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The Pharma Innovation Journal 2019; 8(6): 449-459
ISSN (E): 2277- 7695
ISSN (P): 2349-8242
NAAS Rating: 5.03
TPI 2019; 8(6): 449-459
© 2019 TPI
www.thepharmajournal.com
Received: 15-04-2019
Accepted: 17-05-2019
SS More
Department of Soil Science and
Agriculture Chemistry,
DBSKKV, Dapoli, Maharashtra,
India
SE Shinde
Department of Soil Science and
Agriculture Chemistry,
DBSKKV, Dapoli, Maharashtra,
India
MC Kasture
Department of Soil Science and
Agriculture Chemistry,
DBSKKV, Dapoli, Maharashtra,
India
Correspondence
SS More
Department of Soil Science and
Agriculture Chemistry,
DBSKKV, Dapoli, Maharashtra,
India
Root exudates a key factor for soil and plant: An
overview
SS More, SE Shinde and MC Kasture
Abstract
Root exudate is one of the ways for plant communication to the neighboring plant and adjoining of
microorganisms present in the rhizosphere of the root. The chemicals ingredients of the root exudates are
specific to a particular plant species and also depend on the nearby biotic and abiotic environment. The
chemical ingredient exuded by plant roots include amino acids, sugars, organic acids, vitamins,
nucleotides, various other secondary metabolites and many other high molecular weight substances as
primarily mucilage and some unidentified substances. Through the exudation of a wide variety of
compounds, roots may regulate the soil microbial community in their immediate vicinity, cope with
herbivores, encourage beneficial symbioses, change the chemical and physical properties of the soil and
inhibit the growth of competing plant species. Root exudates mediate various positive and negative
interactions like plant-plant and plant-microbe interactions. The present review has been undertaken to
examine the possible role of root exudates on nourishing the neighboring microorganisms present in the
rhizosphere of the root. Plants secrete both high-and low-molecular weight compounds from their roots,
and these root exudates function not only as nutrients for soil microbes but as signal molecules in plant–
microbe interactions. All plants establish symbiotic interactions with rhizobia and arbuscular mycorrhizal
fungi to obtain several nutrients such as nitrogen and phosphate. In these interactions, flavonoids and
strigolactones in root exudates serve as signal molecules to establish the symbiotic interactions. Root
exudates from some plants also function to acidify surrounding soils to acquire phosphate. Here, we
provide an overview of the functions of root exudates with emphasis on the interaction between plants
and soil microbes and also on the acquisition of nutrients from surrounding soil.
Keywords: Root exudates, rhizosphere, phytosiderophores, organic acids etc.
Introduction
Unseen part of the plant secretes chemical compounds which acts as communication signal
between the adjacent plant and microbial community present in the rhizosphere of the root.
Root exudates correspond to an important source of nutrients for microorganisms in the
rhizosphere and seem to participate in early colonization inducing chemotactic responses of
rhizospheric bacteria (Bacilio et al., 2002) [1]. Rhizosphere is defined as a zone of most intense
bacterial activity around the roots of plant (Shukla et al, 2011) [11]. However, for the sake of
practical investigation, the rhizosphere is most often defined as the soil adhering to plant roots
when they are rigorously shaken, throughout which the rhizosphere effect must be observed to
some extent (Kang and Mills, 2004) [25]. The compounds secreted by plant roots serve
important roles as chemical attractants and repellants in the rhizosphere, the narrow zone of
soil immediately surrounding the root system (Estabrook and Yoder, 1998; Bais et al., 2001)
[14, 2]. The chemicals secreted into the soil by roots are broadly referred to as root exudates.
Through the exudation of a wide variety of compounds, roots may regulate the soil microbial
community in their immediate vicinity, cope with herbivores, encourage beneficial symbioses,
change the chemical and physical properties of the soil, and inhibit the growth of competing
plant species (Nardi et al., 2000) [35]. The ability to secrete a vast array of compounds into the
rhizosphere is one of the most remarkable metabolic features of plant roots, with nearly 5% to
21% of all photosynthetically fixed carbon being transferred to the rhizosphere through root
exudates (Marschner, 1995) [31]. Although root exudation clearly represents a significant carbon
cost to the plant, the mechanisms and regulatory processes controlling root secretion are just
now beginning to be examined. Root exudates have traditionally been grouped into low- and
high-Mr compounds. However, a systematic study to determine the complexity and chemical
composition of root exudates from diverse plant species has not been undertaken. Low-Mr
compounds such as amino acids, organic acids, sugars, phenolics, and various other secondary
metabolites are believed to comprise the majority of root exudates, whereas high-Mr exudates
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primarily include mucilage (high-Mr polysaccharides) and
proteins. The rhizosphere is a densely populated area in which
the roots must compete with the invading root systems of
neighboring plant species for space, water, and mineral
nutrients, and with soil-borne microorganisms, including
bacteria, fungi, and insects feeding on an abundant source of
organic material (Ryan et al, 2001) [43]. Thus, root-root, root-
microbe, and root-insect communications are likely
continuous occurrences in this biologically active soil zone,
but due to the underground nature of roots, these intriguing
interactions have largely been overlooked. Root-root and root-
microbe communication can either be positive (symbiotic) to
the plant, such as the association of epiphytes, mycorrhizal
fungi, and nitrogen-fixing bacteria with roots; or negative to
the plant, including interactions with parasitic plants,
pathogenic bacteria, fungi, and insects. Thus, if plant roots are
in constant communication with symbiotic and pathogenic
organisms, how do roots effectively carry out this
communication process within the rhizosphere?
A large body of knowledge suggests that root exudates may
act as messengers that communicate and initiate biological
and physical interactions between roots and soil organisms.
This update will focus on recent advancements in root
exudation and rhizosphere biology.
The Rhizodeposits in soil
Plant species are likely to vary in the radial extent of their
rhizosphere, determined by the amount and composition of
their soluble rhizodeposits, which may exhibit relative
differences in mobility in soil (Jones et al., 2004) [23].
Generally, the mineralization of rhizodeposits is thought to be
rapid (Nguyen et al., 1999; Kuzyakov & Cheng, 2001) [36, 23].
For example, mucilages are reported to have a half-life of
approximately 3 days (Jones et al., 2009) [24], and Ryan et al.
(2001) [43] reported that most amino acids, sugars, and organic
acids are mineralized with a half-life of 30–120 min when
added to the rhizosphere at ecologically realistic
concentrations. However, these latter estimates were arrived
at by adding the compounds to a root mat (a dense population
of roots formed at the base of a container in which a plant is
grown as a consequence of spatial constraint). While it is
possible to find root mats in nature (e.g. between rock cracks),
their form is not representative of most root systems. Exudate
turnover rates based on root mats may be considered
‘averages’ for the entire rhizosphere because bacterial density
is generally greater at basal when compared with apical root
regions of plants grown in soil; therefore, root exudate
turnover rates are likely to be greater at the base when
compared with the apices.
Root rhizosphere communication
Survival of any plant species in a particular rhizosphere
environment depends primarily on the ability of the plant to
perceive changes in the local environment that require an
adaptive response. Local changes within the rhizosphere can
include the growth and development of neighboring plant
species and microorganisms. Upon encountering a challenge,
roots typically respond by secreting certain small molecules
and proteins (Stintzi and Browse, 2000; Stotz et al., 2000) [46,
47]. Root secretions may play symbiotic or defensive roles as a
plant ultimately engages in positive or negative
communication, depending on the other elements of its
rhizosphere. In contrast to the extensive progress in studying
plant-plant, plant-microbe, and plant-insect interactions that
occur in aboveground plant organs such as leaves and stems,
very little research has focused on root-root, root-microbe, and
root-insect interactions in the rhizosphere. The following
sections will examine the communication process between
plant roots and other organisms in the rhizosphere.
