The heavy metal paradox in arbuscular mycorrhizas: from mechanisms to biotechnological applications

Abstract

Arbuscular mycorrhizal symbioses that involve most plants and Glomeromycota fungi are integral and functional parts of plant roots. In these associations, the fungi not only colonize the root cortex but also maintain an extensive network of hyphae that extend out of the root into the surrounding environment. These external hyphae contribute to plant uptake of low mobility nutrients, such as P, Zn, and Cu. Besides improving plant mineral nutrition, arbuscular mycorrhizal fungi (AMF) can alleviate heavy metal (HM) toxicity to their host plants. HMs, such as Cu, Zn, Fe, and Mn, play essential roles in many biological processes but are toxic when present in excess. This makes their transport and homeostatic control of particular importance to all living organisms. AMF play an important role in modulating plant HM acquisition in a wide range of soil metal concentrations and have been considered to be a key element in the improvement of micronutrient concentrations in crops and in the phytoremediation of polluted soils. In the present review, we provide an overview of the contribution of AMF to plant HM acquisition and performance under deficient and toxic HM conditions, and summarize current knowledge of metal homeostasis mechanisms in arbuscular mycorrhizas.

Arbuscular mycorrhizal colonization has little consequence for plant heavy metal uptake in contaminated field soils

“…1). Numerous mechanisms have been proposed for how AMF may affect plant metal uptake, including reducing plant uptake by altering soil metal bioavailability or sequestering metals in their own tissues, or increasing plant uptake by actively translocating metals into plants through pathways presumably evolved for nutrient transfer (reviewed by Schützendübel and Polle 2002; Göhre and Paszkowski 2006; Miransari 2011, Ferrol et al 2016). If AMF colonization decreases plant metal uptake, then AMF would be expected to alleviate plant metal toxicity.…”

“…Alternatively, if colonization increases plant metal uptake, then AMF could exacerbate plant metal toxicity. AMF colonization effects on plant metal uptake also need not be linear (Audet and Charest 2007, Ferrol et al 2016). …”

Incipient local adaptation in a fungus: evolution of heavy metal tolerance through allelic and copy-number variation

“…Metal immobilization occurs through the action of chelating agents. In fungi these can occur both outside and inside the cell, with for example hydrophobins and melanins binding metals to the fungal cell wall 37 and nicotianamine as key in maintaining metal ion homeostasis within the cell [81][82][83] . ROS detoxification occurs when antioxidants (e.g.…”

“…Fifteen candidate genes were involved in metal exclusion and storage, with four genes predicted to actively pump metal ions across membranes located either in the plasma membrane (contributing to extruding metals to the cell exterior) or vesicle and vacuole membranes (creating metal storage that can be either kept in the cell or extruded). Examples of these genes include the cation diffusion facilitator transport proteins that are predicted to aid in zinc ion homeostasis 34 and an iron permease gene predicted to transport iron ions across membranes but also reported to interact with other metal such as zinc and cadmium 33,37 . We detected many more genes involved in membrane transport and metal exclusion and storage (Table 1), however it is unclear how exactly they contribute to heavy metal tolerance in S. luteus.…”

“…These metals cannot therefore be completely excluded from cells and tight regulatory systems ensure balance between heavy metal detrimental excess and deficiency 33,35,36 . Metal homeostasis systems are based on four main concomitant strategies: metal exclusion, storage, immobilization, and ROS detoxification 35,37 . Metal exclusion and storage is achieved through transmembrane transporter proteins that are responsible for moving metal ions across membranes and import or extrude metal ions to/from the cell or into membrane-bound vesicles or vacuoles.…”