589
Bacterial genomics and adaptation to life on plants: implications
for the evolution of pathogenicity and symbiosis
Gail M Preston*, Bernhard Haubold† and Paul B Rainey‡
Many bacteria form intimate associations with plants.
Despite the agricultural and biotechnological significance of
these bacteria, no whole genome sequences have yet been
described. Plant-associated bacteria form a phylogenetically
diverse group, with representative species from many major
taxons. Sequence information from genomes of closely
related bacteria, in combination with technological
developments in the field of functional genomics, provides
new opportunities for determining the origin and evolution of
traits that contribute to bacterial fitness and interactions
with plant hosts.
Addresses
Department of Plant Sciences, University of Oxford, South Parks
Road, Oxford OX1 3RB, UK
*e-mail: [email protected]
†e-mail: [email protected]
‡e-mail: [email protected]
Current Opinion in Microbiology 1998, 1:589–597
http://biomednet.com/elecref/1369527400100589
© Current Biology Ltd ISSN 1369-5274
Abbreviations
COG
clusters of orthologous groups
IVET
in vivo expression technology
MLO
mycoplasma-like organism
PAB
plant-associated bacteria
PGPR plant-growth promoting rhizobacteria
STM
signature tagged mutagenesis
Introduction
Bacteria are inextricably associated with plants as epiphytes and endophytes, pathogens and symbionts. Even
the photosynthetic capacity of plants derives from an
ancient symbiosis between an eukaryotic cell and a relative of modern cyanobacteria [1]. In this review we consider those bacteria that have evolved intimate
associations with plants. These plant-associated bacteria
(PAB) typically exchange signals with their hosts and possess a range of specific adaptations for plant colonisation.
Despite the rapid expansion of genome sequencing, and
the agricultural and biotechnological significance of many
PAB, no complete genome sequence of any PAB has yet
been published. It is even conceivable that the complete
genome sequence of a plant (Arabidopsis) will be available
before the genome sequence of any major bacterial plant
pathogen, symbiont or plant-growth promoting rhizobacteria (PGPR) is completed.
This lack of genome sequences has meant that the excitement of bacterial genomics is yet to impact on the study of
PAB. In this review we aim to draw attention to the value
of the available genome sequence data and to show how it
might be used to address questions concerning the associations that bacteria form with plants and, in particular, the
evolution of symbiosis and pathogenesis. We also consider
the potential benefits likely to accrue from application of
the tools of functional genomics.
Phylogenetic diversity of plant-associated
bacteria
The phylogenetic diversity of PAB suggests that bacteria–plant associations have evolved independently on
many separate occasions (Figure 1). The most thoroughly characterised symbionts and pathogens are found
within the Proteobacteria; however, plant symbionts
such as Frankia and Anabaena spp. are found within the
actinomycetes and cyanobacteria, and plant pathogens
are found within the mollicutes and actinomycetes. In
addition, plants provide a habitat for significant populations of endophytic bacteria, many of which remain
unculturable or unclassified. The impact of these endophytes on plant ecology is yet to be fully explored [2•,3].
The lack of phylogenetically distinct groups of PAB is
exemplified by the Proteobacteria (Figure 2). For example, the genus Pseudomonas (γ subclass) contains the
species P. aeruginosa (an opportunistic animal/human
pathogen), P. syringae (a plant pathogen), and P. fluorescens
and P. putida (isolates of both species are capable of promoting plant growth), while the α subclass contains the
nitrogen-fixing symbiont, Rhizobium and the tumorigenic
plant pathogen Agrobacterium, as well as animal pathogens
such as Brucella and Afipia. From a practical perspective
the close relationship of many PAB to bacteria with
sequenced genomes, such as Erwinia to E. coli (Figures 1
and 2) means that sequence information from these
genomes forms a valuable resource for determining the
identity, origin and evolution of traits that contribute significantly to fitness in PAB.
Functional genomics and adaptation to life on
plants
The currently available data from whole genome
sequences offers many possibilities for comparative analyses. Recent work has shown that classification of homologous genes from sequenced genomes on the basis of
protein similarities into clusters of orthologous groups
(COG) can provide important functional information for
poorly characterised genomes. Orthologues typically have
the same function and therefore it is possible to transfer
functional information from one member to an entire
group. If a newly identified gene is shown to belong to a
particular COG, then the COG system allows automatic
functional and phylogenetic annotation of that gene [4••].
