The major pollutants in the soil are heavy metals. The major heavy metals causing soil contamination is cadmium (Cd), which far exceeds the contamination due to other heavy metal elements (Riaz et al., 2021). As a non-essential element, excessive Cd causes toxicity and affects the growth of plants (Garg et al., 2015; Vatehová et al., 2015). Cadmium has strong biotoxicity and transferability in soil and can be absorbed by plants (Anna et al., 2015). After entering the human body through the food chain, Cd causes toxic effects on some internal organs and damages the human body’s immune system and reproductive system (Xie and Xu, 2003). In recent years, paddy fields have been severely contaminated by Cd, threatening human health (Song et al., 2015; Zhang et al., 2020). So, it’s important to remediate Cd-contaminated soil, specifically the Cd-contaminated paddy soils. Many methods have been used to remediate Cd-contaminated soils (Mahmoud et al., 2021; Wang et al., 2021). Among these, phytoremediation is one of the best biological methods used for extracting, fixing, and concentrating the Cd from the soil through Cd-hyperaccumulators; it is an environmentally friendly approach (Guo and Yang, 2015; Shaheen and Rinklebe, 2015). However, the screened Cd-hyperaccumulators have the problems of low biomass and slow growth, which limit the phytoremediation effects (Guo and Yang, 2015). Therefore, it is necessary to improve the phytoremediation capabilities of these known hyperaccumulators.

Application of plant hormones can be used as a new method to improve the phytoremediation capabilities of hyperaccumulators (Rostami and Azhdarpoor, 2019). The plant hormone salicylic acid (SA) is an intracellular signaling molecule in plants (Kawano and Bouteau, 2013). SA mediates the plants to adapt the abiotic stress (Azooz and Youssef, 2010) and improves plant resistance by increasing photosynthesis and antioxidant enzyme activity, thereby slowing down the damage caused by adversity (Song et al., 2014). Under heavy metal stress, SA improves the resistance of plants (Song et al., 2014; Sofy et al., 2020). SA treatment increased the antioxidant enzyme activity of cauliflower under Cd stress and alleviated the cell damage under Cd stress (Chen, 2009). The peroxidation of barley root tips was inhibited when treated with SA under Cd stress (Tamás et al., 2015). For rice, SA treatment increased its antioxidant enzyme activity and decreased the H₂O₂ content to enhance the resistance to Cd stress (Guo et al., 2007); this also decreases the rice Cd content (Majumdar et al., 2020; Pan et al., 2021). Various other studies have shown similar effects of SA on mung beans, kidney beans and tomatoes under Cd stress (Tissa et al., 2000; Khan et al., 2021). In addition, SA also has demonstrated the effects on hyperaccumulators. SA increased the Cd content and transportation factor and improved the phytoremediation capability of Helianthus tuberosus to Cd (Chen et al., 2011). So, SA could improve the tolerance of plants to Cd stress and enhance the phytoremediation capability of hyperaccumulators; however, there are few studies on the response of the SA-treated hyperaccumulators.

Nasturtium officinale is a genus of cruciferous watercress plants emerging as a Cd-accumulator (Lin et al., 2015). Nasturtium officinale has strong vitality, vigorous growth, wide distribution, and short growth cycle (Chen et al., 2006). However, compared with other Cd-hyperaccumulators (Wei et al., 2004; Zhang et al., 2011b; Zhang et al., 2013), the N. officinale phytoremediation capability needs to be improved. Therefore, the present study aimed to improve the phytoremediation capability of N. officinale and analyzed the effects of SA on the growth and Cd accumulation of N. officinale. The aim of this study was to screen the optimal SA concentration that could improve the N. officinale phytoremediation capability and provide a reference for remedying the Cd-contaminated paddy fields.

The plant hormone SA promotes the growth of plants at an optimal concentration but inhibits plant growth at higher concentrations (Kawano and Bouteau, 2013). Under heavy metal stress, SA can induce the increase in activity of H⁺-ATPase and alleviate the inhibitory effect of this stress on the absorption of mineral elements (Shi and Zhu, 2008). Under Cd stress, SA alleviated the Cd stress and promoted the growth of maize (Krantev et al., 2008). In this study, SA at 100, 150, and 200 mg/L increased the N. officinale biomass, while at 250 mg/L decreased the biomass. These results are consistent with previous reports (Kawano and Bouteau, 2013; Liu et al., 2022), which showed that SA at 100 to 200 mg/L promoted the growth of N. officinale and at 250 mg/L inhibited. The reason is that SA can not only enhance the root vitality, and promote the absorption of nutrients by roots, but also affect cell division by regulating the content of some hormones in plants (Chavoushi et al., 2020). This promotion effect of SA may be related to the increase in plant resistance to Cd (Pál et al., 2005; Zawoznik et al., 2007; Kováčik et al., 2009).

Typically, Cd stress changes the chloroplast ultrastructure and affects the net photosynthetic rate and leaf transpiration, reducing the photosynthesis of non-hyperaccumulator plants (Souza et al., 2011). Meanwhile, SA alleviates the Cd stress inhibition of photosynthetic parameters by protecting the photosynthetic pigments (Popova et al., 2009; Shi et al., 2009). SA treatment increased the chlorophyll content and enhanced the resistance of potatoes to Cd stress (Li et al., 2019). Similar results were observed in ryegrass too (Bai et al., 2015). In this study, SA at 150 mg/L increased the chlorophyll a and b contents in N. officinale under Cd-contaminated conditions but at 100 and 200 mg/L decreased the chlorophyll a/b. SA at other concentrations had no significant impact on the contents of chlorophyll a, b, or chlorophyll a/b. Meanwhile, none of the SA concentrations significantly influenced the carotenoid content. SA helps the plants to uptake and transport nutrients and thus increases the photosynthetic pigment content (Krantev et al., 2008). These results differ from the effects of SA on Cyphomandra betacea (Liu et al., 2022), indicating that different plants respond differently to SA concentrations.

