Disease Suppression

by Mycorrhizal Fungi
 Contents
•Populations of Rhizosphere
•Disease Control by Ectomycorrhizal Fungi
•Disease Control of Soil Borne Pathogens by VAM Fungi
•Disease Control in Above Ground Parts of Plants by Mycorrhizal
Fungi

•Control of Plant Parasitic Nematodes by Mycorrhizal Fungi

•Strategies to Enhance Arbusular Fungal Efficacy in Disease
Control
•Conclusion
•References
2
 Mycorrhizal Colonization

Fig.1 Functions performed by Mycorrhizal Fungi 3

 Major Types of Mycorrhizae

Fig.2 Schematic showing the difference between ectomycorrhizae and endomycorrhizae

colonization of plant roots. © 2013 Nature Education Bonfante, P. & Genre, A. 4
 Mycorrhizae as Biological Control Agents

• provide an effective alternative method for disease

control
• have enormous potentials for use as BCAs for soil-
borne diseases,
• as root diseases are one of the most difficult targets to
manage, (Mukerji, 1999; Xavier & Boyetchko,
2002).

5
Mycorrhizae as Biological Control Agents

• The role of mycorrhizae in disease control is

better observed in arbuscular mycorrhizae than in
ectomycorrhizal associations.
• Disease reduction in host plants is the result and
output of a complex interaction between
mycorrhizal fungi, plants and pathogens (Harrier
and Watson, 2004).

6
 Populations Residing in Rhizosphere

Saprophytic Parasitic
Microbes Symbionts
population

• infect the root

system of plant
• Help in soil
species
formation • Root
• augment of soil • exhibit various
types of disease rhizobia
fertility and
• syndrome viz., • Root fungus
nutrient
transformation root rots, collar
rots, galls, 7
knots, wilts
Fig. 2: Different Populations Residing in Rhizosphere 8
 Provide a physical
barrier

Pro osphe
tor
al in on of

rhiz anism
org
hibi

tec
i

tive re
che roduct
mi c

s
P

Strategies of
Disease Control by
Ectomycorrhizal
Fungi
Se Me
c re t a b

tri ed
t in

Nu hanc
n
tio
g a olites
nt i

En
bio
t ic
s/

Ecological Fitness

9
 1. Provide a physical barrier

• Mantle acts a physical hindrance.

• A pathogen attacking an ectomycorrhizal root system
is initially confronted externally with (mantle), and
then internally with (Hartig’snet)

10
Fig.3 Tangential section of non-mycorrhizal root (A) and ectomycorrhiza (B) of Pinus echinata inoculated
with vegetative mycelium of Phytophthora cinnamomi. Note vesicles of pathogen on root surface and
abundant intracellular cortex infection in (A). Note vesicles on fungus mantle and absence of intracellular
cortex infection in (B) (Marx and Davey 1969).
11
 2.Protective rhizosphere organisms

Both mantle/matrix and Hartig’s net promote the formation of

favourable microbial populations in the soil around the
mycorrhizal roots (Schisler & Linderman, 1987).
Approximately 10 times as many as fungi in rhizosphere of
ectomycorrhizal pine seedling as in those of non-mycorrhizal
seedlings Tribunskaya (1955).

12
 Rhizosphere Soil Type Bacteria R/S Molds R/S Ratio1
Ratio1
 
Millions2   Thousands  
2

Douglas fir mycorrhizal 91.6 3.3 347.3 2.0

root
Douglas fir 28 - 175 -
Non-rhizosphere soil
Red alder mycorrhizal root 580 16.6 455.9 2.3
Red alder non-rhizosphere 35.0 - - 200.0
soil

Table.1 Comparison of Microbial Population in Rhizosphere and Non-Rhizosphere Soil (Nael et

al.,1964)
1.Rhizosphere/nonrhizosphere soil ratio.
2. Counts per gram of soil, oven dry basis. Each value represents a mean of three replicate samples.
13
 Protective rhizosphere organisms
Ectomycorrhizal roots of yellow birch:
•increased the numbers of certain soil bacteria and actinomycetes
•Reduced total numbers of pathogenic fungi around ectomycorrhizae.
•Complete absence of Phythium and Fusarium (Katznelson et al., 1962)
Another study found strong inhibition of
•bacteria, especially aerobic and heterotrophic types
•actinomycetes around actively growing mycelium of Tricholoma matsutake
in forest soils on Pinus densiflora (Ohara and Hamada ,1967)

14
 3. Enhanced Nutrition

• Proper nutrition provides endurance against pathogens.

