Plant Growth Promoting Rhizobia

3 Biotech (2015) 5:355–377
DOI 10.1007/s13205-014-0241-x
REVIEW ARTICLE
Plant growth promoting rhizobia: challenges and opportunities

Subramaniam Gopalakrishnan • Arumugam Sathya •
Rajendran Vijayabharathi • Rajeev Kumar Varshney •
C. L. Laxmipathi Gowda • Lakshmanan Krishnamurthy
Received: 8 May 2014 / Accepted: 19 July 2014 / Published online: 3 August 2014
Ó The Author(s) 2014. This article is published with open access at Springerlink.com
Abstract Modern agriculture faces challenges, such as Keywords Rhizobium PGPR Biocontrol Stress
loss of soil fertility, fluctuating climatic factors and Heavymetal Co-inoculation
increasing pathogen and pest attacks. Sustainability and
environmental safety of agricultural production relies on
eco-friendly approaches like biofertilizers, biopesticides Introduction
and crop residue return. The multiplicity of beneficial
effects of microbial inoculants, particularly plant growth Imbalance in nitrogen (N) cycling, nutritional status,
promoters (PGP), emphasizes the need for further physical and biological properties of soil, incidence of
strengthening the research and their use in modern agri- pests and diseases, fluctuating climatic factors and abiotic
culture. PGP inhabit the rhizosphere for nutrients from stresses are the interlinked contributing factors for reduced
plant root exudates. By reaction, they help in (1) increased agricultural productivity. Agricultural sustainability, food
plant growth through soil nutrient enrichment by nitrogen security and energy renewability depends on a healthy and
fixation, phosphate solubilization, siderophore production fertile soil. However, rapid acceleration of desertification
and phytohormones production (2) increased plant protec- and land degradation by numerous anthropogenic activities
tion by influencing cellulase, protease, lipase and b-1,3 leads to an estimated loss of 24 billion tons of fertile soil
glucanase productions and enhance plant defense by trig- from the world’s crop lands (FAO 2011). The intensity of
gering induced systemic resistance through lipopolysac- such degradation can be realized by the extent of highly
charides, flagella, homoserine lactones, acetoin and degraded (25 %) and slightly/moderately degraded (36 %)
butanediol against pests and pathogens. In addition, the lands, while only 10 % of land is listed to be improving all
PGP microbes contain useful variation for tolerating abi- though high level use of agricultural chemicals have
otic stresses like extremes of temperature, pH, salinity and increased the productivity of available limited lands, high
drought; heavy metal and pesticide pollution. Seeking such energy and environmental costs associated with their use
tolerant PGP microbes is expected to offer enhanced plant necessitate the search for alternative methods of soil fer-
growth and yield even under a combination of stresses. tility and pest management. Recent estimations indicate
This review summarizes the PGP related research and its that by 2030, the increasing population growth and
benefits, and highlights the benefits of PGP rhizobia changing consumption patterns would increase the demand
belonging to the family Rhizobiaceae, Phyllobacteriaceae for food by at least 50 %, energy by 45 % and water by
and Bradyrhizobiaceae. 30 % (IFPRI 2012). These expectations cannot be met
sustainably unless the soil fertility and productivity has
been restored in the already degraded lands. A reversal of
the decline in soil health is a possibility through the use of
S. Gopalakrishnan A. Sathya R. Vijayabharathi green and farm yard manures, composts and crop residues
R. K. Varshney C. L. L. Gowda L. Krishnamurthy (&)
and by crop management options, such as natural fallow,
International Crops Research Institute for the Semi-Arid Tropics
(ICRISAT), Patancheru 502 324, Andhra Pradesh, India intercropping, relay cropping, cover crops, crop rotations
e-mail: l.krishnamurthy@cgiar.org and dual purpose legumes. Among these practices, legumes
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are the well-acknowledged builders and restorers of soil of rhizobia in inducing the plant growth of nonleguminous
fertility, primarily through their association with symbiotic plants has been published by Mehboob et al. (2012).
nitrogen fixation. In Rhizobiaceae family, the constituents increased con-
Use of microbial agents for improving agricultural siderably from 8 in the year 1980 to 53 in 2006 (Willems
productions, soil and plant health had been practiced for 2006). Dispersion of host plants to new geographical
centuries. By the end of the ninenteenth century, the locations might serve as a major source for these new
practice of mixing natural soil with seeds became a rec- rhizobia species. Still, increasing number of rhizobial
ommended method of legume inoculation. Rhizospheric species is expected because of following reasons. Only
soil, inhabited and influenced by the plant roots, is usually 57 % of 650 genera of leguminous plants have been
rich in nutrients when compared to the bulk soil, due to the studied for nodulation. Exploration of large number of
accumulation of numerous amino acids, fatty acids, legume species can potentially lead to the identification of
nucleotides, organic acids, phenols, plant growth regula- many more rhizobial species. Recent advancements in the
tors/promoters, putrescine, sterols, sugars and vitamins taxonomic research with the aid of specific molecular tools
released from the roots by exudation, secretion and depo- are another reason. So, identification and exploration of
sition. This results in enrichment of microorganisms (10- to such potential rhizobia with plant growth promoting
100-folds than the bulk soil) such as bacteria, fungus, algae properties will be useful for sustainable agriculture.
and protozoa, among which bacteria influence the plant
growth in a most significant manner (Uren 2007). Such
rhizobacteria were categorized depending on their prox- Plant growth promoting traits of rhizobia
imity to the roots as (1) bacteria living in soil near the roots
(rhizosphere) (2) bacteria colonizing the root surface (rhi- Plant growth promotion by Rhizobia can be both direct as
zoplane) (3) bacteria residing in root tissue (endophytes), well as indirect. Both these types of promotions are dis-
inhabiting spaces between cortical cells and (4) bacteria cussed as follows:
living inside cells in specialized root structures, or nodules,
which includes two groups—the legume associated rhizo- Direct promotions
bia and the woody plant associated Frankia sp. (Glick
1995). Bacteria that belong to any of these categories and Nitrogen fixation
promote plant growth either directly (nitrogen fixation,
phosphate solubilization, iron chelation and phytohormone Nitrogen (N) is required for synthesis of nucleic acids,
production) or indirectly (suppression of plant pathogenic enzymes, proteins and chlorophyll and hence it is a vital
organisms, induction of resistance in host plants against element for plant growth. Although 78 % of the atmospheric
plant pathogens and abiotic stresses), are referred as plant air is N, this gaseous form is unavailable for direct assimi-
growth promoting rhizobacteria (PGPR). Vessey (2003) lation by plants. Currently a variety of industrial N fertilizers
preferred to categorize the bacteria that belong to the above is used for enhancing agricultural productivity. However,
mentioned first three groups as extracellular PGPR (eP- economic, environmental and renewable energy concerns
GPR) and the fourth group as intracellular PGPR (iPGPR). dictate the use of biological alternatives. Biological nitrogen
This ePGPR includes the genera Bacillus, Pseudomonas, fixation (BNF) is a process of converting atmospheric N into
Erwinia, Caulobacter, Serratia, Arthrobacter, Micrococ- plant assimilable N such as ammonia through a cascade of
cus, Flavobacterium, Chromobacterium, Agrobacterium, reactions between prokaryotes and plants with the use of
Hyphomycrobium and iPGPR includes the genera Rhizo- complex enzyme systems (Wilson and Burris 1947). BNF
bium, Bradyrhizobium, Sinorhizobium, Azorhizobium, accounts for about 65 % of N currently used in agriculture.
Mesorhizobium and Allorhizobium. Legumes are BNF capable and meet their own N needs.
Research on exploring the potential of such PGPR has Major part of N fixed by legumes is harvested as grains, while
been reviewed periodically by many researchers (Bhatta- the soil and the succeeding crops also get benefitted by N in
charyya and Jha 2012; Gray and Smith 2005; Johri et al. the form of root and shoot residues. Legume crops substan-
2003; Lugtenberg and Kamilova 2009). There are many tially reduce the N requirement from external sources
reviews focusing on both ePGPR and iPGPR. However, we (Bhattacharyya and Jha 2012). However, N fixation effi-
intend to provide a detailed review on iPGPR, the rhizobia ciency of legumes varies, and depends on the host genotype,
that belong to the families Rhizobiaceae (excluding the rhizobial efficiency, soil conditions, and climatic factors.
