South African Journal of Botany 113 (2017) 91–102

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South African Journal of Botany

journal homepage: www.elsevier.com/locate/sajb

Review

Effect of plant growth-promoting Rhizobacteria on plant

hormone homeostasis
K.A. Tsukanova a, V.К. Сhеbоtаr a, J.J.M. Meyer c, T.N. Bibikova b,⁎
a
All-Russia Research Institute fоr Agricultural Microbiology, 189620, Shosse Podbelskogo 3, St. Petersburg - Pushkin 8, Russia
b
Moscow State University, Faculty of Biology, 119234, Leninskiye Gory 1, page 12, Moscow, Russia
c
Department of Plant and Soil Sciences, University of Pretoria, Pretoria, 0002, South Africa

a r t i c l e i n f o a b s t r a c t

Article history: Plant growth-promoting rhizobacteria (PGPR) includes a wide variety of bacterial strains from different taxo-
Received 8 December 2016 nomic groups that inhabit plant roots and their rhizosphere. By bringing about complex changes in plant growth
Received in revised form 19 June 2017 and development, PGPR can enhance both productivity of agricultural crops, and their pathogen resistance. Col-
Accepted 28 July 2017
onization by PGPR is associated with changes in plant metabolism, signaling and hormone homeostasis. Different
Available online xxxx
PGPR strains can synthesize phytohormones, metabolize them, or affect plants' hormone synthesis and signal
Edited by R Bottini transduction. This review covers various mechanisms employed by PGPB to alter the homeostasis of the plant
hormones auxin, ethylene, cytokinin, gibberellin, abscisic acid, jasmonic acid and salicylic acid.
Keywords: © 2017 SAAB. Published by Elsevier B.V. All rights reserved.
Phytohormons
PGPR
Auxin
Ethylene
Cytokinin
Gibberellin
Abscisic acid
Jasmonic acid
Salicylic acid

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91
2. Auxin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 92
3. Ethylene . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95
4. Cytokinins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96
5. Gibberellins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96
6. Abscisic acid . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97
7. Salicylic acid and Jasmonic acid . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 98
8. Conclusions and perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99

1. Introduction by a wide variety of mechanisms (Glick, 2012). PGPR are currently in-
tensively studied due to their properties which are of considerable
Plant growth-promoting rhizobacteria (PGPR) consist of the rhizo- value both for traditional and sustainable agriculture (Farrar et al.,
sphere bacteria that can enhance plant growth and stress resistance 2014). PGPR can enhance plant mineral nutrition via associated nitro-
gen fixation (Kuan et al., 2016), mobilization of phosphate in the soil
⁎ Corresponding author. (Chen et al., 2006; Mehta et al., 2015), siderophore production
E-mail address: bibikova@mail.bio.msu.ru (T.N. Bibikova). (Vansuyt et al., 2007; Zhou et al., 2016), stimulation of the mycorrhizal

http://dx.doi.org/10.1016/j.sajb.2017.07.007
0254-6299/© 2017 SAAB. Published by Elsevier B.V. All rights reserved.
92 K.A. Tsukanova et al. / South African Journal of Botany 113 (2017) 91–102
symbiosis development and modulation of root architecture (Navarro-
Rodenas et al., 2016). PGPR can also activate plant pathogen resistance
(Niu et al., 2011; Van de Mortel et al., 2012; Sharifi and Ryu, 2016),
suppress pathogen growth (Ali et al., 2014; Saraf et al., 2014;
Prasannakumar et al., 2015) and alleviate the inhibitory effects of abiotic
stressors like drought (Lim and Kim, 2013), salinity (Kim et al., 2014)
and heavy metal pollution (Gupta et al., 2002; Zhu et al., 2015). Because
of growing public concern about the damaging effects of chemical
fertilizers and pesticides, there is an increasing interest in improving
our understanding of molecular mechanisms of interaction between
plants and their rhizosphere microbial community.
It is well established that PGPR colonization is associated with pro-
found changes in the host plant's development and hormone homeosta-
sis. Phytohormones act as messengers to coordinate cellular activities
and to regulate various cellular processes in plants, including abiotic
stress responses and plant - pathogen interaction. PGPR colonization
brings about many changes in plant development. These changes in-
clude, but are not limited to growth stimulation, modification of root
and shoot architecture, and synthesis of secondary metabolites. As hor-
mones regulate plant growth and development, the effects of coloniza-
tion by PGPR are directly associated with changes in concentration,
localizations and signaling of hormones (Dodd et al., 2010; Spaepen
et al., 2014; Verbon and Liberman, 2016). In this review, we discuss
various ways in which different PGPR strains affect host plant hormone
homeostasis.
It should be noted that many physiological processes in the plant are
regulated by complex interactions between several hormones rather
than by the concentration of some particular hormone (O'Brien and
Benkova, 2013; Naseem et al., 2015). Several recent studies have
examined the complex effect of PGPR on the expression of plant
genes, including the genes that play important roles in signaling, metab-
olism and degradation of phytohormones (Camilios-Neto et al., 2014;
Lara-Chavez et al., 2015). Yet, there is still a lack of comprehensive anal-
ysis of the roles of plant hormones in PGPR - host plant interaction. Here
we review the literature on the role of such phytohormones as auxin,
ethylene, cytokinin, gibberellin, abscisic acid, salicylic acid and jasmonic
acid in the interactions between PGPR and plants.
2. Auxin
Auxin is an important phytohormone that is vital for plant
development and growth. It is required for cell cycle progression
(Demeulenaere and Beeckman, 2014) and for the release of bud dor-
mancy (Rios et al., 2014). It affects the size of the shoot and the root
meristems, defines flower morphogenesis and position of the lateral
organ primordia (Demeulenaere and Beeckman, 2014; Dresselhaus
and Schneitz, 2014; Landrein and Vernoux, 2014). Auxin is necessary
for gravitropism and phototropism of roots and shoots (Retzer et al.,
2014) as well as for shadow avoidance (Ruzza et al., 2014). Auxin can
also modulate plant associations both with pathogenic and symbiotic
microorganisms, coordinating plant responses associated with the es-
tablishment and maintenance of plant – microorganism interactions.
This subject has been well presented in several recent reviews
(Grunewald et al., 2009; Ludwig-Muller, 2014; Liang Pin Ng et al.,
2015; Boivin et al., 2016). Even though auxin research has a long history,
new facts regarding its metabolism, reception and transport as well as
its role within the plant are constantly emerging (Barbez et al., 2012;
Sukumar et al., 2013; de Jong et al., 2014; Kumar et al., 2015; Niu
et al., 2015). Since the majority of physiological processes in the plant
are directly or indirectly associated with this phytohormone, it is not
surprising that PGPR can affect the amount and localization of auxin,
as well as the direction of auxin movement in the plant (Ahmed and
Hasnain, 2014).
There are several locations of auxin synthesis in the plant (Ljung
et al., 2005). The major synthetic activity is localized in the shoot apex
from where auxin flows downwards to the root tip forming a
concentration gradient (Taiz and Zeiger, 2002). Main root (MR) and lat-
eral root (LR) meristems are also sources of auxin (Ljung et al., 2005).
The local maximum concentration is found in the stem cells of the
root meristem (Petersson et al., 2009). After reaching the root tip, the
auxin flow direction is reversed and the hormone reaches the root peri-
cycle. In the zones of the local auxin maximum concentrations, where
the hormone concentration in pericycle reaches the necessary level,
LRs primordia are formed (De Smet et al., 2007). As the MR grows,
primordia leave the initiation zone. If the level of auxin is sufficient,
the primordia develop into LRs and themselves become the sources of
auxin (Ljung et al., 2005; De Smet et al., 2007; Lucas et al., 2008). The
effect of exogenous IAA on the root system of Arabidopsis thaliana
depends on its concentration; in the range of 1.0–5.0 nM it stimulates
the growth of MR and LRs, up to 12.5 nM it inhibits LRs formation and
at 25.0 nM it blocks growth of both the MR and LRs (Ivanchenko et al.,
2010).
How can bacteria affect plant auxin homeostasis? First of all, directly
by synthesizing auxin. There is abundant data indicating that different
PGPR strains synthesize auxin in culture (Spaepen et al., 2007; Ahmed
and Hasnain, 2014). However, the majority of these studies employ a
cheap and accessible Salkowski reaction (Contesto et al., 2010; Iqbal
and Hasnain, 2013) that is designed to estimate the amount of indole
compounds in the solution (in this case, in the culture medium). Since
this reaction is not specific for auxin, one cannot be entirely sure if the
studied strain can indeed synthesize IAA or other biologically active
auxins. In some cases the auxin synthesizing ability of certain PGPB
was demonstrated with more advanced technics, such as GC–MS (Ali
et al., 2009; Ali, 2015), HPLC (Júnior et al., 2011), and biotests
(Tsavkelova et al., 2007). Auxin plays an important role in the establish-
ment and maintenance of beneficial plant – PGPB interaction. For in-
stance, auxin-producing PGPR strains Aeromonas punctata PNS-1,
Serratia marcescens 90–166 and Azospirillum brasilense Sp245 stimulate
growth and induce morphological changes in A. thaliana (Table 1) (Shi
et al., 2010; Iqbal and Hasnain, 2013; Spaepen et al., 2014). In plants in-
oculated with these strains the level of endogenous auxin increases, as
indicated by the elevated expression of DR5-GUS (Tables 2 and 3), a
transgenic construct containing promoters of auxin-induced genes
and the GUS reporter (Shi et al., 2010; Iqbal and Hasnain, 2013;
Spaepen et al., 2014). Moreover, the mutant strain Azospirillum
brasilense FAJ0009, incapable of auxin synthesis, does not induce any
morphological changes in the host plant (Spaepen et al., 2014). At the
same time, the auxin over-producing strain of Burkholderia cepacia
have a greater stimulating effect on rice plants than both control strains
and mutant strains with negligible auxin production (Singh et al., 2013).
This evidence suggests that in these cases auxin synthesis may be the
primary cause of the stimulatory effect of some PGPR strains on host
plants. Interestingly, high concentrations of auxin synthesized by non-
pathogenic strains of rhizobacteria such as Enterobacter sp. I-3 may
have an inhibiting effect on plants (Park et al., 2015). Therefore, to
achieve a stimulating effect on the host plant, the amount of the auxin
produced by the strain should correspond with the optimum for a
given species under given environmental conditions.
Can the PGPB-synthesized auxin be the primary cause underlying in-
creased elongation of the root cells? An increased root growth in PGPR-
colonized plants is routinely explained by the elevated auxin concentra-
tion (Contesto et al., 2010; Shi et al., 2010; Iqbal and Hasnain, 2013;
Poupin et al., 2016). Alternatively, the enhanced root growth may
depend on enhanced loosening of cell walls that accompanies PGPR col-
onization. Partial degradation of cell walls can promote more effective
root colonization by PGPR (Beauregard et al., 2013). Components of
the plant cell wall such as pectins, arabinogalaсtans and xylans are es-
sential for the construction of the matrix exopolysaccharides that aid
PGPR Bacillus sp. biofilm formation (Beauregard et al., 2013). Bacterial
galactosidases split off galactose residues from xylans, pectins,
arabinogalaсtans in the plant cell walls. Galactose is necessary for build-
ing polysaccharides of the biofilm matrix. Therefore, we cannot be
 K.A. Tsukanova et al. / South African Journal of Botany 113 (2017) 91–102 93

