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Principles of Plant-Microbe Interactions

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 Antonie van Leeuwenhoek 81: 373–383, 2002.
© 2002 Kluwer Academic Publishers. Printed in the Netherlands.
373

Microbe–plant interactions: principles and mechanisms

Ben J.J. Lugtenberg∗ , Thomas F.C. Chin-A-Woeng & Guido V. Bloemberg

Leiden University, Institute of Molecular Plant Sciences, Clusius Laboratory, Wassenaarseweg 64, 2333 AL Leiden,
The Netherlands (∗ Author for correspondence)

Key words: anti-fungal metabolites, biofertilizers, biopesticides, colonization, genomics, induced systemic res-
istance, pathogens, phase variation, phytostimulators, quorum sensing, recognition, regulation, rhizoremediators,
two-component systems, Type 4 pili, Type III secretion systems, Type IV secretion systems

Abstract
The present status of research on the molecular basis of microbe–plant interactions is discussed. Principles and
mechanisms which play a role in the interactions of microbial pathogens, biofertilizers, phytostimulators, rhizore-
mediators and biocontrol agents with the plants are treated. Special emphasis is given to colonization, phase
variation, two-component systems, quorum sensing, complex regulation of the syntheses of extracellular enzymes
and secondary metabolites, Type 4 pili and Type III and Type IV secretion systems.

Abbreviations: ACC – 1-aminocyclopropane-1-carboxylic acid; AFM – anti-fungal metabolite; AHL – N-

acylhomoserine lactone; CLSM – confocal laser scanning microscopy; DFI – differential fluorescensce induction;
EPS – extracellular polysaccharide; ISR – induced systemic resistance; IVET – in vivo expression technology; LPS
– lipopolysaccharide; ORF – open reading frame; OT – optical trapping; QS – quorum sensing; PC – phosphatidyl
choline; PCN – phenazine-1-carboxamide; Phl – 2,4-diacetyl phloroglucinol; SAR – systemic acquired resistance;
TTSS – type III secretion system

The challenge of microbiology in the beginning of becoming over-optimistic it is good to realize that even
the 21st century from the best-known organism Escherichia coli K-12,
biochemical function has not yet been established for
In the second half of the twentieth century a major fo- one third of the 4288 ORFs.
cus of microbiology was on trying to understand the Presently, the DNA of several microbes and plants
behaviour of model microbes under laboratory con- which are studied in microbe-plant model systems has
ditions. The challenges for the next decades include been sequenced or will soon be sequenced. On the
understanding of the behaviour of microbes in their other hand, sequencing is still expensive and the se-
natural and often complex habitats, such as the rhizo- quences of many interesting organisms will not soon
sphere and the phyllosphere. A microbe seems largely be available. For example, although the opportunistic
to be driven by principles which also govern our own human pathogen Pseudomonas aeruginosa PAO-1 has
behaviour: a microbe wants to survive, also under hos- been sequenced (5570 ORFs; Stover et al. 2000), it
tile conditions, and if conditions are more favourable is unlikely that the genomic sequences of the many
it will eat and proliferate. In order to understand a mi- Pseudomonas strains which are important plant patho-
crobe’s behaviour in a certain habitat, it is essential gens, phytostimulators, bioremediators or biocontrol
to know which genes are expressed, what their func- agents will soon be available. Based on comparative
tions are, how the gene products interact, how these genomics between E. coli strains it can be predicted
processes depend on biotic and abiotic conditions, and that their genomes not only differ in a few ‘islands’,
towards which behaviour traits this leads. In theory, but that two Pseudomonas strains will differ in hun-
the use of the new technology often designated as ‘Ge- dreds of segments larger than 50 bp. Also the genomes
nomics’ can answer these questions. However, before of fungi and plants are being sequenced, a process
374

which delivers less functional information since only ity is that in the rhizosphere and in the phyllosphere
approx. 1.5% represents ORFs. microbes also interact with each other.
Other novel technologies which will also be useful
to study microbial behaviour are the use of autofluor-
escent proteins in combination with CLSM (confocal Plant recognition by microbes
laser scanning microscopy), atomic force microscopy,
single molecule detection, and DFI (differential fluor- Recognition is considered to be the initial key event
escence induction) combined with OT (optical trap- in the response of plants to microbes. Recognition can
ping) (Allaway et al. 2001). Considering the massive occur through physical interaction – such as through
amounts of information that will be gathered with the adhesins, fimbriae, flagella, and Type III and Type
help of these expensive technologies, networking and IV secretion systems – or through signalling by small
cost-sharing will be key words in the next decades. molecules.
It has been estimated that between 30 and 40 genes
are involved in the biosynthesis and functioning of
Microbe–plant interactions: general type 4 pili in P. aeruginosa (Darzins & Russell 1997).
considerations In this bacterium type 4 pili are involved in the initial
contact between the bacteria and the epithelial cell sur-
Based on their effects on the plant, microbes interact- face, in a unique type of locomotion called twitching
ing with plants can be classified as pathogenic, sap- motility, and in biofilm formation (O’Toole & Kolter
rophytic and beneficial. Pathogens can attack leaves, 1998). Although type 4 pili are present in various plant
stems or roots. An interesting new research field is the pathogens, their role in attachment to plant surfaces
interaction between water-borne microbes and under- is poorly documented. In the case of Xanthomonas
water plants. Saprophytes, which live on dead plant campestris pv. hyacinthi type 4 pili were shown to
material, will not be further treated in this overview al- be involved in attachment to hyacinth leaves whereas
though they play a crucial role in important processes P. syringae pv. phaseolicola attaches to stomata via
such as the cycling of elements and composting. its type 4 pili (Romantschuck & Bamford 1986). Ca-
Beneficial microbes are often used as inoculants macho (2000) obtained evidence for a role of type 4
(Bloemberg & Lugtenberg 2001). They can be classi- pili of P. fluorescens WCS365 in tomato root coloniz-
fied according to the goal of their application: biofer- ation. Dörr et al. (1998) have indicated a role for type 4
tilizers (such as rhizobia, which have been applied pili in attachment of Azoarcus to grass roots as wel as
commercially for over a century), phytostimulators to fungal mycelium. The pilA promoter of Azoarcus is
(such as auxin-producing, root-elongating Azospiril- induced upon starvation in carbon-free medium (Plessl
lum), rhizoremediators (pollutant degraders which use et al. 2000).
root exudate as their carbon source), and biopesticides. One of the interesting and sophisticated mechan-
None of the numerous microbe-plant interactions ism used by bacterial pathogens to attack eukaryotic
is completely understood. Therefore, we have not host cells is a specialized protein secretion system,
chosen for summing up a huge number of facts per the TTSS, that delivers bacterial virulence proteins
interesting microbe but we will restrict ourselves to (‘effector proteins’) directly into the host cell. TT-
a number of newly discovered principles and mech- SSs share four important features (He 1988; Galán
anisms, and discuss a limited number of interactions & Collmer 1999). (i) They are widespread among
between microbes and plants. By now it is clear that plant and animal bacterial pathogens, and mutations
microbes in their interactions with plants, no matter affecting Type III protein secretion often eliminate
whether the microbe is beneficial or pathogenic, of- bacterial virulence completely. More recent evidence
ten use the same mechanisms, although in different suggests also roles of TTSSs in symbiosis and biolo-
combinations and for different purposes. Similarly, it gical control (see further on). (ii) Many of their genes
is clear that microbes in their interaction with plants share sequence similarities with those of the flagel-
use similar strategies as in their interactions with other lar assembly machiney and flagellum-like structures,
eukaryotes such as fungi and humans (Lugtenberg & leading to the speculation that TTSSs are evolution-
Dekker 1999; Chin-A-Woeng et al. 2000; Lugtenberg ary derived from the flagellar assembly apparatus. (iii)
et al. 2001). It is thus good to realise that, although Type III secretion is activated in vivo upon contact
one uses the term microbe–plant interactions, the real- with the host cell. (iv). The TTSS is Sec-independent.
 375