Frankia sp.), Bradirhizobiaceae and Phyllobacteriaceae, Reported quantum of nitrogen fixation ranged from 126 to
having unique association with root nodules of legumes 319 kg N ha-1 in groundnut, 33 to 643 kg N ha-1 in soy-
and induce plant growth in many ways and improving bean, 77 to 92 kg N ha-1 in pigeonpea, 25 to 100 kg N ha-1
sustainability in agriculture. Similar review on the capacity in cowpea, 71 to 74 kg N ha-1 in green gram and 125 to
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3 Biotech (2015) 5:355–377 357
143 kg N ha-1 in black gram (Peoples and Craswell 1992). requires energy, but also it acts as a limiting factor to
Crops like wheat, rice, sugarcane and woody species have yields when conditions are uncongenial.
also the capacity to fix atmospheric N using free living or Nitrogenase, a major enzyme involved in the nitrogen
associative diazotrophs like Cyanobacteria, Azospirillum, fixation has 2 components: (1) dinitrogenase reductase, the
Azocarus etc. However, the contribution of legume-rhizobia iron protein and (2) dinitrogenase (metal cofactor). The
symbiosis (13–360 kg N ha-1) is far greater than the non- iron protein provides the electrons with a high reducing
symbiotic systems (10–160 kg N ha-1) (Bohlool et al. power to dinitrogenase which in turn reduces N2 to NH3.
1992). The symbiotic N contribution is also reported to Depending on the availability of metal cofactor, three types
benefit the cereal crops, such as maize, rice, wheat and sor- of N fixing systems have been identified (1) Mo-nitroge-
ghum with a relative yield increase of 11–353 % (Peoples nase (2) V-nitrogenase and (3) Fe-nitrogenase. Complexity
and Cranswell 1992). of nitrogen fixation can be clearly understood by the con-
Rhizobia can be used as inoculants for enhanced N tribution of several gene clusters for (1) nitrogen fixation
fixation and studies demonstrated their predominance in (nifHDK—nitrogenase, nifA, fixLJ, fixK—transcriptional
nodules for 5–15 years after initial inoculation (Lindström regulator, nifBEN—biosynthesis of the Fe-Mo cofactor,
et al. 1990), and confirming that they are effective colo- fixABCX—electron transport chain to nitrogenase, fix-
nizers persisting in soil for many years in the absence of NOPQ—cytochrome oxidase, fixGHIS—copper uptake and
their host (Sanginga et al. 1994). Still, BNF systems can be metabolism, fdxN—ferredoxin) (2) nodulation (nodA—
realized only through analysis and resolution of major acyltransferase, nodB—chitooligosaccharide deacetylase,
constraints to their optimal performance in the field, their nodC—N-acetylglucosaminyltransferase, nodD—tran-
adoption and use by the farmers. The constraints include scriptional regulator of common nod genes, nodIJ—Nod
environmental, biological, methodological, production factors transport, nodPQ, nodX, nofEF, NOE—synthesis of
level and sociocultural aspects (Bohlool et al. 1992). Nod factors substituents, nol genes—several functions in
BNF ability, N self sustainability and protein-rich synthesis of Nod factors substituents and secretion); and (3)
grains of legumes require high energy and productivity other essential elements (exo—exopolyssacharide produc-
tradeoffs (Hall 2004). Hence, improving yield potential of tion, hup—hydrogen uptake, gln—glutamine synthase,
BNF capable legumes, to a level of cereals, is considered dct—dicarboxylate transport, nfe—nodulation efficiency
difficult. Legumes do not establish a rapid crop ground and competitiveness, ndv—b-1,2 glucan synthesis, pls—
coverage leading to low intercepted photon (radiation) use lipopolysaccharide production) (Laranjo et al. 2014).
efficiency and a low proportion of carbohydrate that is Another study reported the coexistence of symbiosis and
partitioned to the grain. In addition, this area of research pathogenicity determining genes in Rhizobium (Velázquez
had attracted less plant breeding attention till now. The et al. 2005). This coexistence enables the induction of
energy costs of biochemical pathways for the production nodules depending on plant species. Although BNF is an
of proteins and lipids are far greater than that of carbo- energy expensive process, it is the only process through
hydrates. This explains why the protein-rich legumes lack which the atmospheric N is converted to plant usable
behind in yield potential compared to cereals. Production organic N making the greatest quantitative impact on N
of proteins require 2.5 and lipids 3.0 units of photosyn- cycle. Legume–rhizobia (Rhizobium/Bradyrhizobium/Mes-
thates (glucose), while a mere 1.2 units are required for orhizobium) symbiosis is a cheaper source of N and an
the carbohydrates (Penning de Vries et al. 1983) and such effective agronomic practice ensuring adequate supply of
a high energy requirement for protein synthesis and N than the application of fertilizer-N. However, various
accumulation in seeds increases the amount of photosyn- environmental factors limit nitrogen fixation, such as soil
thates requirement thereby reducing the productivity moisture deficiency, osmotic stress, extremes of tempera-
potential of legumes and oil seeds. The seed biomass ture, soil salinity, soil acidity, alkalinity, nutrient defi-
production efficiency of legumes is shown to be lower ciency, overdoses of fertilizers and pesticides; since all
(0.66) per unit of photosythates required as compared to these soil and environmental factors affect the survival and
0.72 of cereals (Sinclair and de Wit 1975). Also, legume infectivity rate of rhizobia—an important driver for BNF
seeds (26 mg g-1 seed) need double the requirement of (Zahran 1999). Recent research is focused to identify rhi-
nitrogen compared to cereals (13 mg g-1 seed) which is zobial strains with resistance to these environmental
one more limiting factor for grain yield productivity. In stresses and explore their potentiality under field condi-
addition, legumes need to be BNF-capable spending large tions. Details of such rhizobia have been discussed in later
amount of energy in this symbiotic relationship contrib- parts of this review.
uting both for the current yield and for enriching the soil Nitrification is an important process in nitrogen cycle in
by 30–40 kg N for every ton of plant biomass produc- which ammonia is converted to nitrite and nitrate by
tivity (Peoples et al. 2009). Thus, not only the BNF nitrifying bacteria such as Nitrosomonas and Nitrobacter.
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The nitrification products are vulnerable to leaching and through intervention of biotic and abiotic processes where
denitrification and an estimated 45 % of applied fertilizer is the phosphate solubilizing activity of the microbes has a
lost by leaching (Jarvis 1996) and 10–30 % by denitrifi- role to play (Sharma et al. 2013). Rhizobia, including R.
cation (Parker 1972). Therefore, a reduced rate or inhibi- leguminosarum, R. meliloti, M. mediterraneum, Brady-
tion of nitrification provides enough time to plant for rhizobium sp. and B. japonicum (Afzal and Bano 2008;
assimilation of fixed N. Plants also produce secondary Egamberdiyeva et al. 2004; Rodrigues et al. 2006; Vessey
metabolites such as phenolic acids and flavonoids for 2003) are the potential P solubilizers. These bacteria syn-
inhibiting nitrification. The natural ability of plants to thesize low molecular organic acids which acts on inor-
suppress nitrification is not currently recognized or utilized ganic phosphorous. For instance, 2-ketogluconic acid with
in agricultural production (Subbarao et al. 2006). However, a phosphate-solubilizing ability has been identified in R.
they have no effects on other soil microbial community. leguminosarum (Halder et al. 1990) and R. meliloti (Halder
For example, it had been demonstrated that nitrification and Chakrabarty 1993). Sometimes mineralization of
inhibitor produced by B. humidicola as root extracts were organic P takes place by several enzymes of microbial
seen to inhibit nitrifying bacteria, with no adverse effects origin, such as acid phosphatases (Abd-Alla 1994a, b),
on other soil microorganisms such as Azospirillum lipofe- phosphohydrolases (Gügi et al. 1991), phytase (Glick 2012;
rum, R. leguminosarum and Azotobacter chroococcum Richardson and Hadobas 1997), phosphonoacetate hydro-
(Gopalakrishnan et al. 2009). This work also demonstrated lase (McGrath et al. 1998), D-a-glycerophosphatase
that, this inhibitory effect vary with the soil type. Nitrifi- (Skrary and Cameron 1998) and C–P lyase (Ohtake et al.
cation and denitrification remain to be the only known 1996). Some bacterial strains are found to possess both
biological processes that generate nitrous oxide (N2O), a solubilization and mineralization capacity (Tao et al.
powerful greenhouse gas contribute to global warming. 2008). Importance of this P solubilizing capacity in
Biological nitrification inhibition is seen as a major miti- enhancing plant growth by M. mediterraneum has been
gation process towards global warming besides improving demonstrated in chickpea and barley plants (Peix et al.
N recovery and N use efficiency of agricultural systems 2001).
(Subbarao et al. 2012).
