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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

Rhizosphere pseudomonads as probiotics improving plant health
1 2,
Department of Applied Biology, College of Agriculture and Life Sciences, Chonnam National University, Gwangju 61186, South Korea
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
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: 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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Plant probiotics 3

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
Liberman, 2016; Zamioudis et al., 2013).
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
to the host surface. Binding to a root surface probably involves
pili from the microbe’s surface (Chen et al., 2015; Wright et al.,
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
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
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