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. 2020 Apr 19;26(5):871–883. doi: 10.1007/s12298-020-00815-0

Triacontanol as a dynamic growth regulator for plants under diverse environmental conditions

Shaistul Islam 1, Firoz Mohammad 1,✉
PMCID: PMC7196594  PMID: 32377038

Abstract

Triacontanol (TRIA) being an endogenous plant growth regulator facilitates numerous plant metabolic activities leading to better growth and development. Moreover, TRIA plays essential roles in alleviating the stress-accrued alterations in crop plants via modulating the activation of the stress tolerance mechanisms. The present article critically focuses on the role of exogenously applied TRIA in morpho-physiology and biochemistry of plants for example, in terms of growth, photosynthesis, enzymatic activity, biofuel synthesis, yield and quality under normal and stressful conditions. This article also enlightens the mode of action of TRIA and its interaction with other phytohormones in regulating the physio-biochemical processes in counteracting the stress-induced damages in plants.

Keywords: Triacontanol, Stress tolerance, Stress-accrued alterations, Biofuel production

Introduction

The sessile nature of plants has threatened their survival under varying environmental perturbations, viz. drought, heavy metal, salt stress etc. However, plants respond to these perturbations through a variety of physio- biochemical, molecular and structural modifications by producing various organic compounds including plant hormones that help them adapt to such changing conditions (Per et al. 2018). Plant hormones are a small group of signaling molecules that plays a vital role in various morphological, photosynthetic, biochemical and developmental processes in crop plants (Ahmad et al. 2016; Fariduddin et al. 2019; Nazir et al. 2019). The roles of abscisic acid, auxin, brassinosteroids, cytokinins, ethylene, gibberellins, Jasmonates, nitric oxide, salicylic acid and strigolactones in plants are well defined; however their mode of action may vary under stress conditions (Morkunas et al. 2014; Wani et al. 2016; Ahanger et al. 2018; Ullah et al. 2018; Fariduddin et al. 2019). Due to their pronounced roles in plants, there is a need for seeking the new plant growth regulators (PGRs) and their roles in modulating the physio-biochemical and developmental processes in plants.

Triacontanol (TRIA) is saturated primary alcohol, first identified in the hay of alfalfa (Ries et al. 1977), has recently been considered as a new PGR that affect a multitude of physio-biochemical processes in crop plants (Karam and Keramat 2017). TRIA naturally occurs in epicuticular waxes in diverse plant species, such as in Croton californicus, Copernica cerifera, Medicago sativa, Jatropha curcas, Oryza sativa, Vaccinium ashei, (Hufford and Oguntimein, 1978; Luzbetak et al. 1978; Lee et al. 1979; Freeman et al. 1979; Uchiyama and Ogasawara, 1981). TRIA being a plant growth-promoting substance enhances the plant growth when applied exogenously at relatively low concentration to most of the crops (Naeem et al. 2012). Its exogenous application enhances plant biomass, photosynthetic pigments, gas exchange parameters, mineral nutrient acquisition, leaf carbonic anhydrase (CA), nitrate reductase (NR) activity, osmolytes accumulation, modulates antioxidant enzyme activities, yield and quality attributes (Naeem et al. 2009, 2019; Waqas et al. 2016; Zaid et al. 2019). TRIA also causes changes in stem, leaf anatomy and affect vascular tissue systems in plants (Çavuşoğlu et al. 2008).

TRIA can suppress or enhance the stress responses by regulating the gene expression (Perveen et al. 2017; Islam et al. 2020). TRIA has been well documented for their essential roles in plants response to abiotic stresses such as acid mist, chilling, drought, heavy metal and salt stress (Muthuchelian et al. 2003a; Naeem et al. 2012; Zaid et al. 2019; Islam et al. 2020). Its exogenous application ameliorates the toxic effect in plants by increasing plant biomass, chlorophyll pigments, gas exchange parameters, quantum efficiency, mineral nutrient acquisition, compatible solutes accumulation and enzymatic and non-enzymatic antioxidant defense system (Perveen et al. 2013, 2016, 2017; Maresca et al. 2017; Zaid et al. 2019). Due to its diverse roles in plants, the present article focuses on the role of TRIA in modulating the plant growth and development under both normal and abiotic stress conditions and its relation with other phytohormones.

