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MOL ECU L AR P LA NT P ATHOL OG Y (201 8) 1 9(10) , 2349 –2359 D OI: 10. 111 1/mp p. 126 93

Review
Rhizosphere pseudomonads as probiotics improving plant health
1 2,
YOUNG CHEOL KIM AND ANNE J. ANDERSON *
1
Department of Applied Biology, College of Agriculture and Life Sciences, Chonnam National University, Gwangju 61186, South Korea
2
Department of Biological Engineering, Utah State University, Logan UT 84322-4105, USA

Vacheron et al., 2013), direct defence against potential pathogens


SUMMARY (Garrido-Sanz et al., 2016; Mavrodi et al., 2013), generation of
Many root-colonizing microbes are multifaceted in traits that systemic resistance to enhance tolerance to varied environmental
improve plant health. Although isolates designated as biological stresses (Pieterse et al., 2014; Rosier et al., 2016) and enhanced
control agents directly reduce pathogen growth, many exert mineral nutrition (Rosier et al., 2016; Vacheron et al., 2013).
additional beneficial features that parallel changes induced in Indeed, the term ‘plant growth-promoting rhizobacteria (PGPR)’
animal and other hosts by health-promoting microbes termed was coined 40 years ago to classify microbes that promote plant
probiotics. Both animal and plant probiotics cause direct antago- growth (Kloepper and Schroth, 1978) The use of this designation
nism of pathogens and induce systemic immunity in the host to has broadened to include isolates that alleviate plant stress from
pathogens and other stresses. They also alter host development pathogens and environmental challenges (Glick, 2012). In this
and improve host nutrition. The probiotic root-colonizing pseudo- article, we illustrate how these PGPR isolates that display an array
monads are generalists in terms of plant hosts, soil habitats and of plant health-promoting activities could also be considered as
the array of stress responses that are ameliorated in the plant. plant probiotics.
This article illustrates how the probiotic pseudomonads, nurtured
by the carbon (C) and nitrogen (N) sources released by the plant
Probiotics
in root exudates, form protective biofilms on the root surface and
produce the metabolites or enzymes to boost plant health. The Probiotics are defined as, ‘Live micro-organisms that, when
findings reveal the multifunctional nature of many of the micro- administered in adequate amounts, confer a health benefit on the
bial metabolites in the plant–probiotic interplay. The beneficial host’ (Hill et al., 2014; Neef and Sanz, 2013). Probiotic activity is
effects of probiotics on plant function can contribute to sustain- associated with a variety of microbes and a range of hosts, includ-
able yield and quality in agricultural production. ing humans and other animals, birds (Jin et al., 1997), fish (Ringø
et al., 2010), crustaceans (Van Hai et al., 2009), insects (Evans
Keywords: antimicrobials, biofertilizer, biofilms, biopesticide, and Lopez, 2004; Thorben et al., 2017) and nematodes (Kim and
induced systemic resistance. Mylonakis, 2012). The functions of probiotics in animals include
the limitation of pathogens through varied mechanisms, such as
reduced potential for binding and invasion, depression of growth
by antibiotics and stimulation of host immunity (Derrien and
INTRODUCTION Veiga, 2017; Neef and Sanz, 2013; Rolfe, 2000). Probiotics in the
gut tissue and on skin maintain a microbial balance that mini-
Plants exist in association with microbes; they function together
mizes disease conditions (Nakatsuji et al., 2017). Thus, there is
physically and have intertwined metabolism, such that the plant
strong similarity in the roles of animal probiotics and plant-
and its microbiome is termed the plant holobiont (Bordenstein
associated microbes, such as the root-colonizing pseudomonads,
and Theis, 2015). Some microbes are pathogenic, causing disease
that have beneficial properties (Fig. 1).
(Agrios, 2005). However, other organisms, the beneficial
Beneficial interactions between eukaryotes and probiotic bac-
microbes, improve plant performance (Cook et al., 1995; Pieterse
teria evolved early, in part to capture the extensive and varied
et al., 2014). A class of beneficial microbes, called biocontrol
capacities of microbial metabolic pathways for the benefit of the
agents, protects against pathogen challenge (Garrido-Sanz et al.,
eukaryote (Fraune and Bosch, 2010; McFall-Ngai et al., 2013).
2016; Mavrodi et al., 2013; Pal and Gardener, 2006). However,
Mutual survival of the host and the probiotic occurs from the don-
beneficial microbes exert positive effects on plants in many ways,
ation of a portion of the host metabolite to nurture microbial
as illustrated in Fig. 1. The outcomes include improved host
growth and permit microbial production of compounds that
growth, altered growth morphology (Pangesti et al., 2013;
enhance host performance (Fig. 2). For the plant, the chemical
*Correspondence: Email: annejanderson33@gmail.com arsenal that reduces the viability of microbial pathogens, insects

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Fig. 1 Summary of the potential probiotic-like


effects associated with plant colonization by
beneficial pseudomonads. The image of a
wheat root tip is shown, colonized by
Pseudomonas chlororaphis O6 and stained to
reveal cells with accumulations of nitric oxide.

and nematodes and the metabolites/enzymes that stimulate Sustainable Agriculture’, illustrates the array of potentially effec-
induced stress tolerance are all examples of cross-kingdom inter- tive microbes and their modes of activity for biocontrol, plant
actions. The production of these types of metabolite that induce growth promotion and increased stress tolerance, as well as
stress tolerance in the host is a key trait of a probiotic microbe. issues of commercialization (Lugtenberg, 2015). Microbes are
already commercially formulated into biocontrol-active products or
Probiotics and their potential to improve crop those that improve plant nutrition (Glick, 2012). Moreover,
production probiotic-like activities of certain microbes in the plant micro-
biome are being touted in commercial bio-agricultural formula-
Just as probiotics are being extensively studied for human and
tions, such as MicraCulture, NTEXX Soil Probiotic Inoculant and
animal health (Nakatsuji et al., 2017; Thomas et al., 2015), a bet-
SCD Probiotics-Bio Ag. Indigo and Marron Bio Innovations are
ter understanding of plant-beneficial microbes may contribute to
examples of companies seeking formulations of probiotics for
sustainable agricultural productivity and quality (Glick, 2012;
improved plant performance.
Timmusk et al., 2017). Currently, agriculture is being challenged
This article focuses on the properties of root-colonizing pseu-
to keep pace with the demands of an increasing global popula-
domonads which illustrate their probiotic-like nature for the plant
tion. Crop yields are being perturbed by climate change, with
host. This focus augments the literature in which the beneficial
altered rainfall and temperature patterns, combined with reduced
aspects of other microbes are discussed from different viewpoints.
availability of prime land and quality water for irrigation
For example, the article of Glick (2012) provides a solid introduc-
(Chakraborty et al., 2000; Olesen and Bindi, 2002). Thus, agricul-
tion to mechanisms that are related to biofertilization, improved
ture must integrate new procedures, and investment in the rela-
growth and plant tolerance to disease and environmental stress.
tionship between plant probiotics and crops could be a powerful
Other work has focused on Bacillus isolates (Shafi et al., 2017) or
direction (Mauchline and Malone, 2017; Reid and Greene, 2012).
the lesser studied beneficial microbes with biocontrol potential,
The concept of plant-beneficial microbes as probiotics has already
such as Streptomyces (Rey and Dumas, 2017; Viaene et al., 2016).
been introduced in the literature. The genetic diversity of pseudo-
Rarely does a beneficial effect on plant health correlate with only
monads with probiotic activity was discussed by Picard and Bosco
(2008). Related topics have also been included in a publication
entitled, ‘Bacteria in Agrobiology: Plant Probiotics’ (Maheshwari,
2012), and the value of probiotics in agriculture was discussed by
Berlec (2012). Flores-Felix et al. (2015) used the term ‘plant probi-
otic’ to describe a Phyllobacterium which, as a root colonizer,
improves strawberry plant growth and increases vitamin C content
in the fruits. Hu et al. (2017) introduced the role of pseudomonads
as plant probiotics through their biological control activity.
The concept of the inclusion of beneficial microbes as biofertil-
izers and biopesticides, i.e. probiotics, as a strategy for sustainable
agriculture is established. For example, Bashan (1998) discussed
the commercial formulation of inocula of beneficial microbes. The Fig. 2 Schematic diagram of the basic positive interplay between the
2015 book, ‘Principles of Plant–Microbe Interactions: Microbes for metabolism of the plant and its probiotic-like root colonizers.

