The 2 sites were divided into 4 replicated field blocks with a final plant density of 2200 tree h-1. Half of the trees were inoculated with a commercial inoculum made of a mix of mycorrhizal species. The sites presented different physico-chemical characteristics (e.g., texture: sandy soil versus silty-loam soil and organic matter: 5.7% versus 3.4% for Pierrelaye and Fresnes-sur-Escaut, respectively) and various trace element contamination levels.
Finally, this study demonstrated that this biofertilization approach could be recommended as an appropriate phytomanagement strategy, due to its capacity to significantly improve poplar productivity without any perturbations in soil mycobiomes.
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Aims: Afforestation of trace-element contaminated soils
has been demonstrated to be an attractive option for bioremediation due to the lower costs and dispersion of contaminants than conventional cleanup methods
Mycorrhizal fungi form symbiotic associations with plants
contributing to their tolerance towards toxic elements and actively participating to the biorestoration processes
The aim of this study was to deepen our understanding on the effects of mycorrhizal inoculation on plant development and fungal community at two trace-element contaminated sites (Pierrelaye and Fresnes-sur-Escaut
France) planted with poplar (Populus trichocarpa x Populus maximowiczii)
Methods: The 2 sites were divided into 4 replicated field blocks with a final plant density of 2200 tree h-1
Half of the trees were inoculated with a commercial inoculum made of a mix of mycorrhizal species
The sites presented different physico-chemical characteristics (e.g.
texture: sandy soil versus silty-loam soil and organic matter: 5.7% versus 3.4% for Pierrelaye and Fresnes-sur-Escaut
respectively) and various trace element contamination levels
inoculation showed a significant positive effect on poplar biomass production at the two sites
Fungal composition study demonstrated a predominance of the phylum Ascomycota at both sites
with a dominance of Geopora Arenicola and Mortierella elongata
and a higher proportion of ectomycorrhizal and endophytic fungi (with the highest values observed in Fresnes-sur-Escaut: 45% and 28% for ECM and endophytic fungi
well known for their capacity to have positive effects on plant development in stressful conditions
Pierrelaye site showed higher frequency (%) of mycorrhizal tips for ectomycorrhizal fungi (ECM) and higher intensity (%) of mycorrhizal root cortex colonization for arbuscular mycorrhizal fungi (AMF) than Fresnes-sur-Escaut site
which translates in a higher level of diversity
this study demonstrated that this biofertilization approach could be recommended as an appropriate phytomanagement strategy
due to its capacity to significantly improve poplar productivity without any perturbations in soil mycobiomes
through the inoculation of mycorrhizal strains to improve the quantity and diversity of the fungal community
to determine whether inoculum introduced during planting had a long-term effect on the growth of poplar
The sediment deposit site of Fresnes-sur-Escaut (F) is linked to past mining and metal-smelting activities
The properties of the two study soils represent two contrasting environments. The Pierrelaye site has a sandy soil (&gt; 80% sand), whereas the sediment of the Fresnes-sur-Escaut site has a silt-loam texture with higher mean organic matter (OM) content than the former (5.7% vs 3.4%; <a href="#B71">Phanthavongsa et&#xa0;al., 2017</a>)
bulk pHH2O of the two soils was similar and slightly alkaline
Half of the whips were inoculated (4 inoculated plots per clone) with a mycorrhizal consortium (as described in next section)
while the other half was left uninoculated (4 control plots per clone)
The fungal inoculum consisted of the AM fungus Rhizophagus irregularis DAOM 197198 strain (Agronutrition
which are both produced by Symbiom (Landskroun
Symbivit contains six AMF: Rhizophagus intraradices BEG140
Ectovit contains six ECM fungi: Hebeloma mesophaeum
Pisolithus arrhizus and Scleroderma citrinum
Propagule number (spores or mycelia) was 250000/L and 1800/L of Symbivit and Ectovit inocula
About 26000 propagules (25000 Symbivit + 180 Ectovit + 900 Agronutrition) were delivered to each tree
10 top-soil (0-20&#xa0;cm) samples were collected in each plot with a hand auger at a distance of 20&#xa0;cm from the trunks
and mixed together to form a composite sample that was used for chemical analyses
8 samples per site were selected based on the pseudo-total metal(oid) concentrations to perform the agronomic characterization
The samples were force air-dried at 40&#xb0;C to constant mass
Germany) and sieved to pass a 200 &#xb5;m mesh (AS 200
The following analyses were contracted to a private laboratory (Galys
K+ (K2O) and Na+ (Na2O); organic matter (OM) (NF ISO 14235); total nitrate (N) (NF ISO 13878); total phosphorus (P) (NF ISO 11263); total CaCO3 (NF ISO 10693); cation exchange capacity (CEC) (NF X 31-130); and soluble boron (B) (NF X 31-122)
Table&#xa0;1 CaCl2-extractable TE concentrations of topsoil samples (0-20&#xa0;cm) from the two sites (mg kg-1 DW)
