Fpls 09 00112

REVIEW
published: 09 February 2018

doi: 10.3389/fpls.2018.00112
The Chemistry of Plant–Microbe

Interactions in the Rhizosphere and
the Potential for Metabolomics to
Reveal Signaling Related to Defense
Priming and Induced Systemic
Resistance
Msizi I. Mhlongo 1 , Lizelle A. Piater 1 , Ntakadzeni E. Madala 1 , Nico Labuschagne 2 and
Ian A. Dubery 1*
Edited by:
Aurelio Ciancio, 1
Department of Biochemistry, University of Johannesburg, Johannesburg, South Africa, 2 Department of Plant and Soil
Consiglio Nazionale delle Ricerche Sciences, University of Pretoria, Pretoria, South Africa
(CNR), Italy
Reviewed by:
Robert David Hall, Plant roots communicate with microbes in a sophisticated manner through chemical
Wageningen University & Research, communication within the rhizosphere, thereby leading to biofilm formation of beneficial
Netherlands
microbes and, in the case of plant growth-promoting rhizomicrobes/-bacteria (PGPR),
Anton Hartmann,
Helmholtz Zentrum München – resulting in priming of defense, or induced resistance in the plant host. The knowledge
Deutsches Forschungszentrum für of plant–plant and plant–microbe interactions have been greatly extended over recent
Gesundheit und Umwelt, Germany
years; however, the chemical communication leading to priming is far from being
*Correspondence:
Ian A. Dubery well understood. Furthermore, linkage between below- and above-ground plant
idubery@uj.ac.za physiological processes adds to the complexity. In metabolomics studies, the main
aim is to profile and annotate all exo- and endo-metabolites in a biological system
Specialty section:
This article was submitted to that drive and participate in physiological processes. Recent advances in this field
Plant Microbe Interactions, has enabled researchers to analyze 100s of compounds in one sample over a short
a section of the journal
Frontiers in Plant Science
time period. Here, from a metabolomics viewpoint, we review the interactions within
Received: 02 October 2017
the rhizosphere and subsequent above-ground ‘signalomics’, and emphasize the
Accepted: 22 January 2018 contributions that mass spectrometric-based metabolomic approaches can bring to the
Published: 09 February 2018 study of plant-beneficial – and priming events.
Citation:
Mhlongo MI, Piater LA, Madala NE, Keywords: chemical communication, induced resistance, metabolites, metabolomics, plant–microbe
Labuschagne N and Dubery IA interactions, priming, signalomics
(2018) The Chemistry
of Plant–Microbe Interactions
Abbreviations: ABA, Abscisic acid; AHL, N-acyl-homoserine lactone; ET, Ethylene; ETI, Effector-triggered immunity;
in the Rhizosphere and the Potential
GC-MS, Gas chromatography mass spectrometry; ISR, Induced systemic resistance; JA, Jasmonic acid; LC-MS, Liquid
for Metabolomics to Reveal Signaling
chromatography mass spectrometry; MAMP, Microbe-associated molecular pattern; MeJA, Methyl jasmonic acid; MeSA,
Related to Defense Priming Methyl salicylic acid; MTI, MAMP-triggered immunity; LP, Lipopeptide; PGPR, Plant growth-promoting rhizo-microbes/-
and Induced Systemic Resistance. bacteria; PRR, Plant pattern recognition receptors; QqQ, Triple quadrupole; QS, Quorum sensing; qTOF, Quadrupole
Front. Plant Sci. 9:112. time-of-flight; RMPP, Rhizomicrobe-induced plant priming; SA, Salicylic acid; TOF, Time-of-flight; UHPLC-MS, Ultra-high
doi: 10.3389/fpls.2018.00112 performance liquid chromatography coupled to mass spectrometry; VOC, Volatile organic compound.
Frontiers in Plant Science | www.frontiersin.org 1 February 2018 | Volume 9 | Article 112

Mhlongo et al. Signalomics in Defense Priming
INTRODUCTION: SUSTAINABLE features, but differ in the intensity or amplitude of the host
PRODUCTION OF FOOD PLANTS responses (Zipfel, 2008; Zhang and Zhou, 2010; Dempsey and
Klessig, 2012). Damage-associated molecular patterns (DAMPs)
The world is facing a concerning challenge to produce sufficient are molecules arising from necrotic, damaged or stressed cells,
food in a sustainable manner, with an increasing global e.g., cutin monomers, small peptides, and cell wall fragments.
population and decreasing food resources. Food plant production Plants recognize these molecules in a similar manner as MAMPs
is hampered by a plethora of biotic stresses such as pathogens and respond by activating defense signaling cascades (Herman
and herbivores (Iriti and Faoro, 2009; Gust et al., 2010; Thakur et al., 2008; Yamaguchi et al., 2010; Liu et al., 2013; De Coninck
and Sohal, 2013). To defend themselves, plants rely on innate et al., 2015). These plant defense responses are strictly regulated
immunity of which the success in fighting disease infections in order to minimize resource expenditure and fine-tune the
or herbivore feeding depends on how rapid and strong an signaling cascades. This crucial role is fulfilled by phytohormones
activated immune can be deployed. To combat plant diseases like SA, JA, and ET as essential signaling molecules (Bartoli et al.,
and limit the use of pesticides and herbivore agrochemicals, 2013) for both local and systemic responses. It is important to
genetic modification has been used (Bhandari, 2014). However, note that this basic signaling defense is more complex because
the use of such strategies has caused major debates citing of other phytohormones including ABA, auxins, cytokinins,
environmental – (Aktar et al., 2009; Bhandari, 2014) and gibberellins, and brassinosteroids (BRs) that interplay in the
consumer concerns (Ferreira et al., 2012); hence, the need for background. Recently, even more plant signaling molecules such
new eco-friendly strategies. In the context of plant protection, as azelaic acid (AZA), pipecolic acid (PIP), and strigolactones
priming refers to a stimulus or treatment for improved responses have been reported (Pieterse et al., 2009; Denancé et al., 2013;
to upcoming environmental challenges. Colonization of plant Vos et al., 2013). In order to establish an effective symbiotic
roots by beneficial microbes in the rhizosphere is such a stimulus relationship between plants and PGPR, these preformed barriers
since it may result in ISR which have a positive effect on the ability and innate immunity defenses have to be bypassed through
of the plant to defend itself against attack by pathogens infecting chemical communication between plant and microbe (Figure 1).
the leaves (Hilker et al., 2015). Here, we highlight chemical Recent findings indicate that symbionts and pathogens deploy
communication in the rhizosphere (plant roots interacting with similar molecular strategies to dampen and overcome immune
plant-beneficial rhizobacteria and – fungi) and ISR or RMPP as responses, and that the MAMP/PRR recognition system is also
an environmentally friendly method to combat pathogens and engaged in cooperative plant-microbe interactions with beneficial
herbivores, as investigated through the use of LC coupled to microbial communities that can lead to root colonization.
MS-based metabolomics. This suggests a multifaceted management role by microbial
communities of the innate immune system for controlled
accommodation of beneficial microbes vs. pathogen elimination
(Hacquard et al., 2017).
PRE-FORMED BARRIERS AND PLANT
IMMUNE RESPONSES: POTENTIAL
OBSTACLES FOR INTERACTIONS WITH CHEMICAL COMMUNICATION WITHIN
RHIZOMICROBES THE RHIZOSPHERE
Plants use preformed defense mechanisms aimed at preventing The rhizosphere is one of the most complex ecosystems on
both pathogen entrance and herbivore feeding (Figure 1). earth and is inhabited by various organisms including nematodes,
Failure hereof, either below- or above-ground (De Coninck et al., fungi, bacteria, and arthropod herbivores (Venturi and Keel,
2015), leads to plant activation of an immune response termed 2016). Compared to bulk soil, the rhizosphere is associated
microbe/pathogen-associated molecular pattern (MAMP)- with increased bacterial abundance and activity, but lower
triggered immunity (MTI) which relies on the detection diversity. Plants are known to effect a selective pressure on the
of conserved microbial signature molecules (MAMPs) via microbial community found in the rhizosphere and community-
extracellular transmembrane receptors or PRRs (Jones and level analysis have revealed differential microbial communities
Dangl, 2006; Conrath et al., 2009; Sanabria et al., 2009; Deslandes associated with different plant species. This suggests a definite
and Rivas, 2012; Denancé et al., 2013; Gao et al., 2013). Some role of plant-derived metabolites in the microbiome assemblage
pathogens are capable of down-regulating MTI by the secretion in the rhizosphere (Hacquard et al., 2017; Yang et al., 2017;
of effector molecules, thereby leading to effector-triggered Zhang et al., 2017). The common PGPR genera in the rhizosphere
susceptibility (ETS). To overcome this, plant resistance (R) includes: Bacillus, Pseudomonas, Enterobacter, Acinetobacter,
proteins recognize these molecules and activate a second line of Burkholderia, Arthrobacter, and Paenibacillus (Finkel et al., 2017;
defense which is a rapid and robust response termed ETI (Pieterse Sasse et al., 2017; Zhang et al., 2017).
et al., 2009; Gao et al., 2013; De Coninck et al., 2015), and which Recent knowledge advancement in plant-beneficial microbe
is associated with the hypersensitive response (HR). The MTI interactions has led to the development and commercialization
and ETI sections of induced immunity are complementary, and of microbial inoculation (either one or a consortium) to improve
signaling interactions occur between MTI and ETI at very early plant health. These inoculants are natural or synthetic microbial
stages. Furthermore, MTI and ETI share many biochemical communities (Johns et al., 2016). This is done in one of the