Table 1
Morphological changes in the host plant following inoculation with a PGPR strain (↑- increase, ↓- decrease).

Strain Isolated from Host plant Effect on shoot Effect on root Reference
system

Aeromonas punctata PNS-1
Azospirillum brasilense FP2
Azospirillum brasilense
Sp245
Bacillus sp. B55
Bacillus sp. LZR216
Bacillus subtilis GB03
Burkholderia phytofirmans
PsJN
Phyllobacte-rium
brassicacea-rum STM196
Pseudomonas putida
MTCC5279
Serratia marcescens 90–166
Triticum aestivum
Data absent
Data not found
Rhizosphere of transgenic
ethylene-insensitive plant
Nicotiana attenuata 35S:etr1
Roots of Arabidopsis thaliana
Data not found
Roots of Állium sp.
Roots of Brassica napus
Desert soils of Rajastan, India Arabidopsis thaliana Raw mass, shoot branching,
Roots of Cucumis sativus
Arabidopsis thaliana Data absent MR growth↑ Iqbal and Hasnain (2013)
LR formation↑
Length and number of LR↑
Triticum aestivum Data absent Length and raw mass↑ Camilios-Neto et al. (2014)
Arabidopsis thaliana Raw mass↑ MR growth↓ Spaepen et al. (2014)
Number of LR↑
Length and number of RH↑
Nicotiana attenuata Area and number of MR and LR length ↑ Meldau et al. (2012)
leaves, stem length↑
Arabidopsis thaliana Raw mass↑ MR growth↓ J. Wang et al. (2015)
LR growth↑
Arabidopsis thaliana Raw mass↑ Data absent Ryu et al. (2003), Zhang et al.
Number of leaves↑ (2007), Xie et al. (2009)
Number of seeds↑
Arabidopsis thaliana Raw mass↑ MR growth↑ Poupin et al. (2013, 2016)
Life cycle acceleration Number of RH↑
Arabidopsis thaliana Data absent LR growth↑ Contesto et al. (2010), Galland
Length of RH↑ et al. (2012)
Data absent Srivastava et al. (2012)
seed formation↑
Arabidopsis thaliana Data absent MR growth↓ Shi et al. (2010)
LR growth↑

