Content uploaded by Nourhan Naga
Author content
All content in this area was uploaded by Nourhan Naga on Apr 05, 2023
Content may be subject to copyright.
375
Symbiotic Relationships withFungi:
FromMutualism toParasitism
MohammadMagdyEl-Metwally, AmalAhmedIbrahimMekawey,
YasserEl-Halmouch, andNourhanGaberNaga
1 Introduction
Fungi are a dynamic population with a great impact in the plant, animal, and human
body. In the case of a plant, they are associated to the whole plant especially roots
and rhizospheres with remarked effect on the tness and productivity of the plant
(Vicente etal. 2013; Vandenkoornhuyse etal. 2015).
This collection of fungi is termed mycobiome “a characteristic fungal commu-
nity inhibiting a generally well-dened habitat which has distinct physical and
chemical properties” (Dridi etal. 2011; Mendes etal. 2011). The combination of the
plant and its mycobiome leads to environmental adaptation in plants which is essen-
tial for maintaining the function of terrestrial ecosystems (Chialva et al. 2018;
Cavicchioli etal. 2019). Soil mycobiome have many effects on plant growth and
development and inhibition of plant diseases by imposing physiological restrictions
on pathogens establishing and infecting plant tissues (Kumar etal. 2012). They give
the rhizosphere system some resistance to invaders (Van Elsas etal. 2012). They
also provide nutrients, which play a crucial role in some processes such as
M. M. El-Metwally (*)
Faculty of Science, Botany and Microbiology Department, Damanhour University,
Damanhour, Egypt
A. A. I. Mekawey
Regional Center of Mycology and Biotechnology, Al Azhar University, Nasr City, Egypt
Y. El-Halmouch
Faculty of Science, Botany and Microbiology Department, Kfrelsheikh University,
Kafr El Sheikh, Egypt
Faculty of Sciences and Technology, Nantes University, Nantes, France
N. G. Naga
Faculty of Science, Botany and Microbiology Department, Alexandria University,
Alexandria, Egypt
© The Author(s), under exclusive license to Springer Nature
Switzerland AG 2023
Y. M. Rashad etal. (eds.), Plant Mycobiome,
https://doi.org/10.1007/978-3-031-28307-9_15
376
phosphorus solubilization and nitrogen xation. These processes support the nutri-
ents uptake from the soil and promote plant protection by hindering agents of plant
stresses, such as infection by pathogens and pests (Mendes etal. 2013; Quecine
etal. 2014). All living microorganisms; microbiota live associated with each other
or with other organisms in different types of relationships like synergism, amensal-
ism, antagonism, parasitism, predation, and competition (Fig.1).
In general, these types are divided into two large groups according to the degree
of benet and harm of the two partners of the relationship. Positive interactions such
as commensalism or mutualism or synergism among microbial members are more
prevalent. They can signicantly affect the productivity of the bioprocess in indus-
trial production (Hernandez etal. 2019). Contrary to that, the negative interactions
exclude one organism from the community structure, such as parasitism, predation,
or amensalism (Ghosh etal. 2016). In an asymmetric contact called amensalism,
one species suffers harm or even dies while the other is untouched (Willey
etal. 2011).
Fig. 1 The six different types of symbiotic relationships between the species. The dark black
arrow mentions the direction of benefaction. Interrupted arrow mentions the harmful direction
M. M. El-Metwally etal.
377
2 Mutualism inPlant Fungi Symbiosis
The sassily of plants derived it to make multitrophic interactions with other
organisms, mainly microorganisms, which are diversely localized and have
remarkable functional lifestyles. Mutualism implies ‘relative benets’ in associa-
tions involving two or more different organisms. Mutualism is an obligatory or
highly specic interaction between two populations in which both of them benet
from each other. It usually required a close physical connection in which both part-
ners may act as if they are one. When they exist separately, the physical tolerance
and metabolic activities will be different for every single symbiont (Leung and
Poulin 2008).
Mutualisms are everywhere in the biosphere and are fundamentally important in
evolution and ecology (Bronstein 2015). The fungal plant mutualism is benecial to
host plants by conferring tness benets on hosts. It promotes plant growth and
production (Yuan etal. 2019), improves resistance to herbivores e.g. insects (Estrada
etal. 2013), enhances tolerance to biotic stress (Khare etal. 2018). It also increases
the accumulation of useful secondary metabolites (Gupta and Chaturvedi 2019;
Yuan et al. 2019) and confers tolerance to abiotic stress (Sabra et al. 2018).
Mutualism includes plant-symbiotic nitrogen xation, plant–Mycorrhizae and
plant–endophyte associations. The rst two associations have been discussed in
other parts in this edition so we add some light in plant endophytes association.
Summary of mutulism types (Selim and Zayed 2017)
Mutualism according to the partner’s selection
(1) Obligatory (2) Facultative
when both microorganisms live together in
close proximity, and each of them cannot
survive without its mutualistic partner
when one of the two partners can survive
without its mutualistic partner by itself in some
conditions
Mutualism according to interaction purposes
(1) Trophic mutualism: (2) Defensive mutualism:
it is also called resource–resource interactions.
It is a type of mutualistic association, which
comprises the exchange of nutrients between
two species
it is also called service–resource relationships.
It appears when one organism provides shelter
or protection from predators or pathogens,
while the other provides food
(3) Service–service mutualism: it appears when one species receives service from its partner in
return for transporting another service to the other organism
2.1 Plant–Endophyte Association
Endophytic fungi are obligate mutualists in plants and they introduce essential ther-
motolerance to the symbiosis (Redman etal. 2002). Endophytes have been identi-
ed in growing plants in all types of environments and represent a large taxonomic
diversity of fungi. This suggests the convergent and redundant appearance of endo-
phytism in different times and spaces during the co-evolution of plants and fungi.
Symbiotic Relationships withFungi: FromMutualism toParasitism
378
Plant-mycoendophyte interactions are symbiotic. This symbiotic relationships are
ranging from mutualism through commensalism to parasitism (Rodriguez and
Redman 2008; Aly etal. 2011). Actually, endophytes can shift their lifestyle, being
latent saprotrophs, pathogens, temporary residents, mutualists, or commensals
(Suryanarayanan 2013). Some endophytes can survive as decomposers on leaves
after the death of plant tissues, suggesting that mutualism could derive from sapro-
phytism (Suryanarayanan 2013).
Host and mycoendophyte specic factors as well as external environmental fac-
tors play signicant roles in shaping plant-mycoendophyte interactions. Such as
host and fungal species (Jia etal. 2016; Fesel and Zuccaro 2016; Wang etal. 2019),
growth and plant age (Jia etal. 2016), communication pattern (Fesel and Zuccaro
2016), and physiological stress (Rodriguez and Redman 2008). External factors
such as light conditions and other abiotic stressors (Bacon etal. 2008; Alvarez-
Loayza etal. 2011). In plant, mycoendophyte phytohormones form a part of the
host’s released metabolites which function as signal molecules that facilitate
host- endophyte crosstalk and in turn determine the success of endophyte interac-
tions and colonization (Lubna etal. 2018; Xu etal. 2018). Many genera of fungi are
endophytes such as Trichoderma spp., Epicoccum spp., Penicillium spp., Alternaria
spp., Cladosporium spp., Fusarium spp., Chaetomium spp., Cladosporium spp.,
Aspergillus spp., Curvularia spp., Gilmaniella spp., Arthrobotrys spp., Acremonium
spp., Colletotrichum spp., Fusarium spp., Saccharomyces spp., Beauveria spp., and
paecilomyces spp. (Zakaria etal. 2010; Oldroyd etal. 2011; Paul etal. 2012; Fávaro
etal. 2012; Ek-Ramos etal. 2013; Sharma etal. 2019). One endophyte fungal spe-
cies may be associated with many plant species, and vice versa many species of
endophytes may be present in the same species (Rana etal. 2019).
Some fungal endophytes as A. niger CSR3, Phoma glomerata LWL2, and
Penicillium sp. LWL3, have been reported to produce and degrade phytohormones
like auxin, cytokinins, and gibberellins. They enable them to manipulate host
defense responses to infection and facilitate the successful interaction and coloniza-
tion (Lubna etal. 2018). Furthermore, a signicant number of miRNAs induced in
the host during endophyte infection and colonization target hormone-response path-
ways (Formey etal. 2014). Strigolactones are phytohormones which are known to
be involved in plant-microorganism interactions in the rhizosphere (Xie etal. 2010).
Experimental reports have shown that strigolactones have a role in mediating and
shaping plant-fungi interactions including mycoendophytes (Foo etal. 2013).
3 Commensalism inPlant Fungi Symbiosis
The commensal relationship is often between a larger host (unaffected) and a
smaller commensal. In this relation, commensals may obtain nutrients, support,
shelter, or locomotion from the host species. For success, the commensal species
may show great morphological adaptation. This relationship can be contrasted with
mutualism, in which both species benet (Alvarez-Loayza et al. 2011).
M. M. El-Metwally etal.
379
In Plant–fungal interaction commensalism is the undisturbed existence of fungus
inside the plant tissue without affecting the host. It neither provides any benet or
support to plant growth in the form of nutrients or secondary metabolites nor causes
any disease (Ko and Helariutta 2017). But this relationship can affect the plant
immune responses. For example, commensal root microbiota members triggered an
immune response in distant shoot organs and modulate resistance against a wide
range of microbial pathogens and herbivores (Berendsen etal. 2018; Chialva etal.
2020). These responses include commensal-triggered induced systemic resistance
(ISR) and pathogen-triggered systemic acquired resistance (SAR). Some recent evi-
dences indicated that the accumulation of azelaic acid SAR component (AzA) in
tomato leaves occurred in response to rhizosphere microbial commensals (Chialva
etal. 2020). Additionally, there are 116 metabolites in distant shoot organs were
modulated by the local rhizosphere microbiome. In contrast to SAR, initiation of
ISR by benecial root-colonizing microbes primes aboveground plant parts for an
accelerated defense response upon pathogen or insect attack. This phenomenon has
been extensively described by Pseudomonas simiae root colonization of A. thaliana
via transcription factor MYB72, which also regulates the secretion of coumarins in
the rhizosphere. These coumarins have a role in selecting benecial over non-
benecial ISR and has a function in growth-promoting strains exist in the rhizo-
sphere as it acts in concert with the root microbiota to improve iron nutrition (Ota
etal. 2020). Although experimental evidence is lacking, coumarins might also travel
from root to shoot and might contribute to the onset of ISR (Harbort etal. 2020).
Soil conditioning by plant residence time, plant species and mutants, or plant
pathogen pressure resulted in host-induced shifts in rhizosphere microbial commu-
nity composition that are directly linked with the plant’s ability to resist aboveg-
round pests and pathogens. This made the belowground microbial community
composition and aboveground systemic immune outputs more tightly connected
(Pineda etal. 2020). Commensal root microbiota members alleviate plant growth
deciency induced by aboveground changes in temperature or light conditions. It
might inuence the energetic status of aboveground shoot organs, thereby driving
investment into growth when aboveground environmental conditions are subopti-
mal. Systemic defense responses in leaves are induced also by root microbiota
members (Hou etal. 2020).
Prioritization of microbiota-induced growth in the context of aboveground abi-
otic stresses is associated with the down-regulation of microbiota-induced defense
responses. Examples supporting this hypothesis in A. thaliana indicated that: (1)
priority to shade avoidance responses occur at the expense of defense, (2) light and
phytochrome photo perception mechanisms induced by SAR, and (3) root
microbiota- induced growth under suboptimal light coincides with transcriptional
repression of systemic leaf immune responses and increased susceptibility to micro-
bial leaf pathogens (Liu etal. 2020).
Plant commensal microbes have evolved a variety of strategies to interfere with
or bypass microbial-triggered immunity (MTI) to establish symbiosis (Teixeira
etal. 2021). In nature, plants are colonized by different types of microorganisms
from their habitats, including commensal microbes and pathogens (Fitzpatrick etal.
Symbiotic Relationships withFungi: FromMutualism toParasitism
380
2020). The innate immune system of plants suppresses the invasion of pathogenic
microbes. The defense is based on a series of immune responses, such as fungal
chitin, peptidoglycan, agellin 22 (g22), and elongation factor Tu (EF-Tu) (Boller
and Felix 2009). Moreover, symbiotic microbial communities promote mutualism
by suppressing immunity (Buscaill and van der Hoorn 2021). Studies on plants have
so far focused on single microorganisms, and the specic immunomodulatory
effects of different strains have not been integrated into the context of complex
communities.
On the other hand, aboveground biotic and abiotic stresses can modulate root
microbiota assembly, and conversely, root commensals can promote host tolerance
to biotic and abiotic stresses. It remains difcult to experimentally test whether
these two responses are part of a microbiota-root-shoot circuit that promotes stress
resistance in plants. Biotic stresses such as leaf pathogen inoculation can trigger
selective host recruitment of benecial root commensals that modulate aboveg-
round pathogen growth through commensal-induced modulation of the host immune
system. Benecial root commensals were selectively stimulated through the com-
bined action of commensal-mediated pathogen growth suppression and commensal-
induced immune system modulation. Disease-induced re-assembly of benecial
root commensals is not limited to infection by microbial pathogens but has been
also reported during herbivory. For example, compositional shifts in the root micro-
biome of maize mutants decient in benzoxazinoids were correlated with changes
in plant defense, growth, and herbivore resistance of the next plant generation (Liu
et al. 2020). Complementation experiments with the benzoxazinoid; breakdown
product of 6-methoxy-benzoxazolin-2-one (MBOA) indicated that MBOA induced
the shift of rhizosphere microbiota, rather than MBOA itself (Hu et al. 2018).
Therefore, modulation of benzoxazinoids exudation in the rst generation and con-
ditioning of the rhizosphere microbiota is the key to orchestrating leaf defense
responses and suppression of herbivore growth in the second plant generation.
These data suggest a general model in which recognition of aboveground pests in
leaves can signal along the shoot–root axis to modulate rhizosphere microbiota
assembly, thereby leaving a microbial footprint in soil that promotes offspring health.
4 Parasitism inPlant Fungi Symbiosis
An interactive association known as parasitism occurs when two biologically and
phylogenetically distinct species coexist for an extended length of time. In this kind
of interaction, the “host” suffers while the “parasite,” which typically benets does
not. The ability of an organism to cause a disease or pathogenicity is connected with
parasitism. Many recent data suggest that oomycetes evolved plant parasitism sev-
eral times and independently of other eukaryotic pathogens (Meng et al. 2009;
Thines 2014).
In general, in the parasitism relationship at least one (the pathogen) benets.
There are some other cases; both host and pathogen alternate the benets.
M. M. El-Metwally etal.
381
For instance, bacterial nodules in the roots of legume plants and the mycorrhizal
infection of feeder roots of most owering plants. Both biotic and abiotic agents
have an impact on a number of crucial physiological and metabolic processes in the
host that are involved. For example, growth including the production of chlorophyll,
photosynthesis, transpiration, cell wall metabolism, the balance of growth regula-
tors, seed germination, and nutrient uptake (Rizwan etal. 2016; Pandey etal. 2017;
Cohen and Leach 2019; Ganie and Ahammed 2021). In many instances, parasitism
is closely linked to pathogenicity, i.e., the ability of a pathogen to cause disease.
The amount of damage occurred to plants is often much greater than would be
expected. This damage is caused by substances released by the parasite or made by
the host in response to parasite resistance. In many plant-pathogen interactions, an
arsenal of chemicals known as effectors is released by pathogens to aid in infection
(Oliva et al. 2010). These effectors modify plant physiology to suppress plant
defense responses. These effectors either exist in the interaction zone between the
fungal hyphae and the host surface or are transferred inside the plant cells (Lo Presti
etal. 2015). Some of these effectors are recognized directly or indirectly by resis-
tance (R) proteins from the plant and then modulate the innate immunity of the
plant. These R proteins are called avirulence (Avr) proteins. The presence of the ‘R’
gene and the corresponding ‘Avr’ gene leads to the recognition of the pathogen by
the host cell which activates resistance against the pathogen (Patel et al. 2020).
These proteins trigger a set of immune responses termed Effector-Triggered
Immunity (ETI), which frequently lead to a rapid hypersensitive response (HR).
Certain genetic changes such as complete deletion, inactivation, or down-regulation
of the AVR gene, as well as point mutations, allow the recognition between the
pathogen and plant cell to be evaded (Guttman etal. 2014).