Mode of triacontanol action in plants

Researchers have explored the beneficial effect of TRIA on various metabolic processes occurring during seed germination, seedling development, photosynthesis, enzyme activities etc. TRIA also plays a pivotal role in inducing/establishing resistance against various abiotic stresses by regulating gene expression. Overwhelming assumptions led to the identification of a second messenger (l(+)-adenosine) of TRIA as 9-β-l (+)-adenosine, i.e. 9H-purine-6-amine, 9-βl-ribofuranosyl (Ries et al. 1990). The discovery of TRIA mediated formation/release of l (+)-adenosine (abbreviated as TRIM) may have elucidated the first step in the mechanism of TRIA action in plants. The l (+)-adenosine obtained from the TRIA treated plants was found to be identical to that extracted from untreated control plants and was further found to affect the plant processes similar to that of TRIA. TRIA increases the ratio of l (+)-adenosine to d (−)-adenosine in tonoplast (Ries et al. 1990; Ries 1991). Adenosine monophosphate is supposed to be the most portable source for the synthesis of l (+)-adenosine in plants (Olsson and Pearson 1990). Studies with adenosine deaminase indicated that in untreated plants, l (+)-adenosine (non-racemic) might exist in an inactive racemic mixture with d (−)-adenosine. In plants treated with TRIA, the non-racemic adenosine seems to be released to affect plant metabolic processes. Further, it was noticed that non-racemic adenosine obtained from the TRIA treated plants was found to stimulate the plant processes whereas, racemic adenosine (d (−)-adenosine) could not stimulate such plant processes (Ries et al. 1990; Ries 1991). Moreover, Ries and Wert (1992), Savithiry et al. (1992) and Ries et al. (1993) noticed that the exogenous application of l (+)-adenosine affects the plant physio-biochemical processes. Exogenously applied TRIA quickly moves to plant cells through the membrane of epidermal cells and elicits the formation of l (+)-adenosine (Aftab et al. 2010; Keramat et al. 2017; Maresca et al. 2017; Islam et al. 2020). l (+)-adenosine induces calcium ion concentration probably in the tonoplast. The elevated calcium ion may result in its binding to calmodulin protein. The activated calmodulin protein may directly modulate transcription factors (MYB2, CAMTA3, GTL etc.) and actuate the activities of kinases and phosphatases leading to gene expressions like photosynthetic ones and associated genes. It may also regulate stress-mitigating genes, modulate antioxidant defense systems and increase osmolytes accumulation that leads to enhanced growth and development of TRIA treated plants under both normal and stress conditions (Fig. 2). This proposition broadly corroborates the findings of Chen et al. (2002, 2003) and Islam et al. (2020).

Fig. 2.

Fig. 2

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Possible ways of TRIA induced abiotic stress tolerance in plants

Triacontanol and physio-biochemistry

The survey of the literature reveals that TRIA significantly affects morpho-physiology and biochemistry of crop plants under normal conditions (Fig. 1). The findings of various researchers have been summarised below.

Fig. 1.

Fig. 1

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Role of TRIA in plants

Growth

Various studies have showed that TRIA plays an essential role in regulating a broad spectrum of plant morphological responses, for example, it enhances plant height, plant biomass, leaf number and leaf area per plant in most of the harvests (Kumaravelu et al. 2000; Naeem and Khan, 2005; Naeem et al. 2019). Khan et al. (2006) observed that foliar spray of TRIA up to 1 ppm given twice-enhanced fresh and dry weight of shoot and root of Solanum lycopersicum L. The spray treatment of 1 µM TRIA given four times improved height, branch number and dry weight of Papaver somniferum L. over the control (Khan et al. 2007). Further, in controlled environmental conditions, Singh (2008) noticed that spray treatment of 1 µM TRIA given six times proved effective in mediating improvement of all the growth attributes such as plant height, number of tillers and leaves per plant, leaf length and breadth, shoot and rhizomes fresh and dry weight of Zingiber officinale Rosc. and Curcuma longa L. Similar results were observed in Withania somnifera L. and Datura innoxia Mill. by (Nasir 2009). In another study, Artemisia annua L. receiving four sprays of 1.5 ppm TRIA had comparatively higher values for the plant biomass than the control (Aftab et al. 2010). In a subsequent study, a two-spray treatment of 1 µM TRIA proved best for enhancing the shoot length, root length, leaf number, leaf area, shoot and root fresh and dry weight of Ocimum basilicum L. (Hashmi et al. 2010). Further, Coriandrum sativum L. receiving three sprays of 10−6 M TRIA with 10 days interval showed significant values for root, shoot length, fresh, and dry weight than the control (Idrees et al. 2010). Similar results were observed in Zingiber officinale Rosc., Cymbopogon flexuosus L., and Coriandrum sativum L. Senna occidentalis L. (Naeem et al. 2010; Singh et al. 2012; Meena et al. 2014, 2015; Khan et al. 2014). Abubakar et al. (2013) revealed that low TRIA concentration enhanced shoot growth, average leaf area in Punica granatum L. Furthermore, Naeem et al. (2014, 2017) also noticed that at low concentration 1 µM TRIA markedly enhanced plant height, fresh weight, dry weight and leaf area of Mentha arvensis L. over the control. Moreover, Fragaria ananassa receiving two spray treatments of 10 µM TRIA had a significant effect on plant height and leaf number compared to untreated (Baba et al. 2017). Besides, Naeem et al. (2019) reported that five spray treatments of 10−6 M TRIA proved effective in enhancing the Catharanthus roseus L. growth by improving dry and fresh mass, leaf number and leaf area per plant than the control. The enhancement in overall growth attributes might be TRIA mediated activation of l (+)-adenosine, which moves and transmitted signals throughout the plant resulting in stimulation of plant growth, leading to cell enlargement and proliferation, amino acids and protein accumulation (Naeem et al. 2009; Khan et al. 2014). It can be inferred from the above studies that TRIA elicits the formation of l (+)-adenosine, which perks up the various physio-biochemical processes by way of signaling that lead to enhanced growth-related attributes.