There are instances, however, when comparative
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Genomics
Figure 1
Consensus phylogenetic tree constructed from small ribosomal
subunit RNA sequences, illustrating the evolution of genera containing
plant-associated bacteria within the eubacteria. Major genera of plantassociated bacteria are listed for each of the boxed groups. The
phylogeny is a majority-rule consensus of 1000 trees, each inferred
from parametric distances [89] by the neighbour-joining method, as
implemented in PHYLIP [90]. Branch lengths were fitted using the
Fitch-Margoliash algorithm as implemented in [90]. †The α, β and γ
groups of the Proteobacteria contain many genera of plant-associated
bacteria and are described in detail in Figure 2. Bar = genetic
distance. Desulfovibrio fairfieldensis (D. fai, δ Proteobacteria) and H.
pylori (H. pyl, superfamily VI) represent additional Proteobacteria
groups that are not described in Figure 2. A. aeo, Aquifex aeolicus*;
A. nid, Anacystis nidulans; B. bur, Borellia burgdorferi*; B. sub,
Bacillus subtilis*; C. cre, Caulobacter crescentus*; C. tra, Chlamydia
trachomatis*; C. vib, Chlorobium vibrioforme; Chl, chloroplast
(Nicotiana tabacum); D. fai, Desulfovibrio fairfieldensis; D. rad,
Deinococcus radiodurans*; H. pyl, Helicobacter pylori*; M. gen,
Mycoplasma genitalium*; Mit, mitochondria (Nicotiana tabacum);
N. gon, Neisseria gonorrhoeae*; P. aer, Pseudomonas aeruginosa*;
P. gin, Porphrymonas gingivalis*; S. coe, Streptomyces coelicolor*;
T. mar; Thermotoga maritima*. *Marked bacteria are the subject of
genome sequencing projects, as listed by the National Center for
Genome Resources. For additional information see
http://www.ncgr.org/microbe/bacteria.html
genomics can be of limited use when assigning function to
individual genes [5••]. The regulation, function and ecological significance of homologous genes can vary significantly between organisms. Many genes identified via
genome sequencing have no known function, whereas
genes identified using mutagenesis and bioassays often
display little or no homology to previously characterised
genes. Even when homologies are evident, they are sometimes surprising; for example, a recent study of pathogenicity genes in P. syringae identified tRNA homologues
as key factors of pathogenicity [6•].
differential fluorescence induction (DFI). Despite their
potential, there has been little application of these technologies to PAB. In their own right, these technologies
open the door to an enhanced understanding of the mechanistic basis of plant colonisation and infection, but when
used in conjunction with whole genome sequence their
power is greatly increased; providing a means of rapidly
assigning ecological significance to genes of unknown
function as well as providing clues as to possible function.
The challenge of attributing function to sequenced genes
(and conversely, identifying the genes that encode ecologically relevant traits) is being meet by ‘functional
genomics’ [7,8]. Figure 3 outlines three principle strategies that enable the identification of genes that are active
in complex, natural environments: signature tagged mutagenesis (STM), in vivo expression technology (IVET) and
The first IVET-based technology was developed to isolate
plant-induced genes from Xanthomonas campestris [9].
Subsequently, IVET and similar technologies were developed for use in the study of animal pathogenesis [10–13].
Application of IVET and STM to the study of Salmonella
virulence has unveiled novel pathogenicity islands, novel
genes and virulence factors [13,14,15•] — some of these
have close homologues in PAB [16,17•,18]. In addition, the
identification of Salmonella housekeeping genes that show
Bacterial genomics and adaptation to life on plants Preston, Haubold and Rainey
591
Figure 2
Consensus phylogenetic tree constructed from small ribosomal subunit
RNA sequences, illustrating the evolution of diverse lifestyles among the
Proteobacteria. Associations with plants have been reported for the
species listed in bold, whereas *** indicates species which are
commonly regarded as pathogens of plants or animals. The tree is a
majority-rule consensus of 1000 trees, each inferred from parametric
distances [89] by the neighbour-joining method, as implemented in
PHYLIP [90]. Branch lengths were fitted using the Fitch-Margoliash
algorithm, as implemented in PHYLIP [90]. The numbers indicate how
many trees out of 1,000 supported the clades. Bar = genetic distance.