Siderophore formation
Phosphate solubilizers
Iron, a typical essential plant micronutrient, is present in
After nitrogen, phosphorus (P) is the most limiting nutrient soils ranging from 0.2 to 55 % (20,000–550,000 mg/kg)
for plant growth. It exists in both inorganic (bound, fixed, with a significantly different spatial distribution. Iron can
or labile) and organic (bound) forms and the concentration occur in either the divalent (ferrous or Fe2?) or trivalent
depends on the parental material. The concentration had (ferric or Fe3?) states which is determined by the pH and
been shown to range from 140 ppm in carbonate rocks to Eh (redox potential) of the soil and the availability of other
more than 1,000 ppm in volcanic materials (Gray and minerals (e.g., sulphur is required to produce FeS2 or
Murphy 2002). Although the parent material has a strong pyrite) (Bodek et al. 1988). Under aerobic environments,
control over the soil P status of terrestrial ecosystems (Buol iron exists as insoluble hydroxides and oxyhydroxides,
and Eswaran 2000), the availability of P to plants is which are not accessible to both plants and microbes
influenced by pH, compaction, aeration, moisture, tem- (Rajkumar et al. 2010). Generally bacteria have the ability
perature, texture and organic matter of soils, crop residues, to synthesis low molecular weight compounds termed as
extent of plant root systems and root exudate secretions and siderophores capable of sequestering Fe3?. These sidero-
available soil microbes. Soil microbes help in P release to phores are known to have high affinity for Fe3?, and thus
the plants that absorb only the soluble P like monobasic makes the iron available for plants. The siderophores are
(H2PO4-) and dibasic (H2PO42-) forms (Bhattacharyya water soluble and are of two types viz. extracellular and
and Jha 2012). Although the P fertilizer provides the plants intracellular. Fe3? ions are reduced to Fe2? and released
with available form of P, excessive application of them is into the cells by gram positive and negative rhizobacteria.
not only expensive, but also damaging to environment. This reduction results in destruction/recycling of sidero-
Phosphorus accounts for about 0.2–0.8 % of the plant phores (Rajkumar et al. 2010). Siderophores can also form
dry weight, but only 0.1 % of this P is available for plants stable complex with heavy metals such as Al, Cd, Cu etc.
from soil (Zhou et al. 1992). The soil solution remains to be and with radionucleides including and U and NP (Neubauer
the main source of P supply to plants. The P content of et al. 2000). Thus, the siderophore producing bacteria can
agricultural soil solutions are typically in the range of relieve plants from heavy metal stress and assist in iron
0.01–3.0 mg P L-1 representing a small portion of plant uptake. Rhizobial species, such as R. meliloti, R. tropici,
needs. The rest must be obtained from the solid phase R. leguminosarum bv. viciae, R. leguminosarum bv. trifolii,
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3 Biotech (2015) 5:355–377 359
R. leguminosarum bv. phaseoli, S. meliloti and Brady- approximate order of their discovery. It is also believed
rhizobium sp. are known to produce siderophores (Antoun that certain types of dwarfness are due to gibberellin
et al. 1998; Arora et al. 2001; Carson et al. 2000; Chabot deficiency, but it has no effect on roots. Application of
et al. 1996). gibberellins is known to promote bolting of the plants,
parthenocarpy in fruits, increase fruit size and number of
Phytohormone production buds and break down the tuber dormancy. Gibberellins also
help in seed germination as in the case of lettuce and
Phytohormones are the substances that stimulate plant cereals and control flowering and sex expression of flow-
growth at lower/equal to micromolar concentrations. These ers. Many PGP microbes are reported to produce gibber-
include indole-3-acetic (IAA) acid (auxin), cytokinins, ellins (Dobbelaere et al. 2003; Frankenberger and Arshad
gibberellins and abscisic acid. 1995) including Rhizobium, S. meliloti (Boiero et al. 2007).
Indole-3-acetic acid (IAA)—IAA is the foremost phy- Abscisic acid—Abscisic acid in plants is synthesized
tohormone that accelerates plant growth and development partially in the chloroplasts and the whole biosynthesis
by improving root/shoot growth and seedling vigor. IAA is primarily occurs in the leaves. The production of abscisic
involved in cell division, differentiation and vascular acid is accentuated by stresses such as water deficit and
bundle formation and an essential hormone for nodule freezing temperatures. It is believed that biosynthesis
formation. It has been estimated that 80 % of bacteria occurs indirectly through the production of carotenoids.
isolated from the rhizosphere can produce IAA (Patten and The transport of abscisic acid can occur in both xylem and
Glick 1996). The salient ones are A. caulinodans, B.ja- phloem tissues and can also be translocated through
ponicum, B. elkanii, M. loti, R. japonicum, R. legumin- paranchyma cells. The movement of abscisic acid in plants
osarum, R. lupine, R. meliloti, R. phaseoli, R. trifolii and does not exhibit polarity like auxins (Walton and Li 1995).
Sinorhizobium spp. (Afzal and Bano 2008; Antoun et al. Abscisic acid was reported to stimulate the stomatal clo-
1998; Biswas et al. 2000; Boiero et al. 2007; Chi et al. sure, inhibit shoot growth while not affecting or even
2010; Chandra et al. 2007; Dazzo et al. 2005; Naidu et al. promoting root growth, induce seeds to store proteins and
2004; Senthilkumar et al. 2009; Yanni et al. 2001; Weyens in dormancy, induce gene transcription for proteinase
et al. 2009). IAA production in rhizobium takes place via inhibitors and thereby provide pathogen defense and
indole-3-pyruvic acid and indole-3-acetic aldehyde path- counteract with gibberellins (Davies 1995; Mauseth 1991).
way. On inoculation of R. leguminosarum bv. viciae, Rhizobium sp. and B. japonicum had been reported to
60-fold increase in IAA was observed in the nodules of produce abscisic acid (Boiero et al. 2007; Dobbelaere et al.
vetch roots (Camerini et al. 2008). One of the highest 2003).
productions of IAA had been reported with the inoculation
with B. japonicum-SB1 with B. thuringiensis—KR1 1-aminocyclopropane-1-carboxylic acid (ACC) deami-
(Mishra et al. 2009). Co-inoculating Pseudomonas with R. nase ACC deaminase is a member of a large group of
galegae bv. orientalis had shown to produce IAA that had enzyme that utilizes vitamin B6 and considered to be
contributed to increases in nodule number, shoot and root under tryptophan synthase family. Rhizobia has the ability
growth and nitrogen content. Both environmental stress to uptake ACC and convert it into a-ketobutyrate and
factors (acidic pH, osmatic and matrix stress and carbon NH3. This is used as a source of carbon and nitrogen.
limitation) and genetic factors (auxin biosynthesis genes Hence, on inoculation of rhizobia producing ACC
and the mode of expression) were shown to influence the deaminase, the plant ethylene levels are lowered and
biosynthesis of IAA (Spaepen et al. 2007; Spaepen and result in longer roots providing relief from stresses, such
Vanderleyden 2011). as heavy metals, pathogens, drought, radiation, salinity,
Cytokinins—Cytokinin stimulates plant cell division and etc. Strains, such as R. leguminosarum bv. viciae, R. he-
in some instances root development and root hair formation dysari, R. japonicum, R. gallicum, B. japonicum, B. elk-
(Frankenberger and Arshad 1995). It is documented that ani, M. loti and S. meliloti had been known to produce
90 % of rhizospheric microorganisms are capable of ACC deaminase (Duan et al. 2009; Hafeez et al. 2008;
releasing cytokinins and about 30 growth-promoting Kaneko et al. 2000; Ma et al. 2003a, b, 2004; Madhaiyan
compounds of the cytokinin group has been identified from et al. 2006; Okazaki et al. 2004; Sullivan et al. 2002;
microbial origin (Nieto and Frankenberger 1990, 1991). Uchiumi et al. 2004). IAA producing bacteria are reported
Rhizobium strains are also reported as the potent producers to produce high levels of ACC and known to inhibit
of cytokinins (Caba et al. 2000; Senthilkumar et al. 2009). ethylene levels (Glick 2014). Inoculation with these
Gibberellins—Gibberellins, the plant hormones bacteria had shown to promote root elongation, shoot
responsible for stem elongation and leaf expansion has growth, enhanced rhizobial nodulation and minerals
been denoted as GA1 to GA89 depending on the uptake (Glick 2012). It had also been shown that the
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rhizobia producing ACC deaminase are also efficient S. meliloti and B. japonicum have been reported to secrete
nitrogen fixers. The structural gene of ACC deaminase antibiotics and cell-wall degrading enzymes that can inhibit
(acds) in Mesorhizobium sp. is under the control of nif the phytopathogens (Bardin et al. 2004; Chandra et al.
promoter (Nascimento et al. 2012) which generally con- 2007; Ozkoc and Deliveli 2001; Shaukat and Siddqui 2003;
trols the nif gene responsible for nitrogen fixation. Siddiqui and Mahmood 2001; Siddiqui et al. 1998, 2000).