Root-Root Communication
In natural settings, roots are in continual communication with
surrounding root systems of neighboring plant species and
quickly recognize and prevent the presence of invading roots
through chemical messengers. Allelopathy is mediated by the
release of certain secondary metabolites by plant roots and
plays an important role in the establishment and maintenance
of terrestrial plant communities. It also has important
implications for agriculture; the effects may be beneficial, as
in the case of natural weed control, or detrimental, when
allelochemicals produced by weeds affect the growth of crop
plants (Callaway and Aschehoug, 2000) [12]. A secondary
metabolite secreted by the roots of knapweed (Centaurea
maculosa) provides a classic example of root exudates
exhibiting negative root-root communication in the
rhizosphere. Interestingly, ( )-catechin was shown to account
for the allelochemical activity, whereas (+)-catechin was
inhibitory to soil-borne bacteria (Bais et al., 2002c) [4]. In
addition to racemic catechin being detected in the exudates of
in vitro-grown plants, the compound was also detected in soil
extracts from knapweed-invaded fields, which strongly
supported the idea that knapweed's invasive behavior is due to
the exudation of ( )-catechin. Moreover, this study
established the biological significance of the exudation of a
racemic compound such as catechin, demonstrating that one
enantiomer can be responsible for the invasive nature of the
plant, whereas the other enantiomer can contribute to plant
defense. Although studies have reported the biosynthesis of
the common enantiomer (+)-catechin, little is known
regarding the synthesis of ( )-catechin or (±)-catechin as
natural products. One possibility is that (+)-catechin
production is followed by racemization in the root or during
the exudation process. Alternatively, there could be a
deviation from the normally observed stereo- and enantio
specific biosynthesis steps. The flavonols kaempferol and
quercetin are generally perceived as final products, rather than
intermediates, in the pathway (Winkel-Shirley, 2001) [53]. The
correlation of these experiments to the root exudation process
has yet to be determined, but the data should provide a
starting point for further studies on the characterization of
specific committed steps in the synthesis of racemic catechin
in knapweed roots. The above example demonstrates how
plants use root-secreted secondary metabolites to regulate the
rhizosphere to the detriment of neighboring plants. However,
parasitic plants often use secondary metabolites secreted from
roots as chemical messengers to initiate the development of
invasive organs (haustoria) required for heterotrophic growth
(Keyes et al., 2000) [27]. Some of the most devastating
parasitic plants of important food crops such as maize (Zea
mays), sorghum (Sorghum bicolor), millet (Panicum
milaceum), rice (Oryza sativa), and legumes belong to the
Scrophulariaceae, which typically invade the roots of
surrounding plants to deprive them of water, minerals, and
essential nutrients (Yoder, 2001) [55]. It has been reported that
certain allelochemicals such as flavonoids, p-hydroxy acids,
quinones, and cytokinins secreted by host roots induce
haustorium formation (Estabrook and Yoder, 1998 ; Yoder,
2001) [14, 55], but the exact structural requirements of the
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secreted compounds for haustorium induction is not fully
understood.
Root-Microbe Communication
Root-microbe communication is another important process
that characterizes the underground zone. Some compounds
identified in root exudates that have been shown to play an
important role in root-microbe interactions include flavonoids
present in the root exudates of legumes that activate
Rhizobium meliloti genes responsible for the nodulation
process (Peters et al., 1986) [39]. Although the studies are not
yet conclusive, these compounds may also be responsible for
vesicular-arbuscular mycorrhiza colonization (Becard et al.,
1992, 1995; Trieu et al., 1997) [6, 7, 49]. In contrast, survival of
the delicate and physically unprotected root cells under
continual attack by pathogenic microorganisms depends on a
continuous "underground chemical warfare" mediated by
secretion of phytoalexins, defense proteins, and other as yet
unknown chemicals (Flores et al., 1999) [11, 16]. The
unexplored chemodiversity of root exudates is an obvious
place to search for novel biologically active compounds,
including antimicrobials. For instance, Bais et al. (2002b) [4]
recently identified rosmarinic acid (RA) in the root exudates
of hairy root cultures of sweet basil (Ocimum basilicum)
elicited by fungal cell wall extracts from Phytophthora
cinnamoni. Basil roots were also induced to exude RA by
fungal in situ challenge with Pythium ultimum, and RA
demonstrated potent antimicrobial activity against an array of
soil-borne microorganisms including Pseudomonas
aeruginosa (Bais et al., 2002b) [4]. Similar studies by Brigham
et al. (1999) with Lithospermum erythrorhizon hairy roots
reported cell-specific production of pigmented
naphthoquinones upon elicitation, and other biological activity
against soil-borne bacteria and fungi. Given the observed
antimicrobial activity of RA and naphthoquinones, these
findings strongly suggest the importance of root exudates in
defending the rhizosphere against pathogenic
microorganisms. Moreover, the aforementioned studies
complement earlier research that mainly focused on the
regulation and production of these compounds by providing
valuable insights into the biological importance of RA and
shikonin.
Root-Insect Communication
The study of plant-insect interactions mediated by chemical
signals has largely been confined to leaves and stems,
whereas the study of root-insect communication has remained
largely unexplored due to the complexity of the rhizosphere
and a lack of suitable experimental systems. However, root
herbivory by pests such as aphids can cause significant
decreases in yield and quality of important crops including
sugar beet (Beta vulgaris), potato (Solanum tuberosum), and
legumes (Hutchison and Campbell, 1994). One attempt to
study root-insect communication was developed by Wu et al.
(1999) using an in vitro coculture system with hairy roots and
aphids. In this study, it was observed that aphid herbivory
reduced vegetative growth and increased the production of
polyacetylenes, which have been reported to be part of the
phytoalexin response (Flores et al., 1988) [15]. In a more recent
study, Bais et al. (2002a) [3] reported the characterization of
fluorescent -carboline alkaloids from the root exudates of
O. tuberosa (oca). The main fluorescent compounds were
identified as harmine (7-methoxy-1-methyl- -carboline) and
harmaline (3, 4-dihydroharmine; Bais et al., 2002a [3]; Fig. 1,
B-E). In addition to their fluorescent nature, these alkaloids
exhibit strong phototoxicity against a polyphagous feeder,
Trichoplusia ni, suggesting their insecticidal activity may be
linked to photoactivation (Larson et al., 1988). The Andean
highlands, where O. tuberosa is primarily cultivated, are
subjected to a high incidence of UV radiation, and it was
observed that the strongest fluorescence intensity occurred
with oca varieties that showed resistance to the larvae of
Mycrotrypes spp., the Andean tuber weevil (Flores et al.,
1999) [11, 16]. These data suggest that UV light penetrating soil
layers could photoactivate fluorescent -carboline alkaloids
secreted by oca roots to create an insecticidal defense
response.