The TTSS of Yersinia spp. is the best-studied example isms, and (iii) weakening or destruction of target and
(Cornelis & Wolf-Watz 1997). competing organisms. In this respect it should be noted
Proteinaceous pertussus toxins are injected into hu- that little research has been carried out on microbe-
man cells by a Type IV secretion system. Another microbe interactions in the rhizosphere. Investigations
member of this system is used for the transloca- towards the molecular basis of bacterium–fungus in-
tion of single stranded T-DNA-protein complexes by teractions have already started (Smith et al. 1999;
Agrobacterium tumefaciens. The channel is composed Lee & Cooksey 2000). The recent discovery that
of 11 VirB proteins and the VirD4 coupling factor. Pseudomonas biocontrol bacteria not only colonize
Transfer of the VirE2 and VirF proteins into plant the plant root but also hyphae of the pathogenic fungus
cells can also occur independently of T-DNA transport Fusarium oxysporum f.sp. radicis-lycopersici (Lago-
(Vergunst et al. 2000). DNA of broad host range con- podi et al. 2002) indicates that such interactions may
jugative plasmids is also transferred through similar be important. Interestingly, many colonization genes
structures. are shared by plant-beneficial bacteria and human-
A second Type IV secretion system has been pathogenic bacteria, indicating that colonization of
detected (Wood et al. 2001) in the genome of A. eukaryotic tissue by bacteria has started early in evol-
tumefaciens, which is composed of 4 replicons: one ution (Lugtenberg & Dekkers 1999; Lugtenberg et al.
linear chromosome, one circular chromosome, the 2001).
tumor-inducing (Ti) plasmid, and a cryptic plasmid. Using colonization mutants, it was shown that
colonization is crucial for biocontrol of tomato foot
and root rot by the PCN (phenazine-1-carboxamide)
Plant surface colonization by microbes producing P. chlororaphis strain PCL1391 (Chin-A-
Woeng et al. 2000) but not, or to a lower extent, for
Colonization of plant tissues can be visualized by biocontrol of this disease by the ISR inducing P. fluor-
using CLSM analysis of autofluorescent proteins ex- escens strain WCS365 (Dekkers et al. 2000). Interest-
pressed in the bacterial and/or fungal partners (Spellig ingly, P. putida mutants impaired in seed colonization
et al. 1996; Bloemberg et al. 1997; Tombolini et al. have recently been described (Espinosa-Urgel et al.
1999; Lagopodi et al. 2002). Using different forms of 2000). In this respect it is interesting to note that,
autofluorescent proteins, Bloemberg et al. (2000) were after seed inoculation, growth of B. cereus in the sper-
able to visualize three different bacterial populations mosphere of tomato depends on the tomato genotype
simultaneously. Using two differently colored popula- (Smith et al. 1999; Simon et al. 2001).
tions of the same P. fluorescens WCS 365 bacterium, IVET (in vivo expression technology) is a powerful
it was concluded that, after inoculation of seedlings, tool to identify promoters and genes that are expressed
occasionally single bacteria reach a position at a lower specifically under certain conditions, e.g. when a bac-
part of the root where they can divide without being terium interacts with a plant (Rainey 1999) or a fungus
frequently visited by a new invader (Bloemberg et al. (Lee & Cooksey 2000). Considering the high number
2000). of colonization genes, a reasonable understanding of
It is generally assumed that the colonization of the mechanisms of root, seed and leaf colonization can
plant tissue is a crucial step in pathogenesis as well only be obtained if the number of bacterial genes to
as for beneficial effects of microbes on the plant. The be tested for a role in colonization can be reduced by
plant surface contains many microbes which, however, preselection. IVET and Genomics of microbe-plant in-
are not homogeneously distributed. Rather, deserted teractions are promising tools for such a preselection.
areas as well as areas with many microbes, often Genomics is also a good approach to unravel which
present as microcolonies or biofilms, are present. Such plant genes play a role in colonization.
microcolonies are ideal places for bacteria to commu-
nicate with each other, e.g. by QS (quorum sensing).
Many genes and traits are involved in colonization (for Phase variation
a review, see Lugtenberg et al. 2001). The results of
colonization studies show that successful colonization Phase variation results in subpopulations within a bac-
strategies include: (i) good defense of the cell’s in- terial ‘pure culture’ which differ in the make up of
terior, (ii) efficient uptake of low concentrations of their bacterial cell surface. This phenomenon occurs
nutrients, including those provided by other organ- in many pathogens and is assumed to be a strategy to
376

escape the host’s immune system. It also appeared to AHLs are involved in interactions between bacteria
play a role in root colonization (Dekkers et al. 1998). and eukaryotes such as conjugation between Agrobac-
In a bacterial culture subpopulations with different de- terium and plant cells, and production of AFMs and
grees of rhizosphere competence can apparently exist other antibiotics and of extracellular enzymes, all of
next to each other. One of the mechanisms of phase which are produced to attack competitors or foreign
variation is based on the action of a site-specific re- cells. Interestingly, also plants secrete substances that
combinase of the λ-integrase gene family which can mimic bacterial AHL activities (Teplitski et al. 2000).
either delete or reverse DNA fragments. Such DNA It appeared that halogenated furanones produced
rearrangements will largely contribute to the flexib- by a marine red algae are able to disrupt AHL-
ility of bacterial genomes (e.g. Flores et al. 2000). regulated behaviours (Givskov et al. 1996; Kjelleberg
It is important to note that phase variation can af- et al. 1997), presumably by competitive inhibition for
fect important (putative) root colonization traits, such the AHL-receptor protein (Manefield et al. 1999). Mo-
as Type 4 fimbriae, and flagellum-mediated swim- lecules which inhibit the action of AHLs, if applied
ming, swarming and twitching, as well as chemotaxis to pathogens, have promise (as lead compounds) for
(Déziel et al. 2001). disease control. Tobacco has been genetically modi-
fied to secrete AHLs, which appeared to affect bacteria
present in its rhizosphere (Fray et al. 1999).
Extracellular enzymes and secondary metabolites,
Synthesis of extracellular enzymes and secondary such as AHLs and AFMs (anti-fungal metabolites), are
metabolites by microbes very important for the interactions of bacteria in the
rhizosphere. The regulation of the production of these
Two-component systems are present in many gram- molecules is extremely complex, in terms of regulat-
negative bacteria. Usually, a sensor kinase in the cyto- ory genes as well as regulatory environmental factors.
plasmic membrane autophosphorylates upon activa- Regulatory components involve rpoS, the gacS/gacA
tion by an environmental stimulus and subsequently two-component system, a regulatory (PrrB) RNA mo-
phosphorylates a response regulator protein in the lecule (Aarons et al. 2000), as well as an RNA
cytosol which then acts as a transcription factor. The binding protein, RsmA, which is a repressor of sec-
GacA/GacS system is the best studied example but its ondary metabolism. The latter molecule is involved in
environmental stimulus has still not been identified. a GacA-dependent switch from primary to secondary
It should be noted that GacS was formerly known metabolism, acting at the level of translation (Blumer
as LemA. Regulation in P. aeruginosa is extremely et al. 1999).
complex with an extraordinary number of putative Quorum sensing plays a role in the synthesis of
two-component systems: 55 sensors, 89 response reg- several exoenzymes and AFMs such as phenazines
ulators and 14 sensor-response regulator hybrids, far (Pierson et al. 1994; Chin-A-Woeng et al. 2001). A
more than found in other genomes (Stover et al. 2000). two component gacA/gacS system has been described
Some bacteria can communicate with cells of their which interacts with the phzl/phzR quorum sensing
own population and sometimes with other bacteria system (Chancey et al. 1999; Chin-A-Woeng et al.
through exchange of soluble signal molecules. Of 2001).
these, the N-acyl homoserine lactones (AHLs) are the The production of AFMs is often limited. The
best studied examples, but other types of intercel- product of phlR acts as a suppressor of Phl (2,4 di-
lular signal compounds exist. These include cyclic acetyl phloroglucinol) production (Delany et al. 2000),
dipeptides and quinolones in P. aeruginosa (Holden whereas psrA limits PCN production (Chin-A-Woeng,
et al. 1999; Pesci et al. 1999), two unidentified unpublished), and synthesis of pyoluteorin is repressed
low molecular weight compounds in Xanthomonas by the serine protease Lon (Whistler et al. 2000).
campestris (Poplawsky et al. 1998), and a volatile The production of Phl, like that of auxin in Azos-
fatty acyl methyl ester in Ralstonia solanacearum pirillum (Vande Broek et al. 1999) is subject to autoin-
(Flavier et al. 1997). In gram-positive bacteria γ - duction. This autoinduction is countered by the plant
butyrolactones are used for intercellular commu- metabolite salicylate, by the bacterial metabolite py-
nication. Interestingly, one of the AHL QS mo- oluteorin and by fusaric acid, a toxin produced by
lecules has previously been described as a bacteriocin the pathogenic fungus Fusarium (Schneider-Keel et al.
(Schripsema et al. 1996). 2000).
 377

