Maize or corn (Zea mays L.) is considered an internationally important commodity driving world agriculture. In India, the annual production of maize is 27.82 million metric tons with average national productivity of 3.02 tons per hectare (FAOSTAT, 2018). It is grown during Kharif (June–October), Rabi (October to March), and spring (March–June) seasons; however, major production is achieved during the rainy season (Yadav et al., 2015). The production of maize is influenced by numerous biotic stresses, with one of the primary challenges being its susceptibility to various diseases. This susceptibility to diseases poses a significant obstacle to achieving high grain yields in maize cultivation. Banded leaf and sheath blight (BLSB) is a major disease and most prevalent in tropical regions of the world, in south and southeast Asian countries, and specifically in India during the Kharif season. The disease causes losses of up to a hundred percent under favorable conditions (Anonymous, 2017; Devi and Thakur, 2018). BLSB is caused by the soil-borne pathogen Rhizoctonia solani [R. solani f. sp. sasakii (Kuhn)], which is generally identified by the characters of mycelia and sclerotia. The pathogen is recognized as one of the most prevalent, destructive, and adaptable fungi found across many regions worldwide. It has the ability to infect plants from a wide range of taxonomic groups, affecting 32 families and 188 genera of crops such as cereals, millets, pulses, and oilseeds, as well as grasses and weeds (Devi and Thakur, 2018). Cereals are infected by the pathogen belonging to the AG 1-1A anastomosis group of R. solani (Wang et al., 2013). In maize, the disease starts from the first leaf sheath and extends up to the ears to cause maximum damage. High relative humidity and rainfall significantly favor the development and rapid spread of this disease.

The disease is manageable to some extent using single or combinations of different management strategies like cultural, chemical, and biological. Thus, for identifying climate-resilient components, immediate attention is required and, due to the present changing climate, integrated disease management (IDM) is considered the best module for the management of BLSB. Resistance of host plants plays a significant role in the IDM approach. Therefore, identifying resistance genes to this aggressive disease and combining them with high grain yield potentiality is a priority of the Indian maize breeding program. However, BLSB-resistant cultivars are scarce. Limited variation for resistance to BLSB is a major bottleneck for an effective resistance breeding program. Identifying genotypes with genetic resistance, i.e., the capacity to restrict blighted lesion expansion, is quite difficult among maize germplasm as experienced in rice against the same fungus. However, national programs in India, China, Indonesia, and the Philippines are making efforts toward screening genotypes for BLSB resistance. In the All India Coordinated Research Project (AICRP) on maize, both inbred and hybrids have been evaluated for their reaction against BLSB, and some lines with a moderate level of resistance were identified (Hooda et al., 2015). Under such circumstances, chemically induced resistance in the host plant is considered a new potential strategy against many fungal diseases.

Salicylic acid (SA) is a plant growth regulator which plays a significant role in signaling pathways induced by various biotic and abiotic stresses (Saleem et al., 2021). It achieves this by regulating various aspects, including the antioxidant defense system, transpiration rates, stomatal movement, and photosynthetic rate (Nazar et al., 2015). Exogenously applied SA has been observed to induce both local and systemic acquired resistance in diverse plant species against a range of pathogens, such as Fusarium oxysporum (Jendoubi et al., 2015), Penicillium digitatum/Alternaria alternata (Allahverdi Beyk et al., 2021), Magnaporthe grisea (Yang et al., 2019a), Colletotrichum gloeosporioides (He et al., 2017), Xanthomonas spp. (Le Thanh et al., 2017), viruses (Ong and Cruz, 2016; Zhao et al., 2019), and phytoplasma (Ahmed et al., 2022). For instance, in China, foliar application of different concentrations of SA ranging from 0.1 to 5.0 mM resulted in direct and systemic effects on chemical defense responses with an increase in content of total phenol, DIMBOA (2,4-dihydroxy-7-methoxy-2H,1,4-benzoxazin-3(4H)-one), and a significant increase in activity of superoxide dismutase (SOD), polyphenol oxidase, peroxidase, and catalase (Feng et al., 2022). Recently, in Thailand, an SA formulation called Zacha was tested and exogenous application of the same could significantly inhibit the growth of soil-borne fungi Fusarium solani and significantly reduced the disease severity of Fusarium root rot in cassava at 500 ppm (Saengchan et al., 2022). A remarkable resistance against Curvularia lunata was induced in maize when treated with different chemical compounds, including SA. SA, in particular, showed significant effectiveness, resulting in a disease reduction of 49.6% (Chengbo and Huazhi, 2005). In addition to priming the plant for disease resistance, SA has also been reported to ameliorate abiotic stress. In Iran, SA as seed treatment at a concentration of 0.5 mM resulted in the alleviation of lead toxicity by modulating glyoxalase I activity and thereafter reducing methylglyoxal accumulation (Zanganeh et al., 2020). Another study in Saudi Arabia demonstrated that at a concentration of 0.05 mM, SA improved the salinity stress tolerance in maize by regulating phytochromes as well as various organic and inorganic osmolytes (Elhakem, 2020). The role of jasmonic acid (JA) in plants has received extensive research attention due to its crucial roles in mediating plant responses and defenses against biotic and abiotic stresses when applied exogenously in small amounts (Wang et al., 2021). Reports also suggest that plants can defend themselves against necrotrophic pathogens and insects through JA signaling (Liu et al., 2017). Feng et al. (2012) demonstrated that the application of JA had a systemic effect on the quantities of defense chemicals in both the aboveground and belowground parts when either of them was continuously treated with JA. Additionally, it was observed that the phenolic and DIMBOA contents significantly increased after 2–4 weeks of application. Girault et al. (2008) observed that, compared with the control group (18.65%), the exogenous application of the lipid transfer protein–jasmonic acid complex resulted in a remarkable resistance of 80.3% against Botrytis cinerea. Induction of systemic resistance with increased catalase, polyphenol oxidase, and peroxidase activity in cucumber and excellent efficacy of JA against Pythium aphanidermatum was documented by Sabbagh et al. (2018). Like SA, JA has also been shown to alleviate lead stress by improving the physiological processes and enhancing the ability of maize plants to overcome oxidative damage by inducing the activity of antioxidant enzymes such as SOD, peroxidase, catalase, and glutathione and also phenol, ascorbic acid, and total soluble sugar (Sofy et al., 2020). Similarly, salinity tolerance was found to be improved by the exogenous application of JA (Ali et al., 2020). Thus, disease resistance in host plants induced by the exogenous application of SA and JA can be a boon in cost-effective disease management without any ecological consequences. Furthermore, this type of resistance is governed by the accumulation of PR proteins that are known to be associated with systemic acquired resistance (SAR) in plants (Ali et al., 2018; Jain and Khurana, 2018). Despite these observations, the exact mechanism exerted by these inducers through different modes and timings of application remains vague. Further extensive studies are required to elucidate this mechanism. Nevertheless, it has been noted that these inducers interact in a complex manner with the antioxidative metabolism, leading to the modulation of cellular redox homeostasis and ultimately resulting in the activation of defense genes (Hernández et al., 2017; Jabnoun-Khiareddine et al., 2015).

Based on the aforementioned background, the objective of the present investigation was to gather information regarding the management of BLSB disease through the application of plant defense inducers, specifically SA and JA. Additionally, the study aimed to assess the positive effects of these inducers on maize germination and biomass, as well as their in vitro antifungal effect against R. solani f. sp. sasakii. Furthermore, the study aimed to gain insights into the underlying mechanisms of chemically induced disease resistance in maize.

The present study generated information on the management of BLSB disease utilizing plant defense inducers and elucidated the biochemical mechanisms of disease resistance in maize. Chemically induced disease resistance could serve as a viable alternative to true resistance in maize varieties lacking resistance to BLSB. Thus, two plant defense inducers, viz., salicylic acid (SA) and jasmonic acid (JA), were tested in vitro against R. solani and in vivo for restriction of the BLSB disease of maize.

SA being an endogenous growth regulator of phenolic nature can positively influence a range of diverse processes in plants, including percent seed germination, vigor index, mean germination time, plant height, number and area of green leaves (check leaf chlorophyll degradation), stem diameter, and dry weight of the whole plant of cereal crops (Anwar et al., 2013; Alamri et al., 2018; Zhu et al., 2021). Similarly, JA, known as lipid-derived phytohormones, can also regulate overall plant growth under both abiotic and biotic stresses (Siddiqi and Husen, 2019).

Our study demonstrates a positive impact of SA and JA on germination with the increase in the concentration of SA and JA. In the case of the net house condition, a significantly better germination percentage was observed at higher concentrations of JA and SA (100 ppm). The improved germination observed with SA treatment can be attributed to the augmented uptake of oxygen and enhanced α-amylase activity, consequently leading to efficient mobilization of nutrients from cotyledons to the embryonic axis, resulting in increased levels of soluble sugars, amino acids, and proteins (Fardus et al., 2018). A similar positive impact on germination was reported by Ilyas et al. (2017), where they observed the application of SA and JA acid on wheat under drought-ameliorated stress with the increase of germination by 21% and 27%, respectively, which under stress was reduced by 26%. Moreover, an increase in the shoot length by 20% and 23%, respectively, was recorded. However, in contradiction to the present study, a plant (Lavandula angustifolia Mill.) grown in SA-free media could produce healthier and more shoots than the plant grown in SA-treated media. However, plants grown with amended elicitor media were found to have higher polyphenolic and chlorophyll content than the controls, proving a positive impact on the secretion of secondary metabolites (Miclea et al., 2020). In harmony with our findings, Fardus et al. (2018) recorded improved germination and various growth parameters with application of SA exogenously.

In our study, we observed an increase in biomass in maize seedlings treated with SA and JA. However, this increase was found to be statistically insignificant. The increase in biomass can be primarily attributed to changes in hormone functioning or an enhancement in photosynthesis and stomatal conductance, and these factors collectively contribute to the overall growth (Ibrahim et al., 2017). Another possible reason for the increase in biomass could be the induction of meristematic cell division (Vanacker et al., 2001). Furthermore, the increase in biomass could also be attributed to the improvement in the photosynthetic activity of the plant treated with SA or JA at an optimum concentration, which in turn enhances the plant’s ability to produce more glucose, resulting in the accumulation of biomass. (Bukhat et al., 2020; Noor et al., 2022; Li et al., 2023). They improve plant growth through their regulation of various processes. It influences stomatal movements, ensuring optimal gas exchange and water balance. It also plays a role in regulating Rubisco biosynthesis, a key enzyme involved in photosynthesis. Additionally, they enhance the uptake of essential nutrients such as phosphorus and nitrogen, promoting healthy plant growth. Furthermore, it facilitates the efficient transport of carbohydrates within plants, ensuring an adequate supply of energy for growth and development (Fu et al., 2017: Wasternack and Hause, 2013). In concurrence with the current findings, the promotion of dry leaf mass and dry root mass of fennel (Foeniculum vulgare Miller) at a concentration of 0.50 and 0.25 mM of SA, respectively, was documented (Gorni et al., 2017). Similarly, when studying Brassica juncea plants treated with 0.01 mM SA, significant increases in dry root mass (26%) and shoot growth (51%) were reported (Parashar et al., 2014). Further supporting our findings, Bukhat et al. (2020) also observed an increase in root and shoot biomass of radish when treated with 2 mM of SA by 2.89- and 2.80-fold, respectively. In a recent study, it was observed that the exogenous application of JA (120 mM) during salt stress significantly increased the fresh weight, dry weight, root length, and photosynthetic pigments of two soybean varieties, namely, parachinar-local soybean and swat-84 (Noor et al., 2022). In line with our findings, Awan et al. (2021) also demonstrated an increase in fresh and dry weight, shoot, and root length in pearl millet upon treatment with 100 µM of JA. Under in vivo conditions, the PDI of BLSB was significantly reduced to 46.79%, 47.05%, and 48.85% with SA at 100 ppm, SA at 75 ppm, and JA at 100 ppm, respectively (Table 3), compared with the control (69.09%). Moreover, the yield was also significantly increased with different concentrations of inducers, highest at SA@100 ppm with 52.13 × 100 kg ha⁻¹ of grain yield. The decrease in PDI is mainly because of the induction of several defense biochemical pathways. Also, SA and JA cause early defense-related gene induction and late defense-related gene induction in plants, respectively, protecting them from pathogens and insects (Yang et al., 2019b). Application of SA to plants renders the expression of pathogenesis-related genes and other defensive compounds at local and systemic levels conferring immunity (Sivakumar et al., 2014; Wani et al., 2017). Possibly, the exogenous application of SA leads to the accumulation of endogenous SA, which plays a crucial role in conferring disease resistance through the activation of the SA signaling pathway, primarily associated with systemic acquired resistance (SAR). Exogenous treatment with SA to rice has been found to reduce disease severity of blast disease caused Magnaporthe oryzae by inducing the expression of defense-related genes such as PAL, PR1a, PR5, and HSP90 (Yang et al., 2019a). Intriguingly, an SA-based abiotic elicitor called S-Ricemate at 100 ppm or more was demonstrated to reduce the disease severity of leaf blight caused by Xanthomonas oryzae pv. oryzae by 17.71%–12.50% as compared with control (Thepbandit et al., 2021). Earlier results indicated that the jasmonate response reduces damage caused by a wide range of pathogens from different lifestyles in tomatoes (Thaler et al., 2004). In agreement with our findings, Meyer et al. (2006) also reported that SA (2.5 mM) sprayed 20 days before disease inoculation significantly reduced Rhizoctonia foliar blight infection and observed that resistance activators performed better on Rhizoctonia foliar blight control when applied together with fungicides. In concurrence with our results, Ziasmin Islam et al. (2017) observed the dose-dependent effect of SA as a foliar spray on morphological and yield-contributing characters of wheat such as tiller number, effective tiller numbers/plant, spike length, number of spikelets/spike, number of effective spikelets/spike, and number of grains/spike that accredited higher grain yield. Similarly, seed priming with SA could significantly influence the wheat grain filling rate and duration, grain yield, grain protein percent, and total weight of dry seed (Khamseh et al., 2013). In addition, Elgamaal and Maswada (2013) recorded significant enhancement in total chlorophyll, flag leaf area, relative water content, and grain yield with the increase in the concentration of SA in three yellow maize hybrids. Furthermore, exogenous application of SA not only alleviated the inhibitory effect of drought stress but also had a stimulatory effect on physiological traits and grain yield of tested maize hybrids, and hence they opined that foliar application of SA at 0.5 and 1.0 mM is beneficial for boosting the productivity of maize plants apart from higher tolerance to drought stress. It has been also observed that the pretreatment or exogenous application of JA exhibited multi-stress resilience under changing environments, biotic stress conditions (Siddiqi and Husen, 2019) as well as abiotic stress like herbicide (imidacloprid) toxicity in plants (Sharma et al., 2018). Based on previous reports and current findings, it is possible to postulate that an increase in yield may be attributed to the enhancement of various physiological characteristics of plants like source–sink relationship, which directly or indirectly contribute to yield improvement.

In the study, defense inducers exhibited fungicidal properties, and comparatively, SA performed better than JA. SA at 100 ppm could reduce radial growth and weight by 30.37% and 51.99%, respectively. Hence, utilization of SA may contribute dual benefits, viz., acting against the growth of the pathogen and induction of host defense mechanism to contain disease spread. Contrary to our findings, Meyer et al. (2006) reported no mycelial growth inhibition of R. solani causing Rhizoctonia foliar blight of soybean when the concentration of SA was below 10 mg L⁻¹. In another in vitro test, SA did not exert a direct antifungal effect on the mycelial growth of Fusarium oxysporum f. sp. lycopersici. These results indicated the role of SA in the plant to activate the SA pathway leading to induction of antimicrobial peptides such as PR-1 which directly affect the invading fungal pathogen (Mandal et al., 2009). However, in a study conducted by da Rocha Neto et al. (2015), 90% inhibition of fungal germination after 30 min of exposure to the SA was observed with apparent damage to the plasma membrane of conidia, resulting in protein leakage. The antifungal activity of SA was also demonstrated by its ability to induce certain compounds such as phenol-2,4-bis-(1,1-dimethylethyl) against Aspergillus sp. Penicillium cinnamomi in avocado (Rangel-Sánchez et al., 2014). The antimicrobial activity of SA as observed by the reduction of radial growth and weight of mycelia in our study could be attributed to its ability to directly penetrate and initiate multiple interactions with the plasma membrane, which results in the disruption of the lipid bilayer and potential damage to the proteins involved in maintaining cellular permeability. These effects ultimately contribute to an increase in the concentration of reactive oxygen species. In addition, cellular respiration can also be disrupted by redirecting the electron flow away from the cytochrome pathway toward an alternative pathway associated with cyanide (Kapulnik et al., 1992).

