Download Regulation and function of root exudates

Plant, Cell and Environment (2009) 32, 666–681
doi: 10.1111/j.1365-3040.2009.01926.x
Regulation and function of root exudates
DAYAKAR V. BADRI & JORGE M. VIVANCO
Centre for Rhizosphere Biology and Department of Horticulture and LA, Colorado State University, Fort Collins, CO 80523,
USA
ABSTRACT
Root-secreted chemicals mediate multi-partite interactions
in the rhizosphere, where plant roots continually respond to
and alter their immediate environment. Increasing evidence
suggests that root exudates initiate and modulate dialogue
between roots and soil microbes. For example, root exudates serve as signals that initiate symbiosis with rhizobia
and mycorrhizal fungi. In addition, root exudates maintain
and support a highly specific diversity of microbes in the
rhizosphere of a given particular plant species, thus suggesting a close evolutionary link. In this review, we focus mainly
on compiling the information available on the regulation
and mechanisms of root exudation processes, and provide
some ideas related to the evolutionary role of root exudates
in shaping soil microbial communities.
Key-words: ABC transporters; elicitors; mechanism of
secretion; root system architecture; tritrophic interactions.
INTRODUCTION
The main functions of the ‘hidden’ part of the plant, its root
system, have traditionally been thought to be anchorage
and uptake of nutrients and water. However, roots secrete
an enormous range of compounds into the surrounding soil.
This area, called the rhizosphere, can be divided into three
zones: endorhizosphere (root tissue, including the endodermis and cortical layers), rhizoplane (the root surface with
the epidermis and mucilage) and ectorhizosphere (the soil
nearby the root) (Lynch 1987). The first observation that
microbes are more abundant in the rhizosphere than in
distant soil was made by Hiltner (1904), and the first indication concerning root exudation and microbe abundance
was provided by Knudson (1920) and Lyon & Wilson
(1921). In recent years, the field of rhizosphere biology has
explored the relative importance of root exudates in mediating interactions with neighbouring plants and microbes
(Bais et al. 2004, 2006; Weir, Park & Vivanco 2004; Broeckling et al. 2008). Root exudation is part of the rhizodeposition process, which is a major source of soil organic carbon
released by plant roots (Hutsch, Augustin & Merbach 2000;
Nguyen 2003).The quantity and quality of root exudates are
determined by plant species, the age of an individual plant
and external factors like biotic and abiotic stressors. Root
Correspondence: J. M. Vivanco. Fax: +1 970 491 7745; e-mail:
[email protected]
666
exudation clearly represents a significant carbon cost to the
plant (Marschner 1995), with young seedlings typically
exuding about 30–40% of their fixed carbon as root exudates (Whipps 1990). Root exudates contain released ions
(i.e. H+), inorganic acids, oxygen and water, but mainly
consist of carbon-based compounds (Uren 2000; Bais et al.
2006). These organic compounds can often be separated
into two classes: low-molecular weight compounds, which
include amino acids, organic acids, sugars, phenolics and an
array of secondary metabolites, and high-molecular weight
compounds like mucilage and proteins. The classes of compounds secreted by roots are listed in Table 1.
Despite the technical difficulties inherent in the study of
plant roots, significant advances in root research have been
made using molecular and genetic tools. In addition, the
knowledge gained by studying the root system of the model
plant Arabidopsis thaliana (L.) Heynh. has been indispensable in advancing our understanding of the impact of agricultural practices on root development and the impact of
roots (and their exudates) on the soil environment (Bucher
2002). Molecular tools, such as cloning of root-specific
genes, differential and subtractive hybridization techniques
(Conkling et al. 1990; Rodriguez & Chader 1992), differential display (Liang & Pardee 1992), root-specific cDNA
libraries (Bucher et al. 1997) and analyzing root cell-specific
gene expression using a combination of molecular tools
(Birnbaum et al. 2003), have resulted in the rapid compilation of new information on root development, physiology
and biochemistry. In addition, the development of ‘composite plants’ (transgenic ‘hairy root’ systems with nontransgenic shoot systems) by employing Agrobacterium
rhizogenes-mediated transformation methods has enabled
studies of root-specific biochemistry, endosymbiosis, production of secondary metabolites and root-specific interactions (Boisson-Dernier et al. 2001; Choi et al. 2004; Lee et al.
2004; Limpens et al. 2004).
Root exudates mediate both positive and negative interactions in the rhizosphere. The positive interactions include
symbiotic associations with beneficial microbes, such as
mycorrhizae, rhizobia and plant growth-promoting rhizobacteria (PGPR). Negative interactions include association
with parasitic plants, pathogenic microbes and invertebrate
herbivores. In this review, we do not intend to provide
exhaustive coverage of the large body of literature that has
been published on root exudates and their interaction with
soil organisms. The reader is referred to other reviews for
further information on these areas (Bertin, Yang & Weston
© 2009 Blackwell Publishing Ltd
Regulation and function of root exudates 667
Table 1. Classes of compounds released in plant root exudates
Class of compounds
Single componentsa
Carbohydrates
Amino acids
Organic acids
Arabinose, glucose, galactose, fructose, sucrose, pentose, rhamnose, raffinose, ribose, xylose and mannitol
All 20 proteinogenic amino acids, l-hydroxyproline, homoserine, mugineic acid, aminobutyric acid
Acetic acid, succinic acid, l-aspartic acid, malic acid, l-glutamic acid, salicylic acid, shikimic acid, isocitric acid,
chorismic acid, sinapic acid, caffeic acid, p-hydroxybenzoic acid, gallic acid, tartaric acid, ferulic acid,
protocatacheuic acid, p-coumaric acid, mugineic acid, oxalic acid, citric acid, piscidic acid
Naringenin, kaempferol, quercitin, myricetin, naringin, rutin, genistein, strigolactone and their substitutes with
sugars
Catechol, benzoic acid, nicotinic acid, phloroglucinol, cinnamic acid, gallic acid, ferulic acid, syringic acid,
sinapoyl aldehyde, chlorogenic acid, coumaric acid, vanillin, sinapyl alcohol, quinic acid, pyroglutamic acid
Umbelliferone
Benzyl aurones synapates, sinapoyl choline
Cyclobrassinone, desuphoguconapin, desulphoprogoitrin, desulphonapoleiferin, desulphoglucoalyssin
Cyanidin, delphinidin, pelargonidin and their substitutes with sugar molecules
Indole-3-acetic acid, brassitin, sinalexin, brassilexin, methyl indole carboxylate, camalexin glucoside
Linoleic acid, oleic acid, palmitic acid, stearic acid
Campestrol, sitosterol, stigmasterol
Jugulone, sorgoleone, 5,7,4′-trihydroxy-3′, 5′-dimethoxyflavone, DIMBOA, DIBOA
PR proteins, lectins, proteases, acid phosphatases, peroxidases, hydrolases, lipase
Flavonols
Lignins
Coumarins
Aurones
Glucosinolates
Anthocyanins
Indole compounds
Fatty acids
Sterols
Allomones
Proteins and enzymes
a
List of single components presented in this table is reported mainly from the model plant Arabidopsis (see Narasimhan et al. 2003), and the
represented list is partial.