Exudation Alters the Soil Characteristics
A large range of organic and inorganic substances are
secreted by roots into the soil, which inevitably leads to
changes in its biochemical and physical properties (Rougier,
1981) [13]. Various functions have been attributed to root cap
exudation including the maintenance of root-soil contact,
lubrication of the root tip, protection of roots from
desiccation, stabilization of soil micro-aggregates, and
selective adsorption and storage of ions (Griffin et al., 1976;
Rougier, 1981; Bengough and McKenzie, 1997; Hawes et al.,
2000) [13, 8]. Root mucilage is a reasonably studied root
exudate that is believed to alter the surrounding soil as it is
secreted from continuously growing root cap cells (Vermeer
and McCully, 1982; McCully, 1995; Sims et al., 2000) [34, 45].
Soil at field capacity typically possesses a matric potential of
5 to 10 kPa (Chaboud and Rougier, 1984) [42]. It has been
speculated that as the soil dries and its hydraulic potential
decreases, exudates will subsequently begin to lose water to
soil. When this occurs, the surface tension of the exudates
decreases and its viscosity increases. As the surface tension
decreases, the ability of the exudates to wet the surrounding
soil particles will become greater. In addition, as viscosity
increases, the resistance to movement of soil particles in
contact with exudates will increase, and a degree of
stabilization within the rhizosphere will be achieved. For
instance, McCully and Boyer (1997) [34] reported that
mucilage from the aerial nodal roots of maize has a water
potential of 11 Mpa, indicating a large capacity for water
storage when fully hydrated, whereas the mucilage loses water
to the soil as it begins to dry.
This speculation supports the idea that root exudates could
play a major role in the maintenance of root-soil contact,
which is especially important to the plant under drought and
drying conditions, when hydraulic continuity will be lost. The
largest, most coherent soil rhizosheaths are formed on the
roots of grasses in dry soil (Watt et al., 1994). However,
sheath formation requires fully hydrated exudates to permeate
the surrounding soil particles that are then bonded to the root
and each other as the mucilage dries. Young (1995) found that
rhizosheath soil was significantly wetter than bulk soil and
suggested that exudates within the rhizosheath increase the
water-holding capacity of the soil. Furthermore, it has recently
been proposed that in dry soil, the source of water to hydrate
and expand exudates is the root itself. Modern cryo-scanning
microscopy has helped researchers determine that the
rhizosheath of a plant is more hydrated in the early morning
hours compared with the midday samplings (McCully and
Boyer, 1997) [34]. This implies that the exudates released from
the roots at night allow the expansion of the roots into the
surrounding soil. When transpiration resumes, the exudates
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begin to dry and adhere to the adjacent soil particles. Thus, the
rhizosheath is a dynamic region, with cyclic fluctuations in
hydration content controlled to some extent by roots.
Factors affecting root exudates
Microbial activity
Organic compounds in root exudates are continuously
metabolized by root-associated microorganisms at the
rhizoplane and in the rhizosphere. Microbial activity results in
quantitative and qualitative alterations of the root exudate
composition due to degradation of exudate compounds and
the release of microbial metabolites.
Sorption at the soil matrix
Root exudate compounds in soils are differentially affected by
adsorption processes, depending on their charge
characteristics and on ion-exchange properties of the soil
matrix. The lack of charges prevents interactions of sugars
with metal ions both in soil solution and at the soil matrix.
However, adsorption of more hydrophobic organic exudate
compounds such as flavonoids and simple phenolics may be
mediated by hydrophobic interactions with humic
compounds, and also abiotic oxidation of phenolics and
organic acids at Fe and Mn surfaces has been reported. The
adsorption of charged compounds such as carboxylic acids,
though largely dependent on the soil type and pH, generally
tends to increase with the number of negative charges
available for anionic interactions with metal surfaces at the
soil matrix, resulting in rapid removal of certain carboxylate
species from the rhizosphere soil solution. Since metal
complexation and ligand-exchange are mechanisms involved
in mobilization of mineral nutrients (P, Fe) and exclusion of
toxic elements (Al), the most effective organic chelators (e.g.
citrate, oxalate, malate) for these elements frequently exhibit
the most intense soil adsorption. In contrast, sorption of
proteinaceous amino acids and the related mobilization of
mineral nutrients in soils seems to be comparably low, due to
slow reaction kinetics with metal ions. However, the so called
phytosiderophores as nonproteinaceous, tricarboxylic amino
acids behave differently and exhibit a fast reaction with
amorphous iron (ferrihydrite) in soils.
Retrieval mechanisms
Carbon flow in the rhizosphere is not a strictly uni-directional
process from root to soil. Active retrieval mechanisms for
sugars and amino acids have been identified in plant roots,
which were capable of recovering up to 90% of the exudates
passively lost into the rhizosphere. Even the preferential
uptake of organic nitrogen has been reported for plant species
adapted to ecosystems such as arctic tundras, where the rate
of nitrogen mineralization is generally low. These findings are
in good agreement with recent reports on the molecular
biological characterization of root specific transporters for
amino acids and small peptides in higher plants. Similarly,
induction of a re-uptake system for phytosiderophores as Fe
complexes has been reported in graminaceous plant species
under iron deficient conditions. In contrast, no such retrieval
mechanisms could be identified for carboxylic acids. The
ecological significance of retrieval mechanisms for plants
may be related to improved nitrogen and Fe acquisition and to
limitation of carbon losses. Especially for long term studies
on root exudation in closed systems (e.g sterile culture
systems), the impact of selective re-absorption of exudate
compounds has to be taken into account.
Root injury
Various techniques for collection of root exudates are
associated with the risk of root injury by rupture of root hairs
and epidermal cells or rapid change of the environmental
conditions (e.g temperature, pH, oxygen availability) during
transfer of root systems into trap solutions, application of
absorbtion materials onto the root surface, and preparation of
root systems for exudate collection. The possible impact of
those stress treatments may be assessed by measuring
parameters of plant growth in plants either subjected or not
subjected to the collection procedure, and by comparing
exudation patterns after exposure of roots to the handling
procedures with different intensity.
Mechanisms of Root Exudation
Diffusion
Release of the major low molecular weight (LMW) organic
constituents of root exudates such as sugars, amino acids,
carboxylic acids and phenolics is a passive process along the
steep concentration gradient, which usually exists between the
cytoplasm of intact root cells (millimolar range) and the
external (soil) solution (micromolar range). Direct diffusion
through the lipid bilayer of the plasmalemma is determined by
membrane permeability, which depends on the physiological
state of the root cell and on the polarity of the exudate
compounds, facilitating the permeation of lipophilic exudates.
At the cytosolic pH of approximately 7.1-7.4, more polar
intracellular LMW organic compounds such as amino acids
and carboxylic acids usually exist as anions with low plasma
lemma permeability. A positive charge gradient, which is
directed to the outer cell surface as a consequence of a large
cytosolic K+ diffusion potential and of plasma lemma ATPase
mediated proton extrusion, not only promotes uptake of
cations from the external solution, but also the outward
diffusion of carboxylate anions.
Ion-Channels
Root exudation of extraordinary high amounts of specific
carboxylates (e.g. citrate, malate, oxalate, and
phytosiderophores) in response to nutritional deficiency stress
or Al toxicity in some plant species cannot simply be
attributed to diffusion processes. The controlled release of
these compounds, involved in mobilization of mineral
nutrients and in detoxification of Al, may be mediated by
more specific mechanisms. Inhibitory effects by exogenous
application of various anion channel antagonists indicate the
involvement of anion channels with a concomitant release of
protons or K+, probably mediated by plasma lemma ATPase
or K+ channels respectively.