Environmental factors which influence the bio- to ‘smell’ the presence of microbes and of non-self
synthesis of secondary metabolites by pseudomonads organisms in its environments (Boller 1995).
include ions, sugars and glycerol (Duffy & Défago One of the defense strategies which the host plant
1999; Chin-A-Woeng 2000). P. putida PCL1444 was can deploy is the ‘hypersensitive response’ (HR) or
selected from an environmental sample as the strain ‘hypersensitive cell death’. The injured plant cell dies
which had the best combination of naphthalene de- very rapidly, causing necrosis of immediately adjacent
gradation and grass root colonization. Its behaviour tissue (Programmed Cell Death; Lam et al. 2001). This
appeared to be determined to a large extent by grass strategy cuts the pathogen off from its nutrients. It is
exudates components: it grew fastest on the major unable to spread and multiply and will finally die.
grass exudates components glucose and succinic acid Phytopathogenic bacteria often contain a cluster of
and expression of its naphthalene degradation operons conserved genes, the hrp cluster, which is essential for
was highest in the presence of these carbon sources the induction of the hypersensitive response in non-
(Kuiper 2001). These results strongly indicate that by host plants as well as for pathogenesis in susceptible
selecting for the traits fast growth and good colon- host plants. The majority of these hrp genes encode
ization, one in fact selects for efficient utilization of elements of a TTSS for proteins (Lindgren 1997; Van
exudate. Gijsegem et al. 1993) which may be evolutionary
derived from the flagellar structure (Macmab 1999).
Some hrp gene products, including a protein called
Plant pathogens harpin, are assumed to be secreted through the type III
‘syringe’, similar to how flagellin subunits are secreted
Fungi are the most important plant pathogens followed through the hollow cylinder in the flagellum’s basal
by viruses and bacteria. Ordinarily, the plant rejects body and its filament. In the case of the TTSS these
the pathogen: most plants are not normally colonised secreted hrp gene products, presently often designated
and parasitized by the pathogen. They are ‘non-host as ‘effector molecules’, are assumed to be injected
plants’ for these pathogens. This phenomenon is called into the host cell. Delivery of the Avr (avirulence)
‘basic resistance’ or ‘basic incompatibility’. Success- gene product, followed by recognition in the plant
ful parasitism depends on the production of the right cell, is essential for development of plant resistance
combination of pathogenicity factors to attack a par- (e.g. Bonas 2000). In the human pathogen Yersinia
ticular pathogen. In such a case ‘basic compatibility’ enterocolitica several virulence factors, including a
exists between these partners. Basic compatibility is a virulence-associated phospholipase are known to be
highly specific phenomenon between a particular plant exported through the TTSS (Cornelis & Wolf-Watz
species and the appropriate pathogen species or forma 1997; Young et al. 1999).
specialis. The tomato pathogen Cladosporium fulvum grows
An elicitor is a microbial signal which is recog- within the intracellular spaces of the leaves, where
nized by a plant receptor. Subsequent transduction it secretes in susceptible cultivars, as well as during
of the signal can result in a defense response by infection of resistant plants, a polypeptide product of
which the plant may ward off the attack. Most fla- the Avr9 gene which causes HR only in race-specific
gellin molecules e.g. from Bacillus, Escherichia and resistant cultivars which carry the cf9 resistance gene.
Pseudomonas, but not from Rhizobium and Agrobac- The 28 amino acid polypeptide encoded by Avr9 acts
terium, share a stretch of approximately 20 amino as a race-specific elicitor. This and a similar peptide
acids in their N-terminal domain which act as general encoded by Avr4, are used for unravelling the mech-
elicitors (Felix et al. 1999). Other general elicitors are anism of plant resistance (see article by P. de Wit and
β-glucans, chitin fragments (including Nod factors!) colleagues in this volume). Like many plant resistance
and ergosterol. Plants recognise these substances with genes, the Cf9 and Cf4 resistance genes contain many
extremely high sensitivity and specificity (Felix et al. glycosylated leucine-rich repeats which are believed
1999). Many of these general elicitors occur in patho- to interact, directly or indirectly, with other proteins,
gens as well as in saprophytes and symbionts. It is carbohydrates or ligands.
therefore unlikely that recognition of these molecules Important bacterial virulence factors include exo-
induces an all-out defense in the plant. Rather, it toxins such as coronatine (Liyanage et al. 1995) and
has been speculated that these chemoperception sys- the biosurfactant toxin syringomycin (Hutchison &
tems might have an orienting role, allowing the plant Gross 1997). The latter toxin seems to act through the
378

