Plant Gene 18 (2019) 100175

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Plant Gene
journal homepage: www.elsevier.com/locate/plantgene

Unravelling the biochemistry and genetics of ACC deaminase-An enzyme T

alleviating the biotic and abiotic stress in plants
⁎
Shikha Gupta, Sangeeta Pandey
Amity Institute of Organic Agriculture, Amity University Uttar Pradesh, Sector 125, Noida, Uttar Pradesh 201313, India

A R T I C LE I N FO A B S T R A C T

Keywords: The enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase is known for alleviating the adverse effects of
ACC deaminase gene ethylene generated in response various stressors. Phylogenetic analysis of corresponding gene encoding ACC
Ethylene degrading enzyme (acds) reveals their occurrence in diverse group of bacteria and fungi. The transcription of
1-aminocyclopropane-1-carboxylate deaminase acds gene is tightly regulated and expresses differentially under different environmental conditions. Moreover,
Stress tolerance
ACC metabolizing enzyme is an inductive enzyme which expressed only in presence of its substrate, ACC. This
microbial enzyme has prominent role as cost-effective and eco-friendly adjuncts in sustainable agricultural
system because it catalysed the breakdown of immediate precursor of ethylene, i.e. ACC into α-ketobutyrate and
ammonia, and thereby declined the concentration of ethylene and its associated negative effects on growth and
development of plants growing under various biotic and abiotic stressful conditions. Therefore, the present
review attempts to summarizes the knowledge regarding biochemistry and genetics of ACC deaminase enzyme,
prevalence and regulation of corresponding ACC deaminase gene (acds) across different groups of microbes as
well as future research approaches to create transgenic crops containing microbial acds gene to withstand variety
of stressful conditions.

1. Introduction unfavorable environment without deteriorating the soil fertility and

The drastic and unpredictable climate change, as well as rising
population, poses the fundamental threat to the sustainability of global
agricultural production. In addition to these, soil abnormalities like
high salinity and acidity are also responsible for low agricultural pro-
ductivity. The conventional cultivation practices and development of
genetically modified transgenic crops cultivars are majorly exploited in
order to withstand adverse climatic conditions and non-conducive soil
environment. The usage of these techniques has undeniably contributed
to agricultural productivity but poses certain restriction with respect to
ethical standards, time consumption, and environmental risk. The
plant-microbe interaction either symbiotic (bacteria living inside the
root nodules) or endophytic (bacteria inside plant tissues) or rhizo-
spheric (bacteria binding to root surface) or phyllospheric (bacteria
binding on leaf or stem), plays a pivotal role in promoting sustainable
agriculture (Glick et al., 1995; Hallmann et al., 1997; Kozdrój and van
Elsas, 2000; Knief et al., 2011). They are economically feasible and
putative in comparison to inorganic chemical-based fertilizers, pesti-
cides, and insecticides. The best example of this bipartite association so
far documented is the application of rhizobacteria in the agricultural
field for improving plant growth and restoring their health under
natural resources. The plant growth promoting bacteria (PGPR) with 1-
aminocyclopropane-1-carboxylate (ACC) deaminase potential confer
resistance to various abiotic stress conditions such as high temperature,
flood, drought, salinity, and acidity by minimizing the level of stress
triggered ethylene inside the plants. PGPR either thrive in the vicinity
of plant's roots (rhizosphere) or aerial parts of the plant such as leaves
(phyllosphere), or inside the plant tissue (endophytes). PGPR with in-
trinsic activity of ACC deaminase has the potential to serve either as
growth stimulators by promoting synthesis of different plant growth
regulators (auxin, gibberellins, cytokinin and ethylene) or as bio-
fertilizers by solubilizing immobilized nutrients and making them ac-
cessible (zinc, potassium, phosphate, nitrogen) to plants or as biocon-
trol agents by secreting iron-chelating siderophores, hydrogen cyanide,
antibiotics, anti-fungal/cell-wall degrading metabolites and enhancing
induced systemic resistance in plants under harsh climatic conditions
(Glick et al., 2007). There are several studies which have reported the
beneficial influences of plant growth promoting microbes with the ACC
deaminase potential on plants growing under stressed conditions (Glick
et al., 2007; Li et al., 2013; Glick, 2014; Kang et al., 2013). Although in
the conducive environment, ethylene regulates various processes of
plant growth and development but during plant-soil borne pathogen

⁎
Corresponding author at: I 2block, AIOA Amity University Uttar Pradesh, Sector 125, Noida, Uttar Pradesh 201313, India.
E-mail address: sangeetamicro@gmail.com (S. Pandey).