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one microbial phenotype: interactions between plants and their 2010). Similar stimulation of systemic resistance occurs in plants
beneficial bacteria have developed with degrees of redundancy through probiotic colonization (Pieterse et al., 2014).
and interdependence at the molecular level, as evidenced in this Of interest is the finding that many of the chemicals with anti-
article, thus providing robust efficacy in the environment. This arti- microbial activity also trigger systemic resistance in the plant.
cle examines studies on plant-associated pseudomonads that illus- These chemicals include phenazines (Kang et al., 2007), the
trate how the varied beneficial plant responses are akin to the pyoverdine-like siderophores (Maurhofer et al., 1994), 2,4-diace-
responses induced in hosts by probiotics. Different sections are tylphloroglucinol (Weller et al., 2012) and pyrrolnitrin (Park et al.,
used to discuss the relevant mechanisms involved in improved 2011). The quorum sensing signals, which regulate the synthesis
plant health: direct biocontrol of pathogens, induced systemic of many of the antimicrobials in pseudomonads, the acyl homo-
resistance, altered host morphology, improved nutrient provision serine lactones (AHSLs), are also stimulants (Schenk and Schikora,
and the achievement of strong plant surface colonization involving 2015; Schikora et al., 2016). The activation of different resistance
biofilm formation. pathways in the plant occurs. For example, 4-aminocarbonyl phe-
nylacetate induces resistance to the necrosis-causing pathogen
PROBIOTIC TRAIT: DIRECT CONTROL OF Pseudomonas syringae pv. tabaci in tobacco, whereas 2R,3R-
PATHOGENS THROUGH ANTIMICROBIAL butanediol stimulates resistance against a soft rot pathogen, but
PRODUCTION not P. syringae infection (Han et al., 2006b). Metabolites with
Control of pathogen development by antimicrobial products from ‘resistance-inducing’ activity also include peptides. A cyclic small
probiotics is one of their beneficial effects in animal hosts peptide, made up of seven different amino acids, acts as an
(Campana et al., 2017; Ocana and Elena Nader-Macias, 2004). inducer of resistance in tobacco against Tobacco mosaic virus
Similarly, antagonism of pathogen growth is a fundamental pro- infection. This peptide, peptamine, is secreted by Pseudomonas
cess for biocontrol efficacy in plant protection. Metabolites with chlororaphis O6 (Park et al., 2012). Thus, peptides feature in both
antimicrobial activity are diverse in their targets with effects on induced and direct resistance to more than one type of plant
bacteria, fungi, insects and nematodes. Extensive literature exists challenge.
characterizing the antimicrobial products from biocontrol-active The mechanisms underpinning the expression of pathogen
pseudomonads, which shows the diversity of the chemistry and resistance in aerial tissues from microbial root colonization are not
mode of action of the active products (Flury et al., 2017; Haas and fully understood. The volatility of such materials as butanediol, or
Defago, 2005; Raaijmakers and Mazzola, 2012). The chemicals effector movement through the plant, as demonstrated for AHSLs
range from HCN and hydrocarbons that are volatiles, to water- (Klein et al., 2009), could be involved in the systemic nature of
soluble structures, including phenolics, iron (Fe)-binding sidero- the responses. Reactive oxygen species (ROS) output in plant cells
phores and peptides (e.g. Sharifi and Ryu, 2016). Although their contacted with the elicitors is speculated to be a primary signal
chemistry and the genes responsible for their synthesis are (Cuypers et al., 2016; Hossain et al., 2015). For instance, phena-
increasingly documented, their actual potential for synthesis and zines stimulate ROS production in contacted cells through their
function under field conditions has been less well studied (Imperi- electron shuttle potential (Briard et al., 2015). With pyoverdine,
ali et al., 2017). Problems of nutrient availability and environmen- hydrogen peroxide production may be a result of hypoxia induced
tal conditions may limit the efficacy of biocontrol agents in some in the plant cells (Fukao and Bailey-Serres, 2004; Kirienko et al.,
field situations. 2013). Butanediol exposure results in hydrogen peroxide and nitric
oxide accumulation in plant cells (Cho et al., 2013b). Wheat root
PROBIOTIC TRAIT: ALTERED HOST IMMUNITY colonization with a pseudomonad induces the accumulation
IS THE PHENOMENON OF INDUCED SYSTEMIC of superoxide anion, a precursor of hydrogen peroxide
RESISTANCE (Wright et al., 2016).
The induction of localized and systemic resistance in a plant host These stimuli result in priming for intense and fast responses
as a result of microbial colonization echoes the local and systemic when the plant is challenged by an abiotic or biotic stress, as
changes in host immunity stimulated by human probiotics. The reviewed by Mauch-Mani et al. (2017). Priming by AHSLs tunes
changes in humans involve multiple effects, including more the plant for faster responses to microbial or environmental chal-
restricted physical barriers and modified production of the signal- lenges (von Rad et al., 2008) through pathways involving the
ling factors involved in inflammation and immune cell transforma- accumulation of salicylic acid and oxylipins (Schenk and Schikora,
tion (Alvarez et al., 2016; Corthesy et al., 2007; Stecher, 2015; 2015; Schikora et al., 2016), both plant metabolites associated
Steinert et al., 2016). Cell surface features of probiotics, as well as with oxidative stress. Priming, involving salicylic acid responses,
responses to secreted metabolites, are involved in the induced together with the jasmonate and ethylene pathways, is found
changes to animal immunity (Corthesy et al., 2007; Meijer et al., with butanediol treatment (Cho et al., 2008, 2013a). Generally,

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however, defence activation by beneficial pseudomonads is well documented (Glick, 1995, 2012; Glick et al., 2007; Li et al.,
tracked to the activation of the jasmonate/ethylene-regulated pro- 2015). The ACC deaminase destroys ACC, the precursor of ethyl-
tective pathway (Spencer et al., 2003; Van der Ent et al., 2009). ene, promoting enhanced growth through responses to IAA.
However, other plant regulators may be involved, such as abscisic Other microbial metabolites also target the IAA pathway. For
acid (ABA)-responsive genes in induced resistance triggered in instance, the antimicrobial diacetylphloroglucinol, produced by
maize by Pseudomonas putida KT2440 (Planchamp et al., 2014), P. fluorescens, disrupts the signalling pathway for IAA in the plant
and the salicylic acid pathway for the interaction of Pseudomonas to causes changes in root morphology (Brazelton et al., 2008).
fluorescens SS101 with Arabidopsis roots under challenge with However, pathways allowing for IAA production are common in
P. syringae pv. tomato and an insect pest, the army worm, Spo- root-colonizing isolates. These pathways use tryptophan as the
doptera exigua (van de Mortel et al., 2012). IAA precursor (Chen et al., 2015; Dimkpa et al., 2012; Garrido-
The accumulation of metabolites connected with the house- Sanz et al., 2016; Vacheron et al., 2013), thus setting up competi-
keeping pathways of host cells is also shifted and may be associ- tion with the use of this amino acid for the production of the anti-
ated with an overall increase in plant resistance to stress (Tauzin microbial, pyrrolnitrin. The amendment of the plant growth
and Giardina, 2014). For example, Fatima and Anjum (2017) medium with tryptophan leads to a proliferation of elongated root
found increases in neutral sugars and specific dicarboxylic acids in hairs at wheat root tips when colonized with microbes that syn-
the response of tomato to challenge with Fusarium wilt when pro- thesize IAA (Adams et al., 2017; Dobbelaere et al., 1999). Root
tected by a root-colonizing Pseudomonas aeruginosa isolate. hairs function in water and mineral uptake for the plant, as well
Higher levels of a stress-protective metabolite, galactinol, are also as the release of rhizodeposits which provide essential nutrition
seen in pseudomonad-colonized cucumber (Kim et al., 2008). for root-associated microbes (Jin et al., 2014). Thus, the IAA-
induced increase in root hairs may stimulate plant growth through
PROBIOTIC TRAIT: ALTERED HOST greater exploration of the soil volume and, consequently, more
DEVELOPMENT AND MORPHOLOGY extensive nutrient and water availability. The interplay between
Animal probiotics change host development, such as intestinal various plant growth regulators initiated by plant association with
responses with increased lymph nodes in the intestine and T and PGPR has been discussed using several scenarios by Glick (2012).
B cell development in expanding Peyers patches, as well as neuro- In addition, IAA production may affect bacterial function through
nal development in the brain (Desbonnet et al., 2015; Hooper, its cell signalling ability. For instance, IAA changes gene expres-
2004; Hrncir et al., 2008; Wilks, 2007). Likewise, developmental sion in Escherichia coli and Rhizobium cells, enhancing protection
and morphological changes are also observed in plants colonized against stress (Bianco et al., 2006; Donati et al., 2013).
by beneficial bacteria (Vacheron et al., 2013; Verbon and
PROBIOTIC TRAIT: IMPROVED NUTRIENT
Liberman, 2016; Zamioudis et al., 2013).
PROVISION
Increased plant growth with microbial colonization has led to
causal microbes being termed ‘plant growth-promoting rhizobac- One long-standing proposed role of animal and insect gut
teria (PGPR)’ (Kloepper and Schroth, 1978). Diverse and interac- microbes is their ability to enhance nutrition. The essential roles of
tive mechanisms are at play in PGPR-induced plant growth gut microbes for cellulose degradation in ruminants and
responses. The mechanisms already discussed could improve plant wood-degrading insects, such as ants, are examples (Engel and
growth by reduced pathogen stress. Increased leaf surface produc- Moran, 2013; Schwarz, 2001). A more subtle example is increased
tion is correlated with the microbially produced volatiles, butane- mineral availability to the probiotic animal host (Scholz-Ahrens
diol and hydrocarbons, already characterized as elicitors of et al., 2007).
induced systemic resistance or direct pathogen antagonism Well-characterized examples of improved nitrogen (N) and
(Chung et al., 2016). Changes in cell wall-loosening enzymes and phosphorus (P) nutrition are consequences of interactions of
auxin homeostasis accompany plant butanediol exposure (Zhang plants with N fixers, such as the specialist Rhizobium isolates and
et al., 2007). Butanediol exposure also causes partial stomatal clo- mycorrhizal colonizers which form specialized structures for nutri-
sure under normal growth conditions, a phenomenon enhancing ent exchange in roots (Andreote and Pereira, 2017). However, the
water retention within leaf tissue to better allow cell expansion pseudomonad generalists may also contribute to improved plant
(Cho et al., 2008). nutrition. The secretion of siderophores into the rhizosphere for
Plant growth may be actively promoted by microbial modifica- the pseudomonads under Fe-limited conditions may increase Fe
tions of the location and levels of plant growth hormones. Roles uptake into the plant through the use of Fe-loaded pyoverdines
for changed levels of the auxin, indole acetic acid (IAA), and (Tomasi et al., 2013; Vansuyt et al., 2007). Higher Fe levels
ethylene in response to microbial production of the enzyme in planta for plants colonized by the phenazine-producing pseudo-
1-aminocyclopropane-1-carboxylate (ACC) deaminase have been monads may also involve their uptake of FeII generated by

