Next Article in Journal
Morphological Variability amid Genetic Homogeneity and Vice Versa: A Complicated Case with Humidophila (Bacillariophyceae) from Tropical Forest Soils of Vietnam with the Description of Four New Species
Next Article in Special Issue
Molecular Networks Governing Plant Responses to Heat and Cold Stress
Previous Article in Journal
Effects of Nitrogen Application Strategies on Yield, Nitrogen Uptake and Leaching in Spring Maize Fields in Northwest China
Previous Article in Special Issue
Nano-Zinc Oxide Can Enhance the Tolerance of Apple Rootstock M9-T337 Seedlings to Saline Alkali Stress by Initiating a Variety of Physiological and Biochemical Pathways
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Jasmonic Acid Enhances Rice Cadmium Tolerance by Suppressing Cadmium Uptake and Translocation

1
Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, College of Agriculture, Fujian Agriculture and Forestry University, Fuzhou 350002, China
2
Key Laboratory of Ministry of Agriculture and Rural Affairs of Biological Breeding for Fujian and Taiwan Crops, College of Agriculture, Fujian Agriculture and Forestry University, Fuzhou 350002, China
3
College of Future Technology, Fujian Agriculture and Forestry University, Fuzhou 350002, China
4
Shandong Branch of Sinochem Agriculture Holdings, Zibo 256304, China
*
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
Plants 2025, 14(7), 1068; https://doi.org/10.3390/plants14071068
Submission received: 5 March 2025 / Revised: 23 March 2025 / Accepted: 25 March 2025 / Published: 31 March 2025

Abstract

Worldwide, cadmium (Cd) contamination severely threatens rice production and public health. Jasmonic acid (JA) is recognized to be involved in rice Cd stress responses, but the underlying mechanism remains unclear. In this study, we show that JA positively regulates Cd tolerance in rice by repressing Cd uptake and root-to-shoot translocation. Cd exposure rapidly elevated the endogenous JA in rice roots, which was associated with increased expression of JA synthesis and JA-responsive genes. Moreover, silencing the expression of either allene oxide synthase (OsAOS; active in JA biosynthesis) or CORONATINE INSENSITIVE1 (OsCOI1; active in JA perception) resulted in aggravated Cd toxicity and increased Cd accumulation in both the roots and shoots, as well as increased translocation from the root to the shoots. A short-term uptake experiment revealed that silencing of OsAOS and OsCOI1 enhanced root Cd uptake ability. Furthermore, the elevated transcript levels of genes for Cd uptake (OsNramp5, OsNramp1, and OsIRT1) and root-to-shoot translocation (OsHMA2) were observed in OsAOS and OsCOI1 RNAi plants in comparison with wild-type plants. Taken together, our findings suggest that JA enhances rice cadmium tolerance by suppressing Cd uptake and translocation.

1. Introduction

Heavy metal contamination has become a serious ecological concern worldwide, with the increasing release of heavy metals from anthropogenic activities [1,2]. Cadmium (Cd) is considered one of the most hazardous elements for both animals and plants for its high mobility and biotoxicity [3,4]. As a non-essential heavy metal, excessive amounts of soil Cd seriously inhibit plant growth and development by disturbing a series of physiological and biochemical processes, such as water and nutrient uptake, photosynthesis, transcription, and signaling pathways [5]. The accumulation of Cd in plants not only impairs plant growth, crop yield, and quality but also endangers human health via the food chain. Rice (Oryza sativa L.) is the staple food for half of the population of the world. However, Cd is almost ubiquitously present as an environmental pollutant in the rice-growing regions of the world [6,7]. Worse still is that rice appears to take up and accumulate Cd more than other major cereal crops. High Cd accumulation in rice leads to an excessive intake of toxic heavy metals by humans, posing a big threat to public health [2,8,9].
Cd in the soil could be readily absorbed by plant roots and then translocated to other tissues through a series of transporters [10,11]. Over the last decades, several key transporters involved in Cd uptake by the roots and root-to-shoot translocation have been identified in rice [11,12,13]. OsNramp5, a member of the natural resistance-associated macrophage protein family, is functionally characterized as the major transporter for Cd uptake from the soil solution to rice root cells. Knockout of this transporter results in a dramatic reduction in Cd and Mn uptake in rice [14]. In addition, OsNramp1, iron-regulated transporter OsIRT1, and the major facilitator superfamily protein OsCd1 also contribute to the uptake in rice roots [15,16,17]. Moreover, OsHMA2, a P-type heavy metal ATPase, is identified to be responsible for the root-to-shoot translocation of Cd. The knockout of OsHMA2 resulted in large decreases in the translocation of Cd from root to shoot [18,19].
Several signaling pathways, such as abscisic acid (ABA), jasmonic acid (JA), gibberellin, and auxin, have been suggested to be involved in the regulation of Cd stress responses [20,21,22,23]. However, their roles in affecting plant Cd uptake and translocation remain largely unclear. JA is an important phytohormone that is critical for growth, development, reproduction, and stress responses in plants [24,25]. The exposure of plants to Cd induces the expression of JA synthesis and JA-responsive genes, and/or increases endogenous JA levels in Arabidopsis [23,26]. Several studies have demonstrated that the exogenous application of JA could effectively alleviate Cd toxicity in Arabidopsis [23], Capsicum frutescens [27], Solanum nigrum [28], wheat [29], rice [30,31,32], etc. Recently, Wei et al. [31] reported that exogenous MeJA alleviated Cd toxicity, depressed Cd uptake, and modulated Cd distribution in rice seedlings. The decrease in Cd uptake and translocation by exogenous MeJA is correlated with the down-regulation of metal transporter genes in the roots [30,31]. These findings suggest a critical role for JA in controlling Cd uptake and translocation through the transcriptional regulation of the Cd transporter genes in rice.
In this study, we investigated the effect of Cd on JA synthesis in rice roots, and the transgenic RNAi lines of allene oxide synthase (OsAOS), which are involved in JA biosynthesis, and CORONATINE INSENSITIVE1 (OsCOI1), which is involved in JA perception, were used to elucidate the effects of in vivo JA on Cd toxicity, Cd uptake, and translocation in rice [33].