• greater efficiency in nutrient and water uptake (Gerdemann
1968; Thakur and Sharma 2013).
• Hyphae can readily bridge the depletion zone (Ali
asgharzad et al. 2009, Bagheri et al. 2012; Fattah 2013).
• EM have a special role in the mineralization of nitrogen.
•Symbiotic associations increase the production of plant
growth hormones

15
Fig.4 The inset labeled (a) in the diagram to the right illustrates enzyme-
facilitated nutrient acquisition by the fungus. The inset labeled (b) shows how
the fungi use acid to help break down rocky substrates and access their
nutrients.  (Landeweert et al. 2001). 16
 4.Ecological Fitness

•Abiotic stresses predispose the host for its vulnerability to disease infection.
•pest problems are more in nutrient-poor or moisture-deficient soils.
Mycorrhizal plants are often more competitive and
• better able to tolerate environmental stresses than the non-mycorrhizal
plants.
•tree seedlings without mycorrhizae fail to grow in soils low in nutrients but
establish successfully if inoculated with suitable mycorrhizal fungi (Harley
1959).
•ecto-mycorrhizal plants use ammonium (Bledsoe and Rygiewicz 1986).
17
 Ecological Fitness

• Large surface provided by hyphae and hyphal strands enables

sufficient take up rather immobile ammonium.

•Mycorrhizal roots of seedlings of fir (Abies pindrow), spruce

(Picea smithiana) and chilgoza pine ( Pinus gerardiana) showed
tolerance to stress than non mycorrhizal seedlings (Lakhanpal
and Sharma 1988).

•Different species of mycorrhizal fungi have been found to

exhibit varying degree of drought tolerance under conditions of
moisture stress (Trappe 1962). 18
 5. Secreting antibiotics/metabolites

•Several Mycorrhizal fungi produce different types of antibiotics

/metabolites (anti-fungal, Anti-viral and Antibacterial)
•Amanita, Boletinus spp.,
• Cenococcum spp.,
•Lactarius spp.,
• Laccaria laccata,
• Leucopaxillus cerealis var Piceina,
• Pisolithus tinctorius,
•Suillus luteus and
•Thelephora terrestris
19
 Secreting antibiotics/metabolites

Leucopaxillus cerealis var.

piceina

Diatretyne Diatretyne
Diatretyne – 3
nitrile amine

Inhibit

Phytophthora (9 Rhizoctonia (5 Pythium (24 spp)

spp.) spp.) 20
 6. Production of Chemical Inhibitors

Plant cells release inhibitory substances during their metabolic

response to pathogenic attack

 Symbiotic associations enhance the concentration of these

inhibitors many times greater than non symbiotic roots.

Pine (Pinus sylvestris) seedlings with symbiotic association

produce eight times higher concentration of fungistatic
compounds like terpenes and sesquiterpenes (Krupa and Fries
1971). Similar compounds have been also reported in certain
ectomycorrhizal fungi like Amanita and Rhizopogon.
21
 Production of Chemical Inhibitors

 Several mycorrhizal fungi like Amanita rubescans, Boletus variegatus, Pisolithus tinctorius Hebeloma
produce various volatile organic compounds like

• ethanol,

• isobutanol,

• isoamylalcohol,

• acetoin

• isobutyric acid

 These compounds are inhibitory to many pathogenic fungi some of which are:

• Phytophthora cinnamomi,

• Rhizoctonia undulata,

• Phymatotrichum omnivorum,

• Fomes annosus
22
• and Pastalotia rhododendry etc.
Strategies of Disease Control Against Soil
Borne Pathogens by Vesicular Arbuscular
Mycorrhizal (VAM) Fungi

23
 Control of Soil Born Pathogens by VAM
Fungi
•AM fungi can reduce disease incidence and propagule number of several
soil-borne pathogens like Aphanomyces, Fusarium, Rhizoctonia,
Phytophthora, Pythiumand Verticillium(Caron et al., 1986; Liu, 1995;
Mcallister et al.,1994; Vigo et al., 2000; Norman & Hoorker, 2000; Demir &
Akkopru, 2007; Utkhede, 2006; Singh et al., 2000, Sharma et al., 2004; 2007).

•Different mechanisms are possibly involved in the development of an

effective bio protection, acting separately and/or together (Harrier & Watson,
2004).  