https://doi.org/10.1016/j.plgene.2019.100175
Received 19 November 2018; Received in revised form 5 February 2019; Accepted 7 February 2019
Available online 07 February 2019
2352-4073/ © 2019 Elsevier B.V. All rights reserved.
S. Gupta, S. Pandey
Fig. 1. Significance of Ethylene in various aspects of plant growth and devel-
opment.
interaction or adverse climatic conditions sudden rise in ethylene
concentration was reported which has the deleterious effect such as
chlorosis, inhibition of plant growth and often leads to plant senes-
cence. In this context, rhizobacteria producing the enzyme ACC dea-
minase decrease the disproportionate amount of ethylene, by catalyzing
the breakdown of ACC, the immediate precursor of ethylene, into am-
monia and α-ketobutyrate, thereby plays the vital function in alle-
viating the harmful effects of stress factors and its associated ethylene
(Honma and Shimomura, 1978). Hence, the present review makes an
S-AdoMet
synthase
Methionine S-AdoMet
Modified methionine cycle
Fig. 2. Yang methionine pathway for Ethylene Biosynthesis.
2
Plant Gene 18 (2019) 100175
attempt to enhance the understanding of influence of ACC deaminase
on plant metabolic activities, mechanism of enzyme action, biochem-
istry and genetics of ACC deaminase, their role in the environment and
providing tolerance to plants against various abiotic stresses.
2. Ethylene and its biosynthesis
Ethylene is a natural phytohormone, gaseous in nature, consist of
two-carbon bond, facilitates various aspects of normal growth and de-
velopment of plant as illustrated in (Fig. 1).
Apart from these, it also hinders the roots elongation and nodula-
tion, accelerate the aging, senescence and abscission process in plants in
context to stress response (Glick et al., 2007; Tittabutr et al., 2015).
The ethylene biosynthesis mainly involves amino acid methionine,
converted to S-adenosylmethionine (S-AdoMet) (Poel and Straeten,
2014) by S-AdoMet synthase (EC 2.5.1.6) utilizing one molecule of
ATP. S-AdoMet then donates its methyl group in many cellular anabolic
pathways of macromolecules such as nucleic acids, proteins and lipids.
The overall ethylene production comprises 2 steps: - conversion of S-
adenosylmethionine (S-AdoMet) to 1-aminocyclopropane-1-carboxylic
acid (ACC) and 5- methylthioadenosine (MTA) catalysed by ACC syn-
thase (ACS, S-adenosyl-L-methionine methylthioadenosine-lyase,
EC4.4.14) (Yang and Hoffman, 1984). The 5- methylthioadenosine
(MTA) is then recycled back to methionine to replenish the cellular
concentration of methionine during high rates of ethylene synthesis
(Murr and Yang, 1975). The second step is the oxidation of 1-amino-
cyclopropane-1-carboxylic acid (ACC) to ethylene and cyanoformate
ion [NCCO2] - in the presence of oxygen as per the requirement of ACC
oxidase (ACO, EC 1.14.17.4). The cyanoformate ion so formed is con-
sequently dissociated into carbon dioxide and cyanide. The cyanide
then, subsequently metabolized to beta-cyanoalanine by beta-cyanoa-
lanine synthase (EC 4.4.1.9), playing an important role in assimilation
and detoxification of excess cyanide (Singh et al., 2015; Plett et al.,
Different environmental stressors,
inducers, developmental signals
ACC synthase
ACC
MTA
ACC oxidase
Ethylene Cyanide CO2
Detoxified to
Beta-
cyanoalanine
synthase
Beta-
cyanoalanine
S. Gupta, S. Pandey
2009) (Fig. 2).
The enzymes involved in ethylene biosynthesis i.e. ACC synthase
and ACC oxidase are well characterized with respect to structure and
function. ACC synthase is a cytoplasmic enzyme which requires pyr-
idoxal-5′-phosphate (Vitamin B6) as a cofactor for its function. The
corresponding gene encoding ACC synthase was first recognized in
zucchini and tomato plants (Poel and Straeten, 2014). The ACC oxidase
belongs to dioxygenases family require iron (Fe2+) as cofactor and bi-
carbonate (HCO3−) as an enzyme activator. The localization of ACC
oxidase in plants is not fully known. Some researchers reported it as
cytoplasmic enzyme while some suggested it membrane-bound enzyme.
Both the enzymes are multigenic, ACC synthase (encoded by 12 genes)
and ACC oxidase (encoded by 5 genes) in plants, controlled by different
environmental stimuli such as auxin, cytokine, brassinosteroids, ethy-
lene, pathogen attack and mechanical wounding which in turn regulate
the ethylene level in plant species (Wang et al., 2002; Barry et al., 1996;
Ravanbakhsh et al., 2018).
3. Signal transduction pathway of ethylene
Ethylene so synthesized is recognized by dimeric multipass trans-
membrane, endoplasmic reticulum-localized receptors with extra-
cellular copper-dependent ethylene binding domain and intracellular
histidine kinase domain. There are 5 members in the ethylene receptor
family named as ETR1, ETR2, ERS1, ERS2 and EIN4 which promote
negative regulation of ethylene signaling pathway. These hormone re-
ceptors during the absence of effector molecule, ethylene (active state)
stimulate Raf-like serine/threonine kinase, Constitutive triple re-
sponse1 (CTR1), associated with ubiquitylation and degradation of a
nuclear gene regulatory protein called EIN3, responsible for transcrip-
tion of ethylene responsive genes. Therefore, phosphorylation by CTR1
makes EIN2 inactive and eventually downstream signaling pathway for
ethylene biosynthesis is blocked (Wang et al., 2013).
On the other hand, the ethylene binding to its corresponding hor-
mone receptor inactivates and alters the conformation of receptors
which in turn cannot interact with CTR1. As a consequence, CTR1 be-
comes inactivated and eventually, EIN2 is no longer inhibited and de-
graded. The dephosphorylated EIN2 can stimulate the interaction be-
tween the transcription factors such as EIN3, Ethylene Insensitive Like
protein1 (EIL1) and EIN3-binding sequence (EBS) element in the pro-
moter region of various target genes or Ethylene Response Factors
(ERFs) genes and results in expression of ethylene-mediated stress tol-
erance and development response such as fruit ripening (Fig. 3) (Liu
et al., 2015a,b; Johnson and Ecker, 1998; Ravanbakhsh et al., 2018).
The rate of ethylene biosynthesis depends on several factors in-
cluding extreme temperature, light, gravity, nutrition, too much or too
little water, phytopathogenic (fungi, bacteria, viruses) damage or me-
chanical wounding. (Gamalero and Glick, 2015; Glick, 2014).
A paradigm was formulated (Glick et al., 2007; Pierik et al., 2006;
Glick, 2014) which described ethylene as stress hormone and also ex-
plained its formation with time (Fig. 4) when plants are subjected to
various environmental stressors.
According to this model, the first peak of small magnitude is formed
during the onset of stress which accounts for the lower production of
ethylene. This correlates with the limited amount of ACC pool initially
found in the plant tissues. The ethylene so produced in lower amounts
actuates the expression of genes responsible for defense mechanisms
and acquired resistance is developed in plants. Then, one or two days
after environmental stress, the second ethylene peak larger than first in
magnitude, is formed in response to increased expression of ACC syn-
thase gene and subsequently leads to ACC production. This large peak
regarded as “stress ethylene” confers the extensive damage to plants
such as inhibition of root development and consequently impairment of
nutrient uptake potential, prevention of root nodulation in legumes,
destruction of chlorophyll and its associated photosynthetic apparatus,
promotion of epinastic movements in aerial parts of plants, and also
3
Plant Gene 18 (2019) 100175
leads to senescence and abscission process in plants. So, the damage
occurs in plants is an aftermath of pleiotropic effects induced by stress
ethylene rather than the direct effects of stressful conditions (Glick,
2014; Ravanbakhsh et al., 2018).
Therefore, on the basis of such representation, many researchers
and agriculturist around the globe are suggesting to employ those
agents that can lower the ethylene levels (second deleterious ethylene
peak) induced by a variety of environmental stress and its associated
harmful pleiotropic effects. In this regard, ACC deaminase-mediated
deamination of the intermediate substrate of ethylene, ACC is an al-
ternative strategy to lower down the stress induced ethylene and its
associated tolerance. The soil microorganisms expressing ACC deami-
nase enzyme, a significant bacterial trait, support the growth and de-
velopment of plant under stressed conditions by optimizing ethylene
concentration so that it does not reach above the threshold level
(Fig. 5).
4. Enzymology of ACC deaminase
The 1-aminocyclopropane-1-carboxylate (ACC) deaminase (EC
3.5.99.7) is the pyridoxal 5′- phosphate (PLP) dependent, multimeric
(homodimeric or homotrimeric) enzyme of tryptophan synthase beta
superfamily responsible for deamination reaction of ACC, the pre-
decessor of gaseous phytohormone ethylene. The pyridoxal phosphate
(Vitamin B6) acts as a tightly bound cofactor required as 1 mol per
trimeric subunit for ACC deaminase enzyme activity (Singh et al.,
2015).
It has molecular mass 35–42 kDa is localized in cytoplasm of bac-
terial cells (Gamalero and Glick, 2015). It has been regarded as an in-
ducible enzyme which requires substrate, ACC at threshold level as low
as 100 nM in order to induce its activity. The induction of enzymatic
activity by substrate, ACC is validated by switching the nutrient-rich
growth media for ACC deaminase producing bacterial strains to
minimal media containing ACC as its sole nitrogen source. There are
other amino acids homologous to ACC such as L-Alanine, D-Alanine, D-
valine, 2-alkyl-ACC, vinyl-ACC and 2-aminoisobutyric acid, capable of
inducing ACC deaminase activity. Moreover, 2-aminoisobutyric acid
has the same potential as ACC to induce activity (Honma, 1983).
The enzymatic activity of ACC deaminase has been analyzed at
different pH but the maximum affinity for its substrate and competitive
inhibitors was found at pH 8.5–9.0. The enzymatic activity of ACC
deaminase is inhibited by L-amino acids or their derivatives (Honma,
1985).
The highest band of absorption spectra of ACC deaminase was ob-
served at wavelength 326 nm at pH 9.0 (Jacobson et al., 1994; Honma,
1985). The ACC deaminase activity of Pseudomonas putida strain
GR12–2 is found to be optimum at 30 °C (Glick et al., 1998).
The enzyme does not have high affinity for ACC which is reflected
by its Km value, ranges from 1.5 to approximately 17.4 mM at pH 8.5
(Honma, 1983; Hontzeas et al., 2004). The catalytic efficiency (kcat/km)
of the enzyme is approximately 690 M−1S−1 (Klee et al., 1991; Zhao
et al., 2003). The lower values of Km specified that ACC deaminase
should be present in higher amounts (100–1000 fold) to utilize ACC
substrate before ACC oxidase in order to reduce ethylene levels because
ACC oxidase has the greater affinity for ACC than that of ACC deami-
nase (Glick et al., 1998).
5. Mechanism of ACC deaminase enzymatic reaction
The microbial enzyme ACC deaminase hydrolyses stressed plant-
synthesized ACC to α-ketobutyrate and ammonia, ultimately reducing
the stress triggered ethylene and its associated growth inhibition under
environmental stress conditions. The main characteristic of ACC dea-
minase catalysed, second-order reaction is the cleavage of cyclopropane
ring by nucleophilic addition and elimination mechanism as shown
below (Fig. 6) unlike other PLP dependent enzyme catalysed reaction
S. Gupta, S. Pandey Plant Gene 18 (2019) 100175

i. ii.
Absence of Ethylene
Presence of Ethylene
Copper Ethylene
atoms

Inactive
Active
Receptors
Receptors

CTR1 Active State CTR1 Inactive

Active State
EIN2
EIN2 Degradation of
protein: Inactive
EIN2

Transcription of Ethylene
responsive genes: OFF ERF
Target
gene with
EBS
sequence
Ripening and
other
development

Fig. 3. Ethylene signal transduction pathway in the i. absence of ethylene; ii. Presence of ethylene and its impact on plant development.

S-ado-Met

ACC
synthase
Existing pool of
ACC
Increased level of
Ethylene

ACC ACC
oxidase
Stimulated
Ethylene (small by stress
of

and favourable) factors

Amount

Ethylene (large and

deleterious); Stress
ethylene; cause severe
Transcription of damage to plants
Pathogenesis related
and acquired
resistance genes

Time period of stress

Fig. 4. Ethylene formation in relative to time in plants when exposed to stressed conditions.

4
S. Gupta, S. Pandey Plant Gene 18 (2019) 100175

S-ado-Met

ACC
synthase
Existing pool of
ACC
Increased level of
ACC ACC
oxidase
Stimulated Soil
Ethylene

Ethylene (small by stress bacteria

and favourable) factors with ACC
deaminase
potential
of
Amount

Transcription of C4H6O3 + NH3

Pathogenesis related
and acquired
resistance genes

Time period of stress

Fig. 5. Ethylene formation with respect to time in plants inoculated with Plant growth promoting Rhizobacteria (PGPR) with ACC deaminase potential.

because there is an absence of alpha-hydrogen atom of ACC (Glick (Ose et al., 2003) (Fig. 8).
et al., 2007; Singh et al., 2015). The route 2 deviates from route 1 after external aldimine formation
Following are two proposed routes through which ACC deaminase where the nucleophilic attack is carried out by basic Lys(Joshi et al.,
carried out the deamination of its substrate ACC (Walsh et al., 1981; 2012) residue on proton of β-carbon of ACC (pro-S) followed by hy-
Zhao et al., 2003): drogen abstraction from the β-carbon of ACC (pro-R) resulting in the
formation of quinonoid. The further reaction steps after quinonoid
1. Direct β-hydrogen extraction- hydrogen atom is abstracted from formation are identical to that of route1 (Ose et al., 2003).
ACC substrate followed by Lys(Joshi et al., 2012) mediated hydro-
lytic reactions to cleave cyclopropane ring.
6. Molecular characterization of ACC deaminase enzyme
2. Nucleophilic addition followed by beta-hydrogen extraction- nu-
cleophilic attack of the β-carbon of ACC followed by Lys51mediated
The occurrence of ACC deaminase has been documented in all the
hydrogen abstraction to open cyclopropane ring.
three realm of cellular life- Eukarya, Bacteria, and Archaea. The first
existence of ACC deaminase enzyme was reported in bacterium
Initially, the internal aldimine (imine analog of aldehyde group) is
Pseudomonas sp strain ACP and yeast Hansenula saturnus (now re-clas-
formed between pyridoxal phosphate (PLP; cofactor) and ε-lysine re-
sified as Cyberlindnera saturnus). Thereafter, the evidence of ACC dea-
sidue of ACC deaminase enzyme. The α-amino group of ACC displaces
minase activity was found in the diverse range of bacteria, including
ε-lysine residue from the active site of enzyme resulting in the forma-
gram negative and gram positive and in some fungi colonizing different
tion of external aldimine via aminyl intermediate by the trans-aldimi-
ecological habitats such as human host, soil (rhizospheric), plant, water
nation reaction, which is common in both the proposed routes
etc. Among them, the ACC deaminase activity is extensively detected in
(Hontzeas et al., 2006) (Fig. 7).
the rhizospheric zone of soil, specifically rhizobacteria, conferring
In route 1, direct β- hydrogen removal of methylene proton is done
stress tolerance in plants by lowering the concentration of deleterious
by Lys(Joshi et al., 2012) basic residue on external aldimine to form
ethylene induced under stressful conditions (Timmusk et al., 2011;
quinonoid followed by subsequent electronic configuration and proto-
Honma and Shimomura, 1978; Gamalero and Glick, 2015; Singh et al.,
nation to form another molecule of quinonoid. The reaction proceeds
2015; Nascimento et al., 2013).
further by nucleophilic attack on quinonoid by basic lysine amino re-
The molecular characterization of bacterial ACC deaminase activity
sidue and resulted into another quinonoid and 2-aminobut-2-enoate
is done through amplification of corresponding 1000 bp acds gene se-
which in turn undergoes reversible hydrolysis to form final products as
quence located at chromosomal DNA by PCR (Polymerase chain reac-
2-oxobutanoate and ammonium ion and restoring internal aldimine
tion) using either a pair of universal primers (Hontzeas et al., 2005) or

Fig. 6. Enzymatic reaction of ACC deaminase, deaminating

substrate 1-aminocyclopropane-1-carboxylate (ACC).

5
S. Gupta, S. Pandey
Fig. 7. Common pathway of ACC deaminase-catalysed reaction via external aldimine formation by the trans-aldimination.
degenerate primers (Duan et al., 2009; Jha et al., 2012) designed by
various researchers.
In order to distinguish between ACC deaminase and other members
of tryptophan synthase enzyme family like D-cysteine desulfhydrase
enzyme (DCyD), several researchers analyzed their respective gene se-
quences acds and DcyD present in reference organism Pseudomonas sp.
UW4 and reported that some conserved amino acids are important for
ACC deaminase activity in the bacterium, for instance, Lys(Joshi et al.,
2012), required for hydrogen abstraction; Ser(Pierik et al., 2006), a
nucleophilic agent (Glick et al., 2007) and Tyr294,involved in the for-
mation of external aldimine (Ose et al., 2003) while residues Glu295 and
Leu322 are exclusively for recognition of substrate ACC (Glick et al.,
2007). The expression of acds gene is regulated by the availability of
oxygen, the concentration of substrate and resultant products (Singh
et al., 2015). The regulatory mechanism of acds gene varies with dif-
ferent species. However, Li and Glick (2001) has reported the com-
prehensive model of acds gene regulation in organism Pseudomonas
putida UW4.
The transcriptional machinery for acds gene expression consists of
many regulatory elements located upstream of acds such as acdR en-
coding LRP (leucine-responsive regulatory) protein; regulatory protein
such as LRP Box, AcdB Box; FNR box for fumarate-nitrate regulatory
protein and CRP box for binding cAMP receptor protein significant in
anaerobic and aerobic conditions, respectively (Fig. 9) (Singh et al.,
2015; Glick, 2014; Glick et al., 2007; Gamalero and Glick, 2015). The
regulatory protein LRP becomes active and forms LRP-octamer in the
presence of ACC and then activate another regulatory protein AcdB
resulting in the formation of glycerophosphoryl diester
Fig. 8. Elucidation of ROUTE1 (Direct β-hydrogen extraction) for ACC metabolism by ACC deaminase.
6
Plant Gene 18 (2019) 100175
phosphodiesterase which binds with ACC. Then this ternary complex
(LRP-ACC-AcdB) activates the expression of acds gene resulting in the
breakdown of ACC molecule into α-ketobutyrate and ammonia. This α-
ketobutyrate is further metabolized into leucine (branched chain amino
acid), which in turn binds to LRP octamer and dissociate it into inactive
dimers and switch off the transcription of acds gene. While during un-
availability of ACC, the transcription of acdR gene leads to the accu-
mulation of LRP protein and binds at promoter region of LRP Box,
negatively regulates its production by feedback inhibition. This in-
dicates that ACC deaminase is an inducible enzyme stimulates in in
response to substrate ACC only (Gontia et al., 2014).
This regulatory mechanism does not find in some bacterial species
such as Variovorax parrdoxus 5C2 and Achromobacter xylosoxidanis
A551. In some species such as Mesorhizobium loti the expression of acds
gene is regulated by nitrogen-fixing gene nifA2 and σ54 sigma factor. It
has been reported that ACC deaminase producing symbiotic bacteria
such as Mesorhizobium loti reduced the deleterious effects of ethylene on
root nodules, promote nodulation and subsequently nitrogen fixation in
leguminous plants under stressful conditions (Nukui et al., 2006).
In addition to this, there are some other regulatory elements located
downstream of acds gene found in many bacterial genera, for instance,
GntR protein-coding gene in Actinobacteria and Meiothermus positioned
next to acds gene, regulatory elements of LysR family also found in
certain species like Brenneria sp. EniD312, Burkholderia xenovorans
LB4000 and Pantoea sp. At-9B (Singh et al., 2015).
Hontzeas et al., 2005 has concluded lateral gene transfer of acds
gene by conducting comprehensive comparison between acds gene and
16 s rRNA conserved gene sequences from the same bacteria. In many
S. Gupta, S. Pandey
High levels of
LRP protein (inactive)
Feedback Inhibition of LRP
protein
Switch off transcription of acds
1
AcdR LRP AcdB
glycerophosphoryl diester
phosphodiesterase
Octamer of LRP
protein
ACC
AcdB+
ACC+LRP
Ternary complex
switch off
transcription
Fig. 9. The transcriptional machinery for the regulated expression of acds gene encoding ACC deaminase enzyme in the 1. Absence and, 2. Presence of ACC.
nitrogen-fixing species of Mesorhizobium sp. acds genes are horizontally
transferred between the strains by interchanging the nitrogen-fixing
gene cluster. Researchers also suggested that horizontal gene transfer
(HGT) is responsible for the presence of acds gene in fungi species and
different bacterial species (transfer of the gene between different do-
mains) (Prigent-Combaret et al., 2008). But Nascimento et al. (2013)
aligned multiple acds sequences from the wide range of bacterial cells
and suggested that vertical gene transfer mechanism might also be re-
sponsible for the same. Therefore, evolution of acds gene could be re-
sulted from vertical transmission of acds gene with intermittent hor-
izontal gene transfer. However, the exact picture of evolution and
phylogeny of acds gene is unclear (Singh et al., 2015; Li et al., 2015).
7. Plant growth promoting rhizobacteria with ACC deaminase
potential
The abiotic stress includes drought, flooding, salinity, heat, cold,
presence of heavy metals toxicants and nutrient deficiency which has
been reported to be more destructive in crop production worldwide. In
addition to these plants and crops also encounter many harmful bac-
teria, virus, fungal and pests attacks. In response to external stress en-
vironment, plants, being sessile, generates reactive oxygen species,
accumulates hormones such as ethylene, which further triggers sec-
ondary stress such as oxidative stress, nutrient deficiency, root curling
which collectively results in reduction in growth rate, metabolism,
development, productivity of crop growth and ultimately leads to plant
death (Premachandra et al., 2016).
Plant growth promoting bacteria are rhizospheric microbes (root-
colonizing bacteria), form an integral part of soil microbiota that
7
Plant Gene 18 (2019) 100175
FNR CRP acdS
Transcription
Is ON
- O2
ACC DEAMINASE
+ O2
ACC
AMMONIA
+
α-KETOBUTYRATE
Binds to the LRP octamer
L-LEUCINE
interacts with host plants and helps them in ameliorating the negative
impact of stress on their growth and development. Numerous bacteria
belonging to different taxonomic groups such as Agrobacterium,
Arthrobacter, Azotobacter, Azospirillum, bacillus, Burkholderia,
Caulobacter, Chromobacterium, Erwinia, Flavobacterium, Micrococcous,
Pseudomonas, Serratia have paramount significance in agriculture sector
as plant growth promoter. These bacteria promote growth and toler-
ance of plants under environmental stressors by employing two me-
chanisms, namely- direct and indirect (Ahemad and Kibret, 2014;
Bhattacharyya and Jha, 2012).
Among these, the potential of soil bacteria to produce ACC deami-
nase enzyme, significant trait that lowers the concentration of abiotic
stress-induced ethylene and subsequently its associated deleterious ef-
fects such as senescence, chlorosis, root curling, reduced shoot growth,
leaf abscission and ultimately plant death (Glick, 2014; Nascimento
et al., 2018). The ACC deaminase producing bacteria colonizing the
root zone of host plants serve as the sink for plant produced ACC (non-
ribosomal peptide) because when released as root secretion, bacterial
ACC deaminase cleaved it into α-ketobutyrate and ammonia, further
utilized by bacteria for their growth and energy. The ACC deaminase
activity has been reported in numerous species of plant growth pro-
moting bacteria like Agrobacterium genomovars and Azospirillum lipo-
ferum, Alcaligenes, Bacillus, Burkholderia, Enterobacter, Methylobacterium
fujisawaense, Pseudomonas, Ralstoniasolanacearum, Rhizobium, Rhodo-
coccus and Sinorhizobium meliloti and Variovoraxparadoxus.
There is one model-based description of the action mechanism
employed by ACC deaminase producing rhizobacteria (PGPR) for con-
ferring growth and tolerance in plant growth under stressed conditions.
Roots exudates rich in sugar, organic acids, amino acids, phenolics
S. Gupta, S. Pandey
and other small molecules are secreted to external soil environment
(rhizosphere). These nutrients are utilized as the source of energy by
rhizospheric bacteria for their growth and metabolism thereby in-
creasing their number and thus density in the rhizosphere. The amino
acids such as tryptophan are taken up by the associated rhizospheric
bacteria (~ 80%) and the synthesis of phytohormone indole-3-acetic
acid takes place. The newly synthesized IAA so produced by bacteria is
released outside and become available to the host plants. Both bacterial
IAA and plant synthesized natural auxin augments several develop-
mental aspects of plant-like root growth, vascular tissue differentiation,
auxiliary bud formation, apical dominance, and flower organ devel-
opment. It alters the root morphology promoting the formation of lat-
eral roots and adventitious roots that improve the water and nutrient
uptake efficiency of plants (Glick et al., 2007; Glick, 2012).
In addition to this, it also stimulates the production of mRNA
transcripts of ACC synthase (catalyze the formation of ACC from S-
AdoMet), indirectly induced the ethylene and triggered the stress re-
sponse. But the high production of ethylene promotes feedback in-
hibition of transcription of auxin response factors and thereby blocking
the IAA induced activation of ACC synthase transcription (Glick, 2014).
Moreover, some portion of the ACC also releases along with other
molecules either through root exudates or leaves which is then sub-
jected to dissociation to yield α-ketobutyrate and ammonia by the as-
sociated rhizospheric bacteria with ACC deaminase production poten-
tial and subsequently the levels of stress hormone ethylene and its
associated growth inhibition under abiotic stress could be regulated.
Therefore, plants root colonization with bacteria containing ACC dea-
minase improved root and shoot growth and enhanced the tolerance
against environmental stress condition (Glick et al., 1998) (Fig. 10).
8. Bacterial ACC deaminase conferring stress resilience in plants
It has been reported that plant growth promoting rhizobacteria,
specifically with ACC deaminase potential directly shield the plants
from detrimental impact of various abiotic (environmental) factors such
as drought, flooding, salinity etc. (Milosevic et al., 2012; Ma et al.,
2004) and also indirectly enhance protection against several soil borne
pathogens like bacteria, viruses, fungi, pests, insects and root nema-
todes (Dimkpa et al., 2009) (Table 1).
8.1. Water stress: drought and flooding
The stress related to moisture or water in the broader sense can be
defined as drought and flooding, poses serious threat among abiotic
stressors causing substantial loss of crops worldwide. Water deficit or
excess both resulted in several physiological and morphological al-
terations in plants which ultimately decreased the crop quality and
growth.
Under excess water conditions, soil and roots are fully submerged in
the water leading to hypoxic or sometime anoxic conditions, reducing
O2 availability to plants. The plants synthesize large amounts of enzyme
ACC synthase and subsequently, ACC concentration increased in roots.
Since anoxic conditions prevails in the root system, the conversion of
stress triggered ACC into ethylene could not take place due to inability
of ACC oxidase activity, therefore it is translocated to oxidative sur-
roundings of shoots system. This aggravated level of ethylene decreased
soil respiration, root growth, leaf area, leaf abscission, premature se-
nescence, wilting, epinasty (Salazar et al., 2015; Gu et al., 2007). The
application of rhizobacteria with ACC deaminase activity is a beneficial
way to lessen the adverse influence of induced ethylene and thus pro-
mote growth in waterlogging condition.
Drought primarily influenced water-plant potential, minimize sto-
matal conductance and subsequently lowers the chlorophyll content,
disrupt photosynthesis process and thereby loss of carbohydrates
(Vurukonda et al., 2015; Flexas et al., 2013). Various experiments were
carried out by researchers around the globe with a view to assess the
8
Plant Gene 18 (2019) 100175
beneficial role of ACC deaminase possessing bacteria on plant growth
and tolerance when subjected to water stress conditions.
8.2. Salinity
Salinity is also a severe problem which negatively affected the
agriculture production. It mainly increased the ionic concentration of
sodium salts in rhizosphere which results in nutrient deficiency, ion
toxicity (Na+ and Cl− ions), overproduction of free radicals, reduced
potassium as well as phosphorus availability for plants, stress ethylene
production, plasmolysis, inhibition of seed germination, reduces mi-
neral uptake, inhibit root nodulation and nitrogenase activity (Nadeem
et al., 2014) and disturbance in osmoregulation in plants
(Egamberdieva and Lugtenberg, 2014). The plant growth promoting
rhizobacteria yielding ACC deaminase activity improve the root de-
velopment as well as improve tolerance to cope up with high salt
conditions (Egamberdieva, 2013; Qin et al., 2014).
8.3. Heavy metal soil toxicity
The presence of toxicants such as cobalt, copper, iron, manganese,
molybdenum, nickel and zinc in trace amounts is recommended for the
normal plant development which otherwise become toxic and detri-
mental to plant when present beyond threshold limit. The excessive
concentration of inorganic toxicants in rhizosphere decrease the me-
tabolic activity enzymes in cytoplasm, trigger oxidative damage to
cellular structures, exchange with essential nutrient of plants thus de-
pleting soil nutrient reserve, reduce chlorophyll pigment and photo-
synthesis process, negatively affecting activities of certain beneficial
microorganisms associated with plants and thus reducing availability of
soil nutrients to plants (Chibuike and Obiora, 2014). The ACC deami-
nase producers accelerate the rate of roots proliferation which in turn
maximizes the metal uptake potential from surroundings and also,
lowers the amount of stress generated ethylene (Arshad et al., 2007).
Therefore, the introduction of PGPR with an ability to deaminate ni-
trogen source, ACC is a functional and cost-effective biological ap-
proach for soil remediation in ameliorating the negative impact of
metal toxicants in the rhizosphere (Glick, 2010; Govindasamy et al.,
2009; Bisht et al., 2014; Burd et al., 1998; Benson et al., 2017; Liu et al.,
2015a,b).
8.4. Phytopathogen attack
The plant fungal, bacterial pathogens, insects, pests, nematodes and
their associated diseases, major biological problem, damage crop pro-
duction at global scale. The intensive application of agrochemicals,
fungicides, pesticides to control the growth and pathogenesis of pa-
thogen developed of pathogenic strains and also contaminated and
degraded the quality of the soil. The ACC deaminase producing plant
growth promoting microbes can be used as biological control agents
against these phytopathogen attack such as Fusarium wilt (Fusarium
oxysporum), leaf infection (Botrytis cinerea), Bacterial leaf blight
(Xanthomonas oryzae), damping off (Rhizoctonia solani), Southern blight
(Sclerotium rolfsii), Root and stem rot (Phytophthora sp), Damping off
and root rot disease (Pythium ultimum) etc. (Wang et al., 2000; Rasche
et al., 2006; Barnawal et al., 2017; Dixit et al., 2016; Gamalero et al.,
2017; Nascimento et al., 2013).
These microbes either directly suppressed the growth of pathogens
by producing antimicrobial compounds such as antibiotics (for in-
stance, amphisin, 2,4-diacetylphloroglucinol (DAPG), oomycin A, phe-
nazine, pyoluteorin, pyrrolnitrin, tensin, tropolone, oligomycin A, ka-
nosamine, zwittermicin A, and xanthobaccin), bacteriocins, antifungal/
lytic enzymes (chitinases, dehydrogenase, β-glucanase, lipases, phos-
phatases, proteases), flavonoids like compounds called phytoalexins,
signaling molecules such as N-Acyl homoserine lactones that disrupt the
pathogens quorum sensing and subsequent infection, inhibitory
S. Gupta, S. Pandey Plant Gene 18 (2019) 100175

3. PO3- Solubilization 5. Tolerance to Metal Toxicity 6. Suppression of phytopathogen attack

organic acids Phytase, Acid ACC deaminase producers

Phosphate solubilization bacteria secretes

e.g. Gluconic phosphatase, alter root morphology
acid, oxalic phosphonate
acid, citric , and C–P Enhanced metal uptake secretes
antifungal/lytic/c
acid. lyase potential of plants leads to produces
ell wall
bioaccumulation of metals antibitotics
Decline degrading
enzymes
rhizospheric pH
jasmonic
Subsequent degradation of production acid and
Mineralization
Chelates metal metallic /Xenobiotics of hydrcyanic ethylene
of organic
ions bound to P compounds acid for mediates
phosphorous
controlling ISR(induced
pathogens systemic
Release P to Production of osmolyte resistance)
soils (soluble and volatiles maintain
H2PO4-) osmotic balance and
salinity tolerance
Enhanced activity of Competence for Iron
antioxidant enzymes nutrition
such as PO, PAL, SOD,
CAT suppress ROS
mediated oxidative
stress
Provide Iron nutrition

Provide fixed N2
Iron-
Siderophore
Perform Biological
complex
nitrogen fixation

Iron chelating
Siderophore

1. Lowers stress induced ethylene 2. Phytohormone Production 4. Exopolysaccharide production

S-Ado-met
Amino Acids Trp
ACC
(Trp) Root
synthase
Exudates EPS-producing bacteria
ACC ACC
Maintain water potential
Root exudates ACC
deaminase Lateral root Auxin
IAA
development (IAA)
Prevent water loss and
Promote
growth desiccation of plants
α-ketobutyrate Inhibit the Na+ inside
Enhanced
Ethylene mineral and the plant roots
Ammonia
water uptake
Shield the plant from
Plant roots ACCD bacteria Plant roots ACCD phytopathogen attack
bacteria

Fig. 10. Stress tolerance- Direct and Indirect mechanism conferred by PGPR with ACC deaminase activity.

metabolites e.g. HCN, volatile organic compounds (VOCs; acetoin and caused by these soil and foliar borne pathogens (Saraf et al., 2011).
2,3-butanediol), siderophores, or by competing for nutrients and eco- However exact mechanism of action of ACC deaminase needs to be
logical niches or indirectly by priming or enhancing the plant defensive deciphered in all above examples.
system against biotic stress (jasmonates and ethylene-mediated induced
systemic resistance, ISR), increasing the enzymatic activities of anti-
oxidants and defensive enzymes of plants such as catalase, peroxidase, 9. Transgenic plants with ACC deaminase activity
polyphenol oxidases, phenylalanine ammonia lyase, phenolics (Liu
et al., 2017; Mendes et al., 2013; Sindhu et al., 2009). In addition to The reduction in stress ethylene and associated growth enhance-
these, ACC deaminase containing microbes also lowers the level of ment of plant by ACC deaminase bacteria has motivated scientists to
ethylene and its detrimental effects generated in response to infection transfer acds gene encoding ACC deaminase activity into plants as fu-
ture approach to minimize the deleterious effect of ethylene in plants

9
 Table 1
Effect of ACC deaminase producers on plants against various stress conditions.
ACC producing PGPR Effects on host plants
ACC deaminase producing bacteria Transgenic tomato plants
Transformed Pseudomonas fluorescens strain CHA0 Cucumber, potato, canola
seedlings
Enterobacter cloacae and Pseudomonas sp. Tomato plants
Achromobacter piechaudii ARV8 Tomato and pepper
seedlings
A. piechaudii ARV8 Pea (Pisum sativum L.)
P. fluorescens Maize
P. fluorescens strain TDK1 Groundnut (Arachis
hypogea)
Pseudomonas spp. Pea (Pisum sativum L.)
Pseudomonas fluorescens Pea (Pisum sativum L.)
Paenibacillus x Rhizobium tropici common bean (Phaseolus
vulgaris L.)
Variovorax paradoxus 5C-2 Pea (Pisum sativum L.)
Rhizosphere bacteria containing ACC-deaminase Wheat (Triticum aestivum
L.)
Achromobacter xylosoxidans Basil Ocimum sanctum
10
ACC producing PGPR Chili
Bacillus isolate 23-B + Pseudomonas 6-P + Mesorhizobium Cicer arietinum
ciceris
P. putida UW4 Cucumber plants
Bacillus licheniformis K11 Pepper
P. fluorescens and P. migulae Tomato plants
Pseudomonas fluorescens canola (Brassica napus L.)
Micrococcus variansSBA8 Populus deltoides
Paenibacillus xylanexedens and Enterobacter cloacae Canola
Pseudomonas sp. and Pseudomonas fluorescens Wheat (Triticum aestivum
L.)
Citricoccus zhacaiensis B-4 onion seeds (cv. Arka
Kalyan)
Ochrobactrum pseudogrignonense RJ12, Pseudomonas sp. Vigna mungo L. and Pisum
RJ15 and Bacillus subtilisRJ46 sativum L.
Parastrephia quadrangularis Andean Altiplano plant
Trichoderma longibrachiatum T6 Saline rhizospheric soil of
forest
Rahnella aquatilis HX2 vineyard soil
Trichoderma harzianum T Soybean
Pseudomonas protegens MP12 Temperate deciduous
forest
S. Gupta, S. Pandey
Against stress factor Results Source
Heavy metal stress Improved plant growth in soil with metals such as Cd, Co, Cu, Mg, Ni, Pb, or Zn and Grichko et al., 2000
also scavenged the surrounding metals.
Phytopathogen attack Provided resistance against Pythium damping-off, and Erwinia soft rot. It also Wang et al., 2000
improved the root morphology of canola seedlings under gnotobiotic conditions
Flooding ameliorated the effects of flooding stress induced ethylene. Grichko and Glick, 2001
Drought Increment in fresh and dry weight of biomass as well as reduction in ethylene levels Mayak et al., 2004
Drought Increased root and shoot biomass and low moisture content of soil Dodd et al., 2005
Salinity Increased root growth of maize seedlings Kausar and Shahzad, 2006
Salinity Improved plant growth and salt tolerance of plants. Saravanakumar and
Ramasamy, 2007
Drought Reduced the triple response of ethylene under drought conditions and stimulated Arshad et al., 2008
the growth, yield and ripening of pea.
Drought Increased growth and mitigate drought impact on pea under low water stress Zahir et al., 2008
condition
Flooding Promoted growth and mitigate the negative effects of water stress Figueiredo et al., 2008
Drought Improved growth, yield and nutritive value. It also induces local and systemic Belimov et al., 2009
hormone (ABA) signaling under soil drying conditions
Drought Lowered the levels of ethylene, increased root-shoot length, root-shoot biomass and Shakir et al., 2012
thereby improved water and nutrient uptake under axenic conditions
Flooding Enhanced tolerance against water logging stress with minimum production of Barnawal et al., 2012
ethylene and higher herb yield.
Phytopathogen attack Screening PGPR as biocontrol agents against Fusarium wilt disease Joshi et al., 2012
Drought Enhanced germination, root and shoot length, fresh weight and also increased the Sharma et al., 2013
concentration of proline in low osmotic potential
Flooding Enhanced the expression of proteome related to nutrient metabolism, defense Li et al., 2013
responsive and antioxidant enzymes in plant.
Drought Increased gene expression of stress proteins such as Cadhn, VA, sHSP and CaPR-10 Hui and Kim, 2013
Salinity Improved health status and growth under high salt concentration. Ali et al., 2011
Salinity Reduced the ethylene concentration and hence promote growth and development Akhgar et al., 2014
of salt stressed canola seedlings
polyaromatic hydrocarbon Served as biocontrol agents against several phytopathogens and act as PAH Bisht et al., 2014
stressed soil degrader and simultaneously significantly improved the root-shoot morphology
Salinity Increased root length, alter the levels the of IAA and ethylene and increased Yaish et al., 2015
nutrient uptake potential
Cadmium stress stimulated root elongation and reduces ethylene production Govindasamy et al., 2009
Drought Exhibited plant growth promoting traits and improved germination index PEG Selvakumar et al., 2015
induced osmotic stress
Drought (scarcity of Regulated ethylene level, enhanced seed germination, root-shoot length, and dry Saikia et al., 2018
freshwater) biomass, increase the production of antioxidant enzymes and cellular osmolytes.
Salinity Enhanced the biomass and salt tolerance in wheat seedlings under stress conditions Acuña et al., 2019
and also enhance the activity of Superoxide dismutase (SOD)
Salinity Conferred salt tolerance in wheat plants. Zhang et al., 2019a, b
Salinity Promoted plant growth and stress tolerance under salinity stress. Peng et al., 2019
Salt stress Increased ROS scavenging, antioxidant enzymatic activity and stabilized osmotic Zhang et al., 2019a,b
stress.
Grapevine Phytopathogen Produced anti-fungal compounds such as 2,4-diacetylphloroglucinol (2,4-DAPG), Andreolli et al., 2019
attack pyoluteorin, siderophore, ammonia and pyrrolnitrin
Plant Gene 18 (2019) 100175
S. Gupta, S. Pandey Plant Gene 18 (2019) 100175