FIGURE 1 | Overview of physical barriers (waxes, suberin, callose, lignin, etc.) and innate immunity defenses (MTI and ETI) that presents obstacles to potential
microorganisms in establishing a beneficial interaction with plant roots.
following ways: (1) introduction of new microbes into the soil, (2) that VOCs play a greater role in microbial communication than
manipulation of environmental factors (temperature, nutrients, the non-volatile counterparts. Rhizobacteria produce numerous
moisture level, etc.), and (3) growing plants that will influence the VOCs comprising alkanes, alkenes, alcohols, ketones, terpenoids
soil microbe community (Finkel et al., 2017; Pineda et al., 2017). and sulfur compounds. Furthermore, the metabolite complexity
These organisms interact with each other and with the plant of the volatile profiles is attributed to species – or genotype –
in a sophisticated manner, achieved by chemical communication specific metabolism (Kanchiswamy et al., 2015; Tyc et al., 2015;
established in the rhizosphere (Figure 2). In response to Kai et al., 2016).
altered gene expression, plants subsequently release an array Colonization of plant roots by PGPR involve QS, a
of metabolites (primary and secondary). It is through such cell-to-cell communication mechanism through the release
communication that mutual relationships are established that of signals to cognate receptors, thereby influencing gene
are vital for root–root interactions (Mommer et al., 2016), expression in correlation to bacterial population density
nutrient availability, microorganism accumulation, and biofilm (González and Marketon, 2003; Hong et al., 2012; Helman and
formation of soil microbial communities (Rosier et al., 2016; Chernin, 2015). These signals, also referred to as autoinducers,
Sasse et al., 2017), as well as inhibition of soil–borne pathogens allows both intra- and inter-bacterial communication between
(Bertin et al., 2003; Li et al., 2013). In this regard, metabolomic different species (González and Marketon, 2003; Hassan et al.,
approaches have enabled researchers to identify and quantify 2016).
compounds secreted by the microorganisms as well as profiling
the metabolite ‘blends’ present in root exudates that play a Bacteria-to-Plant Communication
vital role in this mutual interaction (Figure 3). The term To establish a symbiotic relation with plants, rhizobacteria
‘signalomics’ describes these metabolomics approaches employed either secrete or emit molecules beneficial to the plant. These
to decipher the chemical communications occurring within the molecules, originating from the rhizosphere, are able to trigger
rhizosphere. specific changes or adjustments to the plant transcriptome. While
phytohormones are growth – and defense regulators produced
Bacteria-to-Bacteria Communication by plants, PGPR are also able to produce these compounds
Soil bacteria present in the microbiome assemblages produce that include auxins, cytokinins, gibberellins, ABA, SA, and JA,
an array of signaling metabolites that affect gene expression among others (Figure 3) (Fahad et al., 2015). VOCs produced
within the host plants, and these compounds have become an by PGPR are involved in maintaining soil health, plant growth
important and interesting subject for researchers. Here, VOCs modulation and resistance induction (Wei-wei et al., 2008; Kai
are the well-documented signaling molecules within bacterial et al., 2009). Certain plants are responsive toward various known
communities (Figure 3). These are low-molecular weight VOCs produced by PGPR such as 2-heptanol, 2-endecanone,
lipophilic compounds synthesized from different metabolic and pentadecane. For example, co-cultivation of Arabidopsis
pathways and serve as a chemical window in which information is thaliana and two PGPR strains (Bacillus subtilis GB03 and
released (Kanchiswamy et al., 2015). Recently is has been shown B. amyloliquefaciens IN937a) in Petri dishes (allowing diffusion of

