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Microbial signaling and plant growth promotion

Article in Canadian Journal of Plant Science July 2014

DOI: 10.4141/CJPS2013-148

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 Microbial signaling and plant growth promotion
Fazli Mabood, Xiaomin Zhou, and Donald L. Smith1
Plant Science Department, McGill University/Macdonald Campus, 21,111 Lakeshore Road,
Ste-Anne-de-Bellevue, Quebec, Canada H9X 3V9.
Received 7 May 2013, accepted 11 September 2013. Published on the web 7 July 2014.
Mabood, F., Zhou, X. and Smith, D. L. 2014. Microbial signaling and plant growth promotion. Can. J. Plant Sci. 94:
10511063. The rhizosphere offers a complex microhabitat where root exudates provide a diverse mixture of organic
compounds that are used as nutrients or signals by the soil microbial population. On the other hand, these soil
microorganisms produce compounds that directly or indirectly assist in plant growth promotion. The widely recognized
mechanisms of plant growth promotion are biofertilization, production of phytohormones, suppression of diseases through
Can. J. Plant Sci. Downloaded from pubs.aic.ca by MCGILL UNIVERSITY on 07/21/14

biocontrol, induction of disease resistance and production of volatile signal compounds. During the past few decades our
understanding of the interaction between rhizobacteria and plants has expanded enormously and this has resulted in
application of microbial products used as crop inoculants (as biofertilizers), for increased crop biomass and disease
suppression. However, this plantmicrobe interaction is affected by adverse environmental conditions, and recent work has
suggested that inoculants carrying plant-to-bacteria or bacteria-to-plant signals can overcome this and promote plant
productivity under stressful environmental conditions. Very recent work has also shown that some plant growth-promoting
rhizobacteria secrete novel signaling molecules that also promote plant growth. The use of rhizobacterial signaling in
promoting plant growth offers a new window of opportunity, especially when we are looking at plants to provide biofuels
and novel bioproducts. Developing technologies that can enhance plant growth and productivity is imperative.

Key words: Plantmicrobe interactions, phytomicrobiome, signal molecules, plant stress,

lipo-chitooligosaccharides, thuricin 17

Mabood, F., Zhou, X. et Smith, D. L. 2014. Signalisation microbienne et acceleration de la croissance des plantes. Can. J.
For personal use only.

Plant Sci. 94: 10511063. La rhizosphere est un micro-habitat complexe dans lequel les exsudats des racines procurent un
melange variable de composes organiques dont les unicellulaires presents dans le sol se nourrissent ou quils utilisent
comme signaux. Parallelement, ces microorganismes synthetisent des composes qui aident directement ou indirectement
la plante a pousser. Parmi les mecanismes abondamment reconnus qui accelerent la croissance des vegetaux figurent la
biofertilisation, la production de phytohormones, la suppression de maladies par la lutte biologique, linduction de la
resistance aux maladies et la genese de composes volatils servant de signaux. Au cours des dernieres decennies, nos
connaissances sur les interactions entre les rhizobacteries et les plantes ont augmente de maniere phenomenale, ce qui a
debouche sur linoculation de substances microbiennes aux cultures (sous forme dengrais biologiques) en vue dune plus
grande production de biomasse et de la suppression des maladies. Les interactions plante-microorganismes sont neanmoins
affectees par les conditions environnementales quand elles sont defavorables et des recherches recentes laissent croire
que les inoculats qui vehiculent les signaux de la plante a la bacterie ou vice-versa pourraient surmonter cette difficulte
et augmenter le rendement des vegetaux qui poussent dans des conditions difficiles. Des travaux tres recents ont egalement
montre quune partie des rhizobacteries qui accelerent la croissance des plantes secretent de nouvelles molecules signal qui
favorisent elles aussi la croissance. Le recours a la signalisation rhizobacterienne pour promouvoir la croissance des
vegetaux ouvre une nouvelle porte, surtout pour les plantes dont on veut tirer des biocarburants et de nouveaux produits
biologiques. Il est imperatif delaborer des technologies qui rehausseront la croissance et le rendement des plantes.

Mots cles: Interactions plante-microbe, phytomicrobiome, molecules signal, stress vegetal,

lipo-chitooligosaccharides, thuricine 17

PLANT GROWTH-PROMOTING RHIZOBACTERIA Plant growth-promoting rhizobacteria (PGPR) in-


AND CROPS POTENTIAL AND INCONSISTENCY
The rhizosphere is a complex habitat containing living
plant roots with associated soil where root exudates
attract and promote microbial growth and metabolism.
The activities of the diverse rhizosphere microbial
community greatly influence many aspects of plant
physiology and growth, including protecting the host
plant from deleterious pathogenic microorganisms.
1 growth promoting rhizobacteria; RZT, root zone temperature;
Corresponding author (e-mail: Donald.smith@
mcgill.ca).
clude bacteria in the soil near plant roots, on the sur-
face of plant root systems, in spaces between root cells
or inside specialized cells of root nodules, that are
Abbreviations: ACC, 1-aminocyclopropane-1-carboxylate;
DAPG, 2,4-diacetylphloroglucinol; ePGPR, extracellular PGPR;
IAA, indole-3-acetic acid; iPGPR, intracellular PGPR; ISR,
induced systemic resistance; JA, jasmonic acid; LCO, lipo-
chitooligosaccharide; MeJA, methyl jasmonate; PGPR, plant
SAR, systemic acquired resistance; VOC, volatile organic
compound