Rhizobial strains also compete for nutrients by displacing
Indirect growth promotions the pathogens. Rhizobia starve the pathogens of available
iron by producing high affinity siderophores and thereby
There are many indirect ways through which rhizobia act as limit the growth of the pathogen (Arora et al. 2001). A
plant growth promoters with their biocontrol properties and study on colonization behavior of P. fluorescens and S.
induction of systemic resistance against phytopathogens and meliloti in alfalfa rhizosphere had sufficiently demon-
insect pests. PGP organisms have the ability to produce many strated the usage of biocontrol agents to suppress pathogens
active principles for biocontrol of various phytopathogens with (Villacieros et al. 2003).
antibiosis production. This includes (1) production of antibi- Pathogens that infect okra and sunflower, such as
otics such as 2,4-diacyetyl phloroglucinol (DAPG), kanos- Macrophomina phaseolina, Rhizoctonia solani and
amine, phenazine-1-carboxylic acid, pyoluteorin, neomcycin Fusarium solani were shown to be controlled with the
A, pyrrolnitrin, pyocyanin and viscosinamide. Among them, usage of B. japonicum, R. meliloti and R. leguminosarum
DAPG is important since it has a broad spectrum antibacterial, (Ehteshamul-Haque and Ghaffar 1993; Ozkoc and Deliveli
antifungal and antihelminthic activity; (2) secretion of sid- 2001; Shaukat and Siddqui 2003). Some more examples
erophores enabling iron uptake depriving the fungal pathogens are cyst nematode of potato controlled by R. etli strain G12
in the vicinity; (3) production of low molecular weight (Reitz et al. 2000), Pythium root rot of sugar beet by R.
metabolites such as hydrocyanic acid (HCN) which inhibits leguminosarum viciae (Bardin et al. 2004) white rot disease
electron transport and hence disruption of energy supply to the in Brassica campestris by M. loti and sheath blight of rice
cells; (4) production of lytic enzymes such as chitinase, b-1,3 by R. leguminosarum bv. phaseoli strain RRE6 and bv.
glucanase, protease and lipase which lyse the pathogenic Trifolii strain ANU843 (Mishra et al. 2006; Chandra et al.
fungal and bacterial cell walls; (5) successfully competes for 2007). Xanthomonas maltophilia in combination with
nutrients against phytopathogens and thereby occupies the Mesorhizobium had been shown to enhance plant growth
colonizing site on root surface and other plant parts and (6) and productivity in chickpea. This was also been shown to
induces systemic resistance in plants by any of the metabolites enhance nodule number, nodule biomass and nodule
mentioned above or by the inducting the production of phenyl occupancy (Pathak et al. 2007). The incidence of collar rot
alanine lyase, antioxidant enzymes such as peroxidase, poly- in chickpea was also shown to reduce by Pseudomonas sp.
phenol oxidase, superoxide dismutase, catalase, lipoxygenase CDB 35 and BWB 21 when co-inoculated with Rhizobium
and ascorbate peroxidase and also by phytoalexins and phe- sp. IC59 and IC76 (Sindhu and Dadarwal 2001). Brady-
nolic compounds in plant cells (Reddy 2013). rhizobium sp. had been shown to control the infection of M.
phaseolina in peanut, while enhancing seed germination,
Biocontrol abilities of rhizobia nodule number and grain yield (Deshwal et al. (2003b).
The use of R. leguminosarum RPN5, B. subtilis sBPR7 and
Biocontrol is a process through which a living organism Pseudomonas sp. PPR8, isolated from root nodules and
limits the growth or propagation of undesired organisms or rhizosphere of common bean, were shown to be successful
pathogens. Several rhizobial strains are reported to have the against M. phaseolina, F. oxysporum, F. solani, Sclerotinia
biocontrol properties. Hence, usage of these strains against sclerotiorum, R. solani and Colletotrichum sp. as dual
soil borne pathogens can lead to potential control. The culture or as cell free culture filtrate (Kumar 2012).
mechanisms of biocontrol by rhizobia include, competition
for nutrients (Arora et al. 2001), production of antibiotics Induction of plant resistance
(Bardin et al. 2004; Chandra et al. 2007; Deshwal et al.
2003a), production of enzymes to degrade cell walls The use of PGP strains are reported to trigger the resistance
(Ozkoc and Deliveli 2001) and production of siderophores of plants against pathogens. This phenomenon is referred
(Carson et al. 2000; Deshwal et al. 2003b). The production as induced systemic resistance (ISR). In this process, a
of metabolites such as HCN, phenazines, pyrrolnitrin, vi- signal is generated involving jasmonate or ethylene path-
scoinamide and tensin by rhizobia are also reported as way and thus inducing the host plant’s defense response.
other mechanisms (Bhattacharyya and Jha 2012). For Various rhizobial species are reported to induce systemic
example, the strains including R. leguminosarum bv. tri- resistance in plants by producing bio-stimulatory agents
folii, R. leguminosarum bv. viciae, R. meliloti, R. trifolii, including R. etli, R. leguminosarum bv. phaseoli and
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3 Biotech (2015) 5:355–377 361
Table 1 Rhizobia and their ability in plant growth promotion them, indigenous and native microbes were more effective
(Modified from Ahmed and Kibert, 2014) and competitive as they are well adapted to the local
Rhizobia Growth promoting References environments (Mrabet et al. 2005). Rhizobia when used as
substances produced microbial inoculants have shown many direct and indirect
PGP properties including traits for stress are represented in
Rhizobium Siderophores, Abd-Alla (1994a, b),
P-solubilization, IAA, Antoun et al. (1998), Tables 1 and 2. Rhizobia having some key tolerance
HCN Deshwal et al. mechanism/pathways against certain stress factor such as
(2003a), Duhan et al. abiotic stresses, heavy metals and pesticides are required as
(1998), Khan et al. these are the major constraints for sustainable agriculture.
(2002), Tank and
Saraf (2010) These mechanisms help rhizobia to execute their beneficial
Rhizobium sp. Growth hormones, IAA, Ahemad and Khan PGP traits under stress conditions. The following are some
siderophores, HCN, (2009a, 2010a, b, c, of the resistance mechanisms adopted by rhizobia for their
ammonia, exo- 2011a, b, c, 2012a), survival and PGP traits for plants under stress conditions.
polysaccharides Joseph et al. (2007), Abiotic stresses, such as drought, extremes of tempera-
Wani et al.(2007b),
Zafar-ul-Hye et al. ture, soil salinity, acidity, alkalinity and heavy metals
(2013) causes severe yield loss. The response of legumes to var-
R. phaseoli IAA Arora et al. (2001), ious stresses depends on the host plant reaction, but this
R. ciceri Siderophores Berraho et al. (1997), reaction can be influenced by the rhizobia and the process
Noel et al. (1996), of symbiosis (Yang et al. 2009). The role of microorgan-
R. meliloti Siderophores
Prabha et al. (2013),
R. Cytokinin Zahir et al. (2010) isms in adaptation of crops to various abiotic stresses is
leguminosarum reviewed by Grover et al. (2010). There are comprehensive
Bradyrhizobium Siderophores, IAA, Abd-Alla (1994a), reviews on tolerance and nodulating capacity of Rhizobium
HCN, P-solubilization Antoun et al. (1998), and Bradyrhizobium to soil acidity, salinity, alkalinity,
Deshwal et al.
temperature and osmotic stress conditions (Graham 1992;
(2003b), Duhan et al.
(1998) Kulkarni and Nautiyal 2000). A list of related studies that
Bradyrhizobium IAA, HCN, ammonia, Ahemad and Khan are in Table 2.
sp. siderophores, exo- (2011c, d, e, 2012b),
polysaccharides Khan et al. (2002), Extremes of temperature
Wani et al. (2007a)
B. japonicum IAA, Siderophores Shaharoona et al.
Global warming and the resultant climate change are
(2006), Wittenberg
et al. (1996) expected to cause land degradation with salinization,
Mesorhizobium IAA, Siderophores, Ahemad and Khan increase the drought episodes and desertification (USDA
sp. HCN, Ammonia, exo- (2009b, 2010d, e, 2012). High temperatures lead to increased drought inten-
polysaccharides, 2012c), Ahmad et al. sity, due to enhanced transpirational water loss. This can
antifungal activity, (2008), Khan et al. lead to reduction in nodule number, rhizobial growth, rate
(2002), Wani et al.
(2008a) of colonization and infectious events, and can lead to delay
M. ciceri IAA, Siderophores Wani et al. (2007c) in nodulation or restrict the nodule to the subsurface
region. This phenomena was observed in alfalfa plants
grown in a desert environment of California (USA) form-
ing fewer nodules in the top 5 cm soil horizon, while
R. leguminosarum bv. trifolii (Mishra et al. 2006; Peng extensively nodulating below this depth (Munns et al.
et al. 2002; Singh et al. 2006; Yanni et al. 2001). Even 1979).
individual cellular components of the rhizobium had been The optimum temperature for rhizobial growth is
shown to induce ISR viz. lipopolysaccharides, flagella, 28–31 °C, while many of them are unable to grow beyond
cyclic lipopeptides, homoserine lactones, acetoin and 37 °C. Rhizobia isolated from hot and dry environments of
butanediol (Lugtenberg and Kamilova 2009). the Sahel Savannah are reported to tolerate temperature up
to 45 °C, but they were found to lose their infectiveness
(Eaglesham and Ayanaba 1984; Hartel and Alexander
Abiotic stress resistance of rhizobia 1984; Karanja and Wood 1988). Similarly, a heat treatment
of 35 and 37 °C to R. phaseoli was found to cause loss of
The best option for developing stress tolerant crops with melanin synthesis plasmid DNA and symbiotic properties
minimized production costs and environmental hazards can (Beltra et al. 1988). In contrast, at 35 and 38 °C, R. legu-
be the use of PGP microbes as stress relievers. Among minosarum bv. phaseoli was found to be infective and
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Table 2 Attributes of rhizobia exerted against abiotic stress on host plants/in vitro
Rhizobia Crop species Screening medium Growth Remarks References
condition
Drought stress
R. tropici co-inoculated with Kidney bean -7, -70 and Greenhouse Enhanced plant Figueiredo
Paenibacillus polymyxa \-85 kPa height, shoot et al. (2008)
dry weight
and nodule
number
Bradyrhizobium sp. – PEG 6000 induced In vitro and pot Enhanced Uma et al.
culture drought (2013)
tolerance, IAA
and EPS
production;
nodulation,
nodule ARA,
nodule N
M. mediterraneum LILM10 Chickpea – Field study Increased Romdhane
nodule et al. (2009)
number, shoot
dry weight
and grain
yield
Water deficient
tolerant strains
were also
NaCl tolerant.