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reduction of FeIII by electron shuttling (Hernandez et al., 2004). biofilms on a root or on other surfaces (Pandin et al., (2017).
Certain phenazines also function as Fe chelators (Briard et al., Other studies have raised the possibility that bacterial biofilm for-
2015; Cornelis and Dingemans, 2013) and, together with the side- mation is important in the process of biocontrol (Al-Ali et al.,
rophores, increase the release of Fe and other essential metals 2017; Chen et al., 2013). Indeed, the formation of a biofilm in the
from minerals in the soil by enhancing dissolution (Cornu et al., buccal cavity of the nematode, Caenorhabditis elegans, has been
2014; Ferret et al., 2015; Grant et al., 2016). cited as an active virulence factor for the biocidal effect of Pseudo-
Improved metal and phosphate uptake to rhizosphere organ- monas brassicacearum (Nandi et al., 2016). This process could be
isms by probiotics relates to their secretion of acidic compounds. relevant to the use of the bacterium as a biocontrol agent for
For example, phosphate release is tied to gluconate secretion for nematodes.
several genera of soil microbes, including pseudomonads (Kim
et al., 2003; Miller et al., 2010). Gluconate also contributes to Processes of biofilm formation in root colonization
metal release from minerals because of metal chelation and acid- Biofilm formation is a multistep process, so that many different
ity, enhancing dissolution (Grant et al., 2016). events are involved. Aggressive root colonization may require
The root-associated microbes may also secrete short-chain microbial cells from a seed inoculum to colonize the growing plant
fatty acids as a result of fermentation processes. For example, iso- root tip, a trait that varies between isolates (Lugtenberg et al.,
butyrate is observed in the rhizosphere solution at higher levels 1991; de Weert et al., 2004). Effective root colonization is essen-
when wheat roots are colonized by a probiotic pseudomonad tial for maximum induction of systemic disease resistance (e.g.
(Anderson et al., 2017; Wright et al., 2016). This fermentation Simons et al., 1997). For example, mutants lacking edd, encoding
product is interesting because, in the gut, the formation of short- 6-phosphogluconate dehydratase in the Entner–Douderoff path-
chain fatty acids is linked to the direct inhibition of pathogenic way (Kim et al., 2007), or dctA, encoding a transporter for organic
bacteria (Wrigley, 2004). In the gut, probiotic synthesis of the fer- acids (Nam et al., 2006), show reduced colonizing potential (e.g.
mentation product, butyrate, provides a carbon (C) source for the Han et al., 2006a; Simons et al., 1997). In addition, the biosynthe-
gut cells and triggers cellular changes boosting host immunity sis of certain amino acids and purine is required (Simons et al.,
(Rivière et al., 2016). Whether short-chain fatty acids also modify 1997), because mutants rendered unable to produce these com-
plant cell metabolism requires investigation. pounds fail in effective root colonization.
Colonization initially requires attachment of the microbial cell
PROBIOTIC TRAIT: THE SIGNIFICANCE OF
to the host surface. Binding to a root surface probably involves
BIOFILM FORMATION BY THE MICROBIAL
pili from the microbe’s surface (Chen et al., 2015; Wright et al.,
COLONIZERS
2016) and, subsequently, the type IV pili may aid in the movement
A population density above a threshold level is required for probi- of pseudomonad cells to generate multilayered biofilms (R€omling,
otic efficacy in the human gut and skin. Indeed, disease symptoms 2013). The microbial catabolism of nutrients released from plant
in the gut, such as irritable bowel disease, or on the skin, are cor- roots (Fig. 2) in the root rhizodeposits (Dakora and Phillips, 2002;
related with a lack of certain microbial colonizers and effective Hirsch et al., 2013) contributes the C and N essential for cell repli-
levels of others (Raskov et al., 2016; Winter and Baumler, 2014). cation and growth, and the synthesis of the gel matrix to bind the
The formation of biofilms of probiotics is important for their func- bacterial cells in the biofilms (R€omling, 2013). The matrix for
tioning in the gut. Strains of Lactobacillus probiotics active in the P. aeruginosa contains an acidic polymer, alginate (Remminghorst
gut bind to the gut mucus and form biofilms in medium mimicking and Rehm, 2006), a neutral polymer, Psl, and a polymer, Pel, of
a gut environment (Salas-Jara et al., 2016). The presence of spe- N-acetylgalactosamine, which is proposed to bind the extracellular
cific mucus-binding pili on isolates of Lactobacillus rhamnosus cor- DNA (eDNA) (Flemming and Wingender, 2010; Ryder et al.,
relates with an increased gut residence time anticipated from 2007). Interactions between pili and Psl have been suggested for
improved host cell binding (Reunanen et al., 2012). Growth as a the formation of the multilayered biofilms of P. aeruginosa cells
biofilm of such Lactobacillus isolates occurs with the production of (R€omling, 2013). The 2-hydroxyphenazine-1-carboxylic acid pro-
metabolites that impair pathogen growth and change host immu- duced by several P. chlororaphis isolates conditions biofilm struc-
nity (Aoudia et al., 2016). For example, the antimicrobial reuterin ture through the enhancement of the release of a biofilm matrix
is produced by biofilms of the probiotic Lactobacillus reuteri (Jones component, eDNA, in P. chlororaphis 30–84 (Wang et al., 2016).
and Versalovic, 2009). Other studies have revealed that probiotic Gel formation and its composition, in turn, could alter channelling
metabolites directly inhibit the formation of biofilms by patho- in the biofilm to have an impact on water, oxygen and nutrient
genic microbes (Hancock et al., 2010; Kim et al., 2009). flow.
The outcomes from plant-associated microbes also depend on Findings with pseudomonads correlate the expression of genes
sustained microbial colonization that may take the form of patchy for biofilm formation with the Gac/Rsm network, which also

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controls the production of many of the antimicrobials in pseudo- during the colonization of wheat roots strongly correlates with
monads (Sonnleitner and Haas, 2011; Veselova et al., 2009; Wang increased tolerance of the plants to drought (Timmusk et al.,
et al., 2013). The chemical signals for this network, the AHSLs (Yu 2014, 2015). It is likely that these isolates also produce other fac-
and Head, 2002), regulate microbial cell surface features, as tors that could be involved in drought stress tolerance, but these
shown by mutational analysis in P. chlororaphis isolate 30–84 properties were not characterized. Drought tolerance and the
(Zhang and Pierson, 2001). However, AHSL synthesis in a rich dynamic role of the root microbiome are also the focus of a review
medium is subject to environmental regulation in a root- by Naylor and Coleman-Derr (2018), in which they discuss how
colonizing pseudomonad, with reduced production on exposure to drought changes the composition and metabolic activities of the
certain surfactants (Housley et al., 2009) or high levels of zinc (Zn) root microbiome with an outcome of improved drought tolerance.
(Goodman et al., 2016). These findings are interesting with Studies of the rhizosphere microbiome in forest soils suggest that
respect to the likely patchiness of metal bioavailability and surfac- drought actively induces biofilm formation (Bouskill et al., 2016).
tant levels within soils. The antimicrobial phenazines promote bio- This conclusion is based on comparisons of metabolites and
films in P. chlororaphis 30–84 (Maddula et al., 2006), possibly by enzymes extracted from forest soils, with and without drought
acting as alternative electron acceptors as oxygen within the stress (Bouskill et al., 2016). The microbial response to drought
layers of the biofilm cells becomes depleted (Dietrich et al., 2013; involves increases in the production of osmolytes, such as treha-
Glasser et al., 2014), and/or as Fe chelators (Briard et al., 2015; lose, which protect cells against dehydration (Bouskill et al.,
Wang et al., 2011). In P. aeruginosa, Fe levels are important in 2016). These findings are interesting with respect to the discus-
biofilm formation as well as in dissolution when the cells are sion that plants or microbes engineered to overproduce trehalose
released (Yu et al., 2016). survive better under drought stress (Glick, 2012). Changes in the
Redundancy in the mechanisms of biofilm formation exists. composition and amounts of metabolites, such as organic acids,
The isolate P. chlororaphis O6 rapidly forms biofilms in the released in root exudates from drought-affected plants probably
absence of AHSLs and phenazines in a defined minimal medium contribute to changes in the root microbiome and function
(Kim et al., 2014), as does its gacS mutant, which lacks both (Bouskill et al., 2016; Calvo et al., 2017; Naylor and Coleman-
AHSL and phenazine synthesis (Anderson et al., 2005). Similarly, Derr, 2018).
biofilm formation and root colonization in P. chlororaphis PA23 The mechanisms by which biofilm formation aids in plant pro-
are not eliminated by a gacS mutation (Poritsanos et al., 2006). A tection are at the speculative stage. The formation of the hydrated
strong effect of nutrition on biofilm formation is also observed matrix of the biofilm may improve water retention to maintain
with other pseudomonads (Petrova and Sauer, 2012). The plastic- both microbial and plant cell functioning under drought (Bouskill
ity of biofilm production may enhance microbial survival in the rhi- et al., 2016). In addition, the hydrated biofilm matrix, through the
zosphere where nutrition and challenges are variable. The concept restriction of diffusion, may concentrate microbial metabolites,
that the cells within the biofilm are protected against stress is such as osmolytes or biocontrol-active structures, for a greater
long-standing in the medical field, because antibiotic resistance in impact on plants as inducers of systemic stress tolerance and as
a biofilm is much higher than for the planktonic cells (O’Toole and deterrents of other rhizosphere organisms (Wright et al., 2016).
Stewart, 2005). Indeed, colonization by P. chlororaphis isolate O6, as patchy bio-
Cells, however, are not irreversibly bound in the biofilm films on the root, primes the plant to express genes associated
(Petrova and Sauer, 2016). Dispersal of cells occurs in response to with tolerance to water deficit when water is withheld (Cho et al.,
a variety of environmental conditions, as demonstrated for varia- 2013b). Moreover, the microbial production of butanediol, which
tion in the Fe level for biofilms of P. aeruginosa (Kostakioti et al., triggers partial stomatal closure, contributes to drought stress tol-
2013). Such release may enable the bacteria from colonized plant erance by allowing the leaves to retain higher water contents dur-
roots to travel in the flux of pore waters and by chemotaxis to ing drought (Cho et al., 2008, 2013a, b; Kim et al., 2012). It is
other colonization sites. Regulatory systems that govern biofilm possible that growth as a biofilm affects the redox potential of
formation thus play significant roles in the functions of the probi- microbial cells to promote fermentative metabolism, such as pro-
otics with their plant hosts. motion of the C flux through the pathway for butanediol synthe-
sis. Other microbial products, such as trehalose and polyamines,
Biofilm formation and relevance to drought tolerance
could also be important to both microbe and root cell survival.
Biofilm formation by root-colonizing microbes may play important Secretion of the polyamine spermidine by a PGPR Bacillus isolate
roles in the protection of the plant as well as the microbe. is instrumental in the induction of drought tolerance in the plant
Increased tolerance to drought stress is seen with plants colonized host (Zhou et al., 2017). Although a role in drought tolerance
by certain bacteria (Kim et al., 2012; Naylor and Coleman-Derr, awaits investigation, polyamine synthesis by P. chlororaphis O6 is
2018) . The capacity for biofilm formation by Paenibacillus isolates linked to its biocontrol potential (Park et al., 2017).