Can. J. Plant Sci. (2014) 94: 10511063 doi:10.4141/CJPS2013-148 1051

 1052 CANADIAN JOURNAL OF PLANT SCIENCE
able to stimulate plant growth through a wide array of
mechanisms (Gray and Smith 2005). PGPR employ
a variety of mechanisms to promote plant growth and
development.
The more widely recognized mechanisms include: (1)
biofertilization (enhanced nutrient availability), (2) sup-
pression of diseases through biocontrol, (3) induction of
disease resistance in plants, (4) production of phytohor-
mones, and (5) production of volatile signal compounds
(Whipps 2001). On the broad scale, PGPR include the
legume-nodulating rhizobia, and as such can be sepa-
rated into those residing outside plant cells (extracellular
 ePGPR) and the rhizobia that live inside plant cells
(intracellular  iPGPR) (Gray and Smith 2005). Appli-
Can. J. Plant Sci. Downloaded from pubs.aic.ca by MCGILL UNIVERSITY on 07/21/14
cation of PGPR to crop production systems, with the
exception of rhizobia, has met with mixed results. PGPR
are often quite unreliable in the field, causing increases
sometimes and not others (Nelson 2004), suggesting that
there is much we do not understand about them. At a
time when we are looking to plants, and crop plants in
particular, to provide biofuels and other novel biopro-
ducts (Ragauskas et al. 2006) while still feeding the
worlds growing population, against a background of
climate change, understanding and developing technol-
ogies that can increase overall plant productivity is
imperative.
For personal use only.
Biofertilization
Some rhizobacteria promote plant growth and develop-
ment by acting as biofertilizers. PGPR acting as biofer-
tilizers improve plant health through: (1) increasing
nutrient availability for plants, (2) biological nitrogen
fixation, and (3) enhancing symbioses as helper bacteria
(Vessey 2003). A biofertilizer is defined as a substance
which contains living microorganisms which, when
applied to seed, plant surfaces, or soil, colonizes the
rhizosphere or the interior of the plant and promotes
growth by increasing the supply or availability of
primary nutrients to the host plant (Vessey 2003).
The most widely used bacterial biofertilizers are the
nitrogen-fixing rhizobia. These are largely rhizobia in the
genera Allorhizobium, Azorhizobium, Bradyrhizobium,
Mesorhizobium, Rhizobium, and Sinorhizobium which
enter into symbiotic associations with their host legume
host plants and fix atmospheric dinitrogen inside root
nodules differentiated for this purpose. Plants utilize the
nitrogen fixed inside the nodule and provide photo-
synthetically fixed carbon to the rhizobia. There has
been an increase in rhizobia-based commercial in-
oculants as biofertilizers (Vessey 2003) and given the
large quantities of fossil fuels used to produce nitrogen
fertilizers and the steep rise in fossil fuel prices over
recent years, a significant expansion in the use of bio-
fertilizers is most likely to continue.
Besides rhizobia, there are other rhizobacteria that
live and fix nitrogen outside of formal symbioses,
and these are referred to as free-living or associative
nitrogen-fixing bacteria, among them are Azospirillum,
Acetobacter, Herbaspirillum, Azoarcus and Azotobacter
(Steenhoudt and Vanderleyden 2000). These rhizobac-
teria have been getting a great deal of attention as
biofertilizers as they are able to fix nitrogen in associa-
tion with non-legume plants (Boddey et al. 1991) and
can be used in marginal lands as a low input way to
provide nutrients to crop plants.
Other than nitrogen fixation, PGPR acting as biofer-
tilizers can promote plant growth by solubilizing nu-
trients that are otherwise not very available for plant
growth. For example phosphate solubilizing bacteria
mobilize phosphorus, making it substantially more
available to plants (Kim et al. 1998; Rodriguez and
Fraga 1999). Some rhizobacteria produce siderophores
that enhance iron availability to plants (Bloemberg
and Lugtenberg 2001) while others play an important
role in micronutrient availability to plants (Fasim et al.
2002).
Biocontrol
PGPR enhance plant growth and development by
controlling deleterious microorganisms through a range
of sometimes complex mechanisms, including produc-
tion of broad spectrum antibiotics, production of narrow
spectrum bacteriocins, production of extracellular lytic
enzymes and enhancement of plant resistance to patho-
genic organisms.
Antibiotics
The role of antibiosis in rhizobacteria-mediated control
of plant pathogens has been an area of extensive research
during the past several decades (Whipps 2001). Anti-
biotic production by fluorescent pseudomonads has
been well documented. Pseudomonads produce many
antibiotic substances, such as 2,4-diacetylphloroglucinol
(DAPG), amphisin, oomycin A, hydrogen cyanide,
phenazine, pyoluteorin, pyrrolnitrin, and cyclic lipopep-
tides (Defago 1993; Nielson et al. 2002; Raaijmakers et al.
2002; de Souza et al. 2003; Nielson and Sorensen 2003).