R. elti (engineered for enhanced Kidney bean – Pot studies Enhanced Suárez et al.
trehalose-6-phosphate synthase) nodules, (2008)
nitrogenase
activity and
biomass
production
Higher
tolerance than
wild type
strains
Temperature stress
Mesorhizobium spp. – 20, 28 and 37 °C In vitro Overproduction Rodrigues
of 60 kDa et al. (2006)
protein by all
the isolates
All the isolates
revealed more
tolerance to
20 °C than
37 °C.
Heat shock at 60 °C for In vitro Variations in the
15 min; 46 °C for 3 h expression of
protein profile
Rhizobium sp. DDSS69 – 5 °C In vitro Induction of 135 Sardesai and
and 119 kDa Babu (2001)
proteins
Variation in the
protein profile
of stressed and
non-stressed
cells
Salt/osmotic stress
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3 Biotech (2015) 5:355–377 363
Table 2 continued
condition
M. ciceri ch-191 Chickpea -salt resistant 50, 75, 100 mM In vitro Decreased plant Tejera et al.
and sensitive cultivars dry weight, (2006)
nitrogenase
activity in
sensitive
cultivars
Less N2 fixation
inhibition,
higher root to
shoot ratio,
normalized
nodule weight
and shoot
K/Na ratio and
reduced foliar
accumulation
of Na ? in
resistant
cultivars
M. ciceri ch-191 – 100–400 mmol NaCl/L In vitro Higher Soussi et al.
tolerance was (2001)
noticed on
200 mmol/L
Altered protein
and LPS
levels
Higher proline
accumulation
than glutamate
Acacia rhizobia. – 0.4-1.4 M NaCl In vitro Presence of Gal and Choi
(40 strains) small and (2003)
large plasmids
Intracellular
accumulation
of free
glutamate
Three rhizobia
strains has
tolerated
1.4 M NaCl
M. ciceri, M. mediterraneum Chickpea 25 mM NaCl Glasshouse M. ciceri Mhadhbi et al.
and S. medicae enhanced the (2004)
nodulation
and CAT
activity
Least decrease
in nodule
protein and
SOD activity
Rhizobia strains Lentil 5.5 Ds m-1 Field study Increased plant Islam et al.
biomass, (2013)
nodule
number and
nodule dry
weight
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Table 2 continued
condition
M. ciceri, M. mediterraneum Chickpea Mannitol—50 mM Aerated Maintenance of Mhadhbi et al.

induced hydroponic growth and (2008)
cultures nitrogen fixing
activity
Increased
antioxidant
enzyme
activity in
nodules
pH stress
Mesorhizobium spp. – 5, 7 and 9 In vitro Large range of Rodrigues
isolate et al. (2006)
variation in
growth at pH
7/9 and others
at pH 5/7
formed nodules in P. vulgaris, but these nodules were sensitive isolates of the same species, however, such phe-
found to remain ineffective (Hungria and Franco 1993). nomenon was not found to express during cold stress
Nevertheless, heat-tolerant, actively nodulating and N2 conditions. This indicates that although the chaperones are
fixing Rhizobium strains have been identified. Adaptation heat shock proteins, their gene expression is stress specific.
of microorganisms to stress is a complex regulatory pro- Plants have various mechanisms for drought tolerance
cess, as it involves the use of proteins and lipopolysac- including drought-escapism, dehydration postponement
charide (LPS) with the up-regulation of an array of genes. and dehydration tolerance (Turner et al. 2000). Plants
Upon exposing the wild and heat resistant Rhizobium sp. to generally overexpress zeatin for delayed leaf senescence as
30 and 43 °C, changes in the cell surface including extra- a drought tolerance mechanism. Alfalfa plants inoculated
cellular polymeric substances/exo polysaccharides (EPS), with engineered strains of S. meliloti with ipt gene showed
LPS and proteins had been demonstrated (Nandal et al. elevated zeatin concentrations and antioxidant enzymes in
2005). Michiels et al. (1994) reported first about the pre- their leaves and survived better under severe drought
sence of a large set of small heat shock proteins in Rhi- conditions (Xu et al. 2012). Vanderlinde et al. (2010)
zobium sp. They observed the expression of eight heat noticed the production of EPS as another tolerance mech-
shock proteins in heat-sensitive strains, where as it was anism. Intra species difference in competitive efficiency
only two in the heat-resistant strains, which indicates that was demonstrated by Krasova-Wade et al. (2006) in which
the heat shock proteins also play key roles in normal cell Bradyrhizobium ORS 3257 was found to compete their best
growth. Münchbach et al. (1999) reported 12 small heat under favorable water conditions while Bradyrhizobium
shock proteins in B. japonicum and classified them into ORS 3260 was the best under limited water conditions.
Class A—sHsp similar to Escherichia coli IbpA and IbpB,
and Class B—sHsps similar to sHsps from other prokary- Salinity
otes and eukaryotes. Among the sHsp family, 13 genes for
small heat shock proteins was detected on B. japonicum Soil salinity is one of the production constraints in the arid
(Han et al. 2008). Among these regulatory systems, chap- and semi-arid tropics world-wide, and about 40 % of the
erones such as DnaK–DnaJ and GroEL–GroES are the key world’s land surface is affected by salinity-related prob-
components of heat shock or stress response. These chap- lems (Zhan et al. 1991). Salinity decreases the nutrition
erones help on hydrophobic domains of the target protein uptake of plants, particularly P, due to their binding with
to regain their native structure since they get denatured Ca ions in salt-stressed soils. It is also known that higher
upon stress (Hartl and Hayer-Hartl 2009). Alexandre and concentration of ions (Na?, Cl-, SO42-) in saline soils gets
Oliveira (2011) reported 53 strains of Mesorhizobium sp. accumulated in the plant cells and inactivate enzymes that
for heat stress and shock protein production by chaperone inhibits protein synthesis and photosynthesis (Serraj et al.
analysis, which revealed the increased transcripts of dnaK 1994; Zhu 2001). Salinity affects bacterial infection pro-
and groESL. They also observed a higher induction of cess (by decreasing the number and the deformation of root
chaperone genes in heat-tolerant isolates than in heat- hairs), nodule growth and functioning (by limiting the
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3 Biotech (2015) 5:355–377 365
nutrient supply via photosynthesis products and oxygen the three osmolytes, glutamate, NAGGN, and trehalose
consumption) and BNF (by reducing the nodule metabo- accumulates (Smith et al. 1994). Osmoprotectants, the
lism, leghemoglobin content and atmospheric nitrogen compatible solutes/osmolytes, also play a dual role as
diffusion). evidenced in S. meliloti by proline-betaine which serves as
Rhizobial species are known to vary in their salt sensi- both osmoprotectant (under high osmotic stress) and
tivity. Some of them are categorized as salt tolerant, such energy source (under low osmotic stress) (Miller-Williams
as R. meliloti (Zhang et al. 1991), R. fredii (Yelton et al. et al. 2006).