subjected to adverse environmental conditions (Grichko and Glick,

Sergeeva et al., 2006

Robison et al., 2001
Grichko et al., 2000

Farwell et al. 2006,

2001; Robison et al., 2001; Nie et al., 2002). A large number of trans-

Zhang et al., 2008

Klee and Kishore,

Reed et al., 1995

Heydarian et al.,
Klee et al., 1991

Nie et al., 2002

Lei et al., 1996
genic plants with foreign acds gene have been genetically engineered to
reduce the deleterious ethylene levels in plants (Table 2). However,
there is a limited report of the performance of transgenic plant con-
Source

1992

2007

2016
taining acds gene under field condition (Farwell et al., 2007). Fur-
thermore, future research should focus on (i) field performance of

as Cd, Co, Cu, Mg, Ni, Pb, or Zn in the soil and also improve their accumulation inside
Significantly increased the plant growth under high concentration of heavy metals such

Reduced the biotic stress induced ethylene concentrations and also diseases symptoms
transgenic plant, (ii) their survival and yield under adverse condition,

Promote the growth of plants in soil supplemented with inorganic compound Cobalt
Significantly increased the plant growth under high concentration of arsenate in the
and (iii) genetic re-arrangement for target gene identification for gene

Increased growth and salt tolerance have been reported in transgenic plants. In
insertion and deletion. Although function of ACC deaminase activity

addition to these, the yield of seed oil under high salinity has also improved
has been reported in tomato, poplar and Arabidopsis plants in context to
ripening and fruit development (Plett et al., 2009; McDonnell et al.,
2009) but their significance in ameliorating the harsh consequences of
Delay the senescence process and reduce ethylene concentration

stress conditions is still less explored. Therefore, a detailed study is

Delay the ripening process by reducing ethylene concentration

needed to determine the distribution of acds gene in different plants and

their role in alleviation of stress.
Increased shoot biomass and reduced Ni accumulation

10. Conclusions and future prospects

This review emphasizes the importance of plants roots colonizing

Lower the levels of ACC in pollen cells

microbes associated with ACC deaminase activity in providing toler-

To withstand high salt concentration

ance by mitigating the adverse impact of against biotic and abiotic

stresses generated ethylene on plants. Therefore, it is essential to
Reduced ethylene synthesis

evaluate the mechanism behind secretion of plant synthesized ACC and

reduction of ethylene generated due to adverse environmental condi-
in transgenic plants

tions and pathogen attack. Understanding of plant-microbe interactions

the plant tissues.

under stressed conditions will help to develop successful agriculture

under various kind of adverse conditions. Physiology of plants and their
responses to various stresses varies. Therefore, it is pivotal to develop
chloride
Effect

new strategies for more specific and efficient ACC deaminase producing
soil.

microbes that can be used as an alternative under saline, acidic, water

logged and drought affected regions.
AcdS gene of Pseudomonas sp. 6GS

ACC deaminase and tryptophan

Acknowledgements
ACC deaminase enzyme of
AcdS gene of Pseudomonas
Transgenic plants carrying genes involved in ACC deaminase biosynthesis along with their application.

Enterobacter cloacae UW4

ACC deaminase enzyme

ACC deaminase enzyme

ACC deaminase enzyme

ACC deaminase enzyme

The authors thank DST-SERB for providing financial support with

ACC deaminase gene

research grant ECR/2017/000080 to carry out the work described in

Transgenic gene

monooxygenase
ACC deaminase

this review. The authors are also thankful to the Amity University Uttar
chlororaphis

Pradesh for providing infrastructural support. There is no conflict of

AcdS gene

interest.

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