ORIGINAL ARTICLE
Co-inoculation of Lolium perenne with Funneliformis mosseae
and the dark septate endophyte Cadophora sp. in a trace
element-polluted soil
Charlotte Berthelot
1
&
Damien Blaudez
1
&
Thierry Beguiristain
1
&
Michel Chalot
2,3
&
Corinne Leyval
1
Received: 25 October 2017 / Accepted: 7 February 2018 / Published online: 3 March 2018
#
Springer-Verlag GmbH Germany, part of Springer Nature 2018
Abstract
The presence of dark septate endophytes (DSEs) or arbuscular mycorrhizal fungi (AMF) in plant roots and their effects on plant
fitness have been extensively described. However, little is known about their interactions when they are simultaneously colo-
nizing a plant root, especially in trace element (TE)-polluted soils. We therefore investigated the effects of Cadophora sp. and
Funneliformis mosseae on ryegrass (Lolium perenne) growth and element uptake in a Cd/Zn/Pb-polluted soil. The experiment
included four treatments, i.e., inoculation with Cadophora sp., inoculation with F. mosseae, co-inoculation with Cadophora sp.
and F. mosseae, and no inoculation. Ryegrass biomass and shoot Na, P, K, and Mg concentrations significantly increased
following AMF inoculation as compared to non-inoculated controls. Similarly, DSE inoculation increased shoot Na concentra-
tion, whereas dual inoculation significantly decreased shoot Cd concentration. Moreover, oxidative stress determined by ryegrass
leaf malondialdehyde concentration was alleviated both in the AMF and dual inoculation treatments. We used quantitative PCR
and microscope observations to quantify colonization rates. They demonstrated that DSEs had no effect on AMF colonization,
while AMF colonization slightly decreased DSE frequency. We also monitored fluorescein diacetate (FDA) hydrolysis and
alkaline phosphatase (AP) activity in the rhizosphere soils. FDA hydrolysis remained unchanged in the three inoculated treat-
ments, but AMF colonization increased AP activity and P mobility in the soil whereas DSE colonization did not alter AP activity.
In this experiment, we unveiled the interactions between two ecologically important fungal groups likely to occur in roots which
involved a decrease of oxidative stress and Cd accumulation in shoots. These results open promising perspectives on the fungal-
based phytomanagement of TE-contaminated sites by the production of uncontaminated and marketable plant biomass.
Keywords Arbuscular mycorrhizal fungi
.
Dark septate endophyte
.
Co-inoculation
.
Cadophora sp.
.
Funneliformis mosseae
.
Heavy metal pollution
Introduction
Intense human activities such as mining, industries, waste
disposal, and fertilizer applications have dramatically in-
creased soil contents of trace elements (TE) (Tóth et al.
2016). TE persist in the environment for a long time, and their
effects on human health and ecosystems are of great concern.
PlantscanbeusedtoreducemetaldispersionfromTE-
contaminated soils into the atmosphere, the soil, and ground-
water. Such phytomanagement is economically attractive be-
cause it produces nonedible biomass for commercial products
such as bioenergy, biofuels, building and construction mate-
rials, or timber (Evangelou and Deram 2014). Adapted TE-
tolerant soil microorganisms can enhance plant growth and
nutrition in such stressed environments (Ma et al. 2011).
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s00572-018-0826-z) contains supplementary
material, which is available to authorized users.
* Corinne Leyval
corinne.leyval@univ-lorraine.fr
1
Université de Lorraine, CNRS, LIEC, F-54000 Nancy, France
2
Université de Bourgogne Franche-Comté, CNRS, Laboratoire
Chrono-Environnement, Pôle Universitaire du Pays de Montbéliard,
F-25211 Montbéliard, France
3
Université de Lorraine, F-54000 Nancy, France
Mycorrhiza (2018) 28:301–314
https://doi.org/10.1007/s00572-018-0826-z
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