makes plants to have adaptive responses to various biotic as well as abiotic environmental stresses (Qiao et al. 2014; Hossain et al. 2015; Santisree et al. 2015; Simontacchi et al. 2015; Sahay and Gupta 2017; Asgher et al. 2017; Sami et al. 2018; Nabi et al. 2019; Sharma et al. 2019). It has been seen that application of NO to seeds or seedlings of different plants resulted in making the plants tolerant to various stresses which includes heat, drought, and salt stresses mainly through two different ways; either by decreasing oxidative toxicity or by increasing antioxidative potential in numerous plants like citrus plants (Tanou et al. 2009), wheat (Wahid et al. 2007), Capsicum annuum (Kaya et al. 2019b), soybean (Ishibashi et al. 2011), maize (De Azevedo Neto et al. 2005), rice (Uchida et al. 2002; Yang et al. 2016), orange seedlings (Fan and Liu 2012), tomato (Siddiqui et al. 2017), strawberry (Kaya et al. 2019a) and other crop species (Hossain et al. 2015; Santisree et al. 2015; Simontacchi et al. 2015). During plant pathogen interactions, NO has an important additional defensive role to play (Durner et al. 1998; Gaupels et al. 2011; Mur et al. 2013). Various researches have revealed the association of NO with plant growth, seed germination, photosynthesis, leaf senescence, pollen growth, and orientation and it is rightly given a name of “plant growth regulator” (Beligni and Lamattina 2001). Moreover, NO has a significant interaction with other plant hormones such as auxins, gibberellins, abscisic acid, cytokinins, ethylene, salicylic acid, jasmonic acid, etc. under diverse stresses. The production of NO is suggested to take place through different pathways which are classified as oxidative or reductive steps.
28.3.1 Role of NO in Drought Stress
In drought stress, i.e. unavailability of water, there is an interaction between NO and abscisic acid (ABA) (Hancock et al. 2012; Sahay et al. 2019). An exogenous application of NO increased the drought tolerance in cut leaves and seedlings of Triticum aestivum by enhancing ABA synthesis with the help of a NO donor (Zhao et al. 2001). Many researchers through their researches in diverse crop plants have experimentally shown that there is an enhancement of plant tolerance to drought stress with the external application of NO (Lei et al. 2007, Hao et al. 2008, Shao et al. 2010, Tian and Lei 2006, Xing et al. 2004; Cechin et al. 2015; reviewed by Santisree et al. 2015; Montilla-Bascón et al. 2017). Moreover, researches have showed that NO is produced as a signal molecule in response to abscisic acid (Mioto and Mercier 2013). In case of Zea mays, it was seen that by the application of NO, it interact with CK’s and results in regulation of photosynthesis and also an increase in adaptation towards drought stress (Shao et al. 2010). Similar results were also reported in case of Arabidopsis thaliana for the induction of senescence by interaction between CK’s and NO (Mishina et al. 2007). Nevertheless, in Arabidopsis thaliana, it was found that over-expression of two ABA receptors (AtPYL4 and AtPYL5) enhanced drought resistance, antioxidant enzyme activity and osmolyte levels. These observations also bring out the role of NO in drought stress response in Arabidopsis (Shi et al. 2014).
