Ectomycorrhizal Fungal Strains Facilitate Cd2+ Enrichment in a Woody Hyperaccumulator under Co-Existing Stress of Cadmium and Salt

Abstract

Cadmium (Cd²⁺) pollution occurring in salt-affected soils has become an increasing environmental concern in the world. Fast-growing poplars have been widely utilized for phytoremediation of soil contaminating heavy metals (HMs). However, the woody Cd²⁺-hyperaccumulator, Populus × canescens, is relatively salt-sensitive and therefore cannot be directly used to remediate HMs from salt-affected soils. The aim of the present study was to testify whether colonization of P. × canescens with ectomycorrhizal (EM) fungi, a strategy known to enhance salt tolerance, provides an opportunity for affordable remediation of Cd²⁺-polluted saline soils. Ectomycorrhization with Paxillus involutus strains facilitated Cd²⁺ enrichment in P. × canescens upon CdCl₂ exposures (50 μM, 30 min to 24 h). The fungus-stimulated Cd²⁺ in roots was significantly restricted by inhibitors of plasmalemma H⁺-ATPases and Ca²⁺-permeable channels (CaPCs), but stimulated by an activator of plasmalemma H⁺-ATPases. NaCl (100 mM) lowered the transient and steady-state Cd²⁺ influx in roots and fungal mycelia. Noteworthy, P. involutus colonization partly reverted the salt suppression of Cd²⁺ uptake in poplar roots. EM fungus colonization upregulated transcription of plasmalemma H⁺-ATPases (PcHA4, 8, 11) and annexins (PcANN1, 2, 4), which might mediate Cd²⁺ conductance through CaPCs. EM roots retained relatively highly expressed PcHAs and PcANNs, thus facilitating Cd²⁺ enrichment under co-occurring stress of cadmium and salinity. We conclude that ectomycorrhization of woody hyperaccumulator species such as poplar could improve phytoremediation of Cd²⁺ in salt-affected areas.

Keywords: Cd flux; MAJ; NAU; NaCl; PM H+-ATPase; Paxillus involutus; Populus × canescens; annexins; calcium-permeable channels.