2. Results

2.1. JA Synthesis Is Enhanced by Cd Exposure

To determine whether Cd stress alters the endogenous JA levels, the transcript levels of key genes involved in JA biosynthesis, JA-responsive marker genes, and the accumulation of JA in rice roots exposed to Cd stress were monitored. The expression levels of genes encoding lipoxygenase (LOX1 and 2) and allene oxide synthase (AOS1 and 2), as well as jasmonate ZIM-domain protein (JAZ11) and JA-inducible Myb transcription factor (JAMYB), were rapidly induced by Cd exposure (Figure 1A–F). Such effect was particularly evident at 3 h after Cd treatment, at the time the transcript levels of the above genes were increased by 9.3, 20.1, 11.3, 9.6, 22.5, and 7.8 fold, respectively, relative to control plants without Cd treatment. Similarly, both JA and JA-Ile levels were significantly increased after Cd treatment (Figure 1G,H). These results indicate that Cd stress could rapidly enhance the JA accumulation.

2.2. Silencing of OsAOS and OsCOI1 Aggravates Cd Toxicity in Rice

To further investigate the role of the JA pathway in the Cd stress response in vivo, the RNAi plants of OsAOS and OsCOI1, two critical genes involved in JA biosynthesis and perception, respectively, were exposed to Cd stress. Both OsAOS and OsCOI1 RNAi plants showed significantly increased sensitivity to Cd stress. After 2 weeks of Cd exposure, the OsAOS and OsCOI1 RNAi plants exhibited stronger growth inhibition and necrosis in the basal part of the stems (Figure 2A–C). In addition, both JA and JA-Ile levels decreased in OsAOS RNAi plants, while only JA-Ile levels slightly decreased in the OsCOI1 RNAi plants under both control and Cd stress conditions (Figure 2D,E). Moreover, Cd exposure decreased the leaf photosynthetic rate and stomatal conductance of all three genotypes. However, the magnitudes of Cd-induced inhibition were significantly higher in RNAi plants (Figure 3A,B). The maximum efficiency of the PSII photochemistry (Fv/Fm) and chlorophyll content were significantly reduced by 2 weeks of Cd exposure in the OsAOS and OsCOI1 RNAi plants, while Cd stress had no significant effect on them in the WT plants (Figure 3C,D). These results indicated that the decreased endogenous JA biosynthesis and perception aggravate Cd toxicity, and the JA signaling pathway is required for Cd tolerance in rice.

2.3. Silencing of OsAOS and OsCOI1 Increases Cd Accumulation

To test the potential effects of JA on Cd uptake and translocation, we determined the Cd accumulation in the rice seedlings of the three genotypes after 7 days of Cd exposure. The OsAOS and OsCOI1 RNAi plants accumulated more Cd in both the shoots and roots compared with the WT plants (Figure 4A,B). After 7 days of Cd exposure, the shoot Cd contents of the OsAOS and OsCOI1 RNAi plants were 63.0% and 61.7% higher than that in WT plants. And the root Cd contents of OsAOS and OsCOI1 RNAi plants were 34.9% and 37.7% higher than that in WT plants. Meanwhile, the silencing of JA biosynthesis and perception also increased the root-to-shoot translocations, which were 20.8% and 17.4% higher than that of the WT plants. These results indicated that the JA signaling pathway is required for reducing root Cd uptake and Cd translocation from the root to shoot in rice.

2.4. Silencing of OsAOS and OsCOI1 Enhances Root Cd Uptake

To confirm the role of JA on Cd uptake, the short-term root uptake experiments using the intact roots of the three genotypes were performed. In all three tested genotypes, the Cd uptake increased with time, from 0 to 120 min. However, the Cd uptake in the OsAOS and OsCOI1 RNAi roots was faster than that in WT roots (Figure 5A). Similarly, the Cd uptake increased with the increasing Cd concentration in the nutrient solution in all three tested genotypes. But the Cd uptake in the OsAOS and OsCOI1 RNAi roots was higher than that in the WT roots for all the exogenous Cd concentrations, except for 10 μM (Figure 5B). These results provided evidence that the JA signaling pathway is required for reducing root Cd uptake in response to Cd stress in rice.