1983), Rhizobium sp. from Acacia senegal, Prosopis chil-
ensis (Zahran et al. 1994) and Vigna unguiculata (Mpe- Soil acidity
pereki and Makoneses 1997), chickpea, soybean (El Sheikh
and Wood 1990), and pigeonpea (Subbarao et al. 1990) Soil acidity (low pH) is yet another abiotic stress that
whereas others as salt sensitive such as R. leguminosarum affects plant growth and cause crop failures which might be
(Chein et al. 1992). The existence of a high degree of due to high concentration of protons and low concentration
phenotypic and genotypic diversity in Sinorhizobium pop- of calcium and phosphate in acidic soils. Low survival and
ulations sampled from marginal soils of arid and semi-arid poor growth of rhizobia and inhibition of initiation and
regions of Morocco has been demonstrated recently formation of root nodules are the important responses that
(Thami-Alami et al. 2010). It was also observed that these lead to the failure of rhizobia–legume symbiosis in acid
salt tolerant isolates also turned out to be water stress tol- soils (Richardson et al. 1988). The addition of lime on acid
erant. The effect of salt stress on halotolerant rhizobia by soils has been followed as a common practice to raise the
their LPS (Lloret et al. 1995; Zahran et al. 1994), protein soil pH creating a favorable conditions for the growth and
profiles (Saxena et al. 1996) and exopolysaccharide (Lloret survival of root nodule bacteria (Watkin et al. 1997).
et al. 1998) have been studied. Large variability in the Graham et al. (1994) proposed some strains of Rhizobium,
efficiency of host plant and rhizobial strains on BNF under Azorhizobium and Bradyrhizobium to be low pH tolerant.
salinity had been reported (Jebara et al. 2001; Aouani et al. Tolerance to acidity by rhizobia was correlated with the
1998). production of extracellular polysaccharide or polyamines/
Salinity generates negative osmotic potential that lowers glutamate concentration in the cell. Muglia et al. (2007)
the soil water potential. Similar to plants, rhizobia also highlighted the role of glutathione, a tripeptide for the
produce many group of metabolites called compatible growth of R. tropici under low pH conditions. Watkin et al.
solutes [trehalose, N-acetylglutaminylglutamine amide (2003) reported the ability of acid tolerant R. legumin-
(NAGGN) and glutamate], osmoprotectants [betaine, gly- osarum bv. trifolii in accumulating higher level of potas-
cine-betaine, proline-betaine, glucans, trehalose, sucrose, sium and phosphorous than an acid sensitive strain. The
ectoine, 3-dimethylsulfoniopropionate (3-dimethylpropio- effect of acid shock on S. meliloti 1021 was analyzed via
thetin or DMSP), 2-dimethylsulfonioacetate (2-dimethyl- oligo-based whole genome microarrays which demon-
thetin or DMSA)] and pipecolic acid and cations [calcium, strated that within 20 min of the shock, the cells had started
potassium] as tolerance mechanism (Chen 2011; Streeter to respond by either up-regulating or down-regulating the
2003; Sugawara et al. 2010). Salt tolerance mechanisms specific genes of various cellular functions or hypothetical
involve several gene families which have been reported proteins of unknown functions (Hellweg et al. 2009). In a
largely in S. meliloti followed by R. etli, R. tropici, Rhi- re-vegetation program on acidic soils, Bradyrhizobium sp.
zobium sp., S. fredii and B. japonicum. The identified gene was found to enhance the nodule number and plant growth
families includes betaine (betS/betABCI/hutWXV) (Boscari when six shrubby legumes, such as Cytisus balansae, C.
et al. 2002), glycine-betaine (AraC) and proline-betaine multiflorus, C. scoparius, C. striatus, Genista hystrix and
(betS/prb) (Boscari et al. 2004; Payakapong et al. 2006; Retama sphaerocarpa, were inoculated with (Rodrı́guez-
Alloing et al. 2006), glucans (ndvABCD), sucrose (zwf) and Echevarrı́a and Pérez-Fernández 2005).
trehalose (zwf) (Chen et al. 2002; Jenson et al. 2002; Barra
et al. 2003), cation efflux (phaA2/phaD2/phaF2/phaG2) Heavy metal resistance of rhizobia
(Jiang et al. 2004) and rpoH2 (Tittabutr et al. 2006), ntrY,
ntrX, greA, alaS, dnaJ, nifS, noeJ, kup (Nogales et al. Pollution of the biosphere by the toxic metals had increased
2002), omp10, relA, greA and nuoL (Wei et al. 2004). dramatically since the beginning of industrial revolution by
Osmolyte production depends not only on type of stress, the dumping of solid wastes and the use of industrial waste
but also on degree of stress. It was reported in S. meliloti waters for irrigation. Ever increasing demand for lands,
that at lower level of salt concentration glutamate accu- forced the farmers to use contaminated sites for crop cul-
mulates; at higher levels, glutamate and NAGGN accu- tivation. Heavy metals are the key pollutants causing
mulates, whereas at extremely higher concentrations, all serious illness to plants, ecosystem and humans by their
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non-degradable nature. For the reclamation and removal of a total of 100 isolates in a site contaminated since 6 years
heavy metals, phytoremediation is suggested to be prac- by a toxic spill. Genetic diversity among the rhizobial
ticed as it preserves natural soil properties and microbial population had also been observed through differences in
biomass (Gianfreda and Rao 2004). The use of microor- size of nodC fragment, heavy metal resistance and sym-
ganisms such as Bacillus sp., Pseudomonas sp., Azoto- biotic properties. Some strains had been observed to have a
bacter sp., Enterobacter sp., and Rhizobium sp. were also broad spectrum resistance and therefore are symbiotically
proposed to speed up the phytoremediation process had effective even under combined stress conditions. Changes
been reviewed in detail by Ma et al. (2011). in physiology were found to lead to the variations in pro-
Rhizobia multiply slowly in soil until they infect a tein profiles that serve as a marker for stress response
compatible host. Rapid growth of rhizobia occurs only after analysis in R. leguminosarum bv. viciae isolated from
successful infection by a single cell and formation of a heavy metal polluted sites (Pereira et al. 2006a).
nitrogen-fixing nodule on the host-root which consists of Similar to the non-nodulating bacterial species, rhizobia
over 108 cycles of bacterial progeny (Downie, 1997). In also has its own features such as EPS and LPS for influ-
heavy metal contaminated sites, after the successful encing heavy metal resistance. EPS are biopolymers that
establishment of symbiosis with the host plant, the heavy possess negatively charged ligands which instantly form
metals tend to accumulate in the nodules. This would be an complexes with metal ions through electrostatic interac-
alternative and less expensive mode to (1) remove heavy tions (Liu et al. 2001; Sutherland 2001). EPS from R. etli
metal from soil (2) enhance soil and plant health with an (strain M4), isolated from an acid mine drainage, was
enhanced nitrogen fixation and other plant growth pro- shown to impact ecosystem near a manganese mine in
moting pathways and (3) help to grow heavy metal-free Northern Australia (Foster et al. 2000; Pulsawat et al.
plant components in any contaminated site contributing to 2003). Lakzian et al. (2002) identified that plasmids are the
food and nutritional security. However, despite demon- major contributing factor for this as highly tolerant strains
strating the extent of benefits through the use of PGPR in were noticed to have 6–9 plasmids whereas moderately
remediation of contaminated sites, there had been very few tolerant strains have only three plasmids. However, an
field studies while most of the successful studies are either alternate view was reported by Pereira et al. (2006b) on
from greenhouse or growth chambers (Lucy et al. 2004). cadmium (Cd) resistance as he found similar number (a
Effects of heavy metals on growth, abundance, mor- maximum of four) plasmids in all the tolerant, moderately
phology and physiology of various strains of R. legumin- tolerant and sensitive isolates. Pereira et al. (2006b) also
osarum have been well documented (Castro et al. 1997; observed that some highly tolerant strains have had no
Chaudhary et al. 2004; Chaudri et al. 2000; Lakzian et al. plasmids and therefore had concluded that, the heavy metal
2002; Smith 1997). Continuous exposure to heavy metals resistance may be related to the plasmids, but there could
leads the viable bacterial cells not only to transform into a also be some other mechanisms conferring metal resis-
non-viable form, but also adversely affects the genetic tance. This study also reported that the concentration of
diversity and nodulation of the host plants (Paton et al. intracellular Cd varies within the groups, where highly
1997; Hirsch et al. (1993). Reductions in bacterial counts tolerant strains have higher quantity. Reports of Figueira
of Rhizobium sp. have been reported with the increasing et al. (2005), Purchase et al. (1997), and Purchase and
concentrations of heavy metals such as Cu, Zn and Pb, Miles (2001), are also support this view.
either sole or in combinations, and variations in the Natural resistance is not sufficient when soils are con-
expression of symbiotic genes including nod genes (Stan taminated heavily and for a longer period. Use of recom-
et al. 2011). binant rhizobia could play a major role in remediation
Studies on effectiveness of rhizobia isolated from long- measures. Microorganisms equipped with high metal-
term contaminated sites (over 40 years) and un-polluted binding capacity through metallothionins for enhancing the
sites revealed that only 15 % of the active isolates were tolerance, sequestration of heavy metals have been widely
effective in polluted sites while 94 % of them were from exploited. Metallothionins (MTs) are the low-molecular
un-polluted sites. A great diversity in terms of plasmid weight, cysteine-rich, metal binding proteins produced by
types has been observed in isolates of un-polluted soil than higher organisms (Kagi 1991). Sriprang et al. (2002)
the isolates from polluted soils. In addition, the dominant engineered the expression of tetrameric human MTL-4
plasmid groups present in un-polluted soils were found to gene under nifH and nolB promoters in M. huakuii subsp.
be absent in isolates of polluted soils and vice versa (Castro rengei B3 that had been shown to establish symbiosis with
et al. 1997). However, these negative impacts had been Astragalus sinicus in Cd-polluted soils and to enhance Cd
specific to exposure time and metal type. This hypothesis uptake by twofolds.
had been demonstrated by Carrasco et al. (2005), who Phytochelatins (PCs), a naturally occurring peptide,
isolated 41 heavy metal resistant isolates of rhizoibia from having metal binding properties and found in a variety of
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3 Biotech (2015) 5:355–377 367
Table 3 Rhizobia and their effects on host plant/in vitro at metal stress conditions
Rhizobia Crop Heavy Growth condition Remarks References
species metal
stress
R. leguminosarum – Cd In vitro Sequestration of Cd Robinson et al.

bv. trifolii NZP561 (2001)
Bradyrhizobium Green Ni, Zn Pot experiments Enhanced growth performance Wani et al.
