Biotechnology Advances 29 (2011) 248–258
Contents lists available at ScienceDirect
Biotechnology Advances
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / b i o t e c h a d v
Research review paper
Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation
of metalliferous soils
Y. Ma a, M.N.V. Prasad b, M. Rajkumar c, H. Freitas a,⁎
a
b
c
Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Coimbra 3000-455, Portugal
Department of Plant Sciences, University of Hyderabad, Hyderabad 500046, India
Graduate School of Agricultural Science, Kobe University, Rokkodai, Nada, Kobe, 657-8501, Japan
a r t i c l e
i n f o
Article history:
Received 15 July 2010
Received in revised form 1 December 2010
Accepted 3 December 2010
Available online 13 December 2010
Keywords:
Toxic metals
Rhizobacteria
Endophytes
Metabolic pathways
Phytohormones
Phytoextraction
Phytostabilization
a b s t r a c t
Technogenic activities (industrial—plastic, textiles, microelectronics, wood preservatives; mining—mine refuse,
tailings, smelting; agrochemicals—chemical fertilizers, farm yard manure, pesticides; aerosols—pyrometallurgical
and automobile exhausts; biosolids—sewage sludge, domestic waste; fly ash—coal combustion products) are the
primary sources of heavy metal contamination and pollution in the environment in addition to geogenic sources.
During the last two decades, bioremediation has emerged as a potential tool to clean up the metal-contaminated/
polluted environment. Exclusively derived processes by plants alone (phytoremediation) are time-consuming.
Further, high levels of pollutants pose toxicity to the remediating plants. This situation could be ameliorated and
accelerated by exploring the partnership of plant–microbe, which would improve the plant growth by facilitating
the sequestration of toxic heavy metals. Plants can bioconcentrate (phytoextraction) as well as bioimmobilize or
inactivate (phytostabilization) toxic heavy metals through in situ rhizospheric processes. The mobility and
bioavailability of heavy metal in the soil, particularly at the rhizosphere where root uptake or exclusion takes
place, are critical factors that affect phytoextraction and phytostabilization. Developing new methods for either
enhancing (phytoextraction) or reducing the bioavailability of metal contaminants in the rhizosphere
(phytostabilization) as well as improving plant establishment, growth, and health could significantly speed up
the process of bioremediation techniques. In this review, we have highlighted the role of plant growth promoting
rhizo- and/or endophytic bacteria in accelerating phytoremediation derived benefits in extensive tables and
elaborate schematic sketches.
© 2010 Elsevier Inc. All rights reserved.
Contents
1.
2.
Heavy metal pollution and microbe-assisted phytoremediation . . . . . . .
Synergism of plant–microbe interactions for cleanup of metalliferous soils . .
2.1.
Rhizobacteria . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2.
Endophytic bacteria . . . . . . . . . . . . . . . . . . . . . . . .
3.
Role of metal-resistant bacteria on plant growth in metal-contaminated soils
3.1.
Plant growth promoting factors . . . . . . . . . . . . . . . . . . .
3.2.
Micro- and macro-nutrient provider . . . . . . . . . . . . . . . .
3.3.
Biological control . . . . . . . . . . . . . . . . . . . . . . . . .
4.
Role of metal-resistant bacteria on metal accumulation by plants . . . . . . .
4.1.
Microbial-induced metal mobilization in phytoextraction . . . . . . .
4.2.
Microbial-induced metal immobilization in phytostabilization . . . .
5.
Concluding remarks and future perspectives . . . . . . . . . . . . . . . .
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
⁎ Corresponding author. Tel.: +351 239855236; fax: +351 239855211.
E-mail address: [email protected] (H. Freitas).
0734-9750/$ – see front matter © 2010 Elsevier Inc. All rights reserved.
doi:10.1016/j.biotechadv.2010.12.001
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
249
249
250
253
253
254
254
255
255
255
255
256
256
256
249
Y. Ma et al. / Biotechnology Advances 29 (2011) 248–258
1. Heavy metal pollution and microbe-assisted phytoremediation
Continued worldwide industrialization has caused extensive environmental and human health problems. A wide variety of chemicals,
e.g., heavy metals, pesticides, chlorinated solvents, etc., have been
detected in different natural resources such as soil, water, and air
(Mansour and Gad, 2010). Among the pollutants, the heavy metals are
of concern to human health due to their cytotoxicity, mutagenicity, and
carcinogenicity (Lim and Schoenung, 2010). Phytoremediation is the
use of plants to remediate polluted soils, an eco-friendly and costeffective technology that is currently receiving considerable global
attention (Glick, 2010). A large number of plant species are capable of
hyperaccumulating heavy metals in their tissues; however, phytoremediation in practice has several constraints at the level of sites as
these are with a variety of different contaminants (Wu et al., 2006a).
Further, the success of phytoremediation of metals depends upon a
plant's ability to tolerate to accumulate high concentrations of the
metals, while yielding a large plant biomass (Grčman et al., 2001). Due
to their importance for practical applications, metal-tolerant plant–
microbe associations have been the objective of particular attention due
to the potential of microorganisms for bioaccumulating metals from
polluted environment or its effects on metal mobilization/immobilization and consequently enhancing metal uptake and plant growth
(Fig. 1). Synergistic use of plants and microbes has been profitable for
cleanup of metalliferous soils (Jing et al., 2007; Glick, 2010).
This review describes how the beneficial partnerships between
plants and their associated bacteria can be exploited as a strategy to
accelerate plant biomass production and influence plant metal accumulation or stabilization with better performance abilities such as adaptive
strategies, metal mobilization, and immobilization mechanisms.
2. Synergism of plant–microbe interactions for cleanup of
metalliferous soils
Plant growth is affected by microbes in various ways. Some microbes
cause diseases and inhibit plant growth; others can actively or passively
promote the growth through a variety of mechanisms (nitrogen fixation,
solubilization of phosphate, production of siderophores, phytohormone,
and ACC deaminase) (Fig. 2); and there are a large number of soil
microorganisms that do not appear to directly affect plant growth one
Phytovolatilization
Phytofiltration
Blastofiltration
Phytoevaporation
Phytostimulation
Phytohydraulics
Phytoaccumulation
Phytodegradation
Phytoextraction
Phytoassimilation
Bioremediation
Phytoconcentration
Phytotransfer
Phytotransformation
Phytomining
Phytoreduction
Phytoimmobilization
Phytostabilization
Phytooxidation
Phytosequestration
Rhizosphere
Nitrilase
Bacterial ACC
deaminase
Desorption
Adsorption
Respiration
Nitroreductases
Cytochromes P450
Precipitation
Acidification
Redox reactions
Hydrolases
Leakage
Oxidases
Chelation
Glucosyltransferases
Exudation
Peroxidases
Rhizoremediation
Transportation
Phytoremediation
Phytocontainment
Complexation
Laccase
Fungi
Bacteria
Fig. 1. Importance of soil–plant–microbial interactions in bioremediation for the cleanup of metals and organics (pesticides, solvents, explosives, crude oil, polyaromatic
hydrocarbons).
250
Y. Ma et al. / Biotechnology Advances 29 (2011) 248–258
way or the other, although this may vary as a result of a range of different
rhizosphere soil conditions including organic matter, pH, temperature,
nutrients, and pollutants level (Glick, 2003; Bais et al., 2006). Table 1
summarizes the published studies on bacterial effects on phytoremediation in metal-contaminated soils as a function of heavy metal, bacteria,
and the involved plant per se.
2.1. Rhizobacteria
Among the rhizosphere microorganisms involved in plant interactions with metal-contaminated soil milieu, the plant growth
promoting bacteria (PGPB) deserve special attention. In general, the
plant-associated bacteria migrate from the bulk soil to the rhizosphere of living plant and aggressively colonize the rhizosphere and
roots of plants (Kloepper and Schroth, 1978). These so-called
rhizobacteria, as abundant symbiotic partners of plants, are considered
plant growth promoting rhizobacteria (Kapulnik, 1991). Rhizobacteria
viz., Achromobacter, Arthrobacter, Azotobacter, Azospirillum, Bacillus,
Enterobacter, Pseudomonas, and Serratia (Gray and Smith, 2005), as
well as Streptomyces spp. have been found to have beneficial effects on
various plants in metal-contaminated environment (Tokala et al., 2002;
Dimkpa et al., 2008a,b, 2009a,b). The mechanisms of plant growth
Fig. 2. Plant growth promoting rhizobacteria and endophytes accelerates phytoremediation of metalliferous soils though modulation of (a) plant growth promoting parameters,
(b) by providing plants with nutrients, and (c) controlling disease through the production of antifungal metabolites. Abbreviations: indole-3-acetic acid (IAA), indole-3-acetamide
(IAM) pathway, indole-3-pyruvate (IPyA) pathway, methionine-S-adenosylmethionine (SAM), 1-aminocyclopropane-1-carboxylate (ACC), 1-aminocyclopropane-1-carboxylate
synthase (ACS), phosphatase (Ptase), ammonia (NH3), hydrogen cyanide (HCN).
251
Y. Ma et al. / Biotechnology Advances 29 (2011) 248–258
Table 1
Recent examples of bacterially assisted phytoremediation of metal-contaminated soils.
Host
Bacterial strain
Source
Beneficial features
Bacterial effects on plants
Reference
Alyssum murale
Microbacterium oxydans
AY509223 (RS)
Rhizosphere of A. murale grown
in Ni-rich serpentine soil
Ni mobilization
Abou-Shanab
et al. (2006)
Atriplex
lentiformus
20 Promising isolates (RS)
ACCD, siderophore, IAA
Bouteloua
dactyloides
20 Promising isolates (RS)
Brassica juncea
Pseudomonas sp. PsA, Bacillus sp.
Ba32 (RS)
Azotobacter chroococcum HKN-5,
Bacillus megaterium HKP-1, B.