2.5. Silencing of OsAOS and OsCOI1 Promotes Expression of Genes for Cd Uptake and Translocation

To explore how the JA pathway affects Cd uptake and translocation in rice plants, we analyzed the expression levels of the genes involved in Cd uptake and translocation by RT-qPCR. The transcript levels of Nramp5 were repressed, while the expressions of Nramp1, IRT1, and HMA2 were elevated by Cd exposure in all three tested genotypes (Figure 6). The mRNA levels of Nramp1, IRT1, and HMA2 were all significantly higher in the OsAOS and OsCOI1 RNAi roots than those in the WT in the absence of Cd. Silencing of the genes involved in JA biosynthesis and perception promoted the expression of all of the tested Cd transporter genes. These results indicate that endogenous JA negatively regulates the expressions of genes involved in Cd uptake and translocation from the roots to the shoots and, hence, decreases the Cd accumulation in rice plants.

3. Discussion

Cd contamination has emerged as one of the most important factors limiting rice production and threatening public health [2,17]. Over the last decades, intensive efforts have been made to identify the key transporters for Cd uptake and translocation in rice [11,17]. However, the precise regulatory signaling pathways affecting the Cd stress response, Cd uptake, and translocation in rice remain poorly understood. In the present study, our results demonstrated that Cd stress promotes rice endogenous JA synthesis, at least partially by the rapid induction of the expression of JA synthesis genes (Figure 1). Moreover, the silencing of the genes involved in either JA biosynthesis or perception resulted in higher Cd accumulation and increased sensitivity to Cd stress (Figure 2, Figure 3 and Figure 4). Therefore, our findings indicated that JA plays an important role in the Cd stress response, and the jasmonate signaling pathway is required for Cd tolerance in rice.
The crucial roles of the JA signaling pathway in mediating growth, development, and stress responses in plants have been investigated extensively [25]. It was previously demonstrated that exogenous application of MeJA could effectively alleviate Cd toxicity in Cd-stressed rice plants and reduce Cd-induced oxidative stress by enhancing the glutathione content and the activity of antioxidant enzymes [32]. Kanu et al. [34] reported that exogenous MeJA could alleviate Cd-induced oxidative stress, increase mineral nutrient uptake, and reduce Cd accumulation in rice plants. Yang et al. and Wei et al. [30,31] indicated that exogenous MeJA depressed Cd uptake and modulated Cd distribution by suppressing the expression of the Cd transporter genes in rice. Here, our results showed that the compromise of JA signaling by silencing of genes involved in JA biosynthesis and perception aggravates Cd toxicity in rice and increased Cd accumulation in both the roots and the shoots (Figure 2, Figure 3 and Figure 4). Furthermore, the short-term root uptake experiments proved that defectiveness in JA biosynthesis and perception enhances root Cd uptake activity (Figure 5). These results indicated that the JA signaling pathway regulates the Cd stress response by reducing root Cd uptake in rice. Similarly, the enhanced sensitivity to Cd stress has also been observed in the tomato JA deficiency mutant spr2 [35], as well as the Arabidopsis JA synthesis mutant ataos and the JA receptor mutant atcoi1 [23], suggesting that the regulatory role of JA signaling pathway in Cd stress response appears to be conserved across different plants species.
Although no specific transporters for Cd uptake and translocation have been found in rice so far, Cd could be easily absorbed by rice roots and translocated to other tissues by a number of other divalent metal transporters, such as Nramp5, Nramp1, HMA2, IRT1, etc. [10,11,17]. In the present study, the transcript levels of Nramp5, Nramp1, IRT1, and HMA2 were all significantly promoted by the compromise of JA biosynthesis and perception, suggesting that JA negatively regulates the expression of genes involved in Cd uptake and translocation. Despite Nramp5 and HMA2 being identified as the major transporter responsible for uptake and root-to-shoot translocation of Cd, respectively, several other transporter and/or regulator genes have also been characterized to be involved in rice Cd uptake and accumulation, such as Cd1, CCX2, ZIP5, ZIP9, HMA3, CAL1, ABCG36 LCT1, etc. [9,10,11]. Thus, it is possible that the JA pathway might also regulate the expression of these genes to influence rice Cd uptake and translocation. Generally, the JA signaling could be rapidly activated by various stresses to regulate the expression of downstream JA-responsive genes [25]. Recently, it has been reported that JA negatively regulates iron acquisition under Fe deficiency conditions by activating the core JA signaling component MYC2, which promotes FIT (FER-like iron deficiency-induced transcription factor) degradation by regulating the expression of a set of bHLH transcription factors, resulting in a reduced expression of AtIRT1 in Arabidopsis [36]. Therefore, it is possible that Cd-induced JA might directly or indirectly repress the expression of genes mediating Cd uptake and root-to-shoot translocation to positively regulate the Cd response in rice. Further efforts on the functional characterization of the key components in the JA signal module mediating Cd uptake and translocation are required for future Cd resistance and/or low-Cd breeding in rice. In addition, compared with other plants, rice appears to display high tolerance to Cd toxicity, and researchers have traditionally used excessively high Cd concentrations to investigate the responses of rice to Cd stress [23,30,31,32]. In the present study, the WT seedlings did not exhibit an abnormal growth phenotype, except for a slight decrease in plant height and necrosis in the basal part of stems, associated with unaffected Fv/Fm and chlorophyll content after a 2-week-long 50 µM Cd treatment (substantially high dose) (Figure 2 and Figure 3). However, Cd concentrations in soil solutions typically remain below 1 μM, even in heavily contaminated areas near smelters [2]. Therefore, further efforts on the potential role of JA in regulating Cd uptake and accumulation in rice grains under realistic Cd concentrations will provide more direct guidance for low-Cd breeding in rice.