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The survival of plants under drought conditions may also be group of talented undergraduate researchers. YCK thanks the Rural
aided through a reduction in the levels of the stress hormone, eth- Development Administration (RDA) for the support of the ‘Cooperative
Research Program for Agriculture Science & Technology Development
ylene, by the microbial production of ACC deaminase (Glick,
(Project No. PJ01250602)’ Rural Development Administration, South
2012). If the pseudomonad possesses the enzyme ACC deami- Korea.
nase, the levels of this precursor for plant-produced ethylene
would be reduced and the effects of IAA promoted. Genes for
CONFLICTS OF INTEREST
ACC deaminase are found in several plant-associated microbes,
including pseudomonads (Hontzeas et al., 2005). However, the The authors have no conflicts of interest with this work.
gene is not found in all beneficial pseudomonad isolates (Garrido-
Sanz et al., 2016). For instance, the isolate P. chlororaphis O6 RE F E RE N C E S
lacks this gene, indicating that, for some microbes, other traits are Adams, J., Wright, M., Wagner, H., Valiente, J., Britt, D. and Anderson, A.
involved in the induction of drought tolerance. The absence of an (2017) Cu from dissolution of CuO nanoparticles signals changes in root morphol-
ogy. Plant Physiol. Biochem. 110, 108–117.
ACC deaminase could also be important, because the plant’s Agrios, G. (2005) Plant Pathology. London: Elsevier Academic Press.
response of induced systemic resistance by some microbes, includ- Al-Ali, A., Deravel, J., Krier, F., Bechet, M., Ongena, M. and Jacques, P. (2017)
Biofilm formation is determinant in tomato rhizosphere colonization by Bacillus
ing P. chlororaphis O6, is dependent on ethylene production for
velezensis FZB42. Environ. Sci. Pollut. Res. 133, 1–11.
the activation of defence gene expression (Spencer et al., 2003). Alvarez, C.-S., Badia, J., Bosch, M., Gim enez, R. and Baldom a, L. (2016) Outer
Thus, restriction of ethylene production through an ACC deami- membrane vesicles and soluble factors released by probiotic Escherichia coli Nissle
1917 and commensal ECOR63 enhance barrier function by regulating expression of
nase may be detrimental in the induction of defence mechanisms tight junction proteins in intestinal epithelial cells. Front. Microbiol. 7, 1981.
by such plant probiotics. Anderson, A.J., Britt, D.W., Johnson, J., Narasimhan, G. and Rodriguez, A.
(2005) Physicochemical parameters influencing the formation of biofilms compared
in mutant and wild-type cells of Pseudomonas chlororaphis O6. Water Sci. Technol.
CONCLUSION: PLANT MICROBIAL COLONIZERS 52, 21–25.
AS PROBIOTICS Anderson, A., McLean, J., McManus, P. and Britt, D. (2017) Soil chemistry influ-
ences the phytotoxicity of metal oxide nanoparticles. Int. J. Nanotechnol. 14,
Many root-colonizing pseudomonads possess traits that endow 15–21.
probiotic-like responses to boost plant performance, enhancing Andreote, F.D. and Pereira, E.S.M.C. (2017) Microbial communities associated
with plants: learning from nature to apply it in agriculture. Curr. Opin. Mirobiol.
both the survival and fitness of both plant and microbe. These 37, 29–34.
properties are also displayed by many other plant-associated Aoudia, N., Rieu, A., Briandet, R., Deschamps, J., Chluba, J., Jego, G., Garrido, C.
microbial species and genera (Glick, 2012; Timmusk et al., 2017). and Guzzo, J. (2016) Biofilms of Lactobacillus plantarum and Lactobacillus fermen-
tum: effect on stress responses, antagonistic effects on pathogen growth and immu-
The synthesis of an array of antimicrobial, insecticidal and nema- nomodulatory properties. Food Microbiol. 53, 51–59.
tocidal compounds, the production of chemical triggers priming Bashan, Y. (1998) Inoculants of plant growth-promoting bacteria for use in agricul-
ture. Biotechnol. Adv. 16, 729–777.
the plant for improved growth and tolerance to abiotic and biotic
Berlec, A. (2012) Novel techniques and findings in the study of plant microbiota:
stresses, as well as root surface colonization involving biofilm for- search for plant probiotics. Plant Sci. 193, 96–102.
mation, are processes involved in their potential as plant probiot- Bianco, C., Imperlini, E., Calogero, R., Senatore, B., Amoresano, A.,
Carpentieri, A., Pucci, P. and Defez, R. (2006) Indole-3-acetic acid improves
ics (Fig. 1). The biofilm of probiotic cells formed on the plant root Escherichia coli’s defences to stress. Arch. Microbiol. 185, 373–382.
surface provides a protective hydrated and physical barrier to the Bordenstein, S.R. and Theis, K.R. (2015) Host biology in light of the microbiome:
root, whilst conferring the potential to provide a longer residence ten principles of holobionts and hologenomes. PLoS Biol. 13, e1002226.
Bouskill, N.J., Wood, T.E., Baran, R., Ye, Z., Bowen, B.P., Lim, H., Zhou, J.,
for secreted microbial metabolites to influence plant cell metabo- Nostrand, J.D., Nico, P., Northen, T.R., Silver, W.L. and Brodie, E.L. (2016)
lism and impair pathogen growth and ingress. The metabolism of Belowground response to drought in a tropical forest soil. I. Changes in microbial
functional potential and metabolism. Front. Microbiol. 7, 525.
the plant and the root-associated probiotics are integrated, lead-
Brazelton, J.N., Pfeufer, E.E., Sweat, T.A., Gardener, B.B. and Coenen, C.
ing to successful performance of the plant holobiont (Fig. 2). Con- (2008) 2,4-Diacetylphloroglucinol alters plant root development. Mol. Plant–
sequently, as in the health industry for animal and human Microbe Interact. 21, 1349–1358.
Briard, B., Bomme, P., Lechner, B.E., Mislin, G.L.A., Lair, V., Pr evost, M.-C.,
probiotics, there is interest in the cataloguing of the parameters Latg e, J.-P., Haas, H. and Beauvais, A. (2015) Pseudomonas aeruginosa manip-
characterized for effective plant probiotics. These findings will be ulates redox and iron homeostasis of its microbiota partner Aspergillus fumigatus
important in the selection and use of plant probiotics (Berlec, via phenazines. Sci. Rep. 5, 8220.
Calvo, O.C., Franzaring, J., Schmid, I., Mu €ller, M., Brohon, N. and Fangmeier,
2012; Ciancio et al., 2016; Premachandra et al., 2016; Zachow A. (2017) Atmospheric CO2 enrichment and drought stress modify root exudation
et al., 2013) in present and future sustainable agricultural of barley. Glob. Change Biol. 23, 1292–1304.
Campana, R., van Hemert, S. and Baffone, W. (2017) Strain-specific probiotic
practices.
properties of lactic acid bacteria and their interference with human intestinal
pathogens invasion. Gut Pathog. 9, 12.
ACKNOWLEDGEMENTS Chakraborty, S., Tiedemann, A.V. and Teng, P.S. (2000) Climate change: poten-
tial impact on plant diseases. Environ. Pollut. 108, 317–326.
AJA thanks the US Department of Agriculture (USDA) for grants for work Chen, Y., Yan, F., Chai, Y., Liu, H., Kolter, R., Losick, R. and Guo, J-H. (2013) Bio-
with isolate O6 (NIFA 1087118) and for their support of an extended control of tomato wilt disease by Bacillus subtilis isolates from natural

