TMP 8 E98

Review paper
Root exudates mediated interactions belowground

Feth el Zahar Haichar
a, *
, Catherine Santaella
b, c, d
, Thierry Heulin
b, c, d
,
Wafa Achouak
b, c, d
a
UMR CNRS 5557, Ecologie Microbienne, IFR41 Bio-Environnement et Sante, Universite Lyon 1, 69622 Villeurbanne, France
b
CEA, DSV, IBEB, Lab Ecol Microb Rhizosphere & Environ Extrem (LEMiRE), 13108 Saint-Paul-lez-Durance, France
c
CNRS, UMR7265 BVME, ECCOREV FR3098, 13108 Saint Paul-Lez-Durance, France
d
Aix Marseille Universite, 13284 Marseille Cedex 07, France
a r t i c l e i n f o
Article history:
Received 21 March 2014
Received in revised form
13 June 2014
Accepted 15 June 2014
Available online 3 July 2014
Keywords:
Plantemicrobe interactions
Signalling molecules
Defence
Symbiosis
Chemotaxis
Nutrients
a b s t r a c t
The root exudate composition reects the contradictory-concomitantly attractive and repulsive-
behaviour of plants towards soil microorganisms. Plants produce antimicrobial, insecticide and nema-
ticide compounds to repel pathogens and invaders. They also produce border cells that detach from roots
and play an important role as biological and physical barrier against aggressors. Plants produce also
metabolites used as carbon source resulting in the attraction of phytobenecial soil microorganisms that
help plants in controlling diseases directly via the production of antimicrobial compounds or indirectly
via the induction of plant systemic resistance. The root exudates may have a direct impact on carbon and
nitrogen cycling, as they exhibit a rhizosphere priming effect towards soil organic matter degraders, and
may inhibit nitrication process by soil nitrifying microorganisms. They also contain signalling molecules
required for the establishment of plant-microorganisms interactions. The composition of root exudates
is therefore broad ranging, consisting of feeding, antimicrobial and signalling molecules. We thus focused
this review on current research concerning the role of the root exudate composition in plant-micro-
organisms interactions and functioning of the rhizosphere.
2014 Elsevier Ltd. All rights reserved.
1. Introduction
The rhizosphere is best dened as the volume of soil around
living roots, which is inuenced by root activity (Hiltner, 1904). This
is a densely populated area inwhich plant roots must compete with
the invading root systems of neighbouring plants for space, water
and mineral nutrients, and with other soil-borne organisms,
including bacteria, fungi and insects feeding on the abundant
source of organic material (Ryan and Delhaize, 2001; Bais et al.,
2004a).
The ability to secrete a wide range of compounds into the
rhizosphere is one of the most remarkable metabolic features of
plant roots, with around 5e21% of total photosynthetically xed
carbon being transferred into the rhizosphere through root exu-
dates (Whipps, 1990; Marschner, 1995; Nguyen, 2003; Derrien
et al., 2004). The quantity and quality of root exudates depend on
the plant species, the age of individual plants and external biotic
and abiotic factors (Jones et al., 2004).
Root exudates are often divided into two classes of compounds:
i) low-molecular weight compounds such as amino acids, organic
acids, sugars and other secondary metabolites, which account for
much of the root exudate diversity, whereas ii) high-molecular
weight exudates, such as mucilage (polysaccharides) and pro-
teins, account for a large proportion of root exudates in terms of
mass (Badri and Vivanco, 2009).
Through the exudation of a wide variety of compounds, roots
may regulate the soil microbial community in their immediate vi-
cinity, cope with herbivores, foster benecial symbioses, change
the chemical and physical properties of the soil, and inhibit the
growth of competing plant species (Nardi et al., 2000; Walker et al.,
2003). Indeed, in addition to providing a carbon- and energy-rich
environment, plants recognize and actively respond specically to
different microorganisms encountered in the rhizosphere, initi-
ating communication with soil microbial communities by produc-
ing signals that modulate colonisation. Plants mediate both positive
and negative interactions in the rhizosphere via root exudates (Bais
et al., 2006; Philippot et al., 2013). The positive interactions include
symbiotic associations with benecial microbes, such as rhizobia,
* Corresponding author.
E-mail addresses: zahar.haichar@univ-lyon1.fr, haichar@yahoo.fr (F.Z. Haichar),
catherine.santaella@cea.fr (C. Santaella), thierry.heulin@cea.fr (T. Heulin), wafa.
achouak@cea.fr (W. Achouak).
Contents lists available at ScienceDirect
Soil Biology & Biochemistry
j ournal homepage: www. el sevi er. com/ l ocat e/ soi l bi o
http://dx.doi.org/10.1016/j.soilbio.2014.06.017
0038-0717/ 2014 Elsevier Ltd. All rights reserved.
Soil Biology & Biochemistry 77 (2014) 69e80
mycorrhiza and plant growth promoting rhizobacteria (PGPR).
Negative interactions include associations with parasitic plants,
pathogenic microbes and invertebrate herbivores.
Here we review the large body of literature that has been pub-
lished on root exudates and their interaction with soil organisms,
while assessing current knowledge related to how plants, via root
exudates, mediate communication with microbial communities in
the rhizosphere.
2. Rhizodeposition concept
For over a century it has been known that plants can dramati-
cally modify their soil environment through the release of carbon
compounds (rhizodeposition) from living plant roots, giving rise to
the so-called rhizosphere effect (Hiltner, 1904). The release of car-
bon (C) from root epidermal and cortical cells leads to a prolifera-
tion of microorganisms within (endorhizosphere) or on the root
surface (rhizoplane), and outside the roots (ectorhizosphere) (Jones
et al., 2004). The rhizosphere may contain up to 10
6
e10
9
bacteria,
10
4
protozoa, 10
1
e10
2
nematodes and 10
5
e10
6
fungi per gram of
rhizosphere soil (Watt et al., 2006; Hinsinger et al., 2009; Mendes
et al., 2013).
The C release in the rhizosphere leads to chemical, physical and
biological characteristics that differ from those of the bulk soil
(Barber and Martin, 1976). The magnitude of these changes in soil
properties is largely determined by the amount and type of C
release from the roots, as well as intrinsic soil characteristics (Jones
et al., 2004; Alami et al., 2000).
The amount of carbon exuded by plants has been quantied
relatively easily in the absence of soil by growing roots in sterile
hydroponic culture and collecting the carbon accumulating in the
external media (for review, Nguyen, 2003). However, this method
lacks ecological relevance (Jones et al., 2009).
The introduction of tracer techniques for labelling of root-
derived C has led to signicant progress of the estimation of C
input into soil (Jones et al., 2009). For example, Kuzyakov and
Domanski (2000) estimated that cereals (wheat and barley) and
pasture plant transfer 20e30% and 30e50% of total assimilated
carbon into the soil respectively. Derrien et al. (2004) estimated to
16% the C input into the soil by wheat plant using
13
CO
2
labelling for
5 h.
Different rhizodeposit nomenclatures have been proposed
based, for instance, on the mechanisms of release, biochemical
nature or functions of rhizodeposits in the rhizosphere (Jones et al.,
2009).
Exudates
Root exudates are part of the rhizodeposition process, which is
the major source of soil organic carbon released by plant roots
(Hutsch et al., 2000; Nguyen, 2003). Exudates are dened as soluble
low-molecular weight components which are lost simply through
passive diffusion and over which the plant exerts little control
(basal exudation) (Bertin et al., 2003; Bais et al., 2006). These ex-
udates include amino acids, organic acids, sugars, phenolics and
other secondary metabolites. Their concentration inside roots is
typically many orders of magnitude greater than in the surrounding
soil solution due to continual removal from the soil by the soil
microbial community and replenishment of internal pools by the
roots (Jones et al., 2009).
Mucilage
Root mucilage forms a gelatinous layer surrounding root tips
and is one of the few clearly visible signs of organic C excretion
from roots (Jones et al., 2009). This substance is mainly composed
of polysaccharides, proteins and some phospholipids (Read et al.,
2003). In most situations, mucilage released into the soil has a
wide range of benets for plants, such as protecting the root mer-
istem from toxic metals, enhancing soil aggregate stability, which
in the long run promotes soil aeration, root growth, prevents soil
erosion and maintains a continuous water ow towards the
rhizoplane (Read et al., 2003). The amounts of mucilage synthe-
sized in vitro range from 11 to 47 mg dm/mg root dm (Nguyen,
2003). However, theses quantities were determined from roots
grown in water or in nutrient solution, which increases the out-
ward diffusion of the mucilage from the periplasmic region (Sealey
et al., 1995). At the present time, to our knowledge, the amount of
mucilage produced in soil remains unknown.
Border cells
Many plants can produce large numbers of metabolically active
root border cells, which are programmed to separate from each
other and to be released from the root cap periphery into the
external environment (Hawes et al., 2000; Stubbs et al., 2004).
Experimentally, border cells can be released into suspension by
brief immersion of the root tip inwater (Hawes and Brigham, 1992).
The separated cells adhere to the root tip in the absence of free
water. The daily rate of border cell production is highly variable
among plant species, from a dozen in tobacco to more than
10,000 cells/day for cotton and pine, with release rates being highly
dependent upon the prevailing environmental conditions (Hawes
and Brigham, 1992).
Gases such as ethylene, CO
2
and H
2
Plant roots release CO
2
into the soil environment from carbo-
hydrate respiration and stimulation by lumichrome, a plant and
bacterial exudate molecule (Phillips et al., 1999). These accumula-
tions are up to 17.5% in the root zone and increased levels of CO
2
can
enhance the dissolution of soil CaCO
3
to produce Ca
2
for plant
uptake (Dakora and Phillips, 2002).
Hydrogen gas (H
2
) is a major byproduct of N
2
xation in le-
gumes, and its production consumes about 5% of net photosyn-
thesis (Dong and Layzell, 2001). Some rhizobia possess genes
encoding for an uptake hydrogenase (Hup) enzyme, which enables
H
2
to be oxidized by the bacteria to yield more energy. However,
many symbioses, lack this uptake hydrogenase (Hup
), and the H
2
produced by the nitrogenase diffuses out of the nodule into the
soil (Golding et al., 2012). This H
2
loss from nodules to soil is
traditionally considered as a disadvantage in Hup
versus Hup
symbiosis. However, the release of H