FIGURE 2 | Types of chemical-based interactions affecting plants. The plant host plus all its symbiotic microbes can be regarded as a community or an ecological
unit (holobiont). (1) Interactions between plant roots and beneficial bacteria within the rhizosphere, (2) competitive interactions between beneficial bacteria and
potential pathogens, (3) attack by potential pathogens on plant roots, (4) counter defense responses against pathogen attack, (5) communication between plants
roots and leaves, and (6) interplant communication through leaves (6a) and roots (6b).
bacterial volatiles from one side to another) resulted in enhanced of root exudates have a direct effect on the rhizosphere
growth of A. thaliana. Here, 3-hydroxy-2-butanone (acetoin) and communities and it has been shown that specific plant species
2,3 butanediol were the common VOCs between the two strains use these compounds to select soil microbe communities. For
(Ryu et al., 2003). example, citric acid identified from cucumber root exudates
Quorum sensing is a population density mechanism used attracted B. amyloliquefaciens SQR9 and cause biofilm formation.
by bacterial communities to communicate and sense their In addition, the banana root exudate fumaric acid attracted
environment. AHLs are the well documented QS signals B. subtilis N11 and stimulated biofilm formation (Zhang et al.,
frequently produced by Gram-negative bacteria (González and 2014). Studies have also shown that strain growth and antifungal
Marketon, 2003; Hassan et al., 2016). AHLs are perceived activity of certain Pseudomonas spp. is dependent on organic
by plants and contribute to the establishment of a bacterial– acids and sugars isolated from tomato root exudates (Kravchenko
plant symbiotic relationship (Schikora, 2016). UHPLC-MS et al., 2003).
(ultra-high performance liquid chromatography coupled to MS) Another class of compounds found in the root exudates
methodology as described in the Section “Metabolomics: A are flavonoids (i.e., 2 phenyl-1,4-benzopyrone derivatives)
Tool for Analysis of Plant Interactions with Rhizomicrobes” which induce bacterial nod genes, thus leading to lipo-
can precisely detect and quantify AHLs as well as the chitooligosaccharides (LCOs) that initiate nodule formation in
N-acyl homoserine degradation products, thereby enabling the roots. Interestingly, LCO also plays a role in interactions
the study of signaling dynamics in QS (Rothballer et al., between arbuscular mycorrhizal fungi and plants. Furthermore,
2018). these flavonoids are able to mimic bacterial QS molecules,
thus influencing bacterial metabolism (Hassan and Mathesius,
Plant-to-Bacteria Communication 2012). QS plays an important role in bacterial genotype and
The chemical complexity of root exudates is dependent on a phenotype regulation for successful root colonization (Rosier
number of external factors such photosynthesis activity, plant et al., 2016). Different types of low carbon molecules are also
size, and soil conditions. These secreted metabolites (Figure 3) present in the root exudates; these molecules serve as precursors
are species- or genotype-specific and can be differentially for biosynthesis of PGPR phytohormones. Tryptophan, which is
modified depending on the secreting source. Given this strong a precursor for indole-3-acetic acid, is concentrated in the root
complexity and specificity, root exudates have the potential tip region (Haichar et al., 2014). In addition, the ET precursor,
to overlay a much more detailed layer of information about aminocyclopropane-1-carboxylic acid (ACC), also exudes from
the communication events in the rhizosphere (Mommer et al., plants and can be used as a source of nitrogen and carbon by
2016; Sasse et al., 2017). Also, the chemical compositions PGPR (Haichar et al., 2012).

FIGURE 3 | Rhizosphere plant and microbial ‘signalomics’. Plants and rhizomicrobes secrete compounds beneficial to each other to establish mutual relationships.
This below–ground interaction, in turn, primes plants against various environmental stimuli that includes abiotic as well as biotic stresses. Perception of the priming
stimulus leads to activation of signaling molecules, primary metabolism regulation and gene activation of enzymes involved in the production of secondary defense
metabolites. When a secondary stimulus is detected the same process as in the priming stage takes place but at an enhanced level to minimize impact on the plant.
Plants are able to pass on the induced primed state to their progeny in a process known as trans-generational priming. In addition, plants communicate with each
other using allelopathic molecules. Abbreviations: volatile organic compounds (VOCs), quorum sensing molecules (QSM), N-acyl homoserine lactones (AHL), SA,
methylsalicylic acid (MeSA), methyljasmonic acid (MeJA) ET.
Plant-to-Plant Communication occur through common mycorrhizal networks between plants,

Communication between plants occurs below- and above- protecting them against degradation and enhancing plant-to-
ground (Figure 2), either through secretion/release of certain plant transmission. Beside rhizosphere signaling, plants do
signaling molecules (Mommer et al., 2016). Root exudates secrete their own VOCs into the air that are carried to
released into the rhizosphere contain a blend of signaling neighboring plants (Figure 3).
molecules that are transmitted to neighboring plants (Badri
and Vivanco, 2009). However, root–root interactions are mostly
studied in the context of species competition and invasive RHIZOSPHERE DEFENSE AND
plants. Allelopathy is the most prominent probability, in PRIME-INDUCING COMPOUNDS
which plants release phytotoxins such as catechin (a flavan-3-
ol flavonoid). This compound is able to mediate intraspecific Over the years, PGPR have been extensively studied for plant
and interspecific interactions, and to inhibit establishment and growth promotion and ISR induction, and are promising
growth of neighboring plants, thus reducing competition and alternatives to chemical fertilization, pesticides, and herbicides
increasing nutrient availability (Thorpe et al., 2009; Mommer (Kloepper et al., 2004; Gupta et al., 2015). PGPR effect beneficial
et al., 2016). Compounds with allelopathic effects belong to one properties through direct mechanisms (i.e., nitrogen fixation,
of the following chemical classes: benzene-derived compounds, mineral solubilization and biosynthesis of phytohormone and
phenolics, hydroxamic acids, and terpenes (Badri and Vivanco, siderophore production) and indirect mechanisms (production
2009; Massalha et al., 2017). On the other hand, VOCs are of antibiotics, hydrolytic enzymes, siderophores, LPs, and ISR)
the most studied allelochemicals in plant-plant interactions. (Beneduzi et al., 2012; Garcia-Fraile et al., 2015; Gupta et al.,
VOC-mediated signaling in the rhizosphere is believed to 2015). Here, we look at the major classes of molecules secreted