formation of ion channels in plant plasma membranes 2000). Some of these molecules are modified during
which initiate a cascade of intracellular signalling the nodulation process (Goosen-de Roo et al. 1991;
events. Pectate lyases are important virulence factors Lugtenberg 1998). The exact role of the PSs (poly-
of soft-rotting erwinias (Keen 1996). saccharides) is hard to unravel since many mutants in
Interestingly, P. aeruginosa strain PA14 is infec- the biosyntheses of these macromolecules are pleio-
tious both for the plant A. thaliana and for mouse. Sev- trophic whereas non-pleiotrophic mutations are some-
eral different mutations reduce pathogenicity in both times complemented by other PSs. A typicality of
hosts, indicating that they encode virulence factors for the LPS of rhizobia is the presence of very long
both plants and animals (Rahme et al. 1995). chain HO-fatty acids, such as 27-OH-C28:0 (Hollings-
worth & Carlson 1989), which can also be present in
Nod-factors (Spaink 2000).
Biofertilizers The membrane phospholipid PC (phosphatidyl-
choline) is a major lipid of eukaryotic mem-
Biofertilization accounts for approximately 65% of the branes, but found in only few prokaryotes, such as
nitrogen supply of crops worldwide. Rhizobiaceae and Bradyrhizobium japonicum, in which 52% of the total
Mycorrhizae are the best-known examples of biofer- phospholipid can consist of PC. A group lead by Otto
tilization. The former microbes are applied to increase Geiger and Isabel Lopez-Lara discovered a new PC
crop yield from leguminous plants, such as soybean, biosynthetic pathway in which choline (present in the
alfalfa and clover grown in nitrogen-poor soil (Spaink rhizosphere) and CDP-diacylglyceride are condensed
et al. 1998). The Mycorrhizae are used for reforesta- (Sohlenkamp et al. 2000). B. japonicum mutants un-
tion of fir plants and act by extending the rhizosphere, able to synthesize PC are inefficient in their symbiosis
thereby enormously increasing the effective root sys- with the soybean host plant (Minder et al. 2001). The
tem of the plant (Bonfante & Perotto 1995; Smith genomes of two Rhizobiaceae have been sequenced.
& Gianninazzi-Pearson 1998). In addition, rather re- Interesting features are the following. (1) The pres-
cently several endophytic nitrogen fixers were dis- ence of genes homologous to those encoding TTSSs
covered. Azoarcus is able to fix nitrogen in Kaller (‘machines’) which are used by pathogenic bacteria to
grass and rice (Reinhold-Hurek & Hurek 1998; Steen- deliver virulence factors into host cells. Recent res-
houdt & Vanderleyden 2000) whereas Herbaspirillum ults show that the rhizobial TTSS secretes specific
and Acetobacter fix N2 in sugar cane (Okon et al. proteins and is involved in the establishment of the
1998). symbiosis. In some cases secreted proteins negatively
Roots of leguminous plants secrete flavonoids affect the nodulation process, perhaps by suppressing
which induce Rhizobium bacteria to form nodules in plant defense responses (Viprey et al. 1998; Marie et
a host-specific way. Some of these flavonoids are able al. 2001; Spaink et al. 2001). (2) The presence of a
to activate the NodD regulatory protein which results 502 kb chromosomally-integrated ‘symbiosis island’
in activation of nod operon which encodes the bio- in Mesorhizobium loti R7A. This island is integrated
synthesis of extremely host-specific Nod-metabolites in a phe-tRNA gene in a process mediated by a P4
(reviewed in Spaink et al. 2000). This host-specificity integrase of which the gene is located on one end of the
is an excellent example of evolutionary fine-tuning of island. The island can be transferred by conjugation to
interactions between microbes and plants. The bac- non-symbiotic mesorhizobia which converts them to
teria enter the plant through infection threads, change Lotus symbionts. The island of strain R7A contains a
into bacteroids in which form they convert atmo- Type IV secretion system similar to the VirB/VirD4
spheric N2 into ammonia. This N-source can be used pilus from A. tumefaciens whereas a similar M. loti
by the plant. To complete the symbiosis, the plant sup- symbiosis island encodes a TTSS (Ronson et al. 2001).
plies the bacteroids with a dicarboxylic acid carbon Natera et al. (2000) analysed proteomes of the
source. symbiosis between Sinorhizobium meliloti strain 1021
Bacterial components which play a role in the and the legume Melilotus alba (white sweetclover)
recognition of the plant in various stages of the nod- with the aim of characterizing symbiosis proteins.
ulation process include the Nod-factors, EPSs (extra- They reported that hundreds of proteins were present
cellular polysaccharides), LPSs (lipopolysaccharides), in altered amounts in the symbiotic vs. the non-
K-antigens (which are structurally very distinct from symbiotic situation.
LPSs) and periplasmatic cyclic glucans (Spaink et al.
 379

Vesicular-arbuscular Mycorrhizae occur in over such microbes can have access to the best food source
80% of all terrestrial plant species (Bonfante & Perotto available in soil, namely root exudates, Kuiper et al.
1995). These fungi are obligate symbionts and colon- (2001) have described an enrichment method for the
ize the cortex of the root in order to obtain carbon isolation of microbes which combine the properties
from their host plant, while assisting the plant with of: (i) degradation of a selected pollutant, and (ii)
the uptake of mineral nutrients, predominantly phos- excellent root colonization. They have termed this pro-
phate, from the soil. In many soils the bioavailable cess ‘rhizoremediation’ instead of phytoremediation
phosphate is present in low concentrations which may to emphasize the roles of the root exudates and the
be limiting for growth (Harrison et al. 1996). The rhizosphere competent microbe.
arbuscular mycorrhizal fungus Gigaspora margarita
harbors a resident population of as many as 250 000
endosymbiotic Burkholderia cells in the cytoplasm of Biocontrol agents or biopesticides
one cell (Ruiz-Lozano & Bonfante 2000).
Preparations of many microbes are commercially
available as biological control agents to protect plants
Phytostimulators against fungi. The major applied organisms are the
bacteria Bacillus, Pseudomonas and Streptomyces and
Some bacteria belonging to the genus Azospirillum the fungi Trichoderma, Gliocladium and Fusarium.
promote plant growth as free-living organisms. A The mechanisms used by these biocontrol agents in-
polar flagellum, of which the flagellin was shown clude the following. (i). Niche exclusion [e.g. by
to be a glycoprotein, is involved in attachment of the frost damage causing leaf colonizing P. syr-
Azospirillum cells to plant roots. Azospirillum fixes ingae (Lindow 1995)]. (ii). Competition for nutrients
atmospheric nitrogen but the observed growth promo- [e.g. for carbon by Fusarium (Alabouvette 1986) and
tion may rather be related to plant growth promoters for Fe3+ siderophore complexes by P. putida strain
produced by the bacterium than by its nitrogen fixing WCS358 (Bakker et al. 1990)]. (iii). Production of
capacity. Indeed, three types of plant growth promot- chitinase by Serratia marcescens (Ordentlich et al.
ing substances have been detected in the supernatant 1987) and by Trichoderma (Sivan & Chet 1989). (iv).
fluids of Azospirillum cultures, namely auxins, cy- Production of AFMs (antifungal metabolites), such
tokinins and gibberellines. Of these, the auxin IAA as Phl (2,4-diacetyl phloroglucinol) [e.g. by pseudo-
(indole-3-acetic acid) is quantitatively the most im- monads (Keel et al. 1990; Bangera & Tomashow
portant one. Three pathways are known to convert 1996), phenazine derivatives (Tomashow & Weller
tryptophan into IAA. Inoculation experiments with 1988; Pierson et al. 1995; Chin-A-Woeng et al.
Azospirillum mutants altered in IAA production sup- 1998; Delany et al. 2001), zwittermycin (Stohl et al.
port the view that after Azospirillum inoculation IAA 1996), pyoluteorin (Nowak-Thompson et al. 1999),
causes increased rooting, which in turn enhances and pyrrolnitrin (Kirnes et al. 1998). Recently it has
mineral uptake (Steenhoudt & Vanderleyden 2000). been discovered that certain biosurfactants also act
Similar results were obtained with a plant growth as AFMs (Stanghellini & Miller 1997; Nielsen et
promoting P. fluorescens strain, which converts exo- al. 2000; Thrane et al. 2000). (v). ISR (Induced
genous tryptophan into IAA. The strain promotes Systemic Resistance) is triggered by certain non-
maturation of radish in greenhouse experiments, pathogenic Pseudomonas rhizobacteria which make
most likely due to the high concentration of trypto- the plant extremely reactive towards a range of patho-
phan measured in radish exudate (G. Bloemberg, N. gens, including leaf pathogens (van Peer et al. 1991;
Makarova, T. Azarova, C. Mulders, L. Kravchenko, M’piga et al. 1997). Flagella, LPS (lipopolysacchar-
I.A. Tikhonovich and B. Lugtenberg, unpublished). ide) and siderophores have been implied as bacterial
components involved in causing ISR (van Loon et al.
1998).
Rhizoremediators ISR differs from SAR (systemic acquired resist-
ance), which is induced upon pathogen infection.
Most environmental pollutants can be degraded by Simultaneous activation of SAR and ISR resulted in
selected microbes. The process stops when the mi- an additive effect on the level of induced protection
crobe is starved of food. In order to ascertain that of Arabidopsis thaliana against P. syringae pv. tomato
380

