Research PaperTranscriptome analysis reveals different mechanisms of selenite and selenate regulation of cadmium translocation in Brassica rapa
Introduction
Cadmium (Cd) is a highly toxic heavy metal. It is wildly distributed in soil and can be readily taken up by vegetables, which are the main source of Cd intake in east Asia [5]. Once Cd enters the exodermis from soil, it is transported in the symplastic and apoplastic pathways before being transferred to the shoot [5]. In the symplastic pathway, Cd is first taken up by protoplasmic influx metal transporters, such as iron-regulated transporter 1 (IRT1), natural resistance-associated macrophage protein 5 (NRAMP5), and yellow-stripe-like transporter 1 (YSL1; [18], [5]). Cd then moves radially to the vascular bundle under the regulation of the symplastic retention, where part of the Cd is complexed by phytochelatins, transported to the vacuoles, and stored by tonoplastic transporters [18], [20], [22], [6]. After arriving at the vascular bundle, Cd is loaded into the xylem by several P-type heavy metal ATPases (HMA) and translocated to the shoot [5].
The apoplastic retention mainly employs enhanced cell walls to limit and even block further movement of Cd to the xylem [18], [2], [32]. Cell walls mainly consist of polysaccharides with abundant functional groups that chelate Cd [32], [37]. Elevated levels of such polysaccharides could result in increased mechanical strength of cell walls and inhibit Cd translocation to the shoot [7], [32], [36]. The apoplastic pathway is primarily controlled by apoplastic barriers, the Casparian bands and suberin lamellae in the endodermis [18], [2]. Both barriers are enhanced cell walls due to the deposition of considerable amounts of lignin and suberin, and are too dense for Cd to pass freely [2], [3]. Therefore, higher levels of suberin and lignin could result in better-developed apoplastic barriers and lower cell wall permeability, thereby causing much less root-to-shoot translocation and accumulation of Cd in plants [23], [27].
Selenium (Se), an essential element for humans, is metabolized in the sulfur pathway, where Se (+6) is first activated under the catalysis of ATP sulfurylase (APS) as a rate-limiting step before being reduced to Se (+4) by glutathione (GSH). Subsequently, Se is rapidly reduced to selenide (–SeH) and joins the seleno-compound cycle to form various seleno-amino acids catalyzed by enzymes such as cystathionine gamma-synthase (CGS), cystathionine beta-lyase (CBL), and homocysteine S-methyltransferase (HMT; [28]). Se is proven to be effective in reducing Cd accumulation in crops by alleviating Cd-induced phytotoxicity and regulating Cd transport [11], [24]. Our earlier studies showed that Se improved Cd distribution in the cell wall and vacuoles in roots, thereby inhibiting Cd translocation [30], [39]. Se can improve the symplastic retention by stimulating phytochelatins (PCs) production and expression of tonoplastic transporters [37], [7]. Furthermore, Se alters the cell wall composition by increasing the levels of polysaccharides [32], [36], [44] and lignin [7] and enhancing Cd adsorption on the cell wall and thus significantly reduces Cd influx into plant cells and translocation to the shoot. However, the effects of Se on suberin production and deposition remain unclear.
Pak choi (Brassica rapa ssp. chinensis) is one of the most consumed leafy vegetables in China and can greatly contribute to Cd in dietary intake [9]. However, the mechanisms by which Se affects Cd transportation and retention in pak choi remain poorly understood, and even less is known about the Se-induced regulation of metal transporters, suberin and lignin synthesis, and cell wall reinforcement. Selenite and selenate are the most abundant Se species in soil, and Se fertilization is widely applied to reduce Cd accumulation in crops. In the current study, we compared the effects of Se, as selenite and selenate, on Cd accumulation and translocation in pak choi at different times, and attempted to explain the underlying mechanisms with the high-performance liquid chromatography (HPLC) speciation of Se and transcriptome analysis. This study provides a theoretical basis for the utilization of Cd-contaminated soil and the safe production of vegetables.
Section snippets
Hydroponic culture of pak choi
A hydroponic experiment with pak choi was conducted in a greenhouse under the following conditions: temperature at 25/15 ℃ (day/night), 14 h d−1 of photoperiod, 240–350 μmol m−2 s−1 of photon flux, and 70% of relative humidity. Full pak choi (Brassica rapa ssp. chinensis, “Hangzhouyoudonger”) seeds were washed with deionized water, surface-sterilized with 10% H2O2 for 30 min, and then thoroughly soaked in saturated CaSO4 (2.50 g L−1) for 4 h. The seeds were sowed in vermiculite, and 12 d later
Uptake of Cd and Se
No significant differences in biomass were observed between any of the treatments at 24 h or 72 h (Fig. S1). At 168 h, selenite increased the fresh weights of shoots and roots by 14% and 31%, respectively, compared to those exposed to Cd only, and the latter difference was significant (p < 0.05, LSD). However, biomass was not significantly affected by selenate.
Cd exhibited distinct accumulation patterns in the shoots and roots of pak choi (Figs. 1a and 1b); the Cd content in shoots at 168 h was
Selenite causes earlier reduction than selenate in Cd accumulation and translocation
Selenite and selenate are the most abundant forms of Se and the most commonly bioavailable inorganic Se species in the soil environment [28]. Therefore, we investigated the effects of these two Se species on the accumulation of Cd in pak choi at 24, 72, and 168 h. In this study, selenite and selenate differently affected the Cd content, uptake rates, and root-to-shoot translocation in the plant, which also varied with exposure time (Fig. 1). Selenite significantly reduced the Cd content in
Funding sources
This work was supported by the National Natural Science Foundation of China (No. 41907146) and China Agriculture Research System (CARS-23-B-15).
Environmental Implication
Cadmium (Cd) is widely-spread in the environment and Cd contamination in soil has also been widely reported. Cd is mainly taken up from soil by plant roots, thereby contributing to human intake through the food chains. Selenium (Se) has been proven effective to reduce Cd accumulation in the edible part of plants, yet the underlying mechanisms are still poorly understood. This work investigated such mechanisms of Se in terms of Se biotransformation and Cd root retention, providing a theoretical
CRediT authorship contribution statement
Yao Yu: Conceptualization, Methodology, Software, Formal analysis, Writing – original draft, Visualization. Qi Wang: Investigation, Formal analysis. Yanan Wan: Investigation, Formal analysis. Qingqing Huang: Methodology, Writing – review & editing, Supervision. Huafen Li: Methodology, Writing – review & editing, Supervision.
Declaration of Competing Interest
The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: Huafen Li reports financial support was provided by the National Natural Science Foundation of the People’s Republic of China. Huafen Li reports financial support was provided by Ministry of Agriculture and Rural Affairs of the People’s Republic of China.
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O, and significantly reduced Cd and Pb exposure to S. cucullate. Chromium adsorption by CNSAC filter layer was half (just 25% of total input) of the Cd and Pb. In treatment P, due to high Cd, Pb and Cr accumulation in S. cucullate, the antioxidant defense mechanism of the plant was collapsed and cell death was observed, which in turn has resulted reduced biomass gain (5% reduction). On the other hand, in treatment P + AC, an antioxidant defense mechanism was active in the form significantly (p ≤ 0.05) increased of SOD, CAT and proline content while reduced MDA, EL, %EB and soluble sugar. So, the application of CNSAC increased the heavy metal removal efficiency of H-VSSF-CW by adsorption of a considerable share of heavy metal and hence, reduced the heavy metal load/exposure to S. cucullate.