by PGPR that are involved in plant protection against soil-borne tomato when compared to a siderophore-deficient mutant of
pathogens and induction of ISR/RMPP. P. aeruginosa which lost its biocontrol ability. Furthermore,
Antibiotics and related molecules are secreted by certain B. subtilis-produced siderophores exhibit antagonistic effects
bacteria and have the ability to inhibit pathogen growth at low against wilt and dry root rot- causing fungi in chickpea (Patil
concentrations (Figure 3). Such compounds from Bacillus and et al., 2014). Also, purified siderophores had similar disease
Pseudomonas genera are the best studied in disease management suppression activity to those observed from the producing
(Haas and Défago, 2005; Saha et al., 2012). For example, 2,4 strains.
diacetylphloroglucinol (2,4 DAPG) is an antibiotic produced by Several reports have demonstrated that AHLs can influence
P. fluorescens that has a 75% inhibition effectiveness against plant physiological processes such as root elongation (Bai et al.,
the soil-borne pathogen Sclerotium rolfsii (Asadhi et al., 2013). 2012), plant perception (Han et al., 2016), and induce a broad
Phenazine-1-carboxylic acid (PCA) is another antimicrobial spectrum resistance (Schikora, 2016). Plant priming by AHLs
compound secreted by the same organism and causes oxidation- has recently been documented with reports that even commercial
reduction and accumulation of superoxides in target cells. available pure AHLs also induce priming in plants (Schenk et al.,
This molecule is effective against wheat disease caused by 2014). For examples, both short and long chain AHLs produced
Gaeumannomyces graminis var. tritici and S. rolfsii, causing by Serratia liquefaciens strain MG1 and P. putida strain IsoF
stem rot in groundnut (Lohitha et al., 2016). Another novel primed tomato plants against A. alternata via SA and ET defense
antibiotic from B. subtilis is zwittermicin which is effective pathway (Schuhegger et al., 2006). Also, in barley endophytic
against a spectrum of soil-borne pathogens (Saraf et al., 2014). Acidovorax radicis N35 rhizobacteria producing 3-hydroxy-
Several bacteria secrete hydrolytic enzymes, e.g., proteases, decanoyl-homoserine lactone induced defense responses and
glucanases, chitinases, lipases and amylases. These enzymes caused accumulation of flavonoids such as saponarin and
degrade numerous cell wall components of fungi and oomycetes lutonarin (Han et al., 2016).
(Bull et al., 2002; Saraf et al., 2005, 2014). Among the metabolites produced by PGPR, volatiles are small
Various PGPR such as Bacillus spp. and others, produce molecules that can effectively promote plant growth, induce
LPs (either linear or cyclic LPs) that act as antibiotics. These resistance and inhibit growth of pathogenic organisms (Ryu et al.,
are classified into three families: iritin, fengycin and surfactin 2004; Beneduzi et al., 2012; Song and Ryu, 2013). For example,
depending on the branching fatty acid (Saha et al., 2012; volatiles emitted by different rhizobacterial isolates were reported
Saraf et al., 2014), and have antagonistic effects against a to inhibit mycelial growth of Rhizoctonia solani (Kai et al., 2007).
wide range of soil-borne pathogens. Besides being antagonistic High vapor pressure volatiles are able to diffuse in the soil (Insam
to pathogens, LPs such as fengycin, surfactin and iturin and Seewald, 2010), which gives these compounds an advantage
are capable of inducing immune responses in plants by to act at distance. In vitro, volatiles from four Bacillus and
acting as bacterial determinants (Ongena et al., 2007; Romero Paenibacillus spp. showed intensive antagonistic activities against
et al., 2007). The role of these molecules in ISR/RMPP soil-borne pathogens including Ascochyta cutrillina, Alternarai
has been studied on various plants. In bean and tomato solani, and A. brassicae. From GC-head space analysis, four
both purified and compounds from producing strains were metabolites namely 2,4 decadienal, oleic acid, diethyl phthalate,
found to induce immune responses or prime plants (Ongena and n-hexadecanoic acid showed overlapping presence among
et al., 2007). B. subtilis S499 can prime cucumber plants the strains (Wei-wei et al., 2008).
against Colletotrichum lagenarium. However, plants treated Plants rapidly recognize both potential pathogens and
with semi-purified LPs were susceptible to C. lagenarium PGPR (Figure 1) in a similar manner based on MAMPs
(Ongena et al., 2005a). Recent studies on LPs involvement such as lipopolysaccharide (LPS) and flagellin, and secondary
in immune responses strongly show that these molecules are metabolites. MAMPs from beneficial microbes are known to
involved in ISR or RMPP. For example, cyclic LPs purified activate MTI, but in this case, the activated defenses do not
from B. amyloliquefaciens subsp. plantarum, isolated from the ward off the beneficial microbes (Van Wees et al., 2008). This
lettuce rhizosphere, primed plants against Rhizoctonia solani is not fully understood, but might involve the nature of the
(Chowdhury et al., 2015). complex chemical communication involved in rhizobacteria-
Siderophores are low molecular weight compounds plant interactions. As mentioned, PGPR produce plant signaling
synthesized by microorganisms under iron limiting conditions. molecules such as auxins, cytokinins, gibberellins, ABA, SA, ET,
With high membrane permeability, siderophores act as ferric ion and JA (Fahad et al., 2015). It is well known that SA, ET, and JA
transport vehicles into microbial cells (Butler and Theisen, 2010). cross-communicate to fine-tune the defense response, depending
The common iron-binding substances in these compounds on the detected stimulus (Dempsey and Klessig, 2012; Derksen
include hydroxamic acid, hydrocarboxylic acid, and catechols, et al., 2013). SA is an interesting signaling molecule produced by
as well as other related structures (Pattus and Abdallah, certain PGPR. For example, several Pseudomonas spp. produce
2000; Butler and Theisen, 2010; Ahmed and Holmström, SA under low iron conditions which is channeled toward
2014). Siderophore production is beneficial to plants (directly SA-containing siderophores (Mercado-Blanco and Bakker, 2007).
supply iron to plants) and is implicated in soil-borne disease However, SA produced by P. aeruginosa (siderophore producing
suppression (reducing competitiveness of soil-borne pathogens) mutant KMPCH) was shown to induce systemic resistance
(Tank et al., 2012). A mutant of P. putita over-expressing (Audenaert et al., 2002; Verhagen et al., 2010). Thus, both
siderophores was more effective against Fusarium wilt in MAMPs and SA are involved in RMPP.