entirely sure if this mechanism is responsible for the partial degradation
of the bonds between cellulose microfibrils, cell wall loosening and,
thus, an increase in the size of the root cells. We can, however, assume
that PGPR may promote root growth, either regardless of the action of
the bacterial auxin or by influencing the level of endogenous plant
auxin. This hypothesis is yet to be tested and supported with the new
evidence.
Exogenous auxin suppresses salicylic acid dependent plant resis-
tance and activates jasmonic acid dependent resistance (Naseem et al.,
2015). Importantly, salicylic acid dependent plant resistance is aimed
against biotrophic pathogens (Yang et al., 2015). Since PGPR can have
both beneficial and detrimental effects on the plant depending on
their amount and ambient conditions (Partida-Martinez and Heil,
2011), the plant may perceive them as weak biotrophic pathogens.
The synthesis of bacterial auxin by PGPR may be part of the strategy
for suppressing the host plant resistance for a more successful coloniza-
tion. Thus, the ability to synthesize auxin, and the amount of synthe-
sized auxin are important characteristics of a PGPR strain, as it can
determine the strain's impact on the plant to a great extent.
PGPR can also affect expression of the plant genes that are part of
auxin synthesis, transport or signaling machinery. In the plants inocu-
lated with the PGPR strains Phyllobacterium brassicacearum STM196
and Bacillus sp. LZR216 (Table 1) the expression of IAA synthesis genes
increases and so does the amount of endogenous IAA in the MR
(Table 2) (Contesto et al., 2010; J. Wang et al., 2015). PGPR Burkholderia
phytofirmans PsJN (Table 1) colonization causes an increase in the ex-
pression of the Arabidopsis genes responsible for the synthesis of trypto-
phan - the IAA precursor, which should result in an increased auxin
synthesis. However, the colonization also causes a decrease in the ex-
pression of the auxin synthesis gene, TAA1 (Table 2) (Poupin et al.,
2016). It is likely the reason why auxin levels in the shoots of colonized
plants are lower (Su et al., 2016). Interestingly, B. phytofirmans PsJN
itself can synthesize auxin (Weilharter et al., 2011).
PGPR сan affect auxin transport by altering activity of auxin influx
and efflux carriers. For instance, PGPR Bacillus sp. LZR216 decreases syn-
thesis of auxin transporters AUX1 and PIN1, 2 and 3 (J. Wang et al.,
2015), while PGPR B. phytofirmans PsJN increases the expression of
PIN2 and PIN3 (Poupin et al., 2016). Interestingly, pin2 mutation de-
creases the growth stimulating effect of both B. phytofirmans PsJN and
Bacillus sp. LZR216 (Table 2).
PGPR can modify host plants' auxin concentration not only by syn-
thesizing it but also by degrading it. For instance, PGPR Pseudomonas
putida 1290 can utilize IAA as a nutritive substrate, thus eliminating
the inhibiting effect of high levels of exogenous IAA on the plant. Both
extracellular application of IAA and IAA-producing strains were used
as a source of exogenous IAA (Leveau and Lindow, 2005). Furthermore,
a PGPR B. phytofirmans PsJN is also capable of degrading IAA. The mutant
strain B. phytofirmans iacC, incapable of IAA degradation, does not re-
duce the inhibiting effect of high levels of exogenous auxin on
A. thaliana plants. Besides, the mutant strain, in contrast to the wild
type B. phytofirmans PsJN, does not increase the plant biomass and the
length of the MR, indicating that this strain's ability to degrade IAA is in-
dispensable for the host plant's growth promotion (Zuniga et al., 2013).
The location of PGPR colonization sites on the root may also be an
important factor. If auxin-producing bacteria actively colonize MR or
LR elongation zone or the zone of LRs formation, the auxin levels in
these areas may locally increase. This is likely to affect the architecture
of the developing root system. Therefore, there is evidence of different
PGPR strains retaining different mechanisms of affecting auxin homeo-
stasis in the host plant.
Some PGPR can synthesize substances with auxin-like activity.
Cyclopeptides were identified in the culture medium of the mutant
PGPR strains Pseudomonas aeruginosa lasI and P. aeruginosa rhlI/lasI de-
ficient in genes that are part of N-acyl-L-homoserine lactone signaling
mechanism. These compounds, yet in smaller amounts, were identified
in the culture medium of the wild type strain (Ortiz-Castro et al., 2011).
Cyclopeptides have a weak auxin-like activity. Mutant strains lasI and
rhlI/lasI had a stronger stimulating effect on A. thaliana than the wild
type P. aeruginosa, enhancing LRs formation and stimulating growth of
the MR. Cyclopeptides stimulate the expression of auxin-induced
marker constructs DR5:uidA and BA3:uidA and also cause degradation
of Aux/IAA, the repressor of auxin-dependent genes, enhancing auxin
signal transduction. This is supported by the fact that auxin receptor
mutants show a decreased response to bacterial cyclopeptides (Ortiz-
Castro et al., 2011). Indole produced by E. coli, Pseudomonas sp. and
Burkholderia sp. as well as pharmacological indole at low concentra-
tions, all have an auxin-like effect on Arabidopsis thaliana, resulting in
an increased formation of LR and an increased shoot biomass. A small
fraction of the indole, that is taken up by the plant, can be converted
into IAA. Interestingly, indole at higher concentrations can act as an
 94
Table 2
Changes in the expression of host plant genes and host plant mutations after inoculation with a PGPR strain (↑- gene expression increased, ↓- gene expression decreased, (+) – capable of producing the substance, (−) – incapable of producing the
substance, d.a.- data absent, CK – cytokinin; GA – gibberellin; JA – jasmonic acid; Et – ethylene).

Strain, host plant Hormone Ability to produce Change in the gene expression or the reaction of mutant plants in phytohormone-associated genes Change the amount Reference
affected phytohormone and/or of phytohormone
Synthesis and Reception Transport Phytohormone-induced
substance affecting
metabolism genes
phytohormone homeostasis

Aeromonas punctata IAA IAA (+) d.a. d.a. d.a. In the root of DR5-GUS↑ d.a. Iqbal and Hasnain (2013)
PNS-1, A. thaliana
Azospirillum brasilense IAA IAA (d.a.) d.a. d. d.a.a. d.a. ETTIN/ARF3, AuxRec ↓ d.a. Camilios-Neto et al. (2014)
FP2, Triticum aestivum Et ACC-deaminase (d.a.) ACO↓ d.a. d.a. d.a. d.a.
Azospirillum brasilense IAA IAA (+) NIT1, NIT2↓ d.a. d.a. In the root of DR5-GUS↑ d.a. Spaepen et al. (2014)
Sp245, A. thaliana GH3.2, GH3.3, GH3.4,
GH3.5, GH3.12↑
Bacillus megaterium CK Cytokinins d.a. Stimulation decreased in d.a. d.a. d.a. Lopez-Bucio et al. (2007),