Besides pseudomonads, Streptomyces, Bacillus and Ste-
notrophomonas spp. have also been shown to produce
antibiotic substances, such as oligomycin A, zwittermicin
A, kanosamine, and xanthobaccin (Hashidoko et al.
1999; Kim et al. 1999; Milner et al. 1995; Milner et al.
1996; Nakayama et al. 1999).
Antibiotics synthesis by bacteria is affected by many
factors, and these include the type of carbon source, pH
of the growth medium, growth temperature and avail-
ability of trace elements (Keel et al. 1989; Ownley et al.
1992, 2003; Georgakopoulos et al. 1994; Milner et al.
1995; Milner et al. 1996; Duffy and Defago 1997, 1999,
2000; Bender et al. 1999b). The presence of particular
nutrient types also affects the biosynthesis of antibiotics
by a particular bacterial strain. The addition of glucose, as
a carbon source to, P. fluorescens CHA0 stimulates the
biosynthesis of DAPG, while it inhibits the biosynthesis
 MABOOD ET AL. * MICROBIAL SIGNALING AND PLANT GROWTH
of pyoluteorin. However, pyoluteorin is the dominant
antimicrobial compound produced by this strain in the
absence of glucose (Duffy and Defago 1999). Interest-
ingly, the age of the host plants also affects production
of antibiotic compounds by selected bacterial strains.
Root exudates from young plants do not induce DAPG
production, while it is induced by the root exudates of
older plants (Picard et al. 2000).
Bacteriocins
Aside from the more classic antibiotics, some rhizobac-
teria are known to produce proteinaceous antimicrobial
peptides known as bacteriocins. These bacteriocins show
Can. J. Plant Sci. Downloaded from pubs.aic.ca by MCGILL UNIVERSITY on 07/21/14
bactericidal or bacteriostatic effects against bacteria
closely related to the producer strain (Jack et al. 1995).
Recently, we have shown that Bacillus thuringiensis
NEB 17 produces a bacteriocin, thuricin 17 (T17), which
shows antimicrobial activity against a broad range of
closely related bacterial species (Gray et al. 2006a).
Kamoun et al. (2005) reported that B. thuringiensis
subsp. kurstaki strain BUPM4 produces bacthuricin
F4 (BF4  a bacteriocin) that shows bactericidal activ-
ity against closely related bacteria. T17 and BF4
have similar molecular weights (T17  3162 Da and
BF4  3160 Da) and share similarity at the N terminus
sequence (Kamoun et al. 2005; Gray et al. 2006a, b).
For personal use only.
We have recently shown that these two bacteriocins
show similar spectra of antimicrobial activities and
thus have structural and functional similarities (Jung
et al. 2008a).
Extracellular Lytic Enzymes
Another mechanism of biocontrol of plant pathogens is
the production of cell wall degrading enzymes that exert
antifungal activities, thus contributing to the biocontol
activity of these rhizobacteria. These cell wall degrading
enzymes include chitinases, glucanases, cellulases, and
proteases that cause lysis and degradation of the
fungal cell walls. Valois et al. (1996) reported that some
actinomycete isolates produced b-1,3-,b-1,4-, and b-1,6-
glucanases that hydrolyze glucans from Phytophthora cell
walls, thus causing lysis of Phytophthora cells were used
for the control of Phytophthora fragariae var. rubi, a
pathogen causing raspberry root rot. Chitinase produ-
cing bacteria such as Enterobacter agglomerans (Chernin
et al. 1995), Bacillus cereus (Pleban et al. 1997) and
Paenibacillus illinoisensis (Jung et al. 2003) decreased the
incidence of disease symptoms caused by Rhizoctonia
solani in cotton and cucumber. Chitinase producing
P. illinoisensis, provides control of blight in pepper
(Capsicum annuum L.) caused by Phytopthora capsici
(Jung et al. 2005).
Extracellular proteases play an important role in
biocontrol. Stenotrophomonas maltophila W81 produce
proteases and are involved in the biocontrol of Pythium
ultimum in sugar beet (Dunne et al. 1997). Cellulase-
producing Micromonospora carbonacea showed biocontrol
1053
activity against Phytophthora cinnamomi, the causal
organism of root rot in Banksia grandis (El-Tarabily
et al. 1996).
Lytic enzymes produced by rhizobacteria are of
great importance in the biological control of fungal
plant pathogens. For instance, Paenibacillus sp. 300
and Streptomyces sp. 385 produce chitinase and b-1,3-
glucanase, which play a crucial role in the biological con-
trol of Fusarium oxysporum f. sp. cucumerinum causing
Fusarium wilt of cucumber (Cucumus sativus) (Singh et al.
1999). Similarly, b-1,3 glucanase produced by Pseudomonas
cepacia lyse fungal cell walls and decrease the incidence
of diseases caused by Rhizoctonia solani, Sclerotium
rolfsii and Pythium ultimum (Fridlender et al. 1993).
Chitinolytic Rhizobacteria and Beneficial
Microorganisms
During the initial interaction of the legumerhizobia
symbiosis, legume plants secrete flavonoids, which
induce the production of Nod factors, which are lipo-
chitooligosaccharides (LCOs), from rhizobia. Nod fac-
tors are structurally similar to chitin in that the main
structure of Nod factor consists of N-acetylglucosamine