2
from nodules alters soil
biology and may indirectly contribute to plant growth (Dong and
Layzell, 2001; Dong et al., 2003). Indeed, the presence of H
2
stimulates the soil H
2
-oxidizing bacterial community that may
foster plant growth promotion through various mechanisms such
as the increase of root elongation by decreasing ethylene levels in
the host plant (Golding et al., 2012), and their presence is bene-
cial to leguminous and non-leguminous plants (Maimaiti et al.,
2007).
2.1. Factors affecting rhizodeposition pattern
Biotic and abiotic factors affecting the release of C fromthe roots
into the soil are numerous and have been extensively reviewed
(Whipps, 1990; Jones et al., 2009). For example, the enormous
plasticity of root growth and root exudation in response to different
soil conditions and particularly to stress factors, such as nutrient
limitation, mineral toxicities, and extremes in soil moisture and soil
F.Z. Haichar et al. / Soil Biology & Biochemistry 77 (2014) 69e80 70
structure, is a well-described phenomenon (Jones et al., 2004;
Neumann et al., 2014).
The literature shows that the total amount of organic C depos-
ited in the rhizosphere can vary greatly according to the plant
ecophysiology. Both the environment and the plant genetics and
physiology can inuence (1) the ux of C from each root to the
rhizosphere, which is related to the root functioning, and (2) the
size and the morphology of the overall root (Nguyen, 2003).
A number of elegant experiments using pulse labelling experi-
ments demonstrate that plant age signicantly inuence C parti-
tioning of photoassimilates between plant-soil compartments (for
review, Kuzyakov and Domanski, 2000; Nguyen, 2003). As the plant
gets older, less carbon is partitioned to belowground. For example,
Meharg and Killham (1990) demonstrated that Lolium perenne
plant translocated 67% and 14% of assimilated
14
CeCO
2
into the soil
after 4 week and 24 week of growing, respectively. Exudation rates
vary with plant developmental stage and also between genotypes
within a single species. Seedlings produce the lowest amounts of
root exudates; this gradually increases until owering and de-
creases again at maturity (Aulakh et al. 2001).
Root branching and root system architecture play a signicant
role in determining the composition of exudates both quantita-
tively and qualitatively (for review, Watt et al., 2006; Badri and
Vivanco, 2009). In general, the zone immediately behind the root
tip is considered to be a major site of exudation (Schroth and
Snyder, 1962). However, it has been observed that the older parts
of the roots also exude organic compounds, and different sites have
been recorded for different plant species (McDougall, 1968; Rovira,
1969). Frenzel (1960) reported that different compounds were
released from different parts of root system: asparagine and thre-
onine from the meristem and root elongation zone; glutamic acid,
valine, leucine and phenylalanine from root hair zone; and aspartic
acid from the whole root. In legumes, young root hairs and cortical
cells around emerging branching roots release avonoids to trigger
nodules only in these root regions (Mathesius et al., 2000).
McDougall and Rovira (1970) used
14
C-labelled compounds to
identify the sites of exudation from wheat roots, and noticed that
non-diffusible material released from both primary and lateral root
tips, and diffusible material released fromthe whole length of roots.
Exudation patterns can also differ in response to the neigh-
bouring plant. Indeed, plants use root-secreted secondary me-
tabolites to regulate the rhizosphere to the detriment of
neighbouring plants (Bais et al., 2004a). This negative plante-
plant interaction is called allelopathy. Plants can produce and
release potent phytotoxins that reduce the establishment,
growth, or survival of susceptible plant neighbours, thus
reducing competition and increasing resource availability (for
review, Weir et al., 2004). Recent evidence suggests that some
plant species can better withstand assault by () catechin, a
potential allelotoxin produced by Centaurea maculosa (spotted
knapweed) through increased secretion of oxalic acid, which
protects the roots against damage incurred by reactive oxygen
species (ROS) resulting from interactions with the allelochemical
(Weir et al. 2006). Analysis of eld soils near C. masculosa
revealed that they contain up to 1.5 mg of () catechin g
1
soil
dm (Perry et al., 2005). Moreover, catechin has been reported at
very low concentration in the rhizosphere of Centaurea stoebe
but higher concentrations may occur periodically (Tharayil and
Triebwasser, 2010).
In this review, we considered the root exudates in terms of
rhizodeposition, including passive and active release of com-
pounds from roots into the soil and the release of border cells from
the root cap. Root exudation clearly represents a signicant carbon
cost for the plant. Stimulation of heterotrophic microbial commu-
nities such as PGPR by root exudates will in return be benecial for
plant growth and health. Plant root exudation is thus a necessary
short-, medium- and long-term investment.
The following sections of this review examine the communi-
cation process established by plant and mediated by root exudates
between plant roots and other microorganisms in the rhizosphere.
3. Plantemicrobe interaction mediated by root exudates
For plants, root exudates represent an important component of
communication with rhizosphere-inhabiting microorganisms
(Fig. 1) and, for this communication, a broad range of substrates and
signalling molecules are produced by plants. Overall, plants pro-
duce a compositionally diverse array of more than 100,000
different low-molecular mass natural products, known as second-
ary metabolites (Bais et al., 2004b). Some of these secondary me-
tabolites have been identied and their functions in the
rhizosphere have been elucidated (Table 1).
3.1. Potential of root exudates to cope with pathogens
Plants, through the exudation of a wide variety of compounds,
attract soil microbial communities, including pathogens, in their
immediate vicinity. Plant roots are relentlessly attacked by patho-
gens via different strategies:
3.1.1. Secretion of antimicrobial compounds
Plants host a broad range of natural products, many of which
have evolved to confer selective advantage to cope with microbial
attacks. Several studies have highlighted the existence of induced
low-molecular mass compounds, respectively referred to as phy-
toanticipins or phytoalexins, and the secretion of a battery of
defence proteins with antimicrobial activity (Bais et al., 2004a,
2006). For example, Walker et al. (2004) showed that during
Pseudomonas aeruginosa infection sweet basil roots secrete ros-
marinic acid (RA), a multifunctional caffeic acid ester that exhibits
in vitro antibacterial activity against P. aeruginosa. Based on geno-
mics data, it was shown that rice, corn, soybean, Arabidopsis thali-
ana and Medicago truncatula are able to produce antimicrobial
indol, terpenoid, benzoxazinone and avonoid natural products
(Bais et al., 2006). Lanoue et al. (2010) showed that, under Fusarium
graminearum attack, the barley (Hordeum vulgare) root system
secreted phenolic compounds with antimicrobial activity. This
secretion of de novo biosynthesized t-cinnamic, p-coumaric, ferulic,
syringic and vanillic acids, identied using liquid chromatography
with photodiode array detection (LC-DAD), was induced within 2
days after Fusarium inoculation. These ndings illustrate the dy-
namics of plant defence mechanisms at the root level. In addition,
in vivo labelling experiments with
13
CO
2
revealed that the secreted
t-cinnamic acid was synthesized de novo within 2 days of fungal
infection. These results suggest that barley plants under attack
respond by de novo biosynthesis and secretion of compounds with
antimicrobial functions that may mediate natural disease
resistance.
In a recent study, the diterpene rhizathalene A was found to be
constitutively produced and released by non-infected A. thaliana
roots (Vaughan et al., 2013). Plants that do not produce rhizatha-
lene A were found to be more susceptible to herbivorous insect
attacks.
A new role was discovered for strigolactones, another class of
terpenoids, that have been extensively studied as phytohormones
and compounds involved in plant symbiosis and in plant infection
by plant root parasites (Xie et al., 2010). The synthetic strigolactone
analog GR24 inhibits the growth of an array of phytopathogenics
fungi when present in the growth medium (Dor et al., 2011), indi-
cating that secreted strigolactones can affect natural enemies
directly or indirectly by modulating hormonal defence pathways
while contributing to belowground plant biotic stress responses
(Dor et al., 2011; Torres-Vera et al., 2013; Baetz and Martinoia,
2013).
Plant families are known to produce some specic chemical
structures for defence (e.g. isoavonoids of Leguminoseae and
sesquiterpenes of Solanaceae), although some chemical classes
have defence functions across plant taxa (e.g. phenylpropanoid
derivatives) (Dixon, 2001). Plants of the Brassicaceae family pro-
duce glucosinolates as secondary metabolites, which are stored in
plant cell vacuoles. When bacteria, fungi or insects infect plants,
glucosinolates are produced along with myrosinase enzymes, cat-
alysing hydrolysis of glucosinolates into isothiocyanates, thiocya-
nates and nitriles that have antimicrobial activities (Halkier and
Gershenzon, 2006).
Plant roots also secrete an array of proteins to defend the plant
against potential soil-borne pathogens. The study of De-la-Pena
et al. (2008) demonstrated that the A. thalianaePseudomonas
syringae (DC3000) interaction induced the secretion of several
plant defence-related proteins. Park et al. (2002) showed that the
hairy roots of pokeweed (Phytolacca americana) are able to secrete
various defence proteins including PAP-H, a ribosome-inactivating
protein (RIP). RIPs are widely distributed plant enzymes that inhibit
protein synthesis by virtue of their N-glycosidic activity, selectively
cleaving an adenine residue from a highly conserved and surface-
exposed stem loop structure in 28S rRNA. This PAP-H has in vitro
N-glycosidase activity against fungal ribosomes, suggesting that
PAP-H can recognize and depurinate fungal ribosomes (Hudak
et al., 2000; Rajamohan et al., 2000; Parck et al., 2002). PAP-H
penetration into the fungal cells may be facilitated by PR proteins
such as chitinase, b-1,3-glucanase, and proteases. Both chitinase
and b-1,3-glucanase are widely distributed enzymes in higher
plants, and have been hypothesized to function synergistically in
plant defence against fungal pathogens (reviewed by Ohme-Takagi
et al., 2000).
These results obtained in vitro suggest that bioactive proteins
and secondary metabolites secreted by plant root may be involved
in plant defence against pathogenic microorganisms. These nd-
ings deserve to be conrmed under natural conditions.
3.1.2. Quorum-sensing inhibition
Many pathogenic bacteria such as Erwinia spp., Pseudomonas
spp. and Agrobacterium spp. possess quorum-sensing (QS) systems
that control the production and secretion of virulence factors (Fray,
2002). Briey, QS is a form of cell-to-cell communication between
bacteria mediated by small diffusible signalling molecules (auto-
inducers, AI), which are responsible for the coordinated actions of
bacteria reaching the quorum. The most commonly reported
types of AI signals are N-acyl homoserine lactones (AHLs) for Pro-
teobateria and peptide-signalling molecules for Firmicutes (Waters
and Bassler, 2005). Bacteria that use QS also have a receptor that
can specically detect signalling molecules, and when the inducer
Fig. 1. Representation of the complex interactions that take place in the rhizosphere between plant roots and microorganisms mediated by root exudates. Roots produce
chemical signals that attract bacteria and induce chemotaxis. Positive interactions mediated by root exudates including growth facilitators or growth regulator mimics that support
growth of plants. Conversely, negative interactions mediated by root exudates involve secretion of antimicrobials, phytotoxins, nematicidal and insecticidal compounds. The arrows
in the panels indicate chemical exchange. PGPR, plant growth promoting rhizobacteria; N, nitrogen; P, phosphate; QS, quorum-sensing.
binds the receptor it activates transcription of target genes,
including those required for inducer synthesis.
The rhizosphere contains a higher proportion of AHL-producing
bacteria as compared to the bulk soil, suggesting that they play a
role in root colonization (Elasri et al., 2001).
Plants have evolved strategies to interfere with the bacterial
AHL signalling system to avoid pathogenesis. Such interference
includes the production of signal mimics, signal blockers, signal-
degrading enzymes, or compounds that block the activity of the
AHL-producing enzymes (Fray, 2002; Rasmussen and Givskov,
2006).
A few years ago, it was reported that root exudates of pea
seedlings (Pisum sativum) had several separable activities that
mimicked AHL signals in well-characterized bacterial reporter
strains, stimulating AHL-regulated behaviours in some strains and
inhibiting them in others (Teplitski et al., 2000). For example, the
addition of root exudates from pea seedlings to a Chromobacterium
violaceum culture inhibits the production of violaceine and exo-
enzymes, which are under the control of QS and involving AHLs.
The compounds responsible have not been identied, but they
preferentially partition into polar solvents. Various species of
higher plants, including pea (P. sativum), crown vetch (Coronilla
varia), M. truncatula, rice (Oryza sativa), soybean (Glycine max) and
tomato (Lycopersicum lycopersicon), were found to secrete com-
pounds having AHL-mimicking activities (Teplitski et al., 2000;
Rasmussen et al., 2005a). AHL signal-mimicking compounds seem
to be important in determining the outcome of interactions be-
tween higher plants and a diverse range of pathogenic
microorganisms.
As mentioned above, another QS interference strategy is inac-
tivation or complete degradation of generated signal molecules.
This can be achieved by different methods such as chemical and
enzymatic degradation. A simple way to inactivate AHL signal
molecules is to increase the pH to above 7, which causes AHL lac-
tonolysis (ring opening) (Yates et al., 2002). A number of higher
organisms use this strategy in defence against invading QS bacteria.
Plants infected with the tissue-macerating plant pathogen Erwinia
carotovora will, as a rst response, actively increase the pH at the
attack site (Yates et al., 2002). This alkalinisation will in turn pre-
vent expression of QS-controlled genes and virulence factors.
In addition to the secretion of AHL-mimicking molecules,
Rasmussen et al. (2005b), using gene chip-based transcriptomics
analysis, revealed that garlic extract contains several QS inhibitors
(QSIs) with specicity for QS-controlled virulence genes in
P. aeruginosa. These QSIs also signicantly reduced P. aeruginosa
biolm tolerance to tobramycin treatment, as well as virulence in a
Caenorhabditis elegans pathogenesis model.
QS is currently an obvious target for a novel class of antimi-
crobial drugs, which would function to efciently block reception of
cognate QS signals in vivo, and thereby be capable of inducing
chemical attenuation of pathogens (Defoird et al., 2010).
3.1.3. Secretion of border cells
Newly synthesized plant tissues such as root tips are inherently
sensitive to biotic and abiotic injury. Indeed, newly synthesized
tissues in the elongation region just behind the root tip is the pri-
mary site where infection by nematodes, fungi, and bacteria is
initiated (Wen et al., 2007). Yet, surprisingly, the 1e2 mm apical
Table 1
Potential functional role of root exudate components identied from different rhizospheres, e.g. tomato, Brassica napus and others (adapted from Jones et al., 2004; Badri and
Vivanco, 2009; Vranova et al., 2013).
Exudates component Functions Specic compounds identied in root exudates
Organic acids Nutrient source
Chemoattractant signals to microbes
Chelators of poorly soluble mineral nutrients
Acidiers of soil
Detoxiers of Al
nod gene inducers
Citric, glutaric, oxalic, malonic
Malic, aldonic, fumaric, erythronic
Succinic, ferulic, acetic, butanoic
Butyric, syringic, valeric, rosmarinic, lactic, glycolic
trans-cinnamic, piscidic, formic
aconitic, pyruvic
vanillic, tetronic
Amino acids Nutrient source
a- and b-alanine proline
asparagine, valine, threonine, aspartate, tryptophan cystein,
ornithine, cystine, histidine, glutamate, arginine, glycine,
homoserine, isoleucine, phenylalanine, leucine, -Aminobutyric acid,
lysine a-Aminoadipic acid, methionine, serine, homoserine
Sugars & Vitamin Promoters of plant and microbial growth nutrient source Glucose, desoxyribose, oligosaccharides galactose, biotin,
maltose, thiamin, ribose, niacin, xylose, rafnose pantothenate,
rhamnose, rhiboavin, arabinose, fructose
Proteins and enzymes Catalysts for P release from organic molecules
Biocatalysts for organic matter transformations
Plante defence
Acid/alkaline, phosphatase
amylase, invertase, prot ease
PR proteins, lipases, b-1,3-glucanases
Purines Nutrient source Ad enine, guanine, cytidine, uridine
Inorganic ions and gases Chemoattractant signals to microbes HCO
3
OH
CO
2
H
2
Phenolics Nutrient source
Microbial growth promoters
nod gene inducers and inhibitors in rhizobia
Resistance inducers against phytoalexins
Detoxiers of Al
Phytoalexins against soil pathogens
Liquiritigenin, luteolin
Daidzein, 4
0
,7-dihydroxyavanone
Genistein, 4
0
,7-dihydroxyavone
Coumetrol, 4,4
0
-dihydroxy-2'-methoxychalcone
Eriodictyol, 4
0
-7-dihydroxyavone
3,5,7,3
0
-tetrahydroxy- 4
0
methoxyavone
naringenin
isoliquiritigenin, 7,3
0
-dihydroxy-4
0
-methoxyavone
umbelliferone, ()- and ()- catechin
Root border cells Produce signals that control mitosis
Produce signals controlling gene expression
Stimulate microbial growth
Release chemoattractant
Synthesize defense molecules for the rhizosphere
Act as decoys that keep root cap infection-free
Release mucilage and proteins
region hosting the root cap and root meristem in plants grown in
soil, hydroponic or laboratory conditions is highly resistant to mi-
crobial infection. The resistant region is correlated closely with the
presence of root border cells on the cap periphery (reviewed by
Hawes et al., 2003). Several lines of evidence suggest that these
cells, which in most species are programmed to be released from
the cap as a metabolically active population of cells into the
rhizosphere, may play a key role in root development and health