Mucilaginosus HKK-1 (RS)
Rhizosphere of quailbush plants
grown in tailings; bulk tailings
samples; mine tailings;
laboratory culture collection
Rhizosphere of quailbush plants
grown in tailings; bulk tailings
samples; mine tailings;
laboratory culture collection
Cr contaminated soil near
Chennai, India
Agronomic soils in Hong Kong
↑ [Ni] uptake of A. murale grown in
the low, medium, and high Ni soils
by 36.1%, 39.3%, 27.7%
(Phytoextraction)
↑ Plant establishment/biomass in
the presence of 10% compost
↓ Need for compost amendment
(Phytostabilization)
↑ Plant establishment/biomass in
the absence of compost
↓ Need for compost amendment
(Phytostabilization)
↑ Plant growth (Phytostabilization)
Bacillus subtilis SJ-101
nd
ACCD, siderophore, IAA
ACCD, siderophore, IAA,
P solubilization
N fixation,
P solubilization,
K solubilization,
respectively; metal
mobilization
IAA, P solubilization,
Ni bioaccumulation
(RS)
B. napus
Enterobacter sp. NBRI K28,
mutant NBRI K28 SD1(RS)
Fly ash contaminated soil,
Raibarielly district, Uttar
Pradesh, India
ACCD, siderophore, IAA,
P solubilization
Pseudomonas sp. Ps29C, Bacillus
megaterium Bm4C (RS)
Serpentine soil, Bragança,
Portugal
ACCD, siderophore, IAA,
P solubilization
Pseudomonas aeruginosa KUCd1
(RS)
Industrial waste-fed canal
nearby Kolkata, India
Siderophore
Enterobacter aerogenes NBRI
K24, Rahnella aquatilis NBRI K3
(RS)
Fly ash contaminated soil,
Raibarielly district, Uttar
Pradesh, India
ACCD, siderophore, IAA,
P solubilization, metal
biosorption
Achromobacter xylosoxidans
Ax10 (RS)
Cu mine soil, São Domingos,
Portugal
ACCD, IAA,
P solubilization
Psychrobacter sp.SRA1 and SRA2,
Bacillus cereus SRA10 (RS)
(Non) rhizosphere soils of A.
serpyllifolium and Phleum
phleoides in serpentine soil,
Portugal
ACCD, siderophore, IAA,
P solubilization, [Ni]
mobilization
Pseudomonas sp. SRI2,
Psychrobacter sp.
SRS8 and Bacillus sp. SN9 (RS)
(Non) rhizosphere of A.murale
and Astragalus incanus in
serpentine soil, Portugal
ACCD, siderophore, IAA,
P solubilization, [Ni]
mobilization
Bacillus sp. RJ16 (RS)
Metal-polluted soil in Nanjing,
China
IAA, [Cd] mobilization
Pseudomonas tolaasii ACC23,
P. fluorescens ACC9,
Mycobacterium sp. ACC14 (RS)
Roots of Graminaceae grasses
from a water meadow in the
South of Milan polluted with Cd,
Ni and Cu
Root of B. napus from heavy
metal-contaminated site in the
suburbs of Nanjing, China
ACCD, siderophore, IAA
Cu-tolerant plant species
growing on a Cu mine
wasteland, Nanjing, China
ACCD, siderophore, IAA,
P solubilization
Copper-tolerant species
Elsholtzia splendens and
Commelina communis
ACCD, siderophore, IAA,
arginine decarboxylase
production
Pseudomonas fluorescens G10,
Microbacterium sp. G16 (EN)
Arthrobacter sp. MT16,
Microbacterium sp. JYC17,
Pseudomonas chlororaphis SZY6,
Azotobacter vinelandii GZC24, and
Microbacterium lactium YJ7 (EN)
Firmicutes sp., Actinobacteria sp.,
Proteobacteria sp. (EN)
ACCD, siderophore, IAA,
[Pb] mobilization
↑ Plant aboveground biomass
(Phytostabilization)
↑ Shoot length, fresh and dry
weights
↑ Total [Ni] uptake by 0.147% (with
SJ-101) and 0.094% (without SJ-101)
Ni on dry mass basis
(Phytoextraction)
↑ Plant biomass, protein and
chlorophyll content
↑ [Ni Zn Cr] uptake
(Phytoextraction)
↑ Shoot length, plant fresh and dry
weight (Phytostabilization)
↑ Shoot length, root length, wet
weight, dry weight, and chlorophyll
↓ [Cd] uptake in shoots by 36.89%
(Phytostabilization)
↑ Plant height, root length, wet and
dry weight, leaf protein and
chlorophyll content
↑ [Ni,Cr] uptake (Phytoextraction)
↑ Root and shoot length, fresh and
dry weight
↑ [Cu] uptake (Phytoextraction)
↑ Root and shoot length, vigour
index (roll towel assay), fresh and
dry weight (pot experiment)
↑ [Ni] bioavailability and uptake
(Phytoextraction)
↑ Fresh and dry weight
↑ [Ni] bioavailability and uptake
(Phytoextraction)
↑ Root elongation (gnotobiotic
conditions), shoot and root dry
weight (pot experiment)
↑ [Cd] plant uptake
(Phytoextraction)
↑ Plant root elongation promotion
activity, shoot and root dry biomass
↑ [Cd] uptake (Phytoextraction)
↑ Root length (root elongation
assay), shoot and root dry weight
(pot experiment)
↑ [Pb] uptake in shoots
(Phytoextraction)
↑ Root length promotion (Strains
MT16, JYC17, SZY6, GZC24, and YJ7
increased root length of Cu-treated
and untreated seedlings by 17–38 and
20–41%) (Phytoextraction)
↑ Root and above-ground tissue dry
weight
↑ Aboveground tissue [Cu] uptake
(Phytoextraction)
Grandlic et al.
(2008)
Grandlic et al.
(2008)
Rajkumar
et al. (2006)
Wu et al.
(2006b)
Zaidi et al.
(2006)
Kumar et al.
(2008)
Rajkumar
and Freitas
(2008a)
Sinha and
Mukherjee
(2008)
Kumar et al.
(2009)
Ma et al.
(2009a)
Ma et al.
(2009b)
Ma et al.
(2009c)
Sheng and
Xia (2006)
Dell'Amico
et al. (2008)
Sheng et al.
(2008b)
He et al.
(2010b)
Sun et al.
(2010)
(continued on next page)
252
Y. Ma et al. / Biotechnology Advances 29 (2011) 248–258
Table 1 (continued)
Host
Bacterial strain
Source
Beneficial features
Bacterial effects on plants
Reference
B. oxyrrhina
Psychrobacter sp.SRA1 and SRA2,
Bacillus cereus SRA10 (RS)
(Non) rhizosphere soils of A.
serpyllifolium and P. phleoides in
serpentine soil, Portugal
ACCD, siderophore, IAA,
P solubilization, [Ni]
mobilization
Ma et al.
(2009b)
Pseudomonas sp. SRI2,
Psychrobacter sp.
SRS8 and Bacillus sp. SN9
(Non) rhizosphere of A.murale
and Astragalus incanus in
serpentine soil, Portugal
ACCD, siderophore, IAA,
P solubilization, [Ni]
mobilization
↑ Root and shoot length, vigour
index (roll towel assay), fresh and
dry weight (pot experiment)
↑ [Ni] bioavailability and uptake
(Phytoextraction)
↑ Fresh and dry weight
Cucurbita pepo
Pseudomonas aeruginosa KUCd1
(RS)
Industrial waste-fed canal
nearby Kolkata, India
Siderophore
Helianthus
annuus
B. weihenstephanensis SM3 (RS)
Serpentine soil, Bragança,
Portugal
Lycopersicon
esculentum
Methylobacterium oryzae
CBMB20, Burkholderia sp. (EN)
Tissues of Oryza sativa
IAA, P solubilization,
[Cu, Zn, Ni] biosorption
and mobilization
ACCD, phytohormone
production, [Ni, Cd]
biosorption
Burkholderia sp. J62 (RS)
A heavy metal polluted paddy
field, China
ACCD, siderophore, IAA,
P solubilization
Pseudomonas sp. RJ10, Bacillus
sp. RJ16 (RS)
Heavy metal-polluted soil in
Nanjing, China
ACCD, IAA, siderophore,
[Cd, Pb] mobilization
Nicotiana
tabacum
Sanguibacter sp., Enterobacter
sp., Pseudomonas sp.
N. tabacum seeds collected from
plants cultivated on a Cd and Zn
enriched soil
nd
Orychophragmus
violaceus
Bacillus subtilis, B. cereus,
Flavobacterium sp., Pseudomonas
aeruginosa (RS)
Heavy-metal-contaminated
sludge, arboretum fields of
Shanghai University
nd
Pisum sativum
Pseudomonas brassicacearum
Am3,
All-Russia Research Institute for
Agricultural Microbiology
collection
ACCD
Cr-contaminated site situated in
the Indian Himalayan Region
Bacterial metal
detoxification
mechanism
Rhizobium sp. RP5 (RS)
Nodules of pea grown in
metal-contaminated Indian
soils
N2 fixation, IAA,
siderophore
Ricinus
communis
Pseudomonas sp. PsM6, P. jessenii
PjM15 (RS)
Serpentine soil, Bragança,
Portugal
Salix caprea
Pseudomonas sp.,
Janthinobacterium lividum,
Serratia marcescens,
Flavobacterium sp., Streptomyces
sp. Agromyces sp. (RS)
Burkholderia cepacia (RS)
Rhizosphere of willows growing
on a contaminated site in
Arnoldstein, Austria
ACCD, siderophore, IAA,
[Ni, Cu, Zn] biosorption
and mobilization
Siderophore, IAA,
[Zn, Cd] immobilization
(except for Agromyces
AR33)
P. marginalis Dp1, Rhodococcus
sp. Fp2 (RS)
Rhodococcus erythropolis MtCC
7905 (RS)
Sedum alfredii
5 bacterial strains (unidentified)
(RS)
Rhizosphere of S. alfredii in the
Pb/Zn mine
nd
Rhizosphere of S. alfredii treated
with multi-metals
nd
↑ [Ni] bioavailability and uptake
(Phytoextraction)
↑ Shoot length, root length, wet
weight, dry weight, and chlorophyll
↓ [Cd] uptake in shoots by 47.40%
(Phytostabilization)
↑ Plant fresh and dry weight
↑ [Cu, Zn] uptake (Phytoextraction)
↓ Ethylene emission, ↑ tolerance index
of the seedlings (gnotobiotic assay),
↑ Plant growth (pot experiment)
↓Uptake and translocation of
[Ni, Cd] (Phytostabilization)
↑ Root and shoot dry weight
↑Total shoot [Pb, Cd] uptake
(Phytoextraction)
↑ Root length (root elongation
assay), root and above- ground
tissue dry weights (pot experiment)
↑ [Cd, Pb] uptake (Phytoextraction)
↑ Shoot and root dry weight by
inoculation with Sanguibacter sp.