C 2 01 8 BSP P A ND J OH N W IL E Y & SO N S L TD M O L E CU L A R P L A NT P AT HO L O G Y (2 0 18 )
V
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8 Y. C. KIM AND A. J. ANDERSON

environments depends on conserved genes mediating biofilm formation. Environ. Flemming, H.-C. and Wingender, J. (2010) The biofilm matrix. Nat. Rev. Microbiol.
Microbiol. 15, 848–864. 8, 623–633.
Chen, Y., Shen, X., Peng, H., Hu, H., Wang, W. and Zhang, X. (2015) Comparative Flores-F elix, J.D., Silva, L.R., Rivera, L.P., Marcos-Garcıa, M., Garcıa-Fraile, P.,
genomic analysis and phenazine production of Pseudomonas chlororaphis, a plant Martınez-Molina, E., Mateos, P.F., Vel azquez, E., Andrade, P. and Rivas, R.
growth-promoting rhizobacterium. Genom. Data, 4, 33–42. (2015) Plant probiotics as a tool to produce highly functional fruits: the case of
Cho, S.M., Kang, B.R., Han, S.H., Anderson, A.J., Park, J.-Y., Lee, Y.-H., phyllobacterium and vitamin C in strawberries. PLoS One, 10, e0122281.
Cho, B.H., Yang, K.-Y., Ryu, C.-M. and Kim, Y.C. (2008) 2R,3R-butanediol, a Flury, P., Vesga, P., P echy-Tarr, M., Aellen, N., Dennert, F., Hofer, N.,
bacterial volatile produced by Pseudomonas chlororaphis O6, is involved in induc- Kupferschmied, K.P., Kupferschmied, P., Metla, Z., Ma, Z., Siegfried, S.,
tion of systemic tolerance to drought in Arabidopsis thaliana. Mol. Plant–Microbe de Weert, S., Bloemberg, G., Ho €fte, M., Keel, C.J. and Maurhofer, M. (2017)
Interact. 21, 1067–1075. Antimicrobial and insecticidal: cyclic lipopeptides and hydrogen cyanide produced
Cho, S.M., Kang, B.R. and Kim, Y.C. (2013a) Transcriptome analysis of induced sys- by plant-beneficial Pseudomonas strains CHA0, CMR12a, and PCL1391 contribute
temic drought tolerance elicited by Pseudomonas chlororaphis O6 in Arabidopsis to insect killing. Front Microbiol. 8, 100.
thaliana. Plant Pathol. J. 29, 209–220. Fraune, S. and Bosch, T.C. (2010) Why bacteria matter in animal development and
Cho, S.M., Kim, Y.H., Anderson, A.J. and Kim, Y.C. (2013b) Nitric oxide and evolution. BioEssays, 32, 571–580.
hydrogen peroxide production are involved in systemic drought tolerance induced Fukao, T. and Bailey-Serres, J. (2004) Plant responses to hypoxia–is survival a bal-
by 2R,3R-butanediol in Arabidopsis thaliana. Plant Pathol. J. 29, 427–434. ancing act? Trends Plant Sci. 9, 449–456.
Chung, J.-H., Song, G.C. and Ryu, C.-M. (2016) Sweet scents from good bacteria: Garrido-Sanz, D., Meier-Kolthoff, J.P., Go €ker, M., Martın, M., Rivilla, R. and
case studies on bacterial volatile compounds for plant growth and immunity. Plant Redondo-Nieto, M. (2016) Genomic and genetic diversity within the Pseudomo-
Mol. Biol. 90, 677–687. nas fluorescens complex. PLoS One, 11, e0150183.
Ciancio, A., Pieterse, C.M.J. and Mercado-Blanco, J. (2016) Editorial: Harnessing Glasser, N.R., Kern, S.E. and Newman, D.K. (2014) Phenazine redox cycling
useful rhizosphere microorganisms for pathogen and pest biocontrol. Front. Micro- enhances anaerobic survival in Pseudomonas aeruginosa by facilitating generation
biol. 7, 1620. of ATP and a proton-motive force. Mol. Microbiol. 92, 399–412.
Cook, R.J., Thomashow, L.S., Weller, D.M., Fujimoto, D., Mazzola, M., Glick, B.R. (1995) The enhancement of plant growth by free-living bacteria. Can. J.
Bangera, G. and Kim, D.S. (1995) Molecular mechanisms of defense by rhizobac- Microbiol. 41, 109–117.
teria against root disease. Proc. Natl. Acad. Sci. USA, 92, 4197–4201. Glick, B.R. (2012) Plant growth-promoting bacteria: mechanisms and applications.
Cornelis, P. and Dingemans, J. (2013) Pseudomonas aeruginosa adapts its iron Scientifica, 2012, 963401. doi: 10.6064/2012/963401.
uptake strategies in function of the type of infections. Front. Cell. Infect. Microbiol. Glick, B.R., Todorovic, B., Czarny, J., Cheng, Z., Duan, J. and McConkey, B.
3, 75. (2007) Promotion of plant growth by bacterial ACC deaminase. Crit. Rev. Plant Sci.
Cornu, J.Y., Elhabiri, M., Ferret, C., Geoffroy, V.A., Jezequel, K., Leva, Y., 26, 5–6.
Lollier, M., Schalk, I.J. and Lebeau, T. (2014) Contrasting effects of pyoverdine on Goodman, J., Mclean, J.E., Britt, D.W. and Anderson, A.J. (2016) Sublethal doses
the phytoextraction of Cu and Cd in a calcareous soil. Chemosphere, 103, 212–219. of ZnO nanoparticles remodel production of cell signaling metabolites in the root
Corthesy, B., Gaskins, H.R. and Mercenier, A. (2007) Cross-talk between probiotic colonizer Pseudomonas chlororaphis O6. Environ. Sci. Nano. 3, 1103–1113.
bacteria and the host immune system. J. Nutr. 137, 781s–790s. Grant, M.R., Tymon, L.S., Helms, G.L., Thomashow, L.S., Kent Keller, C. and
Cuypers, A., Hendrix, S., Amaral dos Reis, R., De Smet, S., Deckers, J., Gielen, H., Harsh, J.B. (2016) Biofilm adaptation to iron availability in the presence of biotite
Jozefczak, M., Loix, C., Vercampt, H., Vangronsveld, J. and Keunen, E. (2016) and consequences for chemical weathering. Geobiology, 14, 588–598.
Hydrogen peroxide, signaling in disguise during metal phytotoxicity. Front. Plant Sci. Haas, D. and Defago, G. (2005) Biological control of soil-borne pathogens by fluo-
7, 470. rescent pseudomonads. Nat. Rev. Microbiol. 3, 307–319.
Dakora, F.D. and Phillips, D.A. (2002) Root exudates as mediators of mineral acqui- Han, S.H., Anderson, A.J., Yang, K.Y., Cho, B.H., Kim, K.Y., Lee, M.C., Kim, Y.
sition in low-nutrient environments. Plant Soil, 245, 35–47. and Kim, Y. (2006a) Multiple determinants influence root colonization and induc-
Derrien, M. and Veiga, P. (2017) Rethinking diet to aid human–microbe symbiosis. tion of induced systemic resistance by Pseudomonas chlororaphis O6. Mol. Plant
Trends Microbiol. 25, 110–112. Pathol. 7, 463–472.
Desbonnet, L., Clarke, G., Traplin, A., O’Sullivan, O., Crispie, F., Moloney, R.D., Han, S.H., Lee, S.J., Moon, J.H., Park, K.H., Yang, K.Y., Cho, B.H., Kim, K.Y.,
Cotter, P.D., Dinan, T.G. and Cryan, J.F. (2015) Gut microbiota depletion from Kim, Y.W., Lee, M.C., Anderson, A.J. and Kim, Y.C. (2006b) GacS-dependent
early adolescence in mice: implications for brain and behaviour. Brain Behav. production of 2R,3R-butanediol by Pseudomonas chlororaphis O6 is a major deter-
Immun. 48, 165–173. minant for eliciting systemic resistance against Erwinia carotovora but not against
Dietrich, L.E.P., Okegbe, C., Price-Whelan, A., Sakhtah, H., Hunter, R.C. and Pseudomonas syringae pv. tabaci in tobacco. Mol. Plant–Microbe Interact. 19,
Newman, D.K. (2013) Bacterial community morphogenesis is intimately linked to 924–930.
the intracellular redox state. J. Bacteriol. 195, 1371–1380. Hancock, V., Dahl, M. and Klemm, P. (2010) Probiotic Escherichia coli strain Nissle
Dimkpa, C.O., Zeng, J., McLean, J.E., Britt, D.W., Zhan, J. and Anderson, A.J. 1917 outcompetes intestinal pathogens during biofilm formation. J. Med. Micro-
(2012) Production of indole-3-acetic acid via the indole-3-acetamide pathway in biol. 59, 392–399.
the plant-beneficial bacterium Pseudomonas chlororaphis O6 is inhibited by ZnO Hernandez, M.E., Kappler, A. and Newman, D.K. (2004) Phenazines and other
nanoparticles but enhanced by CuO nanoparticles. Appl. Environ. Microbiol. 78, redox-active antibiotics promote microbial mineral reduction. Appl. Environ. Micro-
1404–1410. biol. 70, 921–928.
Dobbelaere, S., Croonenborghs, A., Thys, A., Broek, A.V. and Vanderleyden, J. Hill, C., Guarner, F., Reid, G., Gibson, G.R., Merenstein, D.J., Pot, B., Morelli, L.,
(1999) Phytostimulatory effect of Azospirillum brasilense wild type and mutant Canani, R.B., Flint, H.J., Salminen, S., Calder, P.C. and Sanders, M.E. (2014)
strains altered in IAA production on wheat. Plant Soil, 212, 153–162. Expert consensus document: the international scientific association for probiotics and
Donati, A.J., Lee, H.-I., Leveau, J.H.J. and Chang, W.-S. (2013) Effects of indole- prebiotics consensus statement on the scope and appropriate use of the term probi-
3-acetic acid on the transcriptional activities and stress tolerance of Bradyrhi- otic. Nat. Rev. Gastroenterol. Hepatol. 11, 506–514.
zobium japonicum. PLoS One, 8, e76559. Hirsch, P.R., Miller, A.J. and Dennis, P.G. (2013) Do Root Exudates Exert More
Engel, P. and Moran, N.A. (2013) The gut microbiota of insects – diversity in struc- Influence on Rhizosphere Bacterial Community Structure than Other Rhizodeposits.
ture and function. FEMS Microbiol. Rev. 37, 699–735. Hoboken, NJ: Wiley.
Evans, J.D. and Lopez, D.L. (2004) Bacterial probiotics induce an immune response Hontzeas, N., Richardson, A.O., Belimov, A., Safronova, V., Abu-Omar, M.M.
in the honey bee (Hymenoptera: Apidae). J. Econ. Entomol. 97, 752–756. and Glick, B.R. (2005) Evidence for horizontal transfer of 1-aminocyclopropane-1-
Fatima, S. and Anjum, T. (2017) Identification of a potential ISR determinant from carboxylate deaminase genes. Appl. Environ. Microbiol. 71, 7556–7558.
Pseudomonas aeruginosa PM12 against Fusarium wilt in tomato. Front. Plant Sci. Hooper, L.V. (2004) Bacterial contributions to mammalian gut development. Trends
8, 848. Microbiol. 12, 129–134.
Ferret, C., Cornu, J.Y., Elhabiri, M., Sterckeman, T., Braud, A., Jezequel, K., Hossain, M.A., Bhattacharjee, S., Armin, S.-M., Qian, P., Xin, W., Li, H.-Y.,
Lollier, M., Lebeau, T., Schalk, I.J. and Geoffroy, V.A. (2015) Effect of pyover- Burritt, D.J., Fujita, M. and Tran, L.-S.P. (2015) Hydrogen peroxide priming
dine supply on cadmium and nickel complexation and phytoavailability in hydro- modulates abiotic oxidative stress tolerance: insights from ROS detoxification and
ponics. Environ. Sci. Pollut. Res. Int. 22, 2106–2116. scavenging. Front. Plant Sci. 6, 420.