(Hawes et al., 2003; Driouich et al., 2007). Border cells can: (1)
attract and immobilize nematodes, (2) attract zoospores, (3) syn-
thesize defensive structures in response to pathogen attacks and
(4) repel or bind pathogenic bacteria (reviewed by Hawes et al.,
2000, 2003).
A number of studies have provided evidence that border cells
play key role in controlling root interaction with living microbes of
the rhizosphere (Vicr e et al., 2005). First, the number of border cells
increases in response to different stimuli, including pathogens,
metals, carbon dioxide and secondary metabolites (Driouich et al.,
2013). Secondly, border cells are capable of attracting or repelling
pathogenic microorganisms, including bacteria, nematodes and
oomycetes. For example, the infection of pea (P. sativum) roots by
the soil-borne pea pathogen Necteria haematococca revealed an
absence of infection within root tips (Gunawardena and Hawes,
2002, 2005). Recently, Plancot et al. (2013) demonstrated that
root border-like cells of ax and A. thaliana are able to perceive an
elicitation and activate defence responses. In addition, instanta-
neous attraction of nematodes to border cells was clearly observed
when a pea root was placed on water agar inoculated with nema-
todes. Within 30 min, the nematode motility ceased and they
became rigid and inert (Hawes et al., 2000). This immobilization
effect is reversible within a few hours to a few days. If a similar
process occurs in the soil, by the time the nematodes resume their
motility, a root tip growing at a rate of 1 mm/h would be long past
being in danger of penetration (Hawes et al., 2000).
Border cells of legumes and cereals produce a mucilage layer in
response to co-cultivation with pathogenic bacteria (Hawes et al.,
2000). This layer appears to cover root tips and consequently re-
pels them from pathogenic bacteria colonization. Humphrisa et al.
(2005) demonstrated that border cells of Zea mays, and their
associated mucilage, prevented complete colonization of the root
tip by the biocontrol agent Pseudomonas uorescens SBW25. Inter-
estingly, studies have revealed that co-cultivation of border cells
with aluminium results in the production of a mucilage layer
similar to that which is formed in response to pathogenic bacteria
(Hawes et al., 2000).
Thirdly, border cells secrete a diverse array of antimicrobial
metabolites. As mentioned above, border cells maintain a high rate
of metabolic activity after detachment. They synthesize and secrete
phytoalexines and diverse antimicrobial enzymes and proteins,
which are involved in root tip protection against pathogenic attacks
(Wen et al., 2007).
Complete suppression of fungal growth was achieved within
48 h after pea border cells were co-cultivated with Nectria hae-
matocca independently of the roots (Gunawardena et al., 2005). In
this study, the authors suggested that a compound released into the
extracellular environment might be responsible for fungal hyphae
growth inhibition.
In a previous study, two-dimensional gel electrophoresis was
used to demonstrate that proles of proteins synthesized by border
cells differ from those of progenitor cells in the root cap of pea
(Brigham et al., 1995). Recently, Wen et al. (2007) tested the impact
of the secretome of border cells in protecting root tips from infec-
tion by directly measuring the ability of N. haematocca to infect root
tips, with and without treatment with a broad spectrumprotease to
destroy the secretome at inoculation. The authors demonstrated
that when this root cap secretome was proteolytically degraded
during inoculation of pea roots with N. haematococca, the per-
centage of infected root tips increased to 100%. A complex of more
than 100 extracellular proteins was conrmed, by multidimen-
sional protein identication technology, to comprise the root cap
secretome, including cellulases, b-galactosidases, invertases, pro-
teases, calmodulins, chitinases, lipoxygenases, ATPases and perox-
ydases (Wen et al., 2007; De-la-Pena et al., 2008; Ma et al., 2010;
Liao et al., 2012).
Wen et al. (2009) reported that, in addition to histone and other
secretome proteins, extracellular DNA (exDNA) is also a root cap
component and, when this exDNA is enzymatically digested, root
tip resistance to infection is abolished. Furthermore, using an
in vitro assay, it has been shown that arabinogalactan proteins
(AGP) synthesized by pea border cells were able to inhibit devel-
opment of the pathogenic oomycete Aphanomyces euteichesdthis
was the rst report on the antimicrobial properties of AGPs
(Cannesan et al., 2011).
Taken together, the observed responses of border cells to
pathogenic fungi, nematodes and aluminium via the production of
a mucilage layer or the secretion of antimicrobial compounds
demonstrated the key role of border cells in root tip protection.
However, all theses data have been observed in vitro and to our
knowledge, there is no evidence of the role of border cells in root tip
protection under natural conditions.
3.2. Root exudates as symbiosis signalling molecules
A molecular interaction between the plant and symbionts ini-
tiates the symbiosis process mediated by the production of specic
signalling molecules.
Below we describe the molecules exuded by the plant that are
involved in legume-rhizobia, plant-AMF and actinorhizal plant-
Frankia interactions.
3.2.1. Rhizobia
Several molecular signalling pathways, particularly in rhizobia-
legume interactions, have been characterised, highlighting the
ability of bacteria to recognize plant-derived compounds.
Indeed, symbiotic interactions between bacteria from the Rhi-
zobiaceae family and their legume host plants (Fabaceae) is the
result of a molecular dialogue involving a succession of recognition
events based on the perception of signal molecules produced and
secreted by both partners. The rst step in plant-rhizobia recog-
nition is based on the exudation by the plant of the molecular
signal, which activates the genes responsible for inducing the
nodulation process (activation of nod genes) (Hirsch et al., 2001).
3.2.1.1. Flavonoids. In addition to their role in plant defence, a-
vonoids have been widely studied for their role in symbiotic in-
teractions. Flavonoids are plant secondary metabolites synthesized
via the central phenylpropanoid pathway and the acetate-malonate
pathway (Winkel-Shirley, 2002; Hassan and Mathesius, 2012).
More than 4000 different avonoids have been identied in
vascular plants, and approximately 30 nod gene-inducing avo-
noids have been isolated from nine legume genera under axenic
conditions (Cooper, 2004). All avonoids consist of two benzene
rings linked through a heterocyclic pyran or pyrone ring. Specic
substitutions on the ring produce avonols, avones, avanones
and isoavonoids, which have been described as being limited to
the legume family. Flavonoides can act as inducers for certain
rhizobia species and antagonists for others (Cooper, 2007). For
example, the two isoavonoids daidzein and genistein, produced
by soybean (G. max), are effective inducers of Bradyrhizobium
japonicum nod genes, but inhibit Sinorhizobium meliloti nod gene
expression. S. meliloti nod genes can be induced by luteolin exuded
by Medicago sativa, whereas Rhizobium sp. NGR234 nod genes can
be induced by different types of avonoids. This specicity enables
rhizobia to distinguish their hosts from other non-host legumes
(Coop, 2007).
Several studies have demonstrated the role of avonoid in vitro
nodule formation using reporter genes (reviewed by Shaw et al.,
2006). Recently, Wasson et al. (2006) demonstrated the inhibition
of nodule formation by using RNA interference to silence chalcone
synthase (CHS), the enzyme that catalyses the rst committed step
of the avonoid pathway in M. truncatula which induces nod genes
in S. meliloti. Nodule formation and avonoid accumulation could
be induced by supplementation of plants with the avonoid pre-
cursors naringenin and liquiritigenin.
Legume roots continuously exude avonoids into the sur-
rounding soil, but the avonoid concentration increases signi-
cantly in the presence of compatible Rhizobium species (Zuanazii
et al., 1998). The exuded avonoids activate the expression of nod
genes in rhizobia (Peck et al., 2006; Wang et al., 2012). These nod
genes are responsible for the synthesis of Nod factorsdbacterial
signals that are necessary for the initiation of nodules, i.e. new
plant organs (D enari e et al., 1996). Nod factors are perceived by a
receptor in the legume host and trigger a sequence of events,
including curling of root hairs around the invading rhizobia, the
entry of rhizobia into the plant through infection threads, and
nodule development (Cullimore et al., 2001). Nodule formation is
continually regulated by both partners and involves mechanisms
controlling both nodule positions and numbers (Wasson et al.,
2006).
Flavonoids have long been hypothesized to regulate nodule
development through their action as auxin transport inhibitors. It
has been suggested that Nod factor perception could induce certain
avonoids that inhibit auxin transport, causing local auxin accu-
mulation at the nodule initiation site, leading to the initiation of
nodule primordia (Mathesius et al., 1998; Boot et al., 1999). This was
recently demonstrated by silencing chalcone synthase in
M. truncatula roots via RNA interference (Wasson et al., 2006).
Moreover, silencing different branches of the avonoid pathway in
M. truncatula showed that avonols such as kaempferol are most
likely to inhibit auxin transport during nodulation (Zhang et al.,
2009).
3.2.1.2. Non-avonoid molecules. Several non-avonoid molecules
exuded by plant roots can induce the expression of nod genes
(Coop, 2007). For example, Phillips et al. (1992) identied trig-
onelline and stachydrine as major components of alfalfa seeds
(M. sativa L.). Moreover, biological assays have shown that these
natural products induce nod gene transcription in S. meliloti by
activating the regulatory NodD protein.
Lupin seeds also release compounds with inducing proper-
ties: aldonic, erythronic and tetronic acid (Gagnon and Ibrahim,
1998). These molecules are also exuded by Lotus corniculatus
thus inducing nod genes in Mesorhizobium loti (Saeki and Kouchi,
2000). Moreover, B. japonicum nod gene transcription can also be
induced by xanthones (Yuen et al., 1995). Other phenolic com-
pounds such as the simple phenolic compounds vanillin and
isovanillin from wheat, a non-legume, are capable of inducing
nod genes in Rhizobium sp. NGR234 (Le Strange et al., 1990).
In addition to their role in plant defence against phytopatho-
gens, border cells released by plant roots are also involved in the
regulation of nod gene expression in rhizobia. Indeed, Zhu et al.
(1997) demonstrated using lacZ reporter genes that components
released by border cells of P. sativum and M. sativa induce nod gene
expression in Rhizobium leguminosarum bv viciae and Rhizobium
meliloti.
3.2.2. Frankia
Actinorhizal symbiosis results from the interaction between the
actinobacterium Frankia and plants belonging to eight dicotyle-
donous families collectively called actinorhizal (Wall, 2000). The
symbiosis process requires a number of interactions between the
two organisms, but the molecular bases that control symbiosis
onset and its specicity are still unknown. The lack of genetic tools
to study Frankia has restricted progress in understanding the reg-
ulatory events occurring during the early steps of symbiosis.
Common features between actinorhizal and legume symbiosis
have been observed during the rst steps of the infectious process.
Indeed, a similar root hair curling step is observed with both
Frankia and Rhizobium prior to nodule formation, but the Frankia
extracellular deforming factor seems to be structurally and func-
tionally different from the Rhizobium Nod factors (Bagnarol et al.,
2007).
As in the Rhizobium/legume interaction, recognition of host-
derived avonoids is the basic mechanism through which
rhizobia interact specically with their hosts. Indeed, nodulation
may be inuenced by host-derived phenolics (cinnamic, benzoic
and hydroxybenzoic acids) and by Alnus seed avonoid-like com-
pounds, which have been identied as avanone and isoavanone
(Benoit and Berry, 1997). Moreover, it was demonstrated that root
hair curling is enhanced by Frankia exposure to an Alnus glutinosa
root ltrate (Prin and Rougier, 1987; Van Ghelue et al., 1997).
Recently, the strain specicity in MyricaceaeeFrankia symbiosis
was found to be correlated with plant root phenolics (Popovici
et al., 2010). The main plant compounds differentially affected by
Frankia inoculation are phenols, avonoids and hydroxycinnamic
acids. This work provides evidence that during the initial phases of
symbiotic interactions, Myricaceae plants adapt their secondary
metabolism in accordance with the compatibility status of Frankia
bacterial strains, thus suggesting that avonoids might determine
the microsymbiont specicity.
It was found that genes coding for phenylammonia lyase (pal)
and chalcone synthase (chs), involved in avonoids biosynthesis are
activated in A. glutinosa inoculated by Frankia (Hammad et al.,
2003; Kim et al., 2003). More recently, the analysis of a Casuarina
glauca root and nodule expressed sequence tag (EST) database led
to the identication of 8 genes coding for enzymes involved in the
avonoid biosynthesis pathway: chalcone synthase, chalcone
isomerase, isoavone reductase, avonone-3-hydroxylase, avo-
noid-3
0
-hydroxylase, avonoid-3,5-hydroxylase, dihydroavonol-
4-reductase and avonol synthase (Auguy et al., 2011). The ndings
of a kinetic study of the expression of these genes after C. glauca
root inoculation with Frankia associated with a biochemical study
of the avonoid composition of the inoculated roots are consistent
with the involvement of avonoids during actinorhizal symbiosis
(Hocher et al., 2006; Auguy et al., 2011).
A deeper understanding of the actinorhizal symbiosis requires
more efforts in investigating Frankia cultivability and developing
genetic tools, which may provide valuable information on devel-
opmental biology and hostemicrobe interactions.
3.2.3. Arbuscular mycorrhizal fungi (AMF)
Arbuscular mycorrhiza are formed in association with 80% of
land plants. Arbuscular mycorrhizal fungi (AMF) are obligate
symbionts incapable of completing their life cycle in the absence of
a host root. The fungi penetrate and colonize plant roots, where
they differentiate into highly branched structures known as
arbuscules, which are thought to be the principal sites of nutrient
exchange between the two organisms (Akiyama and Hayashi,
2006).
One crucial step in AMF development is the formation of extra-
radical hyphae induced by signal molecules exuded by plants,
leading to the onset of AMF-induced symbiosis. These signal mol-
ecules have been named strigolactones (SLs) and are now
recognized as plant hormones (Koltai, 2013).
3.2.3.1. Strigolactones: branching factors exuded by plants.
They were rst identied over 40 years ago as stimulants of para-
sitic plant (Striga and Orobanche) germination (Cook et al., 1966; Xie
et al., 2010). Later their activity as stimulants of hyphal branching
was discovered in symbiotic AMF (reviewed by Koltai et al., 2012).
Giovannetti et al. (1996) demonstrated that the branching factor
exuded by Ocimumbasiliciminduce hyphae development in Glomus
mosseae. However, this branching factor has yet to be chemically
identied. Currently, we know that SLs are terpenid lactones
derived from carotenoids (Matusova et al., 2005). Their presence
has been demonstrated in a wide variety of plant species, including
dicots, monocots and primitive plants (reviewed by Xie et al., 2010;
Liu et al., 2009; Proust et al., 2011). They are synthesized in a few
different plants parts, but roots are considered to be the main site of
SL biosynthesis (Xie et al., 2010).
SL biosynthesis and sensitivity was recently shown to be
important in the ability of root to recognize or respond to low-
phosphate (Pi) growth conditions (Umehara et al., 2010; Kohlen
et al., 2011; Ruyter-Spira et al., 2011; Mayzlish-Gati et al., 2012).
It was demonstrated that Arabidopsis SL mutants are decient in
their ability to increase root hair (RH) length and density and hence
are unable to respond to low-Pi growth conditions compared with
the wild type (Koltai, 2013). Indeed, the RH number and length are
thought to be directly associated with the plant capacity to absorb
nutrients from the soil.
3.3. Root exudates as nitrication inhibitors
Nitrication is a key process in the global nitrogen cycle that
generates nitrates through microbial activity. It determines the
form of nitrogen (N) present and therefore how N is absorbed,
utilized or dispersed into the environment. This in turn has large
implications as to plant productivity and environmental quality.
During nitrication, the relatively immobile NH
4
is converted to
the highly mobile NO
3
-
. This process strongly inuences N utiliza-
tion by plants, because the NO
3
-
formed, is highly susceptible to loss
from the root zone by leaching and/or denitrication (Subbarao
et al., 2007a).
Regulating nitrication could be a key strategy in improving N
recovery and agronomic N-use efciency in situations where the
loss of Nfollowing nitrication is signicant (Subbarao et al., 2009).
Certain plant can suppress/slowdown soil-nitrication by releasing
inhibitors fromroots, a phenomenon termed biological nitrication
inhibition (BNI) (for review, Subbarao et al., 2006).
Recently, a highly sensitive bioassay using recombinant lumi-
nescent Nitrosomonas europaea, has been developed that can detect
and quantify nitrication inhibitors released from plant roots
(Subbarao et al., 2007a). A number of species including tropical and
temperate pastures, cereals and legumes were tested for BNI in
their root exudate. There was a wide range in BNI capacity among
the 18 species tested; specic BNI (AT units activity g
1
root dm)
ranged from 0 (i.e. no detectable activity) to 18.3 AT units. Among
the tested cereal and legume crops, sorghum, pearl millet, and
groundnut showed detectable BNI in root exudate. Among pasture
grasses, Brachiaria humidicola (Rendle) Schweick, Brachiaria
decumbens showed the highest BNI capacity. Several high- and low-
BNI genotypes were identied within the B. humidicola species. Soil
collected from eld plots of 10 year-old high-BNI genotypes of
B. humidicola, showed a near total suppression (>90%) of nitrica-
tion; most of the soil inorganic N remained in the NH
4
(ammo-
nium) form after 30 days of incubation. In contrast, soils collected
fromlow-BNI genotypes did not showany inhibitory effect; most of
the soil inorganic N was converted to NO
3
after 30 days of incu-