Vesicle transport
Vesicle transport is involved in root secretion of high
molecular weight compounds. The release of mucilage
polysaccharides from hypersecretory cells of the root cap is
mediated by Golgi vesicles. Subsequently the secretory cells
degenerate and are sloughed off. Secretory proteins such as
ecto-enzymes (e.g. acid phosphatase, phytase, peroxidase,
phenoloxidase) are synthesized by membrane-bound
polysomes and cotranslationally enter the endomembrane
system by vectorial segregation into the ER-lumen. While
passing through the Golgi apparatus they are separated from
proteins destinated for the vacuolar compartment, and are
transported to the plasmalemma by transfer vesicles.
Processes involved in exocytosis such as formation of vesicles
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and their fusion with the plasma membrane strongly depend
on extracellular and intracellular calcium levels.
Vesicles have also been implicated in storage and release of
low molecular weight compounds such as phenolics and
phytosiderophores in plant roots but the characterization of
mechanisms remains to be established.
Nutritional Factors
Phosphorus (P)
Root-induced P mobilization in soils
Phosphorus is one of the major limiting factors for plant
growth in many soils. Plant availability of inorganic
phosphorus (Pi) can be limited by formation of sparingly
soluble Ca phosphates, particularly in alkaline and calcareous
soils, by adsorption to Fe- and Al-oxide surfaces in acid soils
and by formation of Fe/Al-P complexes with humic acids.
Phosphorus deficiency can significantly alter the composition
of root exudates in a way, which is at least in some plant
species related to an increased ability for mobilization of
sparingly soluble P sources. Increased root exudation of
carboxylates (e.g. citrate, malate, oxalate, organic
compounds) is a P deficiency response, particularly in
dicotyledonous plant species. Mobilization of Pi by
exogenous application of carboxylates to various soils with
low P availability has been demonstrated in numerous studies
and seems to be mediated by mechanisms of ligand exchange,
dissolution, and occupation of P sorption sites (e.g. Fe/Al-P
and Ca-P) in the soil matrix. Citrate and oxalate were found to
be the most efficient carboxylates with respect to P
mobilization in many of these model experiments, according
to high stability constants for complex formation with Fe, Al
and Ca.
Physiology of carboxylate exudation
Only limited information is available on the physiological
basis of P deficiency-induced root exudation of carboxylates.
Increased carboxylate release is frequently observed in later
stages of P deficiency. Major exudate compounds are malate,
citrate, and also oxalate, especially in plant species where
oxalate replaces malate as the major internal carboxylate
anion. The plant species with intense P deficiency-induced
carboxylate exudation, such as oil-seed rape, chickpea and
white lupin accumulated organic acids mainly in the root
tissue and, moreover, in the root zones where exudation was
most intense (e.g. subapical root zones, proteoid roots). In
contrast, root exudation of carboxylates even decreased in
response to P deficiency in plant species such as Sysimbrium
officinale, wheat, and tomato and was associated with
predominant carboxylate accumulation in the shoots. The
accumulation of organic acids in the root tissue is a
prerequisite for enhanced root exudation of carboxylates
under P-deficient conditions and may be determined by
shoot/root partitioning of carboxylates or of carbohydrates as
related precursors.
Exudation of phenolic compounds
In many plants, P deficiency also enhances production and
root exudation of phenolic compounds. Increased biosynthesis
of phenolics under P deficient conditions was suggested as
another metabolic bypass reaction involved in liberation and
recycling of Pi in P-starved cells. Antibiotic properties of
certain phenolic compounds (e.g. isoflavonoids) in root
exudates may not only counteract infection by root pathogens,
but also prevent the microbial degradation of exudate
compounds involved in P mobilization. Certain root
flavonoids have been identified as signal molecules for spore
germination and hyphal growth of arbuscular mycorrhiza, and
flavonoids are likely to be important also as signaling
compounds for the establishment of ectomycorrhiza.
Phenolics may further contribute to P mobilization by
reduction of sparingly soluble FeIII phosphates. The specific
release of piscidic acid (p-hydroxyphenyl tartaric acid) from
roots of P-deficient pigeon pea (Cajanus cajan L.), which is a
strong chelator for FeIII, has been related to enhanced
mobilization of Fe phosphates in Alfisols. However,
considering comparatively low exudation rates, piscidic acid
may be more relevant as a signalling compound for the
establishment of microbial associations (e.g. AM, rhizobia).
Root-secretory phosphohydrolsases
Enhanced secretion of acid phosphatases and phytases by
plant roots and also by rhizosphere microorganisms under P-
deficient conditions may contribute to Pi acquisition by
hydrolysis of organic P esters in the rhizosphere, which can
comprise up to 30-80% of the total soil phosphorus. In many
soils, however, the availability of organic phosphorus seems
to be limited mainly by the low solubility of certain P forms
such as Ca and Fe/Al-phytates, which can make up a major
propotion of the soil-organic P. The oxalic acid in root
exudates can contribute to some extent to phytate
mobilization in soils. Similarly, in a P-deficient sandy soil,
more Pi was liberated by simultaneous application of acid
phosphatase and organic acids identified in rhizosphere soil
solutuion of Hakea undulata, than by separate application of
organic acids or acid phosphatase, respectively. Another
limiting factor for phosphatase-mediated P mobilization, is
the low mobility of the hydrolytic enzymes (APase, phytase),
mainly associated with the root cell wall and with mucilage in
apical root zones. An alternative function of root secretory
acid phosphatases may be the rapid retrieval of phosphorus by
hydrolysis of organic P, which is permanently lost by
diffusion or from sloughed off and damaged root cells.
Nitrogen and Potassium
Nitrate assimilation
At least in some plant species such as maize, Lupinus
angustifolius L. and tomato, root exudation of di- and
tricarboxylic acids (mainly malate and citrate) seems to be
affected by the form of nitrogen supplied as nitrate or
ammonium. Generally, exudation of the carboxylates
increased with increasing levels of nitrate in the culture
medium. This may be related to the function of carboxylates
in intracellular pH stabilization. Nitrate reduction in roots and
in the shoot is stimulated with increasing nitrate supply, and
results in the production of an equivalent amount of OH-,
which is neutralized by increased biosynthesis of organic
acids or released into the rhizosphere when produced in the
root tissue. The carboxylate anions can be stored in the leaf
vacuoles but are also retranslocated to the roots via phloem
transport when the leaf storage capacity is limited. In the root
tissue, the carboxylate anions are either metabolized by
decarboxylation or can be released into the rhizosphere.
Ammonium assimilation
Excess uptake of cations over anions as a consequence of
increased ammonium supply is balanced by extrusion of
protons and by synthesis of carboxylic acids for pH
stabilization in the root tissue. The remaining carboxylate
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anions are required as acceptors for ammonium assimilation
in the roots, which is associated also with the production of
protons and decarboxylation of organic acids. As a
consequence, tissue concentrations and root exudation of
carboxylates are declining with increased ammonium supply.
High nitrogen concentrations inhibit the production and
release of isoflavonoids from lupin roots. Compared with
nitrate supply, exudation was strongly enhanced by
ammonium application. Similarly, the well-known inhibitory
effect of nitrogen on nodulation during establishment of the
legume-rhizobium symbiosis is mainly caused by nitrate. In
short-term, intense rhizosphere acidification induced by NH4+
nutrition or low rates of NO3- supply may directly stimulate
the release of phenolics and other low molecular weight root
exudate compounds as a consequence of an increased
electrochemical transmembrane potential gradient but also
due to acid-induced impairment of membrane integrity. Since
flavonoids have important functions as chemoattractants, and
nod-gene inducers for rhizobia, nitrogen effects on nodulation
may be explained by differential exudation of these
compounds depending on N form supply and the N nutritional
status of the plants. Root flavonoids are involved also in
pathogen and allelopathic interactions, and these processes
might be similarly affected by nutritional modifications in
root exudation.