S_d2 and consortia
↑ [Cd] translocation and [Cd, Fe]
uptake (Phytoextraction)
↑ Root length (root elongation
assay), biomass of root, stem and
leaf (pot experiment)
↑ water-soluble [Zn] and [Zn]
uptake (Phytoextraction)
↑ Root and shoot biomass,
↑ nutrient (N, P, K, Ca, S, Fe) uptake
in shoots
↑ [Cd] uptake in shoots
(Phytoextraction)
↑ Plant growth in the presence of Cr6
+
concentration at low temperature
↓ Substantial amounts of Cr6+ to Cr3+
(Phytostabilization)
↑ Dry matter, nodule numbers, root N,
shoot N, leghemoglobin, seed yield,
grain protein under in vitro conditions
↓ [Ni, Zn] toxicity and uptake
(Phytostabilization)
↑ Shoot and root dry weight
↑ [Zn] translocation and uptake
(Phytoextraction)
↑ Plant leaf biomass
↓ [Cd, Zn] uptake (except for
Agromyces AR33)
(Phytostabilization)
↑ Plant growth (110% with Zn
treatment), P (56.1% with Cd
treatment)
↑ [Cd, Zn] uptake (243% and 96.3%
with Cd and Zn treatment) in shoots,
tolerance index (134% with Zn
treatment), metal translocation
(296% and 135% with Cd and Zn
treatment) from root to shoot
(Phytoextraction)
↑ Chlorophyll content, plant
biomass and root length, [N, P]
contents, ↓ [Zn, Cd, Cu, Pb] toxicity
↑ [Zn, Cd, Cu, Pb] uptake and
removal from contaminated water
(Phytoextraction)
Ma et al.
(2009c)
Sinha and
Mukherjee
(2008)
Rajkumar
et al. (2008)
Madhaiyan
et al. (2007)
Jiang et al.
(2008)
He et al.
(2009)
Mastretta
et al. (2009)
He et al.
(2010a)
Safronova
et al. (2006)
Trivedi et al.
(2007)
Wani et al.
(2007b)
Rajkumar
and Freitas
(2008b)
Kuffner et al.
(2008)
Li et al.
(2007)
Xiong et al.
(2008)
253
Y. Ma et al. / Biotechnology Advances 29 (2011) 248–258
Table 1 (continued)
Host
Bacterial strain
Source
Beneficial features
Bacterial effects on plants
Reference
Sorghum bicolor
Pseudomonas monteillii (RS)
Termite mound soil, Sudanese
shrubby savanna, Burkina Faso.
Metal-contaminated soils
nd
↑ Shoot and total biomass
↑ [Cd] uptake (Phytoextraction)
↑ Plant biomass (with inoculum
mixture) and shoot biomass
(Br. h, P. p)
↑ Solubility [Cu, Cr] (B.s, B. p),
↑[Cu, Cr, Pb, Zn] uptake in shoot on
Cu-rich soil and [Cr] uptake in shoot
on Cr-rich soil (Phytoextraction)
↑ Plant growth, N and P
accumulation, nodule number and
mycorrhizal infection
↓ [Zn] uptake (Phytostabilization)
↑ In vivo and pot experiment,
growth increment (height, fresh
and dry weight of roots and shoots),
extensive rooting
↓ [Cd] toxicity and uptake
(Phytostabilization)
↑ Growth, nodulation, N content,
seed yield and seed protein
↓ [Ni] toxicity and uptake
(Phytostabilization)
↑ Root and shoot dry weight
↑Total root [ Pb, Cd] and total shoot
[Pb] uptake (Phytoextraction)
Duponnois
et al. (2006)
Abou-Shanab
et al. (2008)
Bacillus subtilis, B. pumilus,
Pseudomonas pseudoalcaligenes,
Brevibacterium halotolerans (RS)
nd
Trifolium repens
Brevibacillus sp. B-I (RS)
A loamy soil from Granada,
Spain
IAA, [Zn] biosorption
Vigna mungo
Pseudomonas aeruginosa MKRh3
(RS)
Rhizosphere of different plant
species from agricultural fields,
India
ACCD, siderophore,
auxin synthesis,
P solubilization
Vine radiata
Bradyrhizobium sp. (vigna) RM8
(RS)
Nodules of greengram grown in
metal-contaminated Indian soils
IAA, siderophore, HCN,
ammonia production
Zea mays
Burkholderia sp. J62 (RS)
A heavy metal polluted paddy
field, China
ACCD, siderophore, IAA,
P solubilization
Vivas et al.
(2006)
Ganesan
(2008)
Wani et al.
(2007a)
Jiang et al.
(2008)
Note: information in this table is arranged in alphabetical order of the host plant scientific names.
Abbreviations: ↑ =Increase; ↓ =Decrease; ACC deaminase =1-aminocyclopropane-1-carboxylate (ACC) deaminase; HCN =hydrogen cyanide; IAA =indole-3-acetic acid; RS =Rhizosphere
bacteria; EN =endophytic bacteria; Nd =not detected.
stimulation differ between bacterial strains and most certainly
depend on the various metabolites released by these different strains
of microbes. For instance, production of the main growth modulating
phytohormones such as auxins, cytokinins, gibberellins, and ethylene
production are attributed to the presence of different strains of
rhizobacteria (Forchetti et al., 2007; Perrig et al., 2007). These hormones
can directly or indirectly alter plant growth together with other bacterial secondary metabolites usually in a concentration-dependent
manner (Ryu et al., 2005; Aslantas et al., 2007; Dimkpa et al., 2009a).
Other beneficial compounds produced by rhizobacteria include
enzymes, osmolytes, biosurfactants, siderophores, nitric oxide, organic
acids, and antibiotics. These may be responsible for suppression of
pathogenic and deleterious organisms (Chakraborty et al., 2006; Sikora
et al., 2007), improved mineral uptake (Dimkpa et al., 2009a),
associative nitrogen fixation (Dobbelaere et al., 2003), tolerance to
abiotic stresses (Sziderics et al., 2007; Belimov et al., 2009; Dimkpa et al.,
2009a), or production of phytohormones (Vessey, 2003). Therefore, for
amelioration of metal toxicity and for promoting plant growth and
health, extensive research efforts are to be made to explore microbial
diversity, their distribution, as well as function in soil autochthonous (in
native habitat) and allochthonous (relocated to alien environment)
habitats.
Barzanti et al., 2007; Sheng et al., 2008b; Mastretta et al., 2009); in
some cases, they may confer to the plant higher tolerance to heavy
metal stress and may stimulate host plant growth through several
mechanisms including biological control, induction of systemic
resistance in plants to pathogens, nitrogen fixation, production of
growth regulators, and enhancement of mineral nutrients and water
uptake (Ryan et al., 2008). Additionally observed beneficial effects due
to bacterial endophytes inoculation are plant physiological changes
including accumulation of osmolytes and osmotic adjustment,
stomatal regulation, reduced membrane potentials, as well as changes
in phospholipid content in the cell membranes (Compant et al., 2005).
Further, the endophytic bacteria isolated from metal hyperaccumulating plants exhibit tolerance to high metal concentrations (Idris
et al., 2004). This may be due to the presence of high concentration
of heavy metals in hyperaccumulators, modulating endophytes to
resist/adapt to such environmental conditions. It is also possible that
the metal hyperaccumulating plants may simultaneously be colonized by different metal-resistant endophytic bacteria ranging wide
variety of gram-positive and gram-negative bacteria (Rajkumar et al.,
2009).
2.2. Endophytic bacteria
3. Role of metal-resistant bacteria on plant growth in
metal-contaminated soils
Endophytic bacteria have been defined as bacteria colonizing the
internal tissues of plants without causing symptomatic infections or
negative effects on their host (Schulz and Boyle, 2006). Endophytic
bacteria reside in apoplasm or symplasm. Although bacterial
endophytes exist in plants variably and transiently (van Overbeek
and van Elsas, 2008), they are often capable of triggering physiological
changes that promote the growth and development of the plant
(Conrath et al., 2006). In general, the beneficial effects of endophytes
are greater than those of many rhizobacteria (Pillay and Nowak, 1997)
and these might be aggravated when the plant is growing under
either biotic or abiotic stress conditions (Barka et al., 2006; Hardoim
et al., 2008). Endophytic bacteria have been isolated from many
different plant species (Lodewyckx et al., 2002; Idris et al., 2004;
In both natural and managed ecosystems, plant-associated
bacteria play a key role in host adaptation to a changing environment.
These microorganisms can alter plant cell metabolism, so that upon
exposure to heavy metal stress, the plants are able to tolerate high
concentrations of metals and thus can better withstand the challenge
(Welbaum et al., 2004). Several of the plant-associated bacteria have
been reported to accelerate phytoremediation in metal-contaminated
soils by promoting plant growth and health and play a significant role
in accelerating phytoremediation (Grandlic et al., 2008; Kuffner et al.,
2008; Kidd et al., 2009; Ma et al., 2009a,b,c; Compant et al., 2010; Dary
et al., 2010). A schematic illustration of plant growth promoting
mechanisms of PGPB in metal-contaminated soils is presented in
Fig. 2.