In response to different stimuli, plants emit numerous competing for available nutrients, preventing contact between
VOCs with signaling and inhibitory properties. These within- the pathogen and the plant root, or by interfering with the
plant VOCs signaling leads to induction and priming of plant mechanisms leading to plant infection (Saraf et al., 2005,
defense (Heil and Silva Bueno, 2007). Among other volatiles 2014).
profiled in head-space experiments, MeSA, MeJA, and cis- The concept of plant priming dates back to 1901 when
jasmone (CJ) are well documented volatile signaling molecules Beauverie and Ray showed that plants infected by a pathogen
(Heil and Silva Bueno, 2007). These were found to induce developed an enhanced defense response against secondary
plant defense and priming against herbivore-feeding in wild infections. This lead to the realization that plants can be
lima beans. CJ has been tested on various plants and it has sensitized/primed to produce an enhanced defense response,
been shown to induce production of defense-related VOCs thereby making the plants more resistant to secondary
such as (E)-ocimene, 6-methyl-5-hepten-2-one and (E)-(1R,9S)- environmental stresses. While it is evident that plant defense can
caryophyllene (Pickett et al., 2007). Also, (Z)-3-hexen-1-ol was be induced and may lead to less resource expenditure (reduced
found to have a two-fold priming effect and modulation of fitness cost), the success depends on the appropriate activation
herbivorous insect behavior (Wei and Kang, 2011). Even though of defenses that can be faster, earlier, more sensitive, or stronger.
progress has been made in understanding the involvement of These timeous activation of suitable defense responses in primed
plant VOCs in signaling, attraction of predators and pathogen plants can save plants from becoming diseased or consumed,
inhibition, there is no knowledge on plant VOCs induced thus adding a benefit of off-set the cost of establishing the primed
in response to ISR/PGPR-priming by rhizomicrobes. However, condition (Conrath et al., 2009, 2015; Tanou et al., 2012; Hilker
metabolomic studies have shown that regardless of the perceived et al., 2015).
stimulus, similar metabolic pathways are activated (Pastor et al., Studies using PGPR have identified genes associated with
2014; Balmer et al., 2015; Mhlongo et al., 2016a,b). Thus, ISR/RMPP. For example, transcriptome analysis of P. fluorescens
such studies suggest that the blend of signaling VOCs is the WCS417r-ISR hosting plants showed systemic expression of
same/similar, leading to production of defense metabolites within defense genes when compared to the control, and P. syringae
the producing plant as well as in distal plants. infection led to identification of genes (mostly JA- and
ET-regulated genes) with more enhanced expression than
non-ISR expressing plants (Bakker et al., 2007; Van Wees et al.,
ISR/RHIZOMICROBE PLANT PRIMING 2008; Conrath et al., 2009; Segarra et al., 2009; Vacheron et al.,
(RMPP) 2013). Also, ISR/RMPP can be induced by PGPR volatiles
without the organisms being in contact with the roots. Bacillus
In the rhizosphere, a complex relationship exists among plants, spp. producing volatiles such as 3-hydroxy-2-butanone and
soil microbes, and soil (Van Dam and Bouwmeester, 2016). (2R,3R)-(-)-2,3-butanediol were found to prime Arabidopsis
The microbial diversity (population and activity) in this zone plants against pathogen infections and herbivore attack (Conrath
is influenced by physical, chemical and biological properties of et al., 2001; Farag et al., 2013; Song and Ryu, 2013; Yi et al.,
the root-associated soil (Barea et al., 2002). The rhizosphere 2013).
is inhabited by both deleterious and beneficial microbes Priming can also be a result of epigenetic changes from small
(Figure 2) that can significantly influence plant growth and interfering RNA (siRNA) or DNA recombination caused by
crop yield (Beneduzi et al., 2012; Vacheron et al., 2013; Garcia- environmental stresses (Bruce et al., 2007; Pastor et al., 2012).
Fraile et al., 2015). The beneficial microbes include symbiotic This form of protection is present in the genetic material of the
bacteria, free-living bacteria, actinomycetes, and mycorrhizal species and would last longer in plants compared to accumulation
fungi that increase nutrients/plant growth enhancer availability of metabolites. Since plants are not capable of communication
and suppress soil-borne pathogens (Garcia-Fraile et al., 2015). with their progeny, a mechanism is required to alert against
Diverse genera of PGPR dominated by Bacillus and Pseudomonas possible stresses that may be encountered in nature (Holeski et al.,
spp. have been identified, and are the most desirable beneficial 2012). It was not until the early 1980s when trans-generational
group for their variable qualities such as plant growth promotion, studies were conducted showing that inoculation of a plant
disease control and bioremediation. The mechanisms utilized by with a disease-causing agent induces resistance in their progeny
PGPR to suppress diseases and herbivores as well as priming not only to the administered agent, but to a wide spectrum of
of plants, have been critically studied and reviewed over the pathogens (Pieterse, 2012; Slaughter et al., 2012). In addition,
last few years (Saraf et al., 2005, 2014; Pineda et al., 2010; other studies showed that plants that have been infected by a
Beneduzi et al., 2012). PGPR may either directly (inhibition of pathogen produce seeds with higher levels of phytoalexins than
metabolism) or indirectly (through competition) reduce soil- controls. Epigenetic changes or trans-generational priming can
borne pathogen infections. Some PGPR such as Bacillus and be inherited by the progeny, where it then controls expression of
Pseudomonas spp. synthesize antibiotics that are active against defense genes (Holeski et al., 2012). In a study where Arabidopsis
various bacterial and fungal pathogens, toxins against insect plants were primed with β-aminobutyric acid (BABA) or by
pests, lytic enzymes that inhibit soil-borne pathogen growth, MAMPs from P. syringae, the progeny showed high levels of
and siderophores. Production of cyanogenic compounds have defense gene expression via the SA-dependent pathway and
also been shown to repel both root and leaf herbivores. Lastly, was resistant to P. syringae and Hyaloperonospora arabidopsidis.
PGPR present in the rhizosphere may prevent plant diseases by These progenies also had a stronger priming phenotype than