bation. The BNI from high- and low-BNI types when added to
N. europaea in pure culture blocked both the ammonia mono-
oxygenase (AMO) and the hydroxylamine oxidoreductase (HAO)
pathways (Subbarao et al., 2007a).
Other crops including rice (O. sativa), maize (Z. mays), wheat and
barley (H. vulgare) were found to lack BNI capacity in their root
systems during initial screening studies (Subbarao et al., 2007b,
2012a; Zakir et al., 2008). Most legumes evaluated showed nega-
tive BNI activity in root exudates, indicating that they are likely to
stimulate nitrication (Subbarao et al., 2007b). Inhibition of nitri-
cation is likely to be part of an adaptation mechanism to conserve
and use N efciently in natural systems that are N limiting (Lata
et al., 1999; Subbarao et al., 2007a).
Synthesis and release of BNIs is a highly regulated attribute
(Subbarao et al., 2007a; Zhu et al., 2012). The form of N applied (i.e.
NH
4
or NO
3
) has a major inuence on the synthesis and release of

BNIs in B. humidicola, sorghum and Leymus racemosus, wild wheat
(Subbarao et al., 2006, 2007a, c, 2009, 2012; Zakir et al., 2008).
Plants grown with NO
3
as N source did not release BNIs from roots,

whereas BNIs were released fromplants grown with NH
4
as their N
source (Subbarao et al., 2007a, 2009; Zakir et al., 2008; Zhu et al.,
2012). Despite high levels of BNIs detected in the root tissues of
NH
4
grown plants, the release of BNIs was observed only when

plant roots were directly exposed to NH
4
(Subbarao et al., 2013a).

Zakir et al. (2008) identied for the rst time the root exuded
compound, methyl 3-(3-hydroxyphenyl) propionate (MHPP),
responsible for BNI by sorghum. The mode of inhibitory action for
MHPP is solely through the AMO enzymatic pathway, and it has no
inhibitory effect on the HAO enzymatic pathway in Nitrosomonas
(Zakir et al., 2008). It was discovered more recently that sorgoleone,
a p-benzoquinone exuded from sorghum roots, has a strong
inhibitory effect on Nitrosomonas sp. activity and that this com-
pound contributes signicantly to the BNI capacity in sorghum
(Subbarao et al., 2013b).
In an elegant study, Subbarao et al. (2009) discovered an
effective nitrication inhibitor in the root exudates of the tropical
forage grass B. humidicola (Rendle) Schweick. Named brachia-
lactone, this inhibitor is a recently discovered cyclic diterpene with
a unique 5-8-5-membered ring system and a g-lactone ring. It
contributed to 60e90% of the inhibitory activity released from the
roots of this tropical grass. Unlike nitrapyrin (a synthetic nitrica-
tion inhibitor), which affects only AMO pathway, brachialactone
appears to block both AMO and hydroxylamine oxidoreductase
enzymatic pathways in Nitrosomonas. Release of this inhibitor is a
regulated plant function, triggered and sustained by the availability
of NH
4
in the root environment.