(van Wees et al. 2000). Ethylene signalling plays a role Blumer C, Heeb S, Pessi G & Haas D (1999) Global GacA-steered
in P. fluorescens WCS417r mediated ISR functions. control of cyanide and exoprotease production in Pseudomonas
fluorescens involves specific ribosome binding sites. Proc. Natl.
Introduction of the ACC deaminase gene, encoding Acad. Sci. 96: 14073–14078.
the cytoplasmic enzyme ACC deaminase, which con- Bonas U, Ballvora A, Büttner D, Hahn K, Lahaye T, Marois E,
verts ACC (1-aminocyclopropane-1-carboxylic acid, a Nennstiel D, Noel L, Pierre M, Szurek B, van den Ackerveken
precursor of ethylene) to ammonia and α-ketobutyrate, G & Rossier O (2000) Hrp type III secretion-mediated signaling
between Xanthomonas and the plant. In: Wit de PJGM, Bissel-
into P. fluorescens strain CHAO improved its ability to ing T, Stiekema WJ (Eds) Biology of Plant-Microbe Interactions
protect cucumber against Pythium damping off. It was (pp 23–28). International Society for Molecular Plant-Microbe
proposed that ACC deaminase decreases the level of Interactions, St. Paul, MN, USA.
pathogen-induced plant ethylene and therefore elimin- Bonfante P & Perotto S (1995) Strategies of arbuscular mycorrhizal
fungi when infecting host plants. New Phytologist 130: 3–21.
ates the pathogen-induced inhibitory effect of ethylene Camacho MM (2000) Molecular characterization of type 4 pili,
on root elongation (Wang et al. 2000). NDHI and PyrR in rhizosphere colonization of Pseudomonas
We would like to finish the overview with a striking fluorescens WCS365. Phd Thesis, Leiden University.
similarity in the strategies of two Pseudomonas strains Chancey ST, Wood DW & Pierson III LS (1999) Two-component
transcriptional regulation of N-acyl-homoserine lactone produc-
to kill eukaryotes. P. aeruginosa kills the nematode C. tion in Pseudomonas aureofaciens. Appl. Environ. Microbiol.
elegans and this killing requires colonization as well 65: 2294–2299.
as the synthesis of the phenazine-derivative pyocyan- Chin-A-Woeng TFC, Bloemberg GV, van der Bij AJ, van der Drift
KMGM, Schripsema J, Kroon B, Scheffer RJ, Keel C, Bakker
ine (Mahajan et al. 1999), whereas P. chlororaphis
PAHM, Tichy H, de Bruijn FJ, Thomas-Oates JE & Lugtenberg
kills fungi, including Fusarium and this killing is ac- BJJ (1998) Biocontrol by phenazine-1-carboxamide-producing
companied by colonization of hyphae (Lagopodi et al. Pseudomonas chlororaphis PCL1391 of tomato root rot caused
2002) and, if present, the root surface (Chin-A-Woeng by Fusarium oxysporum f. sp. radicis-lycopersici. Mol. Plant-
Microbe Interact. 11: 1069–1077.
et al. 2000) as well as by phenazine-1-carboxamide Chin-A-Woeng TFC (2000) Molecular basis of biocontrol of tomato
production (Chin-A-Woeng et al. 1999). foot and root rot by Pseudomonas chlororaphis strain PCL1391.
Phd Thesis, Leiden University.
Chin-A-Woeng TFC, Bloemberg GV, Mulders IHM, Dekkers LC
References & Lugtenberg BJJ (2000) Root colonization by Phenazine-1-
carboxamide-producing bacterium Pseudomonas chlororaphis
Aarons S, Abbas A, Adams C, Fenton A & O’Gara F (2000) A PCL1391 is essential for biocontrol of tomato foot and root rot.
regulatory RNA (PrrB RNA) modulates expression of secondary Mol. Plant-Microbe Interact. 13: 1340–1345.
metabolite genes in Pseudomonas fluorescens F113. J. Bacteriol. Chin-A-Woeng TFC, van den Broek D, de Voer G, van der Drift
182: 3913–3919. KMGM, Tuinman S, Thomas-Oates JE, Lugtenberg BJJ &
Alabouvette C (1986) Fusarium wilt suppresive soils from the chat- Bloemberg GV (2001) Phenazine-1-carboxamide production in
eaurenard region: review of a 10 year study. Agronomie 6: the biocontrol strain Pseudomonas chlororaphis PCL1391 is reg-
273–284. ulated by multiple factors secreted into the growth medium. Mol.
Allaway D, Schofield NA, Leonard ME, Gilardoni L, Finan TM Plant-Microbe Interact. 14: 969–979.
& Poole PS (2001) Use of differential fluorescence induction Cornelis GR & Wolf-Watz H (1997) The Yersinia Yop virulon: a
and optical trapping to isolate environmentally induced genes. bacterial system for subverting eukaryotic cells. Mol. Microbiol.
Environ. Microbiol. 3: 397–406. 23: 861–867.
Bakker PAHM, van Peer R & Schippers B (1990) In: Hornby D (Ed) Darzins A & Russell MA (1997) Molecular genetic analysis of type-
Biological Control of Soil-Borne Plant Pathogens (pp 131–142). 4 pilus biogenesis and twitching motility using Pseudomonas
CAB International, Wallingford. aeruginosa as a model system-a review. Gene 192: 109–115.
Bangera MG & Thomashow LS (1996) Characterization of a Dekkers LC, Phoelich CC, van der Fits L & Lugtenberg BJJ (1998)
genomic locus required for synthesis of the antibiotic 2,4- A site-specific recombinase is required for competitive root col-
diacetylphloroglucinol by the biological control agent Pseudo- onization by Pseudomonas fluorescens WCS365. Proc. Natl.
monas fluorescens Q2-87. Mol. Plant-Microbe Interact. 9: 83– Acad. Sci. 95: 7051–7056.
90. Dekkers, LC, Mulders IHM, Phoelich CC, Chin-A-Woeng TFC,
Bloemberg GV, O’Toole GA, Lugtenberg BJJ & Kolter R (1997) Wijfjes AHM & Lugtenberg BJJ (2000) The sss coloniza-
Green fluorescent protein as a marker for Pseudomonas spp. tion gene of the tomato-Fusarium oxysporum f. sp. radicis-
Appl. Environ. Microbiol. 63: 4543–4551. lycopersici biocontrol strain Pseudomonas fluorescens WCS365
Bloemberg GV, Wijfjes AHM, Lamers GEM, Stuurman N & can improve root colonization of other wild-type Pseudomonas
Lugtenberg BJJ (2000) Simultaneous imaging of Pseudomonas spp. Bacteria. Mol. Plant-Microbe Interact. 13: 1177–1183.
fluorescens WCS365 populations expressing three different auto- Delaney I, Sheehan MM, Fenton A, Bardin S, Aarons S & O’Gara
fluorescent proteins in the rhizosphere: new perspectives for F (2000) Regulation of production of the antifungal metabol-
studying microbial communities. Mol. Plant-Microbe Interact. ite 2,4-diacetylphloroglucinol in Pseudomonas fluorescens F113:
13: 1170–1176. genetic analysis of phlF as a transcriptional repressor. Microbiol.
Bloemberg GV & Lugtenberg BJJ (2001) Molecular basis of plant 146: 537–546.
growth promotion and biocontrol by rhizobacteria. Curr. Op. Delaney SM, Mavrodi DV, Bonsall RF & Thomashow LS (2001)
Plant Biol. 4: 343–350. phzO, a gene for biosynthesis of 2-hydroxylated phenazine com-
 381

