nitrogen-fixing symbioses (Mathesius 2003). Before contact,
the mycorrhizal fungus stimulates the production of fine
roots to increase the contact sites, secreting hormones
including the auxin indole-3-acetic acid (IAA). After
contact, the fungus enters the root and must overcome
defense mechanisms. It switches from a saprophytic to a
biotrophic phase, which recalls the case of biotrophic
parasites.
Signaling mechanisms between partners in the establishment of a nitrogen-fixing symbiosis or a mycorrhizal symbiosis involve common symbiosis genes (SYM) in the plant,
including SYMRK/NORK/DMI2 and DMI3 that code for
receptor-like leucine-rich kinases, CASTOR/DMI1 and
POLLUX encoding ion channels ensuring transmembrane
calcium flux, and (in the case of nitrogen-fixing symbiosis
in Fabaceae) ENOD40 (early nodulin 40) (Oldroyd and
Downie 2006; Reinhardt 2007; Gherbi et al. 2008). The
structure of the Myc factors, i.e., sulfated and non-sulfated
lipo-chito-oligosaccharides consisting of four substituted Nacetylglucosamines, is very close to that of the Nod factors,
which reinforces the view that the two types of symbioses
are functionally very close (Maillet et al. 2011). In terms of
evolution, the bacterial symbioses (relatively young; about
65 million years) and the ectomycorrhizal symbiosis
(also recent; about 180 million years) probably recruited
SYM genes already involved in the arbuscular mycorrhizal
symbiosis, which is older (probably 400 million years)
(Simon et al. 1993).
11.3.5.4 Cooperation
Several bacteria and fungi actively cooperate (syn. associative symbiosis) with the plant. In the case of bacteria, this
ability is mainly found in plant growth-promoting
rhizobacteria* (PGPR) (Fig. 11.11a). PGPR are documented
mainly in Proteobacteria and Firmicutes and to a lesser
extent in Actinobacteria. Growth stimulation usually results
from a combination of direct and indirect phytobeneficial
effects (Dobbelaere et al. 2001). Direct phytobeneficial
effects may entail improved mineral nutrition of the plant,
e.g., via free-living nitrogen fixation or phosphate solubilization (Dobbelaere et al. 2003) and/or improved water
uptake through rhizosphere soil structuration by bacterial
exopolysaccharides (Amellal et al. 1998) or aquaporin stimulation (Groppa et al. 2012). Interference with plant hormonal metabolism may also be involved, via bacterial
production of phytohormones (auxins and cytokinins) and/
or bacterial deamination of 1-aminocyclopropane-1-carboxylate (ACC), the ethylene precursor in the plant (Dobbelaere
et al. 2003). The auxin indole-3-acetic produced by PGPR
helps getting around plant defense mechanisms, thereby
facilitating PGPR colonization of the plant (Remans et al.
2006). Finally, phytobeneficial effects also include triggering of systemic resistance in the plant, in particular, induced
systemic resistance (ISR) pathways relying on jasmonate
and ethylene (van Loon et al. 2006).
Indirect phytobeneficial effects of PGPR entail inhibition
of parasitic bacteria, oomycetes, fungi, nematodes, and even
parasitic plants (e.g., Striga), mainly through competition or
antagonism (Chapon et al. 2002; Raaijmakers et al. 2009).
Competition can take place for macronutrients (such as
organic carbon), micronutrients (such as soluble ferric iron
via high-affinity siderophores), and/or infection sites. Antagonism (syn. amensalism) may involve extracellular lytic
enzymes (e.g., cellulases, chitinases, proteases), which act
on the cell wall of pathogenic microorganisms, their virulence factors (such as fusaric acid from Fusarium
oxysporum, degraded by some Burkholderia), or their intercellular signals (such as N-acyl homoserine lactone in
Pectobacterium carotovorum) (Raaijmakers et al. 2009).