24
Fig. 5 Strategies of Disease Control Against Soil Borne Pathogens by Vesicular Arbuscular Mycorrhizal (VAM) Fungi
25
 1.Enhanced Plant Nutrition

Fig. 6 Phosphorus acquisition efficiency related traits of wheat and barley roots affected by arbuscular mycorrhizal symbiosis in
comparison to a non-colonized counterpart. (A) Representation of P depletion zone around the rhizosphere; (B) Access to smaller soil
pores by AM fungal hyphae; and (C) Modulation of plant P transporters following colonization. (Adapted from Pedro M. de Souza

Campos et al., 2018) 26

 Enhanced Plant Nutrition

Plants that took up larger amounts

of nutrients through their AM
fungal symbionts (e.g.
Glomusintra radices and Glomus
mosseae) have an increased
tolerance for pathogenic
infections (e.g. Bodker et al.1998;
Karagiannidis et al. 2002).
Fig. 7: Effect of inoculation with arbuscular mycorrhizal fungi on
phosphorus uptake in banana plantlets at potting phase (22 weeks after
27
inoculation). Average across nine banana cultivars in a pot experiment.
 Enhanced Plant Nutrition

• In other studies not involving the AM symbiosis, increased

nutrient uptake did not result in improved pathogen tolerance
(Shaul et al.1999; Fritz et al.2006).
• Taxonomic variation within the AM fungal phylum
Glomeromycota, both in terms of nutrient responses
• Members of the Gigasporaceae enhanced nutrient uptake to a
larger extent than those of the Glomeraceae, the latter reduced
pathogen abundance in roots to a greater extent (Maherali and
Klironomos, 2007)
28
 2.Competition for Host Photosynthates

Following root entry,

competition can occur for
 infection sites,
 host photosynthates, and
 root space (Smith and
Read,1997).
Fig. 8 Phytophthora species and arbuscular
mycorrhizal fungi follow analogous steps to
establish a root interaction. Source: PebMed
29
 Competition for Host Photosynthates
 Competition between AMF and pathogens can be used for physical exclusion
of pathogen (Davis and Menge 1980; Hussey and Roncadori, 1982; Smith,
1988), if the host is pre-inoculated with AMF.

 Simultaneous colonization of AMF and the pathogen may not provide a

competitive edge for AMF for inoculum build-up (Daniels and Menge,
1980)

In contrast, some others have noted that competition may not occur between
AMF and other organisms (Sempavalan et al. 1995).

Increasing the richness of AM fungal taxa colonizing the root system may
result in more intense competition with a pathogenic fungus.
30
 3.Root Damage Compensation

AM fungi increase host tolerance of pathogen attack by

compensating for the loss of root biomass or function caused by
pathogens (Linderman, 1994), including nematodes (Pinochet et
al., 1996) and fungi (Cordier et al., 1996).
This represents an indirect contribution to bio control through the
conservation of root-system function, both by
•fungal hyphae growing out into the soil and
• increasing the absorbing surface of the roots
• and by the maintenance of root cell activity through arbuscule
formation (Cordier et al., 1996).
31
 4. Morphological Changes in Host Plant Root

AM fungal colonization
influences root architecture of
the host plant in most studies
by causing a more profusely
branched root system (Price et
al., 1989; Paszkowski et al.
2002; Olah et al. 2005; Gutjahr et al. Fig. 9 Root volume and morphology of

2009). different rootstoks inoculated with different

AMF species, 21 weeks after inoculation
(Source: Aram and Ali, 2015)
32
 Morphological Changes in Host Plant Root
Eggplants colonized by Gigaspora margarita contained
higher lignin concentrations in first order and second order
roots compared to non-mycorrhizal plants, when Verticillium
dahliae was present (Matsubara et al.,1995)
G. mosseae decreased the root branching of tomato under
high P conditions if a plant was attacked by Phytophthora
nicotianae (Trotta et al., 1996).

33
 Morphological Changes in Host Plant Root

Table. 2: Length and necrosis of AMF-colonized

(+AMF) and non-colonized (–AMF) tomato roots
Fig. 10: Effects of colonization by AMF on root system following inoculation with zoospores of
architecture of tomato (a) 20 days (b) 26 days (c) 34 days 34
following sowing. Phytophthora parasitica (Vigo et al., 2000)
 5. Changes in Microbial Community of
Mycorrhizosphere

• Mycorrhizae alter the physiology and/or morphology of root and

plants in general, leading to altered root exudation (Bansal &
Mukerji, 1994).
• Changes in root exudates cause microbial shifts in the
mycorrhizosphere.
• Changes in soil microorganism populations induced by AM
formation may lead to stimulation of certain components of the
microbiota, which in turn may be antagonistic to root pathogens.

35
Fig. 11 Schematic view of the interactions among different components of the mycorrhizosphere. Effects of AM fungi on bacteria: energy supply (1), pH changes(2),competition for nutrients (3), release of inhibitory or
stimulatory compounds (4), root growth stimulation (5), changes in root exudates (6) and effects on soil structure (7). Effects on endophytes or soil pathogens: growth of AM endobacteria (8) and effects on pathogenic fungi.
Further interactions include the effects of mycorrhizosphere bacteria on roots AM receptivity (10), fungal growth (11), propagules germination (12) and soil chemistry (13) (adapted from Johansson et al., 2004)

36
Reduction in number of sporangia and zoospores formed by
cultures of Phytophthora cinnamomi application of extracts
of rhizosphere soil from AM plants (Meyer and
Linderman,1986)

AM fungi and PGPR may cooperate in several ways,

including biological control of root pathogens (Barea et al.,
1996).

37
• PGPR do this mainly by
the production of
antibiotics, hormones,
siderophores and HCN,
and by competition for
colonization sites and
carbon compounds
(Kloepper 1992; Leeman
et al., 1995).

38
Fig. 12 Mechanism of plant growth promotion by rhizobacteria
 6. Physiological Changes in Host
Enhanced P levels modify the phospholipid composition
therefore the root membrane permeability resulting in a
reduction in the leakage of net amount of sugars, carboxylic
acids, and aminoacids into the rhizosphere (Graham and Menge,
1982; Ratnayake et al., 1978; Schwab et al., 1983).
These alterations arrest the chemotactic effect of pathogens to
plant roots and discourage pathogen entry.

39
 Physiological Changes in Host

Prior inoculation of maize plants with G. mosseae decreased

the number of Alternaria alternate colony forming units,

On inoculating both organisms at the same time, there was

no effect on pathogen inoculum density in soil (McAllister et
al. 1996).

40
 7. Phenolics
Cell-wall-bound phenolics strengthen the cell wall and prevent
invasion by pathogens (Graham and Graham, 1991).
level of total soluble plant phenolics increases as synthesis of
phytoalexins following AMF colonization of roots (Morandi
1989; 1996).
Tomato plants inoculated with G. mosseae posed greater
resistance to the pathogen Fusarium oxysporum
Had increased phenylalanine and b-glucosidase activity and total
phenol content in their roots (Dehne and Schonbeck 1979).
41
Table.3 Occurrence of phytoalexin and phenolic
compounds in mycorrhizal compared to non-
mycorrhizal roots of studies 42
 8. Hydrolases

Differential expression of defense-related genes in

mycorrhizal plants has been the recent focus of AMF
mediated bio-control (Blee and Anderson, 1996; Pozo et al.,
2002).
Entery of AMF into host (e.g., tomato) roots induces a local
and transient activation of the host defense mechanism
induction of hydrolytic enzymes such as chitinase,
chitosanase, b-glucanase, and superoxide dismutase (Pozo et
al. 2002). 43
 Hydrolases

portions of the mycorrhizal root system not containing

mycorrhizal structures appear to have alterations in the
constitutive isoforms of the A high positive correlation
enzymes indicating systemic changes following AMF
colonization (Pozo et al.,2002).

between the level of glucanase activity in host tissues and

pathogen resistance has been established (Graham and
Graham 1991).
44
 9. Activation of Host Plant Defense

DuringMechanisms
mycorrhiza formation, modulation of plant defense responses
occurs,
Through cross-talk between salicylic acid and jasmonate dependent
signaling pathways.
It impacts plant responses to potential enemies by priming the tissues
for a more efficient activation of defense mechanisms.
Salicylic acid (SA) co-ordinates defense mechanisms that are
generally effective against biotrophic pathogens,
Jasmonates (JA) regulate wounding responses and resistance against 45

necrotrophs
 Activation of Host Plant Mechanisms

Fig.13 Model for hormonal changes in the roots associated to the arbuscular
mycorrhizal symbiosis. In the early phase of colonization strigolactone (SL)
production is still high. Initially the AMF is perceived as an alien organism and as
a consequence salicylic acid (SA) levels increased. In a well-established 46