(GlcNAc). Some rhizobacteria are known to produce
chitinases that degrade chitin, thus playing an important
role as potential biocontrol agents in the control of
phytopathogenic fungi. However, these rhizobacteria
might affect symbiosis establishment by disrupting in-
ter-organismal signaling, a crucial step in the early stages
of the nitrogen-fixing symbiosis. We have shown that the
soil bacteria Paenibacillus illinoisensis and Bacillus thur-
ingiensis subsp. pakistani produce chitinases that are able
to cleave Nod factors. When purified Nod factors from
B. japonicum [Nod BjV (C18:1, MeFuc)] were treated with
crude chitinases from P. illinoisensis and B. thuringiensis
subsp. pakistani, this led to a substantial degradation of
Nod factor molecules (Jung et al. 2008a).
Induction of Disease Resistance to
Phytopathogens in Plants
Systemic Acquired Resistance
Salicylic acid plays a central role in systemic acquired
resistance (SAR) and its induction of pathogenesis-
related proteins in plants (Ward et al. 1991; Enyedi
et al. 1992; Gaffney et al. 1993; Ryals et al. 1996). Some
rhizobacteria, under iron-limited conditions, are able
to synthesize SA, thereby triggering the SAR pathway
and inducing systemic resistance in plants (Maurhofer
et al. 1994; Buysens et al. 1996; Leeman et al. 1996; De
Meyer and Hofte 1997; Press et al. 1997). Pseudomonas
aeruginosa 7NSK2 produces SA that activates SAR in
bean plants (De Meyer et al. 1999) and a SA-deficient
mutant of P. aeruginosa 7NSK2 loses its ability to
induce resistance to Botrytis cinerea in bean (De Meyer
and Hofte 1997). Introduction of SA biosynthetic genes
into P. fluorescens strain P3, incapable of producing SA,
made this strain capable of producing SA and induced
 1054 CANADIAN JOURNAL OF PLANT SCIENCE
resistance to tobacco necrosis virus in tobacco plants
(Maurhofer et al. 1998).
Induced Systemic Resistance
Inoculation of PGPR onto seeds or seedling roots may
trigger another mechanism in host plants, known as
induced systemic resistance (ISR), for the suppression of
pathogenic microorganisms and arresting disease devel-
opment (van Loon et al. 1998; Kloepper et al. 1999).
Induction of ISR protects plants that are able to resist
subsequent pathogen infections (van Loon 1997). Rhi-
zobacteria mediated stimulation of ISR is considered
different from SAR. SAR involves a systemic activation
of defense responses to necrotizing pathogens in distal
Can. J. Plant Sci. Downloaded from pubs.aic.ca by MCGILL UNIVERSITY on 07/21/14
parts of plants and involves hypersensitive response and
expression of several pathogenesis-related genes (Ryals
et al. 1996); however, ISR, as induced by PGPR, does
not provoke a visible hypersensitive response (Wei et al.
1991). Salicylic acid plays a central role in the SAR
pathway and studies have shown that there is a strong
relationship between SAR and accumulation of SA in
plants (Sticher et al. 1997). However, ISR is not SA
dependent and involves jasmonic acid (JA) and ethylene
in a signal transduction cascade leading to improved
disease resistance (Pieterse et al. 1998).
For personal use only.
Phytohormone Production
Some PGPR produce phytohormones such as auxin,
cytokinin, gibberellin, abscisic acid, ethylene and salicylic
acid. Phytohormone production by PGPR is consid-
ered of great value in agriculture since these hormones
directly affect the physiology and growth of crop plants.
For instance, it has been shown that Azospirillum spp.
produces auxins, cytokinins and gibberellins that enhance
root growth and development, thereby enhancing nutri-
ent uptake and increasing biomass and yield (Steenhoudt
and Vanderleyden 2000). Phytohormone production by
rhizobacteria, especially indole-3-acetic acid (IAA), is
an important source of plant growth promotion. A range
of Bacillus species have been reported to produce IAA
(Chanway and Nelson 1990; Selvadurai et al. 1991).
Karadeniz et al. (2006) reported the production of auxin
(indole-3-acetic acid), gibberellin, cytokinin (zeatin) and
abscisic acid by bacteria Proteus mirabilis, P. vulgaris,
Klebsiella pneumoniae, Bacillus megaterium, and B. cereus.
PGPR are also known to produce cytokinins, hor-
mones important in the control of cell division, chlor-
oplast development and bud formation (Arshad and
Frankenberger 1991; Serdyuk et al. 1995). For instance,
Rhizobium leguminosarum strains promote early plant
growth and development of canola and lettuce due to
their ability to produce phytohormones such as IAA
and cytokinins (Noel et al. 1996). Similarly, Methylo-
bacterium spp. can increase soybean seed germination
and this effect may be mimicked by medium containing
cytokinins (Holland 1994).
Rhizobacteria can also control ethylene biosynthesis
in planta. Some rhizobacteria produce the enzyme
1-aminocyclopropane-1-carboxylate (ACC) deaminase
that cleaves and hydrolyses plant-produced ACC,
thereby lowering ethylene levels in plants. ACC deami-
nase producing rhizobacteria decrease ethylene levels in