4. Materials and Methods

4.1. Plant Materials and Growth Conditions

The rice (Oryza sativa L.) OsAOS and OsCOI1 RNAi lines, as well as their corresponding wild type (cv. Ishikari-Shiroke, WT), were used in this study [33]. Rice seeds were surface sterilized and transferred to a seeding tray for germination. The 7-day-old seedlings were transplanted into a plastic box containing 5 L full-strength modified Kimura B nutrient solution (pH: 5.6, renewed every 3 d), as described by Chen et al. [8]. The rice plants were cultivated in a growth chamber under a 12 h/12 h day/night cycle, with the temperature regime at 27 °C/23 °C, and a light intensity of 300 μmol m−2 s−1. After 4 weeks, the uniform healthy rice seedlings were treated with (Cd) or without (Control) 50 μM CdCl2. To examine the effect of Cd exposure on rice growth, 12 seedlings were harvested after 14 days of Cd treatment and dried at 75 °C for 3 d to measure the shoot and root dry weight.

4.2. Leaf Gas Exchange Analysis

The photosynthetic rates and stomatal conductance of the youngest fully expanded leaves were measured between 9:00 and 11:00 a.m. using a portable photosynthesis system (Li-6400; LI-COR Inc., Lincoln, NE, USA) with a 6 cm2 chamber, and the photo flux density was set to 500 µmol m−2 s−1. Each treatment included six replicates.

4.3. Chlorophyll Fluorescence Analysis

The photosystem II photochemistry efficiency (Fv/Fm) of the youngest fully expanded leaves was analyzed after dark adaptation for 30 min by a pulse amplitude-modulated chlorophyll fluorescence system (Imaging PAM, Walz, Effeltrich, Germany), according to the method of Chen et al. [37]. Chlorophyll content was determined by a spectrophotometer (UV-2550, Shimadzu, Kyoto, Japan) after extraction with 80% ice-cold acetone. Each treatment included six replicates.

4.4. JA and JA-Ile Analysis

Frozen leaves were used for the quantification of JA and JA-Ile by UPLC-MS/MS, as described by Song et al. [38]. In brief, the fine powder of leaf tissues (approximately 200 mg) was extracted with 1 mL of ice-cold ethyl acetate spiked with the internal standards (20 ng of D6-JA and 5 ng of 13C6-JA-Ile). After homogenization by vortexing for 10 min and centrifugation at 13,000 g for 10 min, the supernatants were transferred to 2 mL tubes for vacuum evaporation. Then, the pellets were resuspended in 0.2 mL of 50% (v/v) methanol and centrifuged at 13,000 g for 15 min. The supernatant was transferred to glass vials and then subjected to HPLC-MS/MS analysis (LCMS-8040, Shimadzu, Kyoto, Japan). The JA and JA-Ile contents were quantified by comparing their peak area with the peak area of their respective internal standard. Each treatment included three replicates.

4.5. Cd Content Measurement

Dried rice shoot and root samples were milled to a fine powder for Cd content analysis. The powder was weighed (approximately 500 mg) and digested in nitric acid (GR 65.0–68.0%) in a glass tube at 340 °C on a hot stove, and 20 μL of H2O2 (GR ≥ 30.0%) was added 2–3 times during the digestion. The Cd concentration in the supernatant was then determined using atomic absorption spectrometry (Zeenit700p, Analytik Jena, Jena/Überlingen, Germany). Data were expressed on the basis of dry weight.

4.6. Short-Term Cd Uptake Determination

To examine Cd transport activity in plants, we performed short-term uptake experiments using intact plants of both wild-type rice and the RNAi lines. First, the rice seedlings (4 weeks old) were subjected to an uptake solution containing 50 μM CdCl2 for different times (0, 10, 30, 60, 90, and 120 min) at 25 °C. Meanwhile, the rice seedlings (4 weeks old) were subjected to an uptake solution containing various concentrations of Cd (0, 10, 20, 30, 40, and 50 μM) at 25 °C for 30 min. Then, the roots were separated, dried at 75 °C for 3 d, and used for Cd content determination, as described before.

4.7. Gene Expression Analysis

For gene expression analysis, frozen root samples (approximately 100 mg) were used for RNA extraction. The gene expression analysis was conducted using a quantitative RT-PCR, as previously described by Chen et al. [8], with OsActin as the internal reference gene. The primer specificity was validated through primer-BLAST and verified by a melt curve analysis. The 2−∆∆Ct method was used for the relative expression calculation. All experiments were performed in triplicate using three biological replicates per treatment. The gene-specific primers are listed in Table S1.

4.8. Statistical Analysis

Statistical analysis was performed using the SPSS statistics software (Version 19.0 for Windows, SPSS, Chicago, IL, USA). The data were subjected to an analysis of variance (ANOVA) with Tukey’s test for differences among treatments, and a p value ≤ 0.05 was considered significant between the treatments. All values are presented as the mean ± SE. Graphs were generated using GraphPad Prism 8.0 (GraphPad Software Inc., La Jolla, CA, USA).

5. Conclusions

Our present study reveals that the exposure of rice plants to Cd stress rapidly activates the JA signaling pathway, which positively regulates the Cd response by repressing the transcriptional levels of the genes mediating Cd uptake and root-to-shoot translocation. Our findings provide direct evidence for the in vivo effects of JA on Cd toxicity, Cd uptake, and translocation and highlight the potential of JA signaling in enhancing Cd resistance in rice.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/plants14071068/s1: Table S1: Primers used in the real-time quantitative PCR experiment.