Antagonism may also involve type III secretion system
effectors (cf. Sect. 11.4.3) with the ability to reduce the
virulence of certain pathogens (Rezzonico et al. 2005).
Finally, antagonism can rely on production of antimicrobial
secondary metabolites (antibiosis), such as 2,4diacetylphloroglucinol, and a single antagonistic strain
often produces several of these antimicrobial metabolites
(Raaijmakers et al. 2009). Some pathogens can defend themselves by suppressing the production of these metabolites
(case of 2,4-diacetylphloroglucinol, via fusaric acid from
Fusarium) or the expression of genes involved in root colonization by the antagonistic bacterium (Fedi et al. 1997;
Raaijmakers et al. 2009).
The metabolites released by PGPR are important for their
interactions with the plant and plant pathogens, and many of
them play multiple roles. Indeed, 2,4-diacetylphloroglucinol
(enabling antagonism toward phytoparasites) and some
siderophores such as pyoverdine (involved in iron competition) can also induce plant resistance (Raaijmakers et al.
2009). Phenylacetic acid, synthesized by Azospirillum
brasilense Sp245 and others, is both an auxinic phytohormone and an antimicrobial compound. Therefore, certain
PGPR are multifunctional in that they can act both on plant
(via induction of resistance and ACC deamination) and
phytopathogens (antagonism or competition).
Fungi in cooperation with the plant remain poorly
documented compared with PGPR. Their direct
phytobeneficial effects include solubilization of mineral
nutrients (Trichoderma and Gliocladium) and the induction
of systemic resistance in plants (Trichoderma, Gliocladium,
and nonpathogenic F. oxysporum) (Harman et al. 2004).
However, indirect phytobeneficial mechanisms are more
important. Hyperparasitism toward different phytoparasitic
oomycetes and fungi is one of the modes of action of
Trichoderma. The fungus coils around its target, e.g.,
R. solani, and secretes lytic enzymes (chitinases and
cellulases) that alter phytoparasite cell wall. The degradation
11 Microorganisms and Biotic Interactions
417
the mycorrhizal fungus stimulates the production of fine
roots to increase the contact sites, secreting hormones
including the auxin indole-3-acetic acid (IAA). After
contact, the fungus enters the root and must overcome
defense mechanisms. It switches from a saprophytic to a
biotrophic phase, which recalls the case of biotrophic
parasites.
Signaling mechanisms between partners in the establishment of a nitrogen-fixing symbiosis or a mycorrhizal symbiosis involve common symbiosis genes (SYM) in the plant,
including SYMRK/NORK/DMI2 and DMI3 that code for
receptor-like leucine-rich kinases, CASTOR/DMI1 and
POLLUX encoding ion channels ensuring transmembrane
calcium flux, and (in the case of nitrogen-fixing symbiosis
in Fabaceae) ENOD40 (early nodulin 40) (Oldroyd and
Downie 2006; Reinhardt 2007; Gherbi et al. 2008). The
structure of the Myc factors, i.e., sulfated and non-sulfated
lipo-chito-oligosaccharides consisting of four substituted Nacetylglucosamines, is very close to that of the Nod factors,
which reinforces the view that the two types of symbioses
are functionally very close (Maillet et al. 2011). In terms of
evolution, the bacterial symbioses (relatively young; about
65 million years) and the ectomycorrhizal symbiosis
(also recent; about 180 million years) probably recruited
SYM genes already involved in the arbuscular mycorrhizal
symbiosis, which is older (probably 400 million years)
(Simon et al. 1993).