1Bacteria which have been primarily described as animal pathogens
have also been isolated from plant tissues. 2‘Plant-associated’ species
listed here are also associated with opportunistic infections of wounded
or ‘immune-compromised’ animals. The extent to which strains within
these ‘broad host range’ species are specialised to different ecological
niches is largely unknown.
elevated levels of induction in the host provide an indication of host ecology [13,19].
induced genes is at an early stage a theme is beginning to
emerge of ‘niche-specific traits’, that is, traits shared by
bacteria that occupy the same niche, irrespective of their
phylogenetic position. From a plant–microbe perspective
such traits might include the ability to colonise plant surfaces and tissues, to metabolise plant-derived carbon
sources, and to synthesise plant hormones (phytohormones) or signal molecules that modulate plant physiology and development.
Recently we have developed and applied IVET to study
rhizosphere colonisation by the PGPR P. fluorescens ([20];
PB Rainey, unpublished data). Among the P. fluorescens
genes induced in the rhizosphere are two-component
sensing systems, amino acid transporters, a type III secretion system homologous to the hrp loci of pathogenic bacteria, and a range of novel genes (including genes with
homology to genes of unknown function and genes with
no homology to any sequence in the DNA or protein databases). Some of these genes have homologues across a
range of genera, others are unique to the genus
Pseudomonas (some even appear unique to P. fluorescens),
whereas others have homologues only outside the genus
Pseudomonas. Although our analysis of rhizosphere-
A comprehensive genomics-based approach to the analysis of any organism is clearly powerful, but it is limited in
one important aspect, namely, its ability to determine the
ecological significance of diversity among related strains
[21]. In this respect there is a pressing need for technologies that enable rapid comparison of the genomes and
gene expression patterns of related bacteria. Promising
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Genomics
Figure 3
TOP DOWN
Ecological
significance
&
function
Mutant
Assay
STM
IVET, DFI
Homology
Gene
Expression
Database
Genome
sequence
Genome
organisation
BOTTOM UP
Integrated genomics. A comprehensive
genomics-based strategy involves both
‘bottom up’ (genome sequencing) and ‘top
down’ (function) studies. Each step, from
mutant construction to genome sequencing,
forms part of a web of experiments essential
for establishing the ecological significance of
each individual gene. A key area bridging
‘bottom up’ and ‘top down’ approaches is
‘functional genomics’. Functional genomics
uses high throughput technology to determine
sequence and functional information for large
numbers of genes. Three powerful
approaches are signature tagged
mutagenesis (STM [11]), in vivo expression
technology (IVET [10]) and differential
fluorescence induction (DFI [91•]). These
strategies enable the identification of large
numbers of genes that are active in complex,
natural environments. Dashed arrows indicate
that information can be obtained by inference
(but this is circumstantial and not conclusive).
Current Opinion in Microbiology
developments in DNA chip technologies may provide a
partial solution [22••,23•].
‘Fitness’ islands, adaptive gene clusters and
the dynamic genome
In bacteria it is not unusual to find genes contributing to the
expression of a particular trait linked in operons, or gene
clusters — often forming part of a self transmissible unit,
such as a plasmid or conjugative transposon [24]. In fact it
has been argued that maintenance of the structural integrity
of gene clusters following horizontal transfer has been a driving force in the evolution of operons [25]. The widespread
occurrence of gene clusters involved in a range of ‘adaptive’
phenotypes has led to the suggestion that such clusters
should be viewed as ‘fitness’ islands, which may be either
chromosomally or plasmid borne [26,27•,28•]. Fitness
islands often show evidence of horizontal transfer even
though this capacity may have been lost [27•,29]. The tendency for genes to be linked in operons greatly enhances the
utility of genomics for identifying functionally linked genes.
For example, our analysis of the DNA sequence surrounding a hrcC–IVET fusion strain led to the discovery of a hrp
gene cluster in P. fluorescens (GM Preston, PB Rainey,
unpublished data). The availability of combined physical
and genetic maps (in the absence of complete genome
sequences) can greatly enhance the identification of adaptive gene ‘lodes’ (clusters of genes with adaptive significance), but unfortunately only a relatively small number of
genome maps from PAB exist [30–33].
Parasexual processes operate in PAB populations, just as
they do in other bacteria, and plasmids, insertion elements
and phage are commonplace. Population genetic studies
of PAB have shown evidence of recombination in local
populations of rhizobia [34], among specific groups of leaf
colonising Pseudomonas [35] and in endophytic Azoarcus
[36•]. One of the most striking recent examples of the
importance of horizontal gene transfer in the evolution of
PAB comes from Mesorhizobium loti [37••]. M. loti, like
many rhizobia, contains genes encoding both the nod
(nodulation) and nif (nitrogen fixation) phenotype which
are necessary for the formation of nitrogen-fixing nodules
on leguminous plants. In M. loti these genes are located on
the chromosome, but are part of a 500 kb self-transmissible symbiosis island that integrates into a phe-tRNA gene.