Author Contributions

Conceptualization, D.C., Y.S. and Q.W.; methodology, H.Z.; validation, D.C. and Y.S.; formal analysis, D.C.; investigation, H.Z., Z.L., X.L. (Xinyu Li), X.L. (Xiaodong Liu) and L.F.; resources, D.C., R.Z. and Y.S.; data curation, D.C.; writing—original draft preparation, D.C. and H.Z.; writing—review and editing, Q.W. and Y.S.; visualization, D.C.; supervision, Q.W. and Y.S.; project administration, D.C. and Y.S.; funding acquisition, D.C., R.Z. and Y.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (32271617, 32371588, 32401402, 32471656) and the Distinguished Young Scholars of Fujian Agriculture and Forestry University (xjq2020011).

Data Availability Statement

Data are contained within the article and Supplementary Materials.

Conflicts of Interest

Author Xinyu Li was employed by the Shandong Branch of Sinochem Agriculture Holdings. The remaining 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.

Abbreviations

The following abbreviations are used in this manuscript:
CdCadmium
JAJasmonic acid
RNAiRNA interference
WTWild type
AOSAllene oxide synthase
COICORONATINE INSENSITIVE
LOXLipoxygenase
IRTiron-regulated transporter
NrampNatural resistance-associated macrophage protein
HMAP-type heavy metal ATPase
RT-qPCRReverse transcription–quantitative PCR