pounds in Pseudomonas aureofaciens 30-84. J. Bacteriol 183: urfactant and ion channelforming activities of syringopeptin and
318–327. syringomycin. Mol. Plant-Microbe Interact. 10: 347–354.
Déziel E, Comeau Y & Villemur R (2001) Initiation of biofilm Keel C, Wirthner PH, Oberhansli TH, Voisard C, Burger U,
formation by Pseudomonas aeruginosa 57RP correlates with Haas D & Defago G (1990) Pseudomonads as antagonists of
emergence of hyperpiliated and highly adherent phenotypic vari- plant pathogens in the rhizosphere: role of the antibiotic 2,4-
ants deficient in swimming, swarming, and twitching motilities. diacetylphloroglucinol in the suppression of black root rot of
J. Bacteriol. 183: 1195–1204. tobacco. Symbiosis 9: 327–342.
Dörr J, Hurek T & Reinhold-Hurek B (1998) Type IV pili are in- Keen NT (1996) Bacterial determinants of pathogenicity and avir-
volved in plant-microbe and fungus-microbe interactions. Mol. ulence – an overview. In: Stacey G, Mullin B & Gresshoff PM
Microbiol. 30: 7–17. (Eds) Biology of Plant-Microbe Interactions (pp 145–152) In-
Duffy BK & Défago (1999) Environmental factors modulating anti- ternational Society for Molecular Plant-Microbe Interactions, St.
biotic and siderophore biosynthesis by Pseudomonas fluorescens Paul, MN, USA.
biocontrol strains. Appl. Environ. Microbiol. 65: 2429–2438. Kirner S, Hammer PE Hill DS, Altmann A, Fischer I, Weislo LJ, La-
Espinosa-Urgel M, Salido A & Ramos J-L (2000) Genetic ana- nahan M, van Pée K-H & Ligon JM (1998) Functions encoded by
lysis of functions involved in adhesion of Pseudomonas putida pyrrolnitrin biosynthetic genes from Pseudomonas fluorescens.
to seeds. J. Bacteriol. 182: 2363–2369. J. Bacteriol. 180: 1939–1943.
Felix G, Duran JD, Volko S & Boller T (1999) Plants have a sensit- Kjelleberg S, Steinberg P, Givskov M, Gram L, Manefield M &
ive perception system for the most conserved domain of bacterial Nys de R (1997) Do marine natural products interfere with
flagellin. The Plant Journal 18: 265–276. prokaryotic AHL regulatory systems? Aquat. Microb. Ecol. 13:
Flores M, Mavingui P, Perret X, Broughton WJ, Romero D, Hernán- 85–93.
dez G, Dávila G & Palacios R (2000) Prediction, identification, Kuiper I (2001) Molecular characterization of root colonizing
and artificial selection of DNA rearrangements in Rhizobium: Pseudomonas strains for rhizoremediation. PhD Thesis, Leiden
toward a natural genomic design. Proc. Natl. Acad. Sci. 97: University.
9138–9143. Kuiper I, Bloemberg GV & Lugtenberg BJJ (2001) Selection of
Fray RG, Throup JP, Daykin M, Wallace A, Williams P, Stew- a plant-bacterium pair as a novel tool for rhizostimulation of
art GSAB & Grierson D (1999) Plants genetically modified to polycyclic aromatic hydrocarbon-degrading bacteria. Mol. Plant-
produce N-acylhomoserine lactones communicate with bacteria. Microbe Interact. 14: 1197–1205.
Nature Biotechnol. 17: 1017–1020. Lagopodi AL, Ram AFJ, Lamers GEM, Punt JP, Van den Hondel
Galán JE & Collmer A (1999) Type III secretion machines: bacterial CAMJJ, Lugtenberg BJJ and Bloemberg GV (2002) Novel as-
devices for protein delivery into host cells. Science 284: 1322– pects of tomato root colonization and infection by Fusarium
1328. oxysporum F. sp. radicis-lycopersici revealed by confocal laser
Givskov M, Nys de R, Manefield M, Gram L, Masimillen R, Eberl scanning microscopic analysis using the green fluorescent pro-
L, Molin S, Steinberg PD & Kjelleberg S (1996) Eukaryotic tein as a marker. Mol. Plant-Microbe Interact. 15: 172–179.
interference with homoserine lactone-mediated prokaryotic sig- Lam E, Kato N & Lawton M (2001) Programmed cell death, mi-
nalling. J. Bacteriol. 178: 6618–6622. tochondria and the plant hypersensitive response. Nature 411:
Goosen-de Roo L, de Maagd RA & Lugtenberg BJJ (1991) Anti- 848–853.
genic changes in lipolysaccharide I of Rhizobium leguminosarum Lee S-W & Cooksey DA (2000) Genes expressed in Pseudomonas
bv. viciae in root nodules of Vicia sativa subsp. nigra occur dur- putida during colonization of a plant-pathogenic fungus. Appl.
ing release from injection threads. J. Bacteriol. 173: 3177–3183. Environ. Microbiol. 66: 2764–2772.
Haas D, Blumer C & Keel C (2000) Biocontrol ability of fluores- Lindgren PB (1997) The role of hrp genes during plant-bacterial
cent pseudomonads genetically dissected: importance of positive interactions. Annu. Rev. Phytopathol. 35: 129–152.
feedback regulation. Curr. Opin. Biotech. 11: 290–297. Lindow SE (1995) Control of epiphytic ice nucleation-active bac-
Harrison MJ, Burleigh SH, Liu H & van Buuren ML (1996) teria for management of plant frost injury. In: Lee RE, Warren
Vesicular-Arbuscular mycorrhizae: molecular approaches to in- GJ & Gusta LV (Eds) Biological Ice Nucleation and its Applica-
vestigate phosphate nutrition in the symbiosis. In: Stacey G, tions (pp 239–256). American Phytopathological Society Press,
Mullin B & Gresshoff PM (Eds) Biology of Plant-Microbe St. Paul, MN, USA.
Interactions (pp 515–520) International Society for Molecular Liyanage H, Palmer DA, Ulrich M & Bender CL (1995) Char-
Plant-Microbe Interactions, St. Paul, MN, USA. acterization and transcriptional analysis of the gene cluster for
He SY (1998) Type III protein secretion systems in plant and animal coronafacic acid, the polyketide component of the phytotoxin
pathogenic bacteria. Annu. Rev. Phytopathol. 36: 363–392. coronatine. Appl. Environ. Microbiol. 61: 3843–3848.
Holden MTG, Chhabra SR, Nys de R, Stead P, Bainton NJ, Hill PJ, Lugtenberg BJJ (1998) Outer membrane proteins. In: Spaink HP,
Manefield M, Kumar N, Labatte M, England D, Rice S, Givskov Kondorosi A & Hooykaas PJJ (Eds) The Rhizobiaceae (pp 45–
M, Salmond GPC, Stewart GSAB, Bycroft BW, Kjelleberg S 53). Kluwer Academic Publishers, Dordrecht.
& Williams P (1999) Quorum-sensing cross talk: Isolation and Lugtenberg BJJ & Dekkers LC (1999) What makes Pseudomonas
chemical characterization of cyclic dipeptides from Pseudomo- bacteria rhizosphere competent? Environ. Microbiol. 1: 9–13.
nas aeruginosa and other Gram-negative bacteria. Mol. Micro- Lugtenberg BJJ, Dekkers L & Bloemberg GV (2001) Molecular de-
biol. 33: 1254–1266. terminants of rhizosphere colonization by Pseudomonas. Annu.
Hollingsworth RI & Carlson RW (1989) 27-Hydroxyoctacosanoic Rev. Phytopathol. 39: 461–490.
acid is a major structural fatty acyl component of the lipopoly- M’piga PM, Bélanger RR, Paulitz TC & Benhamou N (1997)
saccharide of Rhizobium trifolii ANU 843. J. Biol. Chem. 264: Increased resistance to Fusarium oxysporum f. sp. radicis-
9300–9303. lycopersici in tomato plants treated with the endophytic bac-
Hutchinson ML, Gross D (1997) Lipopeptide phytotoxins produced terium Pseudomonas fluorescens strain 63-28. Physiol. Mol.
by Pseudomonas syringae pv. syringae: comparison of the bios- Plant Pathol. 50: 301–320.
382