K.A. Tsukanova et al. / South African Journal of Botany 113 (2017) 91–102
UMCV1, A. thaliana (d.a.) rpn12a-1, ahk2–2tk, Ortiz-Castro et al. (2008)
cre1–12/ahk2–2tk,
ahk2–2tk/ahk3 mutants
Bacillus sp. LZR216, IAA IAA (d.a.) NIT1, TAA1, and d.a. PIN1-GFP, PIN2-GFP, In the root of DR5-GUS↑ d.a. J. Wang et al. (2015)
A. thaliana YUCCA1↑ PIN3-GFP, AUX1-YFP↓
Stimulation decreased in
aux1–7 and pin2 mutants
Bacillus subtilis GB03, IAA 3,4-Butanediol, acetoin (+) TSB2, ASA1, IAR3↑ NIT1 d.a. PILS5↓ DR5-GUS in roots ↓, d.a. Zhang et al. (2007)
A. thaliana and NIT2 in shoots↑ in shoots ↑
NIT1 in roots↓ SAUR↑
Bacillus subtilis SYST2, IAA VOCs (+) SlIAA3↑ in leaves d.a. d.a. d.a. IAA↑ Tahir et al. (2017)
Solanum lycopersicum SlIAA1↑ in root
Et ACO-1↓ in root and d.a. d.a. d.a. Et↓
leaves
CK SlCKX1 ↑ in root d.a. d.a. d.a. CK↑
GA 20ox-1 ↑ in leaves d.a. d.a. d.a. GA↑
Burkholderia IAA IAA (+) ASA1 and ASB1↑ 7–9-day-old AFB1–3↓ PIN2, PIN3↑ d.a. IAA in leaves Poupin et al. (2016), Su
phytofirmans PsJN, TAA1↓ 19-day-old AFB1, AFB3↑ PILS3↓ decreased 6 weeks et al. (2016), Zuniga et al.
A. thaliana Stimulation decreased in Stimulation decreased in after inoculation (2013)
iaa1 mutant. eir1–1/pin2 mutant
In tir1, afb1, afb2, afb3
stimulation absent except
for an increase in the
number of RH
Et ACC-deaminase (+) ACS5 and ACO1, ACO2↑ d.a. d.a. d.a. d.a. Poupin et al. (2016)
Lara-Chavez et al. (2015)
GA Gibberellins (−) AtGA3ox1↑ d.a. d.a. d.a. d.a. Poupin et al. (2013)
JA Jasmonic acid (d.a.) LOX2↓ d.a. d.a. d.a. d.a. Pinedo et al. (2015)
Phyllobacterium IAA IAA (+) very inconsiderably In shoots of ASA1, ASB1, Stimulation absent in axr1 Stimulation absent in aux1 In the root of DR5-GUS↑ Inconsiderably more Contesto et al. (2010)
brassicacearum CYP79B2, SUR1, mutant mutant in shoots, less in roots.
STM196, A. thaliana CYP83B1↑
Et ACC- ACS7, ACS11↑ Galland et al. (2012)
deaminase (+)
Pseudomonas putida IAA IAA (d.a.) d.a. d.a. d.a. SAUR9↑ d.a. Srivastava et al. (2012)
MTCC5279, Et ACC-deaminase (d.a.) d.a. d.a. d.a. ERF13 -transcription d.a.
A. thaliana factor↓
JA Jasmonic acid (d.a.) JAR1↑ d.a. d.a. d.a. d.a.
Serratia marcescens IAA IAA (+) d.a. d.a. d.a. In the root of DR5-GUS↑ d.a. Shi et al. (2010)
90–166, A. thaliana
 K.A. Tsukanova et al. / South African Journal of Botany 113 (2017) 91–102 95

Table 3
Functions of genes listed in Table 2.

Gene or transgenic construct Gene products

ACO1,2 1-aminocyclopropane-1-carboxylate oxidase, enzyme of ethylene biosynthetic process

ACS5,7,11 1-aminocyclopropane-1-carboxylate, enzyme of ethylene biosynthetic process
AFB1–3 Auxins receptors
AHK2–2 Cytokinin receptor
AHK3 Cytokinin receptor
ASA1, ASB1 Subunits of anthranilate synthase enzyme, tryptophan pathway enzyme and IAA enzyme
AtGA3ox1 Enzyme of gibberellic acid biosynthetic pathway
AUX1 Influx channel of auxin into the cell
AuxRec Auxin receptor in Triticum aestivum
AXR1 Subunit of enzyme involved in regulation of response to auxin
CRE1–12 Cytokinin receptor
CYP79B2 Enzyme transforming tryptophan into indole-3-acetaldoxime, precursor of indole-glucosinolates and IAA
CYP83B1 Enzyme, transforming indole-3-acetaldoxime into indole-3- acetaldoxime N-oxide, precursor of indole-glucosinolates and IAA
ETTIN/ARF3 Transcription factor regulating expression of auxin induced genes
GH3.2, GH3.3, GH3.4, GH3.5, GH3.12 Enzymes forming IAA conjugates
IAR3 Enzyme hydrolysing conjugates of IAA and amino acids
JAR1 Enzyme of jasmonyl-isoleucine (JA-Ile) conjugate formation
LOX2 Enzyme required for wound-induced jasmonic acid accumulation in Arabidopsis
NIT1 and NIT2 Enzymes transforming indole-3-acetonitril into IAA
PILS3,5 Efflux channels of auxin localized on endoplasmic reticulum membranes
PIN1,2,3 Efflux channels of auxin into the cell
RPN12a-1 The mutant form of the protein which can modulate of the 26S proteasome important for cytokinin regulated growth responses
SAUR Proteins with various functions encoded by a group of auxin-induced genes
SlCKX1 Enzyme of cytokinin biosynthetic pathway in tomato plants
SlIAA3, SlIAA1 Enzyme of auxin biosynthetic pathway in tomato plants
SUR1 Enzyme whose action results in indole-3-thiohydroximate, precursor of indole- glucosinolates and IAA
TAA1 Enzyme of indole-3-pyruvate pathway of IAA synthesis
TIR1 Auxins receptors
TSB2 Subunit of tryptophan-synthase enzyme
YUCCA1 Enzyme of indole-3-pyruvate pathway of IAA synthesis
20ox-1 Enzyme of gibberellic acid biosynthetic pathway in tomato plants