References

  1. Clemens, S.; Aarts, M.G.; Thomine, S.; Verbruggen, N. Plant Science: The Key to Preventing Slow Cadmium Poisoning. Trends Plant Sci. 2013, 18, 92–99. [Google Scholar] [PubMed]
  2. Zhao, D.; Wang, P.; Zhao, F.-J. Toxic Metals and Metalloids in Food: Current Status, Health Risks, and Mitigation Strategies. Curr. Environ. Health Rep. 2024, 11, 468–483. [Google Scholar] [PubMed]
  3. Han, R.; Wang, Z.; Wang, S.; Sun, G.; Xiao, Z.; Hao, Y.; Nriagu, J.; Teng, H.H.; Li, G. A Combined Strategy to Mitigate the Accumulation of Arsenic and Cadmium in Rice (Oryza sativa L.). Sci. Total Environ. 2023, 896, 165226. [Google Scholar] [PubMed]
  4. Zhang, H.; Reynolds, M. Cadmium Exposure in Living Organisms: A Short Review. Sci. Total Environ. 2019, 678, 761–767. [Google Scholar]
  5. Haider, F.U.; Liqun, C.; Coulter, J.A.; Cheema, S.A.; Wu, J.; Zhang, R.; Wenjun, M.; Farooq, M. Cadmium Toxicity in Plants: Impacts and Remediation Strategies. Ecotoxicol. Environ. Saf. 2021, 211, 111887. [Google Scholar]
  6. Zou, M.; Zhou, S.; Zhou, Y.; Jia, Z.; Guo, T.; Wang, J. Cadmium Pollution of Soil-Rice Ecosystems in Rice Cultivation Dominated Regions in China: A Review. Environ. Pollut. 2021, 280, 116965. [Google Scholar]
  7. Zhao, F.-J.; Ma, Y.; Zhu, Y.-G.; Tang, Z.; McGrath, S.P. Soil Contamination in China: Current Status and Mitigation Strategies. Environ. Sci. Technol. 2015, 49, 750–759. [Google Scholar]
  8. Chen, D.; Chen, D.; Xue, R.; Long, J.; Lin, X.; Lin, Y.; Jia, L.; Zeng, R.; Song, Y. Effects of Boron, Silicon and Their Interactions on Cadmium Accumulation and Toxicity in Rice Plants. J. Hazard. Mater. 2019, 367, 447–455. [Google Scholar]
  9. Zhao, F.-J.; Wang, P. Arsenic and Cadmium Accumulation in Rice and Mitigation Strategies. Plant Soil 2020, 446, 1–21. [Google Scholar]
  10. Huang, S.; Yamaji, N.; Ma, J.F. Metal Transport Systems in Plants. Annu. Rev. Plant Biol. 2024, 75, 1–25. [Google Scholar]
  11. Feng, J.; Shen, R.F.; Shao, J.F. Transport of Cadmium from Soil to Grain in Cereal Crops: A Review. Pedosphere 2021, 31, 3–10. [Google Scholar]
  12. Song, Y.; Jin, L.; Wang, X. Cadmium Absorption and Transportation Pathways in Plants. Int. J. Phytorem. 2017, 19, 133–141. [Google Scholar]
  13. Sterckeman, T.; Thomine, S. Mechanisms of Cadmium Accumulation in Plants. Crit. Rev. Plant Sci. 2020, 39, 322–359. [Google Scholar]
  14. Sasaki, A.; Yamaji, N.; Yokosho, K.; Ma, J.F. Nramp5 Is a Major Transporter Responsible for Manganese and Cadmium Uptake in Rice. Plant Cell 2012, 24, 2155–2167. [Google Scholar]
  15. Yan, H.; Xu, W.; Xie, J.; Gao, Y.; Wu, L.; Sun, L.; Feng, L.; Chen, X.; Zhang, T.; Dai, C.; et al. Variation of a Major Facilitator Superfamily Gene Contributes to Differential Cadmium Accumulation between Rice Subspecies. Nat. Commun. 2019, 10, 2562. [Google Scholar]
  16. Chang, J.-D.; Huang, S.; Yamaji, N.; Zhang, W.; Ma, J.F.; Zhao, F.-J. OsNRAMP1 Transporter Contributes to Cadmium and Manganese Uptake in Rice. Plant Cell Environ. 2020, 43, 2476–2491. [Google Scholar]
  17. Hu, J.; Chen, G.; Xu, K.; Wang, J. Cadmium in Cereal Crops: Uptake and Transport Mechanisms and Minimizing Strategies. J. Agric. Food Chem. 2022, 70, 5961–5974. [Google Scholar]
  18. Satoh-Nagasawa, N.; Mori, M.; Nakazawa, N.; Kawamoto, T.; Nagato, Y.; Sakurai, K.; Takahashi, H.; Watanabe, A.; Akagi, H. Mutations in Rice (Oryza sativa) Heavy Metal ATPase 2 (OsHMA2) Restrict the Translocation of Zinc and Cadmium. Plant Cell Physiol. 2012, 53, 213–224. [Google Scholar]
  19. Takahashi, R.; Ishimaru, Y.; Shimo, H.; Ogo, Y.; Senoura, T.; Nishizawa, N.K.; Nakanishi, H. The OsHMA2 Transporter Is Involved in Root-to-Shoot Translocation of Zn and Cd in Rice. Plant Cell Environ. 2012, 35, 1948–1957. [Google Scholar]
  20. Zhu, X.F.; Jiang, T.; Wang, Z.W.; Lei, G.J.; Shi, Y.Z.; Li, G.X.; Zheng, S.J. Gibberellic Acid Alleviates Cadmium Toxicity by Reducing Nitric Oxide Accumulation and Expression of IRT1 in Arabidopsis thaliana. J. Hazard. Mater. 2012, 239, 302–307. [Google Scholar]
  21. Zhu, X.F.; Wang, Z.W.; Dong, F.; Lei, G.J.; Shi, Y.Z.; Li, G.X.; Zheng, S.J. Exogenous Auxin Alleviates Cadmium Toxicity in Arabidopsis thaliana by Stimulating Synthesis of Hemicellulose 1 and Increasing the Cadmium Fixation Capacity of Root Cell Walls. J. Hazard. Mater. 2013, 263, 398–403. [Google Scholar] [PubMed]
  22. Rodríguez-Serrano, M.; Romero-Puertas, M.C.; Pazmino, D.M.; Testillano, P.S.; Risueño, M.C.; Del Río, L.A.; Sandalio, L.M. Cellular Response of Pea Plants to Cadmium Toxicity: Cross Talk between Reactive Oxygen Species, Nitric Oxide, and Calcium. Plant Physiol. 2009, 150, 229–243. [Google Scholar] [PubMed]
  23. Lei, G.J.; Sun, L.; Sun, Y.; Zhu, X.F.; Li, G.X.; Zheng, S.J. Jasmonic Acid Alleviates Cadmium Toxicity in Arabidopsis via Suppression of Cadmium Uptake and Translocation. J. Integr. Plant Biol. 2020, 62, 218–227. [Google Scholar] [CrossRef] [PubMed]
  24. Li, M.; Yu, G.; Cao, C.; Liu, P. Metabolism, Signaling, and Transport of Jasmonates. Plant Commun. 2021, 2, 100231. [Google Scholar]