Potassium nutrition
Only limited information is available on effects of potassium
(K) supply on root exudation. Increased exudation of sugars,
organic acids and amino acids has been detected in maize as a
response to K limitation. This may be related to a K
deficiency-induced preferential accumulation of low
molecular weight N and C compounds at the expense of
macromolecules.
Iron
Although iron (Fe) is one of the major soil constituents (0.5 -
5%) where it is usually present in the oxidized state (Fe3+),
plant availability is severely limited by the low solubility of
Fe- (hydroxides at pH levels favourable for plant growth.
Therefore, plants need special mechanisms for aquiring Fe
from sparingly soluble Fe forms to fit the requirements for
growth, especially in neutral and alkaline soils, where the
availability of Fe is particularly low.
Other micronutrients and heavy metals
Mobilization of micronutrients such as Zn, Mn, Cu, Co and of
heavy metals (Cd, Ni) in soil extraction experiments with root
exudates isolated from various axenically grown plants is well
documented and has been related to the presence of
complexing agents.
Role of Phytosiderophores
Formation of stable chelates with phytosiderophores occurs
with Fe, but also with Zn, Cu, Co and Mn, and can mediate
the extraction of considerable amounts of Zn, Mn, Cu and
even Cd in calcareous soils. There is increasing evidence that
PS release in graminaceous plants is also stimulated in
response to Zn deficiency but possibly also under Mn and Cu
deficiency. Similar to Fe deficiency, the tolerance of different
graminaceous plant species to Zn deficiency was found to be
related to the amount of released PS but correlation within
cultivars of the same species seems to be low.
Role of carboxylates
Mobilization of micronutrients (Mn, Zn, Cu), heavy metals
(Cd), and even uranium in the rhizosophere has been also
related to rhizosphere acidification and to complexation with
organic acids (e.g. citrate) in root exudates. This view is
further supported by intense mobilization of Mn, Zn, Cu, and
Cd observed in soil extraction experiments with leachates
from rhizosphere soil or with organic acid mixtures according
to the root exudate composition of plant species such as
Lupinus albus, Hakea undulata and Spinacia oleracea under
P-deficient conditions, where exudation of carboxylates and
protons is particularly expressed. However, only limited
information exists about the plant availability and uptake of
the metal-carboxylate complexes. Phenolics and organic acids
in root exudates (especially malate) are involved in both
complexation and reduction of Mn. In cluster-rooted plant
species such as Lupinus albus and members of the
Proteaceae, particulary intense exudation of organic acids and
phenolics in response to P deficiency is frequently associated
also with enhanced Mn mobilization in the rhizosphere and
accumulation of high or even toxic Mn levels in the shoot
tissue. Similarly, Mn toxicity was indirectly induced by the
iron deficiency response in flax grown in a calcareous soil
high in extractable Mn but low in Fe. Besides mobilizing
effects of plant root exudates, Mn availability in the
rhizosphere is also strongly affected by the activity of
microorganisms involved in Mn oxidation and Mn reduction,
which in turn depend on root exudates as a carbon source.
Utilization of Cu complexes with humic acids and citrate has
been reported for red clover especially under P-deficient
conditions. Roots of young seedlings of barnyard grass,
maize, rye and wheat secret hydroxamic acids, their
complexes with Fe/III/-ions are available sources of iron. It is
possible that the cyclic hydroxamic acids play a role in the
alternative mechanism of iron uptake. The hydroxamic acids
secreted by barnayard grass roots have an allelopathic role by
inhibiting the roots growth of rice. The cyclic hydroxamic
acid, 2,4-dihydroxy-1,4-benzoxazin-3-one (DIBOA) and its
methoxy analogue, 2-4-dihydroxy-7methoxy-1,4-benzoxazin-
one (DIMBOA), occur as glycosides in the Poaceae, including
maize, wheat and rye, and are implicated in the resistance of
plants to pathogens and insects (Niemeyer 1988) [37]. In
addition to their toxic properties, the cyclic hydroxamic acids
have also been associated with detoxification of triazine
herbicides, inhibition of plant growth regulators (Hasegawa et
al. 1992) [18] and may even have allelopathic properties (Perez
and Ormeno-Nunez 1991) [38].
The grasses possess a special iron uptake mechanism. They
exudate mugineic type compounds (phytosiderophores)
through their roots into the rhizosphere, where they form
complexes with the iron. The grasses take up these mobilized
chelates. There are great differences in phytosiderophore
activity between the plants. So maize and sorghum exude very
little amount of phytosiderophore. The cyclic hydroxamic
acids also form complexes with the Fe (III)-ions, and already
(Klun et al. 1970) [28] supposed them to play a role in the iron
uptake. The tissues of barnyard grass (Echinochloa crus-galli
(L.) P.B.)synthesize cyclic hydroxamic acids, which are
secreted by its roots in free or glycosidic forms. Hydroxamic
acids inhibit rice root growth. The concentration of
hydroxamic acids accumulating in the rhizosphere exceeds
the level that is necessary for a 50% root growth retardation
of rice. Based on this, we assume that cyclic hydroxamic
acids secreted by barnyard grass roots have an allelopathic
role by inhibiting the growth of rice (Petho 1993) [40].
Role of phytosiderophores in zinc efficiency of wheat
In Zn-deficient nutrient solution, durum wheat showed a more
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rapid development of visible Zn-deficiency symptoms than
bread wheat types. Bread wheat types were Zn-efficient and
produced more biomass and durum wheat types under Zn-
deficiency. Under Zn-deficiency, Zn-inefficient durum wheat
lines HI-8498 and PDW-233 released significantly lower
amounts of phytosiderophores than the Zn-efficient bread
wheat PBW-343 and HD-2329. The phytosiderophore release
in bread and durum wheat types was related to efficiency of
Zn uptake across genotypes. The phytosiderophore release in
durum types under Zn deficiency was limited by
phytosiderophore availability in the roots rather than by
release of phytosiderophores. The mixed culture experiment
showed that rhizospheric availability of phytosiderophores is
a factor limiting the acquisition of Zn by Zn-inefficient wheat.
When grown in mixed culture with bread types, Zn-inefficient
durum grew better and acquired more Zn compared to growth
in monoculture. Furthermore, durum types showed a low
transcript level of NAA T which correlated well with the
production and release of phytosiderophores in Zn-deficient
plants (Singh and Kumar 2002) [2].
Role on the Nodulation of Root Nodule Bacteria
The growth of Bradyrhizobium japonicum as well as
Rhizobium leguminosarum bv. Phaseoli growing in minimal
medium was repressed by the addition of hydroxylysine
(Hyl), although the sensitivity of the former to Hyl, seemed to
be lower than that of the latter (Keiko et al. 1999) [26]. The
nodulation efficiency of both Glycine max (L.) inoculated
with B. japonicum cells and Phaseolus vulgaris (L.)
inoculated with R. leguminosarum bv. phaseoli cells was
reduced in the presence of Hyl, concomitantly with the
decrease in the elongation of roots. Besides, the Hyl contents
in the seed (seedling) exudates tended to increase when the
host plants were inoculated with an unfavorable strain for
their nodulation. These results suggest that the Hyl plays a
role in the effective symbiotic relationship by regulating the
growth of the root nodule bacteria on the root surface and / or
the elongation of the host plant's roots.
