Download Bacteria in Agrobiology

Editors
Dinesh K. Maheshwan
Dept. of Botany Mic¡obiology
Meenu Saraf
University School of ScieDoes
Dep. Microbiology and Biotecl ology
curukul Kang¡i Unive¡sity
Gujarat Univerily
Ahmedabad (Gujarat), India
Ha¡idwar (Uttarakhand), India
Abhiflav Aeron
Department of Biosciences
DAV (PG) CoUege
Muzaffamagar (Uttar Pradesh)
India
rsBN
97 8-3 -642-37 240-'7
ÍSBN 9'78 3'642'31241 4 (eBook)
DOI 10.1007/9?8-3 642-31241 -4
Springer lleidelber8 New York Dordrecht London
Libruy of Congrcss Co¡trol Number 2013942485
O Sp.inger Verla8 llerlin Heidelberg 2013
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Cowt illLnÍation: Optical micrcgraph showing cross sectio¡s oi intercellular colonization rice calli and
regeneatcd plantlcts by A. cdulihorl¿ns: CS view of root uninoculated conboli mag¡ilied cross section
view of leaf colonized by A,. cauLit¡oddns in rcgenerated rice planl possible sites of infection and
colonizatio of ce root (fton left to right); sce also Fis. 3.1 in "Endophytic Bacteria Pcrspcctives and
Applications nr Agricultural Crop Production", Senthilkumd M, R. Anandham, M. Madhaiyan, V.
Venkateswaran, Tong Min Sa, in "Bacteria in As.obiolosy: Crop Ecosystems, Dinesh K. M¿]t€shwúi
(Ed.)"
Rackgtoutul: Positi\e ]ñmunofiuorcscence nicrosraph showing re¿ction w,th cells of thc biofertilizer
strai¡ use¡l;n autecologicál biogeography studiest sce also Fig. I0.6 in 'Beneficial Endophytic Rhizobia as
Biofenilizerlnoculets for Rice and the SpatialEcology oflhis Bacteria'Plmi Association", YoussefGaras
Yanni, Frank B. Dazzo, Mohaned f. Zid¿n, in "Bacteria in Agrobioiogy: Crop Ecosystems, Dinesh K.
Maheshwari (Ed.)"
Pr'rirr,l on ¿.id irc"
trt,
r
Sprinser is p¿rt of SprinserScience+Business
Medla (www.sp.inser.com)
Chapter
1,1
The Role of SideroPhores in Plant
Growth-Promoting Bacteria
Ana Fernández Sc¿vino and Raúl O. Pedraza
11.1 Introduction
organisms
I¡on is the fourth most abunda[t element in the earth's crust' and living
is not ¡eadily
recluire iron for growth. Although abundant in the environmeüt' iron
ferric
uriilubl". Und"i u"robic cooditions, f¡ee fer¡ous iron, Fe(II), is oxidized to
soluble
easily
very
not
are
which
polyrners'
iron, Fe([I), forming oxy-hydroxide
(Neilards l9q5).
proteins require
Iron is physiologically indispensable since a great number of
¡eactions
i¡
¡edox
involved
i¡on fo¡ tÉei¡ activities, particutarly the enzymes
the abunfrom
iron
to
scavenge
mechanisms
Organisms have developeá different
them are
of
Examples
envircnment
in
the
sou¡ces
unusable
dá but biologically
ferrous
of
forms
(1) reduction Jf exLiemely insoluble form§ of ferric ion to soluble
ioí thut
(2) use of iron present
b" ur"d
"of erythrocytes
i"oitir,
i¡
hemoglobin by the destruction
"asily,
and hydrolysis of hemogtobin, (3) direct use of the iron stored in
("ápf"*"t tiat sio¡e iron in a form that is soluble' bioavailable' and
degradation of compounds üat bind iror ike transfernontori"), uni (+)
"nzymatic
the
rin (Vasil aod óchsne¡ 1999). But among the variou§ mechanisms employed'
production of iron-binding compounds called siderophores is the best studied'
' The term sidercpho¡e siands fo¡ "i¡on ca¡rie¡s" o¡ "i¡on beare¡s" iÍ Greek' They
high afñnity and
axe water-soluble, Iow-molecular-weight, organic ligarids with
a high-afflnity system for
constitutes
(Kraemer
This
2004).
binding
for
iron
specific
Il1icroolgani§ms This
the uptake of iron from thg extemal medium, pre§ent in maüy
A. Femández Scavino
(8)
2124' Casiua de Correo
Facuitad de Química, Universidad de la República, Gral Flores
1 1 57 Montevideo, Uruguay
e-mail: [email protected]
R.O. Ped¡aza
i^"rfiJJ" ¡'g.*"-1"
y Zootecnia' Univerida¿l Nacional de Tucumán'
Av Kirchner
1900'
4000 Tucumán, Argentina
D.K. Maheshwari ef al.
( eds.\,
Bacteria in ABrobioloÜ: Crop
Productivi¡)'
265
266
A. Femíndez Scavino and R.O. Pedraza
systen has th¡ee componenls: a side¡ophore that acts as a high-afnnity ferric-ionspecil'Lc ligand that is usually released to the extracellulal environment by micrcbes,
a membrane ¡ecepto¡ fo¡ i¡on-bound sideropho¡e (feri-siderophore) complex thal
transpo.ts the chelated iron ac¡oss the microbial membrane, and an enzymatic
system that is p¡esent within the ceLl that can ¡elease fe¡¡ic iofl bound to the
siderophore- The siderophores foÍn soluble complexes with fe¡¡ic ion which, in
natuml environments, is extracted f¡om insoluble iron hydroxides, protetn-boünd
iron f¡om cellular detritus, or from other iron chelates.
This system of high-aff,nity acquisition and rcceptor dependent ransport of
leric ion is associated with growth or ge¡mination factors and with virulence
factors (Crichton and Charloteaux-Waute¡s 1987)- Due to wllich the side¡ophores
production is a common truil of invasive pathogenic microorganisms, synlhetic
analogs of bacteial siderophores attract increasing inte¡est as potential drugs for
the t¡eatment of infections (Bergeron et al. 1999).