Avr genes which are recognized by several R genes were reported in the patho-
systems: Leptosphaeria maculans/oilseed rape (Rouxel and Balesdent 2017),
Magnaporthe oryzae/rice (Kanzaki etal. 2012; Cesari etal. 2013), Fusarium oxys-
porum. lycopersici/tomato (Houterman etal. 2008; Houterman etal. 2009) and both
the fungal pathogen Cladosporium fulvum and the nematode Globodera rostochien-
sis/tomato. R protein recognized Avr proteins as they render the pathogen avirulent
on plants that carry the suitable receptor (Lozano-Torres etal. 2012).
4.1 Hyperparasitism
It is a phenomenon that occurs when pathogens are attacked and killed by a biocon-
trol agent. There are four categories of hyperparasites: obligate bacterial pathogens,
mycoviruses as hypovirulence factors, facultative parasites, and predators.
According to a study carried out by Latz etal. 2016 Actinomyces, Pseudomonas,
and Bacillus rhizosphere bacteria were responsible for Rhizoctonia solani suppres-
sion in potato plants. Endophytic bacteria stimulate plant growth due to their good
properties such as nitrogen xation (Ladha and Reddy 2003), and synthesis of plant
hormones such as IAA (Bal et al. 2013). Also, they play a role in phosphate
Symbiotic Relationships withFungi: FromMutualism toParasitism
382
solubilization (Prakash 2011), inhibition of plant diseases (Sayyed etal. 2013), and
production of some secondary substances such as siderophore. Recent work by (Do
2022) reported that strains of rice root endophytic bacteria; Bacillus velezensis and
Pseudomonas putida can control the Magnaporthe oryzae; the causal agent of blast
disease in rice. Trichoderma species have been reported to be effective against many
plant pathogenic fungi, especially members of oomycetes (Verma et al. 2007).
Trichoderma spp. has a multifaceted mode of approach including competition for
nutrients (Elad 2000), mycoparasitism (Troian etal. 2014), secretion of antimicro-
bial compounds (Xiao-Yan etal. 2006), induction of the plant resistance and the
host growth promotion (Martínez-Medina etal. 2014). Trichoderma has a success-
ful antagonistic effect against various important plant pathogens, such as Pythium
(Tchameni etal. 2020), Phytophthora sp. (Bae et al. 2016), Botrytis (You etal.
2016), Fusarium sp. (Saravanakumar etal. 2016; Sreenayana etal. 2022), Sclerotinia
sclerotiorum (Sumida et al. 2018), Sclerotium rolfsii (Islam et al. 2017),
Macrophomina (Pastrana etal. 2016) and Rhizoctonia solani (Daryaei etal. 2016).
4.2 Types ofParasitism
Parasites can be differentiated based on their life cycles into two categories:
4.2.1 Obligatory
The obligate parasitic fungi cannot complete their life cycle without exploiting a
suitable host. If an obligate parasite cannot obtain a host, it will fail to reproduce.
All obligatory and some non-obligate parasites must either penetrate living cells or
come into close contact with them to obtain nourishment. The two most signicant
biotrophic fungi which cause powdery mildew and rust belong to the biggest cate-
gory of plant pathogenic fungi, which harm numerous economically crucial crops
and signicantly reduce yields (Hückelhoven 2005; Jakupović etal. 2006; Micali
etal. 2008; Yin etal. 2009). Rust and powdery mildew are caused by many fungi
that can create specialized infective structures called haustoria. These haustoria
have been identied as a fungal structure with a key role in disease establishment
and have been implicated in essential processes like nutrient uptake and effector
delivery.
4.2.2 Nonobligatory (Facultative)
Certain saprophytic fungi and bacteria can live on live, dead host tissues and various
nutrient media. These parasites as necrotrophs grow saprophytically, but under spe-
cic circumstances, they attack live plants and cause disease. The nonobligatory
parasites vary in their pathogenicity. They are more resilient and include many
M. M. El-Metwally etal.
383
common fungi such as Rhizoctonia sp., Alternaria sp., Cercospora sp., and
Sclerotium sp. These pathogens have a highly diverse spectrum of hosts. Vascular
wilts, which are frequently caused by Fusarium, Verticillium, Ceratocystis, and
Cephalosporium, occupy a unique position among plant diseases since during the
critical stages of pathogenesis, the fungus is conned within non-living xylem ele-
ments of the host. Most nonobligatory parasites primarily invade and infect plants
by degrading the plant cell wall using lysozymes as one of their primary mecha-
nisms (Nühse 2012; Davidsson etal. 2013).
Parasitic fungi-infected plants are classied generally based on their strategies
into two categories, ectoparasitism, and endoparasitism. Most genera of
Erysiphaceae are ectoparasites. Out of the 17 genera of the Erysiphaceae, only four
genera, Phyllactinia, Leveillula, Queirozia, and Pleochaeta exhibit endoparasitism
(Takamatsu etal. 2016). Mycorrhizas are commonly divided into ectomycorrhizas
and endomycorrhizas. Ectomycorrhizal hyphae penetrate the root cortex with a web
of closely intertwined fungus hyphae (Favre-Godal etal. 2020). The ectomycorrhi-
zas hyphae remain apoplastic outside the protoplasts of the root cells. In other cases,
hyphae may be invasive then representing ectomycorrhizae.
On the other hand, endomycorrhizae and fungal hyphae form coils for the
exchange of metabolites and minerals within the root cells while still staying envel-
oped by a phagocytotic pocket. The hyphal coils may eventually be digested by the
root cells. Endomycorrhiza includes arbuscular, ericoid, and orchid mycorrhiza
(Brundrett 2004).
4.3 Factors Affecting Parasitism
It has been shown that the composition of the rhizosphere microbial community is
inuenced by many environmental factors such as temperature (Brooks etal. 2014),
water content (Abdul Rahman etal. 2021), pH (Javed etal. 2002) (Aydi Ben Aydi-
Ben-Abdallah et al. 2020), CO2 concentration, O2 levels (Abdul Rahman et al.
2021), EC (Aydi-Ben-Abdallah et al. 2020) and the biochemical composition of
root exudates (Bais etal. 2008).
Exogenous environmental factors have a critical role in the predisposition of
plants to infection and disease spread in the host after infection by fungi. The host
damages ranging from small outbreaks to an epidemic-level scale depend mostly on
some climatic, chemical, physical, and biological conditions that can interact with
one another to induce the onset of disease (Thompson etal. 2014). The host-microbe
interaction and the pathogenicity are varied according to the pathogen, the host, the
environment, and the interference of human factors (Fig.2). The host plant’s devel-
opment and resistance, as well as the pathogen’s development or sporulation and
level of virulence, may be affected by environmental and human variables.
Many pathogenic fungi create one or more protein elicitors during plant-microbe
interactions, which can cause the induction of defense responses in plants (Peng
etal. 2011). The mechanisms induced by microbial elicitors include many defense
Symbiotic Relationships withFungi: FromMutualism toParasitism
384
Fig. 2 Diagram
illustrating the main factors
affecting the pathogenicity
reactions like hypersensitive reaction (Allen etal. 2004; Rowland etal. 2005), sys-
temic acquired resistance (Durrant and Dong 2004), reactive oxygen species
(Glazebrook 2005), and biosynthesis of phytoalexins and pathogenesis-related pro-
tein (Silipo etal. 2010). Elicitors are signaling molecules that trigger secondary
metabolites formation in a plant cell by inducing plant defense, hypersensitive
response, and/or pathogenesis-related proteins (Yu etal. 2016). They fall into two
categories: biotic and abiotic. The biotic elicitors are derived from the biological
origin and include proteins, polysaccharides, glycoproteins, or cell-wall fragments
derived from fungi, bacteria, and even plants (Ramirez-Estrada etal. 2016; Ochoa-
Meza etal. 2021). Many physical and chemical factors are effective abiotic elicitors
(Sák etal. 2021). These include ultraviolet irradiation, partial freezing, Ozone, salts
of heavy metals, free radicals, and DNA-intercalating compounds.
Upon the abiotic or biotic elicitor treatment, many metabolic reactions may take
place. For example, the accumulation of many toxic substances such as salicylic
acid and jasmonate (Shinya etal. 2022) and activation of defense enzymes like per-
oxidase, oxidase, superoxidase, catalase, superoxide dismutase, chitinase and
PR-proteins like β-1–3 glucanase. Also, the production of secondary metabolites
was increased like phytoalexin (Shinya etal. 2022), cytokinins, ethylene, salicylic
and abscisic acids (Morimoto etal. 2018), phenols, and lignin content (Patel etal.
2020). In addition to promoting disease resistance, fungal elicitors also play a sig-
nicant role in inducing plant growth and development (Patel etal. 2020).
Some fungal spores have adhesive materials on their surfaces that enable them to
adhere to different surfaces. Once the spore germinates, it often secretes more
enzymes that presumably soften or dissolve the contact cell wall and make its pen-
etration easier. When a pathogen attacks a host plant, the genes of the pathogen are
activated, produced, and release all their chemical weapons of attack against the
M. M. El-Metwally etal.
385
host cell. The primary groups of chemicals generated by plant pathogens that are
thought to be involved in the direct or indirect development of disease are enzymes,
poisons, growth regulators, and polysaccharides (Komon-Zelazowska etal. 2007;
Druzhinina etal. 2011). The toxicity of these chemicals varies widely, and their
relative relevance may differ from one disease to another.
Nematophagous fungus; Arthrobotrys oligospora produces not only chemotaxis
(Bargmann 2006) that trapped nematodes but also produces a sticky substance that
xes the pathogen to the prey. These sugars coat the nematode’s surface and are
involved in the interconnectivity caused by pectin and chemotaxis (Hsueh et al.
2013, 2017).
Pathogenic fungi have the ability to live off the substances manufactured by the
host plants, and some other pathogens depend on these substances for survival.
Additionally, many plant pathogens elaborate phytotoxic compounds when attack-
ing the host which produces a variety of symptoms in sensitive plants. These toxins
are mandatory for the pathogenicity of the sensitive host plant. The development of
plant disease symptoms, such as leaf spots, chlorosis, wilting, necrosis, and growth
inhibition and promotion is signicantly inuenced by fungus toxins (de Moraes
Pontes etal. 2020; Chen etal. 2020). Most pathogenic fungi especially oomycetes
secrete a plethora of effectors into the extra-haustorial space which is then seeped
into the host cytoplasm (Oliva etal. 2010; Oliver and Solomon 2010). In the patho-
genesis of the majority of plant diseases, toxins play a signicant role. It has been
demonstrated that a number of toxic substances produced by phytopathogenic fungi
have been shown to produce all or part of the disease syndrome on the host plant and
on other species of plants that are not normally invaded by these pathogens in
nature. These toxins are called nonhost-specic toxins and affect the virulence of
the pathogen, but they are not necessary to cause disease.
Many reviews reported that the phytotoxins are produced by one fungal genus
(McLean 1996; Kim and Chen 2019) or one fungal species (Chen et al. 2019).
Others stated that fungal interactions with a single plant species or plant group
resulted in the production of phytotoxins (Masi etal. 2018). There are at least 545
fungal phytotoxic secondary metabolites identied to date, including 207
polyketides, 46 phenols, and phenolic acids, 135 terpenoids, 146 nitrogen- containing
metabolites, and 11 other compounds (Xu etal. 2021).
For example, Alternaria is a well-known genus for the production of a variety of
about 70 toxic metabolites (Logrieco etal. 2009; Pavón Moreno etal. 2012). Some
of these metabolites are; altenuene, dibenzo-αpyrones alternariol, tentoxin, alter-
nariol monomethyl ether, and a derivate of both tenuazonic acid and tetramic acid
(Logrieco etal. 2003; Ostry 2008; Noelting etal. 2016; Escrivá etal. 2017; Topi
etal. 2019; Crudo etal. 2019). Tentoxin is produced by Alternaria alternata fungus,
which causes leaf spots and chlorosis in many plants (Noelting etal. 2022). Tentoxin
is a cyclic tetrapeptide that inactivates a protein (chloroplast-coupling factor)
involved in energy transfer into chloroplasts (Durbin and Uchytil 1977; Mochimaru
and Sakurai 1997). This inhibits the light-dependent phosphorylation of ADP to
ATP, in comparison to species that are not sensitive to the toxin, these all-inhibition
Symbiotic Relationships withFungi: FromMutualism toParasitism
386
effects are substantially more pronounced in plant species susceptible to chlorosis
after tentoxin treatment. Alternaria species create a lot of toxic substances like
alternariol and alternariol monomethyl ether (Pero etal. 1973). Additionally, it pro-
duced non-specic toxins in culture ltrates, according to (Anand et al. 2008),
which decreased cotton seedling vigor, root length, shoot length, and seed
germination.
Cercosporin is a photosensitizing perylenequinone which is produced by the fun-
gus Cercospora (Newman and Townsend 2016). It reacts with lipids, proteins, and
nucleic acids of the host cells thereby enhancing the virulence of the pathogen.
Another example of toxins produced by fungi is the fumaric acid which is produced
by Rhizopus spp. in rot disease. Also, oxalic acid toxin which is produced by
Sclerotinia sclerotiorum (Zhou and Boland 1999; Cessna et al. 2000) and
Cryphonectria parasitica (Heiniger and Rigling 1994; Rigling and Prospero 2018).
In various plants, ophiobolins are produced by Cochliobolus sp. (Tian etal. 2017);
ceratoulmin is produced by Ophiostoma ulmi in Dutch elm disease (Temple etal.
1997); fusicoccin is produced by Phomopsis amygdali in the twig blight disease of
peach (Marra etal. 2021); pyricularin is produced by Pyricularia grisea in rice blast
disease (Valent and Chumley 1991); fusaric acid and lycomarasmin are produced by
Fusarium oxysporum in barley wilt; and many others (Liu etal. 2016).
A host-specic is a substance produced by a pathogenic microorganism that is
toxic only to the susceptible hosts of that pathogen and shows little or no toxicity
against the non-susceptible plants (Meena and Samal 2019). It has been established
that certain fungi, including Helminthosporium, Alternaria, Periconia,
Colletotrichum, Phyllosticta, Corynespora, and Hypoxylon, produce these toxins
(Xu etal. 2021).
Among such host-specic toxins produced by fungi are Victorin which are
produced by Helminthosporium victoria (Rines and Luke 1985) in oat leaf blight.
T toxin is produced by race T of Cochliobolus heterostrophus in southern corn
leaf blight (Xiaodong etal. 2018); HC Toxin Race 1 of Cochliobolus carbonum
causes northern leaf spot and ear rot disease in maize(Xiaodong etal. 2018). CCT
toxin is produced by Corynespora cassiicola in tomato (Oka etal. 2006); peritoxin
is produced by Periconia circinate which causes sorghum root rot disease (Macko
etal. 1992); and many others.
Plant pathogens frequently disrupt the hormonal balance of the plant and induce
irregular growth responses that are incompatible with a plant's healthy develop-
ment. Pathogens may cause disease by affecting the growth regulatory systems of
the infected plant through the secretion of growth regulators in the infected plant.
This disturbance in plant growth regulatory systems may lead to abnormal plant
growth responses which cause abnormal symptoms, such as overgrowths, stunting,
rosetting, excessive root branching, stem malformation, leaf epinasty, defoliation,
and suppression of bud growth. Some pathogenic fungi as Fusarium oxysporum in
banana wilt can produce IAA on their own in addition to increasing the levels in
their respective hosts. High concentrations of IAA can suppress the expression of
plant defense genes (Shinshi etal. 1987) and may inhibit the hypersensitive response
M. M. El-Metwally etal.
387
(Jouanneau etal. 1991). Rice seedlings infected with Fusarium fujikuroi grow rap-
idly and become much taller than healthy plants (Hedden and Sponsel 2015). This
observation is referred as gibberellin secretion by the pathogen.
Many studies showed that the microbial community in the plant rhizosphere
depends on the plant species and ecotype (Lundberg etal. 2012; Peiffer etal. 2013;
Lebeis 2014). Some fungal pathogens are restricted to a single plant species, others
to one genus, and others have a wide range of hosts belonging to many families of
higher plants. Fusarium oxysporum attacks only tomatoes to cause tomato wilt dis-
ease. Similarly, Venturia inaequalis, which causes apple scab, affects only apples,
whereas Puccinia graminis which causes stem rust of wheat, attacks only wheat.
Most smut fungi attack the ovaries of monocot spikes and develop in them.
