2,4-diacetylphloroglucinol) that stimulate root growth and/
or exudation, thereby amplifying the rhizosphere effect
(Bonkowski 2004) (Fig. 11.8).
There are also differences according to the microbial
habitat within the phytosphere, in particular at the scale of
the root system. The quantitative importance of root systems
varies depending on pedoclimatic and plant community
properties, with root densities up to 100–200 cm roots per
cm
3 of soil and roots occupying typically 1–5 % of the soil
volume. However, most exchanges between the plant and
the soil, both in terms of nutrients/water acquisition and
rhizodeposition, occur at root tips (Cardon and Whitbeck
2007). Rhizosphere microbial populations are thus higher in
the root elongation and root hair zones compared with the
root cap (Cardon and Whitbeck 2007). Cell differentiation is
accompanied by a decrease in the permeability of plant cell
walls, and therefore older root parts are rather involved in
sap transport. In the case of aerial parts, microbial numbers
depend on leaf position and age, and they are often higher on
the lower side of leaves (Kinkel et al. 2000). Whether on
roots or leaves, microbial growth is stimulated following
lysis of plant cells resulting from attacks by phytoparasites.
Microorganisms on plant surfaces are often found as
microcolonies (sometimes with a cell density of over 10
4
bacteria per microcolony) and biofilms (Wimpenny and
Colasanti 1997; Ramey et al. 2004). This may concern up
to 80 % of the bacterial populations on the surface of leaves
(Morris and Monier 2003). Biofilms occur particularly at the
junction of epidermal cells, at wounds, and (for aerial parts)
at stomata, hydathodes, and along veins (Beattie and Lindow
1999). Biofilm distribution becomes more erratic on older
leaves (Leben 1988) and root tissues (Lu ¨beck et al. 2000).
Biofilms, which include the mucigel matrix in the case of
roots, can be several tens of micrometers thick (Fig. 11.7c).
Their buildup reflects the availability of nutrients (Leveau
and Lindow 2001), and by comparison with other types of
environments, their development level is intermediate
(phyllosphere) to high (rhizosphere) (Wimpenny and
Colasanti 1997).
Finally, a difference can be made between the plant
surface and the interior of the plant, which can also be
colonized by microorganisms (Gamboa et al. 2003).
Microorganisms present in the plant are found in the cortex,
more rarely in the stele (vascular cylinder). They often have
intercellular localization, but some (often parasites or
symbionts) may be within plant cells (Fig. 11.7). In the
case of fungi, the mycelium is either entirely in the plant or
only partly within the plant, as in the case of ectomycorrhizal
fungi (Brundrett 2009). It should be noted that certain
mycorrhizal fungi harbor bacteria, forming multitrophic
associations (Bertaux et al. 2003). Microorganisms present
in the plant but that do not lead to physiological dysfunctions
(as pathogens do) or host differentiation (as bacterial
symbionts nodulating roots do) are termed endophytes. The
plant tissues provide particular environmental conditions,
inasmuch as microorganisms have direct access to available
substrates in the plant, while being directly exposed to
defense mechanisms of the host. The microbial numbers in
the plant are generally low (10
2–5 bacteria per g), except for
some endophytic bacteria (up to 10
8 per g) and especially
symbionts and parasites, when they are engaged in a successful interaction with the host (McInroy and Kloepper
1995; Gamboa et al. 2003).
11.3.3 Sources of Microorganisms Associated
with Plants
Microorganisms interacting with plants have various
provenances. First, many originate from soil. They can find
themselves in contact with plants if they are present in an area
of the soil that is penetrated by a root. However, many terrestrial microorganisms have the ability to actively come into
contact with seeds or roots, through a process of chemotaxis
(for bacteria) or chemotropism (for fungi) triggered by the
perception of plant exudates (Bais et al. 2006). Terrestrial
microorganisms in contact with plants will mostly be
associated to the root system, but some may colonize plant
shoots or fruits. This situation is mainly documented for
pathogens, including fungi such as Fusarium spp. (Deuteromycetes) that produce mycotoxins (Leplat et al. 2013).
Second, certain microorganisms that interact with plants
come in contact with the plant through precipitation and
irrigation water, the fall of atmospheric dust, or wind (Agrios
1997; Morris et al. 2010). Precipitations also lead to runoff
events along the aerial parts of the plants and the soil surface.
This runoff will lead to a redistribution of some
phyllospheric microorganisms. The presence of microorganisms in the atmosphere can be explained by the formation of aerosols, i.e., microdroplets, which originate from
liquid phases that are turbulent or that face convection, e.g.,
by wind. This presence can also be explained by the
transportation, caused by wind or air currents, of microorganisms or microparticles colonized by microorganisms,
including for resting stages such as many fungal spores
(Savage et al. 2012).
Third, animals can act as carriers of microorganisms.
This will particularly involve phytophagous arthropods
(especially insects) and herbivorous mammals, which will
inoculate the plant with their mouthparts, as well as parasitic
animals through their stylet or spear (nematodes) or rostrum
(biting insects) (Villate et al. 2012). However, the mere
contact between the animal (or its feces) and the plant can
also allow plant contamination by microorganisms from the
surface of the animal (or its digestive system), whether
microarthropods or livestock.
