Mycorrhizal and microbial interactions in sustainable management of agricultural and forest ecosystems - SFR Condorcet
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Calais – SFR Condorcet – June 2018
Mycorrhizal and microbial interactions in sustainable
management of agricultural and forest ecosystems
Why do the root microbiota of plants should be considered in the
sustainable management of forest and agricultural ecosystems?
Marc Buée
INRA Nancy, France
UMR 1136 Interactions Arbres - Microorganismes, INRA, Université de Lorraine
Calais – SFR Condorcet – June 2018
From fungus to plant: never alone…
Arbuscular mycorrhizal (AM) fungi are generally capable of
spontaneous germination as long as some physical and
physiological conditions are fulfilled. Germ tube growth occurs
for 1 to 3 weeks (depending on the species of fungus) but
ceases long before consumption of spore reserves if a host
root is not present in the environment
Calais – SFR Condorcet – June 2018
From fungus to plant: never alone…
Pre-symbiotic phase Symbiotic phase
Plant root exudates stimulate fungal growth (branching) and nuclear division
(Buée et al. 2000, MPMI; Akiyama et al. 2005, Nature)
Reciprocal advantages: Glomeromycete fungi produce structures
called arbuscules within root cells to exchange nutrients.
Marc-André Selosse and François Rousset. Science 2011, 333: 828-829
Calais – SFR Condorcet – June 2018
This is an old story of love…
Major evolutionary advances in the cryptospore and plant
macrofossil record during pre-Carboniferous times (Gerrienne Transverse section of Aglaophyton
et al. 2016) major axis showing tissue preservation
and arbuscule-containing cells
The discovery of arbuscules in Aglaophyton major, an Early Devonian land
plant, provides unequivocal evidence that mycorrhizae were established
>400 million years ago. (Remy et al. 1994, PNAS)
Calais – SFR Condorcet – June 2018
This is an old story of love…
Domestication des plantes (10 000 – 6 000 9 700 av. J.-C)
et découverte des mycorhizes (XIX siècle ap. J.-C)
Modern agriculture must deal with© FM
a plant / microbes
coevolution over 400 millions years old
Calais – SFR Condorcet – June 2018
This is an old story of love…
Domestication des plantes (10 000 – 6 000 9 700 av. J.-C)
et découverte des mycorhizes (XIX siècle ap. J.-C)
© FM
Calais – SFR Condorcet – June 2018
Reciprocal advantages: exchange nutrients.
R. Finlay, SLU - Sweden http://www.wsl.ch/Im/publications
https://goodies.pcastuces.com
Calais – SFR Condorcet – June 2018
Ectomycorrhizal symbiosis: healthy and harmonious links thanks chimeric
organs called mycorrhizae (from myco & rhiza)
© FM
Calais – SFR Condorcet – June 2018
Potential utility of fungal inoculations in agricultural and forest
management
Douglas fir 1+1 inoculated: Control (non inoculated):
with Laccaria bicolor S238N Seedlings 1+1Calais – SFR Condorcet – June 2018
Inoculum of mycorrhizal fungi for production systems:
fungal strain conservation and production
Comparison of the controlled inoculation of Douglas fir with Laccaria bicolor
(S238N) which are submitted to the following two conditions:
i) Cryopreservation (liquid nitrogen) in 1993
ii) Alternation of successive subcultures and storages (4°C)
Strong reduction of the mycorrhizal effect (growth promoting effect)Calais – SFR Condorcet – June 2018
Inoculum of mycorrhizal fungi for production systems:
fungal strain conservation and production
i) Cryopreservation (liquid nitrogen)
ii) Alternating steps of subcultures and storages (4°C)
Mycorrhizal rate L. b. (%)
150,00
100,00 Lb 93-12
50,00
Lb 4C° L. b. (Cryopreservation)
T NI
L. b. (successive subcultures)
0,00
B1 B2 B3 B4 Control (without L. b.)