  25. Howe, G.A.; Major, I.T.; Koo, A.J. Modularity in Jasmonate Signaling for Multistress Resilience. Annu. Rev. Plant Biol. 2018, 69, 387–415. [Google Scholar]
  26. Maksymiec, W.; Wianowska, D.; Dawidowicz, A.L.; Radkiewicz, S.; Mardarowicz, M.; Krupa, Z. The Level of Jasmonic Acid in Arabidopsis thaliana and Phaseolus coccineus Plants under Heavy Metal Stress. J. Plant Physiol. 2005, 162, 1338–1346. [Google Scholar]
  27. Yan, Z.; Chen, J.; Li, X. Methyl Jasmonate as Modulator of Cd Toxicity in Capsicum frutescens Var. Fasciculatum Seedlings. Ecotoxicol. Environ. Saf. 2013, 98, 203–209. [Google Scholar]
  28. Yan, Z.; Zhang, W.; Chen, J.; Li, X. Methyl Jasmonate Alleviates Cadmium Toxicity in Solanum Nigrum by Regulating Metal Uptake and Antioxidative Capacity. Biol. Plant. 2015, 59, 373–381. [Google Scholar]
  29. Alikhani, O.; Abbaspour, H.; Afshar, A.S.; Motavalizadehkakhki, A. Studying the Effects of Methyl Jasmonate on Growth Parameters and Anti-Oxidative Capacity in Wheat (Triticum aestivum L.) under Cadmium Stress. Environ. Sci. 2017. Available online: https://api.semanticscholar.org/CorpusID:212614059 (accessed on 9 January 2025).
  30. Yang, J.B.; Wang, H.Y.; Huang, J.; Shan, C.J.; Yan, J.; Zhong, C.W.; Hu, D.; Zhang, Q.; Shen, R.F.; Zhu, X.F.; et al. Jasmonic Acid Improves Cadmium Tolerance in Rice (Oryza sativa) by Reducing the Production of Nitric Oxide. Ecotoxicol. Environ. Saf. 2025, 290, 117722. [Google Scholar]
  31. Wei, T.; Li, H.; Wang, Y.; Chi, M.; Guo, J.; Jia, H.; Zhang, C. Alleviation of Cadmium Toxicity and Minimizing Its Accumulation in Rice Plants by Methyl Jasmonate: Performance and Mechanisms. J. Biotechnol. 2025, 398, 133–145. [Google Scholar]
  32. Li, Y.; Zhang, S.; Bao, Q.; Chu, Y.; Sun, H.; Huang, Y. Jasmonic Acid Alleviates Cadmium Toxicity through Regulating the Antioxidant Response and Enhancing the Chelation of Cadmium in Rice (Oryza sativa L.). Environ. Pollut. 2022, 304, 119178. [Google Scholar] [PubMed]
  33. Ye, M.; Song, Y.; Long, J.; Wang, R.; Baerson, S.R.; Pan, Z.; Zhu-Salzman, K.; Xie, J.; Cai, K.; Luo, S.; et al. Priming of Jasmonate-Mediated Antiherbivore Defense Responses in Rice by Silicon. Proc. Natl. Acad. Sci. USA 2013, 110, E3631–E3639. [Google Scholar] [PubMed]
  34. Kanu, A.S.; Ashraf, U.; Mansaray, L.R.; Abbas, F.; Fiaz, S.; Amanullah, S.; Charley, C.S.; Tang, X. Exogenous Methyl Jasmonate Application Improved Physio-Biochemical Attributes, Yield, Quality, and Cadmium Tolerance in Fragrant Rice. Front. Plant Sci. 2022, 13, 849477. [Google Scholar]
  35. Zhao, S.; Ma, Q.; Xu, X.; Li, G.; Hao, L. Tomato Jasmonic Acid-Deficient Mutant Spr2 Seedling Response to Cadmium Stress. J. Plant Growth Regul. 2016, 35, 603–610. [Google Scholar]
  36. Cui, Y.; Chen, C.-L.; Cui, M.; Zhou, W.-J.; Wu, H.-L.; Ling, H.-Q. Four IVa bHLH Transcription Factors Are Novel Interactors of FIT and Mediate JA Inhibition of Iron Uptake in Arabidopsis. Mol. Plant 2018, 11, 1166–1183. [Google Scholar]
  37. Chen, D.; Cao, B.; Qi, L.; Yin, L.; Wang, S.; Deng, X. Silicon-Moderated K-Deficiency-Induced Leaf Chlorosis by Decreasing Putrescine Accumulation in Sorghum. Ann. Bot. 2016, 118, 305–315. [Google Scholar]
  38. Song, J.; Bian, J.; Xue, N.; Xu, Y.; Wu, J. Inter-species mRNA Transfer Among Green Peach Aphids, Dodder Parasites, and Cucumber Host Plants. Plant Divers. 2021, 44, 1–10. [Google Scholar]
Figure 1. Effect of Cd exposure on JA levels in rice roots. Transcript levels of genes encoding lipoxygenases (LOX1, (A); LOX2, (B)), allene oxide synthases (AOS1, (C); AOS2, (D)), jasmonate ZIM-domain protein (JAZ11, (E)), JA-inducible Myb transcription factor (JAMYB, (F)). Contents of JA (G) and JA-Ile content (H) in rice plants treated with or without 50 μM CdCl2. Data are means ± SE (n = 3). Different letters above bars indicate statistically significant differences between treatments (Tukey’s multiple range test, p ≤ 0.05).
Figure 1. Effect of Cd exposure on JA levels in rice roots. Transcript levels of genes encoding lipoxygenases (LOX1, (A); LOX2, (B)), allene oxide synthases (AOS1, (C); AOS2, (D)), jasmonate ZIM-domain protein (JAZ11, (E)), JA-inducible Myb transcription factor (JAMYB, (F)). Contents of JA (G) and JA-Ile content (H) in rice plants treated with or without 50 μM CdCl2. Data are means ± SE (n = 3). Different letters above bars indicate statistically significant differences between treatments (Tukey’s multiple range test, p ≤ 0.05).
Plants 14 01068 g001
Figure 2. Effect of Cd exposure on growth of WT rice plants and the OsAOS and OsCOI1 RNAi lines. Phenotype (A), dry weight of shoots (B) and roots (C), JA (D) and JA-Ile content (E) of rice plants treated with (Cd) or without (Control) 50 μM CdCl2 for 14 days. Bar, 10 cm. Data are means ± SE (n = 12). Different letters above bars indicate statistically significant differences between treatments (Tukey’s multiple range test, p ≤ 0.05).
Figure 2. Effect of Cd exposure on growth of WT rice plants and the OsAOS and OsCOI1 RNAi lines. Phenotype (A), dry weight of shoots (B) and roots (C), JA (D) and JA-Ile content (E) of rice plants treated with (Cd) or without (Control) 50 μM CdCl2 for 14 days. Bar, 10 cm. Data are means ± SE (n = 12). Different letters above bars indicate statistically significant differences between treatments (Tukey’s multiple range test, p ≤ 0.05).