2003; Karthikeyan & Kulakow 2003; Bais et al. 2004; 2006;
Singh et al. 2004, Weir et al. 2004, Barea et al. 2005; Morgan,
Bending & White 2005; Prithiviraj, Paschke & Vivanco
2007; Bais, Broeckling & Vivanco 2008). Instead, this review
focuses on exploring the current knowledge relating to the
regulation and mechanism of root exudation, and how these
processes impact the plant at both the individual and ecosystem level. Furthermore, in this review, we argue that the
above-ground and below-ground diversities are linked by
plants, and that plant root-secreted compounds act as
signals to modulate underground microbe diversity and vice
versa.
ROOT ARCHITECTURE AND EXUDATION
Plant adaptation and survival in a given environment are
primarily determined by the ability of an individual to
acquire resources (Aerts 1999). The root system plays a big
role in acquisition of resources in a natural heterogeneous
soil environment (Lynch & Brown 2001). Root system
architecture (RSA) changes in nutrient-rich patches of soil
such as that found under conditions of high nitrate and
phosphorus (Ho et al. 2005; Paterson et al. 2006). In addition, the release of organic compounds from roots is a key
factor in mineralizing acquired nutrients and in mediating
plant–microbe interactions (Pierret et al. 2007). Therefore,
modulating growth and root branching in regions of
nutrient-rich patches may be expected to be coincident with
increased root exudation that could affect the nutrient
dynamics and microbial community (Paterson et al. 2006).
Hence, the authors believe that it is relevant to review the
information about RSA and its impact on exudation as one
of the focus points of this article.
Root system development is an important agronomic
trait for plant growth and survival because of its role in
water and nutrient uptake. RSA determines a plant’s survival in a given environment, allowing for the uptake of
resources and in turn the RSA is determined by the soil
environment. A wide variation in RSA of different plant
species suggests that it is determined by inherent genetic
factors. Basically, there are two well-known root system
structures: one is typically found in dicotyledonous species
(Arabidopsis, tomato, pea, etc.) and is usually comprised of
a primary (tap) root and lateral roots; the second one is
typically found in monocotyledonous species (rice, maize)
and is characterized by the development of many adventitious roots in parallel to the primary root (Esau 1965).
RSA is influenced by several biotic and abiotic factors.
Thus, the RSA is a plastic trait in which even genotypically
identical plants can differ depending on their macro- and
micro-environment.The molecular mechanisms responsible
for this plasticity are still poorly understood. A recent
report demonstrated that the lateral root primordial emergence is repressed by limiting water supply, and this
response is associated with abscisic acid and the LATERAL
ROOT DEVELOPMENT2 gene (Deak & Malamy 2005).
Apart from water, there are other exogenous abiotic factors
such as nitrogen (Lopez-Bucio, Cruz-Ramirez & Herreraestrella 2003), phosphorus (Linkhor et al. 2002), iron (Moog
et al. 1995) and light (Cluis, Mouchel & Hardtke 2004; Sorin
et al. 2005) that modulate root branching and RSA. Plants
under phosphorus starvation accumulate sugars and starch
in their leaves, and this increasing load of sucrose to the
phloem functions to relocate carbon resources to the roots,
which increase their size relative to the shoot by initializing
sugar signalling cascades that alter the RSA (Hammond &
White 2008). Under suboptimal nutrient levels of phosphorus, nitrogen and iron, plant species in the family of Proteaceae develop hairy rootlets that are aggregated in
longitudinal rows to form distinct clusters called proteoid
© 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 666–681
668 D. V. Badri & J. M. Vivanco
roots. These roots solubilize the minerals and organic nutrients, and facilitate uptake of inorganic nutrients by
enhanced secretion of carboxylates, phenolics and water
(Lamont 2003). There are other endogenous factors, called
phytohormones, that modulate root branching and RSA;
these include auxin, cytokinin, ethylene, gibberellins,
abscisic acid and brassinosteroids (Malamy 2005; Osmont,
Sibout & Hardtke 2007). RSA is also influenced by biotic
factors, because in nature plant roots are in contact with
saprophytic and pathogenic microbes. For example, after
infection with a specific Ralstonia solanacearum strain, the
lateral root elongation in petunia plants is inhibited, but
new lateral roots with abnormal morphology are induced
(Zolobowska & Van Gijsegem 2006). Similarly, the rhizobacterium Bacillus megaterium also alters the RSA by
inhibiting primary root growth and increasing lateral root
growth in A. thaliana (Lopez-Bucio et al. 2007). RSA in
some plants also changes upon symbiotic interactions such
as those with N-fixing bacteria in legumes (de Billy et al.
2001; Hirsch, Lum & Downie 2001) and mycorrhizae
(Hetrick 1991; Paszkowski et al. 2002).