the parents. Trans-generational priming is achieved through responses are associated with minor fitness costs when compared
defense response memorization and propagation (in both meiosis to naïve plants. Thus, priming activation leads to temporal
and mitosis) by the parents (Luna et al., 2012; Pastor et al., down regulation of other metabolic pathways. Recently it has
2012; Slaughter et al., 2012; Po-Wen et al., 2013). However, been shown that both signaling molecules (Mhlongo et al.,
since there are many mechanisms associated with priming and 2017) and secondary metabolite conjugates accumulated during
research aiming at these are still underway, it is not clear the priming stage (Mhlongo et al., 2016a,b), and can be
how this memorization occurs. The involvement of chromatin converted to their active forms when a secondary stress is
modifications adds to the other metabolite-based mechanisms detected. Glycosylated signaling molecules, specifically that of
since it is directly linked to gene expression patterns that can be AZA, SA, and MeSA, were found to accumulate during LPS-
inherited by the offspring. induced priming of tobacco cells (Mhlongo et al., 2017). Also,
glycosylation of hydroxycinnamic acids was observed in tobacco
cells treated with both chemical and pathogen-derived priming
KEY METABOLIC EVENTS IN DEFENSE agents (Mhlongo et al., 2016a,b). Besides sugar conjugation,
PRIMING the respiratory cycle and tricarboxylic acid cycle (TCA) are
also affected by priming activation (Gamir et al., 2014). In this
The priming ability of PGPR is associated with cell wall regard, TCA intermediates (citrate, malate, 2-oxalate) were found
modification, expression of defense genes, primary metabolite to over-accumulate in BABA-induced priming. Furthermore,
modification and biosynthesis of secondary metabolites (Conrath amino acids serve as building blocks for many secondary
et al., 2009). As shown in Figure 3, priming can be divided in metabolites such as SA, polyamines, tyramine, alkaloids, and
to three major events: (1) perception of the priming stimulus, phenylpropanoids.
(2) secondary stimulus, and (3) trans-generational priming. The Secondary metabolites play an important role in plant
early stages of priming involve signaling by phytohormones and defense systems and environmental adaptation, and their
other signaling molecules. Phytohormones are well-documented presence fluctuates in response to different environmental stimuli
plant metabolites involved in different stages (Figure 3) of (Dörnenburg, 2004). As discussed above, PGPR are able to trigger
plant defense responses or plant priming (Dempsey and Klessig, secondary metabolism by means of different chemical molecules.
2012; Denancé et al., 2013). For example, JA and ET are major Many studies have shown that mycorrhizal or rhizobacterial
hormones in ISR/PGPR priming induction, while SA is the major root colonization quantitatively modify phenolic compounds,
hormone involved in systemic acquired resistance (SAR). Other alkaloids, terpenoids, and essential oils in plants (Toussaint et al.,
phytohormones such as cytokinins, auxins, ABA, gibberellins, 2007; Araim et al., 2009; Ramos-Solano et al., 2015). Using nine
and brassinosteroids are reported to play a role in plant resistance PGPR strains on blackberry plants, Ramos-Solano et al. (2015)
but the significance of these molecules is not well understood showed that phenolics, flavonoids, and anthocyanins were the
(De Vos et al., 2005; Koornneef and Pieterse, 2008; Pieterse et al., modified secondary metabolites associated with delayed post-
2009; Naseem and Dandekar, 2012; Denancé et al., 2013; Uhrig harvest fungal growth on berries. Other secondary metabolites
et al., 2013). These hormones interact either antagonistically such as coumarins and flavonoids also quantitatively changed
or synergistically with the SA-JA-ET signaling backbone and in plants associated with PGPR (van de Mortel et al., 2012). In
reprogram the defense output (Koornneef and Pieterse, 2008; maize significant changes in benzoxaninones were observed in
Verhage et al., 2010; Naseem and Dandekar, 2012). plants associated with mycorrhizal or rhizobacterial colonization
Using P. fluorescens as inducer, a total of 50 metabolites (Song et al., 2011). Also, maize root inoculation with P. putita
were differentially regulated in ISR-induced Arabidopsis plants. KT2440 induced metabolic changes and systemic resistance in
Amongst these, amino acids and sugars were the differentiated the plants. The early responses were via JA- and ABA-dependent
primary metabolites (van de Mortel et al., 2012). ISR/PGPR pathways, and phospholipids were highlighted as the important
priming studies are mostly based on molecular rather than metabolites in the KT2440 interaction. Lastly, benzoxaninones
metabolomics approaches. Hence, knowledge about metabolome were differentially abundant in roots after 3 days (Planchamp
changes during ISR/PGPR priming and the significance thereof, et al., 2014).
is limited. However, the metabolic events in priming in response Microbial compounds such as LPs and AHLs can also
to chemical elicitation are more similar, despite the use of prime plants through modification of secondary metabolites
different stimuli (Pastor et al., 2014; Balmer et al., 2015; Mhlongo (Ongena et al., 2005a; Schenk et al., 2014; Chowdhury et al.,
et al., 2016a,b). As such, metabolic studies employing other agents 2015; Han et al., 2016). LP-overproducing Bacillus activated the
may be used to explain the role of both primary and secondary lipoxygenase enzyme (LOX) regulated pathway (Blée, 2002). In
metabolites in plant priming (Djami-Tchatchou et al., 2017). potato tuber cells, fengycin treatments resulted in activation of
The main role of primary metabolism during plant defense phenylpropanoid pathway metabolism (Ongena et al., 2005b).
is to supply energy for the initiation of plant priming and Moreover, AHLs stimulated callose deposition and accumulation
in the synthesis/activation of phytohormones, phytoanticipins, phenolics, oxylipins and SA in several plant species (Schenk et al.,
and phytoalexins. Here, the energy referred to is required 2014; Schikora, 2016).
for different processes such as defense gene expression of Plants are capable of maintaining the primed state throughout
various defense pathways, plant metabolism regulation and their life cycle and passing it on to the next generation (trans-
resource re-channeling toward defense. As a result, plant priming generational priming) (Figure 3) (Luna et al., 2012; Pieterse,