Actually, exploiting the BNI function using both genetic and
crop/system management approaches is the rst step towards
designing a low-nitrifying agronomic environment in agricultural
systems.
3.4. Root exudates as chemoattractants
As mentioned above, plants exude high levels of carbon sources,
and many of these act as chemoattractants for bacteria and most
motile bacteria are capable of directing their movement in response
to chemical gradientsda behaviour known as chemotaxis. The
chemotactic response of bacteria to root exudates plays a relevant
ecological role in plant-associated bacteria and constitute the rst
step in initiating communication between plant roots and mi-
crobes. Indeed, the chemotactic response of bacteria, such as
Pseudomonas, Rhizobium and Agrobacterium species, increases their
root colonization efciency in the rhizosphere.
Several bacteria were described as presenting positive chemo-
taxis toward different molecules exuded by plants, including
sugars, amino acids, various dicarboxylic acids such as succinate,
malate and fumarate, and aromatic compounds such as shikimate,
quinate, protocatechuate, vanillate, acetosyringone, gallate, cate-
chol and luteolin (Brencic and Winans, 2005). Certain phenolic
compounds exuded by tobacco plants attract the Agrobacterium
tumefaciens C58 strain (Brencic and Winans, 2005). Pseudomonas
putida presents positive chemotaxis to maize-derived aromatic
metabolites (Neal et al., 2012).
Several studies with S. meliloti revealed that certain avonoids
are specic chemoattractants for rhizobia to promote bacterial
movement towards the roots, leading to contact, colonization and
infection and ultimately nodule development (Phillips et al., 1992;
Aguilar et al., 1998).
In addition, chemotaxis is an important mechanism involved in
the tness and virulence of certain species such as Ralstonia sol-
anacearum (Yao and Allen, 2006).
3.5. Root exudates as activator of carbon cycling
Plants also stimulate the growth of rhizospheric microorgan-
isms by releasing high amounts and different types of C from the
roots (Haichar et al., 2008, 2012). Some of these microbial growth
promoting effects are clearly benecial for plant growth, e.g.
through the synthesis of antibiotics and fungicidal compounds like
2,4-diacetylphlorogluciol (DAPG) and cyanide hydrogen (HCN)
(Lalaouna et al., 2012; Haichar et al., 2013). These subsequently act
as antagonists for phytopathogen microorganisms by releasing
plant growth substances like phytohormones and vitamins (Faure
et al., 2009) or promoting non-symbiotic N
2
-xing microorgan-
isms (Richardson, 2009).
Root exudates could supply rhizobacteria with precursors
needed for phytohormone synthesis. An interesting report de-
scribes the mapping of sugar and amino acid availability in Avena
barbata root exudates (Jaeger et al., 1999). This study highlighted
the availability of tryptophan mainly in the root tip region. Tryp-
tophan is the precursor for indole 3-acetic acid, a major auxin,
suggesting that rhizobacteria could exploit root exudate pools for
various growth regulator precursors.
Plants also exude aminocyclopropane-1-carboxylic acid (ACC),
which is an ethylene synthesis precursor and can be used as
carbon and nitrogen sources by rhizobacteria, as recently shown
by acdS expression mainly by root exudates assimilating bacteria
and those inhabiting root tissue (Haichar et al., 2012). The use of
ACC by ACC-deaminase-producing rhizobacteria reduces the
amount of ACC outside the plant and equilibrated the ACC level
outside and inside. Plants release more ACC and therefore pro-
duce less ethylene, which inhibits root elongation (Glick et al.,
1998).
As mentioned above, plants exude a high variety of sugars,
which are also suggested to be involved in the production of exo-
polysaccharides (EPSs) such as glucose and sucrose by rhizospheric
bacteria. For example, a high level of Paenibacillus polymyxa levan
production was achieved when a high sucrose concentration was
present in the culture media. The authors suggested that the
expression of the P. polymyxa sacB gene involved in levan synthesis
could be induced in the rhizosphere by the exuded sucrose, in
particular from the growing apical region of wheat roots (Bezzate
et al., 2000). These EPSs are the main contributors in legu-
meerhizobia interactions, leading to nodulation and nitrogen x-
ation. They have also other functions such as root-adhering soil
structuring, non-legume plant growth promotion or evasion from
the legume defence response during crack entry in roots (Alami
et al., 2000; Morgante et al., 2007).
The production of EPSs by rhizobia has been observed at high
glucose or sucrose concentrations (z20 g/L). This possibly suggests
that: (i) a high concentration of these molecules is exuded by
plants, or (ii) bacteria may produce EPSs with low glucose or su-
crose concentrations in the rhizosphere in the presence of gene
expression inducers.
Root exudation can have a major impact on nutrient acquisition
by plants. Phytosiderophores and other chelating agents play a
pivotal role in acquiring Fe and other micronutrients (Lambers
et al., 2009). Many plants enhance their rate of carboxylate
exudation when their P supply is severely limiting in order to sol-
ubilise adsorbed P (Vance et al., 2003). In addition, exudates may
enhance the activity of phosphate-solubilising bacteria and hence
increase the plant's P supply (Richardson et al., 2011; Richardson
et al., 2009).
Organic substances released from roots may also accelerate the
decomposition of soil organic matter (SOM) and stimulate the
dissolution of insoluble minerals by rhizosphere microorganisms.
Thisso-calledrhizosphereprimingeffect or microbial activation of
nutrient cyclingis baseduponastimulationof microbial activityinthe
rhizosphere bylabileCreleasedbyroots (Jones et al., 2004). According
to Nobili et al. (2001), even very low amounts (mg g
1
soil) of some
primers such as root exudates, may promote SOMturnover leading to
increase N or phosphorus availability to plants (Jones et al., 2004;
Cheng et al., 2014). Published results from experimental studies in
plant growthchambers andglasshouses indicate that the rhizosphere
priming effect (RPE) varies widely, ranging from 17% to 380%
enhancement of SOMturnover (ZhuandCheng, 2011). The RPEcanbe
signicantly inuenced by both plant and soil variables (Cheng et al.,
2014). For example, the RPE of soybean (G. max) was consistently
higher thanthat of wheat (Triticumaestivum) whenbothspecies were
grown in the same soil under the same environmental conditions
(Cheng et al., 2003). Although the quality and quantity of root exu-
dates are thought to be key plant traits controlling RPE (Kuzyakov,
2010), the actual traits responsible for the large observed differences
in RPE are virtually unknown (Cheng et al., 2014).
4. Future research prospects
This review highlighted some of the most recent ndings that
have helped to gain insight into the root exudates-mediated
mechanisms governing plant-microorganisms interactions in the
rhizosphere. It is nowclearly established that root exudates are key
mediators in belowground plant-microorganisms interactions.
The lack of comprehensive knowledge on exudate chemistry
represents a major bottleneck in our understanding of plant-mi-
croorganisms interactions. Even if the characterization of mole-
cules involved in these interactions is increasing, the metabolic
proling of root exudates is limited to the targeted analysis of some
compounds such as organic acids, avonoids, and fatty acids. We
believe that many other compounds that trigger plant-microor-
ganisms interactions are still unknown. Difculties in the
biochemical characterization of exudates could be due to the
inability to extract and analyse trace amounts of potentially labile
natural products.
Studies on the spatial and temporal patterns of root exudates
were conducted mostly under axenic or monoxenic in vitro condi-
tions. In situ assays are required and would provide a better un-
derstanding of their dynamic and role over plant growth cycle.
In the plant-microorganisms biology eld, substantial progress
has been achieved in understanding the role of root exudates in
plant-pathogen and plant-symbiont molecular dialogue and signal
exchange. Similar in-depth investigations of their role in plant-
microorganisms interactions with the broad diversity of plant
species and lifestyles are required. Many crucial questions still
remain open. Is there any specic signalling molecule exchange
between these partners? What is their nature? How are they
temporally and spatially distributed?
Answers to these and other pressing questions will undoubtedly
keep the eld busy for years to come. Future investigations will
thus be necessary to determine the nature of signalling molecules
both from plant and bacteria, under natural conditions.
Metabolomics tools are thus required to determine the whole
inventory of exuded molecules by plants at different stages of plant
development and in different soils, their turnover, their fate in
natural soil, and their role on microbial physiology and functions.
Finally, gaining a greater understanding into howplants differ in
their rhizodeposition patternsdquantitatively and qualitatively,
according to their genotypes and traits, as well as environmental
parameters and soil microbial community is an exciting research
challenge. Achieving this objective requires the willingness of the
researchers working in different elds e plant physiology, ecology,
soil physico-chemistry and microbiology e to be involved in this
interdisciplinary effort. This will lead to improve knowledge on
how the structure and quality of the soil may contribute i) to
modulate the composition of root exudates; ii) to promote bene-
cial interactions in the rhizosphere; and iii) to ameliorate plant
defence and biocontrol of pathogens. Numerous exciting and
fruitful avenues of study of the link between bacterial gene
expression and the nature of root exudates remain open. In a word,
the potential of root exudates has not yet been exhausted.
References
Aguilar, J.M.M., Ashby, A.M., Richards, A.J.M., Loake, G.J., Watson, M.D., Shaw, C.H.,
1998. Chemotaxis of Rhizobium leguminosarum towards avonoid inducers of
the symbiotic nodulation genes. J. Gen. Microbiol. 134, 2741e2746.
Akiyama, K., Hayashi, H., 2006. Strigolactones: chemical signals for fungal symbi-
onts and parasitic weeds in plant roots. Ann. Botany Lond 97, 925e931.
Alami, Y., Achouak, W., Marol, C., Heulin, T., 2000. Rhizosphere soil aggregation and
plant growth promotion of sunowers by an exopolysaccharide-producing
Rhizobium sp. strain isolated from sunower roots. Appl. Environ. Microbiol.
66, 3393e3398.
Auguy, F., Abdel-Lateif, K., Doumas, P., Badin, P., Guerin, V., Bogusz, D., Hocher, V.,
2011. Activation of the isoavonoid pathway in actinorhizal symbioses. Funct.
Plant Biol. 38, 690e696.
Aulakh, M.S., Wassmann, R., Bueno, C., Kreuzwieser, J., Rennenberg, H., 2001.
Characterization of root exudates at different growth stages of ten rice (Oryza
sativa L.) cultivars. Plant Biol. 3, 139e148.
Badri, D.V., Vivanco, J.M., 2009. Regulation and function of root exudates. Plant Cell
Environ. 32, 666e681.
Baetz, U., Martinoia, E., 2013. Root exudates: the hidden part of plant defense.
Trends Plant Sci. 19, 90e98.
Bagnarol, E., Popovici, J., Alloisio, N.J., Marechal, P., Pujic, P., Normand, P.,
Fernandez, M.P., 2007. Differential Frankia protein patterns induced by phenolic
extracts from Myricaceae seeds. Plant Physiol. 130, 380e390.
Bais, H.P., Park, S.W., Weir, T.L., Callaway, R.M., Vivanco, J.M., 2004a. How plants
communicate using the underground information superhighway. Trends Plant
Sci. 9, 26e32.
Bais, H.P., Fall, R., Vivanco, J.M., 2004b. Biocontrol of Bacillus subtilis against infection
of Arabidopsis roots by Pseudomonas syringae is facilitated by biolm formation
and surfactin production. Plant Physiol. 134, 307e319.
Bais, H.P., Weir, T.L., Perry, L.G., Gilroy, S., Vivanco, J.M., 2006. The role of root ex-
udates in rhizosphere interactions with plants and other organisms. Annu. Rev.
Barber, D.A., Martin, J.K., 1976. The release of organic substances by cereal roots into
soil. New Phytol. 76, 69e80.
Benoit, L.F., Berry, A.M., 1997. Flavonoid-like compounds from seeds of red alder
(Alnus rubra) inuence host nodulation by Frankia (Actinomycetales). Plant
Physiol. 99, 588e593.
Bertin, C., Yang, X., Weston, L.A., 2003. The role of root exudates and allelochemicals
in the rhizosphere. Plant Soil 256, 67e83.
Bezzate, S., Aymerich, S., Chambert, R., Czarnes, S., Berge, O., Heulin, T., 2000.
Disruption of the Paenibacillus polymyxa levansucrase gene impairs its ability to
aggregate soil in the wheat rhizosphere. Environ. Microbiol. 2, 333e342.
Boot, K.J.M., van Brussel, A.A.N., Tak, T., Spaink, H.S., Kijne, J.W., 1999. Lipo-chitin oli-
gosaccharides from Rhizobium leguminosarum bv. viciae reduce auxin transport
capacity in Vicia sativa subsp nigra roots. Mol. Plant Microbe Interact. 12, 839e844.
Brencic, A., Winans, S.C., 2005. Detection of and response to signals involved in
host-microbe interactions by plant-associated bacteria. Microbiol. Mol. Biol. 69,
155e194.
Brigham, L.A., Woo, H.H., Hawes, M.C., 1995. Differential expression of proteins and
mRNAs from border cells and root tips of pea. Plant Physiol. 109, 457e463.
Cannesan, M.A., Gangneux, C., Lanoue, A., Giron, D., Laval, K., Hawes, M.,
Driouich, A., Vicr e-Gibouin, M., 2011. Association between border cell responses
and localized root infection by pathogenic Aphanomyces euteiches. Ann. Bot.
Lond. 108, 459e469.