254
Y. Ma et al. / Biotechnology Advances 29 (2011) 248–258
3.1. Plant growth promoting factors
The phytohormone ethylene (C2H4) has a central role in modulating
the growth and cellular metabolism of plants (Ping and Boland, 2004)
and been believed to be involved in disease-resistant biotic/abiotic
stress tolerance, plant–microbe partnership, and plant nutrient cycle.
Among its key role in inducing various physiological changes in plants at
molecular level, the overproduction of ethylene can cause the inhibition
of root elongation, lateral root growth, and root hair formation
(Mayak et al., 2004); however, bacteria are capable of alleviating
the stress-mediated impact on plants by enzymatic hydrolysis of
1-aminocyclopropane-1-carboxylic acid (ACC) (Glick et al., 2007b)
(Fig. 2). ACC is involved in biosynthetic pathway of ethylene, as an
intermediate in the conversion of methionine to ethylene following biosynthetic sequence: methionine–S-adenosylmethionine
(SAM)–ACC–C2H4 (Adams and Yang, 1979). In general, ACC is exuded
from plant roots or seeds and then taken up by the ACC-utilizing
bacteria before its oxidation by the plant ACC oxidase (Contesto et al.,
2008) and cleaved by ACC deaminase to α-ketobutyrate (αKB) and
ammonia. The bacteria utilize the ammonia evolved from ACC as a sole
nitrogen source and thereby decrease ACC within the plant (Penrose
and Glick, 2001) with the concomitant reduction of plant ethylene
(Glick et al., 1998; Belimov et al., 2002). The decreased ethylene levels
in plants hosting ACC-utilizing bacteria derive benefit by stress alleviation and enhanced plant productivity (Cheng et al., 2007; Dell'Amico
et al., 2008; Hardoim et al., 2008). Since SAM is converted by ACC
synthase to ACC, the ACC synthase protein seems to play a main
controlling role in ethylene biosynthesis pathway. In the absence of
ACC-utilizing bacteria, ACC is oxidized by ACC oxidase to form ethylene, cyanide, and CO2. Moreover, the multigene family of ACC synthase and ACC oxidase is regulated independently by biotic and abiotic
factors, thus possibly influence the plant ethylene biosynthesis pathway. An unknown phosphatase (Ptase) or other mechanism regulates
the turnover of the ACC synthase protein from the phosphorylated
form (Pi) to the less stable non-phosphorylated form (Wang et al.,
2002; Hardoim et al., 2008).
Phytohormones that are produced by plant-associated bacteria,
including indole-3-acetic acid (IAA), cytokinins, and gibberellins, can
frequently stimulate germination, growth, reproduction, and protect
plants against both biotic and abiotic stress (Taghavi et al., 2009). As
the most studied phytohormones, IAA produced in the plant shoot
and transported basipetally to the root tips associated with cell
elongation and cell division (Rashotte et al., 2000) contributes to plant
growth and plant defense system development (Navarro et al., 2006).
Further, plant–microbe interactions were determined by different IAA
biosynthesis pathways. For instance, the beneficial plant-associated
bacteria synthesize IAA via the indole-3-pyruvate (IPyA) pathway,
whereas pathogenic bacteria mainly use the indole-3-acetamide
(IAM) pathway (Patten and Glick, 1996; Hardoim et al., 2008)
(Fig. 2). In general, root elongation changes qualitatively based on the
IAA level; therefore, the amount of released IAA could have an
important role in modulating the plant–microbe interaction. Xie et al.
(1996) assessed the ability of IAA producing PGPB to stimulate the
elongation of the roots of canola seedlings under gnotobiotic
conditions. They observed that wild-type Pseudomonas putida GR12-2,
which produces low levels of IAA (2 μg ml−1), promoted the root
elongation by 2- to 3-fold, whereas the mutant P. putida GR12-2/aux1
producing high level of IAA (8.2 μg ml−1) inhibited canola root
elongation. The inhibition of root elongation by P. putida GR12-2/aux1
was attributed to synthesis of ACC due to the interactive effect of high
concentrations of IAA with ACC synthase. Overall, bacteria can facilitate
plant growth by altering the plant hormonal balance either direct or
indirect through ethylene synthesis (Persello-Cartieaux et al., 2003).
Further, 1-aminocyclopropane-1-carboxylate synthase 4 [ACC synthase
gene family] has been transcriptionally induced by IAA in plants, as a
signal molecule initiating a cross-talk between IAA and ethylene (Chen
et al., 2005). In situ, ethylene acts as a feedback inhibitor of the IAA signal
transduction pathway (Glick et al., 2007a). Besides, a number of PGPB
produce cytokinins and gibberellin, which can stimulate the growth of
various plants and modify plant morphology under both stressed and
non-stressed conditions (Gutierrez-Manero et al., 2001; Arkhipova
et al., 2007).
In addition, the PGPB may also contribute in reducing the metal
phytotoxicity by biosorption and bioaccumulation mechanisms. Since
the bacterial cells (approximately 1.0–1.5 mm3) have an extremely
high ratio of surface area to volume, they could adsorb a greater
amount of heavy metals than inorganic soil components (e.g.,
kaolinite, vermiculite) either by a metabolism-independent passive,
or by a metabolism-dependent active process (Ledin et al., 1996; Khan
et al., 2007). Several authors have pointed out that bacterial
biosorption/bioaccumulation mechanism, together with other plant
growth promoting features including the production of ACC deaminase and phytohormones, accounted for improved plant growth in
metal-contaminated soils (Zaidi et al., 2006; Madhaiyan et al., 2007;
Kumar et al., 2009).
3.2. Micro- and macro-nutrient provider
Iron is a necessary cofactor for many enzymatic reactions and
hence is an essential nutrient for virtually all organisms. In the aerobic
conditions, iron exists predominantly as ferric state (Fe3+) and reacts
to form highly insoluble hydroxides and oxyhydroxides that are
largely unavailable to plants and microorganisms. To acquire
sufficient iron, siderophores produced by bacteria can bind Fe3+
with a high affinity to solubilize this metal for its efficient uptake.
Although strategy II plants (Poaceae) release phytosiderophores to
enhance their Fe uptake, phytosiderophores typically have a lower
affinity for iron than microbial siderophores. Thus, these plants are
unable to uptake sufficient amounts of iron. Further, heavy metals that
are accumulated in excess in plant tissues can cause changes in
various vital growth processes and have negative effects on iron
nutrition. Under such conditions, the siderophore producing rhizosphere bacteria might offer a biological rescue system that is capable
of chelating Fe3+ and making it available to plant roots (Fig. 2). The
roots could then take up iron from siderophores–Fe complexes
possibly via the mechanisms such as chelate degradation and release
of iron, the direct uptake of siderophore–Fe complexes, and/or a
ligand exchange reaction (Rajkumar et al., 2010). Several examples of
increased Fe uptake in plants with concurrent stimulation of plant
growth as a result of PGPB inoculations have been reported (Burd
et al., 2000; Carrillo-Castañeda et al., 2003; Barzanti et al., 2007).
Siderophores also promote bacterial IAA synthesis by reducing the
detrimental effects of heavy metals through chelation reaction
(Dimkpa et al., 2008a).
Phosphorus (P) is a major essential macronutrient for biological
growth and development. Soluble P is often the limiting mineral
nutrient for biomass production in natural ecosystems only taken up
2−
in monobasic (H2PO−
4 ) or dibasic (HPO4 ) soluble forms (Glass,
1989), and the elevated levels of heavy metals in soil interfere with
P uptake and lead to plant growth retardation (Zaidi et al., 2006).
Under metal stressed conditions, most metal-resistant PGPB can
either convert these insoluble phosphates into available forms
through acidification, chelation, exchange reactions, and release of
organic acids (Chung et al., 2005) or mineralize organic phosphates by
secreting extracellular phosphatases (Gyaneshwar et al., 2002; van
der Heijden et al., 2008). An increase in P availability to plants through
the inoculation of phosphate-solubilizing bacteria has been reported
in pot experiments and under field conditions (Pal, 1998; Zaida et al.,
2003). In addition, fixation of atmospheric nitrogen is a metabolic
virtuosity of endophytes and rhizobacteria and colonization offers
benefit to the host (Dobbelaere et al., 2003).
Y. Ma et al. / Biotechnology Advances 29 (2011) 248–258
3.3. Biological control
In addition to the above described plant growth promoting
features, the PGPB protect the plants from fungal, bacterial, and
viral diseases, and insect and nematode pests by several mechanisms.
The mechanisms include the production of siderophores (Miethke
and Marahiel, 2007), cell wall lytic enzymes (Backman and Sikora,
2008), and antibiotic metabolites (Schouten et al., 2004) and
induction of systemic resistance in plants (Kloepper et al., 2004; van
Loon et al., 2004). The siderophores produced by PGPB protect the
plant from microbial pathogens by chelating iron in the rhizosphere
and thus reducing its availability to pathogens that are reliant on
available iron in soil (Rajkumar et al., 2010). Some metal-resistant
PGPB have also been reported to be able to produce enzymes such as
chitinase, beta 1,3 glucanase, protease, or lipase, by which they can
lysis the cells of fungal pathogens (van Loon et al., 2006). Besides, the
use of PGPB as an inducer of systemic resistance in crop plants against
various fungal (Wei et al., 1991; Chet and Inbar, 1994), bacterial
(Nautiyal et al., 2006; Indiragandhi et al., 2008b), and viral pathogens
(Raupach et al., 1996; Murphy et al., 2000) has been demonstrated
under both the greenhouse and field conditions.