plants and allow them to be more resistant to a wide
variety of environmental stresses (Glick 2005).
PGPR that produce salicylates are able to induce
SAR in colonized plants. The effects of SA producing
rhizobacteria on plants have been described in section
(16)3.3.
Volatile Signals
Plants communicate with each other using airborne
volatile signal molecules such as methyl salicylate, methyl
jasmonate (MeJA) and ethylene. These compounds are
released, at very low concentrations, by plants and act as
signals to neighboring plants (Farmer and Ryan 1990;
Shulaev et al. 1997; Dong 1998; Baldwin et al. 2006).
Recently, it has been shown than PGPR also commu-
nicate with plants by producing volatile compounds that
are able to play an important role in plant growth
and development and systemic resistance. Ryu et al.
(2003, 2004) demonstrated that rhizobacteria produce a
blend of airborne volatile organic compounds (VOC)
that regulate plant growth and development and induce
systemic resistance in Arabidopsis. The PGPR strains
Bacillus subtilis GB03 and Bacillus amyloliquefaciens
IN937a release two volatile compounds, 3-hydroxy-
2-butanone (acetoin) and 2,3-butanediol (2,3-B), that
promote growth and development of Arabidopsis. PGPR
strains unable to produce these VOCs did not cause plant
growth promotion (Ryu et al. 2003). When Arabidopsis
seedlings were exposed to bacterial VOCs (acetoin and
2,3-B) from B. subtilis and B. amyloliquefaciens for only
4 d the ISR pathway was induced, resulting in symp-
toms of disease caused by Erwinia carotovora subsp.
carotovora (Ryu et al. 2004).
Consistent Inconsistency
In the past two decades, significant research progress
has been made towards understanding the mechanisms
of beneficial plantmicrobe interactions and the way
they promote plant growth and development. Many
products have been successfully brought into commer-
cial formulations and significant among them are
the rhizobia-based inoculants used as biofertilizers and
other PGPR inoculants that promote plant growth and
development directly or indirectly.
The market potential for bio-based products used
for plant growth promotion and biocontrol of plant
diseases is increasing (Haas and Defago 2005). Both
conventional and organic growers are increasingly
taking interest in bio-based products (Rzewnicki 2000).
Many rhizobacteria-based products have already been
tested and successfully commercialized in the green-
house industry, with considerable potential for further
growth (Paulitz and Belanger 2001).
 MABOOD ET AL. * MICROBIAL SIGNALING AND PLANT GROWTH
While PGPR-based products have been used success-
fully for plant growth promotion and the biocontrol of
plant pathogens under laboratory and greenhouse con-
ditions (Paulitz and Belanger 2001), field results have
not always been successful (Nelson 2004). Success in
the greenhouse industries may be due to the controlled
environment and better management, which make the
PGPR-based products more effective (Paulitz and
Belanger 2001). By contrast, field conditions are highly
variable, and lack of knowledge of biotic and abiotic
factors influencing the survival, proliferation and per-
formance of PGPR may be factors affecting the efficacy
of PGPR-based products. However, better understand-
ing of the biotic and abiotic factors influencing PGPR
Can. J. Plant Sci. Downloaded from pubs.aic.ca by MCGILL UNIVERSITY on 07/21/14
activity may aid in the development of better PGPR
inoculant formulations and PGPR-based products
(Bowen and Rovira 1999; McSpadden et al. 2002).
PLANT GROWTH-PROMOTING RHIZOBACTERIA
AND SIGNALS: RHIZOBIAL SIGNALS
A unique aspect of legume plants is that they enter into
symbiotic association with soil bacteria of the genera
Azorhizobium, Bradyrhizobium, Mesorhizobium, Rhizo-
bium, and Sinorhizobium, collectively known as rhizobia.
A successful interaction between the two partners leads
to the formation of a new plant organ, the nodule, where
For personal use only.
bacteria reside in the form of bacteroids and fix atmo-
spheric dinitrogen into ammonia, which is utilized by the
host plant (Perret et al. 2000). The interaction between
host plant and rhizobia is a specialized process and
involves the exchange of signal molecules by the two
partners (Fig. 1). This initial exchange leads to rejection
or acceptance of the appropriate partner and thus
plays an integral role in host specificity. Plants secrete
flavonoid compounds, acting as plant-to-bacteria sig-
nal molecules, which induce the transcription of bacte-
rial nodulation genes, leading to the biosynthesis and
Fig. 1. Signal exchange between legumes and rhizobia as
typied by the soybean  Bradyrhizobium japonicum symbiosis.
The phenylpropanoid pathway is used to produce isolfavoinds,
which bind the NodD promoter, leading to activation of the
nod genes, followed by production of lipo-chitooligosacharides
as signals back to the legume plant.
1055
secretion of LCOs by rhizobia. LCOs act as bacteria-to-
plant signal molecules.