Photosynthesis

Previously conducted studies have showed that TRIA significantly enhanced the physio-biochemical attributes of vegetable, oilseed crops, medicinal and aromatic, ornamental and horticultural crops (Chen et al. 2003; Naeem et al. 2009, 2019). Khan et al. (2007, 2009) observed that chlorophyll and carotenoids content enhanced significantly in Papaver somniferum L. and Solanum lycopersicum L. seedling, sprayed with four times 10−6 M TRIA. Turmeric curcuma longa and Zingiber officinale receiving six sprays of 10−6 M TRIA had higher values for chlorophyll contents (Singh 2008). Similarly, Nasir (2009) noticed that foliar treatment of 10−6.5 M TRIA given six times improved chlorophyll and carotenoids content in Datura innoxia Mill. and Withania somniferum L. In another study, Artemisia annua L. receiving four sprays of 1.5 ppm TRIA had comparatively higher net photosynthetic rate (PN), internal CO2 concentration (Ci), stomatal conductance (gs), carotenoids and total chlorophyll content than the control (Aftab et al. 2010). Moreover, at lower concentration (10−6 M), TRIA markedly enhanced pigment content such as chlorophyll a, b, a + b and carotenoids content by 25.6%, 33.9%, 25.2%, and 13.0% in leaves of Ocimum basilicum L. respectively, over the control (Hashmi et al. 2010). Further, in Coriander sativum L. receiving three sprays of 10−6 M TRIA considerably enhanced the total chlorophyll and carotenoids content (Idrees et al. 2010). Similar results were observed when the foliage of ginger and lemongrass were sprayed with 10−6 M TRIA (Singh et al. 2012; Khan et al. 2014). Foliar spray of 10−6 M TRIA given three times was found to enhance the PN, gs, transpiration rate (E), total chlorophyll and carotenoids content in Lablab purpureus L., Senna occidentalis L. (Naeem et al. 2009, 2010). Similar results were observed when TRIA was applied as a pre-seed-treatment in Brassica napus L. (Shahbaz et al. 2013). The foliage of Coriandrum sativum L. receiving spray treatments of 1000 ppm TRIA effectively enhances chlorophyll content (Meena et al. 2014, 2015). In a subsequent study, Naeem et al. (2011, 2014, 2017) reported an increase in PN, gs, total chlorophyll, and carotenoids content in response to five spray treatments of 10−6 M TRIA in Mentha arvensis L. seedlings. Moreover, in a recent study, Naeem et al. (2019) observed that a lower concentration (1 µM) TRIA proved beneficial in enhancing the gas exchange attributes, total chlorophyll and carotenoids content in Catharanthus roseus L. compared with the control. TRIA rapidly increased the activity and level of ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) and rbcS genes associated with photosynthesis and further reported that higher expression levels of these rbcS genes resulted in improved photosynthetic activity in TRIA treated crops (Chen et al. 2002, 2003). Moreover, TRIA improves the size and number of the chloroplast, which might be responsible for an increase in chlorophyll and carotenoids content resulting in an increase in photosynthetic CO2 assimilation in crop plants (Islam et al. 2020). From the above-appraised literature, it can be concluded that TRIA considerably increases the photosynthetic process in plants by inducing the expression of photosynthetic and related genes including rbcS.

Carbonic anhydrase activity

Carbonic anhydrase (CA) is the second most abundant enzyme in photosynthetic tissues, found to be important in many physiological functions that involve in carboxylation or decarboxylation reactions, inorganic carbon fixation, respiration, photosynthetic electron transport system and maintaining chloroplast pH, and protect enzymes from denaturation (Singh 2008; Bhat et al. 2017). TRIA remarkably enhanced leaf CA activity, when sprayed three times at lower concentration (1 µM) to the foliage of Mentha arvensis L. (Naeem et al. 2009). In a subsequent study, Aftab et al. (2010) observed that foliar sprays of 1.5-ppm TRIA proved best in increasing the CA activity in artemisia leaves over the control. Further, Hashmi et al. (2010) reported a marked increase in CA activity in response to two spray treatments of 10−6 M TRIA to Ocimum basilicum L. foliages. Similar results were observed when the foliage of Coriandrum sativum L., Mentha arvensis L. and Cymbopogon flexuosus L. were sprayed three times with 1 µM TRIA (Idrees et al. 2010; Naeem et al. 2010; Khan et al. 2014). Moreover, Naeem et al. (2011, 2014, 2017) noticed a remarkable increase in the CA activity in response to five foliar treatments of 10−6 M TRIA to the foliage of Mentha arvensis L. In a recent study, Catharanthus roseus L. receiving five sprays of 1 µM TRIA exhibited a significant increase in leaf CA activity compared with the control (Naeem et al. 2019). Thus, TRIA increases the stomatal conductance that may facilitate the CO2 diffusion into the stomata. The entered CO2 becomes readily available in the chloroplast by the TRIA mediated CA activity. CO2 acted by CA and finally, reduced CO2 in the chloroplast stroma by (RuBPCO). The most probable reason for TRIA-mediated enhancement in CA activity may be due to the de novo synthesis and translation/transcription of genes associated with carbonic anhydrase synthesis.