In common with the pathogenicity islands of pathogenic
bacteria, this mobile element carries remnants of phage,
plasmid and transposon. Its ability to convert a free-living
saprophyte into a highly specialised symbiont capable of
close association with a leguminous plant suggests that
elements such as this have an important evolutionary role.
Horizontal gene transfer has also played a significant part
in the dissemination of the type III secretion pathway
among the Proteobacteria [27•]. The type III secretion
pathway is involved the interaction between bacteria and
eukaryotic cells [38] and can be either plasmid encoded
(e.g. Ralstonia solanacearum, Erwinia herbicola, Rhizobium
NGR234), or found in the chromosome as part of a fitness
island (e.g. P. syringae, Erwinia amylovora, Xanthomonas
campestris) [39••,40••,41•]. Comparison of type III genes
from different bacteria suggests that they are nonphyletic in origin; they often have a different guanine (G) and
cytosine (C) content compared to the rest of the genome
and are flanked by sequences indicating an insertion
event. Although originally isolated as pathogenicity
Bacterial genomics and adaptation to life on plants Preston, Haubold and Rainey
genes, their presence in symbiotic and nonpathogenic
bacteria suggests a role in enhancing eukaryote parasitism. For example, nol (type III) mutants of
Sinorhizobium fredii retain the ability to form root nodules,
but the process is retarded [42•]. Similarly, mutations
within the flavonoid-inducible type III secretion pathway
in Rhizobium sp. NGR234 abolishe secretion of y4xL and
NolX and strongly affect the ability of NGR234 to nodulate a variety of tropical legumes [43••]. Type III secretion genes therefore confer a definite, although
sometimes subtle, increase in parasitic fitness [40••,44],
but alone are not sufficient to convert a plant saprophyte
into a pathogen [40••]. Nevertheless, the combination of
both secretion pathway and secreted proteins in a transmissible ‘parasitism’ island provides the potential for parasitism to be acquired in a single horizontal gene transfer
event (given an appropriate genetic background). Such
an event may account for the presence of type III secretion genes in Chlamydia psittaci, a species found outside
the Proteobacteria [45•].
Genomes of bacteria also show substantial dynamism that is
independent of horizontal gene transfer. Insertion elements
and repeated sequence can promote genomic instability by
increasing the frequency with which DNA sequence is
gained or lost — in some cases the enhanced propensity for
genomic rearrangements may have adaptive significance
[46]. The genomes of both rhizobia and Streptomyces are particularly noted for their instability [47•,48•,49,50].
593
in plant pathogenic X. campestris and E. amylovora
[39••,60,61•]. These and similar findings [62,63,64•] suggest that divergent selection operating on a few key traits
has played an important role in the evolution of bacteria.
Host specificity and genetic redundancy
The challenges to our understanding of microbial ecology
presented by considerations of homology and function are
compounded further by the variability and redundancy
found in bacterial genomes. In an ideal world the entire
genome sequences of closely related, but ecologically distinct, strains would be compared, thus enabling the correspondence between variation and function to be
investigated. A primary objective of such a comparison
would be to determine the number of genes that define
host specificity and the ecological and biological significance of variation among alleles [21].
In P. syringae, Xanthomonas spp. and rhizobia, host specificity is defined by both allelic and nonallelic variation.
Evidence that allelic variation has ecological significance is
shown in studies of the avrBs3/pth gene family of
Xanthomonas spp. [65•] and nodABC genes in rhizobia [66].
In both Xanthomonas and Rhizobium variation between alleles affects the host-specificity of gene products — in
Xanthomonas this variation arises as a result of recombination between repeated sequences. Examples of nonallelic
variation affecting host specificity are found among the avr
genes of P. syringae and Xanthomonas spp. [65•], and the
(nod) genes affecting Nod factor structure in rhizobia [67•].
Shared genes, different lifestyles
Horizontal gene transfer not only complicates phylogenetic analyses, but also causes confusion when assigning biological or ecological function to homologous genes.
Identical genes may evolve different roles as a result of
selection in different genetic backgrounds. The type III
secretion genes discussed above provide a clear example,
as do genes for the biosynthesis of auxin (IAA). Auxin
biosynthetic genes are found in both tumorigenic and
necrogenic pathogens (e.g. Agrobacterium spp., E. herbicola
and P. syringae), symbionts (e.g. Bradyrhizobium and
Frankia spp.), in many PGPR and endophytes, and even in
nonplant-associated saprophytes [51,52 •,53]. Because
auxin is a key plant hormone, the presence of these genes
may be highly significant, but homology alone provides no
clue as to their ecological function.