11.3.5.4 Cooperation
Several bacteria and fungi actively cooperate (syn. associative symbiosis) with the plant. In the case of bacteria, this
ability is mainly found in plant growth-promoting
rhizobacteria* (PGPR) (Fig. 11.11a). PGPR are documented
mainly in Proteobacteria and Firmicutes and to a lesser
extent in Actinobacteria. Growth stimulation usually results
from a combination of direct and indirect phytobeneficial
effects (Dobbelaere et al. 2001). Direct phytobeneficial
effects may entail improved mineral nutrition of the plant,
e.g., via free-living nitrogen fixation or phosphate solubilization (Dobbelaere et al. 2003) and/or improved water
uptake through rhizosphere soil structuration by bacterial
exopolysaccharides (Amellal et al. 1998) or aquaporin stimulation (Groppa et al. 2012). Interference with plant hormonal metabolism may also be involved, via bacterial
production of phytohormones (auxins and cytokinins) and/
or bacterial deamination of 1-aminocyclopropane-1-carboxylate (ACC), the ethylene precursor in the plant (Dobbelaere
et al. 2003). The auxin indole-3-acetic produced by PGPR
helps getting around plant defense mechanisms, thereby
facilitating PGPR colonization of the plant (Remans et al.
2006). Finally, phytobeneficial effects also include triggering of systemic resistance in the plant, in particular, induced
systemic resistance (ISR) pathways relying on jasmonate
and ethylene (van Loon et al. 2006).
Indirect phytobeneficial effects of PGPR entail inhibition
of parasitic bacteria, oomycetes, fungi, nematodes, and even
parasitic plants (e.g., Striga), mainly through competition or
antagonism (Chapon et al. 2002; Raaijmakers et al. 2009).
Competition can take place for macronutrients (such as
organic carbon), micronutrients (such as soluble ferric iron
via high-affinity siderophores), and/or infection sites. Antagonism (syn. amensalism) may involve extracellular lytic
enzymes (e.g., cellulases, chitinases, proteases), which act
on the cell wall of pathogenic microorganisms, their virulence factors (such as fusaric acid from Fusarium
oxysporum, degraded by some Burkholderia), or their intercellular signals (such as N-acyl homoserine lactone in
Pectobacterium carotovorum) (Raaijmakers et al. 2009).
Antagonism may also involve type III secretion system
effectors (cf. Sect. 11.4.3) with the ability to reduce the
virulence of certain pathogens (Rezzonico et al. 2005).
Finally, antagonism can rely on production of antimicrobial
secondary metabolites (antibiosis), such as 2,4diacetylphloroglucinol, and a single antagonistic strain
often produces several of these antimicrobial metabolites
(Raaijmakers et al. 2009). Some pathogens can defend themselves by suppressing the production of these metabolites
(case of 2,4-diacetylphloroglucinol, via fusaric acid from
Fusarium) or the expression of genes involved in root colonization by the antagonistic bacterium (Fedi et al. 1997;
Raaijmakers et al. 2009).
The metabolites released by PGPR are important for their
interactions with the plant and plant pathogens, and many of
them play multiple roles. Indeed, 2,4-diacetylphloroglucinol
(enabling antagonism toward phytoparasites) and some
siderophores such as pyoverdine (involved in iron competition) can also induce plant resistance (Raaijmakers et al.
2009). Phenylacetic acid, synthesized by Azospirillum
brasilense Sp245 and others, is both an auxinic phytohormone and an antimicrobial compound. Therefore, certain
PGPR are multifunctional in that they can act both on plant
(via induction of resistance and ACC deamination) and
phytopathogens (antagonism or competition).
Fungi in cooperation with the plant remain poorly
documented compared with PGPR. Their direct
phytobeneficial effects include solubilization of mineral
nutrients (Trichoderma and Gliocladium) and the induction
of systemic resistance in plants (Trichoderma, Gliocladium,
and nonpathogenic F. oxysporum) (Harman et al. 2004).
However, indirect phytobeneficial mechanisms are more
important. Hyperparasitism toward different phytoparasitic
oomycetes and fungi is one of the modes of action of
Trichoderma. The fungus coils around its target, e.g.,
R. solani, and secretes lytic enzymes (chitinases and
cellulases) that alter phytoparasite cell wall. The degradation
11 Microorganisms and Biotic Interactions
417