Recently, siderophores production proved in different plant growth-prcmoting
bacteria (PGPB) as an inportant attribute in the plant growth and phytosanitary
protection (Compant et al. 2005, Maheshwari 2011). Considering the impotant ¡ole
that siderophores productio, can play in ag¡onomic ecosystems, the i¡on content as
a limiting nutriert fo. living organisms, the bacterial siderophores production
paficularly in PGPB, and thc biotech¡ological applications of
I
1
The Role of Siderophorcs in Plant Growth-Promoling
Bacieria
267
The celLuLar uptake ol iron is rcstlicted to its physiologically most relevant
species, ferrous, i.e., Fe(II), and ferric, i.e., Fe(IID. Fer¡ous form is more soluble
in aqueous solutions at neutral pH and then sufficiently available for Iiving cells iI
remains in the reduciive status. Generally, Fe(II) form can be taken up by ubiquitous divalent metal t¡ansporters, although specif,c fenous uptake systems a¡c
loown in bacteria and yeasts (Miethke and Marahiel 2007).
Though iron is required by a majority of micrco¡ganisms, there are some
exceptions like the lactic acid bacteria, as they do nol contain hcme eniymes and
the iron-containing ribonucleotide reductase (Neilands 1995). On the othe¡ hand,
iron can be toxic fo¡ ce¡1ain orga¡tisms. High intraceilulal concentration of felrous
ion may produce hydroxyl radicals (Crichton and Charloteaux-Wauters 1987). This
problem is alleviated with enzymes such as superoxide dismutase, catalase, and
peroxidase that can degrade reactive oxyge¡ species. Iron toxicity is also alleviated
by the prescnce of antioxidants such as glutathione and endonucleases that repair
damages causcd to DNA during redox stress (Ardrews 1998)- It is also well k¡own
that the iron impofls toxicity towards rice plants in lowiand envilonments. After
inundation, reduction of i¡on oxides and hyd¡oxides resulls ir the accumulation of
large amounis of ferrous ioll thal disrupt or overexpres§ metabolic p¡ocesses that
¡esult in damage of the rice plant (Becker and Asch 2005).
siclerophores in
agriculture are presented in this chapter.
71.2.1 lron BioavailabiW
11.2 lron
as a
Limited Nutrient
Iron is an cssential t¡ace nutrie¡t fo¡ most klown orgauisms. The abundance ofiron
most
environments iron deficiency is not caused by 1ow total iron concent¡ations but
by low iron bioavaiLability (Kraemer 2004). In aerobic environment iron is found as
Fe(III), which is irsoiuble under physiological conditions (Powell et a]. 1980;
Mat¿an\e er al. l98q).
More than 100 enzymes involved in primary and secondary metabolism possess
iron-co¡taining cofactors such as iron-sulfur ciuster or heme groups. The reversible
Fe(II),tre(IID redox pair is best suited to catalyze a broad spectrum of redox
rcactions and to rnediate electron chain transfer (Miethke and Marahiel 2007).
These enzyrnes aod cofacto¡s pa¡ticipate in various processes such as respimtio¡1,
activation of oxygen, degradation of hydrogen peroxide and hydroxyl radicals,
amino acid and pyrimidine biosynthesis, the cit¡ic acid cycle, DNA synthesis,
nitrogen fixation, carbon lixation metabolism, photosynthesis, and oxygen binding
(Aodrews 1998). In addition, several transcriptiooal and posthanscriptioflal
regulatom iDteract with i¡on to sense its inlracellula¡ level or the cuüenl stalus of
oxidative stress in orde¡ to efirciently control the expression of a broad array of
genes i¡volved mainly in iron acquisition or in the rcac¡ive oxygen species protec-
in soils is 1-6 V. by weight, and its solubility is dependert on pH. In
tion tH.ntke 2001).
'fhe iron pools in soils and aquatic eÍIvirooments cofltaiü iron complexes (fenic
complexes with olher ligands different from siderophores), iron-bound enzymcs
from det tus plant and mic¡obialce1ls, iron bound to humic and fulvic sr¡bstances,
and iron-bearing nline¡als. A major iron pool io ter¡estrial and aquatic system§ is
collstituted by iron oxides (Kraemer 2004). Some pathogens can mobilize fe¡¡ic
iron directly l¡om i¡on containing eukaryotic host Proteins, like tra[sferin,
lactoferrin, and ferdtin, or from heme using a heme oxygenase (Winkelmann
2007). The sideropho¡es ploductio¡r is a particularly efficient and specialized
iron-acquisition system that confers competitive advantage to many o¡ganisms in
biotic and abiotic ecosystems. Mosl ofthe informatio¡ in biological ircn acquisition
oI
conditio¡s in reduced
is Iocused on aerobic systems since rcducing conditions lead to a strong increa§e
iron solubility and is unlikely to encounter ilon
liÍiting
systems (Ii¡aemer 2004). The iron availability is limited by the solubility, and the
slow dissolution kinetics of iron-beaing mine¡al phases particularly occurs ill
neutral or aikaline environments. The solubility of iron oxides in aerobic systems
depends on the properties of the solids, ol1 the particle size, aod on the pH, ionic
strength, and concentation
of organic ligands in solutiofl (Kraemer 2004). At
reural pH a¡d oxic conditioüs, Fe(II) quickly oxidizes to Fe(III) (Stumm
and
Morgan 1995). In the absence of a stlong organ:ic ligand, Fe(III) precipitates rapidly
as a hydrous fer¡ic oxide, and citrate is too weak to bind iroo and prevent Fe(III)
precipitation in the culture medium (I(onigsberger et a1. 2000).
l
268
A. Femández Scavino and R.O. Pedraza
1
1
The Role of Siderophores in Plant Growth-P¡omotiDg
Bacteria
269
In the soil environment, at around neutml pH, the free FefIU) concentratiol in
equilibrium with ferric oxide hydrates is around 10-17 M (Budzikiewicz 2O1O). But
living microorganisms require higher conce[trations (10-6 M), a¡d when cells
detect coDcenhatio[s below this threshold, the siderophorcs production begins
(Miethke and Marahiel 2007). Siderophores have a pronounced effect on the
solubility of iron oxides ove¡ a wide range of pH due to the exbaordina.ry
thermody¡amic stability of soluble side¡opho¡e-iron complexes. Very small
concenhations of Iiee siderophores in solution have a latge effect on the saturation
state of iron oxides. This siderophore-ilduced disequilibrium can drive dissolution
mechanism such as proton-p¡omoted or liga¡d-promoted iron oxide dissolution.
The adsorption of siderophores to oxide surfaces also induces a diiect sideropho¡eprcmoted surface-controlled dissolutio¡ rnechanism (Kraemer 2004). I¡ addition,
i¡on can also be mobilized by exudation of non-siderophore ligands that arc
ubiq¡ritoüs in soil. Organic acids such as lactate, succinate, fuma¡ate, malate,
acetate, and ami[o acids exuded by roots of iron-stressed plants can also contibute
to the Fe([D solubilization and influence mic¡obial iron acquisition (Fan et al.