It is possible that root branching and RSA play a significant role in determining the composition of exudates both
quantitatively and qualitatively. In addition, the knowledge
of the involvement of particular root cells (i.e. root cap,
epidermal cells and root hairs) in secretion of compounds
from roots is not clearly understood. In general, the zone
immediately behind the root tip is considered to be a major
site of exudation (Pearson & Parkinson 1961; Schroth &
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
(Pearson & Parkinson 1961; Bowen 1968; McDougall 1968;
Rovira 1969). Van Egeraat (1975) demonstrated that the
root tips of the primary and lateral roots were sites of
exudation by spraying ninhydrin on the filter paper where
the plant roots grew. Ninhydrin is a chemical compound
that interacts specifically with amine groups to produce a
purple colour. Since the discovery of this compound in 1910,
it has become a powerful analytical tool in the fields of
chemistry, biochemistry and forensic science. Frenzel (1957,
1960) reported that different compounds were released
from different parts of root system: asparagine and threonine from the meristem and root elongation zone; glutamic
acid, valine, leucine and phenylalanine from root hair zone;
and aspartic acid from the whole root. McDougall & Rovira
(1970) used 14C-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 from the whole length of
roots. In addition,Van Egeraat (1975) found that the release
of compounds was evident at the point of lateral root emergence in primary roots; this emergence leaves open wounds
that are not readily healed by the plant and seep compounds into the soil. Additionally, there are a few recent
reports indicating that root cap and root hair cells are
involved in secretion of compounds (Pineros et al. 2002;
Czarnota et al. 2003; Nguyen 2003). Generally, the apical
meristem of plant roots is covered by a group of cells
arranged in layers called the root cap, which sloughs off as
the root tip wends its way through the soil (Barlow 1975). It
has been proposed that these sloughed-off cap cells play a
significant role in determining the rhizosphere ecology, and
therefore the term ‘border cells’ was proposed (Hawes
1990). Border cells are involved in several functions: they
decrease frictional resistance experienced by root tips
(Bengough & McKenzie 1997), they regulate microbial
interactions through avoidance of harmful microbes
(pathogens) and favouring associations with beneficial
microbes (PGPR) (Hawes 1990; Hawes et al. 1998, 2000)
and they protect against heavy metal toxicity such as aluminium (Morel, Mench & Guckert 1986; Miyasaka &
Hawes 2001). A mucilaginous layer has been observed on
the surface of roots, particularly at the root tip, where it can
form a droplet in the presence of water (Samsevitch 1965).
This mucilage is secreted from the outer layers of root cap
cells and has been observed in most plant species (Paull &
Jones 1975; Miki, Clarke & McCully 1980; Rougier 1981).
However, small drops of mucilage secretion have also been
observed from root hairs or epidermal cells (Werker &
Kislev 1978). This secretion may derive from the root cap or
from the degradation of epidermal cell walls; alternately, it
may be synthesized by rhizoplane microorganisms (Rovira,
Foster & Martin 1979; Foster 1982; Vermeer & McCully
1982).
Root hairs are the extensions of single epidermal cells
and comprise as much as 77% of the total root surface area
of cultivated crops, forming the major point of contact
between the plant and the rhizosphere (Parker et al. 2000).
They play a pivotal role in rhizosphere processes including
anchorage and uptake of water and nutrients (Fan et al.
2001; Grierson, Parker & Kemp 2001; Michael 2001). Apart
from these functions, root hair cells are involved in root
secretion of compounds. Head (1964) observed spherical
droplets of liquid secreted from the tips of root hairs in
young apple roots growing behind a glass plate by using
time-lapse cine-photomicrography. Using light, cryoscanning electron and transmission electron microscopy, it has
also been observed that Sorghum species secrete sorgoleone solely from root hairs (Czarnota et al. 2003).
Besides the root cap and root hair cells, other root cells
are also involved in root secretion of compounds. For
example, maize roots secrete citrates in response to aluminium toxicity. Using the patch clamp technique, it was
determined that citrate secretion was predominant 5 cm
above the root cap, and involved cortex and stellar cells
(Pineros et al. 2002). In addition, comparison of citrate exudation rates in de-capped and capped roots indicated that
the root cap was not playing a role in citrate secretion.
Despite these findings, there is still a need to focus our
attention on root cells involved in root exudation both at
biochemical and molecular levels. Using ninhydrin is still
considered an important tool to identify the sites of exudation on roots, but the limitation of using it is that it is able to
detect only amino acids or ninhydrin-positive compounds in
the exudates. Further, identification of specific root cells
© 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 666–681
Regulation and function of root exudates 669
involved in exudation is now possible, thanks to new
molecular tools, such as the creation and study of Arabidopsis mutants impaired in the formation of specific root
cells.
REGULATION OF ROOT
EXCRETING PHYTOCHEMICALS
Roots are constantly exposed to a range of biotic and
abiotic stresses at the root–soil interface, and they respond
to these stresses by secreting a different blend of chemicals
to protect against negative influences and encourage
positive interactions. Mechanical impedance affecting
root morphology (Groleau-Renaud, Plantureux & Guckert
1998), soil compaction and mild drought conditions
(Brimecombe, De Leij & Lynch 2000) have been shown to
result in increased root secretion. In vitro, different growth
media can change the composition of root exudates of a
particular plant species, thus indicating that specific nutrition plays a role in root exudation. It has also been
reported that nutrient deficiency enhances exudation of
certain metabolites, particularly those that increase the
availability of nutrients for uptake by plant roots (Jones
1998). Environmental factors like temperature, light and
soil moisture also modulate root exudation processes. For
example, exudation of tannins and phenolic compounds in
Vicia faba was greatly reduced at 4 °C compared to the
amounts at 30 °C (Bekkara et al. 1998). Similarly, light
intensity alters the exudation of secondary metabolites
because of changes in photosynthesis. Watt & Evans (1999)
reported that the root exudation process follows diurnal
rhythms, with exudation increasing during light periods.
For example, Almus glutinosa (L.) root exudates have
increased flavonoid content under light conditions
(Hughes et al. 1999). High soil moisture also regulates the
root secretion of compounds because of the limited availability of oxygen, which leads to hypoxia. Hypoxia causes a
respiration shift from aerobic to anaerobic, resulting in the
accumulation of ethanol, lactic acid and alanine at phytotoxic levels (Rivoal & Hanson 1994). Xia & Roberts (1994)
reported that plants escape the toxic effects of accumulated ethanol and lactic acid by secreting these metabolites
from their roots.
The presence (or absence) of particular minerals and
toxic metals in the soil can also alter the composition of root
exudates. It has been shown that plant roots secrete citric,
oxalic and malic acids to detoxify aluminium in the soils,
and the secretions of these organic acids are highly specific
to aluminium stress. In addition, the aluminium-induced
secretion pattern of organic acids varies with plant species
(Ma 2000; Liao et al. 2006; Wang et al. 2006). Phosphorus
deficiency also results in enhanced root secretion of phenolic compounds in certain tree and legume species, and the
specificity of organic acid secretion in response to P deficiency varies with plant species (Dinkelaker, Hengeler &
Marschner 1995; Chishaki & Horiguchi 1997; Dinkelaker
et al. 1997; Neumann, George & Romheld 1998; Neumann
& Romheld 1999). Plant species that normally co-occupy an
ecological niche are likely to have developed mechanisms
of detoxifying toxins produced by one another through oxidation, carbohydrate conjugation or sequestration (Inderjit
& Duke 2003). Recent evidence suggests that some plant
species can better withstand assault by (⫾) catechin, a
potential allelotoxin produced by 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).