Additional examples of homologues with different roles
include sigma-54 transcription factors involved in transcriptional regulation of diverse metabolic processes
[54,55], and virulence (vir) genes from Agrobacterium spp.
and the animal pathogens Helicobacter pylori and Legionella
pneumophila [56•,57•]. Also secreted proteins with different
roles include NodO from R. leguminosarum that shares features with RTX toxins of animal pathogens (e.g. Escherichia
coli haemolysin) [58,59], and an apoptosis-inducing protein
from animal pathogenic Yersinia and Salmonella spp. that
has homologues in both symbiotic Sinorhizobium fredii and
For many pathogens the evolution of host specificity
appears to have taken the form of an ‘arms race’ between
parasite and host [68], with selection pressure driving parasites to continually acquire new effectors with which to
exploit host cells, while losing or modifying those effectors
that have become elicitors of host surveillance mechanisms
[69,70]. Not surprisingly the cumulative effect of this
genetic warfare has resulted in genomes containing multiple virulence loci whose ecological significance is largely
dependent on genetic background and host genotype;
such is the case with the avrE/dspE locus of P. syringae and
E. amylovora [71••,72,73]. The avrE locus contributes
quantitively to virulence in P. syringae pv. tomato strain
PT23, but not in strain DC3000, however, the homologous
locus dspE is absolutely required for pathogenicity in
Erwinia amylovora.
The process of acquiring new virulence factors or host
specificities may be largely mediated by horizontal gene
transfer. This is vividly illustrated by the observation that
genes encoding nod-mediated specificity have co-evolved
with the host plant genome, rather than the bacterial
genome [65•]. Nonallelic variation of virulence and hostspecificity factors, however, also arise by duplication and
divergence. This is exemplified by the paralogous pectate
lyase enzymes of soft-rotting Erwinia spp. that are not
wholly redundant, but tailored to different aspects of
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Genomics
pathogenesis [74]. In other instances, the role of seemingly redundant genes is yet to be resolved [75]. Evaluating
the contribution of individual loci to parasitic fitness in the
context of such genomic complexity is a daunting challenge that would be greatly aided by a complete inventory
of the genes in a bacterial genome.
As our understanding of the genomic determinants of fitness and the influence of genetic background on bacterial
ecology improves, it may be possible to define genomic
templates that predict the effect of multiple traits on bacterial fitness. At present the rapid identification of bacterial isolates is frequently carried out using immunological
tests, PCR and DNA fingerprints. By assessing and
improving the accuracy of these templates against field isolates it may eventually be possible to estimate the pathogenic or symbiotic potential of a bacterium with a simple
genotypic test [76,77].
The minimal parasite
One powerful approach to understanding the evolution
of parasitism and the determinants of bacterial fitness is
the concept of a minimal parasitic genome. This hypothetical organism has no genetic redundancy, just the
additional quotient of genes needed for a free-living
organism to adopt a parasitic lifestyle. Although in some
respects a naive idea, given that variation in gene regulation makes an organism more than the sum of its genes,
it nevertheless provides a useful ‘null hypothesis’ for
genome characterisation. If the genomes of P. syringae,
P. fluorescens and P. aeruginosa could be compared, then an
understanding of fundamental differences between animal pathogen, plant pathogen and saprophyte would
result. P. aeruginosa can induce disease symptoms on
Arabidopsis under controlled conditions, therefore it
should be possible to determine the nature of additional
changes necessary to render it pathogenic in the field.
Similarly, the hrp cluster of P. syringae allows P. fluorescens
to deliver proteins into plant cells and elicit host
defences. It should therefore be possible to determine
the set of additional genes necessary for multiplication in
planta and elicitation of disease symptoms.
An alternative approach to understanding the evolution
of parasites is to study the genome of an organism likely
to contain a minimal gene set [78,79•]. Obligate animal
pathogens, such as Mycoplasma genitalium or Haemophilus
influenzae, show a clear trend toward reduced genome
size and a greater reliance on the metabolic activities of
their hosts [80]. Assuming that obligate plant parasites
show a similar trend, then comparison of the genomes of
obligate endophytes (e.g. Xylella fastidiosa) and their
free-living relatives (e.g. X. campestris) may provide
insights into the minimal gene content of a PAB. At present the degree of genome reduction in obligate plant
parasites is unknown and the extent to which the ‘minimal’ gene content of a plant-parasitic mycoplasma-likeorganism (MLO) resembles that of an animal parasite, or
the genomes of fastidious phloem and xylem-limited
organisms differ, remains to be determined [81].