RM8 gram (2007c)
Rhizobium sp. Hyacinth Co, Cu, Pot experiments Greater HM accumulation in nodules than in roots and Younis (2007)
bean Zn, Cd and field shoots
conditions
Mesorhizobium RC3 Chickpea Cr Pot experiments Increased growth, nodulation, chlorophyll, Wani et al.
leghaemoglobin, nitrogen content, seed protein and seed (2008b)
yield
M. metallidurans sp. – Cd, Zn In vitro Heavy metal resistance Vidal et al.
nov. (2009)
R. leguminosarum Maize Pb Pot experiments Enhanced plant growth and biomass Hadi and Bano
(2010)
S. meliloti Black Cu Pot experiments Enhanced biomass production Fan et al.
medic (2011)
Rhizobium RL9 Lentil Pb, Ni Pot experiments Increased growth, nodulation, chlorophyll, Wani and Khan
leghaemoglobin, nitrogen, seed protein and seed yield (2012, 2013)
plants and microorganisms (Cobbett 2000), can accumulate plants. Chaudri et al. (2000) observed greatly reduced
higher concentration of heavy metals than MTs due to their symbiosis of R. leguminosarum bv. viciae with pea and R.
unique structural features (Mehra and Mulchandani 1995). leguminosarum bv. trifolii with white clover under Zn
Sriprang et al. (2003) transformed PCs gene from Arabi- toxicity as a consequence of reduced numbers of free-
dopsis thaliana (AtPCS) to M. huakuii subsp. rengei B3 living rhizobia in the soil indirectly affecting N fixation
strain for enhancing the adsorption of heavy metals. They and Zn phytotoxicity. Severe yellowing of plants, small
found that the free-living state of the recombinant bacte- leaves, lack of nodules and reduced rhizobial counts has
rium had a higher Cd accumulation while the symbiotic also been observed as the symptoms of heavy metal tox-
state had a higher accumulation of Cu and As than Cd and icity in these toxicity affected plants.
Zn (Ike et al. 2008). Besides nitrogen fixation and heavy metal resistance,
It is necessary to isolate and study the native rhizobial some rhizobia exhibit PGP traits under contaminated
strains from heavy metals contaminated soils, to identify conditions as reported in soybean cv. Curringa and its
the potential of rhizobium–legume symbiosis of particular rhizobial symbiont B. japonicum at higher arsenic (As)
strain for the remediation of the affected area. Such concentrations (Reichman 2007). Guo and Chi (2014)
studies with their contribution are presented in Table 3. reported cadmium (Cd) tolerant Bradyrhizobium sp. to
Rhizobia, such as R. fredii, R. meliloti, R. etli, R. legu- exhibit several PGP traits including synthesis of IAA,
minosarum bv. viceae, R. leguminosarum bv. trifolii, ACC deaminase, siderophores, increased shoot dry
Bradyrhizobium sp. and B. japonicum had been evaluated weights and high level accumulation of Cd in roots of
for heavy metal resistance and of which R. fredii and R. Lolium multiflorum than in un-inoculated control. They
meliloti alone were found to exhibit higher metal toler- also reported that the strain enhanced the extractable Cd
ance against Tellurium (Te) and Selenium (Se) (Kinkle concentrations in the rhizosphere, whereas it decreased
et al. 1994). Nonnoi et al. (2012) demonstrated differ- the Cd accumulation in root and shoot of G. max by
ences in the heavy metal resistance spectrum of S. medi- increasing Fe availability.
cae and R. leguminosarum bv. trifolii strains isolated from Huang et al. (2005) reported developing a multi-process
mercury-contaminated soils. Heavy metals are reported to phytoremediation system (MPPS) for petroleum hydro-
cause harm not only to benefiting microbes, but also to carbons. This employs the use of both PGP bacteria and
host plants. Paudyal et al. (2007) reported the negative specific contaminant-degrading bacteria which metabolize
effect of heavy metals such as Al, Fe and Mo on two the contaminants into non-toxic substances/readily avail-
Rhizobium strains and their symbiotic efficiency on host able compounds while the role of PGP bacteria is still
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prompting plant growth and increasing the plant tolerance A. lipoferum and R. leguminosarum bv. trifolii were co-
to pollutants. MPPS has also the potential for deployment inoculated in white clovers (Tchebotar et al. 1998), pigeon-
to enhance rhizobium-host symbiosis and plant growth at pea and chickpea (Deanand et al. 2002). It was found that
heavy metal contaminated sites. Azospirillum can increase the infection site providing a space
for Rhizobium resulting in higher nodule formation (Tche-
Pesticide tolerance of rhizobia bolas et al. 1988). Co-inoculation with Azospirillum and
Rhizobium were shown to increase phytohormones, vitamins
Pesticide accumulation in soils beyond the recommended and siderophore production (Cassan et al. 2009; Dardanelli
level occurs either by consistently repeated application or et al. 2008). Co-inoculation of common bean with Azospir-
their slow degradation rate. It affects plant growth by illum-Rhizobium was also shown to increase the fixed
altering plant root’s architecture, number of root sites for nitrogen quantity (Reman et al. 2008). Azotobacter was
rhizobial infection, transformation of ammonia into found to be a potential co-inoculant with rhizobium that
nitrates, transformation of microbial compounds to plants enhanced the production of phytohormones and vitamins and
and vice versa. Besides this, growth and activity of free- increase the nodulation (Akhtar et al. 2012; Chandra and
living or endophytic nitrogen fixing bacteria has also been Pareek 2002; Dashadi et al. 2011; Qureshi et al. 2009).
affected (Mathur 1999). Several studies have documented Bacillus sp. was also been reported to induce the PGP ability,
the effects of various pesticides on the reduction of yield (Mishra et al. 2009; Ahmad et al. 2008) and uptake of
microbial diversity and density on various soil types (El nutrients (Stajkovic et al. 2011) including phosphorous
Abyad and Abou-Taleb 1985; Moorma 1988; Martinez- (Singh et al. 2011). Significant increase in weight of the root
Toledo et al. 1996). Numerous microorganisms have the and seed yield of chickpea were reported upon inoculation of
capacity to degrade the pesticides by the action of degra- Rhizobium with B. subtilis OSU-142 and B. megaterium M-3
dative genes in plasmids/transposons/chromosomes (Elkoca et al. 2008). Enhanced nodulation and nitrogen fix-
(Kumar et al. 1996). The influence of broad-spectrum of ation was noticed upon inoculation of Bacillus and Azo-
pesticides on the functional attributes of rhizobia and their spirillum sp. along with rhizobial inoculants in pigeonpea
tolerance to pesticides are reported in Table 4. From the (Rajendran et al. 2008; Roseline et al. 2008). Interaction
literature survey, it was recognized that none of the rhi- between Streptomyces lydius WYEC108 and Rhizobium of
zobia are found to have pesticide tolerance under field pea were shown to promote growth of the plant (Tokala et al.
conditions. So research on isolating, identifying and char- 2002) including nodule number and growth, probably by the
acterizing such resistant rhizobia needs to be vigorously root and nodule colonization of Streptomyces. Enterobacter
pursued as such rhizobia are very much needed considering is another most abundant PGP bacteria that increased the
the quantum of pesticide residue generated currently. yield of nodules on green gram when co-inoculated with
Bradyrhizobium sp. (Gupta et al. 1998). When R. tropici
CIAT899 was co-inoculated with C. balustinum Aur9 it
Synergistic effects of rhizobial co-inoculation resulted in increased root hair formation and infection sites
leading to early nodule development and increased nodule
The in-consistency of beneficial results of microbial use, formation (Estevez et al. 2009). Similar result was obtained
when single microbe was used in the field application, have when Medicago truncatula cv. Caliph was co-inoculated
brought an emphasis on co-inoculation of microbes (Ba- with Pseudomonas fluorescens WSM3457 and Ensifer
shan and de Bashan 2005). Certain specific co-inoculation (Sinorhizobium) medicae WSM419 (Fox et al. 2011).
causes synergy by functioning as helper bacteria to Recently, it was found that nodulation, root and shoot dry
improve the performance of the other bacteria. Therefore in weight, grain and straw yield, nitrogen and phosphorus
such co-inoculations, the combination of PGP bacteria, uptake were significantly increased in chickpea upon co-
rhizobia and the host genotype has to be selected after inoculation with Mesorhizobium sp. and P. aeruginosa
extensively careful evaluations (Remans et al. 2007, 2008). (Verma et al. 2013). Similar plant growth effects along with
A range of PGP microbes can be used with rhizobium that the antagonistic activities against F. oxysporum and R. solani
not only improves legume growth and yield but also cost has been observed on chickpea by co-inoculation of Meso-
effective and efficient. rhizobium, Azotobacter chroococcum, P. aeruginosa and
Azospirillum, a free living diazotroph, Azotobacter, Trichoderma harzianum (Verma et al. 2014). Mehboob et al.