MO L E CU L AR P L A N T P A TH OL O G Y ( 20 1 8) V
C 2 0 18 BSP P A N D JO HN W I L EY & SO NS L TD
Plant probiotics 9
2357

Housley, L., Anderson, T., Sontag, N., Han, S.-H., Britt, D.W. and Anderson, A.J. Lugtenberg, B. (2015) Principles of Plant–Microbe Interactions: Microbes for Sus-
(2009) Pluronics’ influence on pseudomonad biofilm and phenazine production. FEMS tainable Agriculture. Cham, Heidelberg, New York: Dordrecht; London: Springer.
Microbiol. Lett. 293, 148–153. Lugtenberg, B.J.J., de Weger, L.A. and Bennett, J.W. (1991) Microbial stimulation
Hrncir, T., Stepankova, R., Kozakova, H., Hudcovic, T. and Tlaskalova- of plant growth and protection from disease. Curr. Opin. Biotechnol. 2, 457–464.
Hogenova, H. (2008) Gut microbiota and lipopolysaccharide content of the diet Maddula, V.S.R.K., Zhang, Z., Pierson, E.A. and Pierson, L.S III. (2006) Quorum
influence development of regulatory T cells: studies in germ-free mice. BMC Immu- sensing and phenazines are involved in biofilm formation by Pseudomonas chloror-
nol. 9, 65. aphis (aureofaciens) strain 30–84. Microb. Ecol. 52, 289–301.
Hu, J., Wei, Z., Weidner, S., Friman, V.-P., Xu, Y.-C., Shen, Q.-R. and Jousset, A. Maheshwari, D.K. (2012) Bacteria in Agrobiology: Plant Probiotics. Berlin, Heidel-
(2017) Probiotic Pseudomonas communities enhance plant growth and nutrient berg: Springer.
assimilation via diversity-mediated ecosystem functioning. Soil Biol. Biochem. 113, Mauch-Mani, B., Baccelli, I., Luna, E. and Flors, V. (2017) Defense priming: an
122–129. adaptive part of induced resistance. Annu. Rev. Plant Biol. 68, 485–512.
Imperiali, N., Dennert, F., Schneider, J., Laessle, T., Velatta, C., Fesselet, M., Mauchline, T.H. and Malone, J.G. (2017) Life in earth – the root microbiome to the
Wyler, M., Mascher, F., Mavrodi, O., Mavrodi, D., Maurhofer, M. and Keel, C. rescue? Curr. Opin. Mirobiol. 37, 23–28.
(2017) Relationships between root pathogen resistance, abundance and expression of Maurhofer, M., Hase, C., Meuwly, P., Metraux, J.P. and Defago, G. (1994)
Pseudomonas antimicrobial genes, and soil properties in representative Swiss agricul- Induction of systemic resistance of tobacco to tobacco necrosis virus by the root-
tural soils. Front. Plant Sci. 8, 427. colonizing Pseudomonas fluorescens strain CHA 0: influence of the gacA gene and
Jin, C.W., Ye, Y.Q. and Zheng, S.J. (2014) An underground tale: contribution of of pyoverdine production. Phytopathology, 84, 139–146.
microbial activity to plant iron acquisition via ecological processes. Ann. Bot. 113, Mavrodi, D.V., Parejko, J.A., Mavrodi, O.V., Kwak, Y.-S., Weller, D.M.,
7–18. Blankenfeldt, W. and Thomashow, L.S. (2013) Recent insights into the diversity,
Jin, L., Ho, Y., Abdullah, N. and Jalaludin, S. (1997) Probiotics in poultry: modes frequency and ecological roles of phenazines in fluorescent Pseudomonas spp.
of action. World’s Poultry Sci. J. 53, 351–368. Environ. Microbiol. 15, 675–686.
Jones, S.E. and Versalovic, J. (2009) Probiotic Lactobacillus reuteri biofilms produce McFall-Ngai, M., Hadfield, M.G., Bosch, T.C.G., Carey, H.V., Domazet-Loso, T.,
antimicrobial and anti-inflammatory factors. BMC Microbiol. 9, 35. Douglas, A.E., Dubilier, N., Eberl, G., Fukami, T., Gilbert, S.F., Hentschel, U.,
Kang, B.R., Han, S.-H., Zdor, R.E., Anderson, A.J., Spencer, M. and Yang, K.Y. King, N., Kjelleberg, S., Knoll, A.H., Kremer, N., Mazmanian, S.K., Metcalf, J.L.,
(2007) Inhibition of seed germination and induction of systemic disease resistance Nealson, K., Pierce, N.E., Rawls, J.F., Reid, A., Ruby, E.G., Rumpho, M.,
by Pseudomonas chlororaphis O6 requires phenazine production regulated by the Sanders, J.G., Tautz, D. and Wernegreen, J.J. (2013) Animals in a bacterial
global regulator, GacS. J. Microbiol. Biotechnol. 17, 586–593. world, a new imperative for the life sciences. Proc. Natl. Acad. Sci. USA, 110,
Kim, C.H., Han, S.H., Kim, K.Y., Cho, B.H., Kim, Y.H., Koo, B.S. and Kim, Y.C. 3229–3236.
(2003) Cloning and expression of pyrroloquinoline quinone (PQQ) genes from a Meijer, K., de Vos, P. and Priebe, M.G. (2010) Butyrate and other short-chain fatty
phosphate-solubilizing bacterium Enterobacter intermedium. Curr. Microbiol. 47, acids as modulators of immunity: what relevance for health? Curr. Opin. Clin. Nutr.
457–461. Metab. Care, 13, 715–721.
Kim, H.J., Nam, H.S., Anderson, A.J., Yang, K.Y., Cho, B.H. and Kim, Y.C. (2007) Miller, S.H., Browne, P., Prigent-Combaret, C., Combes-Meynet, E., Morrissey,
Mutation in the edd gene encoding the 6-phosphogluconate dehydratase of Pseu- J.P. and O’Gara, F. (2010) Biochemical and genomic comparison of inorganic
domonas chlororaphis O6 impairs root colonization and is correlated with reduced phosphate solubilization in Pseudomonas species. Environ. Microbiol. Rep. 2,
induction of systemic resistance. Lett. Appl. Microbiol. 44, 56–61. 403–411.
Kim, J.S., Kim, Y.H., Park, J.Y., Anderson, A.J. and Kim, Y.C. (2014) The global van de Mortel, J.E., de Vos, R.C.H., Dekkers, E., Pineda, A., Guillod, L.,
regulator GacS regulates biofilm formation in Pseudomonas chlororaphis O6 differ- Bouwmeester, K., van Loon, J.J.A., Dicke, M. and Raaijmakers, J.M. (2012)
ently with carbon source. Can. J. Microbiol. 60, 133–138. Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacte-
Kim, M.S., Cho, S.M., Kang, E.Y., Im, Y.J., Hwangbo, H., Kim, Y.C., Ryu, C.-M., rium Pseudomonas fluorescens SS101. Plant Physiol. 160, 2173–2188.
Yang, K.Y., Chung, G.C. and Cho, B.H. (2008) Galactinol is a signaling compo- Nakatsuji, T., Chen, T.H., Narala, S., Chun, K.A., Two, A.M., Yun, T., Shafiq, F.,
nent of the induced systemic resistance caused by Pseudomonas chlororaphis O6 Kotol, P.F., Bouslimani, A., Melnik, A.V., Latif, H., Kim, J.-N., Lockhart, A.,
root colonization. Mol. Plant–Microbe Interact. 21, 1643–1653. Artis, K., David, G., Taylor, P., Streib, J., Dorrestein, P.C., Grier, A., Gill, S.R.,
Kim, Y. and Mylonakis, E. (2012) Caenorhabditis elegans immune conditioning Zengler, K., Hata, T.R., Leung, D.Y.M. and Gallo, R.L. (2017) Antimicrobials
with the probiotic bacterium Lactobacillus acidophilus strain NCFM enhances from human skin commensal bacteria protect against Staphylococcus aureus and
gram-positive immune responses. Infect. Immun. 80, 2500–2508. are deficient in atopic dermatitis. Sci. Transl. Med. 9, eaah4680.
Kim, Y., Oh, S. and Kim, S.H. (2009) Released exopolysaccharide (r-EPS) produced Nam, H.S., Anderson, A.J., Yang, K.Y., Cho, B.H. and Kim, Y.C. (2006) The dctA
from probiotic bacteria reduces biofilm formation of enterohemorrhagic Escherichia gene of Pseudomonas chlororaphis O6 is under RpoN control and is required for
coli O157: H7. Biochem. Biophys. Res. Commun. 379, 324–329. effective root colonization and induction of systemic resistance. FEMS Microbiol.
Kim, Y.-C., Glick, B.R., Bashan, Y. and Ryu, C.-M. (2012) Enhancement of plant Lett. 256, 98–104.
drought tolerance by microbes. In: Plant Responses to Drought Stress: From Mor- Nandi, M., Berry, C., Brassinga, A.K.C., Belmonte, M.F., Fernando, W.G.D.,
phological to Molecular Features (Aroca, R., ed.), pp. 383–413. Berlin, Heidelberg: Loewen, P.C. and de Kievit, T.R. (2016) Pseudomonas brassicacearum strain
Springer. DF41 kills Caenorhabditis elegans through biofilm-dependent and biofilm-
Kirienko, N.V., Kirienko, D.R., Larkins-Ford, J., W€ ahlby, C., Ruvkun, G. and independent mechanisms. Appl. Environ. Microbiol. 82, 6889–6898.
Ausubel, F.M. (2013) Pseudomonas aeruginosa disrupts Caenorhabditis elegans Naylor, D. and Coleman-Derr, D. (2018) Drought stress and root-associated bacte-
iron homeostasis, causing a hypoxic response and death. Cell Host Microbe, 13, rial communities. Front. Plant Sci. 8, 2223.
406–416. Neef, A. and Sanz, Y. (2013) Future for probiotic science in functional food and die-
Klein, I., von Rad, U. and Durner, J. (2009) Homoserine lactones: do plants really tary supplement development. Curr. Opin. Clin. Nutr. Metab. Care, 16, 679–687.
listen to bacterial talk? Plant Signal. Behav. 4, 50–51. Ocana, V.S. and Elena Nader-Macias, M. (2004) Production of antimicrobial sub-
Kloepper, J.W. and Schroth, M.N. (1978) Plant growth-promoting rhizobacteria on stances by lactic acid bacteria II: screening bacteriocin-producing strains with pro-
radishes. In: Proceedings of the 4th International Conference on Plant Pathogenic biotic purposes and characterization of a Lactobacillus bacteriocin. Methods Mol.
Bacteria, Angers, pp. 879–882. Angers: Station de Pathologie Vegetale et Phyto- Biol. 268, 347–353.
bacteriologie, INRA. Olesen, J.E. and Bindi, M. (2002) Consequences of climate change for European
Kostakioti, M., Hadjifrangiskou, M. and Hultgren, S.J. (2013) Bacterial biofilms: agricultural productivity, land use and policy. Eur. J. Agron. 16, 239–262.
development, dispersal, and therapeutic strategies in the dawn of the postantibi- O’Toole, G.A. and Stewart, P.S. (2005) Biofilms strike back. Nat. Biotechnol. 23,
otic era. Cold Spring Harb. Perspect. Med. 3, a010306. doi: 10.1101/ 1378–1379.
cshperspect.a010306 Pal, K.K. and Gardener, B.M.G. (2006) Biological control of plant pathogens. Plant
Li, Z., Chang, S., Ye, S., Chen, M., Lin, L., Li, Y., Li, S. and An, Q. (2015) Differen- Health Instruct. 1–25. DOI:10.1094/PHI-A-2006-1117-02. 25 pp.
tiation of 1-aminocyclopropane-1-carboxylate (ACC) deaminase from its homologs Pandin, C., Le Coq, D., Canette, A., Aymerich, S. and Briandet, R. (2017) Should
is the key for identifying bacteria containing ACC deaminase. FEMS Microbiol. the biofilm mode of life be taken into consideration for microbial biocontrol
Ecol. 91, fiv112. agents? Microb. Biotechnol. 10, 719–734.