Exudation rates also vary with plant developmental stage
and between genotypes within a single species. Seedlings
produce the lowest amounts of root exudates; this gradually
increases until flowering and decreases again at maturity
(Aulakh et al. 2001). Garcia et al. (2001) showed that root
exudation is positively correlated with root growth; it
means that actively growing root systems secrete more
exudates. Similarly, they observed variations in exudation
patterns between genotypes of the same plant species. For
example, the A. thaliana ecotypes, Col-0 and Ler, differ in
the levels of malate present in their root exudates (Hoekenga et al. 2003). Both qualitative and quantitative differences were observed in the root exudation of different plant
species (Cieslinski et al. 1997), and the differences are
greater if they are less phyologenetically related (Fletcher
& Hegde 1995).
Elicitors are molecules that stimulate defence or stressinduced responses in plants. Gleba et al. (1999) postulated
that chemical and physical elicitors stimulate roots of
various plants to secrete phytochemicals in much higher
quantities than non-elicited plants. Moreover, roots of elicited plants exude an array of compounds not detected in
the exudates of non-elicited plants. In addition, a single
elicitor can trigger induction of different compounds in
different plant species. Exogenous application of defencesignalling molecules, such as salicylic acid (SA), methyl
jasmonate (MeJA) and nitric oxide (NO) induces the
accumulation of a wide range of secondary metabolites
(see review of Zhao, Davis & Verpoorte 2005). Mineral
deficiencies also induce the intrinsic production of elicitors
that mediated signalling responses; for example, potassium
deprivation induces the jasmonic acid-mediated defence
responses (Schachtman & Shin 2007). It has been demonstrated that SA and MeJA are found in the medium of
cultured plant cells (Parchmann, Gundlach & Mueller
1997; Chen et al. 2001), and NO is found in the apoplastic
space of plant roots (Stohr & Ullrich 2002). Noritake,
Kawakita & Doke (1996) reported that NO induces phytoalexin (rishitin) accumulation in potato tuber tissues as
well as in the exudates. Kneer et al. (1999) showed that
roots of hydroponically cultivated Lupinus luteus secrete
genistein, which was induced 10-fold by SA treatment.
Recent evidence suggests that treatment of Arabidopsis
plant roots with SA, MeJA and NO increased the root
exudation of phytochemicals compared with control plant
roots (Badri et al. 2008a). The list of secondary metabolites
shown to be induced by these defence-signalling molecules
is shown in Table 2.
© 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 666–681
670 D. V. Badri & J. M. Vivanco
Plants
Signalling molecule
Targeted secondary metabolites
Arabidopsis thaliana
Avena sativa
Catharanthus roseus
Centella asiatica
Coleus blumei
Cupressus lusitanica
Daucus carota
MeJA, SA
NO
JA, NO
MeJA
MeJA
MeJA
JA
Echinacea pallida
Eschscholtiza californica
Glycine max
MeJA
MeJA, SA
MeJA
Glycyrrhiza glabra
Hyoscyamus niger
Hypericum perforatum
Lithospermum erythrorthion
Lupinus luteus
Lycopersicon esculentum
Oryza sativa
Ocimum basilicum
Panax ginseng
Portulaca
Rauvolfia canescens
Sanguinaria canadensis
Saussurea medusa
Silybum marianum
Solanum tuberosum
Sophora flavescens
Taxus chinensis
MeJA
MeJA, SA
MeJA, SA
MeJA
SA
MeJA
MeJA
MeJA
MeJA, SA
MeJA
MeJA
MeJA
MeJA, SA
MeJA
MeJA, NO
JA, NO
Synthetic MeJA
(HEJA)
MeJA
Indole glucosinolates, camalexin
Avenanthramides
Ajmalicine, catharanthine, vindoline
Asiatocoside, triterpenes
Rosmarinic acid
b-Thujaplicin
6-Methoxymellein, 4-hydroxybenzoic
acid
Alkamides, ketoalkene/ynes
Benzphenanthridines, sanguinarine
Glyceollins, apigenin, daidzein,
genistein, luteolin
Soyasaponin
Hyoscyamine, rishitin, scopolamine
Hypericin
Rosmarinic acid
Genistein
Scopoletin
Momilactones, sakuranetin
Rosmarinic acid, caffeic acid
Ginsenoside
Betacyanin
Raucaffricine
Sanguinarine
Jaceosidin, hispidulin
Silymarin
Rishitin, lubimin, phytuberin
Matrine
Taxoid
Vitis vinifera
Table 2. List of secondary metabolites
induced by defence signalling molecules in
plantsa
Stilbene, resveratrol
a
This list is modified and updated from Zhao et al. (2005).
MeJA, methyl jasmonate; JA, jasmonic acid; SA, salicylic acid; NO, nitric oxide; HEJA,
2-hydroxyethyl jasmonate.
CAN NEIGHBOURS ALTER PLANT ROOT
EXUDATION PROFILES?
The plant root–soil interface is an environment with high
microbial inoculum, composed of both pathogenic and
beneficial microbes (Rouatt & Katznelson 1960; Rouatt,
Katznelson & Payne 1960). Thus, plant roots are constantly
exposed to an array of microbes, and must interact and
defend according to the type of biotic stress (Bais et al.
2004, 2006). How do these interactions affect root exudation? It has also been demonstrated that plants release
host-specific flavonoids in response to compatible rhizobia
strains (Dakora, Joseph & Phillips 1993; Pueppke et al.
1998). Recent evidence shows that microbes can modulate
plant root exudation of proteins (De-la-Pena et al. 2008).
The study of De-la-Pena et al. (2008) clearly demonstrated
that the compositions of proteins present in the root
exudates change upon the presence of a given microbial
neighbour and that the exudation of proteins by a given
bacterium is modulated by the presence of a specific plant
neighbour. This study used two model plants, Arabidopsis
and Medicago, and the microbes Pseudomonas syringae
(DC3000) as a bonafide pathogen of Arabidopsis and
Sinorhizobium meliloti (RM1021) as a symbiont of Medicago. The availability of the genome sequences for all four
organisms allowed tracking down the origin of a given
protein to determine if it was produced by a plant or by a
bacterium. It was found that the interaction between
Medicago–S. meliloti increased the secretion of seven plant
proteins such as hydrolases, peptidases and peroxidases, but
these proteins were not induced in Medicago–P. syringae
interaction. Similarly, the Arabidopsis–P. syringae interaction induced the secretion of several plant defence-related
proteins, but these proteins were not induced in the
Arabidopsis–S. meliloti interaction. Additionally, it was
found that S. meliloti secreted four proteins in high levels
[superoxide dismutase, putative glycine-betain-binding
ATP-binding cassette (ABC) transporter protein, outer
membrane lipoprotein and hypothetical protein SMc02156]
in the presence of Medicago. But in the presence of Arabidopsis, S. meliloti secreted different proteins. Similarly, P.
syringae secreted a different array of proteins in the presence of Arabidopsis or Medicago. These data provide concrete evidence that both plant root and bacterial protein
secretion profiles change in response to the identity of the
neighbour.
