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The Authors
☆
This paper has been recommended for acceptance by Jörg Rinklebe.
Role of the proteome in providing phenotypic stability in control and ectomycorrhizal poplar plants exposed to chronic mild Pb stress
Agnieszka
Szuba
Conceptualization
Methodology
Validation
Formal analysis
Investigation
Resources
Writing - original draft
Writing - review & editing
Visualization
Supervision
Project administration
Funding acquisition
a
∗
aszuba@man.poznan.pl
Łukasz
Marczak
Methodology
Validation
Formal analysis
Investigation
Data curation
Writing - review & editing
b
Rafał
Kozłowski
Methodology
Validation
Investigation
Data curation
Writing - review & editing
c
a
Institute of Dendrology, Polish Academy of Sciences, Parkowa 5, 62-035, Kórnik, Poland
Institute of Dendrology
Polish Academy of Sciences
Parkowa 5
Kórnik
62-035
Poland
Institute of Dendrology, Polish Academy of Sciences, Parkowa 5, 62-035 Kornik, Poland
b
Institute of Bioorganic Chemistry, Polish Academy of Sciences, Noskowskiego 12/14, 61-704, Poznań, Poland
Institute of Bioorganic Chemistry
Polish Academy of Sciences
Noskowskiego 12/14
Poznań
61-704
Poland
Institute of Bioorganic Chemistry, Polish Academy of Sciences, Noskowskiego 12/14, 61-704 Poznan, Poland
c
Institute of Geography and Environmental Sciences, Jan Kochanowski University, Universytecka 7, 24-406, Kielce, Poland
Jan Kochanowski University
Institute of Geography and Environmental Sciences
Universytecka 7
Kielce
24-406
Poland
Jan Kochanowski University, Institute of Geography and Environmental Sciences, Poland
∗
Corresponding author.
Abstract
Lead is a dangerous pollutant that accumulates in plant tissues and causes serious damage to plant cell macromolecules. However, plants have evolved numerous tolerance mechanisms, including ectomycorrhizae, to maintain cellular Pb2+ at the lowest possible level. When those mechanisms are successful, Pb-exposed plants should exhibit no negative phenotypic changes. However, actual molecular-level plant adjustments at Pb concentrations below the toxicity threshold are largely unknown, similar to the molecular effects of protective ectomycorrhizal root colonization. In this study, we (1) determined the molecular adjustments in plants exposed to Pb but without visible Pb stress symptoms and (2) examined ectomycorrhizal root colonization (the role of fungal biofilters) with respect to molecular-level Pb perception by plant root cells. Biochemical, microscopic, proteomic and metabolomic studies were performed to determine the molecular status of Populus × canescens microcuttings grown in agar medium enriched with 0.75 mM Pb(NO3)2. Noninoculated and inoculated with Paxillus involutus poplars were analyzed in two independent comparisons of the corresponding control and Pb treatments. After six weeks of growth, Pb caused no negative phenotypic effects. No Pb-exposed poplar showed impaired growth or decreased leaf pigmentation. Proteomic signals of intensified Pb sequestration in the plant cell wall and vacuoles, cytoskeleton modifications, H+-ATPase-14-3-3 interactions, and stabilization of protein turnover in chronically Pb-exposed plants co-occurred with high metabolomic stability. There were no differentially abundant root primary metabolites; only a few differentially abundant root secondary metabolites and no Pb-triggered ROS burst were observed. Our results strongly suggest that proteome adjustments targeting Pb sequestration and ROS scavenging, which are considerably similar but less intensive in ectomycorrhizal poplars than in control poplars due to the P. involutus biofilter (as confirmed in a mineral study), were responsible for the metabolomic and phenotypic stability of poplars exposed to chronic mild Pb stress.
Graphical abstract
Image 1
Highlights
•
Effects of Pb in non-inoculated and ectomycorrhizal roots were analyzed using OMIC tools.
•
Proteomic signals of intensified Pb sequestration and cytoskeletal changes were found.
•
More PM- and V-type H+ATPases but less 14-3-3 proteins were found in Pb-exposed roots.
•
Stabilization of protein turnover in chronically Pb-exposed plants was observed.
•
The molecular response was less intense in ECM plants due to the fungal bio-filter.
Main finding of the work: Proteome adjustments, whose magnitude was reduced under ECM due to the presence of a fungal biofilter, were responsible for the phenotypic stability of poplars during chronic mild Pb stress.
Keywords
Root proteome
Root metabolome
Heavy metals
Ectomycorrhiza
Increased tolerance
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