Alleviation of heavy metal stress by arbuscular mycorrhizal symbiosis in Glycine max (L.) grown in copper, lead and zinc contaminated soils

Abstract

There are few reports on the use of arbuscular mycorrhizal fungi (AMF) to promote growth and stress tolerance of soybean (Glycine max L.) in agricultural soils contaminated with heavy metals. The present study evaluated the role of AMF in promoting tolerance and growth, as well as uptake of heavy metals in shoots of soybean plants. Soybean plants were inoculated with AMF (Funneliformis mosseae) in a pot experiment polluted with different concentrations of heavy metals [copper (Cu), lead (Pb) and zinc (Zn)] as well as their combination. The tested AMF inoculum promoted the soybean growth and seed yield. Increased colonization of the soybean roots improved the soybean growth through increased phosphorus uptake and accumulation in the plant tissues by 68.8%. The results showed that soybean grown in the contaminated soils inoculated with AMF were more tolerant in alleviating the metals toxicity by retaining the heavy metals in the roots, thereby reducing translocation of Cu, Pb and Zn by 21.8, 57.6 and 67.3% respectively in the aerial part of the plant and improving the overall plant productivity by 59.1%. The findings provide evidence of the potential of AMF in phytoremediation of agricultural soils contaminated with toxic metals.

Introduction

In recent years, the pollution of agricultural soils with heavy metals by anthropogenic activities and agricultural practices, including excessive input of agrochemicals, has become a major concern for the sustainability of production in most crops (Li et al., 2014; Rafique and Tariq 2016). In most contaminated soils, heavy metals such as copper (Cu), lead (Pb) and zinc (Zn) are widespread and non-degradable (Ranjan et al., 2017). Considering the significance of some essential heavy metals such as Cu and Zn for plant structural and enzymes activation, their high soil concentrations can cause plant phytotoxicity and stunted growth (Anjum et al., 2015; Alongi 2017). In addition, ingestion of edible parts of plants such as fruits or grains may pose significant health risks to humans and animals (Toth et al., 2016). Plants have evolved many adaptive and tolerance strategies in alleviating toxicity to heavy metals in contaminated soils (Li et al., 2015). The formation of a symbiotic relationship in roots with arbuscular mycorrhizal fungi (AMF) was reported to be one of the most successful methods for enhancing the tolerance of host plants in soils contaminated with heavy metals (Joner and Leyval 1997; González-Chávez et al., 2019). Arbuscular mycorrhizal fungi are often found in heavy metal-polluted soils (Wang, 2017; Huang et al., 2018). Most plants form a symbiotic relationship with AMF (Smith and Read, 2008). The AMF hyphae acts as an intermediary between plants and fungi for nutrient uptake, in particular phosphorus (P) in exchange for carbohydrates from the host plant (Smith and Read, 2008). Several researchers have recently focused their attention on the use of AMF in contaminated soils to immobilize heavy metals (Gu et al., 2017; González -Chávez et al., 2019). Extra and intra-radical AMF mycelia, as well as vesicles and spores, act as an effective sink of heavy metals (Wang et al., 2017; Liu et al., 2018). In addition, P nutrition is reported to be an essential element in promoting plant tolerance through detoxification of heavy metals (Andrade et al., 2004). Inoculation with AMF improve plant growth and indirectly alleviate the stress induced by excess metals in the soil because of the boost of P uptake by AMF (Zhan et al., 2016). In some findings, AMF decreased plant uptake of heavy metals such as Zn, Cd, and Mn (Li and Christie 2000), whereas, in others increased uptake was reported (Jamal et al., 2002; Liao et al., 2003). Nevertheless, the reports on the impacts of AMF on host plant P absorption under heavy metal toxicity remain contradictory.

Most polluted soils naturally contain a mixture of various heavy metals at various concentrations (Versieren et al., 2016). Therefore, in predicting the phytotoxic effects of multiple metals and their absorption in plants, reports of single metal pollution may not be accurate, since the concentration of heavy metals in plants depend on their soil concentrations and interaction that may be antagonistic or synergistic (Wu et al., 2016). There are inconsistencies in previous studies on the ameliorative effects of AMF inoculation, which could be linked to the fugal species, host plant(Yang et al., 2015) heavy metal type and soil concentrations (Wu et al., 2015; Doubková and Sudová 2016). It is therefore important to provide a precise understanding of the impact of AMF on alleviating the toxicity of heavy metals in crops, as well as their mycoremediation strategies in both single and multi-metal soil contaminations.

Soybean (Glycine max L.) is an oilseed legume commonly cultivated in most parts of the world due to its high quality oil and protein content for livestock and human consumption, as well as for industrial purposes (Adeyemi et al., 2020). In spite of several reports on the growth promoting ability of AMF under heavy metal toxicity, there are limited findings on the effects of AMF on soybean in contaminated soils. Arbuscular mycorrhizal fungal isolate (Funneliformis mosseae) was chosen based on its beneficial effects on plant growth and P uptake in soybean (Thioub et al., 2019) as well as its reported predominance in heavy metal contaminated soils (Yang et al., 2015). Thus, this study presumed that (1) the AMF isolate would support the growth of soybean and P-nutrition in heavy metal contaminated soils, (2) the P-nutrition of AMF would lead to plant tolerance and alter the content, translocation and uptake of Cu, Pb and Zn in soybean tissues.