© 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 666–681
Regulation and function of root exudates 671
At this point, it is appropriate to speculate that if plants
can sense and respond to the presence of a given neighbouring microbe by altering the secretion of proteins for a
particular purpose, it is then possible that plants can sense
and respond to the presence of particular plant neighbours. If a microscopic organism is sensed by the roots
possibly because of specific receptors, then the presence of
a macroscopic neighbouring root might be better perceived by the plant. This sort of perception mechanism suggests a highly sophisticated behavioural pattern by which
plants could alter their physiology and biochemistry based
on the presence of a particular neighbour. The case of
invasive weeds is worth highlighting as a possible example
of this kind of behaviour. For the most part, invasive weeds
are not invasive in their native range where they are kept
in check supposedly by the presence of specialized insects
and pathogens among other factors, whereas the weeds
become highly invasive in the introduced range where
those insects or pathogens are not present. It could be possible to infer that the native surrounding plants and the
overall interaction of the weed with its native plant community might keep it in check by modulating certain physiological or biochemical parameters like favouring defence
as compared to growth. When a weed arrives to a new
location where those evolutionary interactions with plant
neighbours are not present, its biochemistry and physiology could be altered to favour growth over defence.
Further, the presence of the same species as a neighbour
(monoculture) as compared to the presence of a different
individual (polyculture) could be part of the response and
could also alter the balance between defence and growth
among other physiological characteristics. If this sort of
response happens to be true, plants could be exhibiting
some sort of social response. A recent paper has
shown that the outcome of glucosinolates activation in
Arabidopsis was regulated by the presence of neighbouring plants and found that the production of glucosinolates
is increased in a high-density enviornment (large number
of Arabidopsis plants grown together) compared with a
low-density range (few number of Arabidopsis plants
grown together) (Wentzell & Kliebenstein 2008).
MECHANISM OF ROOT SECRETION
In recent years, researchers have made enormous progress
in analyzing the composition of root exudates and their
interactions with neighbours in rhizosphere soil. However,
the mechanism of secretion of root exudates is still poorly
understood. The production and release of root-derived
compounds are commonly constitutive, but may be induced
by biotic or abiotic stress as described previously in this
article. The mechanism by which plant roots secrete
compounds is primarily thought to be a passive process
mediated through three separate pathways: diffusion,
ion channels and vesicle transport (Fig. 1) (Neumann &
Romheld 2000; Bertin et al. 2003).
During diffusion, small polar molecules and uncharged
molecules are transported through permeability nature of
lipid membranes (Sanders & Bethke 2000). This passive
diffusion process depends on membrane permeability
(Guern, Renaudin & Brown 1987) and cytosolic pH (Marschner 1995). Other compounds like sugars, amino acids
and carboxylate anions are transported across membranes
by the aid of proteins, and their direction of movement is
dependent on their electrochemical gradient that allows
them to pass from the cytoplasm of intact root cells (millimolar range) to the soil (micromolar range). Samuel,
Fernando & Glass (1992) showed that the large cytosolic K+
diffusion potential and the extrusion of protons through
ATPase generate a positively charged gradient that
Cytosol
ABC transporter
Fatty acids/ Flavonoids
Vesicular trafficking
Anion channel
Carbohydrates
PM
TMD1
NBD1
TMD2
Diffusion
High-molecular
weight compounds
Low-molecular
weight compounds
Metal
transporters
Silica Aquaporins
Uncharged
molecules
NBD2
2ATP
2ADP + 2Pi
Apoplast
Figure 1. Mechanisms of root exudation of compounds through the plant cell membrane (modified from Bertin et al. 2003). PM, plasma
membrane; TMD, transmembrane domain; NBD, nucleotide-binding domain.
© 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 666–681
672 D. V. Badri & J. M. Vivanco
promotes the release of carboxylate anions. Factors that
affect membrane integrity could also promote the release of
organic acids (Jones & Darrah 1995). In these cases, anion
channels in the roots mediate the controlled release of
these compounds (Ryan, Delhaize & Randall 1995; Zheng,
Ma & Matsumoto 1998; Neumann et al. 1999; Sakaguchi
et al. 1999).
There are specific transporters for sugars, amino acids
and metals that are involved in the secretion of specific
compounds from root cells (Williams, Pittman & Hall
2000; Hussain et al. 2004; Colangelo & Guerinot 2006;
Hirner et al. 2006; Hoekenga et al. 2006; Grabov 2007; Lee
et al. 2007; Svennerstam et al. 2007). Plants have mechanisms of metal homeostasis to avoid excess concentrations
of free metal ions (e.g. Fe, Zn, Mn and Cu); these mechanisms involve coordination of metal ion transporters
for uptake, translocation and compartmentalization (see
review by Hayden & Cobbett 2007). For example, graminaceous species secrete mugineic acid, a metal-binding
ligand secreted from roots into the rhizosphere, and form
Fe(III)-MA ligand to reduce the Fe toxicity and then
enter into the root cells via a specific transporter YSL
identified in maize (Curie et al. 2001; Curie & Briat 2003).
Recent evidence demonstrated that the silicon efflux
transporter from rice is involved in efflux of silicon from
root cells (Ma et al. 2007; Ma & Yamaji 2008). Similarly,
it has been demonstrated that malate transporter
(AtALMT1) plays a critical role in releasing malate from
root cells under aluminium toxicity in Arabidopsis (Kobayashi et al. 2007). There are other transporters like
monosaccharide transporters that are involved in transporting hexoses, pentoses including ribose and polyols
such as myo-inositol and glycerol (Klepek et al. 2005;
Buttner 2007).
Excretion of high-molecular weight compounds by roots
generally involves vesicular transport (Battey & Blackbourn 1993). Knowledge of the vesicle-mediated trafficking of proteins is well understood (see review by Field,
Jordan & Osbourn 2006), but the mechanism of vesiclemediated transport of phytochemicals is not fully characterized (Lin, Irani & Grotewold 2003; Grotewold 2004).