28.3.2 Role of NO in Salt Stress
A worldwide increase in salinity threatens the plant growth, development and production of agriculture (Zhu 2003; Ahmad et al. 2018a; Romero-Munar et al. 2019). According to an estimate there is more than 20% (~45 million ha) of arable land worldwide and approximately 50% of irrigated land is occupied by high salt concentration (Ahmad et al. 2015; Fatma et al. 2016). The high salt conditions are injurious to plant health, as it causes ionic, osmotic and oxidative stress, thereby inhibiting various biochemical and physiological processes responsible for optimal growth and development (Munns and Tester 2008; Khan et al. 2010; Ahanger et al. 2018; Khanam and Mohammad 2018; Jorge et al. 2019). Due to salinity-induced intracellular ion imbalance, the soil nutrient uptake is altered which leads to nutrition deficiencies in plants. While, salinity provokes disintegration of membranes, loss of metabolic functions, leakage of ions, DNA defragmentation, and consequently programmed cell death (Hasegawa et al. 2000; Ahanger and Agarwal 2017; Tang et al. 2019). Salt stress has a relevant effect on a plant as that of the drought stress do. Many experiments have shown the increase in resistance to salt stress (also known as salinity) on the application of NO to the affected plants (Khan et al. 2003; Fatma et al. 2016; Sehar et al. 2019). There are ample evidences suggesting the involvement of NO in alleviation of ill effects of salt stress on various plants. Under salt stress, DELLA proteins play an important role where it restrict the growth and regulate development. Root meristems inhibition under salt stress was achieved by NO generation by auxin concentration reduction (Liu et al. 2015). Furthermore, experiments showed a synergetic interaction between NO and SA resulting in the alleviation of salt stress (Liu et al. 2014). By the application of NO, there was an increase in antioxidant enzyme activity, witnessed in mitochondria of wheat seeds under salt stress, enhancing the germination rate and weight of radicals and coleoptiles. Further experiments were done with wheat plant in which it was seen that the starch content can be reduced and soluble sugar content can be increased on the pretreatment of wheat seeds with NO for 3 days (Almansouri et al. 2001). Association of NO with increased ATP content in wheat seeds was also observed. Enhancement of Na+/K+ ratio was provided by NO application in the callus of Phragmites communis (reed) and Populus euphratica (populus) providing tolerance to salt stress (Zhao et al. 2004). In a recent study, Sehar et al. (2019) studied the involvement of nitric oxide donor (sodium nitroprusside) in the reversal of glucose-inhibited photosynthetic responses in the presence or absence of salt stress (100 mM NaCl) in wheat plants. They found that NO improves photosynthesis of wheat plants in the absence of salt stress, and also reduces glucose-mediated repression of photosynthesis under salt stress. NO accomplished this effect through increase in antioxidant system and concomitant decrease in glucose and ethylene sensitivity under salt stress. In yet another recent experiment, Campos et al. (2019) studied the potential of NO and phytohormone crosstalk in Lactuca sativa plants to salinity stress conditions. Plant exposure to salt stress triggered ionic, osmotic and oxidative stress, which causes imbalance in hormone content, cell death and consequently decreased growth of plants. These changes were correlated with salt ions in tissues. However, NO caused a decrease in Na+ accumulation and stabilized the mineral nutrient status. This resulted in maintenance of photosynthesis rate and growth re-establishment. The NO-signalling also balances the phytohormones content and caused an increase in antioxidant potential and osmotic regulation, with culminates tolerance to the salt stress. Hence it was proved that NO has an immense importance in physiological response alteration which enhances the growth of plant (Liu et al. 2007).
28.3.3 Role of NO in Heavy Metal Stress
There are alterations in root structures due to change in hormonal imbalance under heavy metal stress. One of the common aspects of stress caused by various heavy metals is ROS production (He et al. 2012; Wani et al. 2018). Various researches have showed that NO tends to have an important role in the protection against heavy metal stress like the toxic effects exerted by As (Singh et al. 2009), Cd (Hsu and Kao 2004), Al (Wang and Yang 2005), Cu (Yu et al. 2005) and B (Farag et al. 2017). Application of NO to the plants having toxicities of such heavy metals alleviates the effects under different conditions. NO content sometimes increases and sometimes decreases in response to heavy metal stress making a controversy. Researchers have shown that in case of few plants like pea (Pisum sativum) and Arabidopsis thaliana, Cd tend to reduce the NO production hence resulting in stress (Barroso et al. 2006; Rodríguez-Serrano et al. 2009; Zhu et al. 2012a, b; Xu et al. 2011). In Arabidopsis thaliana, NO accumulation induced by auxin increased the cadmium tolerance (Xu et al. 2011). Application of NO successfully shows an improvement in the antioxidative capacity of Medicago truncatula and reduction of auxin degradation in roots were also seen in the plant under Cd stress (Xu et al. 2010).
28.3.4 Role of NO in Temperature Stress
The adverse effects that results from heat stress can be enlisted as membrane damage, lipid peroxidation, enzyme inactivation, oxidative stress and ultimately disruption of DNA strands (Suzuki and Mittler 2006; Ali et al. 2019). Protein denaturation, oxidative and osmotic stresses and membrane rigidity that can cause ion leakage are some other effects of low temperature (Ruelland et al. 2009; Khan et al. 2017). To deal with such adversities, application of NO turned to be useful to the plants. It was seen that NO also helps in inducing various activities in cold stress like nitric oxide synthase (NOS) and S-nitrosoglutathione reductase (GSNOR) activities. Some residues of other compounds like S-nitrosothiols and nitrates were also observed in case of pea plant (Corpas et al. 2008). Nitrate reductase dependent-NO generation was detected in Arabidopsis thaliana plant when the plant was subjected to 4 °C (Zhao et al. 2009). At low temperatures, there is the production of ABA which leads to the closure of stomata or osmolyte production having deleterious effects on the physiology of plants (Ruelland et al. 2009; Kosová et al. 2012).