Macnab RM (1999) The bacterial flagellum: reversible rotary pro- Poplawski AR, Chun W, Slater H, Daniels MJ & Dow M (1998)
pellor and type III export apparatus. J. Bacteriol. 181: 7149– Synthesis of extracellular polysaccharide, extracellular enzymes
7153. and xanthomonadin in Xanthomonas campestris: Evidence for
Mahajan MS, Tan MW, Rahme LG & Ausubel FM (1999) Mo- the involvement of two intercellular regulatory signals. Mol.
lecular mechanisms of bacterial virulence elucidated using a Plant-Microbe Interact. 11: 68–70.
Pseudomonas aeruginosa Caenorhabditis elegans pathogenesis Preston GM, Bertrand N, Jackson RW & Rainey PB (2001) Type III
model. Cell 96: 47–56. secretion in Pseudomonas fluorescens SBW25. Abstract of 10th
Manefield M, Nys de R, Jumar N, Read R, Givskov M, Steinberg P International Congr. on Mol. Plant-Microbe Interact. (Abstract
& Kjelleberg S (1999) Evidence that halogenated furanones from #671).
Delisea pulchra inhibit acylated homoserine lactone (AHL)- Rahme LG, Stevens EJ, Wolfort SF, Shao J, Tompkins RG &
mediated gene expression by displacing the AHL signal from its Ausubel FM (1995) Common virulence factors for bacterial
receptor protein. Microbiology 145: 283–291. pathogenicity in plants and animals. Science 268: 1899–1902.
Marie C, Broughton WJ & Deakin WJ (2001) Rhizobium type III Rainey PB (1999) Adaptation of Pseudomonas fluorescens to the
secretion systems: legume charmers or alarmers? Curr. Op. Plant plant rhizosphere. Environ. Microbiol. 3: 243–257.
Biol. 4: 336–342. Reinhold-Hurek B & Hurek T (1998) Life in grasses: diazotrophic
Minder AC, Rudder KEE, Narberhaus F, Fischer H-M, Hen- endophytes. Trends in Microbiol. 6: 139–144.
necke H & Geiger O (2001) Phosphatidylcholine levels in Romantschuk M & Bamford DH (1986) The causal agent of halo
Bradyrhizobium japonicum membranes are critical for an effi- blight in bean, Pseudomonas syringae pv. phaseolicola, attaches
cient symbiosis with the soybean host plant. Mol. Microbiol. 39: to stomata via its pili. Microb. Pathog. 1: 139–148.
1186–1198. Ronson C, Sullivan J, Trzebiatowski J, Gouzy J & de Bruijn
Natera SHA, Guerreiro N & Djordjevic MA (2000) Proteome F (2001) Comparative genomics of the symbiosis island of
analysis of differentially displayed proteins as a tool for the Mesorhizobium loti. In: Abstract of 10th International Congr. on
investigation of symbiosis. Mol. Plant-Microbe Interact. 13: Mol. Plant-Microbe Interact. (Abstract #66).
995–1009. Ruiz-Lozano JM & Bonfante P (2000) A Burkholderia strain living
Nielsen TH, Thrane C, Christophersen C, Anthoni U & Sørensen inside the arbuscular mycorrhizal fungus Gigaspora margar-
J (2000) Structure, production characteristics and fungal ant- ita possesses the vacB gene, which is involved in host cell
agonism of tensin – a new antifungal cyclic lipopeptide from colonization by bacteria. Microb. Ecol. 39: 137–144.
Pseudomonas fluorescens strain 96.578. J. Appl. Microbiol. 89: Schnider-Keel U, Seematter A, Maurhofer M, Blumer C, Duffy B,
992–1001. Gigot-Bonnefoy C, Reimmann C, Notz R, Défago G, Haas D
Nowak-Thompson, B, Chaney N, Wing JS, Gould SJ & Loper & Keel C (2000) Autoinduction of 2,4-diacetylphloroglucinol
JE (1999) Characterization of the pyoluteorin biosynthetic gene biosynthesis in the biocontrol agent Pseudomonas fluorescens
cluster of Pseudomonas fluorescens Pf-5. J. Bacteriol. 181: CHA0 and repression by the bacterial metabolites salicylate and
2166–2174. pyoluteorin. J. Bacteriol. 182: 1215–1225.
O’Toole GA & Kolter R (1998) Flagellar and twitching motility Schripsema J, de Rudder KEE, van Vliet TB, Lankhorst PP, de
are necessary for Pseudomonas aeruginosa biofilm development. Vroom E, Kijne JW & van Brussel AAN (1996) Bacteriocin
Mol. Microbiol. 30: 295–304. small of Rhizobium leguminosarum belongs to the class of N-
Okinaka Y, Yang C-H, Ruiz MG & Keen NT (2001) Microarray acyl-L-homoserine lactone molecules, known as autoinducers
profiling of gene expression in Erwinia chrysanthemi 3937 dur- and as quorum sensing co-transcription factors. J. Bacteriol. 178:
ing plant infection. Abstract of 10th International Congr. on Mol. 366–371.
Plant-Microbe Interact. (Abstract #263). Simon HM, Smith KP, Dodsworth JA, Guenthner B, Handelsman J
Okon Y, Bloemberg GV & Lugtenberg BJJ (1998) Biotechnology & Goodman RM (2001) Influence of tomato genotype on growth
of biofertilization and phytostimulation. In: Altman A (Ed) Ag- of inoculated and indigenous bacteria in the spermosphere. Appl.
ricultural Biotechnology (pp 327–349). Marcel Dekker Inc., New Environ. Microbiol. 67: 514–520.
York. Sivan A & Chet I (1989) The possible role of competition between
Ordentlich A, Elad Y & Chet I (1987) Rhizosphere colonization by Trichoderma harzianum and Fusarium oxysporum on rhizo-
Serratia marcescens for the control of Sclerotium RolfsII. Soil. sphere colonization. Phytopathology 79: 198–203.
Bio. Biochem. 19: 747–751. Smith KP, Handelsman J & Goodman RM (1999) Genetic basis in
Pesci EC, Milbank JBJ, Pearson JP, McKnight S, Kende AS, Green- plants for interactions with disease-suppressive bacteria. Proc.
berg EP & IglewskiBH (1999) Quinolone signaling in the cell-to- Natl. Acad. Sci. 96: 4786–4790.
cell communication system of Pseudomonas aeruginosa. Proc. Smith LM, Tola E, de Boer P & O’Gara F (1999) Signalling by the
Natl. Acad. Sci. 96: 11229–11234. fungus Pythium ultimum represses expression of two ribosomal
Pierson III LS, Keppenne VD & Wood DW (1994) Phenazine RNA operons with key roles in the rhizosphere ecology of
antibiotic biosynthesis in Pseudomonas aureofaciens 30-84 is Pseudomonas fluorescens F113. Environ. Microbiol. 6: 495–502.
regulated by PhzR in response to cell density. J. Bacteriol. 176: Smith SE & Gianinazzi-Pearson V (1988) Physiological interactions
3966–3974. between symbionts in vesicular-arbuscular mycorrhizal plants.
Pierson LS, Gaffney T, Lam S & Gong F (1995) Molecular ana- Ann. Rev. Plant Physiol. Plant Mol. Biol. 39: 221–244.
lysis of genes encoding phenazine biosynthesis in the biological Sohlenkamp C, Rudder KEE, Röhrs, V, López Lara IM & Gei-
control bacterium Pseudomonas aureofaciens. FEMS Microbiol. ger O (2000) Cloning and characterization of the gene for
Lett. 134: 299–307. phosphatidylcholine synthase. J. Biol. Chem. 275: 18919–18925.
Plessl J, Dorr J, Hurek T & Reinhold-Hurek B (2000) Interactions Spaink HP, Kondorosi A & Hooykaas PJJ (Eds) (1998) In: The
of Azoarcus spp. with rice: role of type 4 pili. Fourth European Rhizobiaceae: Molecular Biology of Model Plant-Associate
Nitrogen Fixation Conference. Sevilla, Spain. Abstract book, p. Bacteria. Kluwer Academic Publishers, Dordrecht, The Nether-
31. lands.
 383

