Effects of decapitated and root-pruned Sedum alfredii on the characterization of dissolved organic matter and enzymatic activity in rhizosphere soil during Cd phytoremediation

Highlights

• The biomass and Cd uptake in S. alfredii were risen by decapitation and root cutting.

• DOM levels in the soils enhanced with the application of agronomic practices.

• The hydrophilic fractions were increased obviously by decapitation and root cutting.

• Activities of soil enzymes were significantly increased by root-pruned S. alfredii.

• Treated S. alfredii can increased the Cd extraction capacities of DOM.

Abstract

Decapitation and root pruning, can impact plant morphological and physiological characteristics, which may determine the efficiency of phytoremediation. However, the effects of decapitated and root-pruned plants on the characterization of dissolved organic matter (DOM) and enzymatic activity, which determine the bioavailability of soil pollutants, have rarely been reported. This study aims to characterize DOM and enzymatic activity in the rhizosphere soil of Sedum alfredii when treated by decapitation and root pruning. Decapitation, slight pruning (10% root cutting), and their combination stimulated S. alfredii to secrete more DOM in the rhizosphere soil compared with the control. Furthermore, the proportions of hydrophilic increased from 42.7% in the control to 57.1% in the decapitation and slight pruning combination. Soil urease, invertase, and neutral phosphatase activities were higher in the rhizosphere soil of decapitated and root-pruned S. alfredii, and the highest values were observed with their combination. DOM from the soils of decapitated and root-pruned S. alfredii had significantly higher Cd extraction ability compared with that of the untreated species. Based on the findings of this study, we suggest that decapitation and root pruning can improve the phytoremediation efficiency of S. alfredii by increasing the bioavailability of Cd in its rhizosphere.

Introduction

Soil is a common sink for various pollutants, including metals, and anthropogenic activities are one of the major sources of metal contamination globally (Cytryn, 2013). Cd is a highly toxic heavy metal because of its high bioavailability and activity, and has been ranked 7 among the top 20 pollutants because of its detrimental effect on the metabolic systems of living organisms (Yang et al., 2004). In addition to weathering, Cd in soils generally sourced from electroplating, printing, fertilization, municipal sludge, and sewage irrigation (Sterckeman et al., 2019). Cd enters plant tissues via root systems and migrates upward to aerial parts through membrane transporters for essential nutrients, such as Fe, Zn, and Ca (Zhang et al., 2012), and finally causes detrimental effects on human health through the food chain. Therefore, various methods such as chemical washing, excavation, immobilization, and in-situ electrokinetic remediation have been developed to decontaminate Cd-polluted soils. However, these methods are labor-intensive and only effective in small fields (Manousaki et al., 2008). In addition, these technologies also disturb the physical structure and biological function of soils and cannot be used to decontaminate large field areas with slight-to-moderate contamination levels, especially agricultural lands.

Plant-based remediation methods such as phytoextraction, phytostabilization, phytodegradation, and phytovolatilization are more acceptable because they are environmentally friendly and economically feasible (Khan et al., 2018). Fast-growing and high-biomass-producing plants, including Salix viminalis, Thuja orientalis, and Populus tomentiglandulosa (Jagtap et al., 2014), and hyperaccumulators, including Pteris vittata, Sedum alfredii, and Arabis paniculata (Li et al., 2018), have been studied to determine the activation, uptake, migration, accumulation, and tolerance mechanisms of heavy metals. However, high levels of Cd in plant tissues result in excessive generation of reactive oxygen species (ROS), which irreversibly damage cells and cause severe physiological dysfunction such as inhibition of growth rate, reduction of nutrient extraction efficiency, and alteration of chloroplast ultrastructure (Sánchez-Pardo et al., 2015). Therefore, the success of phytoremediation is determined by the balance between metal accumulation and biomass yield of plants.

Enhancing the biomass production and metal extraction of plants is pivotal for phytoremediation in metal-contaminated soils, and thus, a full understanding of plant mechanisms that mobilize and extract the contaminants is necessary. It has been reported that the application of common agronomic management practices such as decapitation and root pruning can improve the phytoextraction effect of Stevia rebaudiana (Pal et al., 2013) and Celosia argentea (Liu et al., 2017) because they can break the apical dominance, which hampers the emergence of lateral apices, thereby enhancing the dry weight, nutrient uptake ability, and transpiration rate of plants.

In addition to the plant itself, plant–soil interactions influence the bioavailability of metals in soils, especially the rhizosphere, and the metal extraction capacity of plants. Various indexes, including pH, moisture content, salinity, soil microorganisms, and organic matter, can impact metal bioavailability in soils. pH changes in plant-growing soils have been investigated; however, inconsistent findings have been reported. For instance, Nicotiana tabacum significantly reduced the pH of its rhizosphere (Loosemore et al., 2004), while Brassica juncea increased the pH by 1.3 after cultivation (Kim et al., 2010). The conflicting findings demonstrate that the reduction of pH in the rhizosphere is not the only mechanism for activating metals in soils by plants, especially by hyperaccumulators.

Dissolved organic matter (DOM) containing hydrophilic and hydrophobic fractions is also an important index that impacts metal bioavailability and toxicity in rhizosphere soils (Borggaard et al., 2019). These compounds can generate metal-organic complexes to increase metal solubility (Chaturvedi et al., 2018), or can compete with metals for adsorption points on the soil surface through preferential adsorption, which decreases the adsorption capacity of soil particles and increases the metal bioavailability for plants (Chen et al., 2018). Christensen and Christensen (2000) established the relationships between the conditional complex formation constant and pH for Cd, Ni, and Zn, and found that chemical fraction and metal mobilization were controlled by DOM when soil pH exceeded 5.5. The results indicated that the characterization of DOM in the rhizosphere soils needs to be investigated.

Furthermore, it has been reported that plants can modulate the microenvironments of their rhizosphere to enhance nutrient uptake via different pathways, including acidification, increasing soil porosity, activating microorganisms, and excreting organic matter (Lin et al., 2018, Vasudevan et al., 2018). In contrast, plants can secrete more DOM into the rhizosphere soils when exposed to metal pollution, reducing the uptake rate of the metal (Guilpain et al., 2018). Previous studies have summarized the characterization of DOM from soil solution, sludge, and rhizosphere soil, with most studies focused on the adsorption capacity of DOM on substrate components and its impact on pollutant mobilization and toxicity (Guillon et al., 2019, Li et al., 2013, Mehmood et al., 2017). However, the effects of decapitation and root pruning on DOM characterization and metal solubility, which determine the success of phytoremediation, have not been fully investigated; therefore, it is crucial to investigate their influences on the rhizosphere soil of decapitated and root-pruned plants during phytoremediation.

S. alfredii, a well-known Cd hyperaccumulator found in South China, can accumulate 9000 mg Cd kg⁻¹ and 29000 mg Zn kg⁻¹ without showing any toxicity symptoms under hydroponic conditions (Wang et al., 2019), which makes it a potential phytoextractor for Cd. Previous studies have suggested that decapitation and root pruning can alter the physiological functions of a Cd hyperaccumulator and increase its Cd uptake efficiency (Liu et al., 2017). Whether these agronomic practices can modulate DOM in the rhizosphere has not been reported yet. The present study aims to (1) estimate the impacts of decapitation and root pruning on dry weight generation and Cd accumulation capacity of S. alfredii; (2) evaluate the changes of concentrations, fractionations, and Cd extraction ability of DOM in the rhizosphere of S. alfredii under different treatments; and (3) reveal the effects of DOM on soil Cd availability and Cd phytoextraction efficiency of S. alfredii.