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Vol. 7(51), pp. 5781-5788, 29 December, 2013
DOI: 10.5897/AJMR2013.6461
ISSN 1996-0808 ©2013 Academic Journals
http://www.academicjournals.org/AJMR
African Journal of Microbiology Research
Review
Influence of phytosiderophore on iron and zinc uptake
and rhizospheric microbial activity
M. L. Dotaniya1*, Dasharath Prasad2, H. M. Meena3, D. K. Jajoria4, G. P. Narolia4, K. K.
Pingoliya4, O. P. Meena2, Kuldeep Kumar5, B. P. Meena1, Asha Ram6, H. Das1 ,
M. Sreenivasa Chari7 and Suresh Pal8
1Indian Institute of Soil Science, Bhopal, India.
2Swami Keshwanand Rajasthan Agricultural University, Bikaner, India.
3Central Arid Zone Research Institute, Jodhpur, India.
4 Maharana Pratap University of Agriculture and Technology, Udaipur, India.
5Central Soil and Water Conservation Research and Training Institute, Dehradun, India.
6National Research Centre for Agroforestry, Jhansi, India.
7Agricultural Research Station, Utukur, Kadapa, India.
8Agricultural Scientists Recruitment Board, New Delhi, India.
Accepted 12 December, 2013
Micronutrients play a vital role in crop production and sustainable crop yield. High crop yield varieties
make soil micronutrients deficient, without incorporating external inputs. Due to deficiency of
micronutrients such as iron (Fe) and zinc (Zn), yield decline drastically. It limits more than
macronutrients, but requirements of these plant nutrients are very less, but plants have self regulated
mechanism, which secrete the phytosiderophore (PS) and mobilize the lower concentration of these
metals to soil solution for easy uptake by plants. Phytosiderophore production is a general response of
plants to Fe and Zn deficiency in particular. The uptake rate of PS-chelated Fe and Zn is 100 and 5 to 10
times higher than that of free Fe and Zn, respectively. Higher amount of carbon containing organic
compounds enhanced the microbial activities in rhizosphere and alter the plant nutrient chemistry in
soil. This article discussed the importance of PS in microbial activity in soil and nutrient uptake
mechanism in plants.
Key words: Iron, phytosiderophores, rhizospheric microbial activity, zinc.
INTRODUCTION
One of the widest ranging abiotic stresses in world
agriculture arises from low iron (Fe) and zinc (Zn)
availability in calcareous soils, particularly in cereals
(Berg et al., 1993; Palmiter and Findley, 1995). A higher
Zn acquisition efficiency, further, may be due to either or
all of the following: an efficient ionic Zn uptake system,
better root architecture that is long and fine roots with
architecture favoring exploitation of Zn from larger soil
volume (Richardson et al., 1989), higher synthesis and
release of Zn-mobilizing phytosiderophore (PS) by the
roots and uptake of Zn-PS complex (Dotaniya et al.,
2013a). Zinc and Fe are the two most important
micronutrients in crop production. More than 50% of the
Indian soils are suffering from zinc and iron deficiency. It
is also a big problem in well aerated calcareous soil. The
release of PS is one of the most important mechanisms
which enhances the mobilization of Fe and Zn in soil and
their uptake by crops (Ackland and McArdle, 1990;
*Corresponding author E-mail: mohan30682@gmail.com.
5782 Afr. J. Microbiol. Res.
Figure 1. Origin of various pools of rhizodeposition (Dennis et al., 2010).
Bar-Ness et al., 1992). Peanut/maize intercropping was a
sustainable and effective agroecosystem that evidently
enhances the Fe nutrition of peanuts in calcareous soils
by the influence of PS (Xiong et al., 2013).
PHYTOSIDEROPHORES
Phytosiderophores are organic substances (such as
nicotinamine, mugineic acids (MAs) and avenic acid etc)
produced by plants (Figure 1) (Mori and Nishizawa, 1987)
under Fe-deficient conditions, which can form organic
complexes or chelates with Fe3+, and increase the
movement of iron in soil (Ueno et al., 2007). It is non
proteineous, low molecular weight acids released by the
graminaceous species under the iron (Wallace, 1991)
and Zn deficiency stress. The PS mobilize micronutrients
Fe, Zn, Mn and Cu from the soils to plant in deficient
condition (Takagi et al., 1984).
