Elsevier

Plant Physiology and Biochemistry

Volume 189, 15 October 2022, Pages 104-114
Plant Physiology and Biochemistry

Physiological and biochemical bases of spermidine-induced alleviation of cadmium and lead combined stress in rice

https://doi.org/10.1016/j.plaphy.2022.08.010Get rights and content

Highlights

  • Cd and Pb combined stress affected the physiological and biochemical parameters that inhibit growth of rice plants.

  • Applied spermidine reduced the harmful effects induced by Cd and Pb.

  • Multivariate analysis demonstrated that spermidine promoted rice growth under Cd and Pb combined stress.

  • The best treatment for alleviating Cd and Pb combined stress is 0.5 mmol L−1 spermidine.

Abstract

Cadmium (Cd) and lead (Pb) pollution is a major environmental issue affecting plant production. Spermidine (Spd) is involved in plant response to abiotic stress. However, the role and associated mechanism of Spd under Cd + Pb combined stress are poorly understood. The potential protective role of Spd at different concentration on rice (Oryza sativa L.) seedlings exposed to Cd + Pb treatment was investigated by a hydroponic experiment in this study. The results showed that exogenous Spd enhanced the tolerance of rice seedlings to Cd + Pb stress, resulted in an increase in plant height, root length, fresh weight and dry weight of roots and shoots. Further, application of Spd decreased the contents of hydrogen peroxide, superoxide anion, malondialdehyde, and the accumulation of Cd and Pb, and increased the contents of mineral nutrient, carotenoids, chlorophyll, proline, soluble sugar, soluble protein, total phenol, flavonoid, anthocyanin, and antioxidant enzymes activities in roots and shoots of rice seedlings under Cd + Pb stress. Particularly, 0.5 mmol L−1 Spd was the most effective to alleviate the adverse impacts on growth and physiological metabolism of rice seedlings under Cd + Pb stress. Principal component analysis and heat map clustering established correlations between physio-biochemical parameters and further revealed Spd alleviated Cd + Pb damage in rice seedling was associated with inhibition of accumulation and translocation of Cd and Pb, increasing the contents of photosynthetic pigments and mineral nutrient and stimulation of antioxidative response and osmotic adjustment. Overall, our findings provide an important prospect for use of Spd in modulating Cd + Pb tolerance in rice plants. Spd could help to alleviate Cd + Pb damage through inhibition of accumulation and translocation of Cd and Pb and stimulation of oxidant-defense system and osmotic adjustment.

Introduction

Heavy metal contamination has been increasing at an alarming rate and has becoming a global problem in recent years due to human activities such as mining, smelting, gasoline, misuse of plastics and dyes, chemical and phosphate fertilizers, irrigation with waste water (Wang et al., 2020a). Due to their high toxicity, bioaccumulation and persistence in the environment, contamination with heavy metals caused serious damage to agricultural systems, crop productivity and even human health through food chain. Among various heavy metals, cadmium (Cd) and lead (Pb) have been predominant as the most predominant heavy metals available in the environment and has received considerable attention (Ronzan et al., 2018). Although both Cd and Pb have no essential role in biological systems, they could be absorbed by plant roots and translocated to shoots. Excessive accumulation of these metals caused various adverse effects on different biochemical and physiological processes in plants, thus reduced the crop quality and yield (Wang et al., 2020a). Previous studies indicated that both Cd and Pb seriously disturbed cell division, mineral nutrient uptake and transport, biosynthesis of photosynthetic pigments, photosynthetic and respiratory processes, protein synthesis, enzyme activities, and active oxygen species (ROS) metabolism, resulting in the inhibition of growth, development and yield of various crops worldwide (Ronzan et al., 2018). For example, Sabir et al. (2020) reported that Cd stress obviously decreased fresh and dry weight of Brassica napus. The growth parameters of Biscutella auriculata L. under Pb stress were also decreased (Peco et al., 2020). Xu et al. (2020) also found that exposure to Cd stress affected the structure of chloroplast membrane, reduced chlorophyll contents, and ultimately inhibited rice growth. Hassan et al. (2020) observed oxidative damage and the decrease of the activities of different antioxidant enzymes in sorghum treated with Cd. Furthermore, many soils are polluted by multiple heavy metals in the world. Cd and Pb often coexist in real agricultural land, which amplifies the damage caused by the single elements and makes it more difficult to assess and remedy (Murtaza et al., 2019). Si et al. (2021) found that Cd and Pb had synergistic effect under combined stress and the toxic effects of their combined metals on the mulberry seedlings were stronger than those of Pb or Cd stress alone. The accumulations of Cd and Pb in Trifolium repens were also enhanced in combined stress of Cd + Pb as compared with single stress (Lanier et al., 2019). Hence, it is urgently necessary to develop effective strategies to reduce the phytotoxic influence of combined stress by Cd and Pb in plants.