The activity of the host defense induction indicative enzymes SOD, CAT, and PAL was assayed in maize (Vivek QPM-9) inoculated with R. solani after treatment (seed treatment) with the plant defense inducers, viz., SA and JA. SOD, which is a widespread metalloenzyme (Jackson et al., 1978), forms the primary defense against reactive oxygen species (ROS) and serves as a highly efficient component of the antioxidant defense system in plant cells, countering ROS toxicity. It plays an important role in the development as well as stress resistance in plants (Cannon et al., 1987). SOD genes catalyze the superoxide radicals ( O 2 - ) into H₂O₂, to protect plant cells against oxidative stress (Dos Santos and Rey, 2006; Hossain et al., 2009). On the other hand, CAT catalyzes hydrogen peroxide conversion into water and oxygen without requiring cellular energy consumption, and it is a major H₂O₂ scavenging enzyme in all aerobic organisms (Ghasemi et al., 2013; Sharma and Ahmad, 2014). PAL is an inducible enzyme that responds to various biotic and abiotic stresses, including pathogenic attacks (MacDonald and D’Cunha, 2007). Its induction is triggered by these stresses, highlighting its role in plant defense mechanisms. PAL is involved in the phenylpropanoid pathway and facilitates the synthesis of cinnamic acid from phenylalanine (Vogt, 2010). Additionally, PAL is actively involved in the biosynthesis of salicylic acid (SA), which serves as a vital signal in plant systemic resistance (Chaman et al., 2003). We observed the activities of all three enzymes, viz., SOD, CAT, and PAL, highest at a concentration of 100 ppm of SA and JA as compared with the control. SA as an endogenous signal molecule playing an important role in the development of systemic resistance in plants is well established (Dempsey et al., 1999). Moreover, SA confers an anti-stress role by stimulating the expression of genes involved in the biosynthesis of antioxidants, thereby enhancing the antioxidant potential of plants further contributing to the plants’ ability to mitigate the harmful effects of stress (Najafabadi and Ehsanzadeh, 2017; Wang et al., 2019). JA regulates plant responses to abiotic and biotic stresses as well as plant growth (Wang et al., 2021). It has an important role in response to the wounding of plants and SAR. The Dgl gene is responsible for maintaining levels of JA during usual conditions in Zea mays as well as the preliminary release of JA immediately after being fed by insects (Galis et al., 2009).

In support of our findings, recently, Khalvandi et al. (2021) demonstrated a significant increase in the activity of enzymatic antioxidants in wheat under drought conditions, viz., PAL, SOD, and CAT by 18.18%, 42.16%, 56.6%, respectively, when SA (0.5 mM) was exogenously applied. Another study also documented an increase in SOD and CAT activity after 7 days with exogenous JA treatment by 48.6% and 36.7% (Awan et al., 2021). In concurrence with our results, Jini and Joseph (2017) observed an increase in SOD and CAT activity in rice varieties ASD16 and BR26 treated with SA (1 mM L⁻¹). Similarly, SOD enzyme activity was found significantly raised in the leaves, skin, and flesh of grapes (Vitis vinifera L.) by the SA treatment at the 1 mM dose (Nazari et al., 2022). As observed in the present study, enhancement of PAL activity was reported in response to R. solani inoculation in cowpea pretreated with SA (Chandra et al., 2007). Similarly, SA spraying on Ya Li pear plants increased PAL activity greatly and contributed to the protection of pear fruits against postharvest diseases (Cao et al., 2006). In addition, in support of our findings, the PAL activity was found to increase to a greater extent in SA-treated tomato plants compared with non-SA-treated plants, which probably enhanced resistance in tomatoes to Fusarium oxysporum f. sp. lycopersici (Mandal et al., 2009). The results of the present study indicate that SA and JA serve as effective inducers of disease resistance in host plants, functioning as potential triggers for systemic resistance. This induction is supported by the activation of essential defense-related enzymatic antioxidants. As a result, the application of SA and JA significantly reduced the incidence of BLSB disease in maize caused by the soil-borne pathogen R. solani. In regard to R. solani, it is presumed that ROS favors the pathogen by rendering cell death as, being a necrotroph, it requires dead cells for its nutrition. Antioxidant enzymes scavenge free radical and hence keeps the ROS concentration under check, therefore possibly indirectly preventing the ingression of the pathogen.

The findings of this study have demonstrated the reduction of disease severity/PDI of BLSB due to the induction of resistance in maize upon exogenous pre-treatment with SA and JA, as evidenced by the activation of defense-related enzymes, namely, SOD, CAT, and PAL. In addition, a significant increase in the yield of maize was also discerned. The abiotic defense inducers SA and JA also testified to suppress the necrotrophic soil-borne phytopathogen R. solani under in vitro conditions. Furthermore, seed priming with the inducers contributed to promotion of germination and biomass of the maize indicating a positive role in the growth and development of maize plants, opening the scope for quality fodder production as well. Maize being an exhaustive crop requires high inputs in crop culture and pest management. Under such circumstances, our study is able to project light on the scope of reducing large quantities of fungicides used for the management of fungal diseases of maize, adopting a plant defense inducer-mediated host resistance approach, upholding a safe environment as well.

The original contributions presented in the study are included in the article/Supplementary Material. Further inquiries can be directed to the corresponding authors.

AK supervision and provided lab facilities. AS supervised biochemical aspects and provided lab facilities. RG conceptualized and designed experiments, supervised, provided resources, and revised and finalized the manuscript. RY supervised field experiments. SH conducted experiments, generated data, and wrote the first draft of the manuscript. LD revised and edited the manuscript. All authors have read and approved the manuscript.