Cheng, W.X., Johnson, D.W., Fu, S.L., 2003. Rhizosphere effects on decomposition:
controls of plant species, phenology, and fertilization. Soil. Sci. Soc. Am. J. 67,
1418e1427.
Cheng, W., Parton, W.J., Gonzalez-Meler, M.A., Phillips, R., Asao, S., McNickle, G.G.,
Brzostek, E., Jastrow, J.D., 2014. Synthesis and modeling perspectives of rhizo-
sphere priming. New Phytol. 201, 31e44.
Cook, C.E., Whichard, L.P., Turner, B., Wall, M.E., Egley, G.H., 1966. Germination of
witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant.
Science 154, 1189e1119.
Cooper, J.E., 2004. Multiple responses of rhizobia to avonoids during legume root
infection. Adv. Bot. Res. 41, 1e62.
Cooper, J.E., 2007. Early interactions between legumes and rhizobia: disclosing
complexity in a molecular dialogue. J. Appl. Microbiol. 103, 1355e1365.
Cullimore, J.V., Ranjeva, R., Bono, J.J., 2001. Perception of lipochitooligosaccharidic
Nod factors in legumes. Trends Plant Sci. 6, 24e30.
Dakora, F.D., Phillips, D.A., 2002. Root exudates as mediators of mineral acquisition
in low-nutrient environments. Plant Soil 245, 35e47.
Defoirdt, T., Boon, N., Bossier, P., 2010. Can bacteria evolve resistance to quorum
sensing disruption? PLoS Pathog. 6, e1000989.
Derrien, D., Marol, C., Balesdent, J., 2004. The dynamics of neutral sugars in the
rhizosphere of wheat: an approach by
13
C pulse-labelling and GC/C/IRMS. Plant
Soil 267, 243e253.
De-la-Pena, C., Lei, Z., Watson, B.S., Sumner, L.W., Vivanco, J.M., 2008. Root secretion
of defense-related proteins is development-dependent and correlated with
owering time. J. Biol. Chem. 285, 30654e30665.
D enari e, J., Debell e, F., Prom e, J.C., 1996. Rhizobium lipochitooligosaccharide nodu-
lation factors: signalling molecules mediating recognition and morphogenesis.
Annu. Rev. Biochem. 65, 503e535.
Dixon, R.A., 2001. Natural products and plant disease resistance. Nature 411,
843e847.
Dor, E., Joel, D.M., Kapulnik, Y., Koltai, H., Hershenhorn, J., 2011. The synthetic
strigolactone GR24 inuences the growth pattern of phytopathogenic fungi.
Planta 234, 419e427.
Dong, Z., Layzell, D.B., 2001. H
2
oxidation, O
2
uptake and CO
2
xation in hydrogen
treated soils. Plant Soil 229, 1e12.
Dong, Z., Wu, L., Kettlewell, B., Caldwell, C.D., Layzell, D.B., 2003. Hydrogen fertil-
ization of soils e is this a benet of legumes in rotation? Plant Cell Environ. 26,
1875e1879.
Driouich, A., Durand, C., Vicre-Gibouin, M., 2007. Formation and separation of root
border cells. Trends Plant Sci. 12, 14e19.
Driouich, A., Follet-Gueye, M.L., Vicre-Gibouin, M., Hawes, M., 2013. Root border
cells and secretions as critical elements in plant host defense. Curr. Opin. Plant
Biol. 16, 489e495.
Elasri, M., Delorme, S., Lemanceau, P., Stewart, G., Laue, B., Glickmann, E., Oger, P.M.,
Dessaux, Y., 2001. Acyl-homoserine lactone production is more common among
plant-associated Pseudomonas spp. than among soilborne Pseudomonas spp.
Appl. Environ. Microbiol. 67, 1198e1209.
Faure, D., Vereecke, D., Leveau, J.H.J., 2009. Molecular communication in the
rhizosphere. Plant Soil 321, 279e303.
Fray, R.G., 2002. Altering plant-microbe interaction through articially manipu-
lating bacterial quorum sensing. Ann. Bot. Lond. 89, 245e253.
Frenzel, B., 1960. Zur atiologie der anreicherung von aminosauren und amiden in
wurzelraum von Helianthes annus. Beitrag zur Klarung Probl. Rhizosphare
Planta 55, 169e207.
Gagnon, H., Ibrahim, R.K., 1998. Aldonic acids: a novel family of nod gene inducers of
Mesorhizobium loti, Rhizobium lupini and Sinorhizobium meliloti. Mol. Plant
Microbe Interact. 11, 988e998.
Giovannetti, M., Sbrana, C., Silvia, A., Avio, L., 1996. Analysis of factors involved in
fungal recognition response to host-derived signals by arbuscular mycorrhizal
fungi. New Phytol. 133, 65e71.
Glick, B.R., Penrose, D.M., Li, J., 1998. A model for the lowering of plant ethylene
concentrations by plant growth-promoting bacteria. J. Theor. Biol. 190, 63e68.
Golding, A., Zou, Y., Yang, X., Flynn, B., Dong, Z., 2012. Plant growth promoting H
2
-
oxidizing bacteria as seed inoculants for cereal crops. Agric. Sci. 3, 510e516.
Gunawardena, U., Rodriguez, M., Straney, D., Romeo, J.T., VanEtten, H.D.,
Hawes, M.C., 2005. Tissue-specic localization of pea root infection by Nectria
haematococca. Mechanisms and consequences. Plant Physiol. 137, 1363e1374.
Gunawardena, U., Hawes, M.C., 2002. Tissue specic localization of root infection by
fungal pathogens: role of root border cells. Mol. Plant Microbe Interact. 15,
1128e1136.
Hassan, S., Mathesius, U., 2012. The role of avonoids in rootrhizosphere signalling:
opportunities and challenges for improving plant-microbe interactions. J. Exp.
Bot. http://dx.doi.org/10.1093/jxb/err430.
Haichar, F.Z., Marol, C., Berge, O., Rangel-Castro, J., Prosser, J.I., Balesdent, J.,
Heulin, T., Achouak, W., 2008. Plant host habitat and root exudates shape soil
bacterial community structure. ISME J. 2, 1221e1230.
Haichar, F.Z., Roncato, M.A., Achouak, W., 2012. Stable isotope probing of bacterial
community structure and gene expression in the rhizosphere of Arabidopsis
thaliana. FEMS Microb. Ecol. 81, 291e302.
Haichar, F.Z., Fochesato, S., Achouak, W., 2013. Host plant specic control of 2,4-
diacetylphloroglucinol production in the rhizosphere. Agronomy 3, 621e631.
Halkier, B.A., Gershenzon, J., 2006. Biology and biochemistry of glucosinolates.
Annu. Rev. Plant Biol. 57, 303e333.
Hammad, Y., Nalin, R., Mar echal, K., Fiasson, K., Pepin, R., Berry, A.M., Normand, P.,
Domenach, A.M., 2003. A possible role for phenylacetic acid (PAA) in Alnus
glutinosa nodulation by Frankia. Plant Soil 254, 193e205.
Hawes, M.C., Brigham, L.A., 1992. Impact of root border cells on microbial popula-
tion in the rhizosphere. Adv. Plant Pathol. 8, 119e148.
Hawes, M.C., Gunawardena, U., Miyasaka, S., Zhao, X., 2000. The role of root border
cells in plant defense. Trends Plant Sci. 5, 128e133.
Hawes, M.C., Bengough, G., Cassab, G., Ponce, G., 2003. Root caps and rhizosphere.
J. Plant Growth Regul. 21, 352e367.
Hiltner, L., 1904. Uber neuere Erfahrungen und Problem auf dem gebiet der Bod-
enbakteriologie und unter besonderer Bercksichtigung der Grndngung und
Brachte. Arb. Dt Landwges 98, 59e78.
Hinsinger, P., Bengough, A., Vetterlein, D., Young, I., 2009. Rhizosphere: biophysics,
biogeochemistry and ecological relevance. Plant Soil 321, 117e152.
Hirsch, A.M., Lum, M.R., Downie, J.A., 2001. What makes rhizobia-legume symbiosis
so special? Plant Physiol. 127, 1484e1492.
Hocher, V., Auguy, F., Argout, X., Laplaze, L., Franche, C., Bogusz, D., 2006. Expressed
sequence-tag analysis in Casuarina glauca actinorhizal nodule and root. New
Phytol. 169, 681e688.
Hudak, K.A., Wang, P., Tumer, N.E., 2000. A novel mechanism for inhibition of
translation by pokeweed antiviral protein: depurination of the capped RNA
template. RNA 6, 369e380.
Humphris, S.N., Bengough, A.G., Grifths, B.S., Kilham, K., Rodger, S., Stubbs, V.,
Valentine, T.A., Young, I.M., 2005. Root cap inuences root colonisation by
Pseudomonas uorescens SBW25 on maize. FEMS Microbiol. Ecol. 54, 123e130.
Hutsch, B.W., Augustin, J., Merbach, W., 2000. Plant rhizodeposition an important
source for carbon turnover in soils. J. Plant Nutr. Soil Sci. 165, 397e407.
Jaeger, C.H.I., Lindow, S.E., Miller, W., Clark, E., Firestone, M.K., 1999. Mapping of
sugar and amino acid availability in soil around roots with bacterial sensors of
sucrose and tryptophan. Appl. Environ. Microbiol. 65, 2685e2690.
Jones, D.L., Hodge, A., Kuzyakov, Y., 2004. Plant and mycorrhizal regulation of rhi-
zodeposition. New Phytol. 163, 459e480.
Jones, D., Nguyen, C., Finlay, D.R., 2009. Carbon ow in the rhizosphere: carbon
trading at the soileroot interface. Plant Soil 321, 5e33.
Kim, H.B., Oh, C.J., Lee, H., Sun An, C., 2003. A type-i chalcone lsomerase mRNA is
highly expressed in the root nodules of Elaeagnus umbella. J. Plant Biol. 46,
263e270.
Kohlen, W., Charnikhova, T., Liu, Q., Bours, R., Domagalska, M.A., Beguerie, S.,
Verstappen, F., Leyser, O., Bouwmeester, H., Ruyter-Spira, C., 2011. Strigolactones
are transported through the xylem and play a key role in shoot architectural
response to phosphate deciency in nonarbuscular mycorrhizal host Arabi-
dopsis. Plant Physiol. 155, 974e987.
Koltai, H., Matusova, R., Kapulnik, Y., 2012. Strigolactones in root exudates as a
signal in symbiotic and parasitic interactions. In: Vivanco, J.M., Balusaka, F.
(Eds.), Signaling and Communication in Plants. Springer, Berlin, pp. 49e73.
Koltai, H., 2013. Strigolactones' ability to regulate root development may be
executed by induction of the ethylene pathway. Plant Signal. Behav. 6,
1004e1005.
Kuzyakov, Y., Domanski, G., 2000. Carbon input by plants into the soil. J. Plant Nutr.
Soil Sci. 163, 421e431.
Kuzyakov, Y., 2010. Priming effects: interactions between living and dead organic
matter. Soil Biol. Biochem. 42, 1363e1371.
Lalaouna, D., Fochesato, S., Sanchez, L., Schmitt-Kopplin, P., Haas, D., Heulin, T.,
Achouak, W., 2012. Phenotypic switching involves GacS/GacA dependent Rsm
small RNAs in Pseudomonas brassicacearum. Appl. Environ. Microbiol. 781,
658e1665.
Lambers, H., Mougel, C., Jaillard, B., Hinsinger, P., 2009. Plantemicrobeesoil in-
teractions in the rhizosphere: an evolutionary perspective. Plant Soil 321, 83e115.
Lanoue, A., Burlat, V., Henkes, G.J., Koch, I., Schurr, U., Rose, U.S.R., 2010. De novo
biosynthesis of defense root exudates in response to Fusarium attack in barley.
New Phytol. 185, 577e558.
Lata, J.C., Durand, J., Lensi, R., Abbadie, L., 1999. Stable coexistence of contrasted
nitrication statuses in a wet tropical savanna system. Funct. Ecol. 13, 762e763.
Le Strange, K.K., Bender, G.L., Djordjevic, M.A., Rolfe, B.G., Redmond, J.W., 1990. The
Rhizobium strain NGR234 nodD1 gene product responds to activation by the
simple phenolic compounds vanillin and isovanillin present in wheat seedling
extracts. Mol. Plant Microbe Interact. 3, 214e220.
Liao, C., Hochholdinger, F., Li, C., 2012. Comparative analyses of three legume spe-
cies reveals conserved and unique root extracellular proteins. Proteomics 12,
3219e3228.
Liu, J., Magalhaes, J.V., Shaff, J., Kochian, L.V., 2009. Aluminum-activated citrate and
malate transporters from the MATE and ALMT families function independently
to confer Arabidopsis aluminum tolerance. Plant J. 57, 389e399.
Ma, W., Muthreich, N., Liao, C., Franz-Wachtel, M., Schtz, W., Zhang, F.,
Hochholdinger, Li, C., 2010. The mucilage proteome of maize (Zea mays L.)
primary roots. J. Proteome Res. 9, 2968e2976.
Maimaiti, J., Zhang, Y., Yang, J., Cen, Y.-P., Layzell, D.B., Peoples, M., Dong, Z., 2007.
Isolation and characterization of hydrogen-oxidizing bacteria induced following
exposure of soil to hydrogen gas and their impact on plant growth. Environ.
Microbiol. 9, 435e444.
Marschner, H., 1995. Mineral Nutrition of Higher Plants. Academic Press, London, UK.
Mathesius, U., Schlaman, H.R., Spaink, H.P., Of Sautter, C., Rolfe, B.G.,
Djordjevic, M.A., 1998. Auxin transport inhibition precedes root nodule for-
mation in white clover roots and is regulated by avonoids and derivatives of
chitin oligosaccharides. Plant J. 14, 23e34.
Mathesius, U., Weinman, J.J., Rolfe, B.G., Djordjevic, M.A., 2000. Rhizobia can induce
nodules in white clover by hijacking mature cortical cells activated during
lateral root development. Mol. PlanteMicrobe Interac. 13, 170e182.
Matusova, R., Rani, K., Verstappen, F.W.A., Franssen, M.C.R., Beale, M.H.,
Bouwmeester, H.J., 2005. The strigolactone germination stimulants of the plant-
parasitic Striga and Orobanche spp. are derived from the carotenoid pathway.
Plant Physiol. 139, 920e934.
Mayzlish-Gati, E., De-Cuyper, C., Goormachtig, S., Beeckman, T., Vuylsteke, M.,
Brewer, P.B., Beveridge, C.A., Yermiyahu, U., Kaplan, Y., Enzer, Y., Wininger, S.,
Resnick, N., Cohen, M., Kapulnik, Y., Koltai, H., 2012. Strigolactones are involved
in root response to low phosphate conditions in Arabidopsis. Plant Physiol. 160,
1329e1341.
McDougall, B.M., 1968. The exudation of C
14
-lebelled substances from roots of
wheat seedlings. In: Transactions of the 9th Congress International Soil Science,
Adelaide 3, pp. 647e655.
McDougall, B.M., Rovira, A.D., 1970. Sites of exudation of
14
C-labelled compounds
from wheat roots. New Phytol. 69, 999e1003.
Meharg, A.A., Killham, K., 1990. Carbon distribution within the plant and rhizo-
sphere in laboratory and eld-grown Lolium perenne at different stages of
development. Soil. Biol. Biochem. 22, 471e477.
Mendes, R., Garbeva, P., Raaijmakers, J.M., 2013. The rhizosphere microbiome: sig-
nicance of plant benecial, plant pathogenic, and human pathogenic micro-
organisms. FEMS Microbiol. Rev. 37, 634e663.
Morgante, C., Castro, S., Fabra, A., 2007. Role of rhizobial EPS in the evasion of
peanut defense response during the crack-entry infection process. Soil. Biol.
Biochem. 39, 1222e1225.
Nardi, S., Concheri, G., Pizzeghello, D., Sturaro, A., Rella, R., Parvoli, G., 2000. Soil
organic matter mobilization by root exudates. Chemosphere 5, 653e658.
Neal, A.L., Ahmad, S., Gordon-Weeks, R., Ton, J., 2012. Benzoxazinoids in root exu-
dates of maize attract Pseudomonas putida to the rhizosphere. PLoS One 7,
e35498.
Neumann, G., Bott, S., Ohler, M.A., Mock, H.P., Lippmann, R., Grosch, R., Smalla, K.,
2014. Root exudation and root development of lettuce (Lactuca sativa L. cv.
Tizian) as affected by different soils. Front. Microbiol. http://dx.doi.org/10.3389/
fmicb.2014.00002 eCollection 2014.
Nguyen, C., 2003. Rhizodeposition of organic C by plants: mechanisms and controls.
Agronomie 23, 375e396.
Nobili, M., Contin, M., Mondini, C., Brookes, P.C., 2001. Soil microbial biomass is