Plant Signals: Flavonoids Their Role and
Potential in Promoting Plant Growth
Flavonoids exuded from host plant roots can act
as important signal molecules in rhizobialegume sym-
bioses. Initially they act as chemoattractants to rhizobia
(Caetano-Anolles et al. 1988) and cause the induction of
nod genes of the host rhizobia (Hartwig et al. 1990). There
is a high degree of specificity, and not all flavonoids
induce the nod genes in all rhizobia; specific flavonoids
induce nod genes in specific rhizobia. It is known that
flavonoids interact with the rhizobial NodD protein
which, upon activation, induces the transcription of the
nod genes. Genistein (an isoflavonoid) induces the nod
genes of Bradyrhizobium japonicum, a microsymbiont
of soybean (Glycine max) (Kosslak et al. 1987), while it
inhibits the nod genes of Rhizobium leguminosarum bv.
viceae, a microsymbiont of pea (Pisum sativum) (Firmin
et al. 1986) and Sinorhizobium meliloti, nodulating alfalfa
(Hirsch et al. 2001). Sinorhizobium meliloti nod genes are
induced by luteolin (a flavone) (Hartwig et al. 1990).
Besides flavonoids, other non-flavonoid compounds
have also been shown to induce the rhizobial nod genes.
These are jasmonates (JA and MeJA) (Mabood and
Smith 2005), aldonic acids (erythronic and tetronic acids)
(Gagnon and Ibrahim 1998) and betaines (stachydrine
and trigonelline) (Phillips 2000).
Genistein and daidzein are the major nod gene inducing
isoflavonoids exuded by soybean roots. The biosynthesis
and excretion of these compounds from plant roots is
inhibited under certain stressful environmental condi-
tions, such as low root zone temperature (RZT). Zhang
and Smith (1996a) reported that low RZT inhibits the
biosynthesis and secretion of genistein from soybean
roots. Low RZT also inhibits the expression of the nod
genes of B. japonicum following induction by genistein
(Zhang et al. 1996) and of Rhizobium leguminosarum
following induction by hesperetin (Begum et al. 2001a).
Thus, application of flavonoid signals to rhizobia might
overcome the negative effect of low temperature and
promote legume nodulation. This was demonstrated
by Zhang and Smith (1995) who reported that pre-
incubation of B. japonicum with genistein promoted
soybean nodulation and nitrogen fixation under low
RZT conditions. Zhang et al. (1996) also showed that
higher genistein concentrations are required for the
maximum induction of the nod genes at suboptimal
temperatures. Genistein pre-incubated B. japonicum cells
also accelerated the early stages of nodulation (infection
and infection thread formation) development of nodules
and the onset of nitrogen fixation (Zhang and Smith
1994).
When genistein was applied onto seeds or in open
furrows at the time of seed sowing, it also promoted
soybean nodulation and nitrogen fixation under low soil
temperature conditions (Zhang and Smith 1996b, 1997).
 1056 CANADIAN JOURNAL OF PLANT SCIENCE
Partial alleviation of inhibitory effects of low RZT was
also demonstrated in R. leguminosarum and pea and
lentil symbiotic association. When R. leguminosarum bv.
viceae cultures were induced with hesperetin and inocu-
lated onto pea and lentil roots in the early stages of
plant growth, it partially alleviated the low RZT
inhibitory effects and promoted nodulation and early
plant growth under greenhouse conditions (Begum et al.
2001a). Naringenin or hesperetin induced cultures of R.
leguminosarum bv. viciae when directly inoculated onto
pea seeds, or into seed furrows at the time of planting,
promoted pea nodulation and plant growth under field
conditions (Begum et al. 2001b). The effect of these
signal molecules is more pronounced under stressful
Can. J. Plant Sci. Downloaded from pubs.aic.ca by MCGILL UNIVERSITY on 07/21/14
conditions as demonstrated by Lira Junior et al. (2003),
who reported that the positive effect of pre-incubated
inoculant with either hesperetin or naringenin was more
pronounced under saline or low RZT conditions.
The role of jasmonates in inducing the nod genes
(Mabood and Smith 2005) and production of LCOs
from B. japonicum (Mabood et al. 2006a, b) has recently
been reported. When B. japonicum cells were pre-induced
with either JA or MeJA and inoculated onto soybean
seedlings, they enhanced nodulation, nitrogen fixation
and plant growth under greenhouse conditions (Mabood
and Smith 2005). Under short season field conditions,
For personal use only.
inoculation of B. japonicum pre-incubated with MeJA
alone or in combination with genistein, enhanced
soybean nodulation, nitrogen fixation (Mabood et al.
2006c) and plant growth and grain yield (Mabood et al.
2006d) in southeastern Quebec, Canada.
Industrial Applications and Market Potential
The use of plant-to-bacteria signal molecules for en-
hancing nodulation and nitrogen fixation has recently
entered the market place. For example, SoyaSignalTM
(containing genistein and daidzein: the nod gene indu-
cers of B. japonicum) was a commercial inoculant used
for promoting nodulation in soybean. SoyaSignal was
applied directly onto seed surface or into soil furrows
containing adequate indigenous bradyrhizobial popula-
tions (Smith and Zhang 1999). When SoyaSignalTM was
tested under field conditions at 127 locations in Canada
and United States (from 1994 to 1999), Leibovitch et al.
(2001) reported that this technology effectively pro-
moted soybean yield (average yield increase of 7%).
Novozymes (http://www.bioag.novozymes.com) is
currently marketing a product under the name Pulse-
Signal II. This unique product contains plant-to-
bacteria signal molecules (flavonoids) that enhance the
recognition step between the plant and the rhizobium,
thus leading to earlier and better nodulation and
nitrogen fixation.
Potential in Promoting Plant Growth