2012; Munné-Bosch and Alegre, 2013; Mauch-Mani et al., with the surroundings (Rochfort, 2005; Lloyd et al., 2015;
2017). Epigenetic modification is the well-documented trans- Tenenboim and Brotman, 2016; Van Dam and Bouwmeester,
generational priming mechanism (Gamir et al., 2014; Mauch- 2016). Below we summarize the main events in an adaptable
Mani et al., 2017). The few reports available on metabolomics metabolomics workflow suitable for the study of plant–microbe
related to trans-generational priming suggest that phytohormone interactions and highlight some analytical advances (Figure 5).
levels are not modified in the progeny of primed plants (Luna
et al., 2012). However, Mandal et al. (2012) showed that progeny Sample Preparation
resistant to tobacco mosaic virus (TMV) had enhanced levels of The sample preparation method(s), to a large extent, determines
primary metabolites, particularly sucrose, glucose, and fructose the type of compounds to be detected. Sample preparation for
and the amino acids; ala, val, ser, thr, gln. Despite the lack any metabolomics study comprises several steps mostly dictated
of documented metabolomic work describing trans-generational by the chosen analytical platform. The main steps include
priming, Gamir et al. (2014) suggested that this process is highly material harvesting at a specific time and quenching to minimize
dependent on the characteristics of the pathogen. For example, metabolic turnover rates. Next, metabolite extraction with
biotrophic stimuli mainly impact primary metabolism while organic solvents or solid phase extraction is performed, taking
insects and necrotrophic fungi trigger secondary metabolism via the matrix in which the metabolites occur into account. This
JA/ET-dependent pathways. is followed by pre-analytical sample preparation (concentration,
purification or derivatization) (Tugizimana et al., 2013; Jorge
et al., 2016).
METABOLOMICS: A TOOL FOR
ANALYSIS OF PLANT INTERACTIONS Separation and Detection
WITH RHIZOMICROBES Gas chromatography, liquid chromatography (LC), and capillary
electrophoreses (CE) coupled to MS have developed into the
Metabolomics, an array of advanced bio-analytical techniques preferred bio-analytical platforms used in metabolomics (Naz,
in conjunction with chemometrics and bioinformatics tools, 2014). GC-MS is usually coupled to a quadrupole (Q), qTOF, and
enables characterization of the perturbations to the metabolomes QqQ mass analyzers. In recent years, TOF analyzer interest has
of interacting organisms (Tugizimana et al., 2013) (Figure 4). grown due to the ability to provide high mass accuracy, higher
As stated, the rhizosphere can contain a spectrum of different duty cycles and fast data acquisition in comparison to Q analyzers
microbial communities, constituting very complex chemical (Lei et al., 2011; Jorge et al., 2016). QqQ analyzers enable
environments. Metabolomics, as a data-driven, hypothesis- easy compound identification and quantification, and overcome
generating scientific approach with the aim to detect and quantify analyte co-elution due to the ability to perform multiple reaction
100s of compounds per analysis (Lloyd et al., 2015), is ideally monitoring (MRM) (Gomez-Gonzalez et al., 2010; Lei et al., 2011;
suited to the analysis of complex interactions and promises to Dzier et al., 2012). Recently, GC-MS analysis using stable isotope
facilitate the modeling of reciprocal responses between plants and probing (SIP) has enabled the elucidation of rate limiting steps in
organisms within the rhizosphere. metabolic pathways (You et al., 2014). The innovation of GCxGC,
Conceptually, and following a reductionist approach, the using two different stationary phases, provides high separation
tritrophic interaction between plant, rhizomicrobe, and pathogen efficiency and peak capacity, and the generated narrow peaks
can be studied separately and in isolation. For example, a require a fast scanning mass analyzer such as TOF or semi-fasts
co-culture metabolomics approach has been proposed (Allwood scan Q (Adahchour et al., 2005; Jin et al., 2015). One major
et al., 2010) to assess the intracellular metabolomes (metabolic setback of GC-MS is that it only analyses volatile and thermally
fingerprints) of both host and pathogen and their extruded stable compounds. To overcome this, derivatization (chemical
(extracellular) metabolites (metabolic footprints). However, in modification) of molecules with -OH, -COOH, -NH, and -SH
order to fully evaluate the changes occurring in the host functional groups by silylation reagents is employed (Villas-Bôas
plant due to these tritrophic interactions under conditions et al., 2011; Abbiss et al., 2015).
relevant to disease and resistance, there is a need for combining LC-MS column chemistry selection and retention mechanisms
the information provided by different techniques, including makes it the technique most used to complement GC-MS.
metagenomics and metametabolomics (Heinken and Thiele, Most LC-MS applications use reverse phase (RP) and normal
2015; Jorge et al., 2016; Ofaim et al., 2017). This novel approach phase (NP) stationary phases with eluates eluted with a mobile
to metabolomics analyses of host–pathogen interactions will phase mixture (e.g., organic solvents and water) (Haggarty and
facilitate a greater understanding of both their independent Burgess, 2017). Other column chemistries include hydrophilic
metabolism and the metabolic cross-talk which represents the interaction (HI), ion-exchange (IE), and porous graphitic carbon
interactome. (PGC) (West et al., 2010). Advances in column dimension and
Recent advances on both analytical instrumentation and – particle size (core-shell and monolithic) has enabled researchers
analysis with high selectivity, accuracy, and robustness, and to analyze a wide range of different analytes with high separation
combined with data processing software developments and efficiency at a high speed (Sanchez et al., 2013; Hayes et al.,
availability of public databases, have facilitated this endeavor. 2014; Preti, 2016; Urio and Masini, 2015). These column
Thus, these progressions have enabled researchers not only to developments lead to the expansion of ultra-high performance
study one aspect of a biological system, but also the interaction liquid chromatography (UHPLC). This chromatography format

FIGURE 4 | Background for metabolomics studies of signaling in the rhizosphere between plant hosts (left) and microorganisms within the rhizosphere (right). The
inter-organismal communication affects the biological information flow from genome to metabolome. The metabolome is complementary to the transcriptome and
proteome, captures the functional, or physiological state of the cell, and provides a communications link between genotype and phenotype. Metabolites also form
part of the regulatory systems in an integrated manner (solid lines indicating regulatory loops). Altered gene expression is ultimately reflected in changes in the
pattern and/or concentration of metabolites. It is through these interactions amongst the members of the central dogma components, that a cell acquires its full
functionality of its cellular metabolism.
is similar to HPLC except that it uses a column with particle primary metabolic pathways (glycolysis, tricarboxylic acid (TCA)
size ≤2 µm, small column diameter (1–1.2 mm) and operates cycle, and pentose phosphate pathway) and is usually coupled to
at high pressure (Sanchez et al., 2013; Fekete et al., 2014; Walter a TOF mass analyzer (Ramautar et al., 2015, 2016).
and Andrews, 2014). Electron spray ionization (ESI) is the most In recent years, MS imaging (MSI) has been advanced and
popular ionization method preferred in biochemical analysis. applied in different metabolic studies. MSI is a new imaging
This is because it is a soft ionization technique with little internal technique that provides the distribution of compounds on the
energy, thus allowing accurate mass determination. Alternatively, surface (cells, tissue, or specific sections). Here, a two or three
by increasing the collision energy, fragmentation can be obtained dimensional image is created by taking measurements across
leading to structural information (Hird et al., 2014; Madala an individual pixel basis (Wheatcraft et al., 2014; Heyman
et al., 2014; Ncube et al., 2014). Collision-induced dissociation and Dubery, 2016; Rao et al., 2016). Compared to other
(CID) with inert gases (He, Ar, or N2 ) is used to obtain more traditional molecular imaging techniques, MSI allows a greater
structural information and this is referred to as tandem MSn amount of information to be obtained by providing well-
experiments (Nizkorodov et al., 2011; Madala et al., 2014). resolved feature distribution for a wide range of metabolites
Tandem MSn instruments either perform tandem MSs in-time (Schwamborn, 2012). MSI techniques are divided into non-
[Ion Trap, Orbitrap, Fourier-transform-ion cyclotron resonance ambient and ambient approaches. Non-ambient approaches
MS (FT-ICR-MS) or in-space (qTOF and QqQ)]. In-time refers such as matrix assisted laser desorption ionization (MALDI)
to the ability to perform multiple stages of MS achieved by MS (Heyman and Dubery, 2016) and TOF secondary ion
allowing ions from the ion source into the ion trap followed by MS (TOF SIMS) have high sensitivity and spatial resolution
fragmentation to generate diagnostic information. On the other (Fletcher et al., 2013; Park et al., 2015). These approaches
hand, in-space refers to instruments with two mass analyzers are, however, time-consuming due to the extensive sample
separated by a collision cell which allows two MS stages (Hird preparation and may introduce errors (Park et al., 2015; Heyman
et al., 2014). and Dubery, 2016; Rao et al., 2016). On the other hand, ambient
CE separates compounds based on charge and size, and offers approaches (desorption electrospray ionization (DESI) MSI, laser
high resolving power. CE-MS is mainly used for intermediate ablation electrospray ionization (LAESI) MSI, air-flow-assisted