Characteristics of phytosiderophores
1) These are molecules with high affinity for Fe3+, and
remove the Fe3+ from minerals and contribute towards
their dissolution.
2) These Fe-chelates are highly soluble and stable over a
wide pH range.
3) They are of crucial importance for the zinc and iron
transport in soils and its supply to plants.
4) Zn-PS have similar structural confirmations as Fe-PS
and a similar regulatory mechanism for the biosynthesis
and/or release of PS under both Zn and Fe deficiencies.
5) A plant releases PS at higher amounts about a few
hours to the onset of the light period. Under continuous
darkness or continuous light, the rate of release of PS is
lower.
6) There has been observed a sharp rise in PS
production three hours after onset of the light period,
which gradually declines thereafter.
IRON DEFICIENCY: A GLOBAL CONCERN
Fe deficiency chlorosis in crop plants is a widespread
nutrient problem particularly in calcareous soils in arid
and semiarid regions, which often results in significant
yield losses (Mortvedt, 1991). Such yield reductions have
been reported in many crops, such as upland rice, maize
and sorghum (Jolley et al., 1996; Dotaniya et al., 2013b).
Dotaniya et al. 5783
Figure 2. Strategy of Fe Acquisition by plants (Tagliavini and Rombola, 2001).
Grazing induced Fe-deficiency chlorosis in wheat was
also reported (Berg et al., 1993). Soil amendments and
foliar sprays of Fe are common methods to correct Fe
deficiency (Bashir et al., 2010). However, these methods
are expensive, time-consuming and may not be effective
for more than one cropping season. Alternatively,
breeding of plant genotypes with higher efficiency in the
acquisition of Fe from the soil is a realistic approach
(Kobayashi and Nishizawa, 2012). Selection for resis-
tance, however, is difficult because of heterogeneous soil
and highly variable environmental conditions that affect
expression of Fe-deficiency chlorosis in the field (Nozoye
et al., 2011). Yellow stripe 1 (ys1) and ys3 are recessive
mutants of maize (Zea mays L.) that show typical
symptoms of Fe deficiency, that is interveinal chlorosis of
the leaves (Tomoko et al., 2013).
A lack of understanding of the factors influencing
chlorosis expression has also impeded the development
of reliable screening methods in the laboratory, controlled
greenhouse, or environmental-chamber environment
(Jolley et al., 1996). So the development of reliable Fe-
deficiency chlorosis screening criterion is a necessary
prerequisite for significant improvement of Fe-deficiency
chlorosis resistance. Recently, many studies suggested
that non-proteinogenic amino acids (PS) release has
been linked to the ability of species and genotypes to
resist Fe- deficiency chlorosis (Hansen et al., 1996;
Romheld and Marschner, 1986). Therefore, PS release
has been suggested as a selection criterion for Fe
efficient graminaceous monocots.
ZINC DEFICIENCY: A GLOBAL CONCERN
Low availability of Zn in calcareous soils is one of the
widest ranging abiotic stresses in world agriculture
particularly in Turkey, Australia, China and India. Global
studies initiated by the Food and Agriculture Organization
(FAO) reported Zn deficiency in 50% of the soil samples
collected from 25 countries (Hansen et al., 1996). It is
one of the most widespread nutritional constraints in crop
plants, especially in cereals. Among cereals, wheat and
rice in particular, suffer from its deficiency. The yield
reduction up to 80% along with reduced grain Zn level
has been observed under Zn deficiency (Fageria et al.,
2002). This deficiency is a serious implication for human
health in countries where consumption of cereal-based
diets predominates. Further, plants grown on zinc-
deficient soils tend to accumulate heavy metals, which
again is a potential human health hazard.