Plants 14 01068 g002
Figure 3. Effect of Cd exposure on photosynthesis of OsAOS and OsCOI1 RNAi lines and corresponding WT rice plants. Photosynthetic rate (A), stomatal conductance (B), maximum efficiency of PSII photochemistry (Fv/Fm), (C) and chlorophyll content (D) of rice plants treated with (Cd) or without (Control) 50 μM CdCl2 for 14 days. Data are means ± SE (n = 6). Different letters above bars indicate statistically significant differences between treatments (Tukey’s multiple range test, p ≤ 0.05).
Figure 3. Effect of Cd exposure on photosynthesis of OsAOS and OsCOI1 RNAi lines and corresponding WT rice plants. Photosynthetic rate (A), stomatal conductance (B), maximum efficiency of PSII photochemistry (Fv/Fm), (C) and chlorophyll content (D) of rice plants treated with (Cd) or without (Control) 50 μM CdCl2 for 14 days. Data are means ± SE (n = 6). Different letters above bars indicate statistically significant differences between treatments (Tukey’s multiple range test, p ≤ 0.05).
Plants 14 01068 g003
Figure 4. The effect of Cd stress on Cd accumulation and translocation of WT rice plants and the OsAOS and OsCOI1 RNAi lines. Cd contents in the shoots (A) and roots (B), and root-to-shoot Cd translocation factor (C) of rice plants treated with 50 μM CdCl2 (Cd) for 7 days. Data are means ± SE (n = 4). Different letters above bars indicate statistically significant differences between treatments (Tukey’s multiple range test, p ≤ 0.05).
Figure 4. The effect of Cd stress on Cd accumulation and translocation of WT rice plants and the OsAOS and OsCOI1 RNAi lines. Cd contents in the shoots (A) and roots (B), and root-to-shoot Cd translocation factor (C) of rice plants treated with 50 μM CdCl2 (Cd) for 7 days. Data are means ± SE (n = 4). Different letters above bars indicate statistically significant differences between treatments (Tukey’s multiple range test, p ≤ 0.05).
Plants 14 01068 g004
Figure 5. Short-term Cd uptake by roots of OsAOS and OsCOI1 RNAi lines and corresponding WT rice plants. (A) Root Cd contents of rice plants treated with 50 μM CdCl2 for different times. (B) Root Cd contents of rice plants treated with different Cd concentrations at 25 °C for 30 min. Data are means ± SE (n = 4).
Figure 5. Short-term Cd uptake by roots of OsAOS and OsCOI1 RNAi lines and corresponding WT rice plants. (A) Root Cd contents of rice plants treated with 50 μM CdCl2 for different times. (B) Root Cd contents of rice plants treated with different Cd concentrations at 25 °C for 30 min. Data are means ± SE (n = 4).
Plants 14 01068 g005
Figure 6. Effect of Cd exposure on expression of genes involved in Cd uptake and translocation in OsAOS and OsCOI1 RNAi lines and corresponding WT rice roots. Transcript levels of genes encoding natural resistance-associated macrophage proteins (Nramp5, (A); Nramp1, (B)), iron-regulated transporter 1 (IRT1, (C)) and P-type heavy metal ATPase (HMA2, (D)) in rice roots treated with or without 50 μM CdCl2 for 7 days. Data are means ± SE (n = 3). Different letters above bars indicate statistically significant differences between treatments (Tukey’s multiple range test, p ≤ 0.05).
Figure 6. Effect of Cd exposure on expression of genes involved in Cd uptake and translocation in OsAOS and OsCOI1 RNAi lines and corresponding WT rice roots. Transcript levels of genes encoding natural resistance-associated macrophage proteins (Nramp5, (A); Nramp1, (B)), iron-regulated transporter 1 (IRT1, (C)) and P-type heavy metal ATPase (HMA2, (D)) in rice roots treated with or without 50 μM CdCl2 for 7 days. Data are means ± SE (n = 3). Different letters above bars indicate statistically significant differences between treatments (Tukey’s multiple range test, p ≤ 0.05).
Plants 14 01068 g006
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Zhang, H.; Liu, Z.; Li, X.; Liu, X.; Fang, L.; Zeng, R.; Wang, Q.; Song, Y.; Chen, D. Jasmonic Acid Enhances Rice Cadmium Tolerance by Suppressing Cadmium Uptake and Translocation. Plants 2025, 14, 1068. https://doi.org/10.3390/plants14071068

AMA Style

Zhang H, Liu Z, Li X, Liu X, Fang L, Zeng R, Wang Q, Song Y, Chen D. Jasmonic Acid Enhances Rice Cadmium Tolerance by Suppressing Cadmium Uptake and Translocation. Plants. 2025; 14(7):1068. https://doi.org/10.3390/plants14071068

Chicago/Turabian Style

Zhang, Hao, Zhengkai Liu, Xinyu Li, Xiaodong Liu, Linzhi Fang, Rensen Zeng, Qiongli Wang, Yuanyuan Song, and Daoqian Chen. 2025. "Jasmonic Acid Enhances Rice Cadmium Tolerance by Suppressing Cadmium Uptake and Translocation" Plants 14, no. 7: 1068. https://doi.org/10.3390/plants14071068

APA Style

Zhang, H., Liu, Z., Li, X., Liu, X., Fang, L., Zeng, R., Wang, Q., Song, Y., & Chen, D. (2025). Jasmonic Acid Enhances Rice Cadmium Tolerance by Suppressing Cadmium Uptake and Translocation. Plants, 14(7), 1068. https://doi.org/10.3390/plants14071068

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop