Microbial volatile compounds in plant health

Full text

Chapter 17
Microbial volatile compounds in plant
health
Rajinder Kaur, Ruth Gill, Gurleen Kaur and Sukhminderjit Kaur
Department of Biotechnology, Chandigarh University, Mohali, Punjab, India
17.1 Introduction
Secondary metabolites (SMs) are the auxiliary metabolites secreted by bacteria in the stationary growth phase. The pro-
duction of SMs starts during the nutritional shutdown when the key nutrients (carbon, nitrogen, and phosphorus source)
required for bacterial growth are exhausted and bacteria shift toward less-preferred nutrient sources leading to short growth
phase but efficient production phase (Barrios-González et al., 2017). These secondary products are not required for the
normal growth and reproduction of the bacteria, but they have been described for their potential applications in agriculture,
pharmaceutical, cosmetics, and food industry (Hussein and El-Anssary, 2019).
Majority of the soil-thriving bacteria are known to produce SMs. Antibiotics are among one of the most important SM
having medical importance. With the advancement in metabolomics, new SMs are being continuously discovered that have
applications in nonmedical fields (Clish, 2015). The term “suppressive soils,”explains the intriguing phenomenon of
inherent capacity of the soil to minimize the manifestations caused by pathogenic microorganisms to the susceptible plant
host, is also due to the ramification of microbial SMs. Although several abiotic factors also contribute to soil suppressive
nature, but the severity of the disease caused by a pathogen may decrease due to the production of SMs by the “plant
beneficial microorganisms”in rhizospheric soil. The rhizospheric soil hosts a heterogeneous group of microorganisms that
compete for nutrient availability and ecological niche to ensure their survival. The soil is also inhabited by plant pathogens
that can deteriorate plant health as well as by plant beneficial microorganisms which can enhance the plant health. The
beneficial microorganisms are collectively known as plant growthepromoting microorganisms (PGPMs). The PGPM
secretes SMs which are known for their roles in nutrient acquisition, cell to cell communication, plant growth regulation,
biocontrol, and symbiosis between microbes and plants (Hibbing et al., 2010;Demain et al., 2000). PGPMs can be broadly
categorized as biofertilizers (that help in nutrient acquisition), phytostimulators (phytohormone producing) or bio-
protectants, biopesticides, or biocontrol agents (those antagonizing plant pathogens). It is evident from literature reports
that one microorganism can have one or more of plant growthepromoting traits which are governed by their additive
effective (Ahemad et al., 2014). In the wake of blooming biofertilizer industry, it becomes important to study various
microbial SMs that can be exploited to develop commercial biostimulants for plant growth.
Here, in this chapter, we have discussed the different classes of volatile and water-soluble SMs and their role in
enhancing the plant growth through various mechanisms.
17.2 Regulation of secondary metabolites production in microbes and their
biosynthetic pathways
Factors such as nutrient exhaustion, osmotic stress, oxidative stress, and unfavorable growth conditions are major reasons
underlying the production of SMs. Among nutrients, carbon, nitrogen, and phosphorus are key factors that regulate the
production of SMs. During primary growth, the production of low molecular weight compounds, for example, butyr-
olactone, binds to the repressor proteins and prevents SM production (Ohnishi et al., 2005). However, the depletion of
nutrients such as glucose in the nutrient media stimulates the production of b-lactam antibiotic cephalosporin C,
The Chemical Dialogue Between Plants and Beneficial Microorganisms. https://doi.org/10.1016/B978-0-323-91734-6.00002-8
Copyright ©2023 Elsevier Inc. All rights reserved. 221

streptomycin, and many aminoglycoside antibiotics (streptomycin, kanamycin, istamycin, and neomycin) in Acremonium
chrysogenum (Ruiz et al., 2010). Ammonia, a common nitrogen source is another major underlying reason for the
repression of SMs such as penicillin, and cephalosporin C and gibberellic acid. In actinomycetes, antibiotic production
(erythromycin, rifamycin, actinomycin, spiramycin, and tylosins) is observed when the nutrient medium lacks nitrogen
source (Sanchez et al., 2002). Level of phosphate also controls the synthesis of antibiotics as seen in Streptomyces lividans
and Streptomyces coelicolor (Martín, 2004). Low phosphate concentration (less than 0.1 mM) favors SM production
(Tenconi et al., 2012), whereas the high phosphate concentrations (above 10 mM) lead to a decrease in SM production as
seen in antibiotic production by Streptomyces (Martín 1989).
At genomic level, different ribosomal and nonribosomal pathways have been elucidated for their role in SMs pro-
duction. Nutrient depletion and abiotic factors such as temperature, moisture, light, and pH affect the expression of arrays
of complex genes that are clustered together in the chromosome of bacteria and fungi (Fig. 17.1). The genes for different
SMs are present in a cassette known as biosynthetic gene clusters (BGCs). Nonribosomal peptide synthetases (NRPSs) and
polyketide synthases (PKSs) are two main classes of BGCs. NRPSs are responsible for the secretion of antimicrobial
peptides, siderophores, and bacteriocins, while PKSs are responsible for the production of polyketides and cyclic lip-
opeptides (CLPs) (Horak et al., 2019). Usually, one BCG is reported to be responsible for the production of one bioactive
compound or one or more SM with same bioactivity. One BGC is responsible for the production of one or several similar
compounds with bioactivities that usually only vary in terms of strength and/or specificity. However, it has been reported
that same BCG is responsible for the production of two metabolites with different bioactivity (Martinet et al., 2019).
17.3 Microbial secondary metabolites and their role in plant growth
Rhizobacteria secretes a large number of SMs, some of which are volatile in nature and water-soluble (Table 17.1). Volatile
compounds are low molecular weight compounds with low boiling point which can easily vaporize and diffuse through
soil pores over large distances. These metabolites are involved in intra and interspecific communication between cells and
FIGURE 17.1 Factors effecting microbial secondary metabolite production.
222 The Chemical Dialogue Between Plants and Beneficial Microorganisms

TABLE 17.1 Various secondary metabolites from different rhizobacteria.
S. No. Secondary metabolite
Rhizobacterial
species Target pathogen Target disease References
1. Oleonitrile, 3-Phenylpropanoic
Acid
Enterobacter tabaci Burkholderia glumae Bacterial panicle blight of rice Pen
˜aloza Atuesta
et al. (2020)
2. Glycolipids Pseudomonas aeru-
ginosa RTE4
Corticium invisium MCC 1841, Fusa-
rium solani MCC 1842
Tea dieback disease Chopra et al.
(2020)
3. Siderophores Bacillus species Colletotrichum gloeosporioides (78%)
and Fusarium oxysporum
Coffee wilt disease Kejela et al.
(2016)
4. Phenazine-1-carboxamide Pseudomonas aeru-
ginosa
P. chlororaphis
Fusarium oxysporum f. sp. radicis
lycopersici
Rhizoctonia solani
Tomato crown and root rot Shanmugaiah
et al. (2010)
5. Hydrogen cyanide (HCN) P. aeruginosa
P. fluorescens
Thielaviopsis basicola
Gaeumannomyces gramini var. tritici
Rhizoctonia saloni
Meloidogyne javanica
Black root rot, take-all disease of wheat,
collar rot, root knot
Jayaprakashvel
et al. (2010)
6. Bacillomycin D Bacillus vallismortis
ZZ185
Fusarium graminearum
Alternaria alternate
Rhizoctonia solani
Cryphonectria parasitica
Aspergillus flavus
Wilting, black rot, black spot, collar rot,
chestnut blight, kernel rot
Zhao et al.
(2010)
7. Iturin A Bacillus subtilis Colletotrichum gloeosporioides, B. cin-
erea, and R. solani
Anthracnose, gray mold rot, collar rot Kim et al. (2010)
8. Siderophore Pseudomonas spp.
Rhizobium meliloti
Verticillium, Pythium, Fusarium, Mac-
rophomina phaseolina
Damping-off, root rot, wilting, stem rot,
seedling blight
Idris et al. (2007)
9. Gluconic acid Pseudomonas strain
AN5
Gaeumannomyces gramini var. tritici Take-all disease of wheat Kaur et al. (2006)
10. Mycosubtilin B. subtilis BBG100 Pythium aphanidermatum Seed blight, rot Leclere et al.
(2005)
11. Xanthobaccin A Lysobacter sp. strain
SB-K88
Aphanomyces cochlioides Damping-off, root rot Islam et al.
(2005)
12. Bacillomycin, fengycin Bacillus amyloli-
quefaciens FZB42
Fusarium oxysporum Fusarium wilt Koumoutsi et al.
(2004)
13. Wuyiencin S. hygroscopiusvar
var. wuyiensis
Botrytis cinerea Gray mold rot Zhong et al.
(2004)
14. Volatile organic compound Pseudomonas spp.
Serratia spp.
Stenotrophomonas
spp.
Many soilborne fungal pathogens Stem rot, root rot, crown rot, vascular
wilts
Dwivedi and
Johri (2003)
Continued
Microbial volatile compounds in plant health Chapter | 17 223

TABLE 17.1 Various secondary metabolites from different rhizobacteria.dcont’d
S. No. Secondary metabolite
Rhizobacterial
species Target pathogen Target disease References
15. Viridepyronone T. viride Sclerotium rolfsii Southern blight Evidente et al.
(2003)
16. Herbicolin Pantoea agglomer-
ans C9-1
Erwinia amylovora Fire blight in apples and pears Sandra et al.
(2001)
17. Cyclic lipopeptides like viscosina-
mide, tensin, amphisin
P. fluorescens
Burkholderia
cepacian
Rhizoctonia solani Collar rot Thrane et al.
(2000)
18. Zwittermicin A14 B. thurigiensis
B. cepacian
Phytophthora medicagnis Root rot Silo-Suh et al.
(1998)
224 The Chemical Dialogue Between Plants and Beneficial Microorganisms

lead to cooperative and competitive behavior (Netzker et al., 2020). Some of these volatile compounds help the plants in
enhancing growth. Water-soluble SMs on the other hand are the polar compounds that can act over short distances only.
These compounds include a broad range of antibacterial and antifungal components, multidomain enzyme complexes, and
iron quenching siderophores.
17.3.1 Volatile compounds
As described earlier, rhizobacteria secrete plethora of numerous volatile compounds that can inhibit the growth of path-
ogenic fungi (Reetha et al., 2014) and even promote plant growth. Among these volatile compounds secreted by rhizo-
bacteria, hydrogen cyanide (HCN), aldehydes, alcohols, ketones, sulfides, terpenes, pyrazines, dimethyl sulfide (DMS),
dimethyl disulfide (DMDS), and dimethyl trisulfide (DMTS) are some important volatile compounds produced by
rhizobacteria.
17.3.1.1 Hydrogen cyanide
HCN is a microbial SM produced after the oxidation of glycine to HCN and carbon dioxide in the presence of electron
acceptors. HCN disrupts the protein functioning by binding to the essential elements such as divalent Cu
2þ
,Fe
2þ
,and
Mn
2þ
ions, inhibiting the electron transport chain. Suspension of electron transport chain cuts off the energy supply to
the bacterial cells, thereby causing death of living organism. Various soil-thriving gram-positive and gram-negative
bacteria belonging to the genre Bacillus,Streptomyces,Pseudomonas,Chromobacterium,Alcaligenes,Aeromonas,
and rhizobium are reported to produce HCN (Alemu, 2016;Anwar et al., 2016). In agriculture, HCN production is linked
to the suppression of various fungal diseases including color rot, damping off, charcoal rot, stem rot, root rot, and
seedling blight (Reetha et al., 2014). HCN producing rhizobacteria have potential role in suppressing growth of crown
gall disease causing Agrobacterium tumefaciens and affecting viability of root-knot nematode Meloidogyne incognita
(Abd El-Rahman et al., 2019).
17.3.1.2 Aldehydes, alcohols, ketones, and sulfides
Aldehydes, alcohols, ketones, and sulfides are antifungal volatile compounds, which are produced by many rhizobacteria.
Pseudomonas chlororaphis (PA23) isolated from soybean roots is known to produce aldehydes and ketones that can inhibit
the growth of Sclerotinia sclerotiorum. Cyclohexanol, benzothiazole, n-decanal, 2-ethyl 1-hexanol, and DMTS produced
by S. sclerotiorum have been reported efficient as antifungal agents. These compounds completely hinder the germination
of ascospores, mycelium, and the survival of sclerotia. Volatiles make direct contact with overwintering structures and
demolish the sclerotial bodies, which result in the depletion of potential inoculums and obstruct the development of disease
(Fernando et al., 2004). Compounds such as 2,3-butadienol have been reported for its role in increasing the growth of
Arabidopsis thaliana and hinder the growth of pathogenic bacteria like Erwinia carotovora (Ryu et al., 2003) and even
enhancing the survival of plant growthepromoting bacteria (Mackie and Wheatley, 1999).
17.3.1.3 Terpenes
Terpenes are made from the terpene-building units known as dimethylallyl pyrophosphate and isopentenyl pyrophosphate,
derived from the deoxy-xylulose phosphate pathway or from the mevalonate pathway (Dickschat, 2011). Initially reported
from plants, these compounds now have been described from fungal origin (Quin et al., 2014), prokaryotes (Yamada et al.,
2015), and also even by some social amebae (Chen et al., 2016). Terpenes from bacteria have been known from over a
century, but their ecological and biological functions are still not known. For example, the biological role of the prominent
terpene geosmin released by soil bacteria is still unexplored. Another metabolite known as albaflavenone from Strepto-
myces albidoflavus with antibacterial properties has been characterized (Gurtler et al., 1994). Streptomyces is surely the
foremost investigated genus responsible for terpene production; however, current research has reported that other taxa of
soil bacteria also produce terpene. The relative genomics study of six bacterial Collimonas strains disclosed that two
Collimonas pratensis strains produced terpene synthase genes. Heterologous expression and biochemical characterization
of Escherichia coli showed that these genes were responsible for the production of a mix of sesquiterpenes with ger-
macrene D-4-ol as a substantial compound (Song et al., 2015). Four monoterpenes (g-terpinene, a-pinene, b-myrcene, and
b-pinene) were discovered in the headspace of C. pratensis strain ter 91 with antimicrobial activity. The b-pinene revealed
inhibition against Staphylococcus aureus, Rhizoctonia solani, and additionally the mixture of all four monoterpenes
hindered the growth of E. coli (Song et al., 2015).
Microbial volatile compounds in plant health Chapter | 17 225

17.3.1.4 Pyrazines
Pyrazines are one of the most extensively studied nitrogen compounds produced by soil bacteria. Pyrazines or 1,4-
diazabenzenes are well known for their antimicrobial activities (Rajini et al., 2011). Pseudomonas,Bacillus,Chon-
dromyces (Dickschatetal.,2005), and Streptomyces (Brana et al., 2014) species have been known for the biosynthesis
of pyrazines. Vlassi and his colleagues (2020) tested Lysobacter capsici AZ78 for the production of mono- and
dialkylated methoxypyrazines. The results of their study highlighted the possible future implementation of pyrazine
derivatives in the control of soilborne plant diseases. Avocado-associated Pseudomonas, Bacillus, and Arthrobacter
promoted in vitro growth of A. thaliana probably due to the production of 2,3,5-trimethylpyrazine (Méndez-Bravo
et al., 2018).
17.3.1.5 Sulfur-containing volatiles
Volatile sulfur compounds and alkyl sulfides consist of large structural diversity ranging from small compounds like DMS,
DMDS, and DMTS to additional complex volatiles like 2-methyltetrahydrothiophen-3-one that are derived from homo-
cysteine in bacteria (Nawrath et al., 2010). Volatile microbial sulfur compounds perform a vital role in plantemicrobe and
interspecific microbeemicrobe interactions (Tyc et al., 2015). DMDS is recognized for its role in quorum-sensing-
inhibiting compound (Chernin et al., 2011) and triggering the bacterial growth and entirely hinder fungal growth (Garbeva
et al., 2014).
17.3.2 Nonvolatile metabolites
PGPR are also known to release many water-soluble metabolites. Polyketide nonvolatile antibiotics such as 2,4 diacetyl
phloroglucinol (DAPG), pyoluteorin, and mupirocin are considered to be effective antibiotics for the suppression of plant
pathogens (Fernando et al., 2005). Their role in combating plant pathogens is described below.
17.3.2.1 4 Diacetyl phloroglucinol
In the rhizosphere of crop plants, there is a pervasive presence of fluorescent Pseudomonads that secretes a broad
range of antimicrobial substances for the suppression of bacteria, fungi, and nematodes (Haas and Keel, 2003).
Consortia of different microbial metabolites work synergistically for the suppression of plant pathogens, but the effect
of antibiotics is considered to be the most vital factor in suppressing the pathogen. Among SMs produced by bacteria,
DAPG is the most important metabolite produced by the plants. It is a phenolic-based molecule produced by the
condensation of one molecule of malonyl coenzyme A and three molecules of acetyl coenzyme A to produce
monoacetyl-phloroglucinol, which is eventually transacetylated to produce phloroglucinol employing a CHS-type
enzyme. Biosynthetic locus for the synthesis of 2,4 DAPG is extremely conserved and contains a cassette that
contain six genes phlABCDEF. Glucose helps to increase the DAPG production in Pseudomonas fluorescens pf-5 and
CHA0, whereas sucrose and Fe
3þ
help to increase DAPG production in P. fluorescens F113. Also, it has been reported
that the Zn
2þ
,Cu
2þ
,andMo
2þ
are the micronutrients that help to trigger the DAPG production in P. fluorescens
CHA0 (Notz et al., 2002).
17.3.2.2 Pyoluteorin
It is a phenolic polyketide containing resorcinol ring. The resorcinol ring is attached to bichlorinate pyrrole moiety,
whereas the biosynthesis of pyrrole is not known. Pyoluteorin was initially isolated from Pseudomonas aeruginosa fol-
lowed by P. fluorescens Pf-5 and P. fluorescens CHA0 (Schnider et al., 1995). Pyoluteorin is known to have many
herbicidal, bactericidal, and fungicidal properties. The major property of pyoluteorin can be seen in cotton seeds where it is
helpful in suppressing the cotton damping-off (Vinay et al., 2016).
17.3.2.3 Mupirocin
P. fluorescens produce many SMs with antimicrobial activities. Among these, pseudomonic acid also known as mupirocin
is an important metabolite with potent bactericidal activity. Mupirocin shows extreme antibacterial activity against
Streptococci, Staphylococci, Neisseria gonorrheae,and Haemophilus influenza (Thomas et al., 2010). However, this
antibiotic shows less sensitivity against anaerobes and gram-positive Bacilli. Mupirocin consists of distinctive chemical
structure and comprise C9 saturated fatty acid (9-hydroxynonanoic acid) associated to monic acid A by an ester bond.
226 The Chemical Dialogue Between Plants and Beneficial Microorganisms

17.3.3 Heterocyclic nitrogenous compounds
Rhizobacteria secrete various extracellular heterocyclic nitrogenous compounds with antimicrobial properties. Some of
them are explained below.
17.3.3.1 Phenazine
Phenazine is a nitrogen-containing heterocyclic, low molecular weight SM secreted by bacteria species of genera Bur-
kholderia,Brevibacterium,Pseudomonas, and Streptomyces. Almost 50 natural phenazine compounds have been studied
and illustrated. Less number of strains of PGPR produces 10 types of phenazine derivatives. PCA, PCN, pyocyanin, and
hydroxyl phenazines are some prevalent identified derivatives of phenazine that are produced by Pseudomonas spp. PCN
and PCA are synthesized by P. fluorescens 2e79, P. chlororaphis (PCL1391), and Pseudomonas aureofaciens 30e84.
P. chlororaphis PA-23 produces PCN and PCA, which shows effectiveness in regulating Sclerotinia stem rot of canola.
Phenazine has a major role in managing the soilborne pathogens and has antifungal action. Nonmotile Tn5 mutants of
P. chlororaphis (PCL1391), which was produced by PCN (chlororaphin) was 1000-fold hindered in competitive tomato
root tip colonization in comparison with wild type that was against Fusarium oxysporum spp.
17.3.3.2 Pyrrolnitrin
Several fluorescent and nonfluorescent Pseudomonas produce chlorinated phenylpyrrole known as pyrrolnitrin. Initially,
isolated from Burkholderia pyrrocinia, now it has been obtained from several Pseudomonas species such as
P. chlororaphis,P. fluorescens,P. aureofaciens,Burkholderia cepacia,Enterobacter agglomerans,Myxococcus fulvus,
and Serratia spp. (Pawar et al., 2019). Earlier, pyrrolnitrin was used for the treatment of fungal skin infections. Thereafter,
it has been explored as agricultural fungicide. Pyrrolnitrin shows its effectiveness against Botrytis cinerea that cause
postharvest disease of pear, apple, and cut flowers. It also possesses impressive antifungal action against P. fluorescens and
R. solani strains that produce pyrrolnitrin minimized take-all disease of wheat. The strain PA-23 of P. chlororaphis showed
its efficacy in controlling Sclerotinia stem rot disease of canola in the field and greenhouse (Van Pee et al., 2000).
P. chlororaphis PA-23 is reported to have pyrrolnitrin and phenazime-1-carboxylic acid (PCA) production genes ho-
mologous to pyrrolnitrin genes of various Burkholderia spp. and P. fluorescens strains (Zhang and Fernanado, 2004a).
17.3.3.3 Cyclic lipopeptides
CLPs are secreted by both gram-positive and gram-negative bacteria. CLPs produced by fluorescent Pseudomonas spp.
consist of 9 or 11 amino acid peptide ring with C10 fatty acid at one of the amino acids. It is synthesized nonribosomally,
and its formation is catalyzed by large peptide synthetase complexes. CLP is endowed with antimicrobial and biosurfactant
(BS) properties. The different strains of P. fluorescens such as DR54, DSS73, and 96.578 secrete three different types of
CLPs, that is, viscosinamide, amphisin, and tensin, that showed potent antifungal activity against R. solani and Pythium
ultimum (Andersen et al., 2003). The production of CLPs endowed with BS and antifungal properties by sugar beete
associated P. fluorescens DR54 strains was studied by Nielsen and Sørensen (2003). Viscosinamide is also known to have
a vital role in cell proliferation and enhancing primary metabolism of rhizospheric strain P. fluorescens DR54 (Nielsen and
Sørensen, 2003).
17.3.4 Antifungal lipopeptide antibiotics
Broad spectrum of bioactive peptides is produced by Bacillus strains that include fengycin, lipopeptides, and iturins
compounds (mycosubtilins, iturins, and bacillomycins) that are amphiphillic membrane-active BSs and peptide antibiotics
with effective antimicrobial properties (Fernando et al., 2005).
17.3.4.1 Bacillomycin
Bacillus subtilis secretes sterol-phospholipid antifungal lipopeptide bacillomycin of family iturin. Bacillomycin Lc is a new
antifungal antibiotic of iturin class and is different from Bacillomycin L by sequence altering from aspartate-1 to asparaine-
1 and from glutamine-5 to glutamate-5. Simultaneously, Moyne et al. (2001) studied two peptide analogs of bacillomycin
D with extreme antifungal activity which showed antagonistic effects against Aspergillus flavus. Several different classes
of bacillomycin, bacillomycin L, bacillomycin Lc, bacillomycin F, bacillomycin D, and bacillopeptins have been isolated
from B. subtilis that are effectiveness against fungal pathogens.
Microbial volatile compounds in plant health Chapter | 17 227

17.3.4.2 Iturins
Various strains of B. subtilis produce CLPs that belong to iturin family. Iturin A is considered to be the powerful antifungal
agent of the family bacillomycin D, bacillomycin F, bacillomycin L, and mycosubtilins. Cyclolipopeptide iturin A con-
stitutes seven residues of alpha and only one residue of beta amino acid. It has strong antimicrobial action against
F. oxysporum, Macrophomina phaseolina,P. ultimum,R. solani,andS. sclerotiorum. Apart from iturin, some of bacterial
strains also produce bacillomycin L and bacilysin. According to the reports of Chitarra et al. (2003), it was explained that
B. subtilis YM10-20 secrete iturin that helps to permeabilize spores of fungi and helps in hindering the spore germination
of Penicillium roqueforti. Seven antifungal compounds were produced Bacillus amyloliquefaciens strain RC2 that
restricted the growth of mulberry anthracnose caused by Colletotrichum dematium. Iturin A2 hindered in vitro growth of
phytopathogenic fungi (Pyricularia oryzae and Rosellina necatrix) and bacteria (Xanthomonas campestris and
A. tumefaciens) recommending that the antibiotics produced by RC-2 has broad spectrum action against several plant
diseases. Also, B. subtilis produces Iturin D that helps to suppress Colletotrichum trifolii (Chitarra et al., 2003).
17.3.4.3 Surfactant-rhizospheric
Bacteria produce beneficial metabolite called as BS or green BS that have potential antifungal activity as well as weak
antibacterial activity. B. subtilis produce CLP surfactins with BS activity. Iturin and surfactin produced by B. subtilis RB14
showed potential activity against R. solani in tomato (Zohora et al., 2016). Bacillus spp. CY22 produces iturin, which
shows both antifungal activity and surfactin activity. P. aeruginosa RTE4 isolated from tea rhizosphere has shown potent
biofungicide potential due to BS production (Chopra et al., 2020).
17.3.4.4 Aminopolyols (zwittermicin A)
Bacillus sp. produces a novel bioactive molecule known as zwittermicin A. This antibiotic has several structural similarities
with polyketide and also owns broad spectrum of activity against several microbes. This is a rare antibiotic that works
against disease-causing oomycetes (Emmert et al., 2004). Bacillus cereus and Bacillus thuringiensis produce zwittermicin
A that effectively inhibited the growth of oomycetes and pathogenic fungi (Emmert et al., 2004).
17.4 Tools for detecting and studying secondary metabolites
The biological and ecological role of SMs is crucial to investigate the importance of microbial SMs in plant growth
promotion; therefore, it becomes crucial to study their biological and ecological role. The number of techniques can be
followed for the analysis of SMs produced by rhizobacterial species. The initial and vital step in the detection and
identification of SM produced by particular bacteria is culturing of the bacterial cells followed by its characterization. It is
important to maintain the culturing conditions such as temperature, nutrients, and oxygen level. The culturing can be done
on different complex media. Broths like Luria Bertani (LB), lysogeny broth, beef extract peptone broth, sucrose and tryptic
soy broth (TSB) and agar media like nutrient agar (NA), plate count agar, and MurashigeeSkoog medium are predominant
types of media used for the isolation of rhizobacterial species that synthesize SMs. Media like LB was employed by Liu
et al. (2020) for the isolation of plant growthepromoting rhizobacteria B. amyloliquefaciens. TSB and NA were used in the
study of Kumar et al. (2014) for the isolation of crucial rhizobacterial species.
Silica gel chromatographic technique is commonly used to purify the SMs from the crude extract (Kumar et al., 2014).
The supernatant is separated by thin layer chromatography (TLC), followed by high-performance liquid chromatography
technique. Ultraviolet (UV) detection is an important measure performed with diode array detector for the analysis of
compounds. The fractions obtained by TLC are directly injected in gas chromatography/electron-ionization-mass spec-
troscopy (GC/EI-MS) (Shifa et al., 2015). As this protocol does not confirm that only bacterial volatiles are expressed,
dynamic and static headspace systems are the favored experimental layout. Kai (2020) used GC/EI-MS in the study and
identified volatile SMs from B. subtilis in which majorly ketones, nitrogen-containing compounds, hydrocarbons, aromatic
compounds, and alcohols. Liquid chromatography-mass spectroscopy (LC-MS) is also a predominant analytical technique
for the identification of SMs. Iturins and fengycins were the major compounds identified in LC-MS (Liu et al., 2020). UV
spectroscopy, nuclear magnetic resonance spectroscopy, and fast atom bombardment mass spectroscopy techniques are
employed to do the detailing of structures of the pure compounds, which are recognized by using the former techniques.
High-resolution mass spectrophotometer data can be identified by using electron spray ionization. The study conducted by
Kumar et al. (2014) used all mentioned techniques and identified cyclo (D-Pro-D-Leu), cyclo (L-Pro-D-Met), cyclo (L-Pro-
D-Phe), cyclo (L-Pro-L-Val), 3,5-dihydrox-4-ethyl-trans-stilbene, and 3,5-dihydroxy-4-isopropylstilbene as major SMs.
228 The Chemical Dialogue Between Plants and Beneficial Microorganisms

Marfey’s method is commonly utilized to know the absolute configuration of compounds. In the study by Kumar et al.
(2014), all the compounds consist of both D and L amino acids in concern to absolute stereochemistry.
17.5 Enhancement of secondary metabolite production in rhizobacteria
Pathogen’s attack on plants triggers the plant to release phytohormones and various signaling molecules that induce de-
fense response in plants by activating induced systemic resistance (ISR). The rhizobacteria inhabiting rhizosphere of plants
produces SMs such as 3-hydroxy-2-butanone(acetoin) and 2,3-butanediol activate ISR in plants and control the disease
(Kloepper et al., 2004). Bacterial species such as Bacillus,Pseudomonas, and Serratia are known to produce an intense
ISR and decreased the rates of pathogen attack. In the recent times, number of researchers has put efforts to enhance the
antibiotic secretion and defense-related volatile compounds. This could be achieved by genetic manipulation of genetic
material of rhizobacteria and overexpression of gene-regulating secretion of broad-spectrum antifungal compounds (Kaur
et al., 2021). Acetoin is a crucial plant growthepromoting volatile compound that is secreted by strains B. subtilis, Bacillus
velezensis, and B. amyloliquefaciens IN9337a. The production of acetoin is crucial for the induction of defense pathway in
plants as the B. subtilis mutant strains like BSIP1173 and BSIP1174 failed to defend the plant against the infection
(Rudrappa et al., 2010). The higher amount of acetoin levels is connected with the induction of defense enzymes such as
peroxidase, polyphenol oxidase, and phenylalanine ammonia lyase. Chung et al. (2016) studied that B. velezensis is
provided with the natural capability to produce acetoin. Though, the concentration of acetoin is mainly lower than needed
functional levels. Peng et al. (2019) developed the knockout strains of B. velezensis by the deletion of bdh,gdh, and alsD
genes with the help of double crossover homologous recombination method. The similar growth pattern was observed in
the recombinant strain, and there was a remarkable increase in acetoin production in comparison to wild strain. A moderate
still effective immune response was obtained in plants in a priming state for activating defense response against pathogen.
Downregulation is achieved by gene manipulation techniques in which various genes involved in the production of
antimicrobial compounds and antibiotics that are extensively utilized as a modernistic perspective with regard to sus-
tainable methods of biotic stress tolerance. Certain Pseudomonas sp. such as P. fluorescens FD6, P. aeruginosa,Pseu-
domonas protegens CHA0, Pseudomonas brassicacearum LBM300, and Pseudomonas fuscovaginae produce
pyoluterorin (Plt), DAPG, pyochelin, hydrocyanic acid, PCA, and pyoverdine which are antimicrobial compounds consists
of antifungal properties (Huang et al., 2017). The deactivation of retS which is a sensory kinase downregulates the
synthesis of related antibiotics in P. fluorescens FD6. Jing et al. (2018) knockout genes of retS for the improvement of
antibiotics biosynthesis in bacterial strain P. protegens Pf-5. There was a increase in the production of DAPG of 20 to 30-
fold along with prominent activity against R. solani. In a similar way, P. protegens H78, a prominent PGPR producing
DAPG and Plt has been manipulated utilizing gene knockout strategies to increase the production of Plt y 14.3 times in
comparison to wild strain (Shi et al., 2019). PCA is one more crucial broad-spectrum antifungal compound observed to be
effective against Phytophthora capsici,R. solani AG1-IA, and F. oxysporum that act on rice, pepper, and tomato. This has
been reported that P. chlororaphis GP72 embraces the potential to produce commercial grade PCA from glycerol;
however, the measure of production is very low (Poblete-Castro et al., 2019). Solaiman et al. (2016) described that
metabolic usage of glycerol in P. chlororaphis NRRL B-30761 can be improve by the coexpression of genes glpF and
glpK concealing glycerol uptake facilitator and glycerol kinase. Similarly, Song et al. (2020) engineered P. chlororaphis
GP72 mutant by coexpressing genes glpF and glpK. The function of genes such as glpR gene and mgsA involved in the
utilization of glycerol has been established using knocked out studies. The PCA production after 36 h was enhanced to
9993.4 mg/L in mutant strain in comparison to 729.4 mg/L in wild strain.
17.6 Conclusion
Soil-thriving plant-associated bacteria have multifarious plant growthepromoting attributes due to the production of SM.
SM production is commonly linked to the enhanced antibacterial and antifungal activity that improves the plant health.
Advancements in the metabolomics techniques allowed better characterization of SMs. SMs from rhizobacteria can be
broadly classified as volatile compounds and water-soluble compounds. Volatile compounds include a broad range of
antibiotics and signaling molecules including HCN, aldehydes, alcohols, ketones, terpenes, and pyrazines that help in
enhancing plant growth. Water-soluble SMs on the other hand include a broad range of antibacterial and antifungal
components including polyketides, pyoluteorin, mupirocin, DAPG, and CLPs. Various literature reports advocate
abovementioned SMs as inevitable for good plant health. However, the amount of these SMs produced by rhizobacteria is
often very low that hinders the biocontrol process. Genetic engineering approaches can be used in future to enhance the SM
production in bacteria. Also, these approaches can be used to insert specific SM production gene in the bacteria in case if
Microbial volatile compounds in plant health Chapter | 17 229

the bacteria lack such genes. Future studies should focus more on the development of rhizobacteria strains with enhanced
production of SMs.
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