Nitrate reductase activity

Nitrate reductase (NR) is an essential enzyme in nitrogen metabolism, responsible for the initiation of nitrate assimilation and hence in protein synthesis (Aftab et al. 2010). Foliar application of TRIA shows a significant effect on NR activity as reported by Naeem and Khan (2005). Naeem et al. (2009, 2010) noticed that three spray treatments of 1 µM TRIA proved best for NR activity by increasing 31.7% and 27.6% in Senna occidentalis L. and Lablab purpureus L. respectively. Further, Hashmi et al. (2010) noticed that two sprays of 1 µM TRIA proved best in enhancing the NR activity in Ocimum basilicum L. by 44.6% compared with the control. Moreover, Coriandrum sativum L. receiving three foliar sprays of 1 µM TRIA showed significant values for NR activity over the control (Idrees et al. 2010). In another study, Naeem et al. (2011) observed that TRIA remarkably enhanced leaf NR activity, when spray treatments of 10−6 M TRIA given five times to the foliage of Mentha arvensis L. Similar results were obtained when the foliage of lemongrass was sprayed three times with same concentration (Khan et al. 2014). Further, Khanam and Mohammad (2018) noticed that leaf NR activity was enhanced remarkably when TRIA at lower concentration (10−6 M) was sprayed two times to foliage of mint. Recently, Catharanthus roseus L. receiving spray treatments of 10−6 M TRIA effectively increased the leaf NR activity (Naeem et al. 2019). An increase in NR activity due to the application of TRIA may be responsible for the enhancement of photosynthetic rate that ultimately increases biomass and productivity.

Mineral nutrient acquisition

Application of TRIA showed a noticeable effect on leaf nitrogen (N), phosphorus (P) and potassium (K) contents in most of the economically important crops (Singh, 2008; Wierzbowska et al. 2010). Nasir (2009) noticed that leaf N, P and K content markedly enhanced in Datura innoxia Mill. and Withania somniferum L. leaves, as sprayed six times with lower concentration (10−6.5 M) of TRIA. In his study, Khan et al. (2009) reported the beneficial effect of TRIA on N, P and K content in leaves of Solanum lycopersicum L. In a subsequent study, Naeem et al. (2009, 2010) noticed an increase in leaf N, P and K content in response to three foliar sprays of 10−6 M TRIA in seedlings of mint. Artemisia annua L. seedlings receiving 1.5 ppm TRIA had comparatively higher values for leaf N, P and K contents than the control (Aftab et al. 2010). In another study, Hashmi et al. (2010) noticed that two sprays of 10−6 M TRIA improved leaf N, P and K content than the other sprayed concentrations in Ocimum basilicum L. Furthermore, Idrees et al. (2010); Singh et al. (2012); Khan et al. (2014) noticed that three spray treatments of 10−6 M TRIA significantly enhanced the N, P and K content in leaves of Coriandrum sativum L., Zingiber officinale Rose., and Cymbopogon flexuosus L. On the basis of the above, it may be concluded that TRIA seems to bring about compositional changes in plants leading to altered nutrient concentration.

Yield and quality

TRIA not only works on physio-biochemical attributes of the plants but also improves the content and yield of most of the economically important harvests (Niranjana et al. 1999; Naeem et al. 2011; Meena et al. 2014, 2015; Shivran et al. 2016). For example, Dhall et al. (2004) noticed that six spray treatments of TRIA (Vipul) to the foliage of tomato resulted in higher yield attributes such as number of fruits, fruit weight, fruit diameter and total yields per plant of Lycopersicum esculentum Mill. than control. Furthermore, Nogalska et al. (2008); Sharma et al. (2008); Singh (2008); Nasir (2009) noticed the beneficial effect of TRIA on yield and yield attributes of Avena sativa L., Malus domistica Borkh., Zingiber officinale Rosc., Curcuma longa L., Withania somniferum L., and Datura innoxia Mill. Khan et al. (2009) revealed that spray of low concentration (10−6 M) TRIA given four times to foliage of Solanum lycopersicum L. significantly enhanced the yield such as weight, number and yield of fruits per plant by 35.4%, 38.0%, and 57.6% respectively, over the control. Naeem et al. (2009, 2010) demonstrated that three foliar treatments of 10−6 M TRIA enhanced the yield and yield attributes of Lablab purpureus L., and Senna occidentalis L. In a subsequent study, Zhang et al. (2009) showed that application of 0.35 g a.i/ha, TRIA enhanced seed yield and harvest index in Medicaga sativa L. over the control. Further, in his study Sharma et al. (2011) noticed that Olea europaea L. receiving sprays of 5, 10, 20 ppm TRIA resulted in increased fruit length, fruit weight, reduced fruit drop, and yield efficiency. Singh et al. (2012); Khan et al. (2014) also revealed that three foliar sprays of 10−6 M TRIA substantially increases yield both quantitatively and qualitatively in Zingiber officinale Rosc. and Cymbopogon flexuosus L. over the control. Foliar application of 5, 10, 15 ml/L Vipul significantly improved flowering, fruit set and reduced flower drop in Punica granatum L. (Abubakar et al. 2012; 2013). Khandaker et al. (2013) and Baba et al. (2017) observed that TRIA have a remarkable effect on yield and quality of flowers in Vigna radiata L., Chrysanthemum morifolium Ramat., Bougainvillea glabra Choisy., and Fragaria ananassa Duch. which may be due to TRIA providing an ingredient for bud formation, development and better-quality of flowers (Reddy et al. 2002). Moreover, in his study, Baba et al. (2017) reported that application of 5 µM and 10 µM TRIA enhance fruit set and yield of the strawberry plant. Besides, Khanam and Mohammad (2017) also noted TRIA mediated enhancement in the yield and content of peppermint oil. It can be inferred from the above literature that TRIA involves in multiple plant physio-biochemical processes like water and nutrient uptake, photosynthesis, translocation of metabolites and photosynthates to the sink, which cumulatively lead to enhanced yield and quality attributes of plants.

