conditions (e.g., rice) can release oxygen through their roots
(Liesack et al. 2000). Depending on these factors, the availability of oxygen in the root zone will be lower (most often)
or higher than in non-rhizosphere soil.
11.3.4.2 Microbial Diversity
To colonize plants, a microorganism must not only use the
trophic resources they provide (in a context of competition
with the rest of the microbial community) but also tolerate
abiotic stress conditions (including desiccation and UV in the
phyllosphere) as well as toxins and other host defense
compounds. The best adapted microorganisms will be thus
favored over the others. This selection process is amplified by
the molecular dialogues with the plant, including microbial
chemotaxis/chemotropism phenomena (cf. Sect. 9.2) and the
ability of certain plants to interfere with bacterial quorum
sensing (Bauer and Robinson 2002). Finally, all terrestrial
microorganisms are not affected the same way by the antimicrobial compounds produced by the other microorganisms
associated with plant (Gilbert et al. 1993; Raaijmakers et al.
2009) and by predation by protozoa (Bonkowski 2004) and
nematodes (Jousset et al. 2009). In total, the trophic stimulation of microbial growth by the plant is therefore selective.
This usually results in a lower microbial diversity when
comparing bulk soil with rhizosphere soil or the surface
with the inside of the plant. However, the species diversity
of plant-associated microorganisms is important, and many
bacterial and fungal taxa have been identified on leaves or
roots (Lindow and Brandl 2003; Morris and Monier 2003;
Garbeva et al. 2004).
Selection of microorganisms by plants can be observed at
different taxonomic levels, from the family to the strain
(Mavingui et al. 1992; Lindow and Brandl 2003; Garbeva
et al. 2004; Cardon and Whitbeck 2007). At the lowest
taxonomic levels, especially the intraspecies level, horizontal gene transfer can influence microbial selection. Indeed,
plants favor horizontal gene transfer events, including the
exchange of conjugative plasmids between bacteria
(Bjorklof et al. 2000). Many abiotic and biotic factors modulate microbial selection by the plant, mainly through an
effect on plant photosynthetic activity (and hence on exudation). This can be reflected by the occurrence of microbial
successions in the rhizosphere, which can be related to host
phenology (Garbeva et al. 2004; Mougel et al. 2006). Plant
selection processes are also scale dependent. Since both the
soil habitat and plant organization/physiology display spatiotemporal heterogeneity, different parts of a same individual plant may display different microbial communities, e.g.,
from one root microsite to another (Garbeva et al. 2004).
In the rhizosphere, the reduction of microbial diversity
resulting from plant selection may be partly compensated by
other processes that enhance genetic variability of microorganisms. First, it is believed that certain constituents
released by the plant, particularly the seed, may have mutagenic effects (Miche ´ et al. 2003). Second, certain bacteria
display phenotypic variation (also termed phase variation), a
process often reversible that generates at high frequency
several different cell types (e.g., with different mobility
patterns) from a single strain (Vial et al. 2006). Phenotypic
variation facilitates root colonization of symbiotic and pathogenic bacteria that have this property (Achouak et al. 2004).
11.3.4.3 Microbial Activities
For microorganisms adapted to plants, trophic stimulation
by exudates leads to an increase in the rates of cell physiological activities, the synthesis of many metabolites (including microbial exopolysaccharides of root mucigel), the rate
of proliferation, and (for bacteria with a viable nonculturable state) the culturability level of cells (Bjorklof
et al. 2000; Lu ¨beck et al. 2000; Bais et al. 2006; Troxler
et al. 2012). This trophic stimulation results in an increase in
overall physiological activity of the microbial community
(van Elsas et al. 2007), for example, in terms of carbon
dioxide production (Griffiths et al. 2004). When considering
a particular microbial function, the plant may have an impact
on the size of the corresponding functional group (by a factor
of 100 or more for rhizosphere ammonifiers) and/or the
implementation level of the function (Cardon and Whitbeck
2007; Patra et al. 2007). This impact varies according to the
stage of development of the plant, the age of the root or leaf,
environmental factors influencing photosynthesis (which
also impacts on microbial numbers and diversity), and the
microbial function considered.
Generally, microbial transformations involving heterotrophic/saprophytic microorganisms are strongly stimulated
by plants (Cardon and Whitbeck 2007). This is the case for
many biodegradation functions for which the substrate
comes exclusively/predominantly from plant exudates
(Griffiths et al. 2004), as in the case of calystegines (Guntli
et al. 1999) and opines, or both from exudates and soil
organic matter (organic nitrogen compounds, cellulose,
etc.). Substrates not of plant origin such as exogenous aromatic compounds degraded by cometabolism are
transformed faster in the rhizosphere (Cardon and Whitbeck
2007). Plants also favor nitrogen fixation (whose energy cost
is high) by nonsymbiotic aerobic bacteria (Patra et al. 2007).
Conversely, transformations carried out by autotrophic
microorganisms (e.g., nitrification) are little affected by the
presence of the plant (Patra et al. 2006). Finally, there are
transformations that are either stimulated or inhibited by the
plant depending on the availability of oxygen and overall
redox conditions in the rhizosphere. This is mainly the case
of fermentations and anaerobic respirations, e.g., denitrification (Patra et al. 2006), which are favored by the presence of
organic rhizodeposits but also require specific redox
conditions partly determined by soil structure and soil
410
Y. Moe ¨nne-Loccoz et al.
(Liesack et al. 2000). Depending on these factors, the availability of oxygen in the root zone will be lower (most often)
or higher than in non-rhizosphere soil.