triggered into activity by trace amounts of substrate. Soil. Biol. Biochem. 33,
1163e1170.
Ohme-Takagi, M., Suzuki, K., Shinshi, H., 2000. Regulation of ethylene induced
transcription of defense genes. Plant Cell. Physiol. 41, 1187e1192.
Park, S.W., Lawrence, C.B., Linden, J.C., Vivanco, J.M., 2002. Isolation and charac-
terization of a novel ribosome-inactivating protein from root cultures of
pokeweed and its mechanism of secretion from roots. Plant Physiol. 130,
164e178.
Peck, M.C., Fisher, R.F., Long, S.R., 2006. Diverse avonoids stimulate NodD1 binding
to nod gene promoters in Sinorhizobium meliloti. J. Bacteriol. 188, 5417e5427.
Perry, L.G., Thelen, G.C., Ridenour, W.M., Weir, T.L., Callaway, R.M., Paschke, M.W.,
Vivanco, M.J., 2005. Dual role for an allelochemical: ()-catechin from
Centaurea maculosa root exudates regulates conspecic seedling establishment.
J. Ecol. 93, 1126e1135.
Phillips, D.A., Joseph, C.M., Maxwell, C.A., 1992. Trigonelline and stachydrine
released from alfalfa seeds activate NodD2 protein in Rhizobium meliloti. Plant
Physiol. 99, 1526e1531.
Phillips, D.A., Joseph, C.M., Yang, G.-P., Martinez-Romero, E., San-born, J.R.,
Volpin, H., 1999. Identication of lumichrome as a Sinorhizobium enhancer of
alfalfa root respiration and shoot growth. Proc. Natl. Acad. Sci. USA 22,
12275e12280.
Philippot, L., Raaijmakers, J.M., Lemanceau, P., van der Putten, W.H., 2013. Going
back to the roots: the microbial ecology of the rhizosphere. Nat. Rev. Microbiol.
11, 789e799.
Plancot, B., Santaella, C., Jaber, R., Kiefer-Meyer, M.C., Follet-Gueye, M.L., Leprince, J.,
Gattin, I., Souc, C., Driouich, A., Vicr e-Gibouin, M., 2013. Deciphering the re-
sponses of root border-like cells of Arabidopsis and ax to pathogen-derived
elicitors. Plant Physiol. 163, 1584e1597.
Popovici, J., Comte, G., Bagnarol, E., Alloisio, N., Fournier, P., Bellvert, F., Bertrand, C.,
Fernandez, M.P., 2010. Differential effects of rare specic avonoids on
compatible and incompatible strains in the Myrica gale-Frankia actinorhizal
symbiosis. Appl. Environ. Microbiol. 76, 2451e2460.
Prin, Y., Rougier, M., 1987. Preinfection events in the establishment of Alnus-Frankia
symbiosis: study of the root hars deformation step. Plant Physiol. 6, 99e106.
Proust, H., Hoffmann, B., Xie, X., Yoneyama, K., Schaefer, D.G., Yoneyama, K.,
Nogu e, F., Rameau, C., 2011. Strigolactones regulate protonema branching and
act as a quorum sensing-like signal in the moss Physcomitrella patens. Devel-
opment 138, 1531e1539.
Rajamohan, F., Pugmire, M.J., Kurinow, I.V., Uckun, F.M., 2000. Modeling and alanine
scanning mutagenesis studies of recombinant pokeweed antiviral protein.
J. Biol. Chem. 275, 3382e3390.
Rasmussen, T.B., Bjarnsholt, T., Skindersoe, M.E., Hentzer, M., Kristoffersen, P.,
Kote, M., Nielsen, J., Eberl, L., Givskov, M., 2005a. Screening for quorum-sensing
inhibitors (QSI) by use of a novel genetic system, the QSI selector. J. Bacteriol.
187, 1799e1814.
Rasmussen, T.B., Skindersoe, M.E., Bjarnsholt, T., Phipps, R.K., Christensen, B.K.,
Jensen, P.O., Andersen, J.B., Koch, B., Larsen, T.O., Hentzer, M., Eberl, L., Hoiby, N.,
Givskov, M., 2005b. Identity and effects of quorum-sensing inhibitors produced
by Penicillium species. Microbiology 151, 1325e1340.
Rasmussen, T.B., Givskov, M., 2006. Quorum-sensing inhibitors as anti-pathogenic
drugs. Int. J. Med. Microbiol. 296, 149e161.
Read, D.B., Bengough, A.G., Gregory, P.J., Crawford, J.W., Robinson, D.,
Scrimgeour, C.M., Young, I.M., Zhang, K., Zhang, X., 2003. Plant roots release
phospholipid surfactants that modify the physical and chemical properties of
soil. New Phytol. 157, 315e321.
Richardson, A.E., 2009. Regulating the phosphorus nutrition of plants: molecular
biology meeting agronomic needs. Plant Soil 322, 17e24.
Richardson, A., Barea, J.-M., McNeill, A., Prigent-Combaret, C., 2009. Acquisition of
phosphorus and nitrogen in the rhizosphere and plant growth promotion by
microorganisms. Plant Soil 321, 305e339.
Richardson, A.E., Lynch, J.P., Ryan, P.R., Delhaize, E., Smith, F.A., Smith, S.E.,
Harvey, P.R., Ryan, M.H., Veneklaas, J.E., Lambers, H., Oberson, A., Culvenor, R.A.,
Simpson, R.J., 2011. Plant and microbial strategies to improve the phosphorus
efciency of agriculture. Plant Soil 4, 59e61.
Rovira, A.D., 1969. Plant root exudates. Bot. Rev. 35, 35e57.
Ruyter-Spira, C., Kohlen, W., Charnikhova, T., van Zeijl, A., van Bezouwen, L., de
Ruihter, N., Cardoso, C., Lopez-Raez, J.A., Matusova, R., Bours, R., Verstappen, F.,
Bouwmeester, H., 2011. Physiological effects of the synthetic strigolactone
analog GR24 on root system architecture in Arabidopsis: another belowground
role for strigolactones? Plant Physiol. 55, 721e734.
Ryan, P.R., Delhaize, E., 2001. Function and mechanism of organic anion exudation
from plant roots. Annu. Rev. Plant Physiol. Mol. Biol. 52, 527e560.
Saeki, K., Kouchi, H., 2000. The lotus symbiont, Mesorhizobium loti: molecular ge-
netic techniques and application. J. Plant Res. 113, 457e465.
Sealey, L.J., McCully, M.E., Canny, M.J., 1995. The expansion of maize root-cap
mucilage during hydration. 1. Kinetics. Physiol. Plant 93, 38e46.
Schroth, M.N., Snyder, W.C., 1962. Exudation patterns from bean seeds and hypo-
cotyls and their effects on Fusarium solanii f. phaseoli (Abstr.). Phytopathology
52, 751.
Stubbs, V.E., Standing, D., Knox, O.G., Killham, K., Bengough, A.G., Grifths, B., 2004.
Root border cells take up and release glucose-C. Ann. Bot. Lond. 93, 221e224.
Shaw, L.J., Morris, P., Hooker, J.E., 2006. Perception and modication of plant
avonoid signals by rhizosphere microorganisms. Environ. Microbiol. 8,
1867e1880.
Subbarao, G.V., Ito, O., Sahrawat, K.L., Berry, W.L., Nakahara, K., Ishikawa, T.,
Watanabe, T., Suenaga, K., Rondon, M., Rao, I.M., 2006. Scope and strategies for
regulation of nitrication in agricultural systems e challenges and opportu-
nities. Crit. Rev. Plant Sci. 25, 303e335.
Subbarao, G.V., Rondon, M., Ito, O., Ishikawa, T., Rao, I.M., Nakahara, K., Lascano, C.,
Berry, W.L., 2007a. Biological nitrication inhibition (BNI) e is it a widespread
phenomenon? Plant Soil 294, 5e18.
Subbarao, G.V., Wang, H.Y., Ito, O., Nakahara, K., Berry, W.L., 2007b. NH
4
triggers the
synthesis and release of biological nitrication inhibition compounds in Bra-
chiara humidicola roots. Plant Soil.
290, 245e257.
Subbarao, G.V., Ban, T., Kishi, M., Ito, O., Samejima, H., Wang, H.Y., Pearse, S.J.,
Gopalakrishnan, S., Nakahara, K., Hossain, A.K.M.Z., Tsujimoto, H., Berry, W.L.,
2007c. Can biological nitrication inhibition (BNI) genes from perennial Leymus
racemosus (Triticeae) combat nitrication inwheat farming? Plant Soil 299, 55e64.
Subbarao, G.V., Nakahara, K., Hurtado, M.P., Ono, H., Moreta, D.E., Salcedo, A.F.,
Yoshihashi, A.T., Ishikawa, T., Ishitani, M., Ohnishi-kameyama, M., Yoshida, M.,
Rondon, M., Rao, I.M., Lascano, C.E., Berry, W.L., Ito, O., 2009. Evidence for
biological nitrication inhibition in Brachiaria pastures. Proc. Natl. Acad. Sci.
USA 106, 17302e17307.
Subbarao, G.V., Sahrawat, K.L., Nakahara, K., Ishikawa, T., Kishii, M., Rao, I.M.,
Hash, C.T., George, T.S., Srinivasa Rao, P., Nardi, P., Bonnett, D., Berry, W.,
Suenaga, K., Lata, J.C., 2012. Biological nitrication inhibition e a novel strategy
to regulate nitrication in agricultural systems. Adv. Agron. 114, 249e302.
Subbarao, G.V., Nakahara, K., Ishikawa, T., Ono, H., Yoshida, M., Yoshihashi, T.,
Zhu, Y., Zakir, H.A.K.M., Deshpande, S.P., Hash, C.T., Sahrawat, K.L., 2013a. Bio-
logical nitrication inhibition (BNI) activity in sorghum and its characterization.
Plant Soil 366, 243e259.
Subbarao, G.V., Sahrawat, K.L., Nakahara, K., Rao, I.M., Ishitani, M., Hash, C.T.,
Kishii, M., Bonnett, D.G., Berry, W.L., Lata, J.C., 2013b. A paradigm shift towards
low- nitrifying production systems: the role of biological nitrication inhibition
(BNI). Ann. Bot. http://dx.doi.org/10.1093/aob/mcs230.
Teplitski, M., Robinson, J.B., Bauer, W.D., 2000. Plants secrete substances that mimic
bacterial N-acyl homoserine lactone signal activities and affect population
density-dependent behaviors in associated bacteria. Mol. Plant Microbe
Interact. 13, 637e648.
Torres-Vera, R., Garcia, J.M., Pozo, M.J., Lopez-Raez, J.A., 2013. Do strigolactones
contribute to plant defence? Mol. Plant Pathol. 15, 211e216.
Tharayil, N., Triebwasser, D.J., 2010. Elucidation of a diurnal pattern of catechin
exudation by Centaurea stoebe. J. Chem. Ecol. 36, 200e204.
Umehara, M., Hanada, A., Magome, H., Takeda-Kamiya, N., Yamaguchi, S., 2010.
Contribution of strigolactones to the inhibition of tiller bud outgrowth under
phosphate deciency in rice. Plant Cell Physiol. 51, 1118e1126.
Vance, C.P., Uhde-Stone, C., Allen, D.L., 2003. Phosphorus acquisition and use:
critical adaptations by plants for securing a non-renewable source. New Phytol.
157, 423e447.
Van Ghelue, M., Lovaas, E., Ringo, E., Solheim, B., 1997. Early interactions between
Alnus glutinosa and Frankia strain ArI3. Production and specicity of root hair
deformation factor(s). Plant Physiol. 99, 579e587.
Vaughan, M.M., Wang, Q., Webster, F.X., Kiemle, D., Hong, Y.J., Tantillo, D.J.,
Coates, R.M., Wray, A.T., Askew, W., O'Donnell, C., Tokuhisa, J.G., Tholl, D., 2013.
Formation of the unusual semivolatile diterpene rhizathalene by the Arabi-
dopsis class I Terpene Synthase TPS08 in the root stele is involved in defense
against belowground herbivory. Plant Cell 25, 1108e1125.
Vicr e, M., Santaella, C., Blanchet, S., Gateau, A., Driouich, A., 2005. Root border-like
cells of Arabidopsis. Microscopical characterization and role in the interaction
with rhizobacteria. Plant Physiol. 2, 998e1008.
Vranova, V., Rejsek, K., Formanek, P., 2013. Aliphatic, cyclic, and aromatic organic
acids, vitamins, and carbohydrates in soil. Sci. World J. 2013, 15. http://
dx.doi.org/10.1155/2013/524239. Article ID 524239.
Walker, T.S., Bais, H.P., Grotewold, E., Vivanco, J.M., 2003. Root exudation and
rhizosphere biology. Plant Physiol. 132, 44e51.
Walker, T.S., Bais, H.P., D eziel, E., Schweizer, H.P., Rahme, L.G., Fall, R., Vivanco, J.M.,
2004. Pseudomonas aeruginosa-plant root interactions. Pathogenicity, biolm
formation, and root exudation. Plant Physiol. 134, 320e331.
Wall, L.G., 2000. The actinorhizal symbiosis. J. Plant Growth Regul. 19, 167e182.
Wang, E., Schornack, S., Marsh, J.F., Gobbato, E., Schwessinger, B., Eastmond, P.,
Schultze, M., Kamoun, S., Oldroyd, G.E., 2012. A common signaling proces that
promotes mycorrhizal and oomycete colonization of plants. Curr. Biol. 22,
2242e2246.
Wasson, A.P., Pellerone, F.I., Mathesius, U., 2006. Silencing the avonoid pathway in
Medicago truncatula inhibits root nodule formation and prevents auxin trans-
port regulation by rhizobia. Plant Cell 18, 1617e1629.
Waters, C.M., Bassler, B.L., 2005. Quorum sensing: cell-to-cell communication in
bacteria. Annu. Rev. Cell. Dev. Biol. 21, 319e346.
Watt, M., Wendy, K.S., Passioura, J.B., 2006. Rates of root and organism growth, soil
conditions, and temporal and spatial development of the rhizosphere. Ann. Bot.
97, 839e855.
Weir, T.L., Park, S.W., Vivanco, J.M., 2004. Biochemical and physiological mecha-
nisms mediated by allelochemicals. Curr. Opin. Plant Biol. 7, 472e479.
Weir, T.L., Bais, H.P., Stull, V.J., Callaway, R.M., Thelen, G.C., Bhamidi, S., Stermitz, F.R.,
Vivanco, J.M., 2006. Oxalate con-tributes to the resistance of Gaillardia grandi-
ora and Lupinus sericeus to a phytotoxin produced by Centaurea maculosa.
Planta 223, 785e795.
Wen, F., Van Etten, H.D., Tsaprailis, G., Hawes, M.C., 2007. Extracellular proteins in
pea root tip and border-cell exudates. Plant Physiol. 143, 773e783.
Wen, F., White, G.J., Van Etten, H.D., Xiong, Z., Hawes, M.C., 2009. Extracellular DNA is
required for root tip resistance to fungal infection. Plant Physiol. 151, 820e829.
Whipps, J.M., 1990. Carbon economy. In: Lynch, J.M. (Ed.), The Rhizosphere. John-
Wiley & Sons Ltd, Essex, UK, pp. 59e97.
Winkel-Shirley, B., 2002. Biosynthesis of avonoids and effects of stress. Curr. Opin.
Xie, X., Yoneyama, K., Yoneyama, K., 2010. The strigolactone story. Annu. Rev.
Phytopathol. 48, 93e117.
Yao, J., Allen, C., 2006. Chemotaxis is required for virulence and competitive tness
of the bacterial wilt pathogen Ralstonia solanacearum. J. Bacteriol. 188,
3697e3370.
Yates, E.A., Philipp, B., Buckley, C., Atkinson, S., Chhabra, S.R., Sockett, R.E.,
Goldner, M., 2002. N Acyl homoserine lactones undergo lactonolysis in a pH-,
temperature-, and acyl chain length-dependent manner during growth of
Yersinia pseudotuberculosis and Pseudomonas aeruginosa. Infect. Immun. 70,
5635e5646.
Yuen, P.Y., Cassini, S.T., De Oliveira, T., Nagem, T.J., Stacey, G., 1995. Xanthone in-
duction of nod gene expression in Bradyrhizobium japonicum. Symbiosis 19,
131e140.
Zakir, H.A.K.M., Subbarao, G.V., Pearse, S.J., Gopalakrishnan, S., Ito, O., Ishikawa, T.,
Kawano, N., Nakahara, K., Yoshihashi, T., Ono, H., Yoshida, M., 2008. Detection,
isolation and characterization of a root-exuded compound, methyl 3-(4-
hydroxyphenyl) propionate, responsible for biological nitrication inhibition by
sorghum (Sorghum bicolor). New Phytol. 180, 442e451.
Zhang, J., Subramanian, S., Stacey, G., 2009. Flavones and avonols play distinct
critical roles during nodulation of Medicago truncatula by Sinorhizobium meli-
loti. Plant J. 57, 171e183.
Zhu, B., Cheng, W.X., 2011. Rhizosphere priming effect increases the temperature
sensitivity of soil organic matter decomposition. Glob. Change Biol. 17,
2172e2183.
Zhu, Y., Zeng, H., Shen, Q., Ishikawa, T., Subbarao, G.V., 2012. Interplay among NH
4
uptake, rhizosphere pH and plasma membrane H
-ATPase deter-mine the