28.4 Salicylic Acid (SA)
Salicylic acid (ortho-hydroxy benzoic acid; SA), a ubiquitously distributed signalling molecule, phenolic in nature, plays a pivotal role in tolerance of various kinds of stresses in diverse crop plants; both biotic and abiotic. Additionally, it plays a role in plants growth and development along with defense responses. Furthermore, various physiological as well as molecular processes like uptake of nutrients, fruit ripening, stomatal movements, photosynthesis, biosynthesis of chlorophyll, pathogenesis-associated protein expression, etc. are regulated by the SA mainly in concentration dependent manner (Khan et al. 2015; Nazar et al. 2017; Zaid et al. 2019). Also, biosynthesis of various secondary metabolites like sinapyl alcohol dehydrogenase, cinnamyl alcohol dehydrogenase and cytochrome P450 are encoded by the SA genes along with the production of different chaperones, heat shock proteins and antioxidants (Jumali et al. 2011). SA is synthesized mainly via two different pathways: isochorismate synthase (ICS) and the phenylalanine ammonia lyase (PAL) in plastids. However, ICS pathway is the major route of biosynthesis of SA in most of the plants where, ICS is biosynthesized from chorismic acid, an end product of shikimic acid pathway (Uppalapati et al. 2007; Catinot et al. 2008; Jayakannan et al. 2015). Various researchers have reported a potential role of SA in amelioration of different abiotic stresses like drought (Miura et al. 2013; Nazar et al. 2015; Lee et al. 2019), salinity (Fahad and Bano 2012; Khodary 2004; Amirinejad et al. 2017; Tahjib-ul-Arif et al. 2018; Alsahli et al. 2019), chilling (Yang et al. 2012; Chen et al. 2016; Wang et al. 2018), metal (Zhao et al. 1995; Zaid et al. 2019) and heat (Fayez and Bazaid 2014; Munir and Shabbir 2018). Other effects of SA includes: ethylene biosynthesis is retarded by the exogenous supplementation of SA, enhancement in the production of photosynthetic pigments and photosynthetic machinery and alleviation of deleterious effects in plants, resulting from exposure to heavy metal (Zhao et al. 1995; Zhang and Chen 2011). PR1 and PR2 (pathogenesis-related genes) are reported to be the SA-inducible genes mainly involved in the modulation of some abiotic stresses in plants (Miura et al. 2013). Also, there are reports suggesting the SA receptors to belong to the family of receptor-like protein kinases (RLKs) as SA is capable of modulating the expression of various RLKs in plants (Ohtake et al. 2000). Despite considerable investigations, the role of SA in stress tolerance at molecular level remains largely unknown.
28.4.1 Role of SA in Heat Stress
Over the past years, different researchers have identified a putative role of SA in regulation of heat stress in plants through the modulation of various physiological and metabolic processes. Heat stress tolerance in different plants under the influence of SA is mainly explained by the amendment of the antioxidant defence mechanism in plants. Activity of various antioxidant enzymes is modulated mainly through the endogenous H2O2 levels under the influence of SA in plants resulting in improvement of plant growth and development. Various researchers have reported the amelioration in growth, biochemical and physiological attributes of different plants viz. corn and soybean (Khan et al. 2003), wheat (Shakirova 2007), Brassica juncea (Fariduddin et al. 2003), wheat seedlings (Hayat et al. 2005), barley seedlings (Pancheva et al. 1996), maize (Khodary 2004), cucumber, grape and many other important plants (Shi et al. 2006; Wang et al. 2010) under heat stress, by the exogenous application of SA to the plant. Furthermore, survival percentage of maize seedlings has been reported to increase by the pretreatment of seeds under heat stress with SA. Also, an enhanced accumulation of osmolytes leading to an improvement of antioxidant system of the plants under heat stress has been reported (Li et al. 2015a, 2015b; Li 2015). After a pretreatment with SA and heat stress, Agrostis stolonifera showed an improvement in growth (increase in green leaf index), membrane stability, lipid peroxidation and photosynthesis. Similarly, the activities of different antioxidant enzymes like superoxide dismutase (SOD) and catalase (CAT) and contents of proline, phenolics and flavonoids in Digitalis trojana were enhanced by the pretreatment of SA in callus cultures under heat stress (Cingoz and Gurel 2016). A reduction in the oxidative damage by heat stress was recorded in Arabidopsis plants after the foliar-application of SA treatment (Larkindale and Knight 2002). Moreover, the leaf-applied SA induced long-term heat tolerance in the grape plant, which might be due to the Ca2+ homeostasis and antioxidant systems (Wang and Li 2006). Many other derivatives of SA (sulphosalicylic acid, methyl salicylate) have been reported to influence the heat tolerance in plants like cucumber and holm oak, respectively (Shi et al. 2006; Llusia et al. 2005). An increase in the contents of protein as well as proline was observed by both SA treatment and heat acclimation leading to the induction of POD and APX activities and a reduction in CAT activity (Chakraborty and Tongden 2005). Kaur et al. (2009) have