auxin antagonist (Bailly et al., 2014). It is noteworthy that in the studies
where auxin in the bacterial culture medium was identified with the
help of the Salkowski reaction, the action of indole as well as of bacterial
auxin was characterized.
Some biologically active substances produced by PGPR do not have
auxin-like activity but still can affect plant auxin homeostasis. The
stimulatory effect of the PGPR strains Bacillus subtilis GB03 and
B. amyloliquefaciens IN937a grown on in vitro A. thaliana, depends on
the synthesis of the volatile compounds acetoin and 3,4-butanediol
(Table 1) (Ryu et al., 2003). Both acetoin and 3,4-butanediol enhance
expression of auxin synthesis genes and elevate endogenous auxin con-
centration in the shoots, while reducing it in the roots of A. thaliana
(Table 2). 3,4-Butanediol and acetoin can also affect the expression of
IAA transporter genes and auxin-induced genes (Zhang et al., 2007).
Bacillus subtilis SYST2 emits organic volatiles albuterol and 1,3-
propanediol, which stimulate tomato plant growth. These organic vola-
tiles cause the enhanced expression of auxin synthesis genes (SlIAA3 и
SlIAA1) and increased endogenous auxin content in tomato plants
(Tahir et al., 2017) (Table 2).
To summarize, PGPR may influence plant auxin homeostasis by var-
ious mechanisms depending on the strain. Understanding the charac-
teristic features of each PGPR strain is essential for its successful use in
agriculture.
3. Ethylene
Ethylene is an important natural plant hormone that is involved in a
number of physiological processes; functioning of apical meristems of
the root and the shoot, root and root hair growth (Vandenbussche
and Van Der Straeten, 2012), development of the “triple response” in
etiolated seedlings (swelling of hypocotyl, root shortening and the ex-
aggeration in the curvature of the apical hook) (Van de Poel et al.,
2015), fruit ripening (Liu et al., 2015), leaf senescence, formation of
stomata, gravitropism (Vandenbussche and Van Der Straeten, 2012)
and response to biotic and abiotic stresses (Song and Liu, 2015; Tao
et al., 2015; Verma et al., 2016). A change in the level of ethylene caused
by PGPR can affect root system development. For instance, low levels of
ACC, the ethylene precursor (ca. 0.04 μM ACC in the medium), stimulate
the formation of LR primordia, slightly higher levels inhibit MR growth
and the formation of primordia while stimulating the development of
initiated primordia into LRs and ACC concentrations from 1 to 5 μM in-
hibit root growth (Ivanchenko et al., 2008). Increased levels of ethylene
also stimulate RH growth as well as RH formation on atrichoblasts, on
which they normally do not form (Dolan, 2001). Ethylene can both in-
hibit and stimulate plant growth, depending on the plant species and
hormone concentration (Vandenbussche and Van Der Straeten, 2012).
PGPR can influence plant ethylene homeostasis by affecting
expression of the genes encoding the ethylene synthesis enzymes,
ACC-synthase and ACC-oxidase. For instance, PGPR Burkholderia
phytofirmans PsJN increases the expression of ACS and ACO genes
in A. thaliana (ACS5, ACO1, ACO2) (Poupin et al., 2016) and
Panicum virgatum (Lara-Chavez et al., 2015) (Table 2), while PGPR
Phyllobacterium brassicacearum STM196 increases the expression
of ACS7 and ACS11 gene in A. thaliana (Galland et al., 2012) (Table 2).
Interestingly, the inoculation of the A. thaliana plants with the
P. brassicacearum STM196 strain results in an enhanced elongation of
RHs, however, this effect was only partially dependent on the ethylene
signaling pathway (Galland et al., 2012).
An enhanced expression of the ethylene synthesis genes is likely as-
sociated with the host plant response to the PGPR colonization: the
plant may perceive it as a biotic stress (Partida-Martinez and Heil,
2011; Lakshmanan et al., 2013; Spaepen et al., 2014). For example,
PGPR Bacillus cereus AR156, which can induce Pseudomonas syringae
pv. tomato DC3000 infection resistance in A. thaliana plants and
cause accumulation of a small amount of transcripts of PR1,2,5
(pathogenesis-related) genes (which is characteristic of SAR) and
PDF1.2 encoding defensin 1.2 protein (which is characteristic of ISR)
(Niu et al., 2011). High concentrations of PGPR suspensions can inhibit
plant growth. For instance, P. thivervalensis (growth-stimulating,
auxin-producing strain) stimulates root growth in A. thaliana at cell
96 K.A. Tsukanova et al. / South African Journal of Botany 113 (2017) 91–102
count of 105 CFU/ml and inhibits it at cell count of 106 CFU/ml (Persello-
Cartieaux et al., 2001). An increased ethylene synthesis may be a part of
the plant defense response to PGPR colonization. Another possible rea-
son for an increased amount of ethylene may be the bacteria-
synthesized auxin, which can stimulate the plant ACC-synthase
(Ruzicka et al., 2007). PGPR also can affect the expression of the
ethylene-induced genes. For instance, inoculation of A. thaliana with
PGPR P. putida MTCC5279 (Table 1) inhibits expression of ERF13 - tran-
scription factor that is part of the ethylene signal transduction chain
(Srivastava et al., 2012) (Table 2).
On the other hand, PGPR can decrease the amount of ethylene in
plant tissues. Inoculation of wheat plants with the PGPR strain
Azospirillum brasilense FP2 (Table 1) resulted in a drop in the expression
of the plant ACC-oxidase (Camilios-Neto et al., 2014) (Table 2). Organic
volatiles emitted by Bacillus subtilis SYST2 inhibit expression of ACO-1
gene and cause a decrease in endogenous ethylene content in tomato
(Tahir et al., 2017) (Table 2).
Many PGPR can express ACC-deaminase and lower the amount of
ethylene in the plant by degrading ACC, the ethylene precursor (Singh
et al., 2015). For example, PGPR strain Variovorax paradoxus 5C-2, that
has ACC-deaminase activity, stimulates growth of the wild type plants
of A. thaliana and of the eto1.1 mutant (ethylene overproducing) while
decreasing both the amount of ACC in the leaves and the plant ethylene
synthesis (Chen et al., 2013). ACC-deaminase gene is present in some
strains of Azospirillum, Rhizobium, Agrobacterium, Achromobacter,
Burkholderia, Ralstonia, Pseudomonas and Enterobacter (Gamalero and
Glick, 2015). PGPR strains with ACC-deaminase activity are known to
mitigate damaging effects of abiotic stresses such as high salinity, soil
pollution with heavy metals and organic pollutants, flooding, drought
and mineral deficiency on plant growth and development (Saleem
et al., 2007; Gontia-Mishra et al., 2014). Inoculation of legume plants
with PGPR strains with ACC-deaminase activity promoted nodule
formation and the establishment of legume-rhizobium symbiosis
(Shaharoona et al., 2006).
Interestingly, following inoculation of A. thaliana plants with PGPR
strains Phyllobacterium brassicacearum STM196, Pseudomonas putida
UW4, Rhizobium leguminosarum bv. viciae 128C53K and Mesorhizobium
loti MAFF303099, a positive influence on RH length is noted both in the
case of the wild type strains with ACC-deaminase activity and in
the case of the AcdS-deficient mutants (AcdS gene encodes ACC-
deaminase). Moreover, AcdS−-strains had a stronger stimulatory effect
on RH growth than the wild type strains. Besides, inoculation of
A. thaliana plants with the mutant strain Pseudomonas putida UW4
AcdS− results in a statistically significant increase in the LR number as
compared with the LR number after inoculation with the wild type
strain (Contesto et al., 2008). Remarkably, inoculation A. thaliana with
PGPR Aeromonas punctata PNS-1 strain that possesses ACC-deaminase
activity stimulate RHs development (Iqbal and Hasnain, 2013), suggest-
ing that ethylene levels in colonized plants do not decrease to the pre-
colonization level.
In summary, different PGPR strains can affect the level of ethylene in
the plant, increasing or decreasing its concentration. For an efficient ap-
plication of PGPR in agriculture, it is necessary to understand the molec-
ular mechanisms through which the strain affects the ethylene levels in
the plant under various conditions.
4. Cytokinins
Cytokinins are the foremost class of plant hormones represented by
a group of N6-substituted adenine derivatives. Cytokinins are involved
in various aspects of plant's life. In particular, they are obligatory for
the cell cycle progression (Schaller et al., 2014). The balance of auxin
and cytokinin determines meristem functioning, root system architec-
ture, formation of lateral organs of the shoot and development of gener-
ative organs (Schaller et al., 2015). Cytokinins regulate chlorophyll
biosynthesis and chloroplast biogenesis (Cortleven and Schmulling,
2015). They are also involved in the development of plant resistance
to biotic and abiotic stresses (Grosskinsky et al., 2011; O'Brien and
Benkova, 2013). Different cytokinins have separate roles in plant phys-
iology. The role of the cis-zeatin-type cytokinins has been in the focus
recently since they show a weak activity in classical biotests, in contrast
to cytokinins of the trans-zeatin type. However, cis-zeatin-type cytoki-
nins play an important role in the signaling associated with dormancy,
growth inhibition and transition to senescence (Schafer et al., 2015).
It has been confirmed that PGPR can influence plant cytokinin con-
centration. Many PGPR strains can synthesize cytokinin (Table 4)
(Arshad and Frankenberger, 1991; Glick, 2012). Platycladus orientalis
plants inoculated with a cytokinin-producing PGPR strain Bacillus
subtilis (AE016877) (Table 4) have an increased level of cytokinin in
the shoots (Liu et al., 2013). PGPR Pseudomonas fluorescens 6–8
(Table 4), capable of cytokinin synthesis, increases the levels of
zeatin riboside and isopentenyl riboside and decreases the level of
dihydrozeatin riboside in the rhizosphere of Brassica napus (Pallai
et al., 2012). However, after the inoculation of A. thaliana plants with a
cytokinin-producing PGPR strain Pseudomonas fluorescens G20–18
(Table 4) the total concentration of all cytokinins in the leaves did not
change significantly even though the amount of cis-zeatin increased
(Grosskinsky et al., 2016). At the same time, the level of zeatin in the
leaves increased after inoculation of A. thaliana plants with a PGPR strain
Burkholderia phytofirmans PsJN, for which cytokinin-synthesizing ability
has not been demonstrated (Su et al., 2016). Expression of cytokinin
synthesis gene SlCKX1 and cytokinin content is enhanced in
tomato plants exposed to organic volatiles emitted by PGPR Bacillus
subtilis SYST2 (Tahir et al., 2017) (Table 2). This data suggests that dif-
ferent PGPR employ different mechanisms to change plant cytokinin
concentration.
PGPR strains capable of cytokinin synthesis can stimulate host plant
shoot growth and fruit formation (Barea and Brown, 1974; Azcon and
Barea, 1975; Liu et al., 2013). PGPR Bacillus megaterium UMCV1 stimu-
lated the growth of LRs in Arabidopsis thaliana, and while cytokinin re-
ceptor genes AHK2 and RPN12 are involved in the mechanism of this
stimulation, the genes that are involved in reception and transport of
auxin and ethylene (AUX1–7, AXR4–1, EIR1, ETR1, EIN2, and RHD6) are
not (Lopez-Bucio et al., 2007; Ortiz-Castro et al., 2008) (Table 2).
Cytokinin-producing PGPR strain Pseudomonas fluorescens 6–8
(Table 4) stimulated MR growth and inhibited LR formation in Brassica
napus (however, a minimal amount of IAA was also found in the culture
media of this strain, which confounds the data interpretation) (Pallai
et al., 2012).
Bacterial cytokinins also promote plant resistance to biotic and abi-
otic stresses. For instance, PGPR Pseudomonas fluorescens G20–18
needs its ability to synthesize cytokinin (Table 4) to improve the resis-
tance of A. thaliana plants to infection with Pseudomonas syringae,
since the mutant Pseudomonas fluorescens G20–18, incapable of
cytokinin synthesis does not affect the plant resistance (Grosskinsky
et al., 2016). Platycladus orientalis plants inoculated with cytokinin-
producing PGPR Bacillus subtilis (AE016877) (Table 4) are more resis-
tant to drought (Liu et al., 2013). In summary, PGPR strains' ability to
synthesize cytokinins or to alter plant cytokinin homeostasis is crucially
important for the understanding of mechanisms of PGPR-dependent
growth stimulation and increased resistance to biotic and abiotic
stresses.
5. Gibberellins
Gibberellins are a group of hormones that perform various functions
in the plant organism. They are the key regulators of reproductive organ
formation and development and ripening of fruit and viable seeds
(Plackett and Wilson, 2016). Gibberellins can both stimulate seed
germination, and suppress it at high temperatures (Urbanova and
Leubner-Metzger, 2016). They positively regulate cell division and elon-
gation, stimulating hypocotyl and stem growth and have a positive
 K.A. Tsukanova et al. / South African Journal of Botany 113 (2017) 91–102 97