Active constituents in the essential oil of aromatic and medicinal plants

Application of TRIA results in a noticeable effect on essential oils by increasing their content and yield. Srivastava and Sharma (1991) and Khan et al. (2007) revealed that application of TRIA showed a significant effect on morphine content in Papaver somniferum L. Foliar application of TRIA at lower concentration (10−6M) considerably enhanced curcumin and total alkaloid content in Withania somnifera Dunal L. and Datura innoxia Mill (Nasir 2009). Leaves of Artemisia annua L. receiving sprays of TRIA showed significant enhancement in contents and yield of artemisinin (Shukla et al. 1992; Aftab et al. 2010). Besides, Idrees et al. (2010) suggested that TRIA enhanced the essential oil content in Coriandrum sativum L. leaflets. Naeem et al. (2010) also noticed a TRIA-mediated enhancement in sennoside and anthraquinone content in Senna occidentalis L. Further, the foliages of Mentha arvensis L. receiving five treatments of 10−6 M TRIA had relatively higher contents of menthol, isomenthone, l-menthone and menthyl acetate, over the control (Naeem et al. 2011, 2017). Moreover, Singh et al. (2012) noticed that TRIA-mediated enhancement in oleoresin (29.7 and 25.1%) and essential oil (18.7 and 14.5%) contents at 180 and 240 DAP, respectively in Zingiber officinale Rosc. Similarly, Khan et al. (2014) revealed that 1 µM TRIA enhances the yield and contents of citral and essential oil in Cymbopogon flexuosus L. Conclusively, the improvement in yield and content of essential oil may be the result of TRIA-mediated enhancement in growth and metabolism of plants.

Triacontanol and biofuel production

Microalgae are the most abundant photosynthetic microorganisms and recognized as the most feasible sources for biofuel production because of ability to convert carbon dioxide into biomass (Mata et al. 2010; Salama et al. 2014). Microalgal oil acts as a good source for biodiesel production (Demirbas and Demirbas 2011; Rawat et al. 2013). Evidences showing that the stimulating effect of different phytohormones on growth and metabolite production (lipids, carbohydrates and proteins) in microalgae for biodiesel production (Salama et al. 2014; Yu et al. 2017). TRIA also has the potential to stimulate microalgal growth and their biodiesel production. For example, Park et al. (2013) noted that TRIA application along with other phytohormones enhanced the growth, chlorophyll, protein contents and biodiesel production in Chlamydomonas reinhardtii. Han et al. (2018) also noted that 5 mg/L TRIA significantly promoted biodiesel production by increased biomass and lipid productivity such as octadecenoic acid, monounsaturated fatty acids. It may be inferred that TRIA enhances algal biomass and metabolite production leading to enhanced algal biofuel production.

Triacontanol and abiotic stress

Abiotic constraints such as heavy metal, salinity, temperature and water stress have a severe impact on plant morphology, physiology and their productivity (Morkunas et al. 2014; Ahanger et al. 2017, 2018; Egamberdieva et al. 2017). It has now been well documented that TRIA acts as a signaliing molecule and induces resistance in plants against various abiotic stress (Naeem et al. 2012; Waqas et al. 2016) (Fig. 2, Table 1). However, the effects of TRIA under such conditions may vary and depends upon the stress type, plant species and concentration of TRIA used. The findings of researchers is summarized below.

Table 1.

Foliar applied TRIA modulating physio-biochemical attributes of plants under stressful conditions

S.no. Plant species Stress type TRIA concentration applied Plant response References
1 Cucumis sativus L. Chilling 0, 0.01, 0.10 mg dm−3 TRIA modulating chlorophyll content, photosynthetic rate (PN), stomatal conductance (gs), transpiration rate (E), peroxidase (POD) and catalase activity (CAT) activities, electrolyte leakage and leaf proline content Borowski (2009)
2 Triticum aestivum L. Salinity 0, 10, 20 µM Increased tolerance by improved dry biomass, POD activity, while decreased proline, hydrogen peroxide (H2O2) and malondialdehyde (MDA) level Perveen et al. (2014)
3 Zea mays L. Drought 0, 2, 5 µM TRIA increased chlorophyll and proline content, CAT, POD and superoxide dismutase (SOD) activities and reduced MDA, H2O2, total phenolics and glycine betaine contents Perveen et al. (2016)
4 Oryza sativa L. Transplant shock 1, 5, 10 µM Alleviated transplant-induced damages by modulating chlorophyll, sucrose content, ascorbate and glutathione (ASA-GSH) redox state, H2O2 and MDA contents Li et al. (2016)
5 Vigna radiata L. Heat 11 µM Enhanced thermal tolerance by improving abscisic acid, jasmonic acid level, mineral nutrients and amino acid content Waqas et al. (2016)
6 Brassica napus L. Heavy metal 0, 10, 20 µM TRIA enhanced shoot fresh weight, total chlorophyll content, enzymatic and non-enzymatic antioxidant activities and reduced MDA and H2O2 levels Maresca et al. (2017)
7 Zea mays L. Salinity 0, 2, 5 µM Enhanced growth, NR activity, proline, total phenolics, soluble protein, shoot potassium content and decreased relative membrane permeability, H2O2, MDA and shoot sodium ion content Perveen et al. (2017)
8 Mentha piperita L. Salinity 1 µM Improved plant biomass, gas exchange parameters, chlorophyll content, proline accumulation, SOD, CAT, POD activities, mineral nutrient acquisition and essential oil content Khanam and Mohammad (2018)
9 Mentha arvensis L. Heavy metal 1 µM Enhanced tolerance by modulating plant biomass, photosynthetic pigments, leaf carbonic anhydrase, nitrate reductase, osmolytes accumulation, mineral nutrient contents, TBARS, H2O2 content and activities of antioxidant Zaid et al. (2019)
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Salt stress