Although the in vitro potential of several PGPB to produce various
anti-pathogenic metabolites (e.g., hydrocyanic acid, lytic enzymes,
and siderophores) is fairly well documented (Nagarajkumar et al.,
2004; Wani et al., 2007c; Indiragandhi et al., 2008a; Trivedi et al.,
2008), the interaction of plant–PGPB–phytopathogens in metalcontaminated soils remains poorly understood. In particular because
both pathogenic and non-pathogenic microbes depend on the
properties of surrounding environment (rhizosphere/tissue interior
of plants) for much of their growth and nutrition (Walker et al., 2003;
Bais et al., 2006) and since these plant-associated microbes may
modulate responses to direct and/or indirect (e.g., heavy metal
induced resistance in plants, altered root exudation) effects of metal
toxicity, further understanding how the metal-resistant PGPB protect
the plants from microbial pathogens in metal-contaminated environment is critical.
4. Role of metal-resistant bacteria on metal accumulation by plants
Although several conditions, for example, the plant growth,
metal tolerance/accumulation, bacterial colonization, and plant
growth promoting potentials must be met for microbe assisted
phytoremediation to become effective, the concentration of bioavailable metals in the rhizosphere greatly influences the quantity of
metal accumulation in plants, because a large proportion of heavy
metals are generally bound to various organic and inorganic
constituents in polluted soil and their phytoavailability is closely
related to their chemical speciation (McBride, 1994). The metabolites released by PGPB (e.g., siderophores, biosurfactants, organic
acids, plant growth regulators, etc.) can alter the uptake of heavy
metals indirectly and directly: indirectly, through their effects on
plant growth dynamics, and directly, through acidification, chelation, precipitation, immobilization, and oxidation–reduction reactions in the rhizosphere.
4.1. Microbial-induced metal mobilization in phytoextraction
Plant-associated bacteria can potentially improve phytoextraction
by altering the solubility, availability, and transport of heavy metal
and nutrients by reducing soil pH, release of chelators, P solubilization, or redox changes. Among the various metabolites produced by
PGPB, the siderophores play a significant role in metal mobilization
and accumulation (Dimkpa, et al., 2009b; Rajkumar et al., 2010), as
these compounds produced by PGPB solubilize unavailable forms of
heavy metal-bearing Fe but also form complexes with bivalent heavy
metal ions that can be assimilated by root mediated processes
255
(Carrillo-Castañeda et al., 2003; Braud et al., 2009). Recently, Braud
et al. (2009) investigated the release of Cr and Pb in soil solution after
inoculation of various PGPB and found that the siderophores
producing PGPB, Pseudomonas aeruginosa was able to solubilize
large amounts of Cr and Pb in soils solution. As an opportunistic
pathogen, P. aeruginosa used in these experiments are therefore only a
model system since regulatory agencies will never give permission for
the deliberate release of this bacterium to the environment.
Furthermore, these authors reported that inoculation of Zea mays
with P. aeruginosa increased Cr and Pb uptake into the shoots by a
factor of 4.3 and 3.4, respectively. Similarly, the role of siderophores
produced by Streptomyces tendae F4 in Cd uptake by bacteria and
sunflower plant was investigated (Dimkpa et al., 2009b). Bacterial
culture filtrates containing hydroxamate siderophores secreted by
S. tendae F4 significantly enhanced uptake of Cd by the plant,
compared to the control. This study showed that siderophores can
help to reduce metal toxicity in bacteria while simultaneously
facilitating the uptake of such metals by plants. In another study,
these effects of siderophores were also reported by Dimkpa et al.
(2009a), who found that the addition of siderophore-containing
culture filtrate of S. tendae F4 to metal-contaminated soils increased
Cd and Cr uptake by cowpea. These studies highlighted the potential
of inoculating soils or plants with siderophore producing PGPB to
further improve their phytoextraction efficiency.
In addition, certain PGPB have been shown to increase heavy metal
mobilization by the secretion of low-molecular-mass organic acids
comprising gluconate, 2-ketogluconate, oxalate, citrate, acetate,
malate, and succinate, etc. An example is the release of 5-ketogluconic
acid by endophytic diazotroph Gluconacetobacter diazotrophicus,
which dissolves various Zn sources such as ZnO, ZnCO3, or Zn3
(PO4)2, thus making Zn available for plant uptake (Saravanan et al.,
2007). Although it is well accepted that organic acids produced by
PGPB play an important role in the mobilization of heavy metals and
mineral nutrients, the inoculation effects of organic acids producing
bacteria on plant growth and metal accumulation in plants are still
poorly understood. The biosurfactants produced by PGPB have also
been demonstrated to enhance heavy metal mobilization in contaminated soils (Braud et al., 2006). For instance, a recent study by Sheng
et al. (2008a) showed that the inoculation of soils with biosurfactantproducing Bacillus sp. J119 significantly enhanced biomass of tomato
plants and Cd uptake in plant tissue. From these studies, it can be
concluded that by inoculating the seeds/rhizosphere soils with
selected metal mobilizing bacteria, it should be possible to improve
bioavailable metal concentrations for plant uptake and thereby
phytoextraction potential in metal-contaminated soils. However, in
spite of many attempts to increase metal bioavailability by adding
microbial iron chelating agents, the strategy usually works in a smallscale laboratory not in the field, since the bacteria typically do little or
nothing to increase metal bioavailability in uncontrolled field (Glick,
2010).
4.2. Microbial-induced metal immobilization in phytostabilization
The use of plant-associated bacteria in phytostabilization strategies may assist plant growth and tolerance to metals, but can also
reduce the metal uptake or translocation to aerial parts of plants by
decreasing the metal bioavailability in the rooting medium. For
survival under metal-stressed environment, plant-associated bacteria
have evolved several mechanisms by which they can immobilize or
transform metals rendering them inactive to tolerate the uptake of
heavy metal ions. The mechanisms that are generally proposed for
heavy metal resistance in bacteria are (1) exclusion of metal by a
permeability barrier or by active export of metal from the cell; (2)
intracellular physical sequestration of metal by binding extracellular
polymers or extra cellular sequestration; (3) detoxification where
metal is chemically modified to render it less active (Rouch et al.,
256
Y. Ma et al. / Biotechnology Advances 29 (2011) 248–258
1995). For instance, binding of metals to anionic functional groups
(i.e., sulfhydryl, carboxyle, hydoxyle, salfonate, amine and amide
groups) immobilizes the metal and prevents its entry into the plant
root. Similarly, the metal binding extracellular polymers comprising
polysaccharides, proteins, humic substances etc. may detoxify metals
by chelating the heavy metals (Pulsawat et al., 2003). The bacterial
siderophores and organic acids can also reduce the metal bioavailability and toxicity by chelating the metal ions (Tripathi et al., 2005;
Dimkpa et al., 2008b). According to Dimkpa et al. (2008b), the
decreasing Ni concentration in cowpea plants is indicative of a Nibinding potential of hydroxamate siderophores. Further, metal
biosorption by microbial inoculants is particularly interesting from
a phytostabilization point of view. For instance, Madhaiyan et al.
(2007) reported that inoculation with endophytic bacteria, Magnaporthe oryzae and Burkholderia sp. increased plant growth but
reduced the Ni and Cd accumulation in roots and shoots of tomato
and also their availability in soil. This effect was due to the increased
metal biosorption and bioaccumulation by bacterial strains. In
addition, bacteria can also interact directly with the heavy metals to
reduce their toxicity and/or modulate their bioavailability: metal
dissolution by bacterial production of strong acids (i.e., H2SO4 produced
by Thiobacillus); production of ammonia or organic bases resulting in
metal hydroxide precipitates; fixation of Fe and Mn on the cell surface in
the form of hydroxides or some other insoluble metal salts; biotransformation via methylation, demethylation, volatilization, complex
formation, oxidation, or reduction (Chen and Cutright, 2003). Although
the establishment of a successful vegetative cover on metal-contaminated soils is challenging, the beneficial bacteria immobilizing heavy
metals and enhancing the plant tolerance to high metal concentrations
and/or promoting plant growth could provide a practical tool for
speeding up the phytostabilization process.
5. Concluding remarks and future perspectives
The role of soil microbiota, specifically rhizospheric and endophytic microorganisms, in the development of phytoremediation
techniques has to be elucidated in order to speed up the process and
to optimize the rate of mobilization/absorption/accumulation of
pollutants. To efficiently phytoremediate metal-contaminated soils,
the bioavailability of metals to plant roots is considered to be a critical
requirement for plant metal bioconcentration or bioimmobilization to
occur. In this regard, it may be possible to employ beneficial bacteria
to alter the bioavailability of metals for improving phytoremediation
of metal contaminants on large scale in the environment. Based on the
foregoing account, supra vide, microbe assisted phytoremediation is a
reliable and dependable process. Further, there are many areas of poor
understanding or lack of information where more research is needed.
These areas are as follows:
1. Very few studies have been published describing the interactions
between plants and microorganisms in metal-contaminated soils.
With the availability of functional properties (i.e., adapting strategies,
production of various metabolites, metal-resistant, biosorption as
well as mobilization/immobilization mechanisms, etc.) of bacterial
isolates, the factors required by bacteria to colonize the rhizosphere
and/or interior tissues of the plant, promote plant growth, and metal
uptake can be identified. Good colonization and survival of the
inoculums under real-life situations will be vital for this approach.
2. Scant information is available on bacterial mediated heavy metal
speciation changes in both rhizosphere and plant interior and to
determine whether such changes could have altered plant growth
and metal accumulation/distribution in plants.
3. Since the plant mediated processes, for example, the exudation of
organic acids or phytosiderophores, could also aid the solubilization and sequestration of metal ion from soil, further research,
including the interactive effects of the PGPB and plant root
mediated process on the solubilization and mobilization of metal
ions in soils, is required in order to explore the mechanisms
underlying bacteria-assisted phytoremediation.