There are reports demonstrating that plant defence
responses are accompanied by trafficking of antimicrobial
compounds to the site of pathogen infection. For example,
pigmented vesicles (such as the antimicrobial flavonoids,
3-deoxyanthocyanidins) accumulate on sorghum leaves at
sites of attempted fungal infection (Snyder & Nicholson
1990; Snyder et al. 1991). Similarly, the pigmented antimicrobial napthoquinones are secreted into the apoplast of
the boraginaceous plant, Lithospermum erythrorhizon by a
vesicle-mediated mechanism in response to fungal elicitation (Tabata 1996; Yazaki et al. 2001, 2002). However, these
studies only demonstrate the vesicle-mediated transport of
phytochemicals in leaf cells, and there is still no clear evidence for the mechanism of phytochemical secretion from
root cells, except for Golgi-mediated transport of mucilage
polysaccharides across the root cap (Neumann & Romheld
2000).
ARE ABC TRANSPORTERS INVOLVED IN
ROOT EXUDATION PROCESSES?
Other mechanisms of transport of defence-related phytochemicals within plant cells include ABC transporters
and multidrug and toxic compound extrusion (MATE)
transporters (Yazaki 2005). The former mechanism involves
directly energized primary transport by ATP hydrolysis, and
the latter an H+ gradient-dependent secondary transport.
Both groups have been implicated in transport of flavonoids to the vacuole (Yazaki 2005). ABC transporters
encompass a large protein family found in all phyla
(Higgins 1992), and the number of these transporters
reported in Arabidopsis exceeds those reported in yeast or
humans (Decottignies & Goffeau 1997; Dean, Hamon &
Chimini 2001; Rea 2007). Plants are sessile and thus require
many adaptive strategies to interact with the environment,
and this suggests that the high number of potential chemicals produced by plants compared to other organisms may
need a higher number of transporters (Dixon 2001). In
bacteria, ABC transporters function as importers and
exporters of compounds from the cell. In eukaryotes, recent
evidence suggests that some plant ABC transporters also
have import functions (Saurin, Hofung & Dassa 1999;
Shitan et al. 2003; Santelia et al. 2005; Terasaka et al. 2005).
Plant ABC proteins are classified into 13 subfamilies on the
basis of protein size (full or half), orientation (forward or
reverse), presence or absence of idiotypic transmembrane/
linker domains and overall sequence similarity (SanchezFernandez et al. 2001). ABC transporters are involved in
diverse cellular processes, such as the excretion of potential
toxic compounds, lipid translocation, heavy metal tolerance,
nutrient transport, salt stress and in disease resistance
(Balzi & Goffeau 1994; Szczypka et al. 1994; Maathuis et al.
2003; Kobae et al. 2006; Stein et al. 2006). In plants, the
best-characterized ABC transporters are the full molecules
belonging to three subfamilies, multidrug resistance-related
protein (MRP), pleiotropic drug resistance protein (PDR)
and multidrug resistance P-glycoproteins (PGP).
Recent studies, using a pharmacological approach, demonstrated that root secretion of certain plant secondary
metabolites is an ATP-dependent process, suggesting that
ABC transporters are involved in root secretion processes
(Loyola-Vargas et al. 2007;Sugiyama,Shitan &Yazaki 2007).
Loyola-Vargas et al. (2007) demonstrated that Arabidopsis
root secretion profiles showed differences (quantitatively
and qualitatively) compared with control in presence of
inhibitors like potassium cyanide, sodium orthovanadate,
verapamil, nifedipine, glibenclamide and quinidine. This
clearly indicates that different active transporting systems
are involved in root secretion process that includes ABC
transporters and P-type ATPases, because all these inhibitors used in this study would deplete the ATP pool in the cell.
In addition, another study reported that the secretion of
genistein, a signal flavonoid involved in rhizobium
symbiosis secreted from soy bean roots, was mediated by an
ABC transporter by an ATP-dependent manner, which
was demonstrated by using the specific ABC transporter
© 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 666–681
Regulation and function of root exudates 673
inhibitor sodium orthovanadate, but the secretion of
genistein was not inhibited by other inhibitors like nigericin,
valinomycin and gramicidin D that inhibit plasma membrane ionophores (Sugiyama et al. 2007). The two previous
evidences describe the involvement of ABC transporters
in root secretion processes indirectly by using inhibitors.
Recently, Badri et al. (2008b) showed direct evidence of the
involvement of ABC transporters in root secretion process
by using Arabidopsis knock-out mutants lacking expression
of specificABC transporter proteins highly expressed in root
cells (lateral root cap, epidermal cells, endodermis). This
study identified three different compounds transported by
distinct ABC transporters, and among those one compound
was tentatively identified as 3-hydroxy-4(Z), 6(Z), 8(Z),
10(Z)-tetraenoic acid. Further, this study showed that one
ABC transporter can transport structurally different compounds, or one compound could be transported by different
transporters. Further investigation to identify other transporting systems (such as MATE) and their substrates
involved in root secretion of phytochemicals is necessary to
reap agricultural and biotechnological benefits from root
exudation.
NOVEL FUNCTIONS OF ROOT EXUDATES
Root exudates engage in several types of interactions both
positive and negative such as plant–plant, plant–microbe
and tritrophic (plant–microbe–nematode) interactions in
the complex rhizosphere. There is exhaustive literature
available on root exudates mediating plant–plant and
plant–microbe interactions (Bertin et al. 2003; Bais et al.
2004, 2006, 2008; Weir et al. 2004; Prithiviraj et al. 2007). In
this review, we focus on two aspects with a few examples
in the literature: tritrophic interactions and self/non-self
recognition.
Unlike plants and microbes, rhizospheric nematodes are
highly mobile and may respond to the chemical communication that occurs between microbes and plants. Tritrophic
(plant, microbe and nematode) interactions are best
described in the context of research with rhizobia, mycorrhizal fungi and plant pathogens (Khan 1993; Khan et al.
2000). The outcome of these studies has shown that
tritrophic interactions in the rhizosphere occur when nematodes and microbes act synergistically to influence plant
growth. A different study shows that the soil-dwelling
nematode Caenorhabditis elegans could also mediate interactions between roots and rhizobia in a positive way leading
to increased nodulation (Horiuchi et al. 2005). This study
demonstrated that the nematode acts as vector by carrying
S. meliloti to the roots of the legume plant in response to
plant root-released volatiles resulting in the initiation of
plant–microbe symbiosis. A similar study reported the
attraction of entomopathogenic nematodes to insectdamaged corn roots in a field setting (Rasmann et al. 2005).
However, the knowledge of the influence of nematodes and
their interactions with plant roots and root secreting compounds and microbes is very limited. An understanding of
the underlying signalling in the rhizosphere related to these
tritrophic interactions could greatly contribute to the
improvement of more ecologically friendly agricultural
practices.