Salt stress is one of the common environmental constraints that adversely affect crop growth, development and their productivity by causing osmotic stress, ionic imbalance, ionic toxicity, metabolic imbalance and reactive oxygen species (ROS) generation (Per et al. 2017, 2018; Islam et al. 2020). ROS accumulation in tissues under salt stress is a common cause, and its accumulation disturbs the cell integrity by way of causing the oxidative stress-induced cellular damage namely denaturation of proteins, enzyme inactivation, lipid peroxidation and nucleic acid damage (Per et al. 2017; Islam et al. 2020). The survey of the literature indicates the positive regulative role of TRIA in enhancing the plants salinity tolerance. Krishnan and Kumari (2008) reported that treatment of 10 mM n-TRIA restored the metabolic processes in Glycine max L. by considerably enhanced the level of relative water contents (RWC), chlorophyll content, soluble sugars, proteins and nucleic acid. Further, Perveen et al. (2013) observed that TRIA alleviated the negative influence of 150 mM salt stress by improving the chlorophyll contents, PN, E, gs, electron transport rate and subsequently reduction in relative membrane permeability in Triticum aestivum L. Similarly, in other study, leaf applied TRIA enhanced salt tolerance in wheat cultivars by markedly increased plant biomass, peroxidase activity, and reduction in the malondialdehyde (MDA) and hydrogen peroxide (H2O2) content (Perveen et al. 2014). Exogenously applied TRIA at 50 and 100 µM reversed the effects caused by the 150 mM salt on growth attributes, gas exchange parameters and photosystem-II efficiency in Helianthus annuus L. (Aziz et al. 2013). Further, Aziz and Shahbaz (2015) also noted that TRIA minimized the salt-induced toxic effects in sunflower by upregulating the activities of glutathione reductase (GR), POD, superoxide dismutase (SOD) enzymes, and accumulation of leaf glycine betaine (GB) and proline content. Similarly, Perveen et al. (2017) noticed similar results when 2 and 5 µM TRIA was applied to the foliages of maize hybrids. They noticed a concentration of 5 µM proved effective in enhancing the salinity tolerance in maize hybrids by markedly improved growth, leaf NR activity, soluble proteins and shoot potassium content, while decreased level of relative membrane permeability (RMP), MDA, H2O2 and Na+ uptake. Moreover, two spray treatments of 1 µM TRIA applied to foliages of Mentha piperita L. nullified the salt-induced damages by improving the growth, chlorophyll, gas exchange parameters such as PN, E, gs, Ci, leaf proline, N, K and P contents, antioxidant enzyme activities and yield and its quality attributes (Khanam and Mohammad 2018). TRIA mediates salinity tolerance in plants by modulating the activity of antioxidant enzymes, leading to a balance between ROS accumulation and scavenging, and thus protecting cell membranes from salinity-induced cellular damages (Karam and Keramat 2017). In summary, it is apparent that exogenously applied TRIA plays an essential role in promoting growth and alleviating salt-induced oxidative damages in plants by increased accumulation of compatible solutes, antioxidant enzyme activity, mineral nutrient acquisition, limiting ROS production and lipid peroxidation.

Heavy metal stress

Metal/metalloid stress has become a serious threat to the environment, leads to a reduction in agricultural productivity and causes several health-hazardous problems to the living organisms (Ullah et al. 2018; Wani et al. 2018). With continuous addition of metal-polluted industrial effluents, agricultural wastes, garbage dumping and sewage wastes, productive/fertile agricultural soils are changed into barren lands, thereby adversely affecting crop growth, development and their productivity. Plants have ability to withstand metal/metalloid-induced damages up to a certain extent by the induction or regulation of indigenously existing tolerance mechanisms (Anjum et al. 2014; Ahanger et al. 2018). Use of TRIA for mitigating metal/metalloid induced damages has been under study and the results so far observed favor strongly the use of TRIA for heavy metal stress mitigation. For example, Muthuchelian et al. (2001) demonstrated that the spray treatments of TRIA at 1 mg kg −1 minimizing the cadmium (Cd) induced damages in Erythrina variegata L. by improving the dry and fresh mass, chlorophyll, carotenoids content, carbon dioxide fixation, Photosystem I (PS I) and PS II activity, Rubisco activity and NR activity. Pretreatment of Zea mays L. grains with 35 ppm TRIA counteracted the Cd toxicity by improving the growth attributes (Ahmad et al. 2013). Further, pretreatment of coriander seedling with 5, 10 or 20 µmol L−1 TRIA ameliorated the arsenic toxicity by improving the antioxidant enzyme activities (Karam et al. 2016). In another study, pretreatment of coriander seedlings with 10 µM TRIA reduced the arsenic-induced oxidative damages through modulating the activities of oxidative markers and non-enzymatic antioxidants (Karam et al. 2017). In addition, Maresca et al. (2017) noticed that spray treatment of 10 and 20 µM TRIA improved Cd tolerance by significantly modulating the activities of antioxidant (both enzymatic and non-enzymatic) enzymes. Besides, Keramat et al. (2017) found that the spray treatment of 10 µmol L−1 TRIA enhanced the arsenic tolerance in Coriandrum sativum L. by modulating the redox status of plant systems through the antioxidant defense ascorbate–glutathione pathway. Moreover, Zaid et al. (2019) also noticed that1µM TRIA spraying to the foliage of Kushal and Kosi cultivars of Mentha arvensis L. enhanced tolerance by improved plant biomass, photosynthesis-related parameters, optimum mineral metabolism, osmolytes accumulation, while reduced TBARS induced oxidative stress by induced antioxidant defense systems. In conclusion, it is apparent that TRIA application as both seed soaking and foliar treatment ameliorates plant growth and crop production under heavy metal stress conditions by improving the photosynthesis-related parameters, modulating the activities of the antioxidant defense system and osmolytes accumulations in stressed plants.

Water stress

Water stress is one of the severe environment constraints and affects the physio-biochemical processes, like growth, stomatal conductance, photosynthesis and stability of cellular components by the synthesis of ROS as well as secondary metabolites (Farooq et al. 2009; Osakabe et al. 2014; Hasanuzzaman et al. 2017). A survey of the available literature shows that TRIA plays a pivotal role in providing tolerance in crop plants exposed to drought, flooding and moisture stress. For example, PEG–induced drought stress in WL 2265 and Sonalika cultivars of Triticum aestivum L. seedling were treated with a mixture of aliphatic alcohol containing 30% TRIA, regulated the physiological changes by increased the seed germination, seedling growth, accumulation of free amino acids, soluble sugars, PEP- carboxylase activity (Thind 1991). Further, Muthuchelian et al. (1997) studied the growth and photosynthesis of water-stressed Erythrina variegata L. seedlings in response to leaf applied 1 gm−3 TRIA. The results obtained from their experiments indicated that TRIA enhanced the stress tolerance by increasing the root and shoot growth rate, RGR, LAI, total chlorophyll and carotenoids contents, carbon dioxide fixation, Rubisco activity and gs. Seedlings of olive varieties receiving a foliar spray of 40 ppm TRIA reversed the water stress-induced injuries by significantly increased water potential and osmolytes contents (Thakur et al. 1998). In jack pine seedlings, spray treatment of 10 µg L−1 TRIA reduced the effects of drought stress by reduced membrane injury (Rajasekaran and Blake 1999). Raghava and Raghava (2010) studied the germination characteristics of water-stressed Vigna unguiculata (L.) seeds in relation to TRIA application. They noticed that TRIA (miraculan) at low concentration (0.4–0.6 ml/L) effectively improved the germination parameters such as germination ability, relative seed germination, germination speed, radical and hypocotyls length, total seedling length and growth, thereby enhanced tolerance of cowpea plants to water stress. Sanadhya et al. (2012) reported that priming of Vigna radiata L. seeds with TRIA enhanced the tolerance ability against the PEG-induced drought stress by substantially increased the germination rate/percentage, root length, shoot length, seedlings fresh and dry weight. Similarly, Suman et al. (2013) found that 5 and 10 µg TRIA proved effective in restoring PEG-induced drought toxicity in rice seedlings by improving seed germination, seedling length, fresh mass, dry mass and activity of CAT, POD and SOD enzymes. Moreover, Perveen et al. (2016) studied the growth of drought-stressed maize cultivars in response to leaf applied 2 and 5 µM TRIA. Their data revealed that drought stress adversely affected the growth, altered soluble proteins, total phenolics, proline, glycine betaine (GB) content and NR activity. However, the treatment of 5 µM TRIA proved beneficial in modulating aforesaid growth and physio-biochemical attributes thereby augmented drought tolerance in Triticum aestivum L. cultivars. In conclusion, TRIA acts as a water stress protectant and promotes growth by improving photosynthetic attributes, modulating the level of antioxidants, osmoprotectants and membrane injury in water-stressed crop plants.

Temperature stress

Climate change leads to fluctuations in temperature. Chilling, freezing or heat stress is known to alter plant physiological and metabolic processes including seed germination, seedling growth, photosynthesis, transpiration, protein, enzyme inactivation, ROS accumulation, membrane disruption and tissue injuries which ultimately leads to plant death (Nahar et al. 2015; Hasanuzzaman et al. 2017; Ahanger et al. 2018). Under such conditions, TRIA acts as a stress protectant by way of increasing tolerance in plants (Naeem et al. 2012). For example, Cavusoglu and Kabar (2007) noticed that exogenously applied 10 µM TRIA overcame the effects of high-temperature stress on germination of Raphanus sativus L. and fresh weight of Hordeum vulgare L. Further, Borowski and Blamowski (2009) examined that TRIA clearly appeased the chilling-induced damages in Ocimum basilicum L. by improved the plant height, dry mass, chlorophyll content, PN, gs, and E rate and quantum efficiency. In a subsequent study, Borowski (2009) observed similar results in Cucumis sativus L. seedlings exposed to chilling stress. They noticed TRIA modulating the leaf chlorophyll content, PN, gs, E rate, CAT, POD activity, leaf proline content and electrolyte leakage under short-term chilling in Cucumis sativus L. Furthermore, Waqas et al. (2016) reported that leaf-applied TRIA augmented tolerance to heat stress as it promoted growth by modulating the endogenous level of abscisic acid (ABA) and Jasmonic acid (JA), amino acid, and nutrient content in Vigna radiata L. While going through the above researches, it may be inferred that TRIA is helpful to overcome temperature stress in plants by way of modulating various physiochemical process as well as concentration/levels of antioxidants, osmoprotectants and phytohormones.