STRATEGY OF FE AND ZN ACQUISITION BY PLANTS
Iron and Zn deficiency induced chlorosis represents the
main nutritional disorder in plants grown on calcareous
and/or alkaline soils because of an extremely low
solubility of soil Fe. Mechanisms of Fe acquisition in
higher plants have been grouped into Strategy I and II
(Figure 2). Strategy I plants (Tagliavini and Rombola,
2001), which include dicotyledons and non-graminaceous
monocotyledons, respond to Fe deficiency by extruding
both protons and reducing substances (phenols) from the
roots, and by enhancing the ferric reduction activity at the
root plasma membrane. This strategy is similar to the Zn
acquisition by plants. The solubilized Fe must be reduced
from Fe+3 to Fe+2 on the plasma membrane before Fe+2
is transported into the root cell through a specific Fe+2
transporter. Strategy II plants (graminaceous species)
synthesize and secrete Fe-chelating substances,
mugineic acids (MAs) from their roots to dissolve
sparingly soluble Fe compounds in the rhizosphere
(Figure 3) (Marschner et al., 1986) and affected by soil
bacteria (Chattopadhyay, 2006; Dipanwita and
Chattopadhyay, 2013). Iron is transported across the
plasma membrane as a complex of PS- Fe+3 through a
specific transport system without prior reduction.
The synthesis of mugineic acid is induced by Fe-
deficiency. The chemical constituents, number and
amount of mugineic acid synthesized and secreted into
the rhizosphere may differ among species and even
cultivars (Xiong et al., 2013). In general, the amount of
5784 Afr. J. Microbiol. Res.
Figure 3. Schematic representations of important processes in strategy II iron acquisition (Dotaniya et al., 2013a).
MAs secreted correlates positively with the ability of the
plants to tolerate Fe deficiency. But siderophore
produced by microbes also enhanced the Fe uptake. If
siderophores and PS are present at similar
concentrations, Fe is preferentially bound to the
siderophores, which may even remove Fe from the Fe-
PS complex. In contrast to many bacterial siderophores,
rhizoferrin from the fungus Rhizopus arrhizus has only a
slightly higher affinity towards Fe compared to PS
(Crowley and Gries, 1994; Zelenev et al., 2005).
Rhizoferrin is a good Fe source for barley, probably
because of exchange of Fe from rhizoferrin to the PS
(Yehuda et al., 1996). It can be amply surmised from the
available literature that Zn and Fe efficiency of cereals
under deficiency is regulated by several factors, most
importantly, the presence of an efficient Zn2+, Fe+2 and PS
complex uptake system.
Manipulation of phytosideriophore biosynthesis and
release is a promising strategy to improve Fe and Zn
efficiency in cereal crops (Wallace, 1991). In Alice maize
cultivar, Zn uptake decreased with increasing stability
constant of the chelate in the order: ZnSO4 (greater than
or equal to) Zn-desferrioxamine > Zn-PS > Zn-EDTA.
Adding a 500-fold excess of free PS over Zn to the
uptake solution depressed Zn uptake in maize mutant
ys1 almost completely (von Wiren et al., 1996). It may be
quite plausible that iron and zinc deficiency tolerance of
graminaceous species can also be achieved through
manipulation of key enzymes of PS biosynthesis that is
Nicotianamine synthase (NAS) and Nicotianamine amino-
transferase (NAAT). This will help in reducing and may
be even totally eliminating the application of zinc and iron
fertilizers to the soil.
EFFECT ON MICROBIAL ACTIVITIES IN
RHIZOSPHERE
The rhizosphere is the narrow region of soil that is
directly influenced by root secretions and associated soil
microorganisms (Giri et al., 2005). Soil which is not part
of the rhizosphere is known as bulk soil. The rhizosphere
contains many bacteria that feed on sloughed-off plant
cells, termed rhizodeposition and the proteins and sugars
released by roots (Curl and Truelove, 1986). It is a
densely microbial populated area of soil in which the
roots must compete with the invading root systems of
neighboring plant species for space, water, and mineral
nutrients, and with soil-borne microorganisms, including
bacteria, fungi, and insects feeding on an abundant
source of organic material (Ryan and Delhaize, 2001).
In 1904, the German agronomist and plant physiologist
Lorenz Hiltner first coined the term "rhizosphere" to
describe the plant-root interface (Figure 4), a word
originating in part from the Greek word "rhiza", meaning
root (Hiltner, 1904; Hartmann et al., 2008). Microbial
population is more affected by the amount and type of C
in soil (Akiyama et al., 2005). Under long term study, it
was found that microbial population is greater in organic
soil as compared to inorganic farming plots (Tu et al.,
2005). In general 10-20% more biomass was measured
in organic soils (Gelsomino et al., 2004). High
secretion of PS in soil, improved the soil fertility and
nutrient mobility in soil (Colmer and Bloom, 1998).
Microbial biomass is an indicator of soil microbial
activities. Generally, in crop production, more biomass
means more fertile soil, which is a good indicator of plant
nutrient (Becard et al., 1992, 1995; Trieu et al., 1997).
Root secretions may play symbiotic or defensive roles as
a plant ultimately engages in positive or negative
communication (Stintzi and Browse, 2000; Stotz et al.,
2000), depending on the other elements of its rhizo-
sphere such as available nutrients, water, space CO2
concentration and C. In contrast to the extensive
progress in studying plant-plant, plant-microbe (Keyes et
al., 2000) and plant-insect interactions that occur in
above ground plant organs such as leaves and stems,
very little research has focused on root-root, root-
microbe, and root-insect interactions in the rhizosphere
Dotaniya et al. 5785
Figure 4. Structure of the rhizosphere in soil (McNear, 2013).
(Shannon et al., 2002). Bacterial siderophores are usually
poor Fe sources for both monocot and dicot plants (Bar-
Ness et al., 1992; Crowley et al., 1992; Walter et al.,
1994). However, in some cases, microbial siderophores
have alleviated Fe deficiency-induced chlorosis in dicots
(Jurkevitch et al., 1988; Sharma et al., 2003; Wang et al.,
1993; Yehuda et al., 2000). On the other hand, plant-
derived Fe-PS complexes appear to be a good Fe source
for bacteria (Jurkevitch et al., 1993; Marschner and
Crowley, 1998).
The organic compounds released through these
processes can be further divided into high and low
molecular weight (HMW and LMW, respectively). By
weight, the HMW compounds which are those complex
molecules that are not easily used by microorganisms
(mucilage, cellulose) make up the majority of C released
from the root (Chin-A-Woeng et al., 1997); however, the
LMW compounds are more diverse and thus have a
wider array of known or potential functions (Bauer and
Mathesius, 2004). Rooting density has a large effect on
uptake per unit PS secretion as a result of overlap of the
zones of influence of neighboring roots (Von Wiren et al.,
1996). The list of specific LMW compounds released from
roots is very long, but can generally be categorized into
organic acids, amino acids, proteins, sugar, phenolics
and other secondary metabolites which are generally
more easily used by microorganisms. It provides the C
source of energy and food, because of plenty of organic
compounds released from roots enhanced the microbial
activity and population. Further increase in microbial
population accelerates the competition for water, C and
space also (Baudoin et al., 2003).
EFFECT OF FERTILITY AND ATMOSPHERIC CO2
CONCENTRATION ON PHYTOSIDEROPHORE
Root exudates is secreted from root in two way: (1)
actively released from the root and (2) by diffuseness
which are passively released due to osmotic differences
between soil solution and the cell (Dakora and Phillips
2002), or lysates from autolysis of epidermal and cortical
cells. These organic compounds may be sugar, non-
protein amino acids mugineic acid (of barley) and avenic
acid (of oats) (Darrah, 1991). Das and Dkhar (2011)
conducted a research with various organic and inorganic
fertilizers and their effect on physico-chemical properties
of rhizosphere (Table 1). They observed that the
application of vermicompost resulted in most pronounced
growth of microbial population compared to inorganic
treatment. Also, application of organic treatments showed
increased rhizosphere soil physicoche-mical properties
which in return lead to the increased microbial population
which is of great importance in nutrient availability of the
studied soil (Kundu et al., 2013). The soil microbial
population also secrets a significant amount of sidero-
phores in soil, however it promotes the root exudates
from plants (Bais et al., 2001). The root exudates play an
important role in root microbe interactions. Flavonoids are
present in the root exudates of legumes that activate
Rhizobium meliloti genes responsible for the nodulation
process (Peters et al., 1986). Fertilizer and lime
applications typically result in increased bacterial
numbers and decreased fungal biomass (Lovell et al.,
1995).
Bacterial communities in the rhizosphere are not static,
but will fluctuate over time in different root zones, and
bacterial composition will differ between different soil
types, plant species, plant growth seasons and local
communities (Semenov and Brooks, 1999). Changes
induced in the soil by the growing root provide additional
niches for soil microbes. Soil types and growth stages are
important factors in shaping rhizobacterial community
structure (Latour et al., 1996; Seldin et al., 1998;
Herschkovitz et al., 2005) and may be the strongest
factor affecting bacterial communities in potato rhizo-
5786 Afr. J. Microbiol. Res.
Table 1. Physico-chemical properties of rhizosphere soil influenced by organic and inorganic fertilizers (Das and Dkhar, 2011).
Treatment
pH
Moisture
content
SOC
(%)
Total N
(%)
Av- P
(μ/g)
K
(mg/g)
Soil Respiration
(mg/g)
MBC
(μ/g)
Plant compost
5.6
24.90
1.80
0.32
1.18
0.04
65.1
1015.0
Vermicompost
5.4
24.24
1.50
0.31
2.66
0.05
66.11
2145.7
Integrated plant compost
5.6
24.68
1.75
0.35
2.01
0.04
64.56
1385.1
FYM
4.6
23.82
1.27
0.31
2.24
0.08
56.5
940.9
Control
4.9
23.39
1.60
0.28
2.01
0.05
56.56
656.5
NPK
4.9
23.39
1.60
0.35
2.68
0.04
62.89
798.9
Figure 5. Annual greenhouse gas emissions by sector (www.e-education.psu.edu).
sphere (Van Overbeck and Van Elsas, 2008); plant
species (Grayston et al., 1998; Smalla et al., 2001) and
even ‘cultivar (genotype) within the same species
(Andreote et al., 2009). The rhizosphere is a highly
dynamic environment for bacterial communities and even
small topographical landform changes can alter environ-
mental conditions that may accelerate or retard the
activity of organisms (Ramette et al., 2005).
Soil microbial activities affected the physical, chemical
and biological activities and ultimately crop production.
Increasing environmental factors like CO2 concentration
and atmospheric temperature affected the root exudates
and rhizospheric microbial population. Impacts of
elevated CO2 on soil ecosystems, focuse primarily on
plants and a variety of microbial processes. The
processes considered include changes in microbial
biomass of C and N, soil enzyme activity, microbial
community composition, organic matter decomposition,
and functional groups of bacteria mediating trace gas
emission in terrestrial and wetland ecosystems. Except
from CO2, other gases that is CH4, N2O and other gases
play a significant role in global climate phenomena
(Figure 5).
The cocktail of chemicals released is influenced by
plant species, edaphic and climactic conditions which
together shape and are shaped by the microbial
community within the rhizosphere. There is still very little
known about the role that a majority of the LMW
compounds play in influencing rhizosphere processes
(Cheng et al., 1996). A growing body of literature is
beginning to lift the veil on the many functions of root
exudates as a means of acquiring nutrients (acquisition of
Fe and P), agents of invasiveness (that is allelopathy) or
as chemical signals to attract symbiotic partners
(chemotaxis) (rhizobia and legumes) or the promotion of
beneficial microbial colonization on root surfaces
(Bacillus subtilis, Pseudomonas florescence) (Bais et al.,
2004, Park et al., 2003).
FUTURE NEED OF RESEARCH
1) More research should be on the biotechnological side,
separation and insertion of high phytosiderophor
responsible gene in crop plant, which is crucial for crop
production in low fertility areas.
2) Also, research should be done on the use of
alternative combat methods, against elevated CO2
concentration without compromising positive effect on PS
release.
CONCLUSIONS
A healthy crop production requires a good status of plant
nutrient. It play crucial role in plant metabolism and
ultimately in edible part. In nutrient deficient condition,
plant growth is limited and poor yield is obtained.
Phytosiderophors are secreted from plant root, and it is a
life saving mechanism in plants. It enhances the plant
nutrient uptake and improves the soil health. Iron
availability is low in most aerobic soil, and microorga-
nisms and plants release low molecular-weight com-
pounds (chelators) which increase Fe availability. It spe-
cially enhances the uptake of Fe and Zn in lower
concentration. Increasing root exudates in soil enhances
the soil fertility level as well as microbial biomass. These
soil microbes play vital role in nutrient transformation
reactions in soil and nutrient uptake by crop plants.
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