So far, several chemical, physical and biological approaches were practiced for decreasing the adverse effects from heavy metal stress. Of all these approaches, the exogenous application of plant growth regulators has been recognized as an economical and effective approach for largescale use on heavy metal contaminated farmlands (Spormann et al., 2021). Polyamines (PAs) are a kind of phytohormone-like aliphatic nitrogenous compounds in plants. Previous studies showed PAs were involved in many physiological processes of plants, such as cell division, organ development, fruit ripening, and abiotic stress (Kiekowska and Adamus, 2021). PAs mainly include putrescine (Put), spermine (Spm), and spermidine (Spd). Among which, Spd is most closely related to stress tolerance in the plants. Jankovska-Bortkevič et al. (2020) found Spd improved cold resistance of winter oilseed rape by activating a defensive response, increasing free proline content, and delaying ethylene emission. Fang et al., 2020 reported that Spd significantly increased biomass, decreased active oxygen (ROS) content, and markedly promoted the antioxidant enzymes activities of germinating soybeans under NaCl stress. In addition, Li et al. (2018) showed that Spd could mitigate the adverse effects of drought stress on photosynthetic pigments by maintaining the thylakoid membranes in an orderly arrangement. Recently, considerable attention has been paid to the role of PAs on plant growth under heavy metal stress. Exogenous PAs treatment could enhance the heavy metal stress tolerance (Ahanger et al., 2020). For example, application of exogenous Spd enhanced Pb tolerance in Salix matsudana, Cd tolerance in Hydrocharis dubia, and Mn tolerance in Brassica juncea (Hussain et al., 2019; Tang et al., 2017; Yang et al., 2013). Jiang et al. (2021) reported that Spd alleviated the adverse effects of aluminum toxicity in rice by reducing Al concentration, elevating other nutrient elements and photosynthetic performance. PAs are considered not only simply as direct protective molecules, but also as a stress signal regulator involved in a complex signaling system. PAs also play a major role in balancing ROS levels of cells, thus protecting the cells from oxidative stress (Tajti et al., 2018). Exogenous application of Spd could activate non-enzymatic and enzymatic antioxidant defense of mung bean to reduce the levels ROS and oxidative stress (Nahar et al., 2017). Tang et al. (2019) also found that exogenous Spd decreased the accumulation of ROS by up-regulating the contents of soluble protein, superoxide dismutase (SOD) in S. matsudana under Cd stress. Despite many researches describing the effects of heavy metal toxicity on plant, the precise mechanisms of how PAs control plant responses under heavy metal stress remain elusive. Furthermore, there have been no reports of the role of PAs on plant growth under combined heavy metal stress.

Rice (Oryza sativa L.), one of the most important food cereals, could easily absorb Cd and Pb (Ronzan et al., 2018). Previous studies have shown that Cd and Pb could be accumulated in diverse organs and tissues of rice, which not only inhibited the growth and development, but also posed a risk to humans through the food chain (Doğru, 2020; He et al., 2014). Our preliminary experiment displayed that combined stress by Cd and Pb caused more serious inhibition in the biomass of rice roots and shoots than single stress (data not shown). Correspondingly, improving Cd and Pb tolerance of rice is highly valuable for rice production. To our knowledge, the effect of exogenous application of Spd on various morpho-physiological parameters of rice subjected to Cd + Pb stress has not been investigated yet. Therefore, our research aimed to explore the effects and mechanism of exogenous Spd in rice seedlings under Cd + Pb stress. The growth performance, photosynthetic pigments, antioxidant enzymes, osmolytes, secondary metabolites, mineral nutrient contents, as well as accumulation and translocation of Cd and Pb under varied levels of Spd were analyzed. This study can extend our knowledge of the beneficial roles of Spd and provide some basis for the application of Spd to improve plant tolerance against combined heavy metal stress.

Section snippets

Plant materials, growing conditions and treatments

Seeds of rice (Oryza sativa L. cv. Zhongyou 169) were obtained from Tongren xintiandi agriculture co., Ltd, China. The rice seeds were surface sterilized with 5% (v/v) sodium hypochlorite solution for 15 min, thoroughly washed several times with sterile deionized water and soaked in distilled water at 25 °C for 24 h. The soaked seeds were sown in Petri dishes and allowed to germinate on wet filter paper at 28 °C for 10 d. The uniformly germinated seeds were transplanted to hydroponic medium

Growth parameters and contents of photosynthetic pigments and mineral nutrients

The treatment of Cd + Pb significant inhibited the growth of rice seedlings and decreased contents of photosynthetic pigments and mineral nutrients of roots and shoots (Table 1, Fig. S1 and Tables S1 and S2). However, Spd at 0.1–2.0 mmol L−1 improved plant height, root length, dry and fresh weight, and contents of photosynthetic pigments and mineral nutrients in rice seedlings under Cd + Pb stress, especially 0.5 mmol L−1 Spd treatment. Compared with Cd + Pb treatment alone, the plant height,

Discussions

As is known to all, heavy metal pollution including Cd and Pb represents a serious threat to agricultural crops, which will negatively affect plant growth and development. In this study, rice seedlings exposure to Cd + Pb stress exhibited visible toxic symptoms with a decline of plant height, root length, as well as dry and fresh weight (Table 1). Similar findings were shown in sunflower plants under Cd stress, and Ceratophyllum demersum under Cu + Zn stress (Hak et al., 2020; Saidi et al., 2021

Conclusion

In conclusion, Spd could promote the rice growth under Cd + Pb stress and 0.5 mmol L−1 Spd had the best mitigative effect. Spd reduced the accumulation of Cd and Pb, improved the levels of photosynthetic pigments, osmolytes, secondary metabolites and antioxidant enzymes activities, and thus mitigated ROS toxicity on cell membranes and photosynthetic systems in rice seedlings under Cd + Pb treatment. Therefore, our study recommend the use of Spd as an effective biostimulator to boost heavy

Author contribution statement

JH and YR conceived the project, designed the experiments and supervised the research work. JG conducted the experiments, analyzed the data and wrote the first draft of the manuscript. CH helped in data curation, software validation and statistical analysis. XJ contributed to the data interpretation and manuscript preparation. DS helped in manuscript editing. All authors read and approved the manuscript.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31460100, 31660477), Postgraduate Research & Practice Innovation Program of Jiangsu Province, China (KYCX21-2872 and KYCX22-3107).

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