C 2 01 8 BSP P A ND J OH N W IL E Y & SO N S L TD M O L E CU L A R P L A NT P AT HO L O G Y (2 0 18 )
V
2358
10 Y. C. KIM AND A. J. ANDERSON

Pangesti, N., Pineda, A., Pieterse, C.M.J., Dicke, M. and van Loon, J.J.A. (2013) Schenk, S.T. and Schikora, A. (2015) AHL-priming functions via oxylipin and sali-
Two-way plant mediated interactions between root-associated microbes and cylic acid. Front. Plant Sci. 5, 784.
insects: from ecology to mechanisms. Front. Plant Sci. 4, 414. Schikora, A., Schenk, S.T. and Hartmann, A. (2016) Beneficial effects of bacteria–
Park, J.Y., Oh, S.A., Anderson, A.J., Neiswender, J., Kim, J.C. and Kim, Y.C. plant communication based on quorum sensing molecules of the N-acyl homoser-
(2011) Production of the antifungal compounds phenazine and pyrrolnitrin from ine lactone group. Plant Mol. Biol. 90, 605–612.
Pseudomonas chlororaphis O6 is differentially regulated by glucose. Lett. Appl. Scholz-Ahrens, K.E., Ade, P., Marten, B., Weber, P., Timm, W., Acil, Y.,
Microbiol. 52, 532–537. Glu€er, C.-C. and Schrezenmeir, J. (2007) Prebiotics, probiotics, and synbiotics
Park, J.Y., Yang, S.Y., Kim, Y.C., Kim, J.-C., Dang, Q.L., Kim, J.J. and Kim, I.S. affect mineral absorption, bone mineral content, and bone structure. J. Nutr. 137,
(2012) Antiviral peptide from Pseudomonas chlororaphis O6 against Tobacco 838s–846s.
Mosaic Virus (TMV). J. Kor. Soc. Appl. Biol. Chem. 55, 89–94. Schwarz, W.H. (2001) The cellulosome and cellulose degradation by anaerobic bac-
Park, J.Y., Kang, B.R., Ryu, C.M., Anderson, A.J. and Kim, Y.C. (2017) Polyamine teria. Appl. Microbiol. Biotechnol. 56, 634–649.
is a critical determinant of Pseudomonas chlororaphis O6 for GacS-dependent bac- Shafi, J., Tian, H. and Ji, M. (2017) Bacillus species as versatile weapons for plant
terial cell growth and biocontrol capacity. Mol. Plant Pathol. 19, 1257–1266. pathogens: a review. Biotechnol. Biotechnol. Equip. 31, 446–459.
Petrova, O.E. and Sauer, K. (2012) Sticky situations: key components that control Sharifi, R. and Ryu, C.M. (2016) Are bacterial volatile compounds poisonous odors
bacterial surface attachment. J. Bacteriol. 194, 2413–2425. to a fungal pathogen Botrytis cinerea, alarm signals to Arabidopsis seedlings for
Petrova, O.E. and Sauer, K. (2016) Escaping the biofilm in more than one way: eliciting induced resistance or both? Front. Microbiol. 7, 196.
desorption, detachment or dispersion. Curr. Opin. Mirobiol. 30, 67–78. Simons, M., Permentier, H.P., de Weger, L.A., Wijffelman, C.A. and
Picard, C. and Bosco, M. (2008) Genotypic and phenotypic diversity in populations of Lugtenberg, B.J.J. (1997) Amino acid synthesis is necessary for tomato root colo-
plant-probiotic Pseudomonas spp. colonizing roots. Naturwissenschaften, 95, 1–16. nization by Pseudomonas fluorescens strain WCS365. Mol. Plant–Microbe Interact.
Pieterse, C.M.J., Zamioudis, C., Berendsen, R.L., Weller, D.M., Van Wees, 10, 102–106.
S.C.M. and Bakker, P.A.H.M. (2014) Induced systemic resistance by beneficial Sonnleitner, E. and Haas, D. (2011) Small RNAs as regulators of primary and
microbes. Annu. Rev. Phytopathol. 52, 347–375. secondary metabolism in Pseudomonas species. Appl. Microbiol. Biotechnol. 91,
Planchamp, C., Glauser, G. and Mauch-Mani, B. (2014) Root inoculation with 63–79.
Pseudomonas putida KT2440 induces transcriptional and metabolic changes and Spencer, M., Ryu, C.-M., Yang, K.-Y., Kim, Y.C., Kloepper, J.W. and Anderson, A.J.
systemic resistance in maize plants. Front. Plant Sci. 5, 719. (2003) Induced defence in tobacco by Pseudomonas chlororaphis strain O6 involves
Poritsanos, N., Selin, C., Fernando, W.G.D., Nakkeeran, S. and de Kievit, T.R. at least the ethylene pathway. Physiol. Mol. Plant Pathol. 63, 27–34.
(2006) A GacS deficiency does not affect Pseudomonas chlororaphis PA23 fitness Stecher, B. (2015) The roles of inflammation, nutrient availability and the commen-
when growing on canola, in aged batch culture or as a biofilm. Can. J. Microbiol. sal microbiota in enteric pathogen infection. Microbiol. Spectr. 3(3), MBP-0008-
52, 1177–1188. 2014. doi: 10.1128 /microbiolspec.MBP-0008-2014.
Premachandra, D., Hudek, L. and Brau, L. (2016) Bacterial modes of action for Steinert, A., Radulovic, K. and Niess, J. (2016) Gastro-intestinal tract: the leading
enhancing of plant growth. J. Biotechnol. Biomat. 6, 236. role of mucosal immunity. Swiss Med. Wkly. 146, w14293.
Raaijmakers, J.M. and Mazzola, M. (2012) Diversity and natural functions of antibi- Tauzin, A.S. and Giardina, T. (2014) Sucrose and invertases, a part of the plant
otics produced by beneficial and plant pathogenic bacteria. Annu. Rev. Phytopa- defense response to the biotic stresses. Front. Plant Sci. 5, 293.
thol. 50, 403–424. Thomas, L.V., Suzuki, K. and Zhao, J. (2015) Probiotics: a proactive approach to
von Rad, U., Klein, I., Dobrev, P.I., Kottova, J., Zazimalova, E., Fekete, A., health. A symposium report. Br. J. Nutr. 114, S1–S15.
Hartmann, A., Schmitt-Kopplin, P. and Durner, J. (2008) Response of Arabi- Thorben, G., Andreas, V. and Gerrit, J. (2017) Probiotic Enterococcus mundtii iso-
dopsis thaliana to N-hexanoyl-DL-homoserine-lactone, a bacterial quorum sensing late protects the model insect Tribolium castaneum against Bacillus thuringiensis.
molecule produced in the rhizosphere. Planta, 229, 73–85. Front. Microbiol. 8, 1261.
Raskov, H., Burcharth, J., Pommergaard, H.C. and Rosenberg, J. (2016) Irritable Timmusk, S., Abd El-Daim, I.A., Copolovici, L., Tanilas, T., K€ annaste, A.,
bowel syndrome, the microbiota and the gut–brain axis. Gut Microbes, 7, Behers, L., Nevo, E., Seisenbaeva, G., Stenstro €m, E. and Niinemets, U. €
365–383. (2014) Drought-tolerance of wheat improved by rhizosphere bacteria from harsh
Reid, A. and Greene, S.E. (2012) How microbes can help feed the world. In: A environments: enhanced biomass production and reduced emissions of stress vola-
Report on a American Academy of Microbiology, p. 32. Washington, DC: American tiles. PLoS One, 9, e96086.
Society of Microbiology. Timmusk, S., Kim, S.-B., Nevo, E., Abd El Daim, I., Ek, B., Bergquist, J. and
Remminghorst, U. and Rehm, B.H.A. (2006) In vitro alginate polymerization and Behers, L. (2015) Sfp-type PPTase inactivation promotes bacterial biofilm forma-
the functional role of Alg8 in alginate production by Pseudomonas aeruginosa. tion and ability to enhance wheat drought tolerance. Front. Microbiol. 6, 387.
Appl. Environ. Microbiol. 72, 298–305. Timmusk, S., Behers, L., Muthoni, J., Muraya, A. and Aronsson, A.-C. (2017)
Reunanen, J., von Ossowski, I., Hendrickx, A.P.A., Palva, A. and de Vos, W.M. Perspectives and challenges of microbial application for crop improvement. Front.
(2012) Characterization of the SpaCBA pilus fibers in the probiotic Lactobacillus Plant Sci. 8, 49.
rhamnosus GG. Appl. Environ. Microbiol. 78, 2337–2344. Tomasi, N., De Nobili, M., Gottardi, S., Zanin, L., Mimmo, T., Varanini, Z.,
Rey, T. and Dumas, B. (2017) Plenty is no plague: Streptomyces symbiosis with Ro€mheld, V., Pinton, R. and Cesco, S. (2013) Physiological and molecular char-
crops. Trends Plant Sci. 22, 30–37. acterization of Fe acquisition by tomato plants from natural Fe complexes. Biol.
Ringø, E., Løvmo, L., Kristiansen, M., Bakken, Y., Salinas, I., Myklebust, R., Fert. Soils, 49, 187–200.
Olsen, R.E. and Mayhew, T.M. (2010) Lactic acid bacteria vs. pathogens in the Vacheron, J., Desbrosses, G., Bouffaud, M.-L., Touraine, B., Mo€ enne-Loccoz,
gastrointestinal tract of fish: a review. Aquaculture Res. 41, 451–467. Y., Muller, D., Legendre, L., Wisniewski-Dy e, F. and Prigent-Combaret, C.
Rivière, A., Selak, M., Lantin, D., Leroy, F. and De Vuyst, L. (2016) Bifidobacteria (2013) Plant growth-promoting rhizobacteria and root system functioning. Front.
and butyrate-producing colon bacteria: importance and strategies for their stimula- Plant Sci. 4, 356.
tion in the human gut. Front. Microbiol. 7, 979. Van der Ent, S., Van Wees, S.C.M. and Pieterse, C.M.J. (2009) Jasmonate signal-
Rolfe, R.D. (2000) The role of probiotic cultures in the control of gastrointestinal ing in plant interactions with resistance-inducing beneficial microbes. Phytochemis-
health. J. Nutr. 130, 396S–402S. try, 70, 1581–1588.
€mling, U. (2013) Microbiology: bacterial communities as capitalist economies.
Ro Van Hai, N., Buller, N. and Fotedar, R. (2009) The use of customised probiotics in
Nature, 497, 321–322. the cultivation of western king prawns (Penaeus latisulcatus Kishinouye, 1896).
Rosier, A., Bishnoi, U., Lakshmanan, V., Sherrier, D.J. and Bais, H.P. (2016) A Fish Shellfish Immunol. 27, 100–104.
perspective on inter-kingdom signaling in plant-beneficial microbe interactions. Vansuyt, G., Robin, A., Briat, J.-F., Curie, C. and Lemanceau, P. (2007) Iron
Plant Mol. Biol. 90, 537–548. acquisition from Fe-pyoverdine by Arabidopsis thaliana. Mol. Plant–Microbe Inter-
Ryder, C., Byrd, M. and Wozniak, D.J. (2007) Role of polysaccharides in Pseudomo- act. 20, 441–447.
nas aeruginosa biofilm development. Curr. Opin. Microbiol. 10, 644–648. Verbon, E.H. and Liberman, L.M. (2016) Beneficial microbes affect endogenous
Salas-Jara, M.J., Ilabaca, A., Vega, M. and Garcıa, A. (2016) Biofilm forming Lac- mechanisms controlling root development. Trends Plant Sci. 21, 218–229.
tobacillus: new challenges for the development of probiotics. Microorganisms, 4, Veselova, M.A., Klein, S.H., Bass, I.A., Lipasova, V.A., Metlitskaya, A.Z.,
35. Ovadis, M.I., Chernin, L.S. and Khmel, I.A. (2009) Quorum sensing systems of