Donor-receiver bioassay was designed to eliminate the effects
of the competitive interference for resources from allelopathic
effects (Hisashi et al 2007) [21]. Seeds of cress (Lepidium
sativum), lettuce (Lactuca sativa), timothy (Phleum pratense)
or ryegrass (Lolium multiflorum) were incubated with 4-
dayold buckwheat (Fagopyrum esculentum) seedlings for 3
days in Petri dishes under controlled laboratory condition.
The growth of cress, lettuce, timothy and ryegrass seedlings
was inhibited by the presence of buckwheat seedlings, and
increasing the number of buckwheat seedlings increased the
growth inhibition. One inhibiting substance was found in the
culture solution in which buckwheat seedlings were
hydroponically grown for 10 days. These results suggest that
buckwheat seedlings may inhibit the neighboring plant
growth due to exudation of allelopathic substance into the
neighboring environment. Thus, the inhibitory effect of buck
heat was probably caused by allelopathic chemical reactions.
Rhizodeposition under combined soil physical stresses
We investigated the effects of combined soil physical stresses
of compaction and drought on the production of fully
hydrated mucilage (mucilage) and root border cells (RBCs) in
maize Somasundaram et al. 2009. [48] The exudation of carbon
and water were also estimated using stable isotopes of
13Cand deuterated water (D20) under same soil Conditions.
As plant age progressed during seedling stage, mucilage
production increased, however, RBCs release did not. Soil
compaction increased the release of D2O, RBCs, and
production of mucilage which implies the function of roots to
reduce mechanical impedance during root penetration. Drying
stress increased only carbon release, but reduced the others.
This indicates that RBCs adhere more strongly to the root cap
due to drying of mucilage, and water release may be reduced
to save the water loss. The highest rhizodeposition of
mucilage, RBCs and D2O were occurred under wet compact
soil condition, however, that of carbon occurred under dry
compact soil condition. Roots of grasses in response to iron
deficiency markedly increase the release of chelating
substances ('phytosiderophores') which are highly effective in
solubilization of sparingly soluble inorganic FeIII compounds
by formation of FeIII phytosiderophores (Romheld and
Marschner 1986) [51]. In barley (Hordeam vulgare L.), the rate
of iron uptake from FeIII phytosiderophores is 100 to 1000
times faster than the rate from synthetic Fe chelates (eg. Fe
ethylene Diamine Tetraacetate) or microbial Fe siderophores
(e.g. ferrichrome). Reduction of FeII is not involved in the
preferential iron uptake from FeIII phytosiderophores by
barley. This is indicated by experiments with varied pH,
addition of bicarbonate or of a strong chelator for FeII (e.g.
bathophenanthroline disulfonate). The results indicate the
existence of a specific uptake system for FeIII
phytosiderophores in roots of barley and all other
graminaceous species. In contrast to grasses, cucumber plants
(Cucumis sativus L.) take up iron from FeIII
phytosiderophores at rates similar to those from synthetic Fe
chelates. Furthermore, under Fe deficiency in cucumber,
increased rates of uptake of FeIII phytosiderophores are based
on the same mechanism as for synthetic Fe chelates, namely
enhanced FeIII reduction and chelate splitting. Two strategies
are evident from the experiments for the acquisition of iron by
plants under iron deficiency.
Table 1: Root exudates detected in higher plants
Class of compounds
Single components
Sugars
Arabinose, glucose, fructose, galactose, maltose, raffinose, rhamnose, ribose, sucrose, xylose
Amino acids and amides
all 20 proteinogenic amino acids, aminobutyric acid, homoserine, cysrathionine, mugineic acid phytosiderophores
(mugineic acid, deoxymugineic acid, hydroxymugineic acid, epi-hydroxymugineic acid, avenic acid, distichonic acid
A)
Aliphatic acids
Formic, acetic, butyric, popionic, malic, citric, isocitric, oxalic, fumaric, malonic, succinic, maleic, tartaric,
oxaloacetic, pyruvic, oxoglutaric, maleic, glycolic, shikimic, cis-aconitic, trans-aconitic, valeric, gluconic
Aromatic acids
p-hydroxybenzoic, caffeic, p-coumaric, ferulic, gallic, gentisic, protocatechuic, salicylic, sinapic, syringic
Miscellaneous phenolics
Flavonols, flavones, flavanones, anthocyanins, isoflavonoids
Fatty acids
Linoleic, linolenic, oleic, palmitic, stearic
Sterols
Campestrol, cholesterol, sitosterol, stigmasterol
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Enzymes
Amylase, invertase, cellobiase, desoxyruibonuclease, ribonuclease, acid phosphatase, phytase, pyrophosphatase
apyrase, peroxidase, protease
Micellaneous
Vitamins, plant growth regulators (auxins, cytokinins, gibberellins), alkyl sulphides, ethanol, H+,K+ Nitrate,
Phosphate, HCO3-
Rioval and Hanson, in 1993 study on Evidence for a large and sustained glycolytic flux to lactate in anoxic roots of some members of the
halophytic genus Limonium
Momilactone B., 12.5 g, was detected in culture solution in
which three 80 day-old rice plants were grown
hydroponically. At this time, the stage of these rice plants was
panicle initiation, and length of their shoots and roots was
about 110 and 35 cm, respectively. Since the culture solutions
were renewed every two days during the experiment, one rice
plant considered releasing 2.1g of momilactone B into the
solution per day. Mimilactone B was detected in shoots and
roots of 80-day-old rice plants and the concentration of
mimilactone in the shoots was 3.5-fold greater than that in the
roots. Mimilactone B had already been found in rice leaves
and straw. However, it was first reported by Hisashi and
Takashi (2004) [20] that rots of rice seedlings contain
mimilactone B. The present result suggests that roots of
development rice plants also have mimilactone B.
Plants are usually stressed and competing with neighbouring
plants for resources such as light, nutrients and water in the
natural ecosystems. As one of the strategies for survival,
many plant species release allelochemical to inhibit the
germination and growth of their neighboring plants. Rice was
also found to produce and release growth inhibiting
allelochemical into their neighboring environments (Hisashi
and Takashi 2004) [20]. However, the chemical structures of
these allelochemicals are still unknown. Mimilactone B
inhibited the germination and growth of other plant species,
and the inhibitory activity was comparable to that of ABA.
The rice seedlings at an early developmental stage released
mom lactone B into their neighboring environment and the
level released was enough to inhibit the growth of their
neighboring plants. Momilactone B may act as an
allelochemical and play an important role in the competition
with neighboring plants. Using symbiotically N2-fixing
legumes as green manures is a way to supply N from the
atmosphere to cropping ecosystems. Usually whole plants of
the green manure are incorporated into soil; hence, the
belowground parts as well as the aboveground parts would
contribute to N transfer to succeeding crops. However, little is
known about the contribution of the belowground parts alone
(Bongsu et al., 2008) [10]. We assessed N transfer from below
ground parts compared to whole plants of two legumes,
Crotalaria spectabilis and Sesbania rostrata. Each of the
legumes was grown approximately for 3 months in a Ij2000a
Wagner pot filled with soil media, and then the roots alone
(R) or shoot and root (5 +R) were harvested and incorporated
in the pots. Tender green mustard (Brassica rapa) as the
succeeding crop was grown for 66 days in these pots without
additional fertilizer. Although the amount of N in green
manure in 5 +R pots was approximately 4-fold higher than
that in R pots, differences in N uptake by tender green
mustard between the 5+R and R pots were smaller (1.7-fold
for C. spectabilis and 2.3-fold for S. rostrata). This means
that N recovery rate by tender green mustard was significantly
higher in R than in 5+R pots with either green manures.