Another well-studied example of tritrophic interactions
is the communication mediated by plant root-secreted compounds with parasitic plants and arbuscular mycorrhizal
fungi (AMF). Plants use a wide range of compounds to
attract beneficial organisms and deter harmful organisms.
However, the attraction of beneficial organisms could
also lead to abuse by malevolent organisms. The classical
example of such a case is the relationship between plants,
beneficial mutualistic AMF and harmful parasitic plants
which is mediated by the root-secreted compound strigolactone and its derivatives (Bouwmeester et al. 2007).
Strigolactones are detected in low quantities in the exudates of a range of plant species including maize, pearl
millet, red clover, tomato, Lotus japonicus and Menispermum dauricum (Sugimato 2000; Sato et al. 2003; Awad et al.
2006). Numerous previously unrelated facts from past
research about this complex interaction can now be integrated into a schematic way: (1) low phosphate in soil is
conducive to AMF symbiosis (Smith & Read 1997); (2)
phosphate starvation induces secretion of strigolactone
from plant roots (Yoneyama et al. 2007); (3) strigolactones
promote AMF colonization of host plants (Gomez-Roldan
et al. 2007); (4) strigolactones also promote parasitic plant
infection (Bouwmeester et al. 2003); and (5) AMF colonization prevents parasitic plant infection through the downregulation of germination stimulant production (Lendzemo
et al. 2007). Besides those functions of strigolactones and
their related compounds, two recent studies demonstrate
that they are also involved in the inhibition of shoot branching (Gomez-Roldan et al. 2008; Umehara et al. 2008).
There is communication between above-ground and
below-ground parts of the plant to prevent or limit
pathogen-causing diseases. A corresponding intra-plant
signalling between roots and shoots was demonstrated
in herbivory (Rasmann et al. 2005). In this study, it was
demonstrated that western corn rootworm (WRC) larvae
feeding on maize leaves induce the secretion of the belowground plant signal (E)-b-caryophyllene by maize roots to
recruit an entomopathogenic nematode. Certain beneficial
rhizobacteria activate the plant defence responses to
prevent foliar diseases (Ryu et al. 2004). Similarly, plant
roots secrete signalling compounds to attract symbionts
such as rhizobium and AMF (Kent Peters & Long 1988;
Besserer et al. 2006), but what plant root signals are
involved in recruiting beneficial rhizobacteria has been
poorly studied. Recent evidence (Rudrappa et al. 2008)
demonstrated that l-malic acid, an intermediate of the tricarboxylic acid (TCA) cycle secreted from plant roots, is
involved in recruiting the beneficial rhizobacteria Bacillus
subtilis FB17 in a dose-dependent manner. This study
further demonstrated that the secretion of l-malic acid
from roots was enhanced by foliar inoculation of the pathogen P. syringae pv. tomato (Pst DC3000). This study should
pave the way for the understanding of signals that tie
above- and below-ground responses in plants.
© 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 666–681
674 D. V. Badri & J. M. Vivanco
The below-ground competition driven by plant roots is a
ubiquitous phenomenon in many natural and semi-natural
types of vegetation. Several studies have confirmed that
roots respond to neighbouring roots in a very specific
manner that depends on the identity of the neighbour
(Maina, Brown & Gersani 2002; de Kroon, Mommer &
Nishiwaki 2003; Falik, de Kroon & Novoplansky 2006).
Recent evidence suggests that plants can recognize kin, thus
influencing competitive conditions in root interactions,
allowing greater root allocation when grown with strangers
rather than with siblings (Dudley & File 2007). The mechanism behind self/non-self root discrimination still remains
obscure, but it has been suggested that root exudates could
play a role in this response (de Kroon 2007). Ariel
Novoplansky’s article in this issue, ‘Behaviour Under Competitive Conditions, Including Self Recognition’, provides
more detailed information on this aspect.
ARE ROOT EXUDATES INVOLVED IN
CO-EVOLUTIONARY RELATIONSHIPS IN
THE RHIZOSPHERE?
Some of the examples given in the previous section pertain
to artificial environmental or highly controlled greenhouse
conditions, so the reader might ask how root exudation is
playing a role in affecting or contributing to biodiversity
under natural conditions. The diversity of the microbial
(bacterial and fungal) communities in soil is extraordinary,
and 1 g of soil could contain more than 10 billion microorganisms belonging to thousands of different species
(Roselló-Mora & Amann 2001). Soil microbial populations
are involved in a framework of interactions known to affect
key environmental processes, like biogeochemical cycling
of nutrients, plant health and soil quality (Barea et al. 2005;
Giri et al. 2005). Most of the dynamic microbial interactions
happen near the plant roots and in the root–soil interface,
an area called the rhizosphere (Lynch 1987; Barea et al.
2005; Bais et al. 2006; Prithiviraj et al. 2007). There is variation in microbial communities in rhizosphere soil that supposedly depends on the age of the plant, crop species and
soil type (Wieland, Neumann & Backhaus 2001; Buyer,
Roberts & Russek-Cohen 2002; Kowalchuk et al. 2002;
Hogberg, Hogberg & Myrold 2007). Most importantly,
recent evidence suggests that specific plant species cultivate
their own soil fungal community composition and diversity,
and that this ‘cultivation’ is mediated by root secreting compounds (Broeckling et al. 2008). In this study, two model
plant species (A. thaliana and Medicago truncatula) were
grown in their native soil (collected in natural communities)
and in the other plant’s soil under greenhouse conditions. It
was found that Arabidopsis maintained its own fungal community in resident soil, but not in the non-resident soil
(Medicago-grown soil). When the plants were grown in a
third soil that did not support Arabidopsis or Medicago
plants, the microbial communities in those soils declined
dramatically as in the non-resident soil treatments. The
same response was observed when root exudates were
added to the soil rather than growing plants, thus indicating
that plants drive these responses by the release of root
exudates and that this interaction has a co-evolutionary
component.
Another study (Broz, Manter & Vivanco 2008) showed
a similar observation but under field conditions. This study
found that soils collected in Montana from high-density
stands of the invasive plant spotted knapweed had significant declines in fungal community composition and diversity compared with soil collected from low-density stands
of the weed. The fact that invasive weeds decrease the
diversity and relative numbers of microbes (Broz et al.
