The excessive uptake and accumulation of heavy metals, including cadmium (Cd), inhibit plants’ growth and development (Kranner and Colville, 2011; Haider et al., 2022). The presence of cadmium disturbs plant functions, such as uptake of water and mineral nutrients inhibition of photosynthetic machinery (Baryla et al., 2001). In addition, Cd stress causes the over a reduction of NADPH and thus cause an imbalance in electron transport from photosystem II (PSII) to photosystem I (PSI) and consumption of electrons in generating reducing equivalents, thereby resulting in ROS (reactive oxygen species) production. The generated ROS species at the PSI end can cause photoinhibition of PSII and PSI. Plants can avoid PSI photoinhibition by limiting the electron transport from PSII to PSI (lowering PSII activity) or re-routing electrons by providing alternative electron acceptors, such as cyclic electron transport (Taiz et al., 2015; Ogbaga and Athar, 2019; Shahzadi et al., 2021; Umer Chattha et al., 2021). These antioxidant enzymes scavenge ROS and protect the cellular structures (Bukhat et al., 2020; Askari-Khorasgani et al., 2021; Yasir et al., 2021). Photosystem II is more protected from ROS species than PSII by a battery of antioxidant enzymes (Taiz et al., 2015; Farid et al., 2018; Tikkanen and Grebe, 2018), which include superoxide dismutase (SOD), ascorbate peroxidase (APX), and catalase (CAT; Foyer et al., 2012; Foyer, 2018; Nazir et al., 2021). However, photoinhibition of PSII is protected by activating the xanthophyll cycle photoprotective component of non-photochemical quenching (NPQ). Sufficient evidence is available that demonstrates that various plant growth regulators, osmoprotectants, antioxidant signaling compounds can efficiently modulate nutrient uptake and transport, PSII activity, and antioxidants, thereby regulating plant growth under normal or stress conditions (Zhao et al., 2013; Athar et al., 2015; Ahmad et al., 2019; Ayyaz et al., 2021).

Jasmonate (JA) and methyl jasmonate (MeJA; methyl ester of JA) are well-known plant growth regulators that affect different biochemical and physiological processes (Yu et al., 2019; Bukhat et al., 2021), such as stomatal opening and photosynthetic activity (Yan et al., 2015). Several studies have shown that MeJA induces a stimulatory effect on photosystem II (PSII) photochemistry and photosynthetic pigments under normal conditions (Attaran et al., 2014; Qiu et al., 2020). While working with Brassica juncea Per et al. (2016) evidenced from transmission electron microscopy that MeJA protected the structure of chloroplast from cadmium toxicity. In addition, some studies showed that MeJA modulates the activities of some key antioxidant enzymes in different plants during heavy metal stress, such as in B. juncea (Per et al., 2016), Kandelia obovata (Chen et al., 2014), and Brassica napus (Farooq et al., 2018) Likewise, several studies showed that MeJA application in lower concentrations improved plant tolerance against abiotic stresses including Cd stress (Walia et al., 2007; Keramat et al., 2009; Per et al., 2016).

Pea (Pisum sativum L.) is one of the most crucial leguminous vegetable crop, whose yield is affected by Cd stress. Because of available information about MeJA, it is hypothesized that MeJA application might have improved the growth and yield of pea under cadmium stress. Although it is known that MeJA can change the PSII activity and activities of antioxidant enzymes, it is not yet known whether MeJA can also modulate solar energy absorption by PSII, and its distribution in electron transport or photochemistry and xanthophyll cycle under heavy metal stress conditions, including Cd stress. Since MeJA suppresses the growth and photosynthetic activity under stress conditions, when jasmonate signaling activates antioxidants enzymes and redirects metabolism from growth to defense, it is apt to assess up to what extent exogenously applied MeJA modulates the antioxidant mechanism and photosynthetic responses in pea plants to alleviate the adverse effects of Cd stress. The study’s secondary objective was to assess genotypic variability for these responses in local pea germplasm.