observed that SA pretreatment leads to heat tolerance at seedling stage in Brassica species by increasing total soluble sugar and growth of plants as well as by enhancing the activities of some enzymes (invertase, CAT and POD). Moreover, the expression of some noteworthy proteins (heat shock proteins; HSPs) along with some new proteins was stimulated after pretreatment with SA. In yet another study, it has been reported that the expression of HSP21 was modulated by the application of SA to the leaves of the plant (grapevine) under study. The levels of HSP21 remained high throughout the experiment in the SA-treated plants as compared to the control, helping the plant to recover thus conferring heat tolerance to the plant (Wang et al. 2011). There are other reports related to heat tolerance by foliar application of SA, involving HSPs in tomato, mung bean and hyacinth bean. The genes involved in the ascorbate-glutathione cycle and activities of several reactive oxygen species (ROS) scavenging antioxidant enzymes are regulated by the SA treatment in these plants (Rai et al. 2018a, 2018b). In a study carried out by Liu et al. (2006), an interrelationship has been reported between SA and ABA. It was observed that the levels of SA and ABA was modulated during heat stress and the presence of SA (conjugated as well as free form) is much imported to the plant as compared to ABA in conferring heat tolerance to the plants. Clarke et al. (2004) correlated the level of SA and basal heat tolerance in Arabidopsis genotypes with modified SA signalling. Thus, from the above discussion, it is clear that SA modulated different mechanisms to confer heat stress tolerance in various crop plants.
28.4.2 Role of SA in Metal Stress
Heavy metals present in the agricultural lands due to various anthropogenic activities lead to perturbation of various physiological, biochemical and metabolic processes in different plants leading to a disturbed growth and reduced productivity (Weast 1984; Boussama et al. 1999; Aftab et al. 2011; Ahmad et al. 2018b; Wani et al. 2018). Various researchers have reported an important role of SA in alleviating the stress caused by the heavy metals present in the environment. Lead- and mercury-induced stress in rice has been studied by Mishra and Choudhuri (1999) where pretreatment with SA protected rice from the heavy metals induced membrane disruption. Also, Cd-induced toxicity in barley (Metwally et al. 2003), maize (Pál et al. 2002; Krantev et al. 2008), mustard (Zaid et al. 2019), peppermint (Ahmad et al. 2018b), soybean (Drazic and Mihailovi 2005), alfalfa (Drazic et al. 2006) and rice (Panda and Patra 2007; Chao et al. 2010) was positively alleviated by SA application (foliar applied or pretreatment) to these plants. Yang et al. (2003) studied the effect of Al on Cassia tora where it was found that SA application conferred tolerance to the plant to withstand the deleterious effects of the heavy metal stress. It was reported that the Cassia tora under Al stress accumulated citrate in their roots as result of SA application. Ill effects caused by lead and mercury in rice were also mitigated by the exogenous application of salicylic acid. It was reported that the enhancement in the activity of lipoxygenase was regulated by the application of SA (exogenous) (Mishra and Choudhuri 1999). Gill et al. (2016) studied the protective effects of exogenously applied SA on Cr toxicity in the black and yellow-seeded Brassica napus L. The findings of these authors demonstrated the enhanced activity of enzymatic antioxidants and gene expression, secondary metabolism and the transcript level of specific stress associated proteins in root and leaf of these plants under Cr toxicity. Cd tolerance due to the application of SA in different plants is attributed to the improvement of antioxidant system of the plant as SA enhances the activity of SOD, peroxidase, dehydroascorbate reductase, GR which help in scavenging the ROS produced in these plants (Ahmad et al. 2018b; Khanam and Mohammad 2016; Kazemi et al. 2011; Zhang et al. 2011; Bai et al. 2014). Furthermore, in a report by Krantev et al. (2008) similar results were recorded where the growth of the plant, activities of RUBP carboxylase and PEP, carboxylase and antioxidant enzymes (APX, SOD) were improved whereas, activity of CAT, rate of lipid peroxidation and leakage of electrolytes was reduced in maize leaves, thus conferring Cd tolerance to the plant. Along with the above mentioned physiological and biochemical processes, SA also modulates the expression of certain genes and proteins that lead to lower H2O2 content in the plants resulting in membrane stability under heavy metal stress (Chao et al. 2010). Kumari and Pandey-Rai (2018) studied the effect of SA on Artemisia annua under arsenic (As) stress. It was reported that SA helps in sequestration of As into the vacuoles and the regulation of artemisinin biosynthesis by the synthesis of oxylipins, which modulate the expression of MAPKs. Moreover, different transcription factors (MYC, WRKY) are upregulated by these MAPKs resulting into a positive effect on the biosynthesis of secondary metabolites (artemisinin) along with the mitigation of heavy metal stress.
28.4.3 Role of SA in Drought Stress
Drought stress (water deficit) that affects plants, is a multidimensional stress which leads to various dysfunctions (physiological and biochemical) at different organizational levels of the plant like turgor reduction, growth, photosynthetic rate, stomatal conductance and damages of cellular components, decrease in water potential, production of radical scavenging compounds, regulation and alteration of gene expression, etc. (Janda et al. 2007; Yordanov et al. 2000; Farooq et al. 2009; Aimar et al. 2011; Kunert et al. 2016; Joshi et al. 2016). In a study by Da Silva et al. (2017a), SA application enhanced the growth of sesame plant under drought stress resulting in mitigating the ill effects of the stress. Also, there are reports where SA application delimits the synthesis of ROS in plants under water stress. Furthermore, application of SA increases the expression of mitochondrial alternative oxidase (AOX; an important enzyme for stress tolerance) in stressed plants (Tang et al. 2017; Zhang and Chen 2011). Responses of tomato plant under drought stress showing negative growth, reduction in photosynthetic and biochemical parameters (membrane stability index, leaf water potential, NR and CA activity, contents of chlorophyll and relative water) and an upregulation of proline content and antioxidant enzymes (CAT , POX and SOD) were enhanced by the application of exogenous SA at lower concentration (Hayat et al. 2008). From the survey of scientific literature, various reports indicate a stress-tolerance role of SA in different plants like tomato and bean (Senaratna et al. 2000), Salvia officinalis (Abreu and Munné-Bosch 2008), wheat (Hamada 1998; Hamada and Al-Hakimi 2001; Singh and Usha 2003), barley (Bandurska and Stroinski 2005), sunflower (Hussain et al. 2008), etc. Soaking of seeds (wheat) in SA (an aqueous degraded product of acetyl SA), confer drought resistance to the seedlings, improving the shoot and root dry weights, transpiration rate by protecting the photosynthetic apparatus of the plant from oxidation (Hamada 1998; Hamada and Al-Hakimi 2001). Singh and Usha (2003) also confirmed these results, where the plants showed a marked enrichment in growth (moisture content, dry mass), physiology (activity of Rubisco and superoxide dismutase (SOD) and content of total chlorophyll) and yield of the plants irrespective of the concentration of SA or levels of drought stress applied when compared to the control plants. Similar reports where seeds of tomato and bean have been soaked in SA/acetyl SA to study the response of the plants to drought stress. It was recorded that the seedling survival rate increased by the applied concentration (0.1 Mm and 0.5 mM) of SA/acetyl SA (Senaratna et al. 2003). Bandurska and Stroinski (2005) interestingly reported that the application of SA to the barley plants improved ABA content, suggesting a concomitant role of ABA for the development of drought tolerance by the application of SA. However, some of the reports suggest that by the application of SA (to maize) did not improve drought tolerance, however rendering plants more susceptible to drought (Németh et al. 2002). Horváth et al. (2007) also reported negative results for the application of SA to Chinese spring wheat however, application of SA to winter wheat Cheyenne gave no effect to the plant. Contrary to the previous two plants application of an SA analogue (4-hydroxybenzoic acid) increased the drought tolerance in Cheyenne plants. Thus, suggesting the role of SA in imparting drought tolerance depends upon the type and concentration of SA applied and the genotype of the plant and severity of the stress (Yuan and Lin 2008).
28.4.4 Role of SA in Salinity Stress
Salinity is one of the important abiotic stresses, affecting the growth and physiology of plants. Salt stress may result into responses like, osmotic conductance, toxicity and imbalance of specific ion, and oxidative stress, leading to the production of reactive oxygen species (Tester and Davenport 2003) and inversely resulting in a decrease of plant weight and thus reduction in plant productivity (Ashraf and Harris 2004). SA is a phytohormone that modulates plant physiological responses conferring stress tolerance to the plant (Ahmad et al. 2011; Janda et al. 2012; Khan et al. 2014). In a report by Azooz et al. (2011), treatment with SA to Vicia faba under salt stress (sea water treatment) ameliorated the ill effects of salinity leading to an increase of osmolyte and free amino acids (proline) accumulation. Also an increase in biomass accumulation, growth and antioxidant system has been registered in the plant under study. Khan et al. (2014) have also confirmed the beneficial effects of SA application to salt-stressed Vigna radiata L. leading to a decrease in the levels of ethylene and better partitioning of salt ions. Also, some reports confirm an increase in the levels of endogenous ABA and proline along with an improvement of growth and yield of wheat plant under salt stress in response to SA application (Shakirova et al. 2003). Improvement of growth, accumulation of biomass, cell division, and activity improvement of photosynthetic apparatus as well as different antioxidant enzymes have been reported after the application of SA (Da Silva et al. 2017a). Janda et al. (2012) reported that salt stress have deleterious effects on the photosynthesis and membrane stability of barley plant; which were improved by the exogenous application of SA. Similar results were reported in maize, where the application of SA to salt-stressed plant leads to reduction in accumulation of Na and improvement of growth and development of the plant under salt stress (Gunes et al. 2007). Furthermore, various researchers have reported the amelioration of salt stress induced changes in different plants viz. barley (El-Tayeb 2005), wheat (Hamada and Al-Hakimi 2001; Sakhabutdinova et al. 2004), tomato (Tari 2002; Tari et al. 2004, 2010; Szepesi 2005; Szepesi et al. 2008a, b; Gémes et al. 2008), Salvia officinalis L. (Sahar et al. 2011), Arabidopsis (Poór et al. 2012) Iris hexagona (Wang et al. 2001). Moreover, application of SA to salt-stressed barley plants by improving the contents of photosynthetic pigment and maintenance of membrane integrity resulted in salt tolerance (El-Tayeb 2005). Application of SA to salt-stressed plants also result in a decrease in lipid peroxidation due to a decrease in Na content and a significant increase in the contents of K and Mg. The activities of various antioxidant enzymes (SOD, CAT, GPX) was also increased by the application of SA with a decrease in contents of dehydroascorbate reductase and in the ascorbate and glutathione contents (He and Zhu 2009). The activity of these antioxidant enzymes was also modulated by the application of SA in tomato plants along with an increase in the accumulation of various osmolytes (sugars, sugar alcohol, proline) in the plant (Tari 2002; Tari et al. 2004, 2010; Szepesi 2005; Szepesi et al. 2008a, b; Gémes et al. 2008). Sahar et al. (2011) also reported similar results in Salvia officinalis L. plant. In contrast to the earlier reports, Hao et al. (2012) studied a line of mutant Arabidopsis (snc1, NahG, npr1–1, snc1/NahG and wild type plant) where high SA accumulation lead to an increase in salt-induced damage and reduced SA proved to be favourable for the plant. Similarly, reports for soybean under salt stress show a decrease in the levels of endogenous free SA content (Hamayun et al. 2010). Thus, from the above literature it is clear that SA is a potent phytohormone which confers salt stress resistance in different crop plants.
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Acknowledgements
We are thankful to the host institution Aligarh Muslim University, Aligarh 202002, India and our workplace at Plant Physiology and Biochemistry Section, Department of Botany, Aligarh Muslim University, Aligarh for providing us seat to work. We apologize to those authors whose work could not be cited due to space limitations.
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Sadiq, Y., Zaid, A., Khan, M.M.A. (2020). Adaptive Physiological Responses of Plants under Abiotic Stresses: Role of Phytohormones. In: Hasanuzzaman, M. (eds) Plant Ecophysiology and Adaptation under Climate Change: Mechanisms and Perspectives I. Springer, Singapore. https://doi.org/10.1007/978-981-15-2156-0_28
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