MO L E CU L AR P L A N T P A TH OL O G Y ( 20 1 8) V
C 2 0 18 BSP P A N D JO HN W I L EY & SO NS L TD
Plant probiotics 11
2359

regulation, synthesis of phenazine antibiotics, and antifungal activity in rhizo- stress responses in wheat imposed by CuO nanoparticles. PLoS One, 11,
spheric bacterium Pseudomonas chlororaphis 449. Russ. J. Genet. 44, 1400. e0164635.
Viaene, T., Langendries, S., Beirinckx, S., Maes, M. and Goormachtig, S. (2016) Wrigley, D.M. (2004) Inhibition of Clostridium perfringens sporulation by Bacter-
Streptomyces as a plant’s best friend? FEMS Microbiol. Ecol. 92, fiw119. oides fragilis and short-chain fatty acids. Anaerobe, 10, 295–300.
Wang, D., Lee, S.H., Seeve, C., Yu, J.M., Pierson, L.S. 3rd. and Pierson, E.A. Yu, H. and Head, N.E. (2002) Persistent infections and immunity in cystic fibrosis.
(2013) Roles of the Gac-Rsm pathway in the regulation of phenazine biosynthesis Front. Biosci. 7, d442–d457.
in Pseudomonas chlororaphis 30–84. MicrobiologyOpen, 2, 505–524. Yu, S., Wei, Q., Zhao, T., Guo, Y. and Ma, L.Z. (2016) A survival strategy for
Wang, D., Yu, J.M., Dorosky, R.J., Pierson, L.S. III and Pierson, E.A. (2016) The Pseudomonas aeruginosa that uses exopolysaccharides to sequester and store
phenazine 2-hydroxy-phenazine-1-carboxylic acid promotes extracellular DNA iron to stimulate Psl-dependent biofilm formation. Appl. Environ. Microbiol. 82,
release and has broad transcriptomic consequences in Pseudomonas chlororaphis 6403–6413.
30–84. PLoS One, 11, e0148003. Zachow, C., Mu €ller, H., Tilcher, R., Donat, C. and Berg, G. (2013) Catch the best:
Wang, Y., Wilks, J.C., Danhorn, T., Ramos, I., Croal, L. and Newman, D.K. novel screening strategy to select stress protecting agents for crop plants. Agron,
(2011) Phenazine-1-carboxylic acid promotes bacterial biofilm development via fer- 3, 794–815.
rous iron acquisition. J. Bacteriol. 193, 3606–3617. Zamioudis, C., Mastranesti, P., Dhonukshe, P., Blilou, I. and Pieterse, C.M.
de Weert, S., Dekkers, L.C., Kuiper, I., Bloemberg, G.V. and Lugtenberg, B.J.J. (2013) Unraveling root developmental programs initiated by beneficial Pseudomo-
(2004) Generation of enhanced competitive root-tip-colonizing Pseudomonas bac- nas spp. bacteria. Plant Physiol. 162, 304–318.
teria through accelerated evolution. J. Bacteriol. 186, 3153–3159. Zhang, H., Kim, M.-S., Krishnamachari, V., Payton, P., Sun, Y., Grimson, M.,
Weller, D.M., Mavrodi, D.V., van Pelt, J.A., Pieterse, C.M., van Loon, L.C. and Farag, M., Ryu, C.-M., Allen, R., Melo, I.S. and Par e, P.W. (2007) Rhizobacte-
Bakker, P.A. (2012) Induced systemic resistance in Arabidopsis thaliana against rial volatile emissions regulate auxin homeostasis and cell expansion in Arabidop-
Pseudomonas syringae pv. tomato by 2,4-diacetylphloroglucinol-producing Pseu- sis. Planta, 226, 839.
domonas fluorescens. Phytopathology, 102, 403–412. Zhang, Z. and Pierson, L.S. 3rd. (2001) A second quorum-sensing system regulates
Wilks, M. (2007) Bacteria and early human development. Early Hum. Dev. 83, 165–170. cell surface properties but not phenazine antibiotic production in Pseudomonas
Winter, S.E. and Baumler, A.J. (2014) Dysbiosis in the inflamed intestine: chance aureofaciens. Appl. Environ. Microbiol. 67, 4305–4315.
favors the prepared microbe. Gut Microbes, 5, 71–73. Zhou, C., Ma, Z., Zhu, L., Xiao, X., Xie, Y., Zhu, J. and Wang, J. (2017) Rhizobac-
Wright, M., Adams, J., Yang, K., McManus, P., Jacobson, A., Gade, A., McLean, J., terial strain Bacillus megaterium BOFC15 induces cellular polyamine changes that
Britt, D. and Anderson, A. (2016) A root-colonizing Pseudomonad lessens improve plant growth and drought resistance. Int. J. Mol. Sci. 17, 976.

C 2 01 8 BSP P A ND J OH N W IL E Y & SO N S L TD M O L E CU L A R P L A NT P AT HO L O G Y (2 0 18 )
V