FIGURE 5 | Flowchart for plant metabolomic studies. The three main steps of a metabolomic analysis are sample preparation, data acquisition, and data mining.
These three steps are interrelated and lead to the discovery of signatory biomarkers, metabolite annotation, and biochemical interpretation.
desorption electrospray ionization (AFADESI)-MSI, and nano- The widely used chemometric methods are unsupervised
DESI MSI), requires less sample preparation and thus produce clustering [principal component analysis (PCA)] and supervised
images of a native state. However, this native state analysis comes [orthogonal projection to latent structures discriminant analysis
with low sensitivity and resolution compared to non-ambient (OPLS-DA)] (Trivedi and Iles, 2012; Worley and Powers, 2013).
approaches (He et al., 2015; Rao et al., 2016). Recently, single
cell analysis (SCA), also referred to as single cell MS (SCMS), Metabolite Annotation and Identification
has received more attention due to the ability to provide chemical Metabolite identification is the ultimate goal of any untargeted
composition of biological samples at cellular level. SCA uses non- metabolomics study. Over the years, databases incorporating
ambient, ambient and direct extraction (live single-cell video MS) mass spectra, compound names and structures, statistical models
approaches (Fujii et al., 2015; Onjiko et al., 2015; Rao et al., 2016). and metabolic pathways have been developed. Such databases
complement each other, however, a restricting factor is that
Data Analysis and Visualization the information is scattered and limited by the number of
Metabolomics generates large amounts of complex datasets identified metabolites (Fukushima and Kusano, 2013; Sakurai
that require both storage and data processing tools (reduction et al., 2013, 2014). Recently, a number of databases incorporating
of data complexity) (Okazaki and Saito, 2012; Berg et al., MS or nuclear magnetic resonance (NMR)-based metabolomics
2013; Tugizimana et al., 2014). This can be achieved by using and statistical tools have been developed, i.e., MeRy-B, MeltDB,
free statistical tools such as MarVis1, Mzine, XCMS, MAVEN, and SetupX (Ferry-Dumazet et al., 2011; Fukushima and
Metaboanalyst, MetAlign (Benton et al., 2008) as well as Kusano, 2013). Also, a number of integrated databases (e.g.,
commercial software such as Markerlynx (Waters), Profiling PlantMetabolomics.org) are also emerging (Bais et al., 2010).
solutions (Shimadzu), Mass profiler pro (Agilent) and Metabolic These include full annotation of metabolites, metabolic profiling
profiler (Bruker). Such tools focus on homogenous information and statistical tools. This indicates that integrated databases will
generation for further statistical analysis. Each calculated m/z facilitate metabolomic developments and advances in biological
ion is defined by the same variables that only correspond to systems.
it. Recently, Kuich et al. (2015) developed a software (Maui-
VIA) specifically for GC-MS data processing. The second step Metabolomics Data Storage and ‘Omics’
of data analysis involves the application of multivariate statistical Data Integration
tools to reduce data dimensionality, variables discrimination and Initiatives for metabolic data production, storage, dissemination,
to reveal shared features among samples (sample clustering). and analysis to encourage data sharing among researchers have

been attempted. MetaboLights is an open access database that phytopathogens. ISR/PGPR priming is a result of the complex
contains data, including meta- and raw data, from GC-MS and rhizosphere interaction between plant roots and PGPR, leading
LC-MS published metabolomics work (Steinbeck et al., 2012). to pre-conditioning of plants for an enhanced defense response
An integrative study is driven by two purposes: (1) gene against secondary stimuli. Most studies done on ISR/PGPR
function prediction, and (2) systemic interaction characterization priming are gene- or transcription-based with very few on
of biological systems (Rochfort, 2005; Fukushima et al., 2009; metabolomics. However, the limited studies available suggest
Fernie and Stitt, 2012). ‘-Omics’ analysis produces enormous that the early stages involve biosynthesis of signaling molecules
data sets describing cellular components, their interaction and followed by modulation of both primary - and secondary
state of biological networks. Thus, computational methods are metabolism. When secondary stimuli are subsequently perceived,
needed to reduce this dimension across the wide spectrum triggered events occur in an enhanced manner. These different
of ‘-omics’ data (Blazier and Papin, 2012; Conesa and Herna, physiological states (naïve, primed and primed and triggered) are
2014). Metabolic network construction is an advantageous reflected in changes to the metabolomes and can be investigated
platform for ‘-omics’ data integration. It is a manually curated, through targeted and untargeted metabolomics approaches.
computational framework that explains gene–protein reaction However, such studies generally focus on single organisms rather
relationships, assembled from annotated genomes, biochemical than studying the more complex system consisting of plant,
reactions, and cell phenotypes (Herrgård et al., 2006; Blazier and rhizomicrobes and pathogen. Through increased technological
Papin, 2012). Thus, to systematically investigate complex host– advances, both biologically and chemically, we are now better able
microbial interactions, a systems biology approach is required to study in detail the chemical changes which are associated with
that integrates high-throughput data and computational network microbe-plant interactions and the biochemical mechanisms
models. For example, Heinken and Thiele (2015) proposed a behind them. Metametabolomics, targeted at the phytobiome
constraint-based modeling and analysis approach, that enables would therefore be a future approach aimed at unraveling the
the prediction of mechanisms behind metabolic host-microbe complexity of chemical communication in the rhizosphere.
interactions on the molecular level.
AUTHOR CONTRIBUTIONS
CONCLUSION AND OUTLOOK Conceived and designed the research: MM and ID. Contributed
to the paper and revised it critically for important intellectual
Recent studies have highlighted the complexity of the content: MM, LP, NM, NL, and ID. All authors gave approval to
rhizosphere as an interlinked ecosystem consisting of different the final version.
microorganisms that can enhance plant growth through different
mechanisms. Chemical communication plays an important
role in establishing a mutual relationship between plant roots FUNDING
and PGPR. In addition, both plants and PGPR determine the
community of PGPR found in the rhizosphere. In attempts The research was partially funded by the South African National
to unravel rhizosphere signalomics, several metabolites, both Research Foundation (NRF) through grant support (number
primary and secondary, have been identified to be the major 95818) to ID.
messengers between plant roots and PGPR. Here, root exudates
and PGPR metabolites (non-volatile and volatile) play major
roles in establishing a mutual relationship. PGPR are also capable ACKNOWLEDGMENTS
of interfering with phytohormone-linked signaling to inhibit
or limit defense responses. PGPR do not only enhance plant The NRF and the University of Johannesburg are thanked for
growth, but also prime plants against infection by different fellowship support to MM.
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The Chemistry of Plant–Microbe

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