Spaink HP (2000) Root nodulation and infection factors produced Van Loon LC, Bakker PAHM & Pieterse CMJ (1998) Systemic res-
by rhizobial bacteria. Ann. Rev. Microbiol. 54: 257–288. istance induced by rhizosphere bacteria. Annu. Rev. Phytopathol.
Spaink HP, Bladergroen MR, Badelt K, Stronk OP & Schlaman 36: 453–483.
WRM (2001) Avirulence factors from symbiotic bacteria. In: Van Peer R, Niemann GJ & Schippers B (1999) Induced res-
Abstract of 10th International Congr. on Mol. Plant-Microbe istance and phytoalexin accumulation in biological control of
Interact. (Abstract #12). fusarium wilt of carnation by Pseudomonas sp. strain WCS417r.
Spellig T, Bottin A & Kahmann R (1996) Green fluorescent pro- Phytopathology 81: 728–734.
tein (GFP) as a new vital marker in the phytopathogenic fungus Van Wees SCM, Swart de EAM, van Pelt JA, van Loon LC &
Ustilago maydis. Mol. Gen. Genet. 252: 503–509. Pieterse CMJ (2000) Enhancement of induced disease resist-
Stanghellini ME & Miller RM (1997) Biosurfactants: Their identity ance by simultaneous activation of salicylate- and jasmonate-
and potential efficacy in the biological control of zoosporic plant dependent defense pathways in Arabidopsis thaliana. Proc. Natl.
pathogens. Plant Disease 81: 4–12. Acad. Sci. 97: 8711–8716.
Steenhoudt O & Vanderleyden J (2000) Azospirillum, a free-living Vergunst AC, Schrammeijer B, den Dulk-Ras A, de Vlaam CMT,
nitrogen-fixing bacterium closely associated with grasses: ge- Regensburg-Tuïnk TJG & Hooykaas PJJ (2000) VirB/D4-
netic, biochemical and ecological aspects. FEMS Microbiol. dependent protein translocation from Agrobacterium into plant
Rev. 24: 487–506. cells. Science 290: 979–982.
Stohl EH, Stabb EV & Handelsman J (1996) Zwittermicin A and Viprey V, Del Greco A, Golinowski W, Broughton WJ & Perret
Biological control of Oomycete pathogens. In: Stacey G, Mullin X (1998) Symbiotic implications of type III protein secretion
B & Gresshoff PM (Eds) Biology of Plant-Microbe Interactions machinery in Rhizobium. Mol. Microbiol. 28: 1381–1389.
(pp 475–486). International Society for Molecular Plant-Microbe Wang C, Knill E, Glick BR & Défago G (2000) Effect of transferring
Interactions, St. Paul, MN, USA. 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase genes
Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, into Pseudomonas fluorescens strain CHAO and its gacA deriv-
Hickey MJ, Brinkman FS, Hufnagle WO, Kowalik DJ & Lagrou ative CHA96 on their growth-promoting and disease-suppressive
M et al. (2000) Complete genome sequence of Pseudomo- capacities. Can. J. Microbiol. 46: 898–907.
nas aeruginosa PAO1, an opportunistic pathogen. Nature 406: Whistler CA, Stockwell VO & Loper JE (2000) Lon protease influ-
959–964. ences antibiotic production and UV tolerance of Pseudomonas
Teplitski M, Robinson JB & Bauer WD (2000) Plants secrete sub- fluorescens Pf-5. Appl. Environ. Microbiol. 66: 2718–2725.
stances that mimic bacterial N-acyl homoserine lactone signal Whiteley M, Lee KM & Greenberg EP (1999) Identification of
activities and affect population density-dependent behaviors in genes controlled by quorum sensing in Pseudomonas aeru-
associated bacteria. Mol. Plant-Microbe Interact. 13: 637–648. ginosa. Proc. Natl. Acad. Sci. 96: 13904–13909.
Thomashow LS & Weller DM (1988) Role of phenazine antibiotic Wood DW, Chen L, Chen Y, Monks DE, Raymond C, Bovee D,
from Pseudomonas fluorescens in biological control of Gaeu- Clendenning J, Kutyavin T, Zhou Y, Setubal JC, Okura VK,
mannomyces graminis var. tritice. J. Bacteriol. 170: 3499–3508. Kitajima JPW, Dolan M, Tomb JF, Zhang S, Kaul R, Olson
Thrane C, Nielsen TH, Nielsen MN, Sørensen J & Olsson S MV, Gordon MP & Nester EW (2001) Sequencing and ana-
(2000) Viscosinamide-producing Pseudomonas fluorescens DR lysis of the Agrobacterium tumefaciensgenome. Abstract of 10th
54 exerts a biocontrol effect on Pythium ultimum in sugar beet International Congr. on Mol. Plant-Microbe Interact. (Abstract
rhizosphere. FEMS Microbiol. Ecol. 33: 139–146. #284).
Tombolini R, van der Gaag DJ, Gerhardson B & Jansson JK Young GM, Schmiel DH & Miller VL (1999) A new pathway for the
(1999) Colonization pattern of the biocontrol strain Pseudo- secretion of virulence factors by bacteria: the flagellar export ap-
monas chlororaphis MA 342 on Barley seeds visualized by paratus functions as a protein-secretion system. Proc. Natl. Acad.
using green fluorescent protein. Appl. Environ. Microbiol. 65: Sci 96: 6456–6461.
3674–3680.
Vande Broek A, Lambrecht M, Eggermont K & Vanderleyden J
(1999) Auxins upregulate expression of the indole-3-pyruvate
decarboxylase gene in Azospirillum brasilense. J. Bacteriol. 181:
1338–1342.

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