Dematiaceous fungi cause wilt to invade susceptible plants through the roots and
basal wounds to reach the vascular bundles. Depending on the cropping season,
cultivar type, and stage of plant development, the microbial community in the rhi-
zosphere of potato plants might vary (da Silva etal. 2003). Also, the plant growth
stage had a greater impact on fungal community composition than bacterial com-
munity composition (Schlemper etal. 2018).
Many studies showed that the microbial population in the plant rhizosphere is
inuenced at least in part by the species and ecotype of the plant (Bulgarelli etal.
2012; Lundberg etal. 2012; Peiffer etal. 2013; Lebeis 2014). Plants can control soil
microbial population through their root exudates serving as nutrient sources, chemi-
cal stimulants, or inhibitors for associated microorganisms. Chemical analysis of
the Arabidopsis thaliana root exudates shows many variations between ecotypes,
suggesting a way by which the plant controls the assembly of the community
(Micallef etal. 2009). The chemical components which are found in A. thaliana root
exudates, as well as the rhizosphere microbiome, change as the plant develops. This
nding shows that A. thaliana sends out growth-stage-specic signals that inuence
the microbiome of its roots (Chaparro etal. 2014).
In addition, it has been noted that the microbial communities associated with
potato cultivars are varied at different growth stages (İnceoğlu etal. 2010). Recent
studies on maize (Hou etal. 2018) and wheat (Simonin et al. 2020) rhizosphere
microbial communities have demonstrated that the plant types change the microbial
community under stable environmental conditions. Finally, the physiological state
of the plant also inuences its microbiome. Susceptible plants that have specic
receptors for certain pathogens become diseased (Bhaskar etal. 2021). While plants
that lack such receptors remain resistant to pathogens and develop no symptoms.
Plants species or varieties that do not produce one of the substances essential for the
survival of an obligate parasite, or for its development would be resistant to this
pathogen. Most plants and activities of the pathogen may partially or almost totally
defend themselves with the aid of various combinations of naturally occurring or
induced chemical compounds or defense structures.
Many pathogens that succeed to enter nonhost plants naturally fail to cause
infection. This suggests that the resistance to infection displayed by plants
against some pathogens is the result of chemical defense mechanisms rather than
Symbiotic Relationships withFungi: FromMutualism toParasitism
388
structural ones. Plants release a range of chemicals through the surface of their
shoots and roots that have a pathogen-inhibiting effect. For instance, fungi toxic
exudates on the leaves of some plants, e.g., sugar beet and tomato inhibit the germi-
nation of spores of fungi Cercospora and Botrytis respectively.
Root exudates play an important role in understanding the relationships between
plants and soil microorganisms, ranging from mutualistic to pathogenic. Recent
research employing rRNA gene pyrosequencing showed that root exudate changes
are mostly controlled by molecular cross -talk between plants and soil microorgan-
isms (Chaparro etal. 2014; Sugiyama etal. 2014). It was observed that the root
exudates are the rst step toward colonization for many rhizosphere bacteria (Tan
etal. 2013). They stimulate spore germination for root parasitic fungi (Harrison
1998; Clocchiatti et al. 2021), seed germination for owering parasitic plants
(El-Halmouch etal. 2006), and cyst hatching of nematodes (Turner and Subbotin
2013). In addition, root exudates can act as specic stimulatory compounds and
antimicrobials which have a considerable toxic effect on the rhizosphere microora.
Root exudates are a complex mixture of high and low molecular-weight chemicals,
many of which can trigger plant growth-pmoting rhizobacteria (PGPR) responses
(Bais etal. 2008; Broeckling etal. 2008; Liu etal. 2017; Feng etal. 2018; Sharma
etal. 2020). It was demonstrated that tiny sugars, polysaccharides, amino acids,
aromatic chemicals, phenolics, and small organic acids are thought to be key drivers
of bacterial and/or fungal attraction in the rhizosphere (de Weert etal. 2002; Ling
etal. 2011; Neal etal. 2012; Zhang etal. 2020).
The compounds present in A. thaliana root exudates vary with the plant’s devel-
opmental stages. For example, A. thaliana sends out growth-stage-specic signals
that inuence the microbiome of its roots (Chaparro etal. 2014). Also, some other
evidence indicated that the microbiome of the soil can be shaped by the composition
of root exudates that are released by host plants (Shi etal. 2011). Moreover, it was
concluded that the host growth stage affects root physiology and changes the quality
and amount of root exudates. As a result, these changes select root-associated
microbiota during various growth stages (Duneld and Germida 2003; Sugiyama
etal. 2014). The secretion composition varies along the root length and this results
in distinct bacterial communities along the root length (Ofek etal. 2011).
Zoospores of Phytophthora sp. may be attracted by the root and/or exudates of
their hosts (Zentmyer 1961; Chepsergon etal. 2020; Bassani etal. 2020). Pythium
species depend on seed and seedling exudates for either oospore germination
(Stanghellini and Burr 1973; Martin and Loper 1999; Nzungize etal. 2012), sporan-
gial germination (Nelson 1991), or zoospore attraction towards the host (Heungens
and Parke 2000; Zhang etal. 2020). Contrary, maize root exudates inhibit the zoo-
spore activity, cyst germination, and mycelial growth of Phytophthora sojae (Zhang
etal. 2019, 2022).
M. M. El-Metwally etal.
389
5 Signaling andQuorum Sensing inPlant Symbiotic
Relationships withFungi
A large number of endophytes can colonize the plants; as a consequence, particular
balancing mechanisms are required for their survival. This is a sophisticated pro-
cess; quorum sensing (QS) plays a pivotal role in this communication. QS can be
dened as a cell-to-cell communication system and it is a cell density-dependent
microbial communication that controls gene expression by forming freely diffusible
compounds called autoinducers (AIs) or quorum sensing molecules (QSMs) (Fuqua
etal. 2001; Williams etal. 2007; Cornforth etal. 2014; Naga etal. 2021). These AIs
synchronize responses across a density population to achieve crosstalk and inhibit
the chemical defense of other organisms (Teplitski etal. 2011). QS is critical in
microbe-microbe and plant-microbe crosstalks in all ecological niches (Safari etal.
2014). Since its discovery in the luminescent marine bacteria Vibrio scheri
(Nealson and Hastings 1979), it has been identied in a wide range of bacteria. QS
regulates cell-cell communication, virulence factors, motility, competence, biolm
formation, antibiotic production, and sporulation (Miller and Bassler 2001).
Through modulation of virulence factors, it allows environmental adaptation to
microbial interactions with plants (Antunes et al. 2010). For decades, QS was
thought to be limited to bacterial systems, eukaryotic QS gained attraction after the
revolutionary discovery of farnesol compound as the QSM in the pathogenic fungus
Candida albicans (Hornby etal. 2001) and some other fungal species were reported
to have QS mechanisms and produce AIs (Table1). QS regulates the expression of
virulence genes in a variety of microorganisms, in addition to mediating a variety of
functions (Antunes etal. 2010). Other growth of microorganisms has been reported
to be inhibited or slowed by certain QSMs. For example, farnesol could inhibit the
growth of Saccharomyces cerevisiae by lowering the level of diacylglycerol (DAG),
effectively suppressing the G1 stage of the cell cycle (Machida et al. 1999).
Astonishingly, cross-kingdom signaling was reported to be mediated by both bacte-
rial and fungal QSMs. For example, eukaryotes signaling could approve an efcacy
to interfere with bacterial quorum signals (Ismail etal. 2016) and similarly, bacteria
could inuence fungal QS (Martín-Rodríguez etal. 2014). In addition, endophytes
exhibited a communication system network mediated by QS to control the expres-
sion of many genes among their conned populations, maintain their colonization
in host plants, and counteract phytopathogens (Venkatesh Kumar etal. 2019). Qs
allows for complex cross-talks between diverse endophytic microorganisms com-
munities in planta. A pioneering study recently revealed the role of autoinducer-2
(AI-2) in endophytic fungi and bacteria inter-kingdom signaling systems
(Tourneroche etal. 2019).
Surprisingly, plants also showed efcacy to synthesize QS-like molecules
(Hartmann etal. 2014). N-acylated homoserine lactones (AHLs) serve as the most
widely AI used in proteobacteria. QSMs that mimic AHL have been detected in
some plants as Oryza sativa (rice) and Phaseolus vulgaris (bean) (Pérez-Montaño
etal. 2013). These biomolecule analogs can bind to bacterial receptors and inhibit
Symbiotic Relationships withFungi: FromMutualism toParasitism
390
Table 1 Some fungal QS molecules and the mediated processes
Fungi strain QSMs Mediated processes Reference
Candida albicans Farnesol Morphogenesis, pathogenicity Hornby etal.
(2001)
Tryptophol Chen etal.
(2004)
Tyrosol Chen etal.
(2004)
Phenylethanol Chen etal.
(2004)
Farnesoic acid Hogan (2006)
Saccharomyces
cerevisiae
Tryptophol Adhesion, invasive growth,
morphogenesis
Hogan (2006)
Tyrosol Chen etal.
(2004)
Phenylethanol Chen etal.
(2004)
Aspergillus terreus Butyrolactone I Secondary metabolite synthesis Raina etal.
(2012)
A. nidulans γ-hepatolactone Secondary metabolite synthesis Williams etal.
(2012)
A. avus Oxylipins Sporulation, mycotoxin
production
Affeldt etal.
(2012)
Penicillium
sclerotiorum
γ-butyrolactone Phospholipase A2 inhibitory
activity
Raina etal.
(2010)
Neurospora crassa Unknown Conidial anastomosis Roca etal.
(2005)
Cryptococcus
neoformans
Amino acid
peptides
Virulence Lee etal. (2007)
Debaryomyces
hansenii
Ammonia Adhesion Gori etal. (2011)
Penicillium
decumbens
Farnesol Cell wall biogenesis Guo etal. (2011)
P. sclerotiorum γ-butyrolactone Phospholipase A2 inhibitory
activity
Raina etal.
(2010)
Ophiostoma
occosum
Cyclic
sesquiterpenes
Yeast-mycellium dimorphism Berrocal etal.
(2014)
QS-based biolm development in Pantoea ananatis and Sinorhizobium fredii
(Pérez-Montaño etal. 2013). As a result, QS is more than a communication system
used by microbes; it represents a more complex interactive phenomenon used by
competing ecological niches like bacteria, fungi, and plants. Plants harbor a variety
of microbes in their endospheric, rhizospheric, and phyllospheric microbiomes pos-
sibly coinciding with their origin. Hence, it is clear that co-evolutionary forces have
endowed plants with the ability to produce signaling molecules to mimic microbial
AIs (Teplitski etal. 2011; Hartmann etal. 2014). Research in agriculture and bio-
technology today puts a great deal of attention on the complex interactions between
plants and bacteria.
M. M. El-Metwally etal.
391
In a natural microbial community, a microbe’s virulence is not only controlled by
QS but can also be modied by other members of the community that occupy the
same niche (Brader etal. 2017). Certain microorganisms can inhibit QS, this phe-
nomenon is named by quorum quenching (QQ) and it mediates inter and intra-
kingdom cross-talks (Dong et al. 2007). QQ can be achieved by inhibiting
auto-inducer synthesis, preventing auto-inducer binding to their receptors, or by
degrading them (Natrah etal. 2011). A variety of endophytic fungi was reported to
exhibit QQ in articial cultures, making them a potential source of alternative medi-
cine against pathogenic microbes that utilize QS for virulence (Table2).
Some endophytic bacteria and fungi use the QQ as antivirulence strategy (Kusari
etal. 2014, 2015). In general, some QQ enzymes were reported to mediate the dis-
ruption of AIs (Hong etal. 2012). For example, lactonase and acylase enzymes can
degrade AHL in Gram-negative bacteria by inactivating the lactone ring (Whitehead
etal. 2001) (Fig.3). Oxidoreductase enzyme can interfere with bacterial communi-
cation by reducing or oxidizing the acyl chain of AHLs rather than breaking them
down (Hong etal. 2012).
AHL is composed of a homoserine lactone moiety and a variable-length acyl
chain. Lactonase enzyme hydrolyses AHL lactone bonds, making it incapable of
binding the target transcriptional factors required to synthesize virulence proteins.
Lactonase was discovered in Endophytic Enterobacter that was isolated from the
woody plant climber; Ventilago madraspatana (Rajesh and Rai 2014). Interestingly,
lactonase enzyme from Enterobacter sp. CS66 isolated from another medicinal
plant had a lower degrading AHL activity. However, it signicantly inhibited
Table 2 Fungal endophytes have anti-quorum sensing potential
Endophytic fungi Source Test strain Reference
Penicillium
restrictum
Silybum marianum Hybrid of bacterial strains
AH2759
Figueroa etal. (2014)
Khuskia (LAEE21) Marine plants Chromobacterium violaceum
CVO26
Martín-Rodríguez
etal. (2014)
Fusarium
(LAEE13)
Sarocladium
(LAEE06)
Lasiodiplodia sp.
Epicoccum
(LAEE14)
Fusarium
graminearum
Ventilago
madraspatana
Chromobacterium violaceum
CVO26
Rajesh and Rai (2013)
Aspergillus sp. Agricultural eld Pseudomonas aeruginosa Dawande etal. (2019)
Penicillium sp.
Fusarium sp.
Phoma sp.
Alternaria
alternata
Carica papaya Pseudomonas aeruginosa Rashmi etal. (2018)
Phomopsis tersa Carica papaya Pseudomonas aeruginosa Meena etal. (2020)
Symbiotic Relationships withFungi: FromMutualism toParasitism
392
Fig. 3 QQ enzymes; lactonase enzyme (a) and acylase enzyme (b)
QS-dependent virulence factors production of Pectobacterium atrosepticum
(Shastry etal. 2018). It suggests that various endophytic QQ enzymes evolved mod-
ications, and their primary activity is to disrupt the virulence factors of surround-
ing microorganisms. Phomopsis tersa is an endophytic fungus isolated from Carica
papaya that was recently discovered to reduce Pseudomonas aeruginosa
QS-regulated virulence factors (Meena etal. 2020). As a result, it is clear that endo-
phytes use QS and QQ to regulate the virulence and other related phenomena of
resident and invading microorganisms, allowing them to survive inside plant tissues.
Many plants and their products exhibited anti-quorum sensing properties (Koh
and Tham 2011; Kim and Park 2013; LaSarre and Federle 2013; Peter etal. 2019;
Naga etal. 2022). Plants have been observed to disrupt QSMs through increased
phytohormones production such as cytokinins and auxins, reactive oxygen species
(ROS) generation, and the genes related to plant immune responses expression (von
Rad etal. 2008; Bai etal. 2012; Schenk et al. 2012). They produce antivirulence
quorum sensing inhibitors (QSIs), for example, glycyrrhiza glabra avonoids
reduced the virulence of Acinetobacter baumannii (Bhargava etal. 2015). Similarly,
soft rot in potato is caused by Pectobacterium and depends on QS to synchronize its
virulence factor and the plant cell wall degrading enzymes interfere with plant phe-
nolic volatiles and disrupt its QS (Joshi etal. 2016). Furthermore, the reduction in
AHL accumulation following treatment with plant volatiles indicating a direct inter-
action with N-acyl homoserine lactone synthase or regulatory protein (Joshi
etal. 2016).
As a result, it is clear that plants are highly dependent on QQ and QS to sustain
their endophytic microbiome for their growth, virulence, and sporulation. In light of
this, the plant endospheric microbiome offers a favorable environment for endo-
phytic microorganisms to compete in.
M. M. El-Metwally etal.
393
5.1 Endophytism Interactions
Endophytic behavior varies greatly and ranges from pathogenism, mutualism, and
saprophytism (Saikkonen etal. 1998; Schulza and Boyle 2005). In physiological
adaptation to uctuating habitats, the transition between various lifestyles serves as
an evolutionary determinant, providing phenotypic diversity to fungi. After coloniz-
ing several plants, the endophytic fungi may have a range of lifestyles depend on the
transmission mode, infection pattern, the age of the plant, climate changes, and the
genotype of the endophyte and host (Saikkonen etal. 1998; Freeman etal. 2001).
One microbial species may have strains that are mutualistic, pathogenic, or com-
mensal (Sheibani-Tezerji etal. 2015). Microbes from various strains share some
genomes due to intra-specic existence, which allows the plant defense system to
attack them identically. Comparative genomic research of endophytes and patho-
gens showed that their virulence factors are analogous. But, some endophytes
lacked the essential virulence factors that act as a dening characteristic (Lòpez-
Fernàndez etal. 2015). It is noteworthy to mention that a colonized fungus can
change its lifestyle from pathogenism to endophytism or vice-versa. This relies on
the metabolic and/or genetic condition of its interacting partners as well as environ-
mental conditions (Márquez et al. 2007; Redman et al. 2001; Unterseher and
Schnittler 2010). However, the genetic bases of switching in endophytic lifestyles is
not understood (Redman etal. 2001; Unterseher and Schnittler 2010).