Bacterial Signals: Nod Factors Their Role and
Flavonoids acting as plant-to-bacteria signals induce the
transcription of the nodulation (nod) genes of rhizobia.
Coordinated expression of many of the bacterial nod
genes (nod, noe, nol) is necessary for the biosynthesis of
the so called Nod factors, more specifically called LCOs
(Stacey et al. 1995). LCOs are key signal molecules
acting as bacteria-to-plant signals and, as such, play a
major role in the recognition of the micro-symbiont by
the host plant and initial events leading to the organo-
genesis of a nodule in the host plant. Lerouge et al.
(1990) were the first to identify the chemical structure of
Nod factor from S. meliloti and since then researchers
investigating the rhizobialegume symbiosis, have been
successful in isolating and characterizing a wide range of
Nod factors from other rhizobia [see reviews by
DHaeze and Holsters (2002) and Hanin et al. (1999)].
Nod factor production is adversely affected by low
temperatures (Zhang et al 2002; Duzan et al. 2006) so
that low root zone temperature conditions can retard
the effective establishment of the legumerhizobia
nitrogen-fixing symbiosis and lessen any other beneficial
effects nod factors have.
Nod factors are active at very low concentrations. At
submicromolar concentrations, they induce many phy-
siological changes in their host plants, such as root hair
deformation, calcium spiking, changes in hormone
levels, gene expression and initiation of nodule organo-
genesis in legumes plant roots (Denarie and Cullimore
1993; DHaeze and Holsters 2002; Goedhart et al. 2003).
Although non-legumes do not form nodules in
association with rhizobia, studies have shown that
non-legume plants are also able to respond to Nod
factors. Nod factors produced by rhizobia are able to
stimulate plant growth (Souleimanov et al. 2002;
Prithiviraj et al. 2003; Almaraz et al. 2007). Nod factors
promoted cell division in carrot mutants (De Jong et al.
1993) and stimulated early somatic embryo development
in Norway spruce (Dyachok et al. 2002). Purified Nod
factor (Nod Bj-V C18:1, MeFuc) from B. japonicum
promoted root growth of soybean when applied in
hydroponic solution (Souleimanov et al. 2002). Olah
et al. (2005) confirmed these finding by reporting that Nod
factors stimulated lateral root formation in Medicago
truncatula. We have also seen clear enhancement of
Arabidopsis thaliana root growth due to LCO treatment
(Khan et al. 2011).
Nod factors from B. japonicum, at submicromolar
concentrations, promoted seed germination and early
seedling growth of diverse crop plants including legumes
and non-legumes (Prithiviraj et al. 2003). Chen et al.
(2007) reported that foliar application of LCOs to
tomato promoted flowering and increased yield of
greenhouse grown tomato plants. The role of LCOs in
enhancing barley seed germination (Miransari and
Smith 2009) and pea and vetch seed germination,
growth and nodulation (Kidaj et al. 2011) has also
been reported.
Enhanced germination and seedling growth, along
with the mitogenic nature of LCOs, suggest accelerated
meristem activity. This may lead to increased sink
 MABOOD ET AL. * MICROBIAL SIGNALING AND PLANT GROWTH
demand and the observed increases in mobilization of
seed reserves (Prithiviraj et al. 2003) and increased
photosynthetic rates (Almaraz et al. 2007) for more
developed plants, both of which lead to increased
growth (Khan et al. 2008). However, if this is at play
it is interacting with growth related stress responses
(see below).
When applied to soybean leaves LCO from B. japoni-
cum caused transient (25 d) increases in photosynthetic
rate under growth chamber conditions (Almaraz et al.
2007; Khan et al. 2008) and increased soybean yield
(25%) under field conditions (Smith et al. 2003;
Almaraz et al. 2007). While the increase in photosyn-
Can. J. Plant Sci. Downloaded from pubs.aic.ca by MCGILL UNIVERSITY on 07/21/14
thetic rate due to the application of bacteria-to-plant
signal molecules is new, previous studies have suggested
that symbiotic microbes increase plant photosynthetic
rates: rhizobia (Maury et al. 1993), mycorrhizal fungi
(Kucey and Paul 1982), PGPR (Zhang et al. 1997;
Bai et al. 2003) and bacteria that produce lumichrome
(Phillips et al. 1999). It is often assumed that these
increases in photosynthetic rates are related to increased
sink demand by the symbionts. Increased sink demand
causes increased photosynthetic rates, while reduced
sink strength has the opposite effect (Pieters et al. 2001;
Tekalign and Hammes 2005). Cockcroft et al. (2000)
showed that tobacco plants engineered to have a faster
For personal use only.
cell cycle grow substantially faster, presumably because
of increased sink strength in more active meristems,
leading to increased photosynthetic rates. LCOs are
known to activate specific plant genes and act as
mitogens (Long 1989; Denarie et al. 1996; Perret et al.
2000; Patriarca et al. 2004).
We have shown that foliar application of LCOs
induces resistance of soybean plants to powdery mildew
(Duzan et al. 2005) associated with an increase in
phenylalanine ammonia lyase, the first committed step
of the phenylpropanoid pathway, leading to biosynth-
esis of antimicrobial compounds such as phytoalexins.
Given that LCOs induce defense responses in Medicago
cell cultures and roots (Savoure et al. 1997), that LCOs
show structural similarity to chitin (they have a chitin
backbone), and that chitin induces defense responses in
plants (Khan et al. 2003), it possible that LCOs induce
aspects of plant defense responses, similar to chitin. We
have recently shown that the largest group of known
genes activated by spray treatment of soybean with
LCOs are stress response genes (Wang et al. 2012).
Industrial Applications and Market Potential
Nod factors are now being used on a commercial scale
to promote nodulation and plant growth. Novozymes
(http://www.bioag.novozymes.com) is currently market-
ing a product under the name Optimize. This unique
product combines quality nitrogen inoculants with
Novozymes LCO promotor technology. The unique
LCO molecule enhances nutritional capabilities of the
1057
plant making them grow faster. Optimize is applied in
both liquid and granular formulations.
PLANT GROWTH-PROMOTING RHIZOBACTERIA
AND SIGNALS: OTHER SIGNALS THURICIN 17
AND BACTHURICIN F4