Height of the plant (cm) Total biomass (g)
12,00 4,00
10,00
3,00
8,00
93-12 Lb 10-93
6,00 2,00
4°C Lb 4C°
4,00
Témoin 1,00 T NI
2,00
0,00 0,00
B1 B2 B3 B4 B1 B2 B3 B4Calais – SFR Condorcet – June 2018
Never alone…
The ectomycorrhizal root tip hosts several bacteria
(ectomycorrhizosphere)
Frey-Klett and Garbaye, New Phytol
(2005)
roots
ectomycorrhiza
bacteria
soilCalais – SFR Condorcet – June 2018
Never alone…
Some bacteria stimulate the ectomycorrhizal symbiosis
L. bicolor S238N
Control
% of mycorrhizal roots
Treatment Nursery 1 Nursery 2 Nursery 3
Fungus alone 60 43 83
Fungus + 87 * 83 * 99 *
helper bacterium
Duponnois and Garbaye, Rev. Forest. Fr., 1992Calais – SFR Condorcet – June 2018
Pseudomonas fluorescens BBc6 – GFP biofilm
on the hypahe of Laccaria bicolor S238N
Deveau Aurélie, INRACalais – SFR Condorcet – June 2018
How helper bacteria interact with ECM fungi
and influence symbiosis ?Calais – SFR Condorcet – June 2018
An in vitro assay to analyse mutualistic interactions between L. bicolor and
Pseudomnas fluorescens BBc6R8
Bacterial colony
Fungal plug
Fungal matCalais – SFR Condorcet – June 2018
An in vitro assay to analyse mutualistic interactions between L. bicolor and
Pseudomnas fluorescens BBc6R8
Bacterial colony
Fungal plug
Fungal mat
6
pCalais – SFR Condorcet – June 2018
An in vitro assay to analyse mutualistic interactions between L. bicolor and
Pseudomnas fluorescens BBc6R8
Bacterial colony
Fungal plug
Fungal mat
6
pModel of the interaction between L. bicolor and P. fluorescens BBc6R8
1. P. fluorescens BBc6R8 is attracted by fungal exudates
2. The consumption of fungal exudates enhances bacterial survival
3. The bacterium produces metabolites that induce
the increase of fungal survival and growth in vitro and in tree nurseries
4. Some authors suggest that bacteria could produce eDNA filaments
trapping extracellular pathogens
P. fluorescens
1 BBc6R8
2
Fungal exudates +
L. bicolor S238N
Bacterial metabolites
Brûlé et al. (2003)
Deveau et al. (2007, 2010, 2014) 3
Cusano et al. (2010)
Zhang et al. 2015
Guennoc et al. 2018Calais – SFR Condorcet – June 2018
Biocontrol potential:
Mycorrhiza consortia suppress the fusarium root rot in common bean
Fusarium solani
Fusarium solani
Control + AMF2
Four AMF formulations have been tested: variable mixtures of AM fungi strains, Glomus intraradices (Gli),
Glomus hoi (Glh), Gigaspora margarita (Gim) and Scutellospora gigantea (Scg).
AMF1 treatment (with a mixture of Gli, Scg and Gim)
AMF2 treatment (with a mixture of Glh, Scg and Gim)
AMF3 treatment (with a mixture of Glh, Gli and Gim)
AMF4 treatment (with a mixture of Glh, Gli and Scg), Eke et al. 2016Calais – SFR Condorcet – June 2018
Biocontrol potential:
Arbuscular mycorrhizal fungi can Increase resistance to soil-borne pathogens
Modulation of plant defense signaling during mycorrhiza establishment. (i) Upon germination, AM
fungi grow toward the root and form appresoria at the root surface. At this stage, the plant reacts
with an increase in SA levels. (ii) In a compatible interaction, SA levels decrease as the fungus
colonizes the cortex. (iii) JA biosynthesis occurs in arbuscule containing cells.
Drawing by J. Perez-Tienda.
Eke et al. 2016Calais – SFR Condorcet – June 2018
An increasingly complex patchwork of microbesCalais – SFR Condorcet – June 2018
A single European aspen (Populus tremula) tree individual may
potentially harbour hundreds of species of ectomycorrhizal fungi
Bahram et al. 2010Calais – SFR Condorcet – June 2018
A single European aspen (Populus tremula) tree individual may
potentially harbour hundreds of species of ectomycorrhizal fungi
Rarefied species accumulation curve of EcMF (triangle) associated with a single aspen
tree, its 95% confidence intervals (dotted lines) and the minimum species richness
estimates: Chao 2 (open circle), Jacknife 2 (open square) and ICE (open triangle).
Bahram et al. 2010Why such diversity!?
Functional complementarity and redundancy
Peziza depressa (A1) Byssocorticium Tomentella
atrovirens (A1) lateritia (A1)
Buée et al. 2007Why such diversity!?