11.3.4.2 Microbial Diversity
To colonize plants, a microorganism must not only use the
trophic resources they provide (in a context of competition
with the rest of the microbial community) but also tolerate
abiotic stress conditions (including desiccation and UV in the
phyllosphere) as well as toxins and other host defense
compounds. The best adapted microorganisms will be thus
favored over the others. This selection process is amplified by
the molecular dialogues with the plant, including microbial
chemotaxis/chemotropism phenomena (cf. Sect. 9.2) and the
ability of certain plants to interfere with bacterial quorum
sensing (Bauer and Robinson 2002). Finally, all terrestrial
microorganisms are not affected the same way by the antimicrobial compounds produced by the other microorganisms
associated with plant (Gilbert et al. 1993; Raaijmakers et al.
2009) and by predation by protozoa (Bonkowski 2004) and
nematodes (Jousset et al. 2009). In total, the trophic stimulation of microbial growth by the plant is therefore selective.
This usually results in a lower microbial diversity when
comparing bulk soil with rhizosphere soil or the surface
with the inside of the plant. However, the species diversity
of plant-associated microorganisms is important, and many
bacterial and fungal taxa have been identified on leaves or
roots (Lindow and Brandl 2003; Morris and Monier 2003;
Garbeva et al. 2004).
Selection of microorganisms by plants can be observed at
different taxonomic levels, from the family to the strain
(Mavingui et al. 1992; Lindow and Brandl 2003; Garbeva
et al. 2004; Cardon and Whitbeck 2007). At the lowest
taxonomic levels, especially the intraspecies level, horizontal gene transfer can influence microbial selection. Indeed,
plants favor horizontal gene transfer events, including the
exchange of conjugative plasmids between bacteria
(Bjorklof et al. 2000). Many abiotic and biotic factors modulate microbial selection by the plant, mainly through an
effect on plant photosynthetic activity (and hence on exudation). This can be reflected by the occurrence of microbial
successions in the rhizosphere, which can be related to host
phenology (Garbeva et al. 2004; Mougel et al. 2006). Plant
selection processes are also scale dependent. Since both the
soil habitat and plant organization/physiology display spatiotemporal heterogeneity, different parts of a same individual plant may display different microbial communities, e.g.,
from one root microsite to another (Garbeva et al. 2004).
In the rhizosphere, the reduction of microbial diversity
resulting from plant selection may be partly compensated by
other processes that enhance genetic variability of microorganisms. First, it is believed that certain constituents
released by the plant, particularly the seed, may have mutagenic effects (Miche ´ et al. 2003). Second, certain bacteria
display phenotypic variation (also termed phase variation), a
process often reversible that generates at high frequency
several different cell types (e.g., with different mobility
patterns) from a single strain (Vial et al. 2006). Phenotypic
variation facilitates root colonization of symbiotic and pathogenic bacteria that have this property (Achouak et al. 2004).
11.3.4.3 Microbial Activities
For microorganisms adapted to plants, trophic stimulation
by exudates leads to an increase in the rates of cell physiological activities, the synthesis of many metabolites (including microbial exopolysaccharides of root mucigel), the rate
of proliferation, and (for bacteria with a viable nonculturable state) the culturability level of cells (Bjorklof
et al. 2000; Lu ¨beck et al. 2000; Bais et al. 2006; Troxler
et al. 2012). This trophic stimulation results in an increase in
overall physiological activity of the microbial community
(van Elsas et al. 2007), for example, in terms of carbon
dioxide production (Griffiths et al. 2004). When considering
a particular microbial function, the plant may have an impact
on the size of the corresponding functional group (by a factor
of 100 or more for rhizosphere ammonifiers) and/or the
implementation level of the function (Cardon and Whitbeck
2007; Patra et al. 2007). This impact varies according to the
stage of development of the plant, the age of the root or leaf,
environmental factors influencing photosynthesis (which
also impacts on microbial numbers and diversity), and the
microbial function considered.
Generally, microbial transformations involving heterotrophic/saprophytic microorganisms are strongly stimulated
by plants (Cardon and Whitbeck 2007). This is the case for
many biodegradation functions for which the substrate
comes exclusively/predominantly from plant exudates
(Griffiths et al. 2004), as in the case of calystegines (Guntli
et al. 1999) and opines, or both from exudates and soil
organic matter (organic nitrogen compounds, cellulose,
etc.). Substrates not of plant origin such as exogenous aromatic compounds degraded by cometabolism are
transformed faster in the rhizosphere (Cardon and Whitbeck
2007). Plants also favor nitrogen fixation (whose energy cost
is high) by nonsymbiotic aerobic bacteria (Patra et al. 2007).
Conversely, transformations carried out by autotrophic
microorganisms (e.g., nitrification) are little affected by the
presence of the plant (Patra et al. 2006). Finally, there are
transformations that are either stimulated or inhibited by the
plant depending on the availability of oxygen and overall
redox conditions in the rhizosphere. This is mainly the case
of fermentations and anaerobic respirations, e.g., denitrification (Patra et al. 2006), which are favored by the presence of
organic rhizodeposits but also require specific redox
conditions partly determined by soil structure and soil
410
Y. Moe ¨nne-Loccoz et al.