The Gram-positive genome
This review has largely ignored Gram-positive PAB such
as Streptomyces scabies, Frankia spp. and Clavibacter michiganensis, in part because much more is known about the
genomes and molecular biology of Gram-negative PAB.
Research into Streptomyces spp. has revealed that their linear chromosomes display a high level of genetic instability, with the potential for adaptation through deletion and
amplification [47•]. The S. scabies pathogenicity gene nec1
is flanked by transposon sequences and has an atypical
GC content, indicating that horizontal gene transfer may
also be significant in the evolution of plant associations
among Gram-positive bacteria [82•]. It is even possible
that horizontal gene transfer has lead to the exchange of
traits between Gram-negative and Gram-positive PAB,
and between free-living PAB and intracellular parasites.
For example, both Frankia spp. and rhizobia produce
phytohormones and have similar nitrogenase genes, but
as yet there is no evidence of nod genes in Frankia spp.
[83]. From a genomics perspective, Bacillus subtilis is an
important bacterium [84••] and although predominantly
soil dwelling it is sometimes found in the soil surrounding plant roots. The genome of B. subtilis shows many
interesting features including the presence of bacteriophage and genes involved in the metabolism of plantderived carbon compounds, such as opines and starch.
Conclusions
Genomics is revolutionising our understanding of the biological world. Although it is yet to fully impact on the study
of PAB, it is clear that there are many potential benefits.
The currently available whole genome sequences from
non-PAB provide a valuable resource and the tools of functional genomics have the potential to yield novel answers
to previously intractable problems. Ultimately of course,
for a comprehensive genomics-based understanding of
PAB, genomes of these bacteria must be sequenced — in
this respect the present lack of PAB genome sequences is
a serious shortcoming.
The phylogenetic diversity of PAB along with the range of
associations they form with plants means that selection of
representative genomes for sequencing is not straight forward. We suggest, however, the following minimum list of
PAB on the grounds of agricultural importance and intensity of scientific research: the pathogens P. syringae pv.
tomato, X. campestris (both are pathogenic on the model
plant, Arabidopsis), Ralstonia solanacearum and A. tumefaciens; the symbiont S. meliloti (or S. leguminosarum) and the
PGPR P. fluorescens. In addition, the complete genome
sequence of a MLO would be invaluable as would the
sequence of a Gram-positive PAB such as Frankia.
Two main surprises are arising from genome comparisons
that affect our understanding of PAB. First, at a genetic
Bacterial genomics and adaptation to life on plants Preston, Haubold and Rainey
level, the distinction between saprophyte, symbiont, and
plant and animal pathogen is almost nonexistent. For
example, symbionts and pathogens deploy the same
plant cell wall degrading enzymes, phytohormones, protein secretion mechanisms and secreted proteins in their
interactions with plants. Similarly, plant and animal
pathogens share common virulence factors, even to the
extent that a single strain of P. aeruginosa can cause disease symptoms in both plants and animals [85••].
Furthermore, many plant-associated species include
strains that cause opportunistic infections of animals
(e.g. Burholderia cepacia). Even ‘beneficial’ symbionts
such as rhizobia or Frankia spp. can have detrimental
effects on crops [86,87]. Such differences in ecological
role may be due to relatively minor alterations in the regulation, presentation or final targets of particular factors.
The second surprise is the extent of the genome that
either is or has been mobile. A consequence of this
mobility is the propensity for evolution in prokaryotes to
occur in ‘leaps’. A commonly held model of the evolution
of parasitism posits that selection leads to the evolution
of parasites with reduced virulence [88]. Accordingly,
symbionts and endophytes are often considered to have
evolved from pathogens. The fact, however, that small
amounts of DNA transferred between strains can convert
a saprophyte into a symbiont, or a pathogen, or vice
versa, suggests that symbiosis may have evolved by various routes. Rapid evolution among bacterial populations
is nothing new, but the ability to unravel the mechanistic basis opens a new and exciting era in the microbiology of plant-associated bacteria.
6.
•
Acknowledgements
17.
•
This work is supported by grants from the Biotechnology and Biological
Sciences Research Council, Royal Society and BTP plc. We are grateful
to Nicolas Bertrand, Micaela Gal and Mike Travisano for comments on
the manuscript.
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