Fresnes-sur-Escaut (F) and Pierrelaye (P) and two treatments (Control
Diameter at breast height (dbh, 1.3&#xa0;m) and total tree height (Htot) were measured in late autumn of 2017 (7 growing seasons), on 384 individual trees from the 8 plots (i.e., 24 trees per plot, excluding the border trees). Shoot biomass was calculated from Htot and dbh measurements that were taken for each tree (<a href="#B18">Ciadamidaro et&#xa0;al., 2017</a>)
These primers target a short portion of the fungal ITS region
which is appropriate for Illumina sequencing
Reads were assigned to each sample according to a unique barcode. Paired reads were grouped on a contig using the mothur pipeline (<a href="#B79">Schloss et&#xa0;al., 2009</a>). ITS1 sequences that were extracted using 18S and 5.8S motifs were searched on contigs using HMMER software (<a href="http://hmmer.org">http://hmmer.org</a>)
Contigs were then filtered by length (100 &lt; x &lt; 350 bp)
homopolymer (&lt; 10 bp) and unknown base (&lt; 0 bp)
The contigs were pre-clustered at 100% identity
Rare sequences that were represented by fewer than 2 reads in less than 2 different samples were removed from the analysis. Taxonomic assignments were performed using the database UNITE v7.2 (<a href="http://unite.ut.ee">http://unite.ut.ee</a>; <a href="#B56">K&#xf5;ljalg et&#xa0;al., 2013</a>)
Operational taxonomic units (OTUs) were then constructed using the Needleman-Wunsch distance and average neighbour clustering (Unweighted Pair Group Mean Averaging
The number of reads per sample was calculated after random sub-sampling of 30 000 reads
All statistical analyses, except for %M, were performed in the R environment (v. 3.6.1, <a href="#B74">R Core Team, 2019</a>)
Normality and homoscedasticity of the data were verified using Shapiro-Wilk tests and Bartlett&#x2019;s tests
Comparisons of treatment means were performed using post hoc tests following a one-way ANOVA
Tukey&#x2019;s tests were performed to separate multiple treatment means; Student&#x2019;s t-test were applied only when there were only two subgroups
All tests were considered significant at P&#xa0;&lt;&#xa0;0.05
Pgirmess and Vegan packages in R were used for the calculation of richness and diversity indices. Rarefaction curves were generated with the rarecurve function in Vegan (<a href="#B70">Oksanen et&#xa0;al., 2019</a>)
Two-dimensional non-metric multi-dimensional scaling (NMDS) was estimated using the Bray-Curtis method (k = 3) using the metaMDS function in the vegan package in R
The resulting clustering trees were paired with a heatmap of Spearman&#x2019;s correlations (rs) between the relative abundances created with heatmap.2 from the gplots package
The numbers of OTUs that were shared between treatments were created using Venn diagrams implemented by VennDiagram in the Vegan package in R
PCA (principal component analysis) was performed using the FactoMinR package (<a href="#B62">L&#xea; et&#xa0;al., 2008</a>)
Data below detection-limits were considered to be null for the calculation of the principal components
and ellipses were drawn at the 95% confidence interval of the barycentre of each species
In general, concentrations of CaCl2-extractable TE were higher at the Pierrelaye site just for Cu concentrations (<a href="#T1">Table&#xa0;1</a>)
After an additional growth period of 7 years, the inoculation treatment still had a significant effect on the biomass yield of Skado, which increased by +16 and +18% at Pierrelaye and Fresnes-sur-Escaut, respectively (<a href="#T2">Table&#xa0;2</a>)
the biomass production at the Pierrelaye site was greater than that at the Fresnes-sur-Escaut site
The fresh tree biomass increased by 101% (control) and 102% (inoculated) in Pierrelaye between 2015 and 2017
whereas it only increased by 74% (control) and 70% (inoculated) at Fresnes-sur-Escaut
Table&#xa0;2 Dendrometric parameters for poplars at the two experimental sites (Fresnes-sur-Escaut and Pierrelaye)
Cd and Zn were higher in Fresnes-sur-Escaut samples
had consistently higher concentrations in the bark compared to the wood
The greatest difference was observed for Ca (16- to 18-fold difference)
inoculation had no effect on element accumulation
the ratio of these concentrations between inoculated and non-inoculated samples ranged from 0.8 to 1.1
Figure&#xa0;1 Principal component analysis showing the correlations of the nutrients (A) and potential toxic elements (B) for the two study soils (Fresnes-sur-Escaut and Pierrelaye)
in two different plant tissues (wood and bark) and for the two treatments (control
Results of the Monte Carlo permutation test demonstrate the different distributions of the nutrients and potential toxic elements (P = 0.001)
Figure&#xa0;2 Values of microbial biomass carbon (MBC; mg C kg-1 dry soil) (A)
Intensity (%) of mycorrhizal root cortex colonization (% AMF) (B) and frequency (%) of mycorrhizal tips (% ECM) (C) for the two sites (Fresnes-sur-Escaut
Different letters above the bars denote significant differences by one way ANOVA (p&lt;0.05)
Table&#xa0;3 Richness and diversity indices of the fungal communities from the two sites (Fresnes-sur-Escaut
comparing the OTU dataset with the initial mycorrhizal species inoculated at the plantation stage