Differences in C/N ratio of the green manures could not likely
explain the higher N recovery rate in R pots. Bioassay of the
aqueous extracts from the green manure with lettuce seedlings
suggested that growth inhibitory effects might be responsible
for the lower recovery rate in 5+R treatment.
The influence of root exudates on colonization of arbuscular
mycorrhizal (AM) fungi was evaluated. Root exudates of
cucumber (Cucumis sativus) and carrot (Daucus carota) were
supplied to each of the seedlings grown in soil containing AM
fungi (Kubota et al 2004) [32]. AM colonizaiton was
significantly suppressed in C. sativus treated with root
exudates from D. carota as well as in D. carota treated with
root exudates from C. sativus. Detection (%) of AM fungi
belonging to Glomus and Acaulospora and/or Entrophospora
was remarkably reduced in C. sativus and D. carota treated
with root exudates from D. carota and C. sativus, respectively.
Percent of colonization in cucmber treated with root exudates
of carrot was 68% while it was 81 and 79 % in cucumber
treated with root exudates from cucmber and water,
respectively. Percent of colonizaiton in carrot showed similar
tendency with low AM colonization (58%) by cucumber root
exudates treatment and high AM colonization (74 and 82%)
by carrot root exudates and water treatment, respectively.
Such supression effect on AM colonization by the plant root
exudates was reported in case of supplying root exudates from
non-mycorrhizal plant species such as mustard and sugar beet.
In this study, root exudates collected even from the
mycorrhizal plant species, cucumber and carrot, showed
suppression on AM colonization in ach plant.
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Fig 1: Plant root exudates mediate a rhizospheric interactions: At the species level (right side), Multitrophic interactions (bottom), and At the
community level (left side). http://www.nrcresearchpress.com/doi/full/10.1139/cjb-2013-0225
Conclusion
Root exudates serve important role as chemical attractant and
repellants in the rhizosphere. It changes the chemical and
physical properties of soil and inhibit the growth of
competing plant species. Nearly 5% to 21% of all photo
synthetically fixed carbon being transferred to the rhizosphere
through root exudates. Root exudates in their various
forms may regulate plant and microbial communities in the
rhizosphere. Flavonoids and other phenolic compounds
released by plant roots have important functions in plant
pathogenic interactions, feeding deterrence, nematode
resistance, all opathic interactions and as signal molecules for
the establishment of symbiotic association. Hydroxylysine
plays a role in the effective symbiotic relationship by
regulating the growth of the root nodule bacteria on the root
surface. Rice plant produce mom lactone B and it may acts as
an allelochemical and play and important role in the
competition with Neighbouring plant.
References
1. Bacilio JM, Aguilar FS, Ventura ZE, Perez CE,
Bouquelet S, Zenteno E. Chemical characterization of
root exudates from rice (Oryza sativa) and their effects on
the chemotactic response of Endo Phyticbacteria. Plant
Soil. 2002; 249:271–277.
2. Bais HP, Loyola Vargas VM, Flores HE, Vivanco JM.
~ 458 ~
The Pharma Innovation Journal
Root specific metabolism: the biology and biochemistry
of underground organs. In vitro Cell Dev Biol Plant.
2001; 37:730–741
3. Bais HP, Park SW, Stermitz FR, Halligan KM, Vivanco
JM. Exudation of fluorescent-carbolines from Oxalis
tuberosa L. roots. Phytochemistry. 2002a; 61:539-543.
4. Bais HP, Walker TS, Schweizer HP, Vivanco JM. Root
specific elicitation and antimicrobial activity of
rosmarinic acid in hairy root cultures of sweet basil
(Ocimum basilicum L.). Plant Physiol Biochem. 2002b;
40:983–995.
5. Bais HP, Walker TS, Stermitz FR, Hufbauer RA,
Vivanco JM. Enantiomeric dependent phytotoxic and
antimicrobial activity of ()-catechin; a rhizosecreted
racemic mixture from Centaurea maculosa (Spotted
Knapweed). Plant Physiol. 2002c; 128:1173-1179.
6. Becard G, Douds DD, Pfeffer PE. Extensive in vitro
hyphal growth of vesicular-arbuscular mycorrhizal fungi
in presence of CO2 and flavonols. Appl Environ
Microbiol. 1992; 58:821-825.
7. Becard G, Taylor LP, Douds DD, Pfeffer PE, Doner LW.
Flavonoids are not necessary plant signal compounds in
arbuscular mycorrhizal symbiosis. Mol Plant-Microbe
Interact. 1995; 8:252–258.
8. Bengough AG, McKenzie BM. Sloughing of root cap
cells decreases the frictional resistance to maize (Zea
mays L.) root growth. J Exp Bot. 1997; 48:885-893.
9. Bhupinder Singh, Santosh Kumar. Evidence for the role
of phytosiderophores in zinc efficiency of wheat. Nature
Biotech. 2002; 19:446-469.
10. Bongsu Choi, Masamichi Ohe, Jiro Harada, Hiroyuki
Daimon Role of belowground parts of green manure
legumes, crotalaria spectabilis and Sesbania rostrata, in N
uptake by the succeeding tendergreen mustard plant.
Plant Prod. Sci. 2008; 11(1):116-123.
11. Brigham LA, Michaels PJ, Flores HE. Cell-specific
production and antimicrobial activity of naphthoquinones
in roots of Lithospermum erythrorhizon. Plant Physiol.
1999; 119:417–428.
12. Callaway RM, Aschehoug ET. Invasive plants versus
their new and old neighbors: A mechanism for exotic
invasion. Science. 2000; 90:521–523.
13. Chaboud A, Rougier M. Identification and localization of
sugar components of rice (Oryza sativa L.) root cap
mucilage. J Plant Physiol. 1984; 116:323–330.
14. Estabrook EM, Yoder JI. Plant-plant communications:
rhizosphere signaling between parasitic angiosperms and
their hosts. Plant Physiol. 1998; 116:1-7.
15. Flores HE, Pickard JJ, Hoy MW. Production of
polyacetylenes and thiophenes in heterotrophic and
photosynthetic root cultures of Asteraceae. 1988; 7:233-
254.
16. Flores HE, Vivanco JM, Loyola-Vargas VM. “Radicle”
biochemistry: the biology of root-specific metabolism.
Trends Plant Sci. 1999; 4:220–226.
17. Griffin GJ, Hale MG, Shay FJ. Nature and quantity of
sloughed organic matter produced by roots of axenic
peanut plants. Soil Biol Biochem. 1976; 8:29-32.
18. Hasegawa K, Togo S, Urashima M, Mizutani J,
Kosemura S, Yamamura S. An auxin-inhibiting
substance from light-grown maizeshoots.
Phytochemistry. 1992; 31:3673-3676.
19. Hawes MC, Gunawardena U, Miyasaka S, Zhao X. The
role of root border cells in plant defense. Trends Plant
Sci. 2000; 5:128–133.
20. Hisashi Kato-Noguchi, Takeshi Ino. Release level of
momilactone B from rice plants. Plant Prod. Sci. 2004;
7(2):189-190.
21. Hisashi Kato-Noguchi, Hideki Sugimoto, Masashi
Yamada. Buckwheat seedlings may inhibit other plant
growth by allelopathic substaces. Environ. Control Biol.