4. In order to implement these PGPB-assisted phytoremediation in
the field level, intensive future research is needed on understanding the diversity and ecology of plant-associated PGPB in multiple
metal-contaminated soils. No doubt, further understanding of the
role of naturally adapted indigenous microbes that have been
cultured and enriched in the laboratory on phytoremediation
potential of various plants in multiple metal-contaminated soils
would also provide better results for improving this technology.
Acknowledgments
M.N.V.P. and H.F. thankfully acknowledge the financial support by
the Department of Science and Technology (DST), Government of
India, New Delhi [DST/INT/PORTUGAL/PO-22/04/16-7-2007], and
GRICES (Gabinete de Relacoes Internacionais da Ciencia e do Ensino
Superior, Ministerio da Ciencia, Technologia e Ensino Superior, Lisbon,
Portugal) in the frame work of the Indo-Portugal Programme of
Cooperation in Science and Technology.
References
Abou-Shanab RAI, Angle JS, Chaney RL. Bacterial inoculants affecting nickel uptake by
Alyssum murale from low, moderate and high Ni soils. Soil Biol Biochem 2006;38:
2882–9.
Abou-Shanab RA, Ghanem K, Ghanem N, Al-Kolaibe A. The role of bacteria on heavy-metal
extraction and uptake by plants growing on multi-metal-contaminated soils. World J
Microbiol Biotechnol 2008;24:253–62.
Adams DO, Yang SF. Ethylene biosynthesis: identification of l-aminocyclopropanecarboxylic acid as an intermediate in the conversion of methionine to ethylene.
Proc Natl Acad Sci U S A 1979;76:170–4.
Arkhipova TN, Prinsen E, Veselov SU, Martinenko EV, Melentiev AI, Kudoyarova GR.
Cytokinin producing bacteria enhance plant growth in drying soil. Plant Soil
2007;292:305–15.
Aslantas R, Cakmakci R, Sahin F. Effect of plant growth promoting rhizobacteria on
young apple tree growth and fruit yield under orchard conditions. Sci Hortic
2007;11:371–7.
Backman PA, Sikora RA. Endophytes: an emerging tool for biological control. Biol
Control 2008;26:1–3.
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM. The role of root exudates in rhizosphere
interactions with plants and other organisms. Annu Rev Plant Biol 2006;57:233–66.
Barka EA, Nowak J, Clément C. Enhancement of chilling resistance of inoculated
grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia
phytofirmans strain PsJN. Appl Environ Microbiol 2006;72:7246–52.
Barzanti R, Ozino F, Bazzicalupo M, Gabbrielli R, Galardi F, Gonnelli C, et al. Isolation and
characterization of endophytic bacteria from the nickel hyperaccumulator plant
Alyssum bertolonii. Microb Ecol 2007;53:306–16.
Belimov AA, Safronova VI, Mimura T. Response of spring rape to inoculation with plant
growth-promoting rhizobacteria containing 1-aminocyclopropane-1-carboxylate
deaminase depends on nutrient status of the plant. Can J Microbiol 2002;48:189–99.
Belimov AA, Dodd IC, Hontzeas N, Theobald JC, Safronova VI, Davies WJ. Rhizosphere
bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase yield
of plants grown in drying soil via both local and systemic hormone signalling. New
Phytol 2009;181:413–23.
Braud A, Jézéquel K, Vieille E, Tritter A, Lebeau T. Changes in extractability of Cr and Pb
in a polycontaminated soil after bioaugmentation with microbial producers of
biosurfactants, organic acids and siderophores. Water Air Soil Pollut 2006;6:3–4.
Braud A, Jézéquel K, Bazot S, Lebeau T. Enhanced phytoextraction of an agricultural Cr-, Hgand Pb-contaminated soil by bioaugmentation with siderophore producing bacteria.
Chemosphere 2009;74:280–6.
Burd GI, Dixon DG, Glick BR. Plant growth-promoting bacteria that decrease heavy
metal toxicity in plants. Can J Microbiol 2000;46:237–45.
Carrillo-Castañeda G, Munoz JJ, Peralta-Videa JR, Gomez E, Gardea-Torresdey JL. Plant
growth-promoting bacteria promote copper and iron translocation from root to
shoot in alfalfa seedlings. J Plant Nutr 2003;26:1801–14.
Chakraborty U, Chakraborty B, Basnet M. Plant growth promotion and induction of
resistance in Camellia sinensis by Bacillus megaterium. J Basic Microbiol 2006;46:
186–95.
Chen H, Cutright TJ. Preliminary evaluation of microbial mediated precipitation of
cadmium, chromium, and nickel by rhizosphere consortium. J Environ Eng
2003;129:4–9.
Chen YF, Etheridge N, Schaller GE. Ethylene signal transduction. Ann Bot (Lond)
2005;95:901–15.
Cheng Z, Park E, Glick BR. 1-aminocyclopropane-1-carboxylate deaminase from
Pseudomonas putida UW4 facilitates the growth of canola in the presence of salt.
Can J Microbiol 2007;53:912–8.
Y. Ma et al. / Biotechnology Advances 29 (2011) 248–258
Chet I, Inbar J. Biological control of fungal pathogens. Appl Biochem Biotechnol
1994;48:37–43.
Chung H, Park M, Madhaiyan M, Seshadri S, Song J, Cho H, et al. Isolation and
characterization of phosphate solubilizing bacteria from the rhizosphere of crop
plants of Korea. Soil Biol Biochem 2005;37:1970–4.
Compant S, Reiter B, Sessitsch A, Nowak J, Clement C, Barka EA. Endophytic colonization
of Vitis vinifera L. by a plant growth-promoting bacterium, Burkholderia sp. strain
PsJN. Appl Environ Microbiol 2005;71:1685–93.
Compant S, Clément C, Sessitsch A. Plant growth-promoting bacteria in the rhizo- and
endosphere of plants: their role, colonization, mechanisms involved and prospects
for utilization. Soil Biol Biochem 2010;42:669–78.
Conrath U, Beckers GJM, Flors V, García-Agustín P, Jakab G, Mauch F, et al. Priming:
getting ready for battle. Mol Plant–microbe Interact 2006;19:1062–71.
Contesto C, Desbrosses G, Lefoulon C, Béna G, Borel F, Galland M, et al. Effects of
rhizobacterial ACC deaminase activity on Arabidopsis indicate that ethylene
mediates local root responses to plant growth-promoting rhizobacteria. Plant Sci
2008;175:178–89.
Dary M, Chamber-Pérez MA, Palomares AJ, Pajuelo E. “In situ” phytostabilisation of
heavy metal polluted soils using Lupinus luteus inoculated with metal resistant
plant-growth promoting rhizobacteria. J Hazard Mater 2010;177:323–30.
Dell'Amico E, Cavalca L, Andreoni V. Improvement of Brassica napus growth under
cadmium stress by cadmium-resistant rhizobacteria. Soil Biol Biochem 2008;40:
74–84.
Dimkpa CO, Svatoš A, Dabrowska P, Schmidt A, Boland W, Kothe E. Involvement of
siderophores in the reduction of metal-induced inhibition f auxin synthesis in
Streptomyces spp. Chemosphere 2008a;74:19–25.
Dimkpa C, Svatoš A, Merten D, Büchel G, Kothe E. Hydroxamate siderophores
produced by Streptomyces acidiscabies E13 bind nickel and promote growth in
cowpea (Vigna unguiculata L.) under nickel stress. Can J Microbiol 2008b;54:
163–72.
Dimkpa CO, Merten D, Svatoš A, Büchel G, Kothe E. Metal-induced oxidative stress
impacting plant growth in contaminated soil is alleviated by microbial siderophores.
Soil Biol Biochem 2009a;41:154–62.
Dimkpa CO, Merten D, Svatos A, Büchel G, Kothe E. Siderophores mediate reduced and
increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus
annuus), respectively. J Appl Microbiol 2009b;107:1687–96.
Dobbelaere S, Vanderleyden J, Okon Y. Plant growthpromoting effects of diazotrophs in
the rhizosphere. Crit Rev Plant Sci 2003;22:107–49.
Duponnois R, Kisa M, Assigbetse K, Prin Y, Thioulouse J, Issartel M, et al. Fluorescent
pseudomonads occurring in Macrotermes subhyalinus mound structures decrease Cd
toxicity and improve its accumulation in sorghum plants. Sci Total Environ
2006;370:391–400.
Forchetti G, Masciarelli O, Alemano S, Alvarez D, Abdala G. Endophytic bacteria in
sunflower (Helianthus annuus L.): isolation, characterization, and production of
jasmonates and abscisic acid in culture medium. Appl Microbiol Biotechnol
2007;76:1145–52.
Ganesan V. Rhizoremediation of cadmium soil using a cadmium-resistant plant
growth-promoting rhizopseudomonad. Curr Microbiol 2008;56:403–7.
Glass ADM. Plant Nutrition: An Introduction to Current Concepts. Boston: Jones and
Bartlett Publishers; 1989. p. 234.
Glick BR. Phytoremediation: synergistic use of plants and bacteria to clean up the
environment. Biotechnol Adv 2003;21:383–93.
Glick BR. Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 2010;28:
367–74.
Glick BR, Penrose DM, Li J. A model for the lowering of plant ethylene concentrations by
plant growth-promoting bacteria. J Theor Biol 1998;190:63–8.
Glick BR, Cheng Z, Czarny J, Duan J. Promotion of plant growth by ACC deaminaseproducing soil bacteria. Eur J Plant Pathol 2007a;119(3):329–39.
Glick BR, Todorovic B, Czarny J, Cheng Z, Duan J, McConkey B. Promotion of plant
growth by bacterial ACC deaminase. Crit Rev Plant Sci 2007b;26:227–42.
Grandlic CJ, Mendez MO, Chorover J, Machado B, Maier RM. Plant growth-promoting
bacteria for phytostabilization of mine tailings. Int J Environ Sci Technol 2008;42:
2079–84.