Plants are susceptible to heavy metal toxicity, including Cd. Cd inhibits plant growth via interference with cell division, hormonal homeostasis, photosynthesis, nutrient uptake, and enhancing oxidative stress (Rizwan et al., 2018; Huang et al., 2020; Dobrikova et al., 2021). In this study, the exposure of Cd considerably repressed the growth of pea plants, which is similar to earlier studies with different crop species (Huang et al., 2020; Shahzad et al., 2021; Wei et al., 2021). However, the toxic effects were compensated by the addition of MeJA. Previous research has shown that MeJA can modulate growth by altering antioxidant enzymatic activity increasing photosynthetic pigments and hormones under both biotic and abiotic stresses(Yan et al., 2015; Butt et al., 2019; Tayyab et al., 2020). In view of these reports, it is suggested that the ameliorative effect of MeJA on the growth of pea cultivars under Cd stress was possibly due to its impact on photosynthetic pigments, chloroplastic activity, and antioxidant enzymes.

Plant growth suppression caused by Cd is linked with changes in photosynthetic pigments, chloroplastic structures, and photosynthetic rate (Per et al., 2016; Qiu et al., 2020). In this study, Cd stress reduced the chl a, chl b, total chl, and carotenoids in pea leaves. The decrease in photosynthetic pigment content in three pea cultivars can be explained in view of some earlier studies in which it has been demonstrated that the high accumulation of Cd in leaves altered chlorophyll metabolism by affecting the activity of chlorophyll biosynthesis enzymes and chloroplast ultrastructure (Qiu et al., 2020). Application of MeJA increased photosynthetic pigments in pea cultivars. These results are analogous to earlier studies that demonstrated that MeJA promoted the accumulation of photosynthetic pigments in citrus (Qiu et al., 2020) and Vicia faba (Ahmad et al., 2017) exposed to metal stress.

The photosynthetic efficiency of plants is critical because it directly affects plant growth and productivity (Athar and Ashraf, 2005; Ogbaga et al., 2018). Cd stress significantly affected PSII structural and functional activity in all pea cultivars, which is in agreement with earlier research in which it was found that higher accumulation of Cd reduces the PSII structural ability and functional activity of Thellungiella salsuginea plants (Goussi et al., 2018). They explained it as Cd stress damages the PSII antenna and core resulting in reduced efficiency of PSII and impaired electron transport, as has been observed in this study. However, MeJA treatment enhanced the quantum yield [Y(II) and (Fv/Fm)] and electron transport rate ETR (II) of PSII. Several previous reports showed that MeJA improved photosynthesis-related attributes in Mentha arvensis (Zaid and Mohammad, 2018) and Triticum aestivum (Kaya et al., 2021) MeJA improved the parameters mentioned above.

On the other hand, increased energy dissipation in all Cd-stressed pea plants, as evidenced by elevated Y(NPQ) and Y(NO) values, indicates more energy loss along with reduced efficiency of PSII. This could be due to a reduction in carbon dioxide fixation in the Calvin cycle. Due to Cd stress, the production of excessive ROS denatures the D1 protein of PSII (Ruban et al., 2012). Usually, non-photochemical quenching gives a quick response and prevents ROS generation by dissipation of light energy in the form of heat through the antenna complex (Lambrev et al., 2012).