about half of these were detected after 7 years
and Hebeloma mesophaeum and Laccaria proxima (the ECM)
Figure&#xa0;3 Barplots showing the fungal community composition at the phylum (A) and class (B) level in soil for each site (Fresnes-sur-Escaut
To obtain a global view of the total fungal OTUs that were observed, the fungal communities of different sites and treatments are represented in a Venn diagram (<a href="#f4">Figure&#xa0;4A</a>). The sums of fungal OTUs observed in the four samples were 449, 457, 606 and 483 for the F_C, F_I, P_C and P_I treatments, respectively. The total number of OTUs in the present study was 781, while only 227 (29% of the total OTUs) were shared between the two sites (<a href="#f4">Figure&#xa0;4A</a>)
regardless of the site that was considered
especially for the Pierrelaye soil with a total of 421 OTUs (53%)
OTUs that were specific to each community represented between 5 to 6% for the Pierrelaye site
and from 6 to 8% for the Fresnes-sur-Escaut site
the highest proportion of unique OTUs was found in the inoculated treatment (F_I) for the Fresnes-sur-Escaut soil
Figure&#xa0;4 (A) Overlap of the different fungal communities from the two sites (Fresnes-sur-Escaut
The number of OTUs shared by all the communities were 227
(B) NMDS plot of the fungal community structure for the two sites using the Bray-Curtis dissimilarity measure
Each point represents the fungal community of a given sample
the two treatments for the two sites overlapped substantially
demonstrating the high degree of similarity between the communities in the two different treatments
A heatmap was constructed with the 50 most abundant OTUs in each of the two treatments for the two sites and showed clear clustering between the fungal communities of the two sites and a strong homogeneity between the communities of the control and inoculated samples (<a href="#f5">Figure&#xa0;5</a>)
while only 4 were unique to the Fresnes-sur-Escaut site
although they were not apportioned equally between the two treatments
Figure&#xa0;5 Comparison of the abundance of fungal OTUs among the 50 most abundant OTUs in at least one of the two sites (Fresnes-sur-Escaut
The dendrogram represents linkage clustering using Euclidean distance measures
OTU delineation was based as the cutoff of 97% sequence similarity
Assignements between brackets indicate the lower taxonomic level associated with the OTU using the Greengenes database
four OTUs for the Pierrelaye site that were represented by OTU00025 (Minimedusa polyspora)
OUT00016 (Solicoccozyma aeria) and OTU00046 (Cladorrhinum foecundissinum) were highly abundant in inoculated samples
OTU00045 (Minimedusa polyspora) was more abundant in control samples
OTU00031 (Mortierella alpina) and OTU00039 (Inocybe rimosa) were more abundant in the inoculated treatment
in which a smaller bark proportion compared to trunk
Rarefaction analyses and richness indices revealed that much of the total diversity detectable with Illumina-based sequencing was obtained. The demonstration of higher richness and diversity in the Pierrelaye site (a sandy site with lower concentrations of TE) compared to the Fresnes-sur-Escaut site (a silt-loam site with higher concentrations of TE) was consistent with the previous study of <a href="#B36">Foulon et&#xa0;al. (2016a)</a>
in which the Pierrelaye soil exhibited high richness and diversity indices
this hypothesis is greatly supported by an increase of biomass for the inoculated Skado poplars over time at the two sites
the symbiotic association of poplar with these two important groups of fungi could have favoured marked plant development and tolerance of the Skado clone to TE contamination
as well as resistance to antibiotics and antibiotic production
The data presented in the study are deposited in the ENA repository
Writing&#x2014;original draft preparation: LC
All authors have read and agreed to the published version of the manuscript
All authors contributed to the article and approved the submitted version
This research was funded by Agence Nationale de la Recherche (ANR)
grant number ANR-10-INTB-1703-01-BIOFILTREE&#x201d; and Natural Sciences and Engineering Research Council of Canada (NSERC) Strategic Project Grant to DK
We thank Voies Navigables de France (VNF) for allowing access to the Fresnes site and WFJ PARSONS for the English revision
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations
Any product that may be evaluated in this article
or claim that may be made by its manufacturer
is not guaranteed or endorsed by the publisher
The Supplementary Material for this article can be found online at: <a href="https://www.frontiersin.org/articles/10.3389/fpls.2022.993301/full#supplementary-material">https://www.frontiersin.org/articles/10.3389/fpls.2022.993301/full#supplementary-material</a>
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Received: 13 July 2022; Accepted: 05 October 2022;Published: 28 October 2022
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*Correspondence: Lisa Ciadamidaro, <a id="encmail">bGlzYS5jaWFkYW1pZGFyb0B1bml2LWZjb210ZS5mcg==</a>
Universit&#xe9; Bourgogne Franche-Comt&#xe9;
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