Bacillus, Psuedomonas, Serretia, and Enterobacter are some (2013) had a recent detailed review highlighting the effects
of the genera that are successfully used with rhizobium as co- of co-inoculation of rhizobia with various rhizospheric
inoculants. Azospirillum, was found to enhance growth and bacteria. Although there are many combinations of bacteria
yield of several leguminous crops upon inoculation (Rose- were explored for use, still there is a need for an advanced
line et al. 2008). Improved nodulation was found when comprehensive research in the area.
123
3 Biotech (2015) 5:355–377 369
Table 4 Rhizobia and their beneficial attributes exerted on host plant/in vitro at pesticide stress conditions
Rhizobia Crop Pesticides Concentrations Condition Remarks References
species
Herbicides
Rhizobium MRP1 Pea Quizalafop-p- 40, 80 and Pot Enhanced biomass, nodulation, Ahemad and
Rhizobium MRL3 Lentil ethyl 120 lg/kg experiments leghaemoglobin content, root and shoot N, Khan
soil root and shoot P, seed yield and seed protein (2009a,
Mesorhizobium Chickpea
Clodinafop 400, 800 and 2010b, d)
MRC4
1,200 lg/kg
soil
Rhizobium MRP1 – Metribuzin 850, 1,700 and In vitro Concentration-dependent progressive decline Ahemad and
Rhizobium MRL3 2,550 lg/L in PGP substances except exo- Khan
Glyphosate 1,444, 2,888 polysaccharides (2011a, b,
Mesorhizobium
and 2012a, c)
MRC4
4,332 lg/L
Bradyrhizobium
MRM6
R. – Terbuthylazine 4, 8, 16, 32 In vitro Growth decline was in the order of Singh and
leguminosarum and 64 mg/L Terbuthylazine [ Prometryn [ Simazine Wright
RCR 1045 (2002)
Simazine 4.3, 8.6, 17.2,
34.4 and
68.8 mg/L
Prometryn 4, 8, 16, 32
and 64 mg/L
Bentazon 4.1, 8.2, 16.4, No adverse effects on growth
32.8,
65.6 mg/L
Insecticides
Rhizobium MRL3 Chickpea, Fipronil 200, 400, and Pot Enhanced the biomass, nodulation, Ahemad and
R. Pea, 600 mg/kg experiments leghaemoglobin content, root and shoot N, Khan
leguminosarum soil root and shoot P, seed yield and seed protein (2009b,
Lentil
MRP1 Pyriproxyfen 1,300, 2,600, 2010a, 2011f)
Mesorhizobium and
MRC4 3,900 mg/kg
soil
Rhizobium MRP1 – Imidacloprid 100, 200 and In vitro Concentration-dependent progressive decline Ahemad and
Rhizobium MRL3 300 lg/L in PGP substances except exo- Khan
Thiamethoxam 25, 50 and polysaccharides (2011a, b,
Mesorhizobium
75 lg/L 2012a, c)
MRC4
Bradyrhizobium
MRM6
Fungicides
Rhizobium MRP1 – Hexaconazole 40, 80 and In vitro Concentration-dependent progressive decline Ahemad and
Rhizobium MRL3 120 lg/L in PGP substances except exo- Khan
Metalaxyl 1,500, 3,000 polysaccharides (2011a, b,
Mesorhizobium
and 2012a,c)
MRC4
4,500 lg/L
Bradyrhizobium
MRM6 Kitazin 96, 192 and
288 lg/L
Rhizobium MRP1 Pea Tebuconazole 100, 200 and In vitro Concentration-dependent progressive decline Ahemad and
300 lg/L in PGP substances except exo- Khan
polysaccharides, HCN and ammonia (2011d)
100, 200 and Pot Enhanced the biomass, nodulation,
300 lg/kg experiments leghaemoglobin content, root and shoot N,
soil root and shoot P, seed yield and seed protein
123
370 3 Biotech (2015) 5:355–377
Conclusion different doses of herbicide stress. Pestic Biochem Physiol

98:183–190
Ahemad M, Khan MS (2010c) Insecticide-tolerant and plant growth
Rhizosphere is a unique niche that provides habitation and promoting Rhizobium improves the growth of lentil (Lens
nutrition to PGP microorganisms. In turn, these microor- esculentus) in insecticide-stressed soils. Pest Manag Sci
ganisms produce multiple benefits of induced plant growth, 67:423–429
defense against diseases and survival under stress with many Ahemad M, Khan MS (2010d) Growth promotion and protection of
lentil (Lens esculenta) against herbicide stress by Rhizobium
other unknown benefits. The present review documents the species. Ann Microbiol 60:735–745
potential of PGP rhizobia and highlights the unique proper- Ahemad M, Khan MS (2010e) Improvement in the growth and
ties of plant growth induction, defense pathways and the symbiotic attributes of fungicide-stressed chickpea plants fol-
resistance spectrum available against various abiotic stresses lowing plant growth promoting fungicide-tolerant Mesorhizobi-
um inoculation. Afr J Basic Appl Sci 2:111–116
on a variety of agricultural crops. However, the extent of Ahemad M, Khan MS (2011a) Effect of pesticides on plant growth
success in realizing the benefits of PGP tends to diminish as it promoting traits of green gram-symbiont, Bradyrhizobium sp.
moves from laboratory to greenhouse and to fields, which strain MRM6. Bull Environ Contam Toxicol 86:384–388
reflects the scarcity of research on the beneficial effects of Ahemad M, Khan MS (2011b) Ecotoxicological assessment of
pesticides towards the plant growth promoting activities of
PGP microbes under field conditions. Therefore, generation Lentil (Lens esculentus)-specific Rhizobium sp. strain MRL3.
of comprehensive knowledge on screening strategies and Ecotoxicology 20:661–669
intense selection of best rhizobacterial strain for rhizosphere Ahemad M, Khan MS (2011c) Insecticide-tolerant and plant growth
competence and survival is the current need to enhance the promoting Bradyrhizobium sp. (vigna) improves the growth and
yield of green gram [Vigna radiata (L.) Wilczek] in insecticide
field level successes. Identification of such potential rhizo- stressed soils. Symbiosis 54:17–27
bial strains and developing a robust technology for the use by Ahemad M, Khan MS (2011d) Effect of tebuconazole-tolerant and
smallholder farmers is still in its infancy. Thus, additional plant growth promoting Rhizobium isolate MRP1 on pea-
comprehensive research to exploit the potential of PGP rhi- Rhizobium symbiosis. Sci Hortic 129:266–272
Ahemad M, Khan MS (2011e) Plant growth promoting fungicide
zobia would provide for expansion of this research area, tolerant Rhizobium improves growth and symbiotic characteris-
commercialization and improve sustainability in agricultural tics of lentil (Lens esculentus) in fungicide-applied soil. J Plant
production. Growth Regul 30:334–342
Ahemad M, Khan MS (2011f) Insecticide-tolerant and plant growth
Conflict of interest Authors hereby declare no conflict of interest. promoting Rhizobium improves the growth of lentil (Lens
esculentus) in insecticide-stressed soils. Pest Manag Sci
Open Access This article is distributed under the terms of the 67:423–429
Creative Commons Attribution License which permits any use, dis- Ahemad M, Khan MS (2012a) Ecological assessment of biotoxicity
tribution, and reproduction in any medium, provided the original of pesticides towards plant growth promoting activities of pea
author(s) and the source are credited. (Pisum sativum)-specific Rhizobium sp. strain MRP1. Emir J
Food Agric 24:334–343
Ahemad M, Khan MS (2012b) Productivity of green gram in
tebuconazole-stressed soil, by using a tolerant and plant growth
promoting Bradyrhizobium sp. MRM6 strain. Acta Physiol Plant
34:245–254
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3 Biotech (2015) 5:355–377

Plant growth promoting rhizobia: challenges and opportunities

M. ciceri, M. mediterraneum Chickpea Mannitol—50 mM Aerated Maintenance of Mhadhbi et al.

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Conclusion different doses of herbicide stress. Pestic Biochem Physiol

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