Acid mist

Acid mist is one of the common environmental factor that significantly alters plant growth and physio-biochemical processes (Gadallah 2000). Exogenous application of 1 mg kg−1 TRIA protected the Erythrina variegata L. seedling from acid mist damage by modulating the plant biomass, leaf density, leaf area, chlorophyll, carotenoids, soluble proteins, starch content, leaf NR activity, photosystem (PS) I, II and RuBPC activity (Muthuchelian et al. 2003a). In another study, Muthuchelian et al. (2003b) noticed that spray treatment of 1 mg kg −1 TRIA ameliorated the acid mist induced toxicity by restoring the photosynthetic machinery in Samanea saman Jacq. seedlings.

Transplant shock

Transplanting temporary stagnates the plant growth and developmental processes. TRIA by acting as a stress modulator can suppress the adverse effects induced through transplant shock in plants. For example, a spray treatment of 10 µM TRIA proved most effective in restoring the transplant shock induced-growth inhibition and oxidative damage in rice seedlings by significantly enhanced sucrose content, CAT, POD activities and redox state of ASA and GSH (Li et al. 2016).

Cross talk/substitution with other plant hormones

The survey of literature revealed that the various metabolic processes such as embryogenesis, seed germination, seedling development, photosynthesis, leaf senescence etc. are upregulated via the interactions between various plant hormones (Ahmad et al. 2016; Per et al. 2018; Jogawat 2019). Studies depicted that TRIA along with other plant hormones regulates diverse metabolic processes in crop plants under both normal and stressful conditions. The literature on TRIA crosstalk with other plant hormones is scanty. It has examined both synergistic and antagonistic effects with other plant hormones. Application of TRIA and chloromequat chloride (CCC) resulted in an antagonistic effect on endogenous hormone levels when applied to Artemisia annua L. seedlings (Shukla et al. 1992). They noticed TRIA increased GA activity, but decreased ABA level, while as CCC showed reversed effect. TRIA had a synergistic effect with GA3 on growth, physio-biochemical, and yield attributes of treated crops such as Solanum lycopersicum L., Artemisia annua L. and Coriandrum sativum L. (Khan et al. 2007; Aftab et al. 2010; Idrees et al. 2010). TRIA also had an additive effect with benzyladenine (BA) or benzyl amino purine (BAP) and indole-3-butyric acid on growth and essential oil production in Thymus mastichina L. (Fraternale et al. 2003). Gatica et al. (2008) noticed the similar type of interaction with indole acetic acid (IAA) and BAP on somatic embryogenesis. Further, Verma et al. (2011) observed that TRIA and BA work in a synchronized manner by enhancing chlorophyll content, hill reaction activity and antioxidant enzyme activity in Arachis hypogaea L. Co-application of TRIA, homobrassinosteroids and sodium alginate, resulted in a synergistic increase in growth, physio-biochemical, yield and essential oils content in Mentha arvensis L. (Naeem et al. 2014, 2017). Additionally, application of TRIA restored the salt-induced inhibitory effects on Mentha piperita L. similar to GA, and SA treated seedlings (Khanam and Mohammad 2018). Similarly, Karam et al. (2017) revealed a mutually synergistic effect between NO and TRIA in reducing arsenic-induced damages in coriander. Studies at biophysical level (in model membranes or at organismal level) showed that TRIA and JA worked in antagonist way by opposing in expressing their function (Ramanarayan and Swamy, 2004; Swamy et al. 2009). Similarly, Soundararajan et al. (2018) observed the negative effect of TRIA and JA on in vitro rhizogenesis of tomato tissues. They further noticed that TRIA promoted growth and development by inducing the other growth-promoting substances, namely IAA, GA, UDP-N-acetyl glucosamine, gallate, trigonelline, serotonin as well as melatonin.

Conclusion

TRIA acts a potent PGR that can effectively modulate diverse plant physio-biochemical processes such as growth, photosynthesis and productivity of several groups of crop plants. TRIA deeply implicates in plant responses to environmental cues. TRIA improves the stress tolerance in crop plants by regulating the gene expression like photosynthetic and its associated genes, stress mitigating genes and levels of antioxidant (enzymatic and non-enzymatic), osmolytes, ROS and rate of lipid peroxidation against the environmental cues, such as acid mists, heavy metal, salinity, water and temperature stress, transplant shock etc. Foliar application of TRIA proved effective in regulating the growth and physio-biochemistry of various economically essential crop plants under normal and stressful conditions. From the above-appraised literature, it can be concluded that TRIA opens up new approaches for plants resistance against various environmental cues as it has great potential to nullify the stress-induced toxicity through modulating the stress-accrued alterations in morpho-physiological, biochemical and developmental processes of crop plants. However, there is need to carry out research work for its biosynthesis, mode of action and the receptors involved in signaling while regulating several developmental and metabolic processes in crop plants.

Acknowledgements

Shaistul Islam is thankful to University Grants Commission New Delhi India for providing the research fellowship.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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