2008) in the soil strengthens our belief that there is a
co-evolutionary link between roots and soil microbes that
is mediated by the release of root exudates. In the case of
the weed, when it arrives in a new place, it simply wipes
out the soil microbes in that location through the release
of root exudates. These exudates could either have negative effects on the microbes (antimicrobials) or are simply
not the correct carbon source required to support the
growth of the microbes. It is possible that after a certain
period, the weeds might start to culture a microbial community resembling those of their native range; however,
this scenario is unlikely because the full ecological community of the native range would be nearly impossible to
duplicate. Such a community is composed of a variety of
other plants, each releasing their own root exudates and
modifying the soil microbial community for the benefit of
their ecosystem. When this ecosystem is affected such as
by the introduction of a new plant with no co-evolutionary
history, the decline in co-evolved soil microbes might
affect physiological processes in some of the plants. In an
invaded range, this could lead to some of the plants being
made less competitive and ultimately vulnerable to the
weed’s invasion. A similar correlation could be made with
monocultures of crops: it could be hypothesized that such
crops are drastically altering the microbial composition of
a given soil. It is known that plant crops in their native
habitats do not produce as much as the same crop in a
non-native habitat, and this has usually been attributed to
inputs (soil properties and nutrients) and weather. For
instance, potatoes grow very small with low yield in the
Andes of South America, its centre of origin and domestication. Based on the ideas provided earlier, one could
speculate that crops in their native land are exposed to a
significant number of co-evolved soil microbes, including
beneficial and pathogenic ones, and that these microbes
have co-evolutionary interactions that maintain an overall
balance, preventing any particular species from becoming
dominant. On the other hand, a crop grown in a nonnative habitat can have high yields because of the low
number of soil pathogens; however, if a particular inoculum of a pathogen were to arrive to the system, it could
easily flourish and become dominant because of the lack
of other competing and co-evolved microbes (Fig. 2). A
possible example of this situation is the potato famine of
Ireland (circa 1845–1852) where Phytopthora infestans
decimated most of the potato fields within a few years of
being introduced.
© 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 666–681
Regulation and function of root exudates 675
Native habitat
(a)
Introduced habitat (recent)
(b)
Introduced habitat (old)
(c)
Figure 2. Co-evolutionary link of a given plant with soil microbes. A plant in its native habitat (a) survives relatively well even in the
presence of diverse set of microbes, some of which are pathogenic. However, because of co-evolved interactions between rhizosphere
microbes, all organisms are kept in check and none of them become dominant. When a plant is taken to a new habitat (b), it grows better
than in native habitat (a) because of the lack of co-evolved pathogens present in the new habitat and could eventually decrease the
diversity of the microbes in the soil. However, if a pathogen were to arrive in the new habitat (b), it could become dominant in the
rhizosphere because of the lack of other co-evolved microbes to keep the potential pathogen in check, resulting in scenario (c). As a
result, the plant could die (c).
FURTHER LINKS BETWEEN ABOVE- AND
BELOW-GROUND RESPONSES
An increasing number of studies have probed the ecological
significance of changes in root exudation patterns, but the
clearest evidence of significance comes from the studies
that seek a mechanistic basis for plant responses to herbivory. For example, the root herbivore Heterodera trifolii
causes changes in the root exudation patterns of white
clover, stimulating the biomass and activity of soil microbes.
These positive effects subsequently create a positive feedback with the plant, ultimately benefiting plant growth in
longer term (Hamilton & Frank 2001; Ayres et al. 2004).
Another example is AMF that enhances plant species diversity in early successional communities (Van der Heijden
et al. 1998), because they promote subordinate herb species
relative to the dominant graminoids and also help to distribute the soil resources evenly, reducing the ability of
certain species to monopolize resources (Van der Heijden
2004). It is obvious that the association of roots and AMF is
initiated by root secreting compounds called strigolactones.
Recently, several studies have determined that the rootand shoot-induced responses in different plant species show
that below-ground root-induced responses to different
pathogenic microbes alter several direct (production of
toxins) or indirect (volatiles) defence responses in the plant
above-ground that can affect the above-ground multitrophic interactions (Bezemer & Van Dam 2005). Positive
and negative feedback mechanisms operate between plant
and soil biota through root secreting compounds, which
strongly influence rates of nutrient cycling and vegetation
change.
CONCLUSIONS AND FUTURE DIRECTIONS
The secretion of phytochemicals and proteins from roots is
an important way for plants to respond to and alter their
environment. Over the last several years, research and technical advances have provided a better understanding of
how root exudates mediate communication between plants
and other organisms. These advances could be applied to
agricultural systems to enhance production by increasing
defence responses against soil-borne pathogens and/or
favouring association with beneficial soil microbes. In addition, this knowledge could be applied to develop better
methods of reclaiming land infested with invasive weeds,
heavy metals or toxic compounds. Exciting trends are
emerging from different but interconnected strands of
research in the field of rhizosphere biology. However,
efforts should now focus on decoding the chemical dialogues between organisms in the multifarious rhizosphere.
In addition, there is a need to understand the mechanism
and regulation of root exudation to better utilize phytochemical production for enhanced agricultural benefit. A
major challenge for researchers is to characterize new
transport systems and regulatory mechanisms involved in
the root secretion process. This will lead to a greater understanding of root-secreted phytochemicals and their role in
the rhizosphere. Another major challenge is absolute characterization of the chemical components of root exudates
involved in favouring disease resistance and facilitating
more beneficial associations with microbes in the rhizosphere. Enormous knowledge of the secondary metabolites
of root exudates is currently available, but it is important to
tease out the role of proteins secreted as root exudates to
© 2009 Blackwell Publishing Ltd, Plant, Cell and Environment, 32, 666–681
676 D. V. Badri & J. M. Vivanco
complete the scenario. Finally, there is a need for a deeper
understanding of the role of root secreting compounds in
determining the link between below-ground and aboveground interactions and vice versa, and also the abiotic
factors that interact with biotic interactions to drive ecosystem properties. This is a major challenge that can be
addressed most effectively by interdisciplinary teams of scientists: plant ecologists working with soil chemists, soil
physicists, chemists and plant pathologists. In addition, it is
very clear that research on root behaviour is needed to
provide ecological and evolutionary data to understand
multitrophic interactions and the link between belowground and above-ground diversity for the benefit of balanced ecosystem.
ACKNOWLEDGMENTS
The work in JMV laboratory was supported by the National
Science Foundation (MCB-0542642) and US Department
of Defense SERDP (SI 1388). We acknowledge the journal
Plant, Cell & Environment for inviting us to write this
article. Lastly, we apologize to those authors whose work
could not be discussed because of the space limitation.
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Received 20 August 2008; received in revised form 3 December 2008;
accepted for publication 4 December 2008
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