Gray EJ, Smith DL. Intracellular and extracellular PGPR: commonalities and distinctions in the plant–bacterium signaling processes. Soil Biol Biochem 2005;37:
395–412.
Grčman H, Velikonja-Bolta S, Vodnik D, Kos B, Leštan D. EDTA enhanced heavy metal
phytoextraction: metal accumulation, leaching, and toxicity. Plant Soil 2001;235:
105–14.
Gutierrez-Manero FJ, Ramos-Solano B, Probanza A, Mehouachi J, Tadeo Francisco R, FR
Talon M. The plant growth-promoting rhizobacteria Bacillus pumilus and Bacillis
licheniformis produce high amounts of physiologically active gibberellins. Physiol
Plant 2001;111:206–11.
Gyaneshwar P, Naresh Kumar G, Parekh LJ, Poole PS. Role of soil microorganisms in
improving P nutrition of plants. Plant Soil 2002;245:83–93.
Hardoim PR, van Overbeek LS, van Elsas JD. Properties of bacterial endophytes and their
proposed role in plant growth. Trends Microbiol 2008;16:463–71.
He LY, Chen ZJ, Ren GD, Zhang YF, Qian M, Sheng XF. Increased cadmium and lead
uptake of a cadmium hyperaccumulator tomato by cadmium-resistant bacteria.
Exotoxicol Environ Saf 2009;72:1343–8.
He CQ, Tan GE, Liang X, Du W, Chen YL, Zhi GY, et al. Effect of Zn-tolerant bacterial
strains on growth and Zn accumulation in Orychophragmus violaceus. Appl Soil Ecol
2010a;44:1–5.
He LY, Zhang YF, Ma HY, Su LN, Chen ZJ, Wang QY, et al. Characterization of copperresistant bacteria and assessment of bacterial communities in rhizosphere soils of
copper-tolerant plants. Appl Soil Ecol 2010b;44:49–55.
257
Idris R, Trifonova R, Puschenreiter M, Wenzel WW, Sessitsch A. Bacterial communities
associated with flowering plants of the Ni hyperaccumulator Thaspi goesingense.
Appl Environ Microbiol 2004;70:2667–77.
Indiragandhi P, Anandham R, Madhaiyan M, Sa TM. Characterization of plant growthpromoting traits of bacteria isolated from larval guts of Diamondback moth Plutella
xylostella (Lepidoptera: Plutellidae). Curr Microbiol 2008a;56:327–33.
Indiragandhi P, Anandham R, Kim KA, Yim WJ, Madhaiyan M, Sa TM. Induction of
defense responses in tomato against Pseudomonas syringae pv. tomato by
regulating the stress ethylene level with Methylobacterium oryzae CBMB20
containing 1-aminocyclopropane-1-carboxylate deaminase. World. J Microbiol
Biotechnol 2008b;24:1037–45.
Jiang CY, Sheng XF, Qian M, Wang QY. Isolation and characterization of a heavy metalresistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its
potential in promoting plant growth and heavy metal accumulation in metalpolluted soil. Chemosphere 2008;72:157–64.
Jing Y, He Z, Yang X. Role of soil rhizobacteria in phytoremediation of heavy metal
contaminated soils. J Zhejiang Univ Sci 2007;8:192–207.
Kapulnik Y. Plant-growth-promoting rhizobacteria. In: Waisel Y, Eshel A, Kafkafi U, editors.
Plant Roots the Hidden Half. New York: Marcel Dekker Inc.; 1991. p. 347–62.
Khan MS, Zaidi A, Wani PA. Role of phosphate-solubilizing microorganisms in
sustainable agriculture—a review. Agron Sustain Dev 2007;27:29–43.
Kidd P, Barceló J, Bernal MP, Navari-Izzo F, Poschen C. Trace element behaviour at the root–
soil interface: implications in phytoremediation. Environ Exp Bot 2009;67:243–59.
Kloepper JW, Schroth MN. Plant growth-promoting rhizobacteria on radishes.
Proceedings of the 4th International Conference on Plant Pathogen Bacteria, 2.
1978. p. 879–82.
Kloepper JW, Ryu CM, Zhang S. Induced systemic resistance and promotion of plant
growth by Bacillus species. Phytopathology 2004;94:1259–66.
Kuffner M, Puschenreiter M, Wieshammer G, Gorfer M, Sessitsch A. Rhizosphere
bacteria affect growth and metal uptake of heavy metal accumulating willows.
Plant Soil 2008;304:35–44.
Kumar K, Singh N, Behlh HM, Srivastava S. Influence of plant growth promoting bacteria
and its mutant on heavy metal toxicity in Brassica juncea grown in fly ash amended
soil. Chemosphere 2008;72:678–83.
Kumar KV, Srivastava S, Singh N, Behl HM. Role of metal resistant plant growth
promoting bacteria in ameliorating fly ash to the growth of Brassica juncea. J Hazard
Mater 2009;170:51–7.
Ledin M, Krantz-Rulcker C, Allard B. Zn, Cd and Hg accumulation by microorganisms,
organic and inorganic soil components in multicompartment system. Soil Biol
Biochem 1996;28:791–9.
Li WC, Ye ZH, Wong MH. Effects of bacteria on enhanced metal uptake of the Cd/Znhyperaccumulating plant, Sedum alfredii. J Exp Bot 2007;58:4173–82.
Lim SR, Schoenung JM. Human health and ecological toxicity potentials due to heavy
metal content in waste electronic devices with flat panel displays. J Hazard Mater
2010;177:251–9.
Lodewyckx C, Vangronsveld J, Porteous F, Moore ERB, Taghavi S, van der Lelie D.
Endophytic bacteria and their potential applications. Crit Rev Plant Sci 2002;21:
583–606.
Ma Y, Rajkumar M, Freitas H. Inoculation of plant growth promoting bacterium
Achromobacter xylosoxidans strain Ax10 for the improvement of copper phytoextraction by Brassica juncea. J Environ Manage 2009a;90:831–7.
Ma Y, Rajkumar M, Freitas H. Improvement of plant growth and nickel uptake by nickel
resistant-plant growth promoting bacteria. J Hazard Mater 2009b;166:1154–61.
Ma Y, Rajkumar M, Freitas H. Isolation and characterization of Ni mobilizing PGPB from
serpentine soils and their potential in promoting plant growth and Ni accumulation
by Brassica spp. Chemosphere 2009c;75:719–25.
Madhaiyan M, Poonguzhali S, Sa T. Metal tolerating methylotrophic bacteria reduces
nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon
esculentum L.). Chemosphere 2007;69:220–8.
Mansour SA, Gad MF. Risk assessment of pesticides and heavy metals contaminants in
vegetables: a novel bioassay method using Daphnia magna Straus. Food Chem
Toxicol 2010;48:377–89.
Mastretta C, Taghavi S, van der Lelie D, Mengoni A, Galardi F, Gonnelli C, et al. Endophytic
bacteria from seeds of Nicotiana tabacum can reduce cadmium phytotoxicity. Int J
Phytorem 2009;11:251–67.
Mayak S, Tirosh T, Glick BR. Plant growth-promoting bacteria confer resistance in
tomato plants to salt stress. Plant Physiol Biochem 2004;42:565–72.
McBride MB. Environmental Chemistry in Soils. Oxford: Oxford Univ. Press; 1994.
p. 406.
Miethke M, Marahiel MA. Siderophore-based iron acquisition and pathogen control.
Microbiol Mol Biol Rev 2007;71:413–51.
Murphy JF, Zehnder GW, Schuster DJ, Sikora EJ, Polstan JE, Kloepper JW. Plant growthpromoting rhizobacteria mediated protection in tomato against tomato mottle
virus. Plant Dis 2000;84:779–84.
Nagarajkumar M, Bhaskaran R, Velazhahan R. Involvement of secondary metabolites and
extracellular lytic enzymes produced by Pseudomonas fluorescens in inhibition of
Rhizoctonia solani, the rice sheath blight pathogen. Microbiol Res 2004;159:73–81.
Nautiyal CS, Mehta S, Singh HB. Biological control and plant-growth promotion by
Bacillus strains from milk. J Microbiol Biotechnol 2006;16:184–92.
Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, et al. A plant miRNA
contributes to antibacterial resistance by repressing auxin signaling. Science
2006;312:436–9.
Pal SS. Interaction of an acid tolerant strain of phosphate solubilizing bacteria with a
few acid tolerant crops. Plant Soil 1998;198:169–77.
Patten CL, Glick BR. Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol
1996;42:207–20.
258
Y. Ma et al. / Biotechnology Advances 29 (2011) 248–258
Penrose DM, Glick BR. Levels of 1-aminocyclopropane-1-carboxylic acid (ACC) in
exudates and extracts of canola seeds treated with plant growth-promoting
bacteria. Can J Microbiol 2001;47(4):368–72.
Perrig D, Boiero ML, Masciarelli OA, Penna C, Ruiz OA, Cassan FD, et al. Plant-growthpromoting compounds produced by two agronomically important strains of
Azospirillum brasilense, and implications for inoculant formulation. Appl Microbiol
Biotechnol 2007;75:1143–50.
Persello-Cartieaux F, Nussaumev L, Robaglia C. Tales from the underground: molecular
plant–rhizobacteria interactions. Plant Cell Environ 2003;26:189–99.
Pillay VK, Nowak J. Inoculum density, temperature, and genotype effects on in vitro
growth promotion and epiphytic and endophytic colonization of tomato
(Lycopersicon esculentum L) seedlings inoculated with a pseudomonad bacterium.
Can J Microbiol 1997;43:354–61.
Ping L, Boland W. Signals from the underground: bacterial volatiles promote growth in
Arabidopsis. Trends Plant Sci 2004;9:263–6.