We isolated Bacillus thuringiensis NEB17 from soybean
root nodules (Bai et al. 2002b) and when co-inoculated
with B. japonicum it enhanced soybean nodulation (Bai
et al. 2003). We have shown that this bacterium produces
a novel antimicrobial peptide Thuricin 17 (a bacteriocin
of molecular weight 3.1 kDa), which is not toxic to B.
japonicum and shows antimicrobial activity against a
broad range of closely related bacterial species (Gray
et al. 2006a). Another bacteriocin (Bacthuricin F4) was
reported by Kamoun et al. (2005), which is produced by
B. thuringiensis subsp. kurstaki strain BUPM4. These
bacteriocins share amino acid sequence similarity at
the N terminus and based on these two molecules we
proposed a new class of bacteriocins: class IId (Gray et al.
2006b). We have recently shown that these two bacter-
iocins also show similar spectra of antimicrobial activities
and thus have structural and functional similarities (Jung
et al. 2008b). Bacteriocins are bacteria-produced peptides
that are either bactericidal or bacteriostatic to specific
bacterial strains, often those closely related to the strains
producing them (Jack et al. 1995). They provide a
competitive advantage for the producer strain (Wilson
et al. 1998).
We have recently discovered that treatment with
class IId bacteriocins stimulated early growth of corn
and soybean (Lee et al. 2009) in a manner similar to that
caused by LCOs. A protein produced by a PGPR
Serratia strain also increased photosynthesis and growth
(Bai et al. 2002a).
Application of thuricin 17 to soybean plants induced
aspects of plant disease resistance as well. We have
recently shown that thuricin 17 increased total phenolics,
phenylalanine ammonia lyase activity and the levels
of peroxidase and superoxide dismutase enzymes (Jung
et al. 2008c). In another recent study we have reported
that these class IId bacteriocins (thuricin 17 and
bacthuricin F4) are able to induce phenylalanine ammo-
nia lyase, peroxidase and ascorbate peroxidase activities
in soybean leaves (Jung et al. 2011).
Given the stimulatory effect of these class IId
bacteriocins on plant growth and development, there
appears a great potential for these molecules on the
commercial scale. Production of thuricin 17 is substan-
tially easier, and therefore more economic, than LCOs.
Thuricin 17 producing B. thuringiensis NEB 17 is a
fast growing bacterium while B. japonicum (producing
LCOs) is a slow-growing bacterium. In addition, B.
japonicum produces small quantities of LCO, while
B. thuringiensis NEB 17 produces a substantially larger
amount of thuricin 17 (unpublished data). However,
there is a lack of understanding of how these molecules
 1058 CANADIAN JOURNAL OF PLANT SCIENCE
increase plant growth and further work is needed to
uncover the mechanism of action of these molecules.
CONCLUDING REMARKS AND PROSPECTS
FOR FUTURE RESEARCH
Field-grown plants are always associated with a suite of
bacterial (rhizobacteria when root associated) and other
microbes, some of which provide a range of benefits
and promote plant growth (enhanced nutrient uptake,
control of crop pathogens, direct stimulation of plant
growth). This community of bacteria constitutes the
phytomicrobiome. The community of plant growth pro-
moting rhizobacteria (PGPR) and other commonly root
Can. J. Plant Sci. Downloaded from pubs.aic.ca by MCGILL UNIVERSITY on 07/21/14
associated microbes constitute as rhizomicrobiome, with
the remainder being a phyllomicrobiome. The level of
diversity in the plant rhizosphere is particularly high
and exploration of this microbial community is likely
to reveal a wide range of potential mechanisms for
improving crop growth through low input technologies.
For instance, field observations (unpublished) have
indicated that signal (LCOs and thuricin 17) effects
were greatest when spring conditions were cold and wet.
In addition, Atti et al. (2005) demonstrated that LCO
application to drought-stressed soybean plants caused
major physiological changes, which resulted in rebound
For personal use only.
of moderately stressed plants, as compared with non-
LCO treated controls. We have now shown, very
conclusively, that the effects of both LCOs and thuricin
17 are much greater when applied under stressful
conditions (salt, drought, cold) than under optimum
conditions (Smith 2009a, b, 2010; Subramanium 2009;
Subramanian et al. 2010a, b, 2011). This suggests that
these signals are operating through one of the estab-
lished stress response pathways, or a new one, and that
this can dramatically stimulate crop growth in the
presence of stresses, such as low temperature, salt and
drought. The details of the underlying mechanism are
now being addressed. The interaction between at least
one system of PGPR effecter system and the state of the
environment during crop growth may explain at least
some of the inconsistencies in PGPR effectiveness. More
recently, and related to the work of theme four, we
have shown that the application of these signals to
canola can cause accelerated germination and changes in
development leading to altered panicle architecture and
yield potential. It would seem that exploitation of the
phytomicrobiome offers interesting biological opportu-
nities for crop management, adaptation of crops to
climate change conditions and enhanced global food
security.
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