Table 4
Cytokinins found in the culture medium of PGPR strains.

PGPR strain Cytokinins in the culture medium Reference

Azotobacter Substances with cytokinin activity Barea and Brown (1974)

paspali
Azotobacter vinelandii, Azotobacter beijerinckii Substances with cytokinin activity Azcon and Barea (1975)
Bacillus subtilis (AE016877) Trans-zeatin Liu et al. (2013)
Pseudomonas fluorescens 6–8 Zeatin riboside, isopentenyl riboside, dihydrozeatin riboside Pallai et al. (2012)
Pseudomonas fluorescens G20–18 Trans-zeatin riboside, dihydrozeatin riboside, isopentenyl adenosine Garcia de Salamone et al. (2001)
Pseudomonas putida G8–32, Dihydrozeatin riboside Garcia de Salamone et al. (2001)
Pseudomonas putida GR12–2,
Pseudomonas chlororaphis 63–28,
Burkholderia cepacia Ral–3
Pseudomonas sp. PN-4-SAN, PN-10-SAN, AN-2-NAG, AN-4-NAG Cytokinins (no definite compounds identified) Kapoor and Kaur (2016)

effect on leaf size and root meristem size (Martinez et al., 2016). Exog-
enous gibberellin can stimulate shoot growth and xylem development
(Guo et al., 2015; G.L. Wang et al., 2015) and inhibit root growth (G.L.
Wang et al., 2015). A component of the gibberellin signaling system,
the DELLA repressor of gibberellin-induced genes, is the key factor of
plant growth inhibition under stress (Magome and Kamiya, 2016;
Martinez et al., 2016).
PGPR can influence the amount of endogenous gibberellin in plants,
in a fashion similar to other hormones. For example, some PGPR strains
can synthesize gibberellins (Table 5) (Bottini et al., 2004). After inocula-
tion of plants with gibberellin-producing PGPR strains Bacillus cereus
MJ-1 (Joo et al., 2005) and Promicromonospora sp. SE188 the amount
of endogenous gibberellins in the shoots of host plants increases
(Kang et al., 2014) (Table 5). Gibberellin-producing PGPR Leifsonia soli
SE134 and Enterococcus faecium LKE12 (Table 5) stimulate shoot growth
in mutant rice plants deficient in gibberellin synthesis. This shows that
these strains compensate for the absence of plant gibberellins with
added bacterial gibberellins (Kang et al., 2014; Lee et al., 2015). Besides,
PGPR can stimulate the synthesis of the plant's own gibberellins. Inocu-
lation with gibberellin-producing PGPR strains of Promicromonospora
sp. SE188 and Bacillus amyloliquefaciens RWL-1 results in an increased
amount of gibberellins in the plant, including those absent in the culture
media of these strains (Kang et al., 2014; Shahzad et al., 2016). PGPR
strain Burkholderia phytofirmans PsJN, which does not synthesize gib-
berellins, stimulates the expression of AtGA3ox1 gene encoding the en-
zyme of one of the final stages of gibberellin synthesis in A. thaliana
(Poupin et al., 2013) (Table 2). GExpression of gibberellin synthesis
gene 20ox-1 and gibberellin content are enhanced in plants that have
been exposed to the organic volatiles emitted by PGPR Bacillus subtilis
SYST2 (Tahir et al., 2017) (Table 2). To summarize, PGPR-related in-
crease the gibberellin levels in the plant, is an existing mechanism of
plant growth stimulation.
6. Abscisic acid
Abscisic acid (ABA) is the plant hormone that is synthesized in re-
sponse to abiotic stresses (drought, cold, salt stress, soil pollution) and
activates the genes responsible for stress resistance (Sah et al., 2016).
It inhibits seed germination, induces plant senescence and abscission
of leaves and fruits, promotes stomatal closure and affects the root sys-
tem architecture (Munemasa et al., 2015; Sah et al., 2016).
Several PGPR strains can synthesize ABA (Table 6) (Sgroy et al.,
2009; Salomon et al., 2014; Cohen et al., 2015). When plants are inocu-
lated with ABA-producing strains such as Bacillus licheniformis Rt4M10,
Pseudomonas fluorescens Rt6M10, Azospirillum brasilense Sp 245
(Table 6), the internal ABA content increases, and the plant becomes
more resistant to drought (Salomon et al., 2014; Cohen et al., 2015).
On the other hand, some PGPR strains can break down ABA. For in-
stance, plants inoculated with PGPR strains Rhodococcus sp. P1Y and
Novosphingobium sp. P6W (Table 6), which can degrade ABA, have
shown a decrease in shoot ABA levels (Belimov et al., 2014). However,
PGPR strain Variovorax paradoxus 5C-2 (Table 6), which cannot break
down ABA, also decreased ABA levels in host plants (Jiang et al.,
2012). Since all of the above-mentioned strains stimulate plant growth
irrespective of their effect on the ABA content in plant tissues, it cannot
be ruled out that other, ABA - independent mechanisms are used by
these PGPR for plant growth stimulation.
Inoculation with a PGPR strain Azospirillum lipoferum USA 59b
(Table 6) increases the amount of ABA in plant tissues (Cohen et al.,
2009). Interestingly, however, if inoculated plants were treated with
an inhibitor of gibberellin synthesis, the amount of ABA decreased as
compared with non-inoculated plants (Cohen et al., 2009). Considering
that gibberellins are ABA antagonists in numerous physiological pro-
cesses, this suggests that Azospirillum lipoferum USA 59b is involved
not only in increasing the level of ABA, but also in its stabilization.
Some PGPR can synthesize several phytohormones (Dodd et al.,
2010). These phytohormones can be antagonistic, playing opposite
roles in the life of plants. For instance, Bacillus licheniformis Rt4M10
and Pseudomonas fluorescens Rt6M10 (Salomon et al., 2014) and a num-
ber of strains isolated from the halophyte Prosopis strombulifera (Sgroy
et al., 2009) synthesize both ABA and hormones that are ABA antago-
nists, such as gibberellins and cytokinins. It is unclear how the balance
between the hormones synthesized by PGPR is maintained during colo-
nization. Therefore, it is difficult to predict the effects of the particular