408
Y. Moe ¨nne-Loccoz et al.
or exudation, thereby amplifying the rhizosphere effect
(Bonkowski 2004) (Fig. 11.8).
There are also differences according to the microbial
habitat within the phytosphere, in particular at the scale of
the root system. The quantitative importance of root systems
varies depending on pedoclimatic and plant community
properties, with root densities up to 100–200 cm roots per
cm
3 of soil and roots occupying typically 1–5 % of the soil
volume. However, most exchanges between the plant and
the soil, both in terms of nutrients/water acquisition and
rhizodeposition, occur at root tips (Cardon and Whitbeck
2007). Rhizosphere microbial populations are thus higher in
the root elongation and root hair zones compared with the
root cap (Cardon and Whitbeck 2007). Cell differentiation is
accompanied by a decrease in the permeability of plant cell
walls, and therefore older root parts are rather involved in
sap transport. In the case of aerial parts, microbial numbers
depend on leaf position and age, and they are often higher on
the lower side of leaves (Kinkel et al. 2000). Whether on
roots or leaves, microbial growth is stimulated following
lysis of plant cells resulting from attacks by phytoparasites.
Microorganisms on plant surfaces are often found as
microcolonies (sometimes with a cell density of over 10
4
bacteria per microcolony) and biofilms (Wimpenny and
Colasanti 1997; Ramey et al. 2004). This may concern up
to 80 % of the bacterial populations on the surface of leaves
(Morris and Monier 2003). Biofilms occur particularly at the
junction of epidermal cells, at wounds, and (for aerial parts)
at stomata, hydathodes, and along veins (Beattie and Lindow
1999). Biofilm distribution becomes more erratic on older
leaves (Leben 1988) and root tissues (Lu ¨beck et al. 2000).
Biofilms, which include the mucigel matrix in the case of
roots, can be several tens of micrometers thick (Fig. 11.7c).
Their buildup reflects the availability of nutrients (Leveau
and Lindow 2001), and by comparison with other types of
environments, their development level is intermediate
(phyllosphere) to high (rhizosphere) (Wimpenny and
Colasanti 1997).
Finally, a difference can be made between the plant
surface and the interior of the plant, which can also be
colonized by microorganisms (Gamboa et al. 2003).
Microorganisms present in the plant are found in the cortex,
more rarely in the stele (vascular cylinder). They often have
intercellular localization, but some (often parasites or
symbionts) may be within plant cells (Fig. 11.7). In the
case of fungi, the mycelium is either entirely in the plant or
only partly within the plant, as in the case of ectomycorrhizal
fungi (Brundrett 2009). It should be noted that certain
mycorrhizal fungi harbor bacteria, forming multitrophic
associations (Bertaux et al. 2003). Microorganisms present
in the plant but that do not lead to physiological dysfunctions
(as pathogens do) or host differentiation (as bacterial
symbionts nodulating roots do) are termed endophytes. The
plant tissues provide particular environmental conditions,
inasmuch as microorganisms have direct access to available
substrates in the plant, while being directly exposed to
defense mechanisms of the host. The microbial numbers in
the plant are generally low (10
2–5 bacteria per g), except for
some endophytic bacteria (up to 10
8 per g) and especially
symbionts and parasites, when they are engaged in a successful interaction with the host (McInroy and Kloepper
1995; Gamboa et al. 2003).
11.3.3 Sources of Microorganisms Associated
with Plants
Microorganisms interacting with plants have various
provenances. First, many originate from soil. They can find
themselves in contact with plants if they are present in an area
of the soil that is penetrated by a root. However, many terrestrial microorganisms have the ability to actively come into
contact with seeds or roots, through a process of chemotaxis
(for bacteria) or chemotropism (for fungi) triggered by the
perception of plant exudates (Bais et al. 2006). Terrestrial
microorganisms in contact with plants will mostly be
associated to the root system, but some may colonize plant
shoots or fruits. This situation is mainly documented for
pathogens, including fungi such as Fusarium spp. (Deuteromycetes) that produce mycotoxins (Leplat et al. 2013).
Second, certain microorganisms that interact with plants
come in contact with the plant through precipitation and
irrigation water, the fall of atmospheric dust, or wind (Agrios
1997; Morris et al. 2010). Precipitations also lead to runoff
events along the aerial parts of the plants and the soil surface.
This runoff will lead to a redistribution of some
phyllospheric microorganisms. The presence of microorganisms in the atmosphere can be explained by the formation of aerosols, i.e., microdroplets, which originate from
liquid phases that are turbulent or that face convection, e.g.,
by wind. This presence can also be explained by the
transportation, caused by wind or air currents, of microorganisms or microparticles colonized by microorganisms,
including for resting stages such as many fungal spores
(Savage et al. 2012).
Third, animals can act as carriers of microorganisms.
This will particularly involve phytophagous arthropods
(especially insects) and herbivorous mammals, which will
inoculate the plant with their mouthparts, as well as parasitic
animals through their stylet or spear (nematodes) or rostrum
(biting insects) (Villate et al. 2012). However, the mere
contact between the animal (or its feces) and the plant can
also allow plant contamination by microorganisms from the
surface of the animal (or its digestive system), whether
microarthropods or livestock.
408
Y. Moe ¨nne-Loccoz et al.