Pb Stress and Ectomycorrhizas: Strong Protective Proteomic Responses in Poplar Roots Inoculated with Paxillus involutus Isolate and Characterized by Low Root Colonization Intensity

The commonly observed increased heavy metal tolerance of ectomycorrhized plants is usually linked with the protective role of the fungal hyphae covering colonized plant root tips. However, the molecular tolerance mechanisms in heavy metal stressed low-colonized ectormyocrrhizal plants characterized by an ectomycorrhiza-triggered increases in growth are unknown. Here, we examined Populus × canescens microcuttings inoculated with the Paxillus involutus isolate, which triggered an increase in poplar growth despite successful colonization of only 1.9% ± 0.8 of root tips. The analyzed plants, lacking a mantle-a protective fungal biofilter-were grown for 6 weeks in agar medium enriched with 0.75 mM Pb(NO3)2. In minimally colonized 'bare' roots, the proteome response to Pb was similar to that in noninoculated plants (e.g., higher abundances of PM- and V-type H+ ATPases and lower abundance of ribosomal proteins). However, the more intensive activation of molecular processes leading to Pb sequestration or redirection of the root metabolic flux into amino acid and Pb chelate (phenolics and citrate) biosynthesis coexisted with lower Pb uptake compared to that in controls. The molecular Pb response of inoculated roots was more intense and effective than that of noninoculated roots in poplars.