2007; 45(1):27-32.
22. Hutchison WD, Campbell CD. Economic impact of the
sugarbeet root aphid (Homoptera: Aphididae) on
sugarbeet yield and quality in southern Minn. J Econ
Entomol. 1994; 87:465-475.
23. Jones DL, Hodge A, Kuzyakov Y. Plant and mycorrhizal
regulation of rhizodeposition. New Phytol. 2004;
163:459-480.
24. Jones DL, Nguyen C, Finlay RD. Carbon flow in the
rhizosphere: carbon trading at the soil–root interface.
Plant Soil. 2009; 321:5-33.
25. Kang S, Mills AL. Soil bacterial community structure
changes following disturbance of the overlying plant
community. Soil Sci. 2004; 169(1):55-65.
26. Keiko Sasaki-Igawa, Tetsuya Sato, Hiroshi Masuda,
Takuji Ohwada. Role of Hydroxylysine on the
Nodulation of Root Nodule Bacteria, Bioscience,
Biotechnology, and Biochemistry. 1999; 63(11):1859-
1864.
27. Keyes WJ, O’Malley RC, Kim D, Lynn DG. Signaling
organogenesis in parasitic angiosperms: xenognosin
generation, perception, and response. J Plant Growth
Regul. 2000; 19:217–231.
28. Klun JA, Tipton CL, Robinson JF. Isolation and
identification of 6, 7-dimethoxy-2-benzoxazolinone from
dried tissues of Zea mays (L.) and evidence of its cyclic
hydroxamic acid precursor. J Agr. Food Chem. 1970;
18:663–665.
29. Kuzyakov Y, Cheng W. Photosynthesis controls of
rhizosphere respiration and organic matter
decomposition. Soil Biol Biochem. 2001; 33:1915–1925.
30. Larson RA, Marley KA, Tuveson RW, Berenbaum MR.
Carboline alkaloids: mechanisms of phototoxicity to
bacteria and insects. Photochem Photobiol. 1988; 48:665-
674
31. Marschner H. Mineral Nutrition of Higher Plants, Ed 2.
Academic Press, London, 1995.
32. Kubota M, Hyakumachi M, Mitsuo Miyazawa. Influence
of root exudates from Cucumis sativus and Daucus carota
on arbuscular mycorrhizal coloniztion. J Oleo Sco. 2004;
53(4):207-210.
33. McCully ME. Water efflux from the surface of field-
grown grass roots: observations of cryo-scanning electron
microscopy. Physiol Plant. 1995 95:217-224.
34. McCully ME, Boyer JS. The expansion of root cap
mucilage during hydration: III. Changes in water
potential and water content. Physiol Plant. 1997; 99:169-
177.
35. Nardi S, Concheri G, Pizzeghello D, Sturaro A, Rella R,
Parvoli G. Soil organic matter mobilization by root
exudates. Chemosphere. 2000; 5:653-658.
36. Nguyen C, Todorovic C, Robin C, Christophe A, Guckert
A. Continuous monitoring of rhizosphere respiration after
labelling of plant shoots with (CO2)-C-14. Plant Soil.
1999; 212:191–201.
37. Niemeyer HM. Hydroxamic acids (4-Hydroxy-l,4-
benzoxazin-3-ones), defence chemicals in the gramineae.
~ 459 ~
The Pharma Innovation Journal
Phytochemistry. 1988; 27:3349-3358.
38. Perez FJ, Ormeno-Nunez J. Differences in hydroxamic
acids content in roots and root exudates of wheat
(Triticum aestivum L.) and rye (Secale cereale L.):
Possible role in allelopathy. J Chem. Ecol. 1991;
17:1037-1043.
39. Peters NK, Frost JW, Long SR. A plant flavone, luteolin,
induces xpression of Rhizobium meliloti nodulation
genes. Science. 1986; 233:977-980.
40. Petho M. Occurrence of cyclic hydroxamic acids in the
tissues of barnyard grass (Echinochloa crus-galli/L./P.
B.), and their role in allelopathy. Acta Agron. Hungarica.
1993; 42:197-202.
41. Rioval J, AD Hanson. Evidence for a large and sustained
glycolytic flux to lactate in anoxic roots of some
members of the halophytic genus Limonium. Plant
Physiol. 1993; 101:553.
42. Rougier M. Secretory activity at the root cap. In W
Tanner, FA Loews, Eds, Encyclopedia of Plant
Physiology, New Series, Plant Carbohydrates II. Springer
Verlag, Berlin. 1981; 13:542-574.
43. Ryan PR, Delhaize E, Jones DL. Function and
mechanism of organic anion exudation from plant roots.
Annu Rev Plant Phys. 2001; 52:527–560.
44. Shukla Keshav Prasad, Shivesh Sharma, Nand Kumar
Singh, Vasudha Singh, Kirti Tiwari, Sphoorti Singh.
Nature and role of root exudates: Efficacy in
bioremediation African Journal of Biotechnology. 2011;
10(48):9717-9724.
45. Sims IM, Middleton K, Lane AG, Cairns AJ, Bacic A.
Characterisation of extracellular polysaccharides from
suspension cultures of members of the Poaceae. Planta.
2000; 210:261-268.
46. Stintzi A, Browse J. The Arabidopsis male-sterile mutant,
opr3, lacks the 12-oxophytodienoic acid reductase
required for jasmonate synthesis. Proc. Natl. Acad. Sci.
USA. 2000; 97:10625-10630.
47. Stotz HU, Pittendrigh BR, Kroymann J, Weniger K,
Fritsche J, Bauke A et al. Induced plant defense
responses against chewing insects. Ethylene signaling
reduces resistance of Arabidopsis against Egyptian cotton
worm but not diamondback moth. Plant Physiol. 2000;
124:1007-1018.
48. Somasundaram, Sutharsan, Thertham P Rao, Jiro
Tatsumi, Morio Iijima. Rhizodeposition of mucilage, root
border cells, carbon and water under combined soil
physical stresses in Zea mays L. Plant Prod. Sci. 2009;
12(4):443-448.
49. Trieu AT, Van Buuren ML, Harrison MJ. Gene
expression in mycorrhizal roots of Medicago truncatula.
In HE Flores, JP Lynch, D Eissentat, Eds, Radical
Biology: Advances and Perspectives on the Function of
Plant Roots. American Society of Plant Physiologists,
Rockville, MD, 1997, 498-500.
50. Vermeer J, McCully ME. The rhizosheath of Zea: new
insight into the structure and development. Planta. 1982;
156:45–61.
51. Romheld Volker, Marschner Horst. Evidence for a
specific uptake system for iron phytosiderophores in
roots of grasses. Plant Physiol. 1986; 80:175-180.
52. Watt M, McCully ME, Canny MJ. Formation and
stabilization of rhizosheaths of Zea mays L.: effect of soil
water content. Plant Physiol. 1994; 106:179-186.
53. Winkel-Shirley B. Flavonoid biosynthesis: a colorful
model for genetics, biochemistry, cell biology and
biotechnology. Plant Physiol. 2001; 126:485–493.
54. Wu T, Wittkamper J, Flores HE. Root herbivory in vitro:
interaction between root and aphids grown in aseptic
coculture. In Vitro Cell Dev Biol Plant. 1999; 35:259-
264.
55. Yoder JI. Host-plant recognition by parasitic
Scrophulariaceae. Curr Opin Plant Biol. 2001; 4:359–
365.