Table 5
PGPR strains with physiologically active gibberellins found in the culture medium (↑- increase, ↓- decrease).

Strain Isolated from Host plant used in the experiment Morphological changes in the host plant Reference

Acinetobacter calcoaceticus SE370 Soil Cucumis sativus, Brassica rapa subsp. Mass and length of shoot and root↑ Kang et al. (2009)
pekinensis, Glebionis coronaria
Bacillus amyloliquefaciens RWL-1 Seeds of Oryza sativa Oryza sativa Mass and length of shoot and root↑ Shahzad et al. (2016)
Bacillus cereus MJ-1 Rhizosphere Capsicum annuum Mass and length of shoot and root↑ Joo et al. (2004)
Bacillus macroides CJ-29 Rhizosphere Capsicum annuum Mass and length of shoot and root↑ Joo et al. (2004)
Bacillus pumilus CJ-69 Rhizosphere Capsicum annuum Mass and length of shoot and root↑ Joo et al. (2004)
Burkholderia sp. KCTC 11096BP Soil Cucumis sativus, Glebionis coronaria Mass and length of shoot and root↑ Joo et al. (2009)
Enterococcus faecium LKE12 Soil Oryza sativa Mass and length of shoot ↑ Lee et al. (2015)
Leifsonia soli SE134 Soil Solánum lycopérsicum Mass and length of shoot↑ Kang et al. (2014)
Promicromonospora sp. SE188 Soil Solánum lycopérsicum Mass and length of shoot↑ Kang et al. (2012)
98 K.A. Tsukanova et al. / South African Journal of Botany 113 (2017) 91–102

Table 6
PGPR effect on the amount of ABA in the plant and on morphological and physiological changes in the plant after inoculation (↑- increase, ↓- decrease).

Strain Isolated from Ability to synthesize Host plant in the Effect of the strain Morphological and physiological Reference
or degrade ABA experiment on ABA level in changes in host plant after
in vitro the plant inoculation

Azospirillum brasilense Data not found Synthesis - yes Arabidopsis thaliana In shoots ↑ Mass of shoots and roots↑ Cohen et al. (2008, 2015)
Sp 245 Number of LR↑
Stomatal conductance↓
Photosynthesis pigments ↑
Resistance to drought ↑
Azospirillum lipoferum Data not found Data absent Zéa máys In shoots↑ Mass of shoots and roots↑ Cohen et al. (2009)
USA 59b Length of shoot, area of leaves↑
Resistance to drought↑
Bacillus licheniformis Rhizosphere of Synthesis - yes Vitis vinifera In shoots ↑ Length of shoot and root, Salomon et al. (2014)
Rt4M10 Vitis vinifera area of leaves↑
Resistance to drought ↑
Novosphingobium sp. Rhizosphere of Degradation - yes Oryza sativa and In shoots↓ MR length ↑ Belimov et al. (2014)
P6W Oryza sativa Solánum lycopérsicum
Pseudomonas fluorescens Rhizosphere of Synthesis - yes Vitis vinifera In shoots ↑ Length of shoot and root, Salomon et al. (2014)
Rt6M10 Vitis vinifera area of leaves↑
Resistance to drought ↑
Rhodococcus sp. P1Y Rhizosphere of Degradation - yes Oryza sativa and In shoots↓ MR length↓ Belimov et al. (2014)
Oryza sativa Solánum lycopérsicum Number of LR↑
Variovorax paradoxus Rhizosphere of Synthesis - no, Pisum sativum In shoots and Mass of shoots and roots↑ Jiang et al. (2012)
5C-2 Brassica juncea degradation - no roots↓ Stomatal conductance↑
L. Czern. In phloem↑

strain on the plant. This is likely to depend both on the plant species and
on the environmental factors. Besides, the normal level of endogenous
ABA in plants may be necessary for the manifestation of the stimulation
effect of the PGPR strain on the plant. For instance, Bacillus megaterium
stimulates growth of Solánum lycopérsicum wild type but inhibits
growth of ABA-synthesis deficient mutants (Porcel et al., 2014).
Thus, PGPR can affect the level ABA in the plant, in this way influenc-
ing its growth and abiotic stress resistance. Unfortunately, no data on
the effect of PGPB on plant ABA signal transduction components is cur-
rently available.
7. Salicylic acid and Jasmonic acid
Plants possess systemic resistance of two major types: SAR (systemic
acquired resistance) associated with the signaling pathways of salicylate
and ethylene; and ISR (induced systemic resistance) associated with the
signaling pathways of jasmonate and ethylene (Van der Ent et al., 2009).
SAR is characterized with the hypersensitive response at the site of the
attack and with the accumulation of pathogen-related proteins (PR-pro-
teins) in other parts of the plant, cell wall remodeling and the build-up
of defense compounds (Yang et al., 2015). ISR is accompanied by the
accumulation of specific proteins, an increase in callose and phenolic
compounds content in the cell wall and an increased synthesis of
phytoalexins (Okada et al., 2015). Jasmonic acid is also involved in the
development of abiotic stress resistance (Ahmad et al., 2016). SAR typi-
cally develops in response to the attack of biotrophic pathogens while
ISR develops in response to necrotrophic ones. Numerous data also indi-
cate that the signaling pathways of salicylic acid and jasmonic acid are
antagonistic (Yang et al., 2015).
Several endophytic PGPB synthesize jasmonic acid and salicylic acid
(Forchetti et al., 2007; Chen et al., 2014). Inoculation of host plants
with PGPR strains Pseudomonas fluorescens Pf4 and P. aeruginosa Pag
(Singh et al., 2003), Bacillus amyloliquefaciens LJ02 (Li et al., 2015)
(Table 7), resulted in a rise of the endogenous level of salicylic acid in
various parts of plants. Burkholderia phytofirmans PsJN causes the
accumulation of salicylic acid in the cell culture of Vitis vinifera
(Bordiec et al., 2011). Interestingly, inoculation with gibberellin-
producing strains Promicromonospora sp. SE188 (Kang et al., 2012)
and Bacillus amyloliquefaciens RWL-1 (Shahzad et al., 2016) (Table 5)
also resulted in an increased level of salicylic acid in plant tissues.
Pseudomonas putida MTCC5279 (Table 1) increases the expression of
jasmonate-isoleucine conjugate synthesis gene JAR1 in A. thaliana plants
(Srivastava et al., 2012), while Burkholderia phytofirmans PsJN, on the
contrary, decreases the expression the gene responsible for jasmonic
acid synthesis and wound-induced jasmonic acid accumulation LOX2
in A. thaliana (Pinedo et al., 2015) (Table 2).