In plants, H₂O₂ acts as a second messenger for growth, mediating various physiological and biochemical processes; however, excessive H₂O₂ induces oxidative stress (Zhang, 2018). SA and H₂O₂ play significant roles in plant stress resistance and have a specific interaction with each other (Zhang et al., 2011a; Zhang, 2018). Under Cd stress, SA removes the reactive oxygen species (ROS) by regulating the antioxidant enzyme activities (Zhang et al., 2011a). In this study, 250 mg/L SA increased the POD activity of N. officinale under Cd-contaminated condition, and 150, 200, and 250 mg/L SA increased the CAT activity. These results are not completely consistent with the previous report on Cyphomandra betacea (Liu et al., 2022) but consistent with the observations in pea (Popova et al., 2009; Khan et al., 2021), indicating that SA has different impacts on the various plants’ antioxidant system. On the other hand, SA inhibits the activity of key enzymes, including POD, polyphenol oxidase, and phenylalanine ammonia lyase, to slow down lignin synthesis, delaying senescence (Wu et al., 2006). These results reflected that SA improved the resistance of N. officinale to Cd. Besides, SA could alleviate oxidative damage under Cd-contaminated conditions. In addition, SA at 150, 200, and 250 mg/L concentrations decreased the SOD activity of N. officinale, and at 100, 150, 200, and 250 mg/L concentrations decreased the soluble protein content, which is not consistent with the previous reports (Wang et al., 2009; Liu et al., 2022). Because plants synthesize Cd-containing free amino acids, decreasing soluble protein content; however, a few important soluble proteins may not be seriously affected (Krantev et al., 2008), which needs further study.

Under high pH (pH > 6.0), the soil Cd exists as insoluble compounds formed through complexation, chelation, and precipitation, thereby reducing the soil available Cd concentration. With the decrease in pH, other forms of soil Cd are easily converted into exchangeable Cd, increasing the soil available Cd concentration (Dou et al., 2020). In this experiment, only 250 mg/L SA decreased the soil pH, indicating that SA stimulated the plant roots to secrete organic acids to acidify soil (Li et al., 2008). The different concentrations of SA increased the soil exchangeable Cd concentration; moreover, soil exchangeable Cd concentration was negatively correlated with soil pH. This observation is consistent with the previous study (Dou et al., 2020), which showed that beneficial for Cd uptake in N. officinale. SA decreased the Cd contents in roots and leaves of tomato and in various organs of Populus deltoids × P. cathayana under Cd stress (Wang, 2016; Wang et al., 2019). In rice, SA decreased the Cd accumulation in grains and ears at grain filling and maturity stages but increased the Cd accumulation in leaves at maturity stage. However, no significant impact of SA was observed on Cd accumulation in rice roots and stems (Liu, 2016). In this experiment, only 200 and 250 mg/L SA increased the N. officinale root Cd content, and 150, 200, and 250 mg/L SA increased the shoot Cd content. SA at 100, 150, and 200 mg/L concentrations increased the root Cd extraction and shoot Cd extraction. These results are consistent with the hyperaccumulators studies (Chen et al., 2011) but different from the reports on non-hyperaccumulators (Wang, 2016; Wang et al., 2019). Thus, our observations confirm that SA could promote the N. officinale Cd uptake for two reasons: (1) SA improved the N. officinale resistance to Cd, thus enhancing the Cd absorption capacity of N. officinale. Because the correlation analysis showed that both the root Cd and shoot Cd contents were positively correlated with the POD activity and CAT activity. (2) SA stimulated the plant roots to secrete organic acids to decrease the soil pH, thus increasing the soil available Cd concentration. Correlation analysis showed that both the root and shoot Cd contents were positively correlated with the soil exchangeable Cd concentration but were negatively correlated with the soil pH. Moreover, the grey relational analysis showed that the root Cd extraction, root biomass, and shoot biomass were the top three closely associated factors with the shoot Cd extraction. Therefore, the study indicated that the root Cd extraction, root biomass, and shoot biomass played an important role in determining the shoot Cd extraction capability (phytoremediation capability) of N. officinale.

SA at 100, 150, and 200 mg/L concentrations promoted the N. officinale growth by increasing its biomass under Cd-contaminated conditions. Only 150 mg/L SA increased the chlorophyll a and b contents. Meanwhile, SA at different concentrations increased the POD activity, CAT activity, and Cd content to some extent, but decreased the SOD activity and soluble protein content. SA at 100, 150, and 200 mg/L increased the Cd extraction. In addition, the SA concentration showed a regression relationship with both the root and shoot Cd extractions, and the root Cd extraction, shoot biomass, root biomass had closely associated with the shoot Cd extraction. Thus, the study confirmed that SA could improve the N. officinale phytoremediation capability for Cd-contaminated paddy fields. However, future work should explore how SA promotes Cd accumulation in N. officinale.

The original contributions presented in the study are included in the article/supplementary material. Further inquiries can be directed to the corresponding author.

YaZ, investigation, data curation, and writing- original draft preparation. RZ, YiZ, QA, HL, AL, and LW, investigation and data curation. LL, conceptualization and methodology. All authors contributed to the article and approved the submitted version.

This work was supported by the Project of Shaanxi Provincial Science and Technology Department (2022ZY1-CGZY-07).

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.

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