release of BNIs in sorghum roots e possible mechanisms and underlying hy-
pothesis. Plant Soil 358, 131e141.
Zhu, Y., Pierson, L.S., Hawes, M.C., 1997. Lnduction of microbial genes for patho-
genesis and symbiosis by chemicals from root border cells. Plant Physiol. 115,
1691e1698.
Zuanazzi, J.A.S., Clergeot, P.H., Quirion, J.C., Husson, H.P., Kondorosi, A., Ratet, P.,
1998. Production of Sinorhizobium meliloti nod gene activator and repressor
avonoids from Medicago sativa roots. Mol. Plant Microbe Interact. 11, 784e794.

TMP 8 E98

Hochgeladen von

Dokumentinformationen

Originalbeschreibung:

Originaltitel

Copyright

Verfügbare Formate

Dieses Dokument teilen

Dokument teilen oder einbetten

Freigabeoptionen

Stufen Sie dieses Dokument als nützlich ein?

Sind diese Inhalte unangemessen?

Copyright:

Verfügbare Formate

TMP 8 E98

Hochgeladen von

Copyright:

Verfügbare Formate

Review paper

Root exudates mediated interactions belowground

symbiosis. However, the release of H

after 30 days of incu-

) has a major inuence on the synthesis and release of

as N source did not release BNIs from roots,

grown plants, the release of BNIs was observed only when

(Subbarao et al., 2013a).

in the root environment.

uptake, rhizosphere pH and plasma membrane H

-ATPase deter-mine the

Das könnte Ihnen auch gefallen