Most fungi produce a variety of different types of siderophores, aod individual
organism may p¡oduce a set of siderophores covering a wide range of physicochemical properties. This diversity allows fungi to overcoúe the adverse local
conditions of ircn solubility and the outcompetitio[ by motile bacteria that can
migrate towards increasing nutrient concentations (Winkelmann 2007). More than
100 structurally different fungal siderophores are known, though all of them have a
peptidic ring in common. One of the four major classes, the ferrichromes,
comprises diverse structurcs that arc recognized by their resista[ce to degradation
in the environment, particularly whe¡ they are complexed with iron (Wi¡kelmann
2007). Virtually all aerobic bacteria and fungi produce siderophores (Neilands and
Leong 1986). Though, this popeÍy is a clear advantage for microorganisms
inhabiting aerobic envi¡onme¡ts. Most of the facultative bacteria isolated of íce
paddy soils rcported as siderophore producers (Loaces et al. 2011). It rcmains to be
elucidated if these bacteria a¡e effectively producing siderophorcs in such anoxic
soils wherc ion piobably is present as Fe(II).
There are microorganisms which are unable to produce sideropiores. Saccharo-
1997).
myces cerevis¡ae lacks the ability to synthesize siderophores, although it can utilize
siderophorcs produced by other species via rcductive and nonreductive i¡on assimilation (Eisse¡dle et al. 2003). In addition, Pandey et al. (1994) studied 23 strains of
lactic acid bacteria for their ability to produce siderophores. The growth of seve¡al
strains tested was uflaffected by an ircn deficie¡rcy, and no dtect effect due to iron
chelation by a synthetic iron chelator was observed. Hence, the autho$ confirmed
that these strains of lactic acid bacteria do not rcqu(e iron.
11.2.2
Siderophores from Dilferent Organisms
Various pla¡ts belon gto family Poaceae (graminaceous grasses): funBi and sevsral
bacterial genera are known to sequester üon using siderophores (Neilands 1957;
'laka9i 1976: Wid<elmann 1992).
A specialized mecha¡ism for iron uptake is obseúed it Paaceae plants
which, via roots, rclease iron-chelating nonproteinogenic amino acids called
phytosiderophores. According to Rómheld and Marschner (1986), there are two
strategies for the acquisition of iron by plants under iron deficiency. St¡ategy I (in
rtrost lotr-Poaceae species) is cha¡acterized by an inducible plasma membraner
bound reductase aod an enhancement of H+ release. St¡ategy II (in grasses) is
characterized by an enhanced release of phytosiderophores and by a highly specifrc
üptake system for Fe(Itr) phytosidercphores. This st¡ategy seems to have seveml
ecological advantages over stategy I such as solubilization of spa¡ingly soluble
inorganic Fe(IID compounds in the rhizosphere and less inhibition by high
pH. Thus, mugineic acid is produced by barley, distichonic acid by barley, avenic
acid A by oats, deoxymugineic acid by wheat, hydroxymugineic acid by rye, and
nicotinamide by tobacco. Sorne plant like barley is able to take up ferriphytosiderophores 100-1,000 times faster than other ferri-chelators (Castignetti a¡d
Smaüelli 1986). It has been observed that the lower affinities of phytosiderophores
by i¡on, comparcd to microbial siderophores, are partly compensated by high
exudation rates by Poaceae plant roots resulting in local ligand concentrations in
the millimola¡ range in the rhizosphere, whereas the bacterial hydroxamate
siderophorc concentration is fou¡ orders lower (Rómheld 1991).
11.2.3 Siderophores in Soil
In most enviro¡mental systems, siderophorcs mainly exist in complexed foIm
(Kraemer 2004). Their concentmtions in soil depend on the soil hodzons, but the
rhizospherc shows highel concent¡atio¡s than bulk soil (Bossier et al. 1988). Powell
et al. (1980) have estimated hyd¡oxamate siderophore concenhations in soil
solütions between
l0-7 and 10-8 M.
Rómheld (1991) has estimared thar
phytosiderophore co¡centations can ¡each local conceritrations of up to 10-3 M
since plarts are able to exude phytosiderophore at high rates into the rhizospherc.
The concent¡ation of microbial sideropho¡es depends orl the envi¡onmental
conditions. Ferrioxamine B-type siderophores, produced by most actinomycetes
§eilafids and Leong 1986), were the most abundant siderophore prcducer in a
tiller-amerded soil system, whereas the ferrichrome type produced in smalle¡
quantities by several fungi (Crowley et al. 1987). On the othei hand, Holmstróm
et a1. (2004) identif,ed the main sideropho¡es in coniferous forest soils intensively
colonized by ectomycor¡hizal hyphae as fer¡ichrome ard ferricrocin, with the
fomer detected in nanomola¡ concenkations in humic layers ovgrlying granitic
rock and soils (Holmstróm et al- 2004). Ferric¡ocin is a widespread siderophore
in fo¡est soils that seems to be resistant to the p¡oteases exc¡eted by plants and
!i
I
Z'tO
A. Femández Scavino and R.O. Pedraza
Gram-positive bacteria (Winkelmann 2007). It is now coosidercd that organic nonside¡ophore ligands, as seve¡ai amino acids and organic acids like citrate, can be
exudated by plants aod influence the iron availability. These ligands are ubiquitous
in soil
and might have a syne¡gistic or inhibitory effect o¡l the siderophores
dissolution rates (Kraemer 2004).
Fu¡thermorc, Kraemer (2004) proposed that the compressive understanding of
the role of sideraphores in increasing iron oxide solubility and p¡omoting dissolu
tion in soils requires the consideratiofl of the rates of va¡ious
processes that
occurred simullaneously. Thus, the siderophore exudation rates, the uptake, and
the degradation ¡ates, as well as the loss oI siderophores by adsorption on other
mineral sufaces, the partitioning of iron into humic substances, and the complexa-
tion of me{ai other than iron (which stability may be signiflcaüt, specially for
AI(I[) or.for Ca(II) that is often present in mr-rch higher
concentrations), shorrld be conside¡ed. In addition, iron oxides in natu¡al terrest¡ial
envi¡onmeflts are often coated with humic and fulvic acids, exo-polysaccharidos, or
biogenic low-molecular-weight organic acids, and the inhibitory, competitive, or
synergistic effects of such substances on sidercphore-controiled iron acquisition
need to be investigated.
simiiar ions as
1l
The Role of Sideroplrores in Plant Crowlh-Promoting
Bacte¡ia
2'11
sirlerophores. The peptide chain canying the ligand siles usually contains cycLic
st¡uctures at the extuemes that prevent their degradation by proteolytic enzymes.
The peptidic
siderophores
are produced by
fluorescent Pseudomonas
(pyoverdines), as weli as by species of the Senera Azotobacter, Mycobacterium,
Rhodococcus, a¡dby many enterobacteria and by most of fungi. This also includes
lipopeptide sideropho¡es produced
Nocardia,
a;rd Mycobactet
ium.\he
by
species
of the genera Butkholderia,
siderophores based on di- and tri-aminoalkane
skeletons are produied by few rhizobía, Patacoccus, Burkholderia'
Agrobacteríum, and. several Actinomycele§- Siderophores based on citric acid are
produced by bacteria from the genen Bacíllus, Acinetobacfer, Arthrobacter,
Ochobactrurn, Rhízobium, Synechococcus, Vibr¡o, Ralstonía, Staphylococcus,
ancl Marinobacter (Budzikiewicz 2010). Thus, the §tability of Fe(III) siderophore
complexes vades i¡I a range about 30 o¡de¡s of magíitude depending on the
siderophore structure and on the liSand type. Also, the pH of the environment
strongly influences the chelation efñciency (Miethke and Ma¡ahiel2007). Although
Gram-negative a¡d Gram-positive bacteria have differcnce§ in their cell stucture,
they share some genes in common for both specific sideropho¡es transpoft and ironbinding proteins (Clarke et al. 2000).
Many bacteria produce mo¡e than one type of sideropho¡e or have more than onc
iron uptake system to take up multiple siderophores (Neilands 1981). Recently,
11.3 MicrobialSiderophores
Microbial siderophores show g¡eat variability
may be due to genetic lactor or biochemical
in thei¡ chemical structu¡es. This
othe¡ compounds able lo bind i¡on wlth comparable afflnity to the known bacterial
siderophores have been ¡eported. The degradation Product of an acylhomoserire
lactone (signal molecuie in the Quorum Sensing §ystem) producedby Pseudomonas
aeruginosa possibly is an uDrecognized mechani§m for ilon solubjl'ization
(Kaufmann et aI.2005). Recently detail description on types and chemisty of
siderophores rs reviewed by Desai and A¡chana (2011).
11.3.1 Chemical Struct res
1i
Siderophores a¡e ton-chelating seconda¡y metabolites with masses below 2,000 Da
I
i
i
I
I
i
11.3.2 Biochetnical and Genetic Detetminants Involved
in Bacterial Siderophores Production
(Budzikiewicz 2010). Almost 500 side¡ophores with known stucturc have been
reported (Boukhalfa and C¡umbliss 2002), and several hundred active on-chelator
compounds have been cha¡acte¡ized and purifred (Hider and Kong 2010). Most, but
not all, of siderophoies are hexadentate ligands forming 1:1 coñplexes with Fe(III)
(Kraen-rer 2004), and thet capability to form stable complexes with Fe(II) is ¡ather
low (Miet[ke and Marahiel 2007).
The major Fe(IID ligand types are catecholates, hydroxamates, and alphahydroxycarboxylates and often are combined in the same molecuie of siderophore
(Budzikiewicz 20i0). Carboxylate siderophores a¡e produced by microorganisms
that live in acidic environments, e.g., fungi, but these could nof compete with
stronger siderophores such as catechoiates at physiological pH (Dertz and
Raymond 2003), since catecholates have higher affinity for Fe(II!. These ligands
a¡e supported in different chemical structurcs such as peptides, di- and tri.
aminoalkanes, and siderophores based on cit¡ic acid along with miscellafleoüs
Siderophores production as a response to iron limit¿ition i§ widgspread among
aerobic microorganisms (Neilards et al. 1987). It ha§ been repo ed that among
302 diffe¡ent fluorescent Pseudomonas stains isolated from soils, 297 produced
detectable sideropho¡es unde¡ iron deficiency (Cocozza and E¡colani 1997).
Although this iron-acquisition system is induced unde¡ i¡on-limiting conditions,
other environmental factors such as pH, the prcsence of other tmce elements, and
the availability of carbon, nitrogen, and phosphorous sou¡ce§ also influence the
siderophores production (Duffy and Defago i999). This system involves several
steps: int¡acellula¡ biosynthesis of siderophorc§, exudation of siderophores in the
ext¡aceilular space, iron mobilization by competitive complexation o¡ dissolution
of
iron-bearing mine¡als, and recognition
a¡d uptake of ferric
siderophore
1rP"
2'/2
A. Femández Scavino and R.O. Pedraza
complexes by highly efficie[t t¡ansport systems o¡ liberation of ircn frcm the
siderophorc complex and uptake of iron (Boukhalfa and Crumbliss 2002).
The system requires tightiy rcgulated enzymes and transport systems that allow
concerted siderophore biosyDthesis, sec¡etion, siderophorc-delivered iron uptake,
and ircn release. In bacteria, gene regulaüori of side¡ophorc uülization and ilon
homeostasis is mediated mai¡ly at the transcriptional level by the feIric upt¿-ke
rcprcssor Fur (in Gram-negative and low mol 7¿ GC G¡am-positive bacte¡ia) or by
the diphüeria toxi¡ regulator DtxR (in G¡am-positive high GC contents
as
streptomycetes arld corynebactsria) (Hantke 2001). The synthesis of catecholates
mostly depends o¡ the no¡fibosomal peptide synthetases, whercas hydroxamate
and carboxylate sideropho¡es a¡e assembled by dive$e enzymes such
as
monooxygenases, decarboxylases, and aninot¡ansferases (Miethke and Ma¡ahiel
2OO7).
In bacteria, the main rcute for the uptake ofFe complexed in sidercphorcs is the
import of the complex into the cytosol through specif,c tansporte¡s. Morcover, the
organisms that can use exogenous siderophorcs (synthesized by other organisms)
showed ftequently a geater battery of Fe-siderophore importers than siderophore
exporters (Miethke and Marahiel 2007). 'fhe i¡on release from the Fe(III)
siderophore complex into the cytosol comprises either the reduction to Fe(II) by
relatively unspecinc ferric siderophore reductases o¡ the hydrolysis of the complex
by specif,ó enzymes that liberate Fe(III) which is further rcduced or complexed by
other cellular ircn components (Miethke and Marahiel 2007).
Morcover, the role of side¡ophores might not be limited to the iron chelation.
The nitrogen-f,xing bacteril]J]r, Azotobacter vinelandíí produces at least flve different siderophores, where concentmtion increases sha¡ply at low iron concenhation in
diazokophic cultures allhough their production is not suppressed at high iron
concentration (Bellenger et al. 2008). Kraepiel et al. (2009) suggested that
A. t inelandii may produce siderophorcs to acquire molybdenum (Mo) and vanadium
(V), two important metals requi¡ed for nitrogen fixation, when these metals arc
limiting in diazotrophic cultures.
11.3.3 Siilerophores Influence the Interaction Among
Organisms
Srderophores production can modiFy lhe i¡leraction among organisms in the environme¡t leading to mechanisms of cooperation o¡ competence,
The capability of sensing iron in the environment is an advantage by the
siderophore-producing organism and may help other microorganisms that do rlot
have this capability or that are not so competitive. Many microo¡ganisms arc able to
utilize the Fe(m) complexes of siderophores which they have not synthesized. The
persistence in soils of ferrichromes, the most common fungal siderophorcs, be¡elits
other microorgatrisms that have the rccepto6 for the uptake of these siderophores as
1I
The Role ofsiderophores in Plant Growth-Promoting Bacte
a
213
in case of seve¡al enterobacteria like Pdñ toea, Enterobacler, Er,uinia, andYersinia
(Wi¡kelman¡ 2007). Aiso, the uptake of bacte.ial siderophorcs by fungi, like
Saccharomyces and Aspergillus, has been obseryed (I{aas 2003, Heyma¡¡ et al.
2000; Lesr¡isse et al. 1998), and the e¡terobactin, the predominant siderophore
produced by enterobacteria, can also be utilized by Saccharomlces, a nonsiderophore-producing microorganism (Winkelma¡¡ 2007).
In addition, it has been p¡oposed that partial degradation offungi siderophores o¡
i¡on exchange between bácterial siderophores and phytosiderophores is involved in
the üon rutrition of Poaceae plants (Yehuda et al. 1996; Winkelmann 2007). An
indirect effect of cooperation has been postulated by Knepiel et al. (2009) between
non-nodulating plants and free-living diazotuophs inhabiting their rhizosphere.
Besides i¡on, several metals are complexed and accumulated in plant leaves that
when decomposed i¡ topsoil constitute a source of esse¡tial minerals for the
nihogen flxation, from which the piants beneflt. The diazotrophic bacteria extract
these essential minerals tbrough the excreted siderophores.
Competence among microorganisms is wetl itlu§frated by several examples and
can beneñt or be negatiye fo¡ the siderophorc-producing microorganism. In general
bacterial sidercphores, though differi¡g in their abilities to sequester iron, deprive
pathogedc fungi of this esseDtial element since the fu[gal §ideropholes have lower
affinity for Fe([I). This cqnstitutes one of the main mechani§ms of biocontrol of
plant pathogenic ftrngi (Loper and He¡kels 1999). Thei ability to use a large
numbe¡ of heterologous siderophores has been confirmed by the presence of
many homologues of iron-siderophore receptor genes iri their gelomes (Comelis
and Matthijs 2002; Kaufmann et al.2005). Conversely, siderophore producers can
be invaded by nonproducing cheats from the same o¡ different §pecies that have the
siderophore receptol§. Siderophores production is metabolically expensive to individual producers but benefits all cells in the vicinity able to caplu¡e ironside¡ophorc complexes produced by other cells of the same species (Harri§on
et al. 2008). On the other hand, certain microorganisms synthesize structurally
distinct siderophores apparently a§ a strategy to ove¡come the competition of
c!\eatefs. Streptomlces species produce two dilfe¡ent sidercphores with two independent uptake systems; whereas ferdoxamines ca.n be taken by several olganisms,
the ferric coelichelin complex can be selectively abso¡bed into Streptomyces
coelicolor cells through an independent uPtake system (ChalLis and Hopwood
2003). Additionally, the capability of micrcorganisms to degrade siderophores in
soil can modify the interactio¡ established through siderophores production. It has
been reported that bacteria of the genus AzosplrilLum in p:u¡e culture§ are ahle to
degrade ferrioxamines whe[ present as i¡on-free compounds (Winkelmann 9t ai.
1999).
A singular case may be the endophytic bacte a that colonize intemal tissues of
the plants and their ¡elationship with the siderophores production. In Uruguay it has
been shown that at the end of the cropping cycle, the leaves of three diffe¡ent ¡ice
by high amounts of siderophore-producing bacteria
(Fig. 11.1), '¡/ilh Pantoed arr<l Pse domonas a§ the predomina¡t genem. Furthermorc, the proportion of siderophore-producing bacteria to heterotrophic hacteria
varieties we¡e colonized
i
274
A. Fcr¡ández Scavino ¿nd R O. Pedr¿ra
Fig. 11,1 Enumcration
e¡dophyric hcrerotruphrc
bacreria
IHB)il¡d endoph) rrc
E 4
; ..
B Jr
leaves ol three ri.. v.,. er,e(
crltrvatcd rn Urxtsuq ar d)c
B J
cnd ol th€ crop sei\on. [P. El ü
26
Prso 144;1'f. INIA Tacuari: L
2
IO,INIA Olimar. The values rePre\cnr thc mern ol
o 15
rriplicatc plors rn a ñeld
B
helcroüoohic siJcroDhorepro,lucins bacleria (HSPB) in
expenment
05
l
':
.
1
!
i
IT
IO
EP
augr¡e¡ted in leavcs wher the plant grew, and they increased in ¡oors compared to
rhizospheric soil alter the flooding, when the environment becomes anoxic (Loaces
et al. 2011). They remained strongly associated to the plant tissues although in vitro
iniibition towa s pathogenic fungi or PCPB was not observed. Apparently,
siderophore-producing bacteria we¡e selected into the plant tissues, though the
beneflt for the pla¡t results is still [nclear. Their role captu.ing Fe(III) generated
by lhe oxidation of Fe(lI) in oxic micro,nichcs illto the plant or in the rhizosphere,
increasing the iron availability locally, or reducing the Fe(II) toxicity towards the
pla¡t by accumulationof the sequestered metal into the bacte¡ial cells shouid not be
dismissed (Loaces et al. 2011).
Finally, the ¡ole of siderophore producing bacte¡ia as bacte¡ial growth promoters
should be also cr¡nside¡ed. 'fhe (until now) uncultu¡ed bacteda may be stimulated
and become cuitu¡able in the presence of sidercphore-producing bacteria. Recentiy
D'Onofrio et al- (2010) have showD that previously r¡rcultu¡ed isolates from marine
sediment biofilrn, g¡ow on a Petri dish in the presence of cultu¡ed o¡ganisms f¡om
the same environmeflt. 'Ihis he]per strain p¡oduces a grcw facto¡ identiñed as new
acyl-rlesferrioxamine siderophor.e.
¡
t.
Ii
ti.
ti
i
I
11.4
i
I
¡
li
I
l
I
ll
I
f
I
lr
The Role of Siderophores in I,lan! Growth-Promoling Bacteria
1.1.4.1 Plant Growth-Promoting Bacturta: Mechanisms
oÍ Action
5
¿q
0
1i
Siderophores Production in Plant Growth,Promoting
Bacteria
Siderophores have been implicated for both direct and indtect enhancement of
plant growth by rhizospheric microorganisms. The ecological signif,cance
of mic¡obial siderophores in soil and plant surfaces has att¡acted the attention of
PGPB are a heterogeneous group of bacteria, such as thc geñera. Azotobdcter,
Azospírillum, Azoarcus, HerbaspiriLlum, Pseudomonas, arrcl Rhiu.úium, amorLg
othe¡s, that can be found in the rhizosphere at root surfaces and in association
witlr inne¡ root tissues and other h¿rbitats (Ahmad et al. 2008). The enhancement of
platrt growth using PGPB is well documented (Reed and Glick 2004; Bashan and de
Bashan 2010), and these organisms have also been used to rcduce plant stress
associated with phytoremediation strategies for metal-contaminated soils (Reed and
Glick 2005).
PGPB enhance plant growth through different mechanisms, such as (1) enhaocing asymbiotic nitrogen nxation (Khan 2005) or indirectly affecti¡g symbiotic Nz
fixation, nodulation, or nodule occupancy (Fuhfna¡n and Wollum 1989);
(2) reducing ethylene production, allowing piants to develop longer roots, and
bette¡ establishment du¡ing ea¡ly s¡ages of growth, due to the synthesis of 1aminocyclop¡opane 1-carboxylatc (ACC) deaminase whjch moduiates the level
of ethylene by hydrolyzing ACC, a prccursor of ethylene, in ammonia and
o-ketobutyrate (Glick et ai. 1998); (3) p¡oduction of hormones such as auxins,
cytokinins, ancl gibberellins (Glick 1995; Ahmad et al. 2008); (4) r'aising tire
solubihzation of nutrierts with resulting inc¡ease in the supply of bioavailable
pltosphoious aod olher kace elements for plant nut¡itior (Glick 1995); and
(5) synthesis of antibiotic and othe¡ pathogen-depressing substances such as
siderophores, volatiles, and chelating agents that protcct plants f¡om that afltago,
nize phytopatogens. (Kamncv and Lelie 2000; Toflora et aI.2011,2012). These
mic¡oorganisms can also increase plant tolerance to environmental st¡esses such as
flooding (Grichko and Glick 2001), salt stress (Mayak et aI.2004a), aod water
deflciency (Mayak et al. 2004b). PGPB are not only signincant from an agricultural
point of view, as they ca¡r also play an imporlant role in sojl remediation strategies,
¡ot only by
cnhancing g¡owth and successful establishment
of
plants in
contaminated soils but also by increasing the availability of contaminants, as
repofed for heavy metals, namely, Zn and Ni, in Thlaspi caerttlescens (Whiting
et al. 2001) a,¡d )n Alyssum murale andThlaspí goesingense (Abou-Shanab et al.
2003; Id¡is et al. 2004). Recently I(urrrar et a1. (2010) obscrved reductior of
chemical fe¡tilize¡ by using combination of root-nodulating Sinorhizobium f'edii
KCC5 and rhizospherc Pseudomonas fiuorescens L?K2.
11.4.2 Siderophores as a Competitive Advantage for Plant
Growth
wo¡kers.
GiveD that i¡on is an essential nutrient, plants have evolved strategies for its
acquisition, which, in dicotylcdonous plants such as cowpea (Vigna ungtLiculata),
276
11
A. Femández Scavino and R'O- Pedraza
I
l
I
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il
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i
t,
I!
I
f
I
I
l
il
I
I,
¡i
I
n
I
I
tl
!
ü
ti
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[]
t¡
Nowadays, contlol of plant diseases is performed by the intensive use of chemical
products that may cause enviroDme[tal pollution, pathogen resistance, increase in
production costs, and serious risks to the environment and huma¡ health Ao
altemative of c¡op protection against pathogens is the biological conkol exerted
by some PGPB. Several factorc can affacr the eff,cacy of siderophores as control
agents against plant pathogen§, the most important among them being type of
microorganism, target phytopathogen, and medium composition (Glick and Bashan
1997). Because of their catabolic versatility, theü excellent rcot-colonizing
abiliües, and thei¡ capacity to produce a wide range of antifungal metabolites, the
soil-bome fluo¡escent pseudomonads have ¡eceived particular attention as efficient
biological control agents (Nautiyal et al. 2003). They produce several siderophores
such as pyoverdine, pyochelin, azotobactin, salicylic acid, and pseudomonine
(Dave ard Dube 2000; Me¡cado-Blanco et al. 2001; Labuschagne et aI 2010)'
A-ll these side¡ophores conbibute to disease suppression through the competition
for ironHowever, siderophorcs production in the genus Azospirillum' an important
Sharrna and Johri (2003) repo¡ted about malze seeds i¡oculated with
siderophore-producing pseudomonads with the aim to develop a system suitable
for bette¡ iron uptake under ton-stessed conditions. They found that inoculation of
maize seeds with fluorescent Pseudomonas spp. stains GRP3A and PRS showed
significant i¡crease in germination percentage and plant growth. Maximum §hoot
and root length and dry weight were obseNed with 10 pM Fe(tr) along with
bacterial inoculants, suggesting that application of siderophore-producing plant
growth-prcmoting bacterial strains positively influences the crop productivity in
calcarcous soil system. Pandey et al. (2005) fotr,d Pseudomonas aeruginosaGRC|
having proliñc production ability of hydroxamate siderophore in iron-deficient
conditio¡s. The siderophore of GRC1 was purifled and characterized. The pudñed
siderophore appeared to be of pyoverdine type with tyPical amino acid composition. In field t/raLs, P. aeruginosa GRC1 enha¡ced the grcwth of Brassica
campestris var P:usa Gold (Indian mustad).
Allhough extensive ¡esearch has been di¡ected to colTect chlorosis (iron
deflciency) by the application of available iron compounds to the §oil and by
selective plart breedi¡g to prcduce Fe-chlo¡osis-resistant cultivar§, during the last
years, the possible implication of §iderophores Production by PGPB has been
considered as a potential way to improve plant growth, rodulation, and N2 fixation
in i¡on-deflcient conditions. The beneficial effect of usi[g siderophore-producing
s]c¡ains of Bradyrh¡zobium sp. ar,d Rhízobíum melílotí was reported by O'Hara et al.
(1988) a¡d Gill et al. (1991), respectively. In addition, siderophore-producing
ability might favor the persistence of rhizobia in iron-deficient §oils (J-esueur
membe¡ of PGPB, is a biocontrol mechanism that has been scarcely studied Saxena
et al. (1986) a¡d Shah et at. (1992) reported the production of salicylic acid (SA)
among siderophores ptoduced by Azospíríllum lipoferum lndet iron-starved
conditions. Salicylic acid (SA) besides being a compound with sideroPho¡e activity
(Visca et al. 1993) is a precursor in the biosynthesis of mic¡obial catechol-type
siderophores, such as ye$i¡.iabactin, pyoverdine, and pyochelin (Cox et al 1981;
Jones et al. 2007; Serino et al. 1995). Moreover, it v,'as demonstrated to play a
crucial ¡ole as an endogenous regulator of localized and systemic acquired resis
tance (SAR) against pathogen infection in many plants (Delarey et al. 1994)'
The¡efore, SA-producing strains may increase defen§e mechani§ms in plants'
However, bacterial SA participation on plant-induced systemic rcsistance (ISR) is
stiil cont¡ovemial (Siddiqui and Shaukat 2005; Cornelis and Matthi§j 2007). It was
hypothesized that bacterial SA excreted to the medium was recognized by plarit
roots inducing signals fo¡ systemic resistance (Maurhofer et aI 1998), although in
some interactions, it has been proposed that SA may not be the pdmary signal for
ISR induction (Prcss et al. 199?), but other siderophores could be imPlicated
(Siddiqui and Shaukat 2004).
Recently, it wa§ rcPofed thaf A. brasilense siderophorc§ coDtain a¡tifungal
activity against Colletotrichum acutatum, tlte causal agent of anthracnose disease
in stawberry crop (Tortora et al. 2011). They demonstrated that under ironJimiting
conditio¡s, different stains of A. brasilense produce siderophores, exhibiting
different yields and rates of production according to their origin. The bacteria
shains have also been isolated from rhizosphele or iriner tissues of strawberry
roots and stolons (Fig. 11.2).
et al. 1995).
il
ü
I
2'7'7
Díseases
1980).
I
Bacteria
77.4.3 Importance of siderophores in Plant Protection Against
is based ori strategy I. Unlike strategy II fou[d in grass monocotyledo[ous plant§,
I does not involve the release of phyto§ide¡opho¡e§. Rather, it is
characterized by ao enha¡ced Fe(m) reductase activity, release of rcductarits such
as phenolics, and acidiñcation of fhe rhizosphere (Rómheld and Marschner 1986).
Furthermo¡e, in stategy I plants, microbial §iderophore§ have been reported to
promote plant growth under Fe deficiency (Crowley et a1. 1991).
In a work about enhanced plant growth by sidercpho¡es produced by PGPB,
specific st¡ains of the Pseudomonas fruorescens-putída group have been used as
seed inoculants on crop plants to p¡omote growth and increase yields (Kloepper
et al. 1980). Seve¡al wo¡kers observed that the§e bacteia rapidly coionized
plant roots of potato, sugar beet, Édish, and other crop plants, which caused
statistically signiflcant yield incrcases in f,eld tests (Maheshwari 2011). These
results prompted them to investigate üe mechanism by which plant growth was
enhanced. Most of these workers have concluded that these bacteria exe ed their
plant growth-promoting activity by depdving native microflora of i¡on as they werc
able to prcduce extracellular siderophores which eff,ciefltly complexed environmental iron, making it less available to certain native microflora (Kloepper et a.1.
strategy
I
The Role of Siderophores in Plant Growth Promoting
l
l'l
A. Femández S!.rvino 3nd R.O. Pedr¿zr
218
50
^40
a
I
1
The RoLe of Siderophores in Ptant Crowih Pronroting Dact€
a
279
total soluble phenolic compouncls and callose depositions and the trlnsient accu_
mulation of SA- The latter brings about the upregulation of defen§e-related genes,
such as those encoding pathogenesis related proteins like PR1, chiti¡ases, and
glucanasc. The¡efore, the activation of a systemic defcnse rcsponse, together with
the plant g¡owth-promoting effect exefted by A. bra.silense REC3 (Pedrazá ei al'
2010), could, in part, expiain the iflcrease of strawbery plants' tolerance to
aDthracnose disease caused by C. acutatum Mll.
1
1.4.4
Biote chnologic al Applicd tio n iru
Agriculture
In agriculture, the increasing int¡oduction of new biotcchnological product§
30
20
10
has
ailowed the achievement of higher yields i¡ almost every present-day commercial
crop, leading at the same time to a higher quality and minimizing ecological
damage. In this conlext, agro biotechnology may be used to develop environmentally safe and economically sound alternative§ to chemical fe ilizels and pesticides'
New products aIe currcntly being dcveloped th¡ough úe stimulation of plant selfdefense by tlle application of PGPB for biological co[trol diseasc and as plant
growth promoters (bioferlilizers), applied as inoculanis. In Table 11.1 are shown
several examples of PGPB siderophore producers, some of them already used as
inoculants.
0
tr'ig. 11.2 Percent of siderophores yield production (SY 7o) of differcnt A. Drar¡l¿nr¿ st¡ains
isolated from strawbenl planls, using CAS agar plates assay. Type srain A- á/arll¿l1.'e Sp7 was
used as the controL for comparison of A. á¡drile¿re isolates tesled. Thc coni¡ol and rhizospherc
(RLC), root endophytic (REC), and first stolon endophytic (PEC) slrains werc cvaluated after
7 days of inculration ai 30 "C
Clremical assays revealed that A. basílense REC2 and REC3 secrete catechol-
type siderophores, including SA, detected by TLC couPled with fluorescence
§pectroscopy and gas chromatography mass spectomctry analysis. Siderophores
protluccd by these strains showed in vifro antifungal activity agzrinst C. acutatum
M11. Additionally, this later coincided with ¡esults ol¡tained from phytopathological tests pe ormed iñ plants, where rcduction of anth¡acnose syrnptoms on straw
berry plants previously ifloculated w\th A. brasilense was observed. These
outcomes suggested that some strains of A. brasilense could act as biocontrol
agent preventing antfuacnose disease in st¡awberry and involved siderophore. In
recent work, the same authors provided evidence that endophytic rcot colonizatio¡]
of strawbeüy plants with A. brasílense strain REC3 confers §y§temic protection
against C. acutdtum M 1 1 by the direct activation of some plant defen§e reactions
and also pdmes the plant for a stronger defense ¡eaction \{hen exposed to further
infection (Torto¡a et al.2012). Defense mecha¡isms induced by A- brasílense
REC3 included the reinforcemenf of plant ce1l wall by inc¡easing the content of
Much rescarch has been dedicated 10 the development of
Pseudamonds
inoculants and olher biological products cotlstituted by active metabolites §uch as
antibiotics and siderophorcs as biocontloL agents (Mark et al.20O6)' Pseudomonas
spp. have been el'ficiently used lor bioco¡trol in the past decade, and at prc§ent time,
there are seve¡al commercial products aheady in the market. For example, there is a
biological product constituted by antimicrobial metabolite§ such as side¡opho¡e
pyoverdine and SA produced by P. aeruginosa PSS, very effective against
Peronospora tabacifia in tobacco culture, Alternaría solani in tomato, and
P seudoperonospora c¿be¿sls itl cucumber (Diaz de Villegas 2007).
Microbe-assisted phytoremediation provide§ plants with natural metai
solubilizing cholalors which do not ¡epre§ent a potential source of envi¡o¡rmental
pollution, At the same time a§ with microbial chelator§, plant growth promotion can
be enhanced through bacterially produced phytohon¡ones (e.9., auxins). Recently,
Dimkpa et al. (2008) studicd the simultaneous produclion of sideropholes and
auxins by Streplomyces aiming for luture application in plant growth and
phytoremediation in a metal-contanrinaterl soil. Standard auxin and siderophore
detection assays ¡ldicated that dilÍerc11t Streptomrc¿§ slrains -can prodllce thesc
metabolites sinultaneousiy. Howeve¡, Al3*, Cd2*, Cu2*' Fe3*, and Ni2* o¡ a
combination of Fe3' and Cd2* and Fe3" and Niz+ affected auxin production negativeiy, as revealed by §pectrophotometry and gas chromatography mass sPectrometry. This effect was more dramatic in a siderophore-deficient mutaot. In contrast,
except for Fe, all lhe metals stimulated siderophores production. Mass sPectromehy
showed that side¡ophore and auxin containing supea¡latants irom a rcprescniative
lr
A. Femández Scavino a¡d R-O. Pedraza
Table 11.1 Exañples oIsome siderophore producers within the plant growth-promoting bacteria
(PGPB) and their main features
PGPB
Main fealürcs
Produces at least frve different siderophores types
May produce siderophores to acquire Mo and V for
nirrogen ñxation when ¡hese merals ¡re limiring
in diazoÍophic culrures
Pseudomona:
fúotescens
Used as seed inoculants on crop planls to p.omote
growth and increase yields
Bradtrhizobium sp. Improve nodulatión and N2 flxation in i¡on,deficient
Rhízobium
conditions
Bellenger et al.
(2008)
Kraepiel et al. (2009)
Kloeppe¡ et at.
(1980)
O'Ha¡a et al. (1988),
CiIl et al. (1991)
meliloti
Azospirillum
lipoferun
AzospiríU m
brusilense
Produces salicylic ácid among other siderophores
ünderiron-starvedconditions
Produces siderophores with antifungal activity
Saxena er al. (1986),
Shah et al. (1992)
Tortora et
a1.
(201I)
againsf Colle¡otrichum acutatum, the ca]usal
agent of anthracnose disease in strawbenl, crop
domonas
aerug¡nosa
Pse
Produces siderophore pyoverdine and salicylic acid; Diaz de Villegas
very effective against Peronospara tabacina in
(200'7)
tobacco culture, A/¡¿¡¡aria rold,ri in tomato, and
Pseudoperonospara cub¿rs$ in cucumber
GL canacetobacter Nitrogen-flxing acetic acid bacrerium prodücing Logeshwara¡ et al.
Slreptomyces species contairi three different hydroxamate siderophores, revealing
the individual binding responses of these siderophores to Cd2+ and Ni2+ and, thus,
showing their auxin-stimulating effects. They concluded that sideropho¡es promote
auxin synthesis in the presence of At3*, Cd2", Cu2*, and Ni2* by chelaring these
metals. Chelation makes the metals less able to inhibit the synthesis of auxins and
potentially incrcases the plant growth-promoting effects of auxins, which irl tum
enhances the phytoremediation potential of plants.
11.5 ConcludingRemarks
Agrochemicals, including fefilizers and pesticides, are extensively used in agricul,
tural production ro control pests, diseases, and weeds, minimizing the yield losses
and maintaining high Foduct quality. The i¡creasing cost and the negative impact
of agrochemicals á¡d thei¡ de$adation products in the environmental are mrjor
ecological and health problems. Therefore, the use of PGPB as biofe¡tilizers or
biocontol agents, most of which a¡e siderophores producers, is quite promising to
support an eco friendly a¡d sustainable agricultu¡e.
11
The Role of Siderophores in Plant Growth Promoting Bacteria
28t
Literature available revealed that sidercphores production is not directly li¡ked
to the plant growth promotion neither to plant Plotection; side¡oPhores are involved
on iron availability in soii afld in fhe inte¡action between plant and microorganisms
in tlis habitat. The importa¡ce of sideropholes is known since more than 30 years'
and many siderophorc-producing bacteria that benefit the c¡ops, promote their
g¡owth, or protect them against pathogens have been reported. Howeve¡, it is still
not enti¡ely known if this mechanism effectively operates in the interaction and
whether it is the only one. Assuming that siderophore-producing microorgalisms
can obtain certain competitive advantages in the soi1, where Fe(II! is not easily
available, they are not the only attribute obtaining that benef,t as siderophore iron
complexes may persist, be destroyed, or utilized by othe¡ organisms. Nevertheless'
the role that sideroPhores can play as signal molecule§ or regulators in the microbeplant interactions is evide¡t and opens great persPectives for biotechnological
applications in ag culture.
Acknowtcdgments The laboratory work of ROP was parlially suPpofed by CIUNT and
ANPCyT gra¡ts (PICT 2007 N"472). The research of AFS wa§ suppored bv CSIC (Comisión
Sectorial de Investigación Científica, Universidad de la República), PEDECIBA (Programa de
Desarroilo de Ciencias Básicas), and AMI (Agencia Nacional de Investigación e Innovación,
Ur¡rguay). The authors acknowledge rhe support of CYTED through the DIMIAGRI ñerwork
project.
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