Pulsawat W, Leksawasdi N, Rogers PL, Foster LJR. Anions effects on biosorption of Mn(II) by
extracellular polymeric substance (EPS) from Rhizobium etli. Biotechnol Lett 2003;25:
1267–70.
Rajkumar M, Freitas H. Effects of inoculation of plant-growth promoting bacteria on Ni
uptake by Indian mustard. Bioresour Technol 2008a;99:3491–8.
Rajkumar M, Freitas H. Influence of metal resistant-plant growth-promoting bacteria
on the growth of Ricinus communis in soil contaminated with heavy metals.
Chemosphere 2008b;71:834–42.
Rajkumar M, Nagendran R, Lee KJ, Lee WH, Kim SZ. Influence of plant growth promoting
bacteria and Cr6+ on the growth of Indian mustard. Chemosphere 2006;62:741–8.
Rajkumar M, Ma Y, Freitas H. Characterization of metal-resistant plant-growth
promoting Bacillus weihenstephanensis isolated from serpentine soil in Portugal.
J Basic Microbiol 2008;48:1–9.
Rajkumar M, Ae N, Freitas H. Endophytic bacteria and their potential to enhance heavy
metal phytoextraction. Chemosphere 2009;77:153–60.
Rajkumar M, Ae N, Prasad MNV, Freitas H. Potential of siderophore-producing bacteria
for improving heavy metal phytoextraction. Trends Biotechnol 2010;28:142–9.
Rashotte AM, Brady SR, Reed RC, Ante SJ, Muday GK. Basipetal auxin transport is
required for gravitropism in roots of arabidopsis. Plant Physiol 2000;122:481–90.
Raupach GS, Liu L, Murphy JF, Tuzun S, Kloepper JW. Induced systemic resistance in
cucumber and tomato against cucumber mosaic virus using plant growth-promoting
rhizobacteria. Plant Dis 1996;80:891–4.
Rouch DA, Lee TOB, Morby AP. Understanding cellular responses to toxic agents: a
model for mechanisms-choice in bacterial resistance. J Ind Microbiol 1995;14:
132–41.
Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN. Bacterial endophytes: recent
developments and applications. FEMS Microbiol Lett 2008;278:1–9.
Ryu CM, Hu CH, Locy RD, Kloepper JW. Study of mechanisms for plant growth
promotion elicited by rhizobacteria in Arabidopsis thaliana. Plant Soil 2005;268:
285–92.
Safronova VI, Stepanok VV, Engqvist GL, Alekseyev YV, Belimov AA. Root associated
bacteria containing 1-aminocyclopropane-1-1carboxylate deaminase improve
growth and nutrient uptake by pea genotypes cultivated in cadmium supplemented soil. Biol Fertil Soils 2006;42:267–72.
Saravanan VS, Madhaiyan M, Thangaraju M. Solubilization of zinc compounds by the
diazotrophic, plant growth promoting bacterium Gluconacetobacter diazotrophicus.
Chemosphere 2007;66:1794–8.
Schouten A, van der Berg G, Edel-Hermann V, Steinberg C, Gautheron N, Alabouvette C,
et al. Defense responses of Fusarium oxysporum to 2,4-diacetylphloroglucinol, a broadspectrum antibiotic produced by Pseudomonas fluorescens. Mol Plant–microbe
Interact 2004;17:1201–11.
Schulz B, Boyle C. What are endophytes? In: Schulz BJE, Boyle CIC, Sieber TN, editors.
Microbial Root Endophytes. Berlin: Springer-Verlag; 2006. p. 1-13.
Sheng XF, Xia JJ. Improvement of rape (Brassica napus) plant growth and cadmium
uptake by cadmium-resistant bacteria. Chemosphere 2006;64:1036–42.
Sheng XF, He LY, Wang QY, Ye HS, Jiang C. Effects of inoculation of biosurfactantproducing Bacillus sp. J119 on plant growth and cadmium uptake in a cadmiumamended soil. J Hazard Mater 2008a;155:17–22.
Sheng XF, Xia JJ, Jiang CY, He LY, Qian M. Characterization of heavy metal-resistant
endophytic bacteria from rape (Brassica napus) roots and their potential in
promoting the growth and lead accumulation of rape. Environ Pollut 2008b;156:
1164–70.
Sikora RA, Schafer K, Dababat AA. Modes of action associated with microbially induced
in planta suppression of plant–parasitic nematodes. Australas Plant Pathol 2007;36:
124–34.
Sinha S, Mukherjee SK. Cadmium-induced siderophore production by a high Cd-resistant
bacterial strain relieved Cd toxicity in plants through root colonization. Curr Microbiol
2008;56:55–60.
Sun LN, Zhang YF, He LY, Chen ZJ, Wang QY, Qian M, et al. Genetic diversity and
characterization of heavy metal-resistant-endophytic bacteria from two coppertolerant plant species on copper mine wasteland. Bioresour Technol 2010;101:501–9.
Sziderics AH, Rasche F, Trognitz F, Sessitsch A, Wilhelm E. Bacterial endophytes
contribute to abiotic stress adaptation in pepper plants (Capsicum annuum L.). Can J
Microbiol 2007;53:1195–202.
Taghavi S, Garafola C, Monchy S, Newman L, Hoffman A, Weyens N, et al. Genome
survey and characterization of endophytic bacteria exhibiting a beneficial effect on
growth and development of poplar. Appl Environ Microbiol 2009;75:748–57.
Tokala RK, Strap JL, Jung CM, Crawford DL, Salove H, Deobald LA, et al. Novel plant–
microbe rhizosphere interaction involving S. lydicus WYEC108 and the pea plant
(Pisum sativum). Appl Environ Microbiol 2002;68:2161–71.
Tripathi M, Munot HP, Shouche Y, Meyer JM, Goel R. Isolation and functional
characterization of siderophore-producing lead- and cadmium-resistant Pseudomonas
putida KNP9. Curr Microbiol 2005;50:233–7.
Trivedi P, Pandey A, Sa T. Chromate reducing and plant growth promoting activities of
psychrotrophic Rhodococcus erythropolis MtCC 7905. J Basic Microbiol 2007;47:
513–7.
Trivedi P, Pandey A, Palni LMS. In vitro evaluation of antagonistic properties of
Pseudomonas corrugate. Microbiol Res 2008;163:29-336.
van der Heijden MGA, Bardgett RD, van Straalen NM. The unseen majority: soil
microbes as drivers of plant diversity and productivity in terrestrial ecosystems.
Ecol Lett 2008;11:296–310.
van Loon LC, Bakker PAHM, Pieterse CMJ. Systemic resistance induced by rhizosphere
bacteria. Annu Rev Phytopathol 2004;36:453–83.
van Loon LC, Rep M, Pieterse CMJ. Significance of inducible defence-related proteins in
infected plants. Annu Rev Phytopathol 2006;44:1-28.
van Overbeek L, van Elsas JD. Effects of plant genotype and growth stage on the
structure of bacterial communities associated with potato (Solanum tuberosum L.).
FEMS Microbiol Ecol 2008;64:283–96.
Vessey JK. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 2003;255:
571–86.
Vivas A, Biro B, Ruíz-Lozanoa JM, Azcon R. Two bacterial strains isolated from a Zn-polluted
soil enhance plant growth and mycorrhizal efficiency under Zn toxicity. Chemosphere
2006;52:1523–33.
Walker TS, Bais HP, Grotewold E, Vivanco JM. Root exudation and rhizosphere biology.
Plant Physiol 2003;132:44–51.
Wang KLC, Li H, Ecker JR. Ethylene biosynthesis and signaling networks. Plant Cell
2002;14:S131–51.
Wani PA, Khan MS, Zaidi A. Effect of metal tolerant plant growth promoting
Bradyrhizobium sp. (vigna) on growth, symbiosis, seed yield and metal uptake by
greengram plants. Chemosphere 2007a;70:36–45.
Wani PA, Khan MS, Zaidi A. Effect of metal-tolerant plant growth-promoting Rhizobium
on the performance of pea grown in metal-amended soil. Arch Environ Contam
Toxicol 2007b;55:33–42.
Wani PA, Khan MS, Zaidi A. Chromium reduction, plant growth-promoting potentials,
and metal solubilization by Bacillus sp. isolated from alluvial soil. Curr Microbiol
2007c;54:237–43.
Wei G, Kloepper JW, Tuzun S. Induction of systemic resistance of cucumber to
Colletotrichum orbiculare by select strains of plant growth-promoting rhizobacteria.
Phytopathology 1991;81:1508–12.
Welbaum GE, Sturz AV, Dong Z, Nowak J. Managing soil microorganisms to improve
productivity of agro-ecosystems. Crit Rev Plant Sci 2004;23:175–93.
Wu CH, Wood TK, Mulchandani A, Chen W. Engineering plant–microbe symbiosis for
rhizoremediation of heavy metals. Appl Environ Microbiol 2006a;72:1129–34.
Wu SC, Cheung KC, Luo YM, Wong MH. Effects of inoculation of plant growth-promoting
rhizobacteria on metal uptake by Brassica juncea. Environ Pollut 2006b;140:124–35.
Xie H, Pasternak JJ, Glick BR. Isolation and characterization of mutants of the plant
growth-promoting rhizobacterium Pseudomonas putida GR12-2 that overproduce
indoleacetic acid. Curr Microbiol 1996;32:67–71.
Xiong J, He Z, Liu D. The role of bacteria in the heavy metals removal and growth of
Sedum alfredii Hance in an aqueous medium. Chemosphere 2008;70:489–94.
Zaida A, Khan MS, Amil MD. Interactive effect of rhizotrophic microorganisms on yield
and nutrient uptake of chickpea (Cicer arietinum L.). Eur J Agron 2003;19:15–21.
Zaidi S, Usmani S, Singh BR, Musarrat J. Significance of Bacillus subtilis strain SJ-101 as a
bioinoculant for concurrent plant growth promotion and nickel accumulation in
Brassica juncea. Chemosphere 2006;64:991–7.