mycorrhiza both SL and SA production are repressed while biosynthesis of

Fig.14  Trichoderma harzianum induces systemic protection against the pathogen Botrytis
cinerea in tomato plants. (A) Leaves of 5 weeks-old tomato plants (cv. Castlemart and
Moneymaker) grown in soil containing or not T. harzianum were challenged with a conidial
suspension of B. cinerea. Lesion diameter was determined 96 h after pathogen inoculation. The
data show the lesion diameter (mm) ±SE (n = 12). Data not sharing a letter in common differ
significantly (P < according to Tukey’s multiple-range test. (B) B. cinerea symptom development
in T. harzianuminoculated and non-inoculated (control) plants (cv. Moneymaker). Ainhoa Martinez-
47
Medina et al., 2013
 10. Antibiosis
Production of antimicrobial substances by AMF are not common.
recently, it was shown that antimicrobial substances (unidentified)
produced by the extraradical mycelium of the AMF species G.
intraradices reduced conidial germination of F. oxysporum f. sp.
chrysanthemi, (Filion et al., 1999).
 Budi et al. (1999) isolated a Paenibacillus sp. strain from the
mycorrhizosphere of Sorghum bicolor plants inoculated with G.
mosseae that exhibited significant antagonism against P.
parasitica..
48
 Disease Control in Above Ground Parts of Plants by
Mycorrhizal
Evidences have Fungi
come which show suppression of leaf attacking
pathogens also.
 Mycorrhizal tomato plants had significantly less symptoms of leaf
spots due to Alternaria solani than in non-mycorrhizal plants.
Both AM and rhizobacteria being root-associated organisms are
together effective against necrotrophic pathogens (Fritz et al., 2006).
Diseases were suppressed in arbuscular mycorrhizal plants (Mukerji
et al., 1997), with more spores found around roots of healthy plants
than around roots of diseased plants (Table 1).
49
Table 4. Number of AMF spores in the roots of diseased and
50
healthy plants (Zaidi & Mukerji, 1983).
 Control of Plant Parasitic Nematodes by
Mycorrhizal Fungi

AMF can also suppress PPN (Pinochet et al., 1996) and Hol
and Cook (2005).
Protective effects against PPN by AMF in plants such as
banana, coffee and tomato (Calvet et al., 2001; Vos et al.,
2012b; Alban et al., 2013; Koffi et al., 2013).
These protective effects ranged from
 a reduction in infection and
 reproduction to an enhanced tolerance.
51
 Control of PPN by VAM Fungi

Fig. 15 Overview of the possible mechanisms by which arbuscular mycorrhizal fungi

can exert bio-control against plant-parasitic nematodes. Source: Front Microbiol. 201552
Fig. 16 Visualization of the experimental set-up of a twin-chamber
with tomato plants used by Dababat and Sikora (2007) and Vos et al.,
(2012b) to study the differential attraction of Meloidogyne incognita
53
to mycorrhizal roots.
Fig. 17 In vitro chemo taxis bio-assay with visualization of nematode tracks on the medium. Pictures were taken 1 h after inoculation with 10
female Radopholus similis nematodes in the middle of the plate. Three hours before nematode inoculation, the opposite wells in the agar
medium were filled with (A) water as control, (B) 1% acetic acid (left hole) versus 0,5M CaCl2 (right hole) as repellent and attractive control,
or (C) exudates of non-mycorrhizal roots (left) versus exudates of mycorrhizal roots (right) to observe chemotactic behavior of the nematode.
Lower nematode movement can be observed in the plate with mycorrhizal root exudates, and the nematodes clearly show a chemotactic
response away from them. Vos et al. (2012c).
54
Strategies to Enhance Arbusular Fungal
Efficacy in Disease Control

Improved Understanding of Microbial (AMF) Ecology and

Ecosystem Functioning

Enhanced AMF Biodiversity

Selection of Effective AMF

Superior Application Technology

55
 Conclusion
Literature presents a wealth of evidence to indicate potential for
AMF-mediated control of plant diseases. Therefore use of
mycorrhizal fungi provides an effective alternative method of disease
control particularly in soil or root-borne diseases. In the biological
control of diseases with the help of mycorrhizae, the results being
host mediated, provide some hope that in future mycorrhizal fungal
technology could be used as a potential bio-control agent.
Mycorrhizae are also promising and effective agents against leaf-
borne pathogens and sedentary plant parasitic nematodes.
56
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Thank you!!!!
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