Table 7
Type of resistance developing in the host plant after inoculation with a PGPR strain and a pathogenic microorganism.

PGPR strain Host plant in the Pathogen Type of resistance in host Reference
experiment plant

Bacillus amyloliquefaciens LJ02 Cucumis sativus Sphaerotheca fuliginea SAR Li et al. (2015)
Bacillus cereus AR156 Arabidopsis thaliana Pseudomonas syringae pv. ISR, SAR Niu et al. (2011, 2016)
tomato DC3000
Bacillus pumilus SE34, Pseudomonas fluorescens 89B61 Solánum Phytophthora infestans ISR Yan et al. (2002)
lycopérsicum
Bacillus subtilis GB03 Arabidopsis thaliana Botrytis cinerea ISR Sharifi and Ryu (2016)
Paenibacillus polymyxa Arabidopsis thaliana Pseudomonas syringae pv. ISR, SAR Lee et al. (2012)
maculicola
ES4326
Pseudomonas aeruginosa Pag, Pseudomonas fluorescens Cicer arietinum Sclerotium rolfsii SAR Singh et al. (2003)
Pf4
Pseudomonas fluorescens SS101 Arabidopsis thaliana Pseudomonas syringae pv. SAR Van de Mortel et al. (2012)
tomato DC3000
Serattia marcescens 90–166 Arabidopsis thaliana Cucumber mosaic virus Fny ISR Ryu et al. (2004)
 K.A. Tsukanova et al. / South African Journal of Botany 113 (2017) 91–102
Many PGPR colonizing the rhizosphere and the roots can induce ISR
(Choudhary and Johri, 2009; Van der Ent et al., 2009). Volatile organic
substances produced by PGPR may be the ISR inductors (Sharifi and
Ryu, 2016). Besides, PGPR can induce salicylic acid mediated pathogen
resistance (Van de Mortel et al., 2012; Li et al., 2015) or induce both
ISR and SAR simultaneously (Table 7) (Bordiec et al., 2011; Niu et al.,
2011; Lee et al., 2012; Niu et al., 2016).
Many microorganisms can use the antagonism between the signal-
ing pathways of jasmonic acid and salicylic acid to increase plant coloni-
zation success. The pathogen Botrytis cinerea produces elicitors of the
salicylic acid signaling pathway (El Oirdi et al., 2011), while the patho-
gen Alternaria solani suppresses the expression of jasmonate-induced
genes via the NPR1 salicylic acid receptor (Rahman et al., 2012), thereby
suppressing ISR development. Biotrophic pathogens such as Pseudomo-
nas syringae may produce substances similar to jasmonate-isoleucine
conjugate (the active form of jasmonic acid in the plant) to suppress
SAR (Gimenez-Ibanez et al., 2016).
PGPR might use some mechanisms similar to those of aforemen-
tioned biotrophic pathogens. It has been shown that bacterial auxin
can suppress the salicylic acid signaling pathway (Naseem et al., 2015)
(see Section 2. “Auxin”). Endophytic PGPR strains isolated from sun-
flower plants could synthesize jasmonic acid in vitro (Forchetti et al.,
2007). Some bacteria from the genera Rhodococcus, Arthrobacter,
Bacillus and Pseudomonas isolated from soil can degrade salicylic acid
(Plotnikova et al., 2001; Sasonova et al., 2008). Bacterial cytokinins
may also influence plant resistance mediated by salicylic acid. High con-
centrations of exogenous cytokinin (100 μM) stimulated both accumu-
lation of salicylic acid and expression of SA-induced genes, which
resulted in increased resistance of A. thaliana to Hyaloperonospora
arabidopsidis Noco2. Whereas low cytokinin concentrations (0.1 μM)
made the plant more susceptible, while blocking activation of salicylic
acid - induced genes (Argueso et al., 2012). This indicates that the influ-
ence of bacterial cytokinin on the plant is concentration-dependent. De-
spite the absence of direct evidence, one can suggest that some PGPR
use the above-mentioned mechanisms for suppressing SAR in host
plants. There is also data suggesting that the salicylic acid signaling
pathway is involved in the process of plant colonization by PGPR. For ex-
ample, rhizosphere microbial community of the mutant A. thaliana
plants deficient in synthesis and/or reception of salicylic acid was al-
tered, whereas in mutants deficient in synthesis and/or reception of
jasmonic acid and ethylene no such effect was observed (Lebeis et al.,
2015).
To conclude, both jasmonic acid and salicylic acid play an important
role in the interactions between PGPR and the host plants. Their role is
associated with the colonization, the formation of the microbial com-
munity of the rhizosphere and the development of plant pathogen
resistance.
8. Conclusions and perspective
PGPR can affect the homeostasis of plant hormones but the molecu-
lar mechanisms employed by bacteria are different for different strains.
PGPR can synthesize phytohormones, metabolize them as well as stim-
ulate or inhibit the plant's own hormone synthesis. Since hormones
tend to have multiple functions in the plant, changes in their amount
and localization result in various effects associated in particular with
the growth stimulation and with the development of resistance to biotic
and abiotic stresses. Therefore, each PGPR strain to be introduced in ag-
riculture, should be studied for its ability to modify homeostasis of plant
hormones. It should be noted that the characteristics of a strain obtained
in in vitro experiments cannot always be reproduced in planta
(Cardinale et al., 2015). Grasping mechanisms of PGPR action would
considerably increase the effectiveness of the PGPR-based preparations
in agriculture. It is important to understand the potential capacity (i.e.
the presence of the genes) of PGPR strain to synthesize phytohormones
and its actual capacity to do so in vitro and in planta. The changes in the
99
gene expression and subsequent metabolic and morphological changes
the strain elicits in a host plant should also be studied. Obtaining
transcriptomes of inoculated plants is a promising research direction
since it helps to obtain multidimensional information on the PGPR-
induced changes in the host plant.
Comparative analysis of PGPR is challenging because of the diversity
of the model systems and considerable variation in the experimental
conditions. Since conditions in various laboratories all over the world
differ a priori, an increase in the number of studies focused on PGPR is
important. The elucidation of the mechanisms of PGPR-plant symbioses
would help researchers to use new promising strains in agriculture. For
an effective application of any strain under particular conditions, this
knowledge is essential.
Acknowledgements
This study was financially supported by the Government of the
Russian Federation, grant 074-U01. The work of V.K. Chebotar was
supported by the Russian Scientific Fund (project no. 14-16-00146).
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