Functional complementarity and redundancy
Litière
Litière L. quietus
C. anomalus
Organo-
Organo-
Leucine
minéral
minéral 0,6
0,5
laccase Glucuronidase
0,4
0,3
0,2
0,1
Phosphatase 0 Xylosidase
Barre = 10 cm
ß-glucosidase Cellobiohydrolase
Chitinase
Cortinarius anomalus
Lactarius quietus
Courty et al. 2007Calais – SFR Condorcet – June 2018
An increasingly complex patchwork of microbes
within a large plant communityCalais – SFR Condorcet – June 2018
Mycorrhizal fungal networks & food web
Simard et al. 1997
Pickles et al. 2017Mycorrhizal fungal networks & food web
Neottia nidus-avis is an orchid with short roots
forming a kind of nest (a). Its roots are colonized by
different fungi (e.g. Sebacinales) which also form
mycorrhizae on the neighboring trees (b). Mycorrhizal
fungi links the orchid roots to the trees, allowing
carbon transfers
(b) Selosse & Roy (2012)
https://fr.wikipedia.org
(a)Calais – SFR Condorcet – June 2018
Socialism in soil? The importance of mycorrhizal fungal
networks for facilitation in natural ecosystems
The existence of these mycorrhizal networks
implies that fungi have the potential to
facilitate growth of other plants and
distribute resources among plants
irrespective of their size, status or identity.
Perspectives in agroforestry…
van der Heijden and Horton, 2009Calais – SFR Condorcet – June 2018
Positive interactions under nurse-plants
Plante nurse : vecteur de
propagation de champignons
mycorhiziens pour optimiser les
performances des opérations de
reboisement au Maroc (IRD /
Cirad). Exemple du caroubier et
de Retama sp.
Effect of soils sampled under Retama sp. (Right)
or from bareground - without plant – (Left) on
carob tree growth four months after sowing.
(Photo Manaut 2007)
Tewksbury & Lloyd 2001; Manaut et al. 2013Calais – SFR Condorcet – June 2018
Agroforestry systems for bridging truffle production and agronomy
Truffe + vigne (Vaucluse) Truffe + céréales (Indre et Loire)
La trufficulture peut être
réalisée en monoculture
ou bien en agroforesterie
à haute valeur ajoutée
Truffe + lavandin (Drôme) Truffe + jachère fleurie
mellifère (Drôme)Calais – SFR Condorcet – June 2018
Modern agriculture now feeds 6,000 million people (*).
Why do the root microbiota of plants should be
considered in the sustainable management of
forest and agricultural ecosystems?
Agricultural trends over the past 40 years.
a, Total global cereal production
b, total global use of nitrogen and phosphorus
fertilizer (except former USSR not included) and area
of global irrigated land
c, total global pesticide production and global
pesticide imports (summed across all countries).
(*)Tilman et al. 2002Calais – SFR Condorcet – June 2018
Why do the root microbiota of plants should be considered in the sustainable
management of forest and agricultural ecosystems?
Several studies have shown that common management practices such as P fertilizer applications
(Black and Tinker 1979; Lu et al. 1994) or intensive tillage (Kabir et al. 1997 Kabir 2005) may
have negative effects of varying degrees on AMF abundance.
Meta‐analyses of 290 published studies
=> effects of various agricultural practices on
mycorrhizal colonization in nonsterile soils,
and the consequence of those effects on yield
and biomass.
Mycorrhizal colonization was increased most
by inoculation (29% increase), followed by
shortened fallow (20%) and reduced soil
disturbance (7%). Increased colonization
resulted in a yield increase in the field of 23%
across all management practices.
Lekberg and Koide, 2005; Jansa et al., 2006Calais – SFR Condorcet – June 2018
Network visualization of the interaction strengths. Interaction strength between the species
subgroups (a) and main species groups (b) in seminatural grasslands on recently, mid-term and
long-term abandoned agricultural fields (the history of agricultural use was comparable).
Morriën et al. 2017FERTILIZERS PESTICIDES
Decreased mycorrhizal Decreased microbial
interaction availability
Lose of fungal partners (and microbial interactions)
Increased dependency Increased dependency
on fertilizers on pesticidesEcology studies the interactions among organisms and their environment. => Ecology in the interest of the agronomy http://www.agroforesterie.fr
Thank you for your attention!
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