For instance, it was observed that the mutualistic endophyte; Epichloe festucae
benets its host plant; Lolium perenne by enhancing the acquisition of nutrients and
this increased the biotic stressors resistance (Schardl 2001). E. festucae NoxA
mutant strain which causes a change from parasitism to mutualism was isolated to
pinpoint the symbiotic genes of E. festucae (Tanaka et al. 2006). NoxA gene in
E. festucae and the symbiosis regulation was activated by GTPase RacA (Tanaka
et al. 2008). ROS are released by the E. festucae NoxA gene, which encodes
NADPH oxidase that caused a signicant infection, loss of apical dominance, pre-
mature senescence, and ultimately death in the L. perenne plant. Further molecular
information about this interaction provided detailed insight into the endophyte’s
intricate regulatory processes displayed by E. festucae within the host L. perenne
(Bharadwaj etal. 2020) (Fig.4). The most intriguing aspect of this interaction is the
endophytes efforts to sustain themselves inside the host by trying to limit its growth
in the intercellular spaces of the host. This autoregulation example shows that bal-
anced antagonisms as well as other antagonism-independent methods may also help
endophytes survive in a mutualistic and a symptomatic manner. Many endophytes
particularly systemic ones that spread vertically are perpetually present in the host
plant and never develop into pathogenic organisms. Some endophytes were evolved
in close association with a specic host such that antagonism is not displayed
against them, and they may have acquired alternative methods of endophytism
maintenance.
Symbiotic Relationships withFungi: FromMutualism toParasitism
394
Fig. 4 Conversion the endophytic fungi E. festucae from endophytism to pathogenism in
L. perenne
Similarly, saprophyte-endophyte shift was reported, but nothing is understood
about the triggers that cause these shifts. For instance, Phomopsis liquidambari B3
fungi can form a mutualistic relationship with some host plants such as Bischoa
polycarpa plant and revealed to exude a variety of enzymes in a saprophytic state
including cellulase, laccase, and polyphenol oxidase (Chuan-Chao etal. 2010; Zhou
etal. 2014). The colonization strategy used by P. liquidambari B3in these plants is
host adapted. They exhibit various growth promotions that are inuenced by nitro-
gen (N2) availability according to observations of colonization dynamics and
promoting of plant growth evaluation as in Oryza sativa and Arabidopsis thaliana.
By studying the genes connected with the saprophytic-endophytic transition, it was
revealed that the most notable genes in P. liquidambari B3 participate in protein
synthesis, ribosome biogenesis, and MAPK signaling and most of which are
up- regulated in the endophyte (Zhou etal. 2017).
In addition, endophytic fungi exhibit a shift towards the pathogenic side of the
spectrum with the aging of the leaves (Saikkonen etal. 1998). Age increases the
prevalence of endophytic fungi which result in more visible outer infections. For
instance, endophytic fungus colonized older Pinus densiora and Pinus thunbergia
M. M. El-Metwally etal.
395
needles more than younger needles (Hata and Futai 1993). Similar to this, Citrus
lemon older seedlings that have the endophytic Metarhizium anisopliae and
Beauveria bassiana strains showed the best survival rate. Consequently, plant aging
has an impact on endophytic lifestyle as it is distinguished by a deciency of critical
nutrients (Bamisile etal. 2020).
Also, it was evaluated that fungal community may be altered from stage to
another according to the developmental stage of plant and this is important in the
change from parasitic to mutualistic. For example, joshua trees relationship with
arbuscular mycorrhizal fungi (AMF) (Harrower and Gilbert 2021). Furthermore,
environmental factors can have an impact on the endophytic fungus symbiotic life-
style. Under certain conditions, the symptomatic endophyte Diplodia mutila of
Iriartea deltoidea plant becomes parasitic (Alvarez-Loayza etal. 2011). The impact
of irradiance on the endophytic transition was also investigated; I. deltoidea was
reported to favor the shaded parts while intense light causes the associated endo-
phyte to become pathogenic. On the contrary, endophytic fungi Periconia macrospi-
nos changes from a mutualistic lifestyle to an extreme pathogenic if the shade
increased (Mandyam and Jumpponen 2015). Salinity was shown to increase
Fusarium solani pathogenicity (Eydoux and Farrer 2020).
To retain the mutualism, there must be a balance between balancing strategies
and antagonisms and in case of any disorder occurrence, disease symptoms may
manifest and the host immune system will reject the fungus (Rai and Agarkar 2016).
The relationship between genetic regulation of the pathways variables and the pro-
cesses is yet unclear. Additionally, systemic endophytes tend to exhibit mutualism
more whereas transitory endophytes are very dynamic. Thus, the above- mentioned
variables may be modifying the balancing tactics to upset the endophytic lifestyle,
pushing the fungus to the maximum pathogenicity.
Endophytes use QQ and QS as anti-pathogenic strategies against invader and
resident microbes, any disruption in these communicating pathways inuence and
destabilize the mutualistic symbiosis. Microbial QSIs can regulate the virulence,
proliferation, and sporulation of a particular target microbe. However, when the
regulating mechanism becomes unstable owing to any intrinsic or external reason,
the target microbe becomes harmful. Additionally, it is possible that plant QSIs bal-
ance the pathogenicity of endophytes in the microecosystem of plant whereas nutri-
tional imbalances may make it unstable. For instance, the fungus E. festucae is
mutualistic and asexually reproducing endophyte of L. perenne that has been exten-
sively investigated (Schardl 2001). Nevertheless, the start of owering in the host
plant triggers the sexual life cycle in some Epichloe spp., which changes the fungi
mutualism to antagonism because resources are being pushed towards owering
(Schardl etal. 2004). It implies that plants devote the entirety of their energy to
owering rather than the virulence resistance of endophytic microorganisms which
leads to changing their lifestyle. Even though these methods of disruption cannot
fully explain this complex phenomenon, their involvement could not be disregarded.
Therefore, uncovering the complex interaction of numerous elements that underlies
endophytic dynamism would require extensive research.
Symbiotic Relationships withFungi: FromMutualism toParasitism
396
Organisms have evolved some complex strategies to interact and tolerate the
environmental changes (Bouyahya etal. 2017). So, they may alter their metabolism
to resist various intrinsic and/or extrinsic stress situations for improved survival in
the changed surroundings (van’t Padje etal. 2016). The fundamental cross-talks
between endophytes and plants are based on secondary metabolites (Huang etal.
2019; Jacoby etal. 2021). The host metabolism is typically induced by endophyte
(Ludwig-Müller 2015). While endophytes supply many metabolites to assist the
host plants in surviving with diverse stress circumstances, plants can produce some
compounds which are essential for their self-defense and the endophytes growth
(Guo etal. 2008). Endophytes can produce secondary metabolites in axenic cul-
tures, and they are being used to make well-known and innovative medicines with
antimalarial, antioxidant, antiviral, and anti-cancerous properties (Kusari et al.
2012). Natural bioactive compounds generated from endophytes come into many
structural classes including steroids, avonoids, phenolics, alkaloids, phenylpro-
panoids, terpenoids, quinones, volatile organic and aliphatic compounds (Schulz
etal. 2002).
It is noteworthy to mention that the endophytes inuence not just the host plant
metabolism, but also the metabolism of any resident endophytes. It is clear from the
fact the large number of secondary metabolites remain equivocal (Lim etal. 2012).
It was reported that microbial interactions are crucial in stimulating the secondary
metabolites production. For example, culturing Streptomyces hygroscopicus with
Aspergillus nidulans enabled polyketide biosynthetic gene cluster activation
(Schroeckh etal. 2009). Also, methyl esters and polyketides production was induced
by culturing Bacillus subtilis bacteria with the endophytic fungus Chaetomiun sp.
(Akone etal. 2016).
In addition, some plant extracts have been reported to act as inhibitors of the
epigenetic modication-related enzymes, hence activating specic quiet biosynthe-
sis pathways of secondary metabolites. For instance, the endophytic fungus
Colletotrichum gloeosporioides isolated from Syzygium aromaticum generated
some metabolites after the addition of the epigenetic modulators curcumin and res-
veratrol from grape and turmeric extracts, respectively (Sharma et al. 2017).
Similarly, Eupenicillium sp. LG41 (fungal endophyte) of Xanthium sibricum when
treated with nicotinamide produced the two recognized metabolites; eupenicinicol
A and eujavanicol A (Li etal. 2017). In a similar manner, treatment of the endo-
phytic fungus Hypoxylon anthochroum of Carica papaya with the curry leaf extract
and garlic led to the stimulation of cryptic bioactive metabolites (Mishra etal.
2020). Diallyl disulde and allyl mercaptan; the two main ingredients of organosul-
fur compounds known for inhibiting histone deacetylases, are reported to be pro-
duced by garlic leaves. Curry leaves also contain mahanine, which repress DNA
methyltransferase. These relationships are based on small diffusible signaling mol-
ecules that can activate normally silent biosynthetic pathways, such as QSMs
(Hughes and Sperandio 2008; Scherlach and Hertweck 2009).
Endophytes are endosymbionts that persist for at least a portion of their life cycle
inside of plants without causing any diseases (Hallmann etal. 1997). They are fre-
quently bacteria or fungi which are stabilized by chemically mediated interactions
M. M. El-Metwally etal.
397
(Wang 2016). For example, hexacyclopeptides antimicrobial was produced by the
endophytic fungi Fusarium solani and bacteria Achromobacter xylosoxidans on
Narcissus tazetta (Wang etal. 2015; Haryani etal. 2020). Hence, it is clear to note
that endophytes developed complex communication strategies due to their sharing
ecosystems and not all these interactions are inherently antagonism-based cross-
talks (Mattoo and Nonzom 2021). Intriguingly, the outcome of this cross-kingdom
symbiosis is shaped by the diverse interactions between endophytic microorgan-
isms and the plant (Rodriguez and Roossinck 2012). For instance, thermotolerance
ability of Dichanthelium lanuginosum was believed to be caused by endophytic
fungus Curvularia protuberata but actually it was caused by the double-stranded
virus carried by the symbiont fungus (Márquez et al. 2007; Rodriguez and
Roossinck 2012).
Few endophytic fungi were reported by harboring bacteria that could change
how they interact with their host plants in some ways (MacDonald and Chandler
1981; Bonfante and Anca 2009; Kobayashi and Crouch 2009). For example,
Burkholderia spp. that thrive within the Gigaspora decipiens fungi could inhibit the
germination of spores (Levy etal. 2003). Numerous endohyphal bacteria have an
impact on endophytic fungi ability to produce metabolites. For instance, after host-
ing Luteibacter sp. bacteria, the endophytic fungi Pestalotiopsis neglecta produced
indole-3-acetic acid at a considerably higher rate (Hoffman etal. 2013). Additionally,
it was discovered that the Phyllosticta capitalensis fungus which is an endophyte of
Buxus sinica produced two novel lactamfused-4-pyrones by harboring
Herbaspirillum sp. bacteria (Wang 2016). Also, it was reported that Cupressus sem-
pervirens endophytic fungi that contain endohyphal bacteria as Bacillus subtilis,
B. pumilus, and Sphingomonas paucimobilis which could produce organic volatile
compounds which have antibacterial activity against many pathogens (Pakvaz and
Soltani 2016). Additionally, endohyphal bacteria were shown to trigger phytohor-
mones, which control the host reproductive system and protect host fungi from
harsh conditions (Arora and Riyaz-Ul-Hassan 2019).
Endosymbiotic bacteria may be facultative or obligatory partners on the fungi
(Bastías etal. 2020). Obligate symbionts reproduce vertically with the fungal host,
but facultative symbionts more closely resemble the free-living members hence
have the capacity to invade fungal hosts (Baltrus etal. 2017). Numerous facultative
nonpathogenic bacteria can colonize plant tissues on their own independent of the
fungal hosts (Glaeser etal. 2016). For instance, endoglucanases and endobetaxyla-
nases enzymes assist the endohyphal bacteria Rhizobium radiobacter F4 to colonize
several plants roots on their own (Guo etal. 2018).
Ectosymbiotic bacteria were observed to inuence the tness of their associated
fungi as well as endosymbiotic counterparts. Numerous microbial interactions ben-
et their partners development and defense in various ways (Schelkle and Peterson
1997; Oh etal. 2018). For instance, Rhizophagus irregularis fungi and Rahnella
aquatilis bacteria exchange of phosphorus, calcium, and carbon was reported to be
essential for their interaction (Zhang etal. 2018). It is interesting to observe that the
AMF fructose exudation was approved to enhance the bacterial genes expression
that code for the enzyme phosphatase which dissolves phosphate (Mattoo and
Symbiotic Relationships withFungi: FromMutualism toParasitism
398
Nonzom 2021). Various endophytes cooperate to support host growth and biocon-
trol mechanisms. For example, inoculation of nitrogen-xing endophytic strains
derived from Phaseolus vulgaris with Rhizobium tropici and nodule endophytic
strains such as Burkholderia, Bacillus, Pseudomonas, and Paenibacillus enhanced
disease resistance against Rhizoctonia solani (Ferreira etal. 2020). In conclusion,
some endophytes that are closely symbiotic with their partners assist in the success-
ful colonization of their partners while exhibiting antagonistic behavior toward
some other endophytes and diseases. Therefore, it would appear that balanced
antagonism is not always a necessary condition for maintaining endophytism.
Theoretically, it can be one of the methods or a part of the complex plan the endo-
phytes utilize to survive inside the host plants.
References
Abdul Rahman NSN, Abdul Hamid NW, Nadarajah K (2021) Effects of abiotic stress on soil
microbiome. Int J Mol Sci 22:9036
Affeldt KJ, Brodhagen M, Keller NP (2012) Aspergillus oxylipin signaling and quorum sensing
pathways depend on G protein-coupled receptors. Toxins (Basel) 4:695–717
Akone SH, Mándi A, Kurtán T, Hartmann R, Lin W, Daletos G, Proksch P (2016) Inducing second-
ary metabolite production by the endophytic fungus Chaetomium sp. through fungal–bacterial
co-culture and epigenetic modication. Tetrahedron 72:6340–6347
Allen RL, Bittner-Eddy PD, Grenville-Briggs LJ, Meitz JC, Rehmany AP, Rose LE, Beynon JL
(2004) Host-parasite coevolutionary conict between Arabidopsis and downy mildew. Science
(80–) 306:1957–1960
Alvarez-Loayza P, White JF Jr, Torres MS, Balslev H, Kristiansen T, Svenning J-C, Gil N (2011)
Light converts endosymbiotic fungus to pathogen, inuencing seedling survival and niche-
space lling of a common tropical tree, Iriartea deltoidea. PLoS One 6:e16386
Aly AH, Debbab A, Proksch P (2011) Fungal endophytes: unique plant inhabitants with great
promises. Appl Microbiol Biotechnol 90:1829–1845
Anand T, Bhaskaran R, Karthikeyan TG, Rajesh M, Senthilraja G (2008) Production of cell wall
degrading enzymes and toxins by Colletotrichum capsici and Alternaria alternata causing fruit
rot of chillies. J Plant Prot Res 48:437–451
Antunes LCM, Ferreira RBR, Buckner MMC, Finlay BB (2010) Quorum sensing in bacterial
virulence. Microbiology 156:2271–2282
Arora P, Riyaz-Ul-Hassan S (2019) Endohyphal bacteria; the prokaryotic modulators of host fun-
gal biology. Fungal Biol Rev 33:72–81
Aydi-Ben-Abdallah R, Jabnoun-Khiareddine H, Daami-Remadi M (2020) Variation in the compo-
sition of the microbial community in the rhizosphere of potato plants depending on cropping
season, cultivar type, and plant development stage. Int J Agri Env Food Sci 4(3):319–333.
https://doi.org/10.31015/jaefs.2020.3.11
Bacon CW, Glenn AE, Yates IE (2008) Fusarium verticillioides: managing the endophytic associa-
tion with maize for reduced fumonisins accumulation. Toxin Rev 27:411–446
Bae S-J, Mohanta TK, Chung JY, Ryu M, Park G, Shim S, Hong S-B, Seo H, Bae D-W, Bae I
(2016) Trichoderma metabolites as biological control agents against Phytophthora pathogens.
Biol Control 92:128–138
Bai X, Todd CD, Desikan R, Yang Y, Hu X (2012) N-3-oxo-decanoyl-L-homoserine-lactone
activates auxin-induced adventitious root formation via hydrogen peroxide-and nitric oxide-
dependent cyclic GMP signaling in mung bean. Plant Physiol 158:725–736
M. M. El-Metwally etal.
399
Bais HP, Broeckling CD, Vivanco JM (2008) Root exudates modulate plant–microbe interactions
in the rhizosphere. In: Secondary metabolites in soil ecology. Springer, pp241–252
Bal HB, Nayak L, Das S, Adhya TK (2013) Isolation of ACC deaminase producing PGPR from
rice rhizosphere and evaluating their plant growth promoting activity under salt stress. Plant
Soil 366:93–105
Baltrus DA, Dougherty K, Arendt KR, Huntemann M, Clum A, Pillay M, Palaniappan K, Varghese
N, Mikhailova N, Stamatis D (2017) Absence of genome reduction in diverse, facultative endo-
hyphal bacteria. Microb Genomics 3
Bamisile BS, Senyo Akutse K, Dash CK, Qasim M, Ramos Aguila LC, Ashraf HJ, Huang W,
Hussain M, Chen S, Wang L (2020) Effects of seedling age on colonization patterns of Citrus
limon plants by endophytic Beauveria bassiana and Metarhizium anisopliae and their inuence
on seedlings growth. J Fungi 6:29
Bargmann CI (2006) Chemosensation in C. elegans. WormBook: The online review of C. elegans
biology [Internet].
Bassani I, Larousse M, Tran QD, Attard A, Galiana E (2020) Phytophthora zoospores: from per-
ception of environmental signals to inoculum formation on the host-root surface. Comput
Struct Biotechnol J 18:3766–3773
Bastías DA, Johnson LJ, Card SD (2020) Symbiotic bacteria of plant-associated fungi: friends or
foes? Curr Opin Plant Biol 56:1–8
Berendsen RL, Vismans G, Yu K, Song Y, de Jonge R, Burgman WP, Burmølle M, Herschend J,
Bakker PAHM, Pieterse CMJ (2018) Disease-induced assemblage of a plant-benecial bacte-
rial consortium. ISME J 12:1496–1507
Berrocal A, Oviedo C, Nickerson KW, Navarrete J (2014) Quorum sensing activity and control of
yeast-mycelium dimorphism in Ophiostoma occosum. Biotechnol Lett 36:1503–1513
Bharadwaj R, Jagadeesan H, Kumar SR, Ramalingam S (2020) Molecular mechanisms in grass-
Epichloë interactions: towards endophyte driven farming to improve plant tness and immu-
nity. World J Microbiol Biotechnol 36:1–28
Bhargava N, Singh SP, Sharma A, Sharma P, Capalash N (2015) Attenuation of quorum sensing-
mediated virulence of Acinetobacter baumannii by Glycyrrhiza glabra avonoids. Future
Microbiol 10:1953–1968
Bhaskar R, Xavier LSE, Udayakumaran G, Kumar DS, Venkatesh R, Nagella P (2021) Biotic
elicitors: a boon for the in-vitro production of plant secondary metabolites. Plant Cell Tissue
Organ Cult:1–18
Boller T, Felix G (2009) A renaissance of elicitors: perception of Microbe–associated molecular
patterns and danger signals by pattern-recognition. Ann Rev Plant Biol 60:379–406
Bonfante P, Anca I-A (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions.
Annu Rev Microbiol 63:363–383
Bouyahya A, Dakka N, Et-Touys A, Abrini J, Bakri Y (2017) Medicinal plant products targeting
quorum sensing for combating bacterial infections. Asian Pac J Trop Med 10:729–743
Brader G, Compant S, Vescio K, Mitter B, Trognitz F, Ma L-J, Sessitsch A (2017) Ecology and
genomic insights into plant-pathogenic and plant-nonpathogenic endophytes. Annu Rev
Phytopathol 55
Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil
fungal community composition and diversity. Appl Environ Microbiol 74:738–744
Bronstein JL (2015) Mutualism. Oxford University Press, Oxford
Brooks DR, Hoberg EP, Boeger WA, Gardner SL, Galbreath KE, Herczeg D, Mejía-Madrid HH,
Rácz SE, Dursahinhan AT (2014) Finding them before they nd us: informatics, parasites, and
environments in accelerating climate change. Comp Parasitol 81:155–164
Brundrett M (2004) Diversity and classication of mycorrhizal associations. Biol Rev 79:473–495
Bulgarelli D, Rott M, Schlaeppi K, Ver Loren Van Themaat E, Ahmadinejad N, Assenza F, Rauf
P, Huettel B, Reinhardt R, Schmelzer E (2012) Revealing structure and assembly cues for
Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95
Symbiotic Relationships withFungi: FromMutualism toParasitism
400
Buscaill P, van der Hoorn RAL (2021) Defeated by the nines: nine extracellular strategies to avoid
microbe-associated molecular patterns recognition in plants. Plant Cell 33:2116–2130
Cavicchioli R, Ripple WJ, Timmis KN, Azam F, Bakken LR, Baylis M, Behrenfeld MJ, Boetius
A, Boyd PW, Classen AT (2019) Scientists’ warning to humanity: microorganisms and climate
change. Nat Rev Microbiol 17:569–586
Cesari S, Thilliez G, Ribot C, Chalvon V, Michel C, Jauneau A, Rivas S, Alaux L, Kanzaki H,
Okuyama Y (2013) The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe
oryzae effectors AVR-Pia and AVR1-CO39 by direct binding. Plant Cell 25:1463–1481
Cessna SG, Sears VE, Dickman MB, Low PS (2000) Oxalic acid, a pathogenicity fac-
tor for Sclerotinia sclerotiorum, suppresses the oxidative burst of the host plant. Plant Cell
12:2191–2199
Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by
plant development. ISME J 8:790–803
Chen H, Fujita M, Feng Q, Clardy J, Fink GR (2004) Tyrosol is a quorum-sensing molecule in
Candida albicans. Proc Natl Acad Sci 101:5048–5052
Chen Y, Kistler HC, Ma Z (2019) Fusarium graminearum trichothecene mycotoxins: biosynthesis,
regulation, and management. Annu Rev Phytopathol 57:15–39
Chen J, Ullah C, Reichelt M, Beran F, Yang Z-L, Gershenzon J, Hammerbacher A, Vassão DG
(2020) The phytopathogenic fungus Sclerotinia sclerotiorum detoxies plant glucosinolate
hydrolysis products via an isothiocyanate hydrolase. Nat Commun 11:1–12
Chepsergon J, Motaung TE, Bellieny-Rabelo D, Moleleki LN (2020) Organize, don’t agonize:
strategic success of Phytophthora species. Microorganisms 8:917
Chialva M, Salvioli di Fossalunga A, Daghino S, Ghignone S, Bagnaresi P, Chiapello M, Novero
M, Spadaro D, Perotto S, Bonfante P (2018) Native soils with their microbiotas elicit a state of
alert in tomato plants. New Phytol 220:1296–1308
Chialva M, Ghignone S, Cozzi P, Lazzari B, Bonfante P, Abbruscato P, Lumini E (2020) Water
management and phenology inuence the root-associated rice eld microbiota. FEMS
Microbiol Ecol 96:aa146
Chuan-Chao D, Yan C, Lin-shuang T, Yang S (2010) Correlation between invasion by endophytic
fungus Phomopsis sp. and enzyme production. Afr J Agric Res 5:1324–1340
Clocchiatti A, Hannula SE, Van den Berg M, Hundscheid MPJ, De Boer W (2021) Evaluation of
phenolic root exudates as stimulants of saptrophic fungi in the rhizosphere. Front Microbiol
12:644046
Cohen SP, Leach JE (2019) Abiotic and biotic stresses induce a core transcriptome response in
rice. Sci Rep 9:1–11
Cornforth DM, Popat R, McNally L, Gurney J, Scott-Phillips TC, Ivens A, Diggle SP, Brown SP
(2014) Combinatorial quorum sensing allows bacteria to resolve their social and physical envi-
ronment. Proc Natl Acad Sci 111:4280–4284
Crudo F, Varga E, Aichinger G, Galaverna G, Marko D, Dall’Asta C, Dellaora L (2019)
Co-occurrence and combinatory effects of Alternaria mycotoxins and other xenobiotics of food
origin: current scenario and future perspectives. Toxins (Basel) 11:640
da Silva KRA, Salles JF, Seldin L, van Elsas JD (2003) Application of a novel Paenibacillus-
specic PCR-DGGE method and sequence analysis to assess the diversity of Paenibacillus spp.
in the maize rhizosphere. J Microbiol Methods 54:213–231
de Moraes Pontes JG, Fernandes LS, Dos Santos RV, Tasic L, Fill TP (2020) Virulence factors in
the phytopathogen–host interactions: an overview. J Agric Food Chem 68:7555–7570
de Weert S, Vermeiren H, Mulders IHM, Kuiper I, Hendrickx N, Bloemberg GV, Vanderleyden J,
De Mot R, Lugtenberg BJJ (2002) Flagella-driven chemotaxis towards exudate components
is an important trait for tomato root colonization by Pseudomonas uorescens. Mol Plant-
Microbe Interact 15:1173–1180
Daryaei A, Jones EE, Glare TR, Falloon RE (2016) pH and water activity in culture media affect
biological control activity of Trichoderma atroviride against Rhizoctonia solani. Biol Control
92:24–30
M. M. El-Metwally etal.
401
Davidsson PR, Kariola T, Niemi O, Palva ET (2013) Pathogenicity of and plant immunity to soft
rot pectobacteria. Front Plant Sci 4:191
Dawande AY, Gajbhiye ND, Charde VN, Banginwar YS (2019) Assessment of endophytic fungal
isolates for its Antibiolm activity on Pseudomonas aeruginosa. Int J Sci Res Biol Sci Vol 6:3
Do QT (2022) Antagonistic activities of endophytic bacteria isolated from rice roots against the
fungus Magnaporthe oryzae, a causal of rice blast disease. Egypt J Biol Pest Control 32:1–11
Dong Y-H, Wang L-H, Zhang L-H (2007) Quorum-quenching microbial infections: mechanisms
and implications. Philos Trans R Soc B Biol Sci 362:1201–1211
Dridi B, Raoult D, Drancourt M (2011) Archaea as emerging organisms in complex human micro-
biomes. Anaerobe 17:56–63
Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E,
Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP (2011) Trichoderma: the genomics of
opportunistic success. Nat Rev Microbiol 9:749–759
Duneld KE, Germida JJ (2003) Seasonal changes in the rhizosphere microbial communities asso-
ciated with eld-grown genetically modied canola (Brassica napus). Appl Environ Microbiol
69:7310–7318
Durbin RD, Uchytil TF (1977) A survey of plant insensitivity to tentoxin. Phytopathology
67:602–603
Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209
Ek-Ramos MJ, Zhou W, Valencia CU, Antwi JB, Kalns LL, Morgan GD, Kerns DL, Sword GA
(2013) Spatial and temporal variation in fungal endophyte communities isolated from culti-
vated cotton (Gossypium hirsutum). PLoS One 8:e66049
Elad Y (2000) Biological control of foliar pathogens by means of Trichoderma harzianum and
potential modes of action. Crop Prot 19:709–714
El-Halmouch Y, Benharrat H, Thalouarn P (2006) Effect of root exudates from different tomato
genotypes on broomrape (O. aegyptiaca) seed germination and tubercle development. Crop
Prot 25:501–507
Escrivá L, Oueslati S, Font G, Manyes L (2017) Alternaria mycotoxins in food and feed: an over-
view. J Food Qual 2017
Estrada C, Wcislo WT, Van Bael SA (2013) Symbiotic fungi alter plant chemistry that discourages
leaf-cutting ants. New Phytol 198:241–251
Eydoux L, Farrer EC (2020) Does salinity affect lifestyle switching in the plant pathogen Fusarium
solani? Access Microbiol 2
Fávaro LCDL, Sebastianes FLDS, Araújo WL (2012) Epicoccum nigrum P16, a sugarcane endo-
phyte, produces antifungal compounds and induces root growth. PLoS One 7:e36826
Favre-Godal Q, Gourguillon L, Lordel-Madeleine S, Gindro K, Choisy P (2020) Orchids and their
mycorrhizal fungi: an insufciently explored relationship. Mycorrhiza 30:5–22
Feng H, Zhang N, Du W, Zhang H, Liu Y, Fu R, Shao J, Zhang G, Shen Q, Zhang R (2018)
Identication of chemotaxis compounds in root exudates and their sensing chemoreceptors in
plant-growth-promoting rhizobacteria Bacillus amyloliquefaciens SQR9. Mol Plant-Microbe
Interact 31:995–1005
Ferreira LDEVM, De Carvalho F, Andrade JFC, Oliveira DP, De Medeiros FHV, Moreira FMDES
(2020) Co-inoculation of selected nodule endophytic rhizobacterial strains with Rhizobium
tropici promotes plant growth and controls damping off in common bean. Pedosphere
30:98–108
Fesel PH, Zuccaro A (2016) Dissecting endophytic lifestyle along the parasitism/mutualism con-
tinuum in Arabidopsis. Curr Opin Microbiol 32:103–112
Figueroa M, Jarmusch AK, Raja HA, El-Elimat T, Kavanaugh JS, Horswill AR, Cooks RG, Cech
NB, Oberlies NH (2014) Polyhydroxyanthraquinones as quorum sensing inhibitors from the
guttates of Penicillium restrictum and their analysis by desorption electrospray ionization mass
spectrometry. J Nat Prod 77:1351–1358
Fitzpatrick CR, Salas-González I, Conway JM, Finkel OM, Gilbert S, Russ D, Teixeira PJPL,
Dangl JL (2020) The plant microbiome: from ecology to reductionism and beyond. Annu Rev
Microbiol 74:81–100
Symbiotic Relationships withFungi: FromMutualism toParasitism
402
Foo E, Yoneyama K, Hugill CJ, Quittenden LJ, Reid JB (2013) Strigolactones and the regulation of
pea symbioses in response to nitrate and phosphate deciency. Mol Plant 6:76–87
Formey D, Sallet E, Lelandais-Brière C, Ben C, Bustos-Sanmamed P, Niebel A, Frugier F, Combier
JP, Debellé F, Hartmann C (2014) The small RNA diversity from Medicago truncatularoots
under biotic interactions evidences the environmental plasticity of the miRNAome. Genome
Biol 15:1–21
Freeman S, Horowitz S, Sharon A (2001) Pathogenic and nonpathogenic lifestyles in Colletotrichum
acutatum from strawberry and other plants. Phytopathology 91:986–992
Fuqua C, Parsek MR, Greenberg EP (2001) Regulation of gene expression by cell-to-cell commu-
nication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35:439
Ganie SA, Ahammed GJ (2021) Dynamics of cell wall structure and related genomic resources for
drought tolerance in rice. Plant Cell Rep 40:437–459
Ghosh S, Chowdhury R, Bhattacharya P (2016) Mixed consortia in bioprocesses: role of microbial
interactions. Appl Microbiol Biotechnol 100:4283–4295
Glaeser SP, Imani J, Alabid I, Guo H, Kumar N, Kämpfer P, Hardt M, Blom J, Goesmann A,
Rothballer M (2016) Non-pathogenic Rhizobium radiobacter F4 deploys plant benecial activ-
ity independent of its host Piriformospora indica. ISME J 10:871–884
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic
pathogens. Annu Rev Phytopathol 43:205
Gori K, Knudsen PB, Nielsen KF, Arneborg N, Jespersen L (2011) Alcohol-based quorum sensing
plays a role in adhesion and sliding motility of the yeast D ebaryomyces hansenii. FEMS Yeast
Res 11:643–652
Guo B, Wang Y, Sun X, Tang K (2008) Bioactive natural products from endophytes: a review. Appl
Biochem Microbiol 44:136–142
Guo H, Ma A, Zhao G, Yun J, Liu X, Zhang H, Zhuang G (2011) Effect of farnesol on Penicillium
decumbens’s morphology and cellulase production. Bioresources 6:3252–3259
Guo Y, Matsuoka Y, Miura T, Nishizawa T, Ohta H, Narisawa K (2018) Complete genome
sequence of Agrobacterium pusense VsBac-Y9, a bacterial symbiont of the dark septate endo-
phytic fungus Veronaeopsis simplex Y34 with potential for improving fungal colonization in
roots. J Biotechnol 284:31–36
Gupta S, Chaturvedi P (2019) Enhancing secondary metabolite production in medicinal plants
using endophytic elicitors: a case study of Centella asiatica (Apiaceae) and asiaticoside.
Endophytes Grow World:310–323
Guttman DS, McHardy AC, Schulze-Lefert P (2014) Microbial genome-enabled insights into
plant–microorganism interactions. Nat Rev Genet 15:797–813
Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agri-
cultural crops. Can J Microbiol 43:895–914
Harbort CJ, Hashimoto M, Inoue H, Niu Y, Guan R, Rombolà AD, Kopriva S, Voges MJ, Sattely
ES, Garrido-Oter R (2020) Root-secreted coumarins and the microbiota interact to improve
iron nutrition in Arabidopsis. Cell Host Microbe 28:825–837
Harrison MJ (1998) Development of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol
1:360–365
Harrower JT, Gilbert GS (2021) Parasitism to mutualism continuum for Joshua trees inoculated
with different communities of arbuscular mycorrhizal fungi from a desert elevation gradient.
PLoS One 16:e0256068
Hartmann A, Rothballer M, Hense BA, Schröder P (2014) Bacterial quorum sensing compounds
are important modulators of microbe-plant interactions. Front Plant Sci 5:131
Haryani Y, Hilma R, Delra N, Martalinda T, Puspita F, Friska A, Juwita D, Farniga A, Ardi F
(2020) Antibacterial activity of Achromobacter sp. and Bacillus sp., bacterial endophytes
derived from Mangrove Ceriops tagal (Perr.) CB Robb. In: IOP conference series: materials
science and engineering. IOP Publishing, p12013
Hata K, Futai K (1993) Effect of needle aging on the total colonization rates of endophytic fungi
on Pinus thunbergii and Pinus densiora needles. J Jpn For Soc 75:338–341
M. M. El-Metwally etal.
403
Hedden P, Sponsel V (2015) A century of gibberellin research. J Plant Growth Regul 34:740–760
Heiniger U, Rigling D (1994) Biological control of chestnut blight in Europe. Annu Rev
Phytopathol 32:581–599
Hernandez D, Kiesewetter KN, Palakurty S, Stinchcombe JR, Afkhami ME (2019) Synergism
and symbioses: unpacking complex mutualistic species interactions using transcriptomic
approaches. Model Legum Medicago truncatula:1045–1054
Heungens K, Parke J (2000) Zoospore homing and infection events: effects of the biocontrol bacte-
rium Burkholderia cepacia AMMDR1 on two oomycete pathogens of pea (Pisum sativum L.).
Appl Environ Microbiol 66:5192–5200
Hoffman MT, Gunatilaka MK, Wijeratne K, Gunatilaka L, Arnold AE (2013) Endohyphal bac-
terium enhances production of indole-3-acetic acid by a foliar fungal endophyte. PLoS One
8:e73132
Hogan DA (2006) Quorum sensing: alcohols in a social situation. Curr Biol 16:R457–R458
Hong K-W, Koh C-L, Sam C-K, Yin W-F, Chan K-G (2012) Quorum quenching revisited– from
signal decays to signalling confusion. Sensors 12:4661–4696
Hornby JM, Jensen EC, Lisec AD, Tasto JJ, Jahnke B, Shoemaker R, Dussault P, Nickerson KW
(2001) Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol.
Appl Environ Microbiol 67:2982–2992
Hou D, Wang R, Gao X, Wang K, Lin Z, Ge J, Liu T, Wei S, Chen W, Xie R (2018) Cultivar-
specic response of bacterial community to cadmium contamination in the rhizosphere of rice
(Oryza sativa L.). Environ Pollut 241:63–73
Hou S, Thiergart T, Vannier N, Mesny F, Ziegler J, Pickel B, Hacquard S (2020) Microbiota-root-
shoot axis modulation by MYC2 favours Arabidopsis growth over defence under suboptimal
light. bioRxiv
Houterman PM, Cornelissen BJC, Rep M (2008) Suppression of plant resistance gene-based
immunity by a fungal effector. PLoS Pathog 4:e1000061
Houterman PM, Ma L, Van Ooijen G, De Vroomen MJ, Cornelissen BJC, Takken FLW, Rep M
(2009) The effector protein Avr2 of the xylem-colonizing fungus Fusarium oxysporum acti-
vates the tomato resistance protein I-2 intracellularly. Plant J 58:970–978
Hsueh Y-P, Mahanti P, Schroeder FC, Sternberg PW (2013) Nematode-trapping fungi eavesdrop
on nematode pheromones. Curr Biol 23:83–86
Hsueh Y-P, Gronquist MR, Schwarz EM, Nath RD, Lee C-H, Gharib S, Schroeder FC, Sternberg
PW (2017) Nematophagous fungus Arthrobotrys oligospora mimics olfactory cues of sex and
food to lure its nematode prey. Elife 6
Hu L, Robert CAM, Cadot S, Zhang XI, Ye M, Li B, Manzo D, Chervet N, Steinger T, Van Der
Heijden MGA (2018) Root exudate metabolites drive plant-soil feedbacks on growth and
defense by shaping the rhizosphere microbiota. Nat Commun 9:1–13
Huang AC, Jiang T, Liu Y-X, Bai Y-C, Reed J, Qu B, Goossens A, Nützmann H-W, Bai Y, Osbourn
A (2019) A specialized metabolic network selectively modulates Arabidopsis root microbiota.
Science (80–) 364:eaau6389
Hückelhoven R (2005) Powdery mildew susceptibility and biotrophic infection strategies. FEMS
Microbiol Lett 245:9–17
Hughes DT, Sperandio V (2008) Inter-kingdom signalling: communication between bacteria and
their hosts. Nat Rev Microbiol 6:111–120
Islam MM, Hossain DM, Nonaka M, Harada N (2017) Biological control of tomato collar rot
induced by Sclerotium rolfsii using Trichoderma species isolated in Bangladesh. Arch
Phytopathol Plant Prot 50:109–116
Ismail AS, Valastyan JS, Bassler BL (2016) A host-produced autoinducer-2 mimic activates bacte-
rial quorum sensing. Cell Host Microbe 19:470–480
İnceoğlu Ö, Salles JF, van Overbeek L, van Elsas JD (2010) Effects of plant genotype and growth
stage on the betaproteobacterial communities associated with different potato cultivars in two
elds. Appl Environ Microbiol 76:3675–3684
Symbiotic Relationships withFungi: FromMutualism toParasitism
404
Jacoby RP, Koprivova A, Kopriva S (2021) Pinpointing secondary metabolites that shape the com-
position and function of the plant microbiome. J Exp Bot 72:57–69
Jakupović M, Heintz M, Reichmann P, Mendgen K, Hahn M (2006) Microarray analysis of
expressed sequence tags from haustoria of the rust fungus Uromyces fabae. Fungal Genet
Biol 43:8–19
Javed N, Khan HU, Hussain Z, Ashfaq M (2002) Effect of temperature, soil pH, agitation inter-
vals and soil types on the spore attachment of Pasteuria penetrans to root knot nematodes,
Meloidogyne javanica. Plant Pathol J
Jia M, Chen L, Xin H-L, Zheng C-J, Rahman K, Han T, Qin L-P (2016) A friendly relationship
between endophytic fungi and medicinal plants: a systematic review. Front Microbiol 7:906
Joshi JR, Burdman S, Lipsky A, Yariv S, Yedidia I (2016) Plant phenolic acids affect the virulence
of P ectobacterium aroidearum and P. carotovorum ssp. brasiliense via quorum sensing regula-
tion. Mol Plant Pathol 17:487–500
Jouanneau J-P, Lapous D, Guern J (1991) In plant protoplasts, the spontaneous expression of
defense reactions and the responsiveness to exogenous elicitors are under auxin control. Plant
Physiol 96:459–466
Kanzaki H, Yoshida K, Saitoh H, Fujisaki K, Hirabuchi A, Alaux L, Fournier E, Tharreau D,
Terauchi R (2012) Arms race co-evolution of Magnaporthe oryzae AVR-Pik and rice Pik genes
driven by their physical interactions. Plant J 72:894–907
Khare E, Mishra J, Arora NK (2018) Multifaceted interactions between endophytes and plant:
developments and prospects. Front Microbiol 9:2732
Kim W, Chen W (2019) Phytotoxic metabolites produced by legume-associated Ascochyta and its
related genera in the Dothideomycetes. Toxins (Basel) 11:627
Kim H-S, Park H-D (2013) Ginger extract inhibits biolm formation by Pseudomonas aeruginosa
PA14. PLoS One 8:e76106
Ko D, Helariutta Y (2017) Shoot–root communication in owering plants. Curr Biol 27:R973–R978
Kobayashi DY, Crouch JA (2009) Bacterial/fungal interactions: from pathogens to mutualistic
endosymbionts. Annu Rev Phytopathol 47:63–82
Koh KH, Tham F-Y (2011) Screening of traditional Chinese medicinal plants for quorum-sensing
inhibitors activity. J Microbiol Immunol Infect 44:144–148
Komon-Zelazowska M, Bissett J, Zafari D, Hatvani L, Manczinger L, Woo S, Lorito M, Kredics
L, Kubicek CP, Druzhinina IS (2007) Genetically closely related but phenotypically divergent
Trichoderma species cause green mold disease in oyster mushroom farms worldwide. Appl
Environ Microbiol 73:7415–7426
Kumar AS, Lakshmanan V, Caplan JL, Powell D, Czymmek KJ, Levia DF, Bais HP (2012)
Rhizobacteria Bacillus subtilis restricts foliar pathogen entry through stomata. Plant J
72:694–706
Kusari S, Hertweck C, Spiteller M (2012) Chemical ecology of endophytic fungi: origins of sec-
ondary metabolites. Chem Biol 19:792–798
Kusari P, Kusari S, Lamshöft M, Sezgin S, Spiteller M, Kayser O (2014) Quorum quenching
is an antivirulence strategy employed by endophytic bacteria. Appl Microbiol Biotechnol
98:7173–7183
Kusari P, Kusari S, Spiteller M, Kayser O (2015) Implications of endophyte-plant crosstalk in
light of quorum responses for plant biotechnology. Appl Microbiol Biotechnol 99:5383–5390
Ladha JK, Reddy PM (2003) Nitrogen xation in rice systems: state of knowledge and future
prospects. Plant Soil 252:151–167
LaSarre B, Federle MJ (2013) Exploiting quorum sensing to confuse bacterial pathogens.
Microbiol Mol Biol Rev 77:73–111
Latz E, Eisenhauer N, Rall BC, Scheu S, Jousset A (2016) Unravelling linkages between plant
community composition and the pathogen-suppressive potential of soils. Sci Rep 6:1–10
Lebeis SL (2014) The potential for give and take in plant–microbiome relationships. Front Plant
Sci 5:287
M. M. El-Metwally etal.
405
Lee H, Chang YC, Nardone G, Kwon-Chung KJ (2007) TUP1 disruption in Cryptococcus neofor-
mans uncovers a peptide-mediated density-dependent growth phenomenon that mimics quo-
rum sensing. Mol Microbiol 64:591–601
Leung TLF, Poulin R (2008) Parasitism, commensalism, and mutualism: exploring the many
shades of symbioses. Vie Milieu/Life Environ:107–115
Levy A, Chang BJ, Abbott LK, Kuo J, Harnett G, Inglis TJJ (2003) Invasion of spores of the arbus-
cular mycorrhizal fungus Gigaspora decipiens by Burkholderia spp. Appl Environ Microbiol
69:6250–6256
Li G, Kusari S, Golz C, Laatsch H, Strohmann C, Spiteller M (2017) Epigenetic modulation
of endophytic Eupenicillium sp. LG41 by a histone deacetylase inhibitor for production of
decalin- containing compounds. J Nat Prod 80:983–988
Lim FY, Sanchez JF, Wang CCC, Keller NP (2012) Toward awakening cryptic secondary metabo-
lite gene clusters in lamentous fungi. In: Methods in enzymology. Elsevier, pp303–324
Ling N, Raza W, Ma J, Huang Q, Shen Q (2011) Identication and role of organic acids in water-
melon root exudates for recruiting Paenibacillus polymyxa SQR-21in the rhizosphere. Eur J
Soil Biol 47:374–379
Liu S, Dai H, Orfali RS, Lin W, Liu Z, Proksch P (2016) New fusaric acid derivatives from the
endophytic fungus Fusarium oxysporum and their phytotoxicity to barley leaves. J Agric Food
Chem 64:3127–3132
Liu Y, Chen L, Wu G, Feng H, Zhang G, Shen Q, Zhang R (2017) Identication of root-secreted
compounds involved in the communication between cucumber, the benecial Bacillus amylo-
liquefaciens, and the soil-borne pathogen Fusarium oxysporum. Mol Plant-Microbe Interact
30:53–62
Liu C, Atanasov KE, Arafaty N, Murillo E, Tiburcio AF, Zeier J, Alcázar R (2020) Putrescine
elicits ROS-dependent activation of the salicylic acid pathway in Arabidopsis thaliana. Plant
Cell Environ 43:2755–2768
Lo Presti L, Lanver D, Schweizer G, Tanaka S, Liang L, Tollot M, Zuccaro A, Reissmann S,
Kahmann R (2015) Fungal effectors and plant susceptibility. Annu Rev Plant Biol 66:513–545
Logrieco A, Bottalico A, Mulé G, Moretti A, Perrone G (2003) Epidemiology of toxigenic fungi
and their associated mycotoxins for some Mediterranean crops. In: Epidemiology of myco-
toxin producing fungi. Springer, pp645–667
Logrieco A, Moretti A, Solfrizzo M (2009) Alternaria toxins and plant diseases: an overview of
origin, occurrence and risks. World Mycotoxin J 2:129–140
Lòpez-Fernàndez S, Sonego P, Moretto M, Pancher M, Engelen K, Pertot I, Campisano A (2015)
Whole-genome comparative analysis of virulence genes unveils similarities and differences
between endophytes and other symbiotic bacteria. Front Microbiol 6:419
Lozano-Torres JL, Wilbers RHP, Gawronski P, Boshoven JC, Finkers-Tomczak A, Cordewener
JHG, America AHP, Overmars HA, Van ‘t Klooster JW, Baranowski L (2012) Dual disease
resistance mediated by the immune receptor Cf-2in tomato requires a common virulence target
of a fungus and a nematode. Proc Natl Acad Sci 109:10119–10124
Lubna AS, Hamayun M, Gul H, Lee I-J, Hussain A (2018) Aspergillus niger CSR3 regulates plant
endogenous hormones and secondary metabolites by producing gibberellins and indoleacetic
acid. J Plant Interact 13:100–111
Ludwig-Müller J (2015) Plants and endophytes: equal partners in secondary metabolite produc-
tion? Biotechnol Lett 37:1325–1334
Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J,
Engelbrektson A, Kunin V, del Rio TG (2012) Dening the core Arabidopsis thaliana root
microbiome. Nature 488:86–90
MacDonald RM, Chandler MR (1981) Bacterium-like organelles in the vesicular-arbuscular
mycorrhizal fungus Glomus caledonius. New Phytol 89:241–246
Machida K, Tanaka T, Yano Y, Otani S, Taniguchi M (1999) Farnesol-induced growth inhibition in
Saccharomyces cerevisiae by a cell cycle mechanism. Microbiology 145:293–299
Symbiotic Relationships withFungi: FromMutualism toParasitism
406
Macko V, Stimmel MB, Wolpert TJ, Dunkle LD, Acklin W, Bänteli R, Jaun B, Arigoni D (1992)
Structure of the host-specic toxins produced by the fungal pathogen Periconia circinata. Proc
Natl Acad Sci 89:9574–9578
Mandyam KG, Jumpponen A (2015) Mutualism–parasitism paradigm synthesized from results of
root-endophyte models. Front Microbiol 5:776
Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ (2007) A virus in a fungus in a plant:
three-way symbiosis required for thermal tolerance. Science (80–) 315:513–515
Marra M, Camoni L, Visconti S, Fiorillo A, Evidente A (2021) The surprising story of fusi-
coccin: a wilt-inducing phytotoxin, a tool in plant physiology and a 14-3-3-targeted drug.
Biomolecules 11:1393
Martin FN, Loper JE (1999) Soilborne plant diseases caused by Pythium spp.: ecology, epidemiol-
ogy, and prospects for biological control. CRC Crit Rev Plant Sci 18:111–181
Martínez-Medina A, Del Mar AM, Pascual JA, Van Wees S (2014) Phytohormone proles induced
by Trichoderma isolates correspond with their biocontrol and plant growth-promoting activity
on melon plants. J Chem Ecol 40:804–815
Martín-Rodríguez AJ, Reyes F, Martín J, Pérez-Yépez J, León-Barrios M, Couttolenc A, Espinoza
C, Trigos Á, Martín VS, Norte M (2014) Inhibition of bacterial quorum sensing by extracts
from aquatic fungi: rst report from marine endophytes. Mar Drugs 12:5503–5526
Masi M, Cimmino A, Reveglia P, Mugnai L, Surico G, Evidente A (2018) Advances on fungal
phytotoxins and their role in grapevine trunk diseases. J Agric Food Chem 66:5948–5958
Mattoo AJ, Nonzom S (2021) Endophytic fungi: understanding complex cross-talks. Symbiosis
83:237–264
McLean M (1996) The phytotoxicity ofFusarium metabolites: an update since 1989.
Mycopathologia 133:163–179
Meena M, Samal S (2019) Alternaria host-specic (HSTs) toxins: an overview of chemical charac-
terization, target sites, regulation and their toxic effects. Toxicol Rep 6:745–758
Meena H, Mishra R, Ranganathan S, Sarma VV, Ampasala DR, Kalia VC, Lee J-K, Siddhardha B
(2020) Phomopsis tersa as inhibitor of quorum sensing system and biolm forming ability of
Pseudomonas aeruginosa. Indian J Microbiol 60:70–77
Mendes R, Kruijt M, De Bruijn I, Dekkers E, Van Der Voort M, Schneider JHM, Piceno YM,
DeSantis TZ, Andersen GL, Bakker PAHM (2011) Deciphering the rhizosphere microbiome
for disease-suppressive bacteria. Science (80–) 332:1097–1100
Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: signicance of plant
benecial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev
37:634–663
Meng S, Torto-Alalibo T, Chibucos MC, Tyler BM, Dean RA (2009) Common processes in patho-
genesis by fungal and oomycete plant pathogens, described with Gene Ontology terms. BMC
Microbiol 9:1–11
Micali C, Göllner K, Humphry M, Consonni C, Panstruga R (2008) The powdery mildew disease
of Arabidopsis: a paradigm for the interaction between plants and biotrophic fungi. Arab Book/
Am Soc Plant Biol 6
Micallef SA, Shiaris MP, Colón-Carmona A (2009) Inuence of Arabidopsis thaliana accessions
on rhizobacterial communities and natural variation in root exudates. J Exp Bot 60:1729–1742
Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199
Mishra R, Kushveer JS, Majumder D, Sarma VV (2020) Stimulation of secondary metabolite pro-
duction in Hypoxylon anthochroum by naturally occurring epigenetic modiers. J Food Meas
Charact 14:946–962
Mochimaru M, Sakurai H (1997) Three kinds of binding site for tentoxin on isolated chloroplast
coupling factor 1. FEBS Lett 419:23–26
Morimoto N, Ueno K, Teraishi M, Okumoto Y, Mori N, Ishihara A (2018) Induced phenylamide
accumulation in response to pathogen infection and hormone treatment in rice (Oryza sativa).
Biosci Biotechnol Biochem 82:407–416
M. M. El-Metwally etal.
407
Naga NG, El-Badan DE-S, Rateb HS, Ghanem KM, Shaaban MI (2021) Quorum sensing inhibit-
ing activity of cefoperazone and its metallic derivatives on Pseudomonas aeruginosa. Front
Cell Infect Microbiol 945
Naga NG, Zaki AA, El-Badan DE, Rateb HS, Ghanem KM, Shaaban MI (2022) Methoxyisoavan
derivative from Trigonella stellata inhibited quorum sensing and virulence factors of
Pseudomonas aeruginosa. World J Microbiol Biotechnol 38:1–13
Natrah FMI, Defoirdt T, Sorgeloos P, Bossier P (2011) Disruption of bacterial cell-to-cell com-
munication by marine organisms and its relevance to aquaculture. Mar Biotechnol 13:109–126
Neal AL, Ahmad S, Gordon-Weeks R, Ton J (2012) Benzoxazinoids in root exudates of maize
attract Pseudomonas putida to the rhizosphere. PLoS One 7:e35498
Nealson KH, Hastings JW (1979) Bacterial bioluminescence: its control and ecological signi-
cance. Microbiol Rev 43:496–518
Nelson EB (1991) Exudate molecules initiating fungal responses to seeds and roots. In: The rhizo-
sphere and plant growth. Springer, pp197–209
Newman AG, Townsend CA (2016) Molecular characterization of the cercosporin biosynthetic
pathway in the fungal plant pathogen Cercospora nicotianae. J Am Chem Soc 138:4219–4228
Noelting MC, Sisterna M, Lovisolo M, Molla-Kralj A, Lori G, Sandoval MC, Sulyok M, Molina
MC (2016) Discoloured seeds of amaranth plant infected by Alternaria alternata: physiologi-
cal, histopathological alterations and fungal secondary metabolites associated or registered. J
Plant Prot Res 56:244–249
Noelting MC, Sisterna MN, Sulyok M, Abbiati NN, Molina MC (2022) Damage caused by
Alternaria alternata to the quality and germination of amaranth seeds. Eur J Plant Pathol
163:193–202
Nühse TS (2012) Cell wall integrity signaling and innate immunity in plants. Front Plant Sci 3:280
Nzungize JR, Lyumugabe F, Busogoro J-P, Baudoin J-P (2012) Pythium root rot of common bean:
biology and control methods. A review. Biotech Agron Soc Environ 16:405–413
Ochoa-Meza LC, Quintana-Obregón EA, Vargas-Arispuro I, Falcón-Rodríguez AB, Aispuro-
Hernández E, Virgen-Ortiz JJ, Martínez-Téllez MÁ (2021) Oligosaccharins as elicitors of
defense responses in wheat. Polymers (Basel) 13:3105
Ofek M, Hadar Y, Minz D (2011) Colonization of cucumber seeds by bacteria during germination.
Environ Microbiol 13:2794–2807
Oh S-Y, Kim M, Eimes JA, Lim YW (2018) Effect of fruiting body bacteria on the growth of
Tricholoma matsutake and its related molds. PLoS One 13:e0190948
Oka K, Okubo A, Kodama M, Otani H (2006) Detoxication of α-tomatine by tomato pathogens
Alternaria alternata tomato pathotype and Corynespora cassiicola and its role in infection. J
Gen plant Pathol 72:152–158
Oldroyd GED, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume-
rhizobial symbiosis. Annu Rev Genet 45:119–144
Oliva R, Win J, Raffaele S, Boutemy L, Bozkurt TO, Chaparro-Garcia A, Segretin ME, Stam R,
Schornack S, Cano LM (2010) Recent developments in effector biology of lamentous plant
pathogens. Cell Microbiol 12:705–715
Oliver RP, Solomon PS (2010) New developments in pathogenicity and virulence of necrotrophs.
Curr Opin Plant Biol 13:415–419
Ostry V (2008) Alternaria mycotoxins: an overview of chemical characterization, producers, toxic-
ity, analysis and occurrence in foodstuffs. World Mycotoxin J 1:175–188
Ota R, Ohkubo Y, Yamashita Y, Ogawa-Ohnishi M, Matsubayashi Y (2020) Shoot-to-root mobile
CEPD-like 2 integrates shoot nitrogen status to systemically regulate nitrate uptake in
Arabidopsis. Nat Commun 11:1–9
Pakvaz S, Soltani J (2016) Endohyphal bacteria from fungal endophytes of the Mediterranean
cypress (Cupressus sempervirens) exhibit invitro bioactivity. For Pathol 46:569–581
Pandey P, Irulappan V, Bagavathiannan MV, Senthil-Kumar M (2017) Impact of combined abiotic
and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-
morphological traits. Front Plant Sci 8:537
Symbiotic Relationships withFungi: FromMutualism toParasitism
408
Pastrana AM, Basallote-Ureba MJ, Aguado A, Akdi K, Capote N (2016) Biological control of
strawberry soil-borne pathogens Macrophomina phaseolina and Fusarium solani, using
Trichoderma asperellum and Bacillus spp. Phytopathol Mediterr:109–120
Patel ZM, Mahapatra R, Jampala SSM (2020) Role of fungal elicitors in plant defense mechanism.
In: Molecular aspects of plant benecial microbes in agriculture. Elsevier, pp143–158
Paul NC, Deng JX, Sang H-K, Choi Y-P, Yu S-H (2012) Distribution and antifungal activity of
endophytic fungi in different growth stages of chili pepper (Capsicum annuum L.) in Korea.
Plant Pathol J 28:10–19
Pavón Moreno MÁ, Alonso G, Martin de Santos R (2012) The importance of genus Alternaria in
mycotoxins production and human diseases. Nutr Hosp 27:1772–1781
Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler ES, Ley RE (2013) Diversity
and heritability of the maize rhizosphere microbiome under eld conditions. Proc Natl Acad
Sci 110:6548–6553
Peng D-H, Qiu D-W, Ruan L-F, Zhou C-F, Sun M (2011) Protein elicitor PemG1 from Magnaporthe
grisea induces systemic acquired resistance (SAR) in plants. Mol Plant-Microbe Interact
24:1239–1246
Pérez-Montaño F, Jiménez-Guerrero I, Sánchez-Matamoros RC, López-Baena FJ, Ollero FJ,
Rodríguez-Carvajal MA, Bellogín RA, Espuny MR (2013) Rice and bean AHL-mimic quorum-
sensing signals specically interfere with the capacity to form biolms by plant-associated
bacteria. Res Microbiol 164:749–760
Pero RW, Harvan D, Blois MC (1973) Isolation of the toxin, altenuisol, from the fungus, Alternaria
tenuis Auct. Tetrahedron Lett 14:945–948
Peter AE, Sudhakar P, Sandeep B V, Rao BG (2019) Antimicrobial and anti-quorum sensing activi-
ties of medicinal plants. In: Implication of quorum sensing and biolm formation in medicine,
agriculture and food industry. Springer, pp189–217
Pineda A, Kaplan I, Hannula SE, Ghanem W, Bezemer TM (2020) Conditioning the soil micro-
biome through plant–soil feedbacks suppresses an aboveground insect pest. New Phytol
226:595–608
Prakash S (2011) Bio-control and plant growth promotion potential of siderophore producing
endophytic Streptomyces from Azadirachta indica A.Juss. J Basic Microbiol 51(5):550–556
Quecine MC, de Araújo WL, Tsui S, Parra JRP, de Azevedo JL, Pizzirani-Kleiner AA (2014)
Control of Diatraea saccharalis by the endophytic Pantoea agglomerans 33.1 expressing
cry1Ac7. Arch Microbiol 196:227–234
Rai M, Agarkar G (2016) Plant–fungal interactions: what triggers the fungi to switch among life-
styles? Crit Rev Microbiol 42:428–438
Raina S, Odell M, Keshavarz T (2010) Quorum sensing as a method for improving sclerotiorin
production in Penicillium sclerotiorum. J Biotechnol 148:91–98
Raina S, De Vizio D, Palonen EK, Odell M, Brandt AM, Soini JT, Keshavarz T (2012) Is quo-
rum sensing involved in lovastatin production in the lamentous fungus Aspergillus terreus?
Process Biochem 47:843–852
Rajesh PS, Rai VR (2013) Hydrolytic enzymes and quorum sensing inhibitors from endophytic
fungi of Ventilago madraspatana Gaertn. Biocatal Agric Biotechnol 2:120–124
Rajesh PS, Rai VR (2014) Molecular identication of aiiA homologous gene from endophytic
Enterobacter species and in silico analysis of putative tertiary structure of AHL-lactonase.
Biochem Biophys Res Commun 443:290–295
Ramirez-Estrada K, Vidal-Limon H, Hidalgo D, Moyano E, Golenioswki M, Cusidó RM, Palazon
J (2016) Elicitation, an effective strategy for the biotechnological production of bioactive high-
added value compounds in plant cell factories. Molecules 21:182
Rana KL, Kour D, Sheikh I, Dhiman A, Yadav N, Yadav AN, Rastegari AA, Singh K, Saxena AK
(2019) Endophytic fungi: biodiversity, ecological signicance, and potential industrial applica-
tions. In: Recent advancement in white biotechnology through fungi. Springer, pp1–62
Rashmi M, Meena H, Meena C, Kushveer JS, Busi S, Murali A, Sarma VV (2018) Anti-quorum
sensing and antibiolm potential of Alternaria alternata, a foliar endophyte of Carica papaya,
evidenced by QS assays and in-silico analysis. Fungal Biol 122:998–1012
M. M. El-Metwally etal.
409
Redman RS, Dunigan DD, Rodriguez RJ (2001) Fungal symbiosis from mutualism to parasitism:
who controls the outcome, host or invader? New Phytol 151:705–716
Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance gener-
ated by plant/fungal symbiosis. Science (80–) 298:1581
Rigling D, Prospero S (2018) Cryphonectria parasitica, the causal agent of chestnut blight: inva-
sion history, population biology and disease control. Mol Plant Pathol 19:7–20
Rines HW, Luke HH (1985) Selection and regeneration of toxin-insensitive plants from tissue
cultures of oats (Avena sativa) susceptible to Helminthosporium victoriae. Theor Appl Genet
71:16–21
Rizwan M, Ali S, Adrees M, Rizvi H, Zia-ur-Rehman M, Hannan F, Qayyum MF, Hafeez F, Ok YS
(2016) Cadmium stress in rice: toxic effects, tolerance mechanisms, and management: a critical
review. Environ Sci Pollut Res 23:17859–17879
Roca MG, Arlt J, Jeffree CE, Read ND (2005) Cell biology of conidial anastomosis tubes in
Neurospora crassa. Eukaryot Cell 4:911–919
Rodriguez R, Redman R (2008) More than 400 million years of evolution and some plants still
can’t make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 59:1109–1114
Rodriguez RJ, Roossinck M (2012) Viruses, fungi and plants: cross-kingdom communication and
mutualism. In: Biocommunication of fungi. Springer, pp219–227
Rowland O, Ludwig AA, Merrick CJ, Baillieul F, Tracy FE, Durrant WE, Fritz-Laylin L, Nekrasov
V, Sjölander K, Yoshioka H (2005) Functional analysis of Avr9/Cf-9 rapidly elicited genes
identies a protein kinase, ACIK1, that is essential for full Cf-9–dependent disease resistance
in tomato. Plant Cell 17:295–310
Rouxel T, Balesdent MH (2017) Life, death and rebirth of avirulence effectors in a fungal pathogen
of Brassica crops, L eptosphaeria maculans. New Phytologist, 214(2): 526–532
Sabra M, Aboulnasr A, Franken P, Perreca E, Wright LP, Camehl I (2018) Benecial root endo-
phytic fungi increase growth and quality parameters of sweet basil in heavy metal contami-
nated soil. Front Plant Sci 9:1726
Safari M, Amache R, Esmaeilishirazifard E, Keshavarz T (2014) Microbial metabolism of
quorum- sensing molecules acyl-homoserine lactones, γ-heptalactone and other lactones. Appl
Microbiol Biotechnol 98:3401–3412
Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of inter-
actions with host plants. Annu Rev Ecol Syst:319–343
Sák M, Dokupilová I, Kaňuková Š, Mrkvová M, Mihálik D, Hauptvogel P, Kraic J (2021) Biotic
and abiotic elicitors of stilbenes production in Vitis vinifera L. cell culture. Plants 10:490
Saravanakumar K, Yu C, Dou K, Wang M, Li Y, Chen J (2016) Synergistic effect of Trichoderma-
derived antifungal metabolites and cell wall degrading enzymes on enhanced biocontrol of
Fusarium oxysporum f. sp. cucumerinum. Biol Control 94:37–46
Sayyed RZ, Chincholkar SB, Reddy MS, Gangurde NS, Patel PR (2013) Siderophore producing
PGPR for crop nutrition and phytopathogen suppression. In: Bacteria in agrobiology: disease
management. Springer, pp449–471
Schardl CL (2001) Epichloë festucae and related mutualistic symbionts of grasses. Fungal Genet
Biol 33:69–82
Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal
endophytes. Annu Rev Plant Biol 55:315–340
Schelkle M, Peterson RL (1997) Suppression of common root pathogens by helper bacteria and
ectomycorrhizal fungi invitro. Mycorrhiza 6:481–485
Schenk ST, Stein E, Kogel K-H, Schikora A (2012) Arabidopsis growth and defense are modulated
by bacterial quorum sensing molecules. Plant Signal Behav 7:178–181
Scherlach K, Hertweck C (2009) Triggering cryptic natural product biosynthesis in microorgan-
isms. Org Biomol Chem 7:1753–1760
Schlemper TR, van Veen JA, Kuramae EE (2018) Co-variation of bacterial and fungal communities
in different sorghum cultivars and growth stages is soil dependent. Microb Ecol 76:205–214
Symbiotic Relationships withFungi: FromMutualism toParasitism
410
Schroeckh V, Scherlach K, Nützmann H-W, Shelest E, Schmidt-Heck W, Schuemann J, Martin K,
Hertweck C, Brakhage AA (2009) Intimate bacterial–fungal interaction triggers biosynthesis
of archetypal polyketides in Aspergillus nidulans. Proc Natl Acad Sci 106:14558–14563
Schulz B, Boyle C, Draeger S, Römmert A-K, Krohn K (2002) Endophytic fungi: a source of novel
biologically active secondary metabolites. Mycol Res 106:996–1004
Schulza B, Boyle C (2005) The endophyte continuum. Mycol Res 109:661–686
Selim SM, Zayed MS (2017) Microbial interactions and plant growth. In: Plant-microbe interac-
tions in agro-ecological perspectives. Springer, pp1–15
Sharma VK, Kumar J, Singh DK, Mishra A, Verma SK, Gond SK, Kumar A, Singh N, Kharwar
RN (2017) Induction of cryptic and bioactive metabolites through natural dietary components
in an endophytic fungus Colletotrichum gloeosporioides (Penz.) Sacc. Front Microbiol 8:1126
Sharma S, Kour D, Rana KL, Dhiman A, Thakur S, Thakur P, Thakur S, Thakur N, Sudheer S,
Yadav N (2019) Trichoderma: biodiversity, ecological signicances, and industrial applica-
tions. In: Recent advancement in white biotechnology through fungi. Springer, pp85–120
Sharma M, Saleh D, Charron J-B, Jabaji S (2020) A crosstalk between Brachypodium root
exudates, organic acids, and Bacillus velezensis B26, a growth promoting bacterium. Front
Microbiol 11:575578
Shastry RP, Dolan SK, Abdelhamid Y, Vittal RR, Welch M (2018) Purication and characterisation
of a quorum quenching AHL-lactonase from the endophytic bacterium Enterobacter sp. CS66.
FEMS Microbiol Lett 365:fny054
Sheibani-Tezerji R, Naveed M, Jehl M-A, Sessitsch A, Rattei T, Mitter B (2015) The genomes of
closely related Pantoea ananatis maize seed endophytes having different effects on the host
plant differ in secretion system genes and mobile genetic elements. Front Microbiol 6:440
Shi S, Richardson AE, O’Callaghan M, DeAngelis KM, Jones EE, Stewart A, Firestone MK,
Condron LM (2011) Effects of selected root exudate components on soil bacterial communi-
ties. FEMS Microbiol Ecol 77:600–610
Shinshi H, Mohnen D, Meins F Jr (1987) Regulation of a plant pathogenesis-related enzyme: inhi-
bition of chitinase and chitinase mRNA accumulation in cultured tobacco tissues by auxin and
cytokinin. Proc Natl Acad Sci 84:89–93
Shinya T, Miyamoto K, Uchida K, Hojo Y, Yumoto E, Okada K, Yamane H, Galis I (2022)
Chitooligosaccharide elicitor and oxylipins synergistically elevate phytoalexin production in
rice. Plant Mol Biol 109:595–609
Silipo A, Erbs G, Shinya T, Dow JM, Parrilli M, Lanzetta R, Shibuya N, Newman M-A, Molinaro
A (2010) Glyco-conjugates as elicitors or suppressors of plant innate immunity. Glycobiology
20:406–419
Simonin M, Dasilva C, Terzi V, Ngonkeu ELM, Diouf D, Kane A, Béna G, Moulin L (2020)
Inuence of plant genotype and soil on the wheat rhizosphere microbiome: evidences for a
core microbiome across eight African and European soils. FEMS Microbiol Ecol 96:aa067
Sreenayana B, Vinodkumar S, Nakkeeran S, Muthulakshmi P, Poornima K (2022) Multitudinous
potential of Trichoderma species in imparting resistance against F. oxysporum f. sp. cucumeri-
num and Meloidogyne incognita disease complex. J Plant Growth Regul 41:1187–1206
Stanghellini ME, Burr TJ (1973) Germination invivo of Pythium aphanidermatum oospores and
sporangia. Phytopathology 63:1493–1496
Sugiyama A, Ueda Y, Zushi T, Takase H, Yazaki K (2014) Changes in the bacterial community of
soybean rhizospheres during growth in the eld. PLoS One 9:e100709
Sumida CH, Daniel JFS, Araujod APCS, Peitl DC, Abreu LM, Dekker RFH, Canteri MG (2018)
Trichoderma asperelloides antagonism to nine Sclerotinia sclerotiorum strains and biological
control of white mold disease in soybean plants. Biocontrol Sci Technol 28:142–156
Suryanarayanan TS (2013) Endophyte research: going beyond isolation and metabolite documen-
tation. Fungal Ecol 6:561–568
Takamatsu S, Siahaan SAS, Moreno-Rico O, Cabrera de Álvarez MG, Braun U (2016) Early evo-
lution of endoparasitic group in powdery mildews: molecular phylogeny suggests missing link
between Phyllactinia and Leveillula. Mycologia 108:837–850
M. M. El-Metwally etal.
411
Tan S, Yang C, Mei X, Shen S, Raza W, Shen Q, Xu Y (2013) The effect of organic acids from
tomato root exudates on rhizosphere colonization of Bacillus amyloliquefaciens T-5. Appl Soil
Ecol 64:15–22
Tanaka A, Christensen MJ, Takemoto D, Park P, Scott B (2006) Reactive oxygen species play a
role in regulating a fungus–perennial ryegrass mutualistic interaction. Plant Cell 18:1052–1066
Tanaka A, Takemoto D, Hyon G, Park P, Scott B (2008) NoxA activation by the small GTPase
RacA is required to maintain a mutualistic symbiotic association between Epichloë festucae
and perennial ryegrass. Mol Microbiol 68:1165–1178
Tchameni SN, Cotârleț M, Ghinea IO, Bedine MAB, Sameza ML, Borda D, Bahrim G, Dinică RM
(2020) Involvement of lytic enzymes and secondary metabolites produced by Trichoderma spp.
in the biological control of Pythium myriotylum. Int Microbiol 23:179–188
Teixeira PJPL, Colaianni NR, Law TF, Conway JM, Gilbert S, Li H, Salas-González I, Panda D,
Del Risco NM, Finkel OM (2021) Specic modulation of the root immune system by a com-
munity of commensal bacteria. Proc Natl Acad Sci 118:e2100678118
Temple B, Horgen PA, Bernier L, Hintz WE (1997) Cerato-ulmin, a hydrophobin secreted by the
causal agents of Dutch elm disease, is a parasitic tness factor. Fungal Genet Biol 22:39–53
Teplitski M, Mathesius U, Rumbaugh KP (2011) Perception and degradation of N-acyl homoser-
ine lactone quorum sensing signals by mammalian and plant cells. Chem Rev 111:100–116
Thines M (2014) Phylogeny and evolution of plant pathogenic oomycetes– a global overview. Eur
J Plant Pathol 138:431–447
Thompson SE, Levin S, Rodriguez-Iturbe I (2014) Rainfall and temperatures changes have con-
founding impacts on P hytophthora cinnamomi occurrence risk in the southwestern USA under
climate change scenarios. Glob Chang Biol 20:1299–1312
Tian W, Deng Z, Hong K (2017) The biological activities of sesterterpenoid-type ophiobolins. Mar
Drugs 15:229
Topi D, Tavčar-Kalcher G, Pavšič-Vrtač K, Babič J, Jakovac-Strajn B (2019) Alternaria myco-
toxins in grains from Albania: alternariol, alternariol monomethyl ether, tenuazonic acid and
tentoxin. World Mycotoxin J 12:89–99
Tourneroche A, Lami R, Hubas C, Blanchet E, Vallet M, Escoubeyrou K, Paris A, Prado S (2019)
Bacterial–fungal interactions in the kelp endomicrobiota drive autoinducer-2 quorum sensing.
Front Microbiol 10:1693
Troian RF, Steindorff AS, Ramada MHS, Arruda W, Ulhoa CJ (2014) Mycoparasitism studies of
Trichoderma harzianum against Sclerotinia sclerotiorum: evaluation of antagonism and expres-
sion of cell wall-degrading enzymes genes. Biotechnol Lett 36:2095–2101
Turner SJ, Subbotin SA (2013) Cyst nematodes. Plant Nematol:109–143
Unterseher M, Schnittler M (2010) Species richness analysis and ITS rDNA phylogeny revealed the
majority of cultivable foliar endophytes from beech (Fagus sylvatica). Fungal Ecol 3:366–378
van’t Padje A, Whiteside MD, Kiers ET (2016) Signals and cues in the evolution of plant–microbe
communication. Curr Opin Plant Biol 32:47–52
von Rad U, Klein I, Dobrev PI, Kottova J, Zazimalova E, Fekete A, Hartmann A, Schmitt-Kopplin
P, Durner J (2008) Response of Arabidopsis thaliana to N-hexanoyl-DL-homoserine-lactone, a
bacterial quorum sensing molecule produced in the rhizosphere. Planta 229:73–85
Valent B, Chumley FG (1991) Molecular genetic analysis of the rice blast fungus, Magnaporthe
grisea. Annu Rev Phytopathol 29:443–467
Van Elsas JD, Chiurazzi M, Mallon CA, Elhottovā D, Krištůfek V, Salles JF (2012) Microbial diver-
sity determines the invasion of soil by a bacterial pathogen. Proc Natl Acad Sci 109:1159–1164
Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A (2015) The importance of the
microbiome of the plant holobiont. New Phytol 206:1196–1206
Venkatesh Kumar R, Singh RP, Mishra P (2019) Endophytes as emphatic communication barriers
of quorum sensing in Gram-positive and Gram-negative bacteria– a review. Environ Sustain
2:455–468
Verma M, Brar SK, Tyagi RD, Surampalli RY, Valero JR (2007) Antagonistic fungi, Trichoderma
spp.: panoply of biological control. Biochem Eng J 37:1–20
Symbiotic Relationships withFungi: FromMutualism toParasitism
412
Vicente CSL, Ikuyo Y, Mota M, Hasegawa K (2013) Pinewood nematode-associated bacteria con-
tribute to oxidative stress resistance of Bursaphelenchus xylophilus. BMC Microbiol 13:1–8
Wang W-X (2016) Crosstalk and antibacterial molecules from endophytes harbored in Narcissus
tazetta and Buxus sinica
Wang W-X, Kusari S, Sezgin S, Lamshöft M, Kusari P, Kayser O, Spiteller M (2015)
Hexacyclopeptides secreted by an endophytic fungus Fusarium solani N06 act as crosstalk
molecules in Narcissus tazetta. Appl Microbiol Biotechnol 99:7651–7662
Wang L, Ren L, Li C, Gao C, Liu X, Wang M, Luo Y (2019) Effects of endophytic fungi diversity
in different coniferous species on the colonization of Sirex noctilio (Hymenoptera: Siricidae).
Sci Rep 9:1–11
Whitehead NA, Barnard AML, Slater H, Simpson NJL, Salmond GPC (2001) Quorum-sensing in
Gram-negative bacteria. FEMS Microbiol Rev 25:365–404
Willey JM, Sherwood L, Woolverton CJ (2011) Prescott’s microbiology. McGraw-Hill, NewYork
Williams P, Winzer K, Chan WC, Camara M (2007) Look who’s talking: communication and quo-
rum sensing in the bacterial world. Philos Trans R Soc B Biol Sci 362:1119–1134
Williams HE, Steele JCP, Clements MO, Keshavarz T (2012) γ-Heptalactone is an endogenously
produced quorum-sensing molecule regulating growth and secondary metabolite production by
Aspergillus nidulans. Appl Microbiol Biotechnol 96:773–781
Xiaodong X, Olukolu B, Yang Q, Balint-Kurti P (2018) Identication of a locus in maize control-
ling response to a host-selective toxin derived from Cochliobolus heterostrophus, causal agent
of southern leaf blight. Theor Appl Genet 131:2601–2612
Xiao-Yan S, Qing-Tao S, Shu-Tao X, Xiu-Lan C, Cai-Yun S, Yu-Zhong Z (2006) Broad-spectrum
antimicrobial activity and high stability of Trichokonins from Trichoderma koningii SMF2
against plant pathogens. FEMS Microbiol Lett 260:119–125
Xie X, Yoneyama K, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopathol 48:93–117
Xu G, Yang S, Meng L, Wang B-G (2018) The plant hormone abscisic acid regulates the growth
and metabolism of endophytic fungus Aspergillus nidulans. Sci Rep 8:1–9
Xu D, Xue M, Shen Z, Jia X, Hou X, Lai D, Zhou L (2021) Phytotoxic secondary metabolites from
fungi. Toxins (Basel) 13:261
Yin C, Chen X, Wang X, Han Q, Kang Z, Hulbert SH (2009) Generation and analysis of expression
sequence tags from haustoria of the wheat stripe rust fungus Puccinia striiformis f. sp. tritici.
BMC Genomics 10:1–9
You J, Zhang J, Wu M, Yang L, Chen W, Li G (2016) Multiple criteria-based screening of
Trichoderma isolates for biological control of Botrytis cinerea on tomato. Biol Control
101:31–38
Yu X, Bi Y, Yan L, Liu X, Wang Y, Shen K, Li Y (2016) Activation of phenylpropanoid pathway
and PR of potato tuber against Fusarium sulphureum by fungal elicitor from Trichothecium
roseum. World J Microbiol Biotechnol 32:1–12
Yuan J, Zhang W, Sun K, Tang M-J, Chen P-X, Li X, Dai C-C (2019) Comparative transcriptomics
and proteomics of Atractylodes lancea in response to endophytic fungus Gilmaniella sp. AL12
reveals regulation in plant metabolism. Front Microbiol 10:1208
Zakaria L, Yaakop AS, Salleh B, Zakaria M (2010) Endophytic fungi from paddy. Trop Life Sci
Res 21:101
Zentmyer GA (1961) Chemotaxis of zoospores for root exudates. Science (80–) 133:1595–1596
Zhang L, Feng G, Declerck S (2018) Signal beyond nutrient, fructose, exuded by an arbuscu-
lar mycorrhizal fungus triggers phytate mineralization by a phosphate solubilizing bacterium.
ISME J 12:2339–2351
Zhang H, He Y, Wu J, Yang Y, Zheng K, Yang M, Zhu S, He X, Zhu Y, Liu Y (2019) Inhibitory
activity of antifungal substances in maize root exudates against Phytophthora sojae. Plant Prot
45:124–130
Zhang H, Yang Y, Mei X, Li Y, Wu J, Li Y, Wang H, Huang H, Yang M, He X (2020) Phenolic acids
released in maize rhizosphere during maize-soybean intercropping inhibit Phytophthora blight
of soybean. Front Plant Sci 11:886
M. M. El-Metwally etal.
413
Zhang Z, Zhao Y, An T, Yu H, Bi X, Liu H, Xu Y, Yang Z, Chen Y, Wen J (2022) Maize and com-
mon bean seed exudates mediate part of nonhost resistance to Phytophthora sojae prior to
infection. Phytopathology® 112:335–344
Zhou T, Boland GJ (1999) Mycelial growth and production of oxalic acid by virulent and hypo-
virulent isolates of Sclerotinia sclerotiorum. Can J Plant Pathol 21:93–99
Zhou J, Yang T, Mei Y-Z, Kang L, Dai C-C (2014) Laccase production by Phomopsis liquidambari
B3 cultured with food waste and wheat straw as the main nitrogen and carbon sources. J Air
Waste Manag Assoc 64:1154–1163
Zhou L, Zhang L-H, Cámara M, He Y-W (2017) The DSF family of quorum sensing signals: diver-
sity, biosynthesis, and turnover. Trends Microbiol 25:293–303
Symbiotic Relationships withFungi: FromMutualism toParasitism