In plants, heavy metal toxicity usually causes oxidative stress due to excessive ROS production, including O²⁻, H₂O₂, and ^·OH. These compounds are highly reactive and toxic; they cause membrane damage and oxidize macromolecules like carbohydrates, proteins, lipids, and DNA (Gill and Tuteja, 2010). Cellular damage caused by heavy metal stress results in the increased production of H₂O₂ that ultimately enhances the peroxidation of membrane fatty acids leading to increased MDA content. MDA is commonly used for plants as the marker for lipid damage and lipid peroxidation that disrupts membrane fluidity, enhances electrolyte leakage, inhibits enzymes’ activity, and interferes with protein channeling (Garg and Manchanda, 2009). In the present study, exposure of pea plants with Cd stress increased the H₂O₂ and MDA content. These results were similar to many studies conducted on P. sativum (Romero-Puertas et al., 2004) and Vigna radiata (Ahmad et al., 2011). The supplementation of MeJA to Cd-stressed pea plants significantly reduced the H₂O₂ and MDA levels indicating that MeJA has the potential to overcome oxidative stress found in intracellular membranes and cell membranes of all pea cultivars. A study supporting this conclusion showed that the application of MeJA enhanced the enzyme activities (APX, CAT, and SOD) of Bunium persicum plants exposed to Cd stress. These results were further supported by Chen et al. (2014), who demonstrated that supplementation of JA reduced MDA concentration in Kandelia obovate in response to Cd stress.

As discussed above, antioxidative machinery can scavenge ROS and protect plants against oxidative damage. In the present study, the increased antioxidant enzyme activities (CAT, POD, and SOD) correspond to those levels observed in B. juncea (Ahmad et al., 2016), Solanum lycopersicum (Cherif et al., 2011), and P. vulgaris (Rady, 2011). Moreover, in Capsicum frutescens plants, JA supplementation to Cd-stressed seedlings increased antioxidative enzyme activities and chlorophyll production (Yan et al., 2015). The application of JA also improved tolerance against Cd stress by increasing phytochelatin levels and activating defense-related genes (Maksymiec et al., 2007). Enzymatic activities enhanced by the JA supplementation can be attributed to the direct association with radicals, such as superoxide. It might be due to cells’ improved ROS quenching capability by producing antioxidative enzymes (Hsu and Kao, 2007; Sirhindi et al., 2016). Overall, MeJA-mediated improvement against Cd toxicity in lipid membranes appears to be linked to increased antioxidant ability.

Furthermore, cadmium present in nutrient solution and soil can be easily absorbed by plants’ roots and transferred to other plant tissues. The highest Cd content in leaves was found in this investigation, which was remarkably lowered by MeJA treatment. Heavy metals usually compete with Zn²⁺, Ca²⁺, Fe²⁺, Mg²⁺, and Mn²⁺ cations to access root cells through these cations transporters. It can be assumed that MeJA treatment enhanced the physiological parameters of all pea varieties and increased the uptake of valuable cations, decreasing Cd content and Cd²⁺ influxes in pea plants, similar to a previous study conducted on tomato plants (Wei et al., 2021). JA application reduced the uptake of Cd and improved antioxidant machinery in Kandelia obovata (Chen et al., 2014). However, the underlying mechanisms concerning how MeJA lowers the uptake of Cd are still unknown.

In the present study, Cd stress caused the higher Cd accumulation in pea plants, disturbing the metabolism for photosynthetic pigment biosynthesis and damaged photosynthetic machinery. Application of MeJA reduced the toxic effects of Cd on photosynthetic pigments and maintained the PSII activity by lowering uptake of Cd, downregulation of electron transport from PSII to PSI, increase in the photoprotective component of NPQ, and partial increase in activities of antioxidant enzymes. This helped the plants maintain cellular redox balance, thereby resulting in lower membrane damage. Thus, it can be inferred that the MeJA-induced growth improvement is related to (i) reduced Cd uptake by roots, (ii) optimization of the photosynthetic apparatus or photosynthetic rate, and (iii) enhanced antioxidant activity.

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found in the article/supplementary material.

SR: conceptualization and supervision. SR and HM: methodology. SR, H-u-RA, and SN: validation. MR and ZZ: formal analysis. Mehwish and SB: investigation. SR: resources. Mehwish: data curation. SB: writing—original draft preparation. MS, MB, WS, SR, HM, H-u-RA, MR and AE: writing—review and editing. SN and MR: visualization. HM: